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Thompson González N, Freedberg L, Higham J, Vogel E, Cords M. Costs and constraints of cellular immune activity during development in an arboreal primate. ROYAL SOCIETY OPEN SCIENCE 2025; 12:241659. [PMID: 40177102 PMCID: PMC11961265 DOI: 10.1098/rsos.241659] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 09/23/2024] [Revised: 01/03/2025] [Accepted: 02/06/2025] [Indexed: 04/05/2025]
Abstract
Evolutionary life history theory predicts that, during development, investment in immunity must be balanced with the demands of growth. How, and at what time scales, this balance is negotiated is unclear. In this study, we examined the potential energetic costs and limitations to cellular immune activity during development, its trade-offs with growth, related sickness behaviour and the role of hypothalamic-pituitary-adrenal (HPA) axis activity in these relationships. We combined biomarker and socio-environmental data on wild juvenile blue monkeys collected over eight months. Rather than detract from energy balance (C-peptide) and growth of lean body mass (creatinine by specific gravity residuals), cellular immune activity (neopterin) increased with energy balance and lean body mass at monthly time scales, suggesting an energetic constraint on cellular immunity. At shorter time scales, higher neopterin diminished subsequent growth. Energetic constraints on immune activity were weakly regulated by HPA activity during low energy states. Our results suggest that cellular immune activity is both costly and limited by physical condition in wild developing primates.
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Affiliation(s)
- Nicole Thompson González
- Integrative Anthropological Sciences, University of California Santa Barbara, Santa Barbara, CA, USA
- Department of Ecology, Evolution, and Environmental Biology, Columbia University, New York, NY, USA
| | - Lucia Freedberg
- Integrative Anthropological Sciences, University of California Santa Barbara, Santa Barbara, CA, USA
| | - James Higham
- Department of Anthropology, New York University, New York, NY, USA
| | - Erin Vogel
- Department of Anthropology, Rutgers University, New Brunswick, NJ, USA
| | - Marina Cords
- Department of Ecology, Evolution, and Environmental Biology, Columbia University, New York, NY, USA
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2
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McCain KM, Mansilla G, Sheldon EL, Zimmer C, Schrey AW, Rowe M, Dor R, Kohl KD, Søraker JS, Jensen H, Mathot KJ, Vu T, Phuong HT, Jimeno B, Buchanan KL, Thiam M, Briskie J, Martin LB. Microbial surveillance versus cytokine responsiveness in native and non-native house sparrows. Biol Lett 2025; 21:20240431. [PMID: 39878139 PMCID: PMC11776021 DOI: 10.1098/rsbl.2024.0431] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/24/2024] [Revised: 09/24/2024] [Accepted: 11/12/2024] [Indexed: 01/31/2025] Open
Abstract
The success of introduced species often relies on flexible traits, including immune system traits. While theories predict non-natives will have weak defences due to decreased parasite pressure, effective parasite surveillance remains crucial, as infection risk is rarely zero and the evolutionary novelty of infection is elevated in non-native areas. This study examines the relationship between parasite surveillance and cytokine responsiveness in native and non-native house sparrows, hypothesizing that non-natives maintain high pathogen surveillance while avoiding costly inflammation. We made this specific prediction, as this pattern could enable invaders to effectively mitigate pathogen risk in a manner commensurate with the life-history priorities of a colonizing organism (i.e. rapid maturation and high reproductive effort). To test this hypothesis, we measured TLR-2 and TLR-4 expression, markers of pathogen surveillance and cytokine responses (changes in IL-1β and IL-10), regulators of inflammation, to a simulated bacterial infection. In non-native sparrows, we found that as TLR-4 expression increased, IL-1β and IL-10 responses decreased, a relationship not observed in native sparrows. Additionally, higher body condition predicted larger IL-1β and IL-10 responses in all birds. These findings suggest that high TLR-4 surveillance may mitigate strong inflammatory responses in non-native sparrows, with pathological and resource-based costs driving immune variation among and within populations.
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Affiliation(s)
- Kailey M. McCain
- Global Enviornmental and Genomic Health Sciences, University of South Florida, Tampa, FL33612, USA
| | - Gabby Mansilla
- Global Enviornmental and Genomic Health Sciences, University of South Florida, Tampa, FL33612, USA
| | - Elizabeth L. Sheldon
- Sorbonne Université, Villefranche Oceanography Laboratory, 181 Chem. du Lazaret, Villefranche-sur-Mer06230, France
| | - Cedric Zimmer
- Laboratoire d’Ethologie Expérimentale et Comparée, LEEC, Université Sorbonne Paris Nord, UR 4443, Villetaneuse93430, France
| | - Aaron W. Schrey
- Department of Biology, Georgia Southern University Armstrong Campus, Science Center 1505,16 11935 Abercorn Street, Savannah, GA31419, USA
| | - Melissah Rowe
- Department of Animal Ecology, Netherlands Institute of Ecology (NIOO‐KNAW), Wageningen6700 AB, The Netherlands
| | - Roi Dor
- Department of Natural Sciences, The Open University of Israel, Ra’anana, Israel
| | - Kevin D. Kohl
- Department of Biological Sciences, University of Pittsburgh, 4249 Fifth Avenue Pittsburgh, Pittsburgh, PA15260, USA
| | - Jørgen S. Søraker
- Department of Biology, Centre for Conservation Biology, Norwegian University of Science and Technology, N-7491 Trondheim, Trondheim, Norway
| | - Henrik Jensen
- Department of Biology, Centre for Conservation Biology, Norwegian University of Science and Technology, N-7491 Trondheim, Trondheim, Norway
| | - Kimberley J. Mathot
- Canada Research Chair in Integrative Ecology, Department of Biological Sciences,CW405 Biological Sciences Building, University of Alberta, EdmontonAB T6G 2E9, Canada
| | - Thinh Vu
- Department of Wildlife, Faculty of Forest Resource and Environmental Management, Vietnam National University of Forestry, Chương Mỹ, Vietnam
| | - Ho Thu Phuong
- Department of Wildlife, Faculty of Forest Resource and Environmental Management, Vietnam National University of Forestry, Chương Mỹ, Vietnam
| | - Blanca Jimeno
- Department of Biological Conservation and Ecosystem Restoration, Pyrenean Institute of Ecology (IPE-CSIC). Av. Nuestra Señora de la Victoria, 22700, Jaca, Spain
| | - Katherine L. Buchanan
- School of Life and Environmental Sciences, Deakin University Geelong, Geelong, Vic3216, Australia
| | - Massamba Thiam
- Laboratory of Zoology of Terrestrial Vertebrates, Fundamental Institute of Black Africa,Cheikh Anta Diop University of Dakar Senegal, Dakar, Senegal
| | - James Briskie
- School of Biological Sciences, University of Canterbury, Christchurch, New Zealand
| | - Lynn B. Martin
- Global Enviornmental and Genomic Health Sciences, University of South Florida, Tampa, FL33612, USA
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Ncho CM, Berdos JI, Gupta V, Rahman A, Mekonnen KT, Bakhsh A. Abiotic stressors in poultry production: A comprehensive review. J Anim Physiol Anim Nutr (Berl) 2025; 109:30-50. [PMID: 39132861 PMCID: PMC11731476 DOI: 10.1111/jpn.14032] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/29/2024] [Revised: 07/24/2024] [Accepted: 07/25/2024] [Indexed: 08/13/2024]
Abstract
In modern animal husbandry, stress can be viewed as an automatic response triggered by exposure to adverse environmental conditions. This response can range from mild discomfort to severe consequences, including mortality. The poultry industry, which significantly contributes to human nutrition, is not exempt from this issue. Although genetic selection has been employed for several decades to enhance production output, it has also resulted in poor stress resilience. Stress is manifested through a series of physiological reactions, such as the identification of the stressful stimulus, activation of the sympathetic nervous system and the adrenal medulla, and subsequent hormonal cascades. While brief periods of stress can be tolerated, prolonged exposure can have more severe consequences. For instance, extreme fluctuations in environmental temperature can lead to the accumulation of reactive oxygen species, impairment of reproductive performance, and reduced immunity. In addition, excessive noise in poultry slaughterhouses has been linked to altered bird behaviour and decreased production efficiency. Mechanical vibrations have also been shown to negatively impact the meat quality of broilers during transport as well as the egg quality and hatchability in hatcheries. Lastly, egg production is heavily influenced by light intensity and regimens, and inadequate light management can result in deficiencies, including visual anomalies, skeletal deformities, and circulatory problems. Although there is a growing body of evidence demonstrating the impact of environmental stressors on poultry physiology, there is a disproportionate representation of stressors in research. Recent studies have been focused on chronic heat stress, reflecting the current interest of the scientific community in climate change. Therefore, this review aims to highlight the major abiotic stressors in poultry production and elucidate their underlying mechanisms, addressing the need for a more comprehensive understanding of stress in diverse environmental contexts.
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Affiliation(s)
- Chris Major Ncho
- Department of Environmental Systems ScienceInstitute of Agricultural Sciences, ETH ZürichZürichSwitzerland
| | - Janine I. Berdos
- Department of Animal ScienceCollege of Agriculture and Forestry, Tarlac Agricultural UniversityMalacampaTarlacPhilippines
| | - Vaishali Gupta
- Division of Applied Life Sciences (BK21 Four Program)Gyeongsang National UniversityJinju‐siRepublic of Korea
| | - Attaur Rahman
- Department of Medicine and TherapeuticsFaculty of Medicine, The Chinese University of Hong KongHong KongChina
| | - Kefala Taye Mekonnen
- Department of Animal ScienceCollege of Agriculture and Environmental Science, Arsi UniversityAsellaOromiaEthiopia
| | - Allah Bakhsh
- Atta‐ur‐Rahman School of Applied Biosciences (ASAB)National University of Sciences and Technology (NUST)IslamabadPakistan
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Giolai M, Laine AL. A trade-off between investment in molecular defense repertoires and growth in plants. Science 2024; 386:677-680. [PMID: 39509497 DOI: 10.1126/science.adn2779] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/01/2023] [Accepted: 09/13/2024] [Indexed: 11/15/2024]
Abstract
Given the negative fitness effects that pathogens impose on their hosts, the benefits of resistance should be universal. However, there is marked variation across plant species in the number of nucleotide-binding leucine-rich repeat receptors, which form a cornerstone of defense. The growth-defense trade-off hypothesis predicts costs associated with defense investment to generate variation in these traits. Our analysis comparing features of the intracellular immune-receptor repertoires with trait data of 187 species shows that in wild plants, the size of the molecular defense repertoire correlates negatively with growth. By contrast, we do not find evidence for a growth-defense trade-off in agricultural plants. Our cross-species approach highlights the central role of defense investment in shaping ecological trait variation and its sensitivity to domestication.
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Affiliation(s)
- Michael Giolai
- Research Centre for Ecological Change, Organismal and Evolutionary Biology Research Program, Faculty of Biological and Environmental Sciences, University of Helsinki, 00014 Helsinki, Finland
| | - Anna-Liisa Laine
- Research Centre for Ecological Change, Organismal and Evolutionary Biology Research Program, Faculty of Biological and Environmental Sciences, University of Helsinki, 00014 Helsinki, Finland
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Challet E, Pévet P. Melatonin in energy control: Circadian time-giver and homeostatic monitor. J Pineal Res 2024; 76:e12961. [PMID: 38751172 DOI: 10.1111/jpi.12961] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/05/2023] [Revised: 04/04/2024] [Accepted: 04/30/2024] [Indexed: 05/26/2024]
Abstract
Melatonin is a neurohormone synthesized from dietary tryptophan in various organs, including the pineal gland and the retina. In the pineal gland, melatonin is produced at night under the control of the master clock located in the suprachiasmatic nuclei of the hypothalamus. Under physiological conditions, the pineal gland seems to constitute the unique source of circulating melatonin. Melatonin is involved in cellular metabolism in different ways. First, the circadian rhythm of melatonin helps the maintenance of proper internal timing, the disruption of which has deleterious effects on metabolic health. Second, melatonin modulates lipid metabolism, notably through diminished lipogenesis, and it has an antidiabetic effect, at least in several animal models. Third, pharmacological doses of melatonin have antioxidative, free radical-scavenging, and anti-inflammatory properties in various in vitro cellular models. As a result, melatonin can be considered both a circadian time-giver and a homeostatic monitor of cellular metabolism, via multiple mechanisms of action that are not all fully characterized. Aging, circadian disruption, and artificial light at night are conditions combining increased metabolic risks with diminished circulating levels of melatonin. Accordingly, melatonin supplementation could be of potential therapeutic value in the treatment or prevention of metabolic disorders. More clinical trials in controlled conditions are needed, notably taking greater account of circadian rhythmicity.
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Affiliation(s)
- Etienne Challet
- Centre National de la Recherche Scientifique (CNRS), Institute of Cellular and Integrative Neurosciences, University of Strasbourg, Strasbourg, France
| | - Paul Pévet
- Centre National de la Recherche Scientifique (CNRS), Institute of Cellular and Integrative Neurosciences, University of Strasbourg, Strasbourg, France
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Kadamani KL, Logan SM, Pamenter ME. Does hypometabolism constrain innate immune defense? Acta Physiol (Oxf) 2024; 240:e14091. [PMID: 38288574 DOI: 10.1111/apha.14091] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/08/2023] [Revised: 11/30/2023] [Accepted: 01/01/2024] [Indexed: 02/24/2024]
Abstract
Many animals routinely make energetic trade-offs to adjust to environmental demands and these trade-offs often have significant implications for survival. For example, environmental hypoxia is commonly experienced by many organisms and is an energetically challenging condition because reduced oxygen availability constrains aerobic energy production, which can be lethal. Many hypoxia-tolerant species downregulate metabolic demands when oxygen is limited; however, certain physiological functions are obligatory and must be maintained despite the need to conserve energy in hypoxia. Of particular interest is immunity (including both constitutive and induced immune functions) because mounting an immune response is among the most energetically expensive physiological processes but maintaining immune function is critical for survival in most environments. Intriguingly, physiological responses to hypoxia and pathogens share key molecular regulators such as hypoxia-inducible factor-1α, through which hypoxia can directly activate an immune response. This raises an interesting question: do hypoxia-tolerant species mount an immune response during periods of hypoxia-induced hypometabolism? Unfortunately, surprisingly few studies have examined interactions between immunity and hypometabolism in such species. Therefore, in this review, we consider mechanistic interactions between metabolism and immunity, as well as energetic trade-offs between these two systems, in hypoxia-tolerant animals but also in other models of hypometabolism, including neonates and hibernators. Specifically, we explore the hypothesis that such species have blunted immune responses in hypometabolic conditions and/or use alternative immune pathways when in a hypometabolic state. Evidence to date suggests that hypoxia-tolerant animals do maintain immunity in low oxygen conditions, but that the sensitivity of immune responses may be blunted.
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Affiliation(s)
- Karen L Kadamani
- Department of Biology, University of Ottawa, Ottawa, Ontario, Canada
| | - Samantha M Logan
- Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada
| | - Matthew E Pamenter
- Department of Biology, University of Ottawa, Ottawa, Ontario, Canada
- University of Ottawa Brain and Mind Research Institute, Ottawa, Ontario, Canada
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Allam NAT, Hamouda RAEF, Sedky D, Abdelsalam ME, El-Gawad MEHA, Hassan NMF, Aboelsoued D, Elmaaty AMA, Ibrahim MA, Taie HAA, Hakim AS, Desouky HM, Megeed KNA, Abdel-Hamid MS. Medical prospects of cryptosporidiosis in vivo control using biofabricated nanoparticles loaded with Cinnamomum camphora extracts by Ulva fasciata. Vet World 2024; 17:108-124. [PMID: 38406364 PMCID: PMC10884584 DOI: 10.14202/vetworld.2024.108-124] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/13/2023] [Accepted: 11/28/2023] [Indexed: 02/27/2024] Open
Abstract
Background and Aim Global efforts are continuing to develop preparations against cryptosporidiosis. This study aimed to investigate the efficacy of biosynthesized Ulva fasciata loading Cinnamomum camphora oil extract on new zinc oxide nanoparticles (ZnONPs shorten to ZnNPs) and silver nanoparticles (AgNPs) as alternative treatments for Cryptosporidium parvum experimental infection in rats. Materials and Methods Oil extract was characterized by gas chromatography-mass spectrometry, loaded by U. fasciata on ionic-based ZnO and NPs, and then characterized by transmission electron microscopy, scanning electron microscopy, and X-ray diffraction. Biosafety and toxicity were investigated by skin tests. A total of 105 C. parvum oocysts/rat were used (n = 81, 2-3 W, 80-120 g, 9 male rats/group). Oocysts shedding was counted for 21 d. Doses of each preparation in addition to reference drug were administered daily for 7 d, starting on post-infection (PI) day (3). Nitazoxanide (100 mg) was used as the reference drug. After 3 weeks, the rats were sacrificed for postmortem examination and histopathological examination. Two blood samples/rat/group were collected on the 21st day. Ethylenediaminetetraacetic acid blood samples were also used for analysis of biochemistry, hematology, immunology, micronucleus prevalence, and chromosomal abnormalities. Results C. camphora leaves yielded 28.5 ± 0.3 g/kg oil and 20 phycocompounds were identified. Spherical and rod-shaped particles were detected at 10.47-30.98 nm and 18.83-38.39 nm, respectively. ZnNPs showed the earliest anti-cryptosporidiosis effect during 7-17 d PI. Other hematological, biochemical, immunological, histological, and genotoxicity parameters were significantly fruitful; hence, normalized pathological changes induced by infestation were observed in the NPs treatments groups against the infestation-free and Nitazoxanide treated group. Conclusion C. camphora, U. fasciata, ZnNPs, and AgNPs have refluxed the pathological effects of infection as well as positively improved host physiological condition by its anticryptosporidial immunostimulant regenerative effects with sufficient ecofriendly properties to be proposed as an alternative to traditional drugs, especially in individuals with medical reactions against chemical commercial drugs.
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Affiliation(s)
- Nesreen Allam Tantawy Allam
- Department of Parasitology and Animal Diseases, Veterinary Research Institute, National Research Centre, 33 El Buhouth Street, Dokki, P.O. Box: 12622, Giza, Cairo, Egypt
| | - Ragaa Abd El-Fatah Hamouda
- Department of Microbial Biotechnology, Genetic Engineering and Biotechnology Research Institute, University of Sadat City, 5 Zone, Sadat City, Munofia, Egypt
| | - Doaa Sedky
- Department of Parasitology and Animal Diseases, Veterinary Research Institute, National Research Centre, 33 El Buhouth Street, Dokki, P.O. Box: 12622, Giza, Cairo, Egypt
| | - Mahinour Ezzeldin Abdelsalam
- Department of General Biology, Center of Basic Sciences, Misr University for Science and Technology, Al Motamayez District, 6 of October, Giza, Cairo, Egypt
| | | | - Noha Mahmoud Fahmy Hassan
- Department of Parasitology and Animal Diseases, Veterinary Research Institute, National Research Centre, 33 El Buhouth Street, Dokki, P.O. Box: 12622, Giza, Cairo, Egypt
| | - Dina Aboelsoued
- Department of Parasitology and Animal Diseases, Veterinary Research Institute, National Research Centre, 33 El Buhouth Street, Dokki, P.O. Box: 12622, Giza, Cairo, Egypt
| | - Amal M. Abou Elmaaty
- Department of Animal Reproduction and Artificial Insemination, Veterinary Research Institute, National Research Centre, 33 El Buhouth Street, Dokki, P.O. Box: 12622, Giza, Cairo, Egypt
| | - Muhammad A. Ibrahim
- Cytogenetics and Animal Cell Culture Lab., National Gene Bank, Agriculture Research Center, 9 Gamaa Street, Giza, Cairo, Egypt
| | - Hanan Anwar Aly Taie
- Department of Plant Biochemistry, Agriculture and Biological Researches Institute, National Research Centre, 33 El-Bohouth St. (Former El-Tahrir St.), Dokki, P.O. 12622, Giza, Cairo, Egypt
| | - Ashraf Samir Hakim
- Department of Microbiology and Immunology, Veterinary Research Institute, National Research Centre, 33 El Buhouth Street, Dokki, P.O. Box: 12622, Giza, Cairo, Egypt
| | - Hassan Mohamed Desouky
- Department of Animal Reproduction and Artificial Insemination, Veterinary Research Institute, National Research Centre, 33 El Buhouth Street, Dokki, P.O. Box: 12622, Giza, Cairo, Egypt
| | - Kadria Nasr Abdel Megeed
- Department of Parasitology and Animal Diseases, Veterinary Research Institute, National Research Centre, 33 El Buhouth Street, Dokki, P.O. Box: 12622, Giza, Cairo, Egypt
| | - Marwa Salah Abdel-Hamid
- Department of Microbial Biotechnology, Genetic Engineering and Biotechnology Research Institute, University of Sadat City, 5 Zone, Sadat City, Munofia, Egypt
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O'Keeffe FE, Pendleton RC, Holland CV, Luijckx P. Increased virulence due to multiple infection in Daphnia leads to limited growth in 1 of 2 co-infecting microsporidian parasites. Parasitology 2024; 151:58-67. [PMID: 37981808 PMCID: PMC10941049 DOI: 10.1017/s0031182023001130] [Citation(s) in RCA: 3] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/20/2023] [Revised: 11/14/2023] [Accepted: 11/15/2023] [Indexed: 11/21/2023]
Abstract
Recent outbreaks of various infectious diseases have highlighted the ever-present need to understand the drivers of the outbreak and spread of disease. Although much of the research investigating diseases focuses on single infections, natural systems are dominated by multiple infections. These infections may occur simultaneously, but are often acquired sequentially, which may alter the outcome of infection. Using waterfleas (Daphnia magna) as a model organism, we examined the outcome of sequential and simultaneous multiple infections with 2 microsporidian parasites (Ordospora colligata and Hamiltosporidium tvaerminnensis) in a fully factorial design with 9 treatments and 30 replicates. We found no differences between simultaneous and sequential infections. However, H. tvaerminnensis fitness was impeded by multiple infection due to increased host mortality, which gave H. tvaerminnensis less time to grow. Host fecundity was also reduced across all treatments, but animals infected with O. colligata at a younger age produced the fewest offspring. As H. tvaerminnensis is both horizontally and vertically transmitted, this reduction in offspring may have further reduced H. tvaerminnensis fitness in co-infected treatments. Our findings suggest that in natural populations where both species co-occur, H. tvaerminnensis may evolve to higher levels of virulence following frequent co-infection by O. colligata.
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Affiliation(s)
- Floriane E. O'Keeffe
- Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin, Ireland
| | - Rebecca C. Pendleton
- Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin, Ireland
| | - Celia V. Holland
- Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin, Ireland
| | - Pepijn Luijckx
- Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin, Ireland
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Wolf SE, Shalev I. The shelterin protein expansion of telomere dynamics: Linking early life adversity, life history, and the hallmarks of aging. Neurosci Biobehav Rev 2023; 152:105261. [PMID: 37268182 PMCID: PMC10527177 DOI: 10.1016/j.neubiorev.2023.105261] [Citation(s) in RCA: 8] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/27/2023] [Revised: 04/10/2023] [Accepted: 05/30/2023] [Indexed: 06/04/2023]
Abstract
Aging is characterized by functional decline occurring alongside changes to several hallmarks of aging. One of the hallmarks includes attrition of repeated DNA sequences found at the ends of chromosomes called telomeres. While telomere attrition is linked to morbidity and mortality, whether and how it causally contributes to lifelong rates of functional decline is unclear. In this review, we propose the shelterin-telomere hypothesis of life history, in which telomere-binding shelterin proteins translate telomere attrition into a range of physiological outcomes, the extent of which may be modulated by currently understudied variation in shelterin protein levels. Shelterin proteins may expand the breadth and timing of consequences of telomere attrition, e.g., by translating early life adversity into acceleration of the aging process. We consider how the pleiotropic roles of shelterin proteins provide novel insights into natural variation in physiology, life history, and lifespan. We highlight key open questions that encourage the integrative, organismal study of shelterin proteins that enhances our understanding of the contribution of the telomere system to aging.
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Affiliation(s)
- Sarah E Wolf
- Department of Biobehavioral Health, Penn State University, University Park, PA 16802, USA.
| | - Idan Shalev
- Department of Biobehavioral Health, Penn State University, University Park, PA 16802, USA
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10
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Hagen EH, Blackwell AD, Lightner AD, Sullivan RJ. Homo medicus: The transition to meat eating increased pathogen pressure and the use of pharmacological plants in Homo. AMERICAN JOURNAL OF BIOLOGICAL ANTHROPOLOGY 2023; 180:589-617. [PMID: 36815505 DOI: 10.1002/ajpa.24718] [Citation(s) in RCA: 4] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 01/27/2022] [Revised: 01/31/2023] [Accepted: 02/08/2023] [Indexed: 02/24/2023]
Abstract
The human lineage transitioned to a more carnivorous niche 2.6 mya and evolved a large body size and slower life history, which likely increased zoonotic pathogen pressure. Evidence for this increase includes increased zoonotic infections in modern hunter-gatherers and bushmeat hunters, exceptionally low stomach pH compared to other primates, and divergence in immune-related genes. These all point to change, and probably intensification, in the infectious disease environment of Homo compared to earlier hominins and other apes. At the same time, the brain, an organ in which immune responses are constrained, began to triple in size. We propose that the combination of increased zoonotic pathogen pressure and the challenges of defending a large brain and body from pathogens in a long-lived mammal, selected for intensification of the plant-based self-medication strategies already in place in apes and other primates. In support, there is evidence of medicinal plant use by hominins in the middle Paleolithic, and all cultures today have sophisticated, plant-based medical systems, add spices to food, and regularly consume psychoactive plant substances that are harmful to helminths and other pathogens. We propose that the computational challenges of discovering effective plant-based treatments, the consequent ability to consume more energy-rich animal foods, and the reduced reliance on energetically-costly immune responses helped select for increased cognitive abilities and unique exchange relationships in Homo. In the story of human evolution, which has long emphasized hunting skills, medical skills had an equal role to play.
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Affiliation(s)
- Edward H Hagen
- Department of Anthropology, Washington State University, Pullman, Washington, USA
| | - Aaron D Blackwell
- Department of Anthropology, Washington State University, Pullman, Washington, USA
| | - Aaron D Lightner
- Department of Anthropology, Washington State University, Pullman, Washington, USA
- Department of the Study of Religion, Aarhus University, Aarhus, Denmark
| | - Roger J Sullivan
- Department of Anthropology, California State University, Sacramento, California, USA
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11
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Wolf SE, Zhang S, Clotfelter ED. Experimental ectoparasite removal has a sex-specific effect on nestling telomere length. Ecol Evol 2023; 13:e9861. [PMID: 36911306 PMCID: PMC9992774 DOI: 10.1002/ece3.9861] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/09/2022] [Revised: 02/02/2023] [Accepted: 02/06/2023] [Indexed: 03/11/2023] Open
Abstract
Parasites are a strong selective force that can influence fitness-related traits. The length of chromosome-capping telomeres can be used to assess the long-term costs of parasitism, as telomere loss accelerates in response to environmental stressors and often precedes poorer survival prospects. Here, we explored the sex-specific effects of ectoparasite removal on morphology and telomere length in nestling tree swallows (Tachycineta bicolor). To do so, we experimentally removed blow fly (Protocalliphora spp.) larvae from nests using Permethrin, a broad-spectrum insecticide. Compared to water-treated controls, insecticide treatment of nests had a sex-biased effect on blood telomere length: ectoparasite removal resulted in significantly longer telomeres in males but not females. While this treatment did not influence nestling body mass, it was associated with reduced feather development regardless of sex. This may reflect a relaxed pressure to fledge quickly in the absence of parasites, or alternatively, could be a negative side effect of permethrin on morphology. Exploring robust sex-specific telomere dynamics in response to early-life environmental pressures such as parasitism will shed light on sexual dimorphism in adult life histories and aging.
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Affiliation(s)
- Sarah E. Wolf
- Department of BiologyIndiana UniversityBloomingtonIndianaUSA
- Department of Biobehavioral HealthPennsylvania State UniversityState CollegePennsylvaniaUSA
| | - Samuel Zhang
- Department of BiologyAmherst CollegeAmherstMassachusettsUSA
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12
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McGrosky A, Pontzer H. The fire of evolution: energy expenditure and ecology in primates and other endotherms. J Exp Biol 2023; 226:297166. [PMID: 36916459 DOI: 10.1242/jeb.245272] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 03/16/2023]
Abstract
Total energy expenditure (TEE) represents the total energy allocated to growth, reproduction and body maintenance, as well as the energy expended on physical activity. Early experimental work in animal energetics focused on the costs of specific tasks (basal metabolic rate, locomotion, reproduction), while determination of TEE was limited to estimates from activity budgets or measurements of subjects confined to metabolic chambers. Advances in recent decades have enabled measures of TEE in free-living animals, challenging traditional additive approaches to understanding animal energy budgets. Variation in lifestyle and activity level can impact individuals' TEE on short time scales, but interspecific differences in TEE are largely shaped by evolution. Here, we review work on energy expenditure across the animal kingdom, with a particular focus on endotherms, and examine recent advances in primate energetics. Relative to other placental mammals, primates have low TEE, which may drive their slow pace of life and be an evolved response to the challenges presented by their ecologies and environments. TEE variation among hominoid primates appears to reflect adaptive shifts in energy throughput and allocation in response to ecological pressures. As the taxonomic breadth and depth of TEE data expand, we will be able to test additional hypotheses about how energy budgets are shaped by environmental pressures and explore the more proximal mechanisms that drive intra-specific variation in energy expenditure.
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Affiliation(s)
- Amanda McGrosky
- Department of Evolutionary Anthropology, Duke University, Durham, NC 27708, USA
| | - Herman Pontzer
- Department of Evolutionary Anthropology, Duke University, Durham, NC 27708, USA.,Duke Global Health Institute, Durham, NC 27708, USA
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13
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Briggs CW, Dudus KA, Ely TE, Kwasnoski LA, Downs CJ. Hemolytic parasites affect survival in migrating red-tailed hawks. CONSERVATION PHYSIOLOGY 2022; 10:coac075. [PMID: 36570735 PMCID: PMC9773370 DOI: 10.1093/conphys/coac075] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 01/31/2022] [Revised: 10/18/2022] [Accepted: 11/18/2022] [Indexed: 06/17/2023]
Abstract
Migrating birds face a myriad of hazards, including higher exposure to parasites and numerous competing energy demands. It follows that migration may act as a selective filter and limit population growth. Understanding how individual-level physiological condition and disease status scale up to population dynamics through differential survival of individuals is necessary to identify threats and management interventions for migratory populations, many of which face increasing conservation challenges. However, linking individual physiological condition, parasite infection status and survival can be difficult. We examined the relationship among two measures of physiological condition [scaled-mass index and heterophil/leukocyte (H/L) ratio], hematozoa (i.e. hemoparasites) presence and abundance, and constitutive immunity in 353 autumn migrating red-tailed hawks (Buteo jamaicensis calurus) from 2004 to 2018. Hematazoa (i.e. Haemoproteus and Leucocytozoon) were in the blood smears from 139 red-tailed hawks (39.4%). H/L ratio decreased with scaled-mass index. Adults had a significantly higher H/L ratio than juveniles. Our two measures of immune defences, hemolytic-complement activity and bacteria-killing ability, were highly positively correlated. Our most notable finding was a negative relationship between Haemoproteus parasitemia and survival (i.e. documented individual mortality), indicating that haemosporidian parasites influence survival during a challenging life stage. The effect of haemosporidian parasites on individuals is often debated, and we provide evidence that parasitemia can affect individual survival. In contrast, we did not find evidence of trade-offs between survival and immune defences.
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Affiliation(s)
- Christopher W Briggs
- Golden Gate Raptor Observatory, Golden Gate National Parks Conservancy, Sausalito, CA 94965, USA
- Department of Biology, Colgate University, Hamilton, NY 13346, USA
- Department of Environmental Biology, State University of New York College of Environmental Science and Forestry, Syracuse, NY 13210, USA
| | - Kris A Dudus
- Golden Gate Raptor Observatory, Golden Gate National Parks Conservancy, Sausalito, CA 94965, USA
- National Park Service, Gulf Breeze, FL 32563, USA
| | - Teresa E Ely
- Golden Gate Raptor Observatory, Golden Gate National Parks Conservancy, Sausalito, CA 94965, USA
| | | | - Cynthia J Downs
- Corresponding author: Department of Environmental Biology, State University of New York College of Environmental Science and Forestry, Syracuse, NY 13210, USA.
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14
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Chen Z, Wang K, Guo J, Zhou J, Loor JJ, Yang Z, Yang Y. Melatonin Maintains Homeostasis and Potentiates the Anti-inflammatory Response in Staphylococcus aureus-Induced Mastitis through microRNA-16b/YAP1. JOURNAL OF AGRICULTURAL AND FOOD CHEMISTRY 2022; 70:15255-15270. [PMID: 36399659 DOI: 10.1021/acs.jafc.2c05904] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 06/16/2023]
Abstract
Staphylococcus aureus is a highly infectious pathogen and is a considerable threat to food hygiene and safety. Although melatonin is thought to exert an ameliorative effect on bovine mastitis, the regulatory mechanisms are unclear. In this study, we first verified the therapeutic effect of melatonin against S. aureus in vitro and in vivo, a screening of differentially expressed miRNAs and mRNAs among the blank, and S. aureus and melatonin + S. aureus groups by high-throughput sequencing identified miR-16b and YAP1, which exhibited 1.95-fold upregulated and 1.05-fold downregulated expression, respectively. Moreover, epigenetic studies showed that S. aureus inhibited miR-16b expression by methylation (increased DNMT1 expression). Additionally, the DNMT1 expression level was significantly decreased by melatonin treatment, which might indicate that the inhibition of DNMT1 by melatonin reduces the effect of S. aureus on miR-16b. The flow cytometry, scanning and transmission electron microscopy, EdU assay, and cell morphology results indicated that miR-16b in bovine mammary epithelial cells (in vitro) and in mice (in vivo) can modulate the maintenance of homeostasis and potentiate the anti-inflammatory response. In addition, YAP1 was demonstrated to be the target gene of miR-16b through quantitative real-time polymerase chain reaction, western blot, RNA immunoprecipitation, and functional assays. This study indicates that melatonin inhibits S. aureus-induced inflammation via microRNA-16b/YAP1-mediated regulation, and these findings might provide a new strategy for the prevention of bovine mastitis, facilitating further studies good of zoonotic diseases caused by S. aureus infection.
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Affiliation(s)
- Zhi Chen
- Yangzhou University, Yangzhou 225009, PR China
| | - Kun Wang
- Yangzhou University, Yangzhou 225009, PR China
| | - Jiahe Guo
- Yangzhou University, Yangzhou 225009, PR China
| | | | - Juan J Loor
- University of Illinois, Urbana, Illinois 61801, United States
| | | | - Yi Yang
- Yangzhou University, Yangzhou 225009, PR China
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15
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Mishra V, Prajapati G, Baranwal V, Mishra RK. NMR-Based Metabolomic Imprinting Elucidates Macrophage Polarization of THP-1 Cell Lines Stimulated by Zinc Oxide Nanoparticles. ACS APPLIED BIO MATERIALS 2022; 5:4873-4885. [PMID: 36126340 DOI: 10.1021/acsabm.2c00603] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/28/2022]
Abstract
Zinc oxide (ZnO) nanoparticles (NPs) have been widely used in industry, cosmetics, drugs, bioimaging, and drug delivery. ZnO NPs have been found to interact and interfere with cellular physiology via macrophages, thereby resulting in macrophage polarization. The functional reprogramming of the cells is synchronized through cellular metabolic adaptations. The current study, therefore, aims to establish crosstalk between ZnO-NP-induced metabolic alterations and macrophage polarization in PMA-activated THP-1 cell lines. We observed moderate to heightened cytotoxic response in terms of cell viability and proliferation. The results also revealed increased Th1-type cytokine and chemokine expression. In order to characterize the changes in metabolite concentration in treatment groups, we employed multivariate data analysis (principal component analysis and partial least-squares discriminant analysis) of 1H NMR spectra. The results revealed biologically relevant patterns and alterations in many metabolic pathways. These alterations and patterns were found to be in line across the immune-cytotoxic axis. Furthermore, the results also implicate the role of carbon metabolism toward the classical activation of macrophage polarization. The omics approach could identify the markers involved in NP-induced toxicity, thus elaborating our vision of cytotoxicity that is currently limited to end-point and cytokine assays. Also, it could be emphasized that metabolic reconfiguration upon NP stimulation could direct macrophage polarization toward classical activation.
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Affiliation(s)
- Vani Mishra
- Nanotechnology Application Centre (NAC), University of Allahabad, Prayagraj 211002, India
| | - Gurudayal Prajapati
- NMR Centre SAIF Laboratory, CSIR-Central Drug Research Institute (CDRI), Lucknow 226031, India
| | - Vikas Baranwal
- Graphene Research Labs Pvt. Ltd., 135 Road 10, KIADB IT Park, Bengaluru 562149, India
| | - Rohit Kumar Mishra
- Centre of Science and Society, Institute of Interdisciplinary Sciences (IIDS), University of Allahabad, Prayagraj 211002, India
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16
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Zhu B. Logic of the Temporal Compartmentalization of the Hepatic Metabolic Cycle. Physiology (Bethesda) 2022; 37:0. [PMID: 35658626 PMCID: PMC9394779 DOI: 10.1152/physiol.00003.2022] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/09/2022] [Revised: 05/05/2022] [Accepted: 05/28/2022] [Indexed: 12/25/2022] Open
Abstract
The mammalian liver must cope with various metabolic and physiological changes that normally recur every day and result primarily from rest-activity and fasting-feeding cycles. In this article, I present evidence supporting a temporal compartmentalization of rhythmic hepatic metabolic processes into four main clusters: regulation of energy homeostasis, maintenance of information integrity, immune response, and genetic information flow. I further review literatures and discuss how both the circadian and the newly discovered 12-h ultradian clock work together to regulate these four temporally separated processes in mouse liver, which, interestingly, is largely uncoupled from the liver zonation regulation.
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Affiliation(s)
- Bokai Zhu
- Aging Institute of UPMC, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania
- Pittsburgh Liver Research Center, University of Pittsburgh, Pittsburgh, Pennsylvania
- Division of Endocrinology and Metabolism, Department of Medicine, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania
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17
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Immunoecology of Species with Alternative Reproductive Tactics and Strategies. J ZOOL SYST EVOL RES 2022. [DOI: 10.1155/2022/3248731] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/18/2022]
Abstract
Alternative reproductive tactics and strategies (ARTS) refer to polymorphic reproductive behaviours in which in addition to the usual two sexes, there are one or more alternative morphs, usually male, that have evolved the ability to circumvent direct intra-sexual competition. Each morph has its own morphological, ecological, developmental, behavioural, life-history, and physiological profile that shifts the balance between reproduction and self-maintenance, one aspect being immunity. Immunoecological work on species with ARTS, which is the topic of this review, is particularly interesting because the alternative morphs make it possible to separate the effects of sex per se from other factors that in other species are inextricably linked with sex. We first summarize the evolution, development, and maintenance of ARTS. We then review immunoecological hypotheses relevant to species with ARTS, dividing them into physiological, life-history, and ecological hypotheses. In context of these hypotheses, we critically review in detail all immunoecological studies we could find on species with ARTS. Several interesting patterns emerge. Oddly, there is a paucity of studies on insects, despite the many benefits that arise from working with insects: larger sample sizes, simple immune systems, and countless forms of alternative reproductive strategies and tactics. Of all the hypotheses considered, the immunocompetence handicap hypothesis has generated the greatest amount of work, but not necessarily the greatest level of understanding. Unfortunately, it is often used as a general guiding principle rather than a source of explicitly articulated predictions. Other hypotheses are usually considered a posteriori, but perhaps they should take centre stage. Whereas blanket concepts such as “immunocompetence” and “androgens” might be useful to develop a rationale, predictions need to be far more explicitly articulated. Integration so far has been a one-way street, with ecologists delving deeper into physiology, sometimes at the cost of ignoring their organisms’ evolutionary history and ecology. One possible useful framework is to divide ecological and evolutionary factors affecting immunity into those that stimulate the immune system, and those that depress it. Finally, the contributions of genomics to ecology are being increasingly recognized and sometimes applied to species with ARTS, but we must ensure that evolutionary and ecological hypotheses drive the effort, as there is no grandeur in the strict reductionist view of life.
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18
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Duh M, Skok K, Perc M, Markota A, Gosak M. Computational modeling of targeted temperature management in post-cardiac arrest patients. Biomech Model Mechanobiol 2022; 21:1407-1424. [PMID: 35763192 DOI: 10.1007/s10237-022-01598-x] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/27/2022] [Accepted: 05/23/2022] [Indexed: 11/28/2022]
Abstract
Our core body temperature is held around [Formula: see text]C by an effective internal thermoregulatory system. However, various clinical scenarios have a more favorable outcome under external temperature regulation. Therapeutic hypothermia, for example, was found beneficial for the outcome of resuscitated cardiac arrest patients due to its protection against cerebral ischemia. Nonetheless, practice shows that outcomes of targeted temperature management vary considerably in dependence on individual tissue damage levels and differences in therapeutic strategies and protocols. Here, we address these differences in detail by means of computational modeling. We develop a multi-segment and multi-node thermoregulatory model that takes into account details related to specific post-cardiac arrest-related conditions, such as thermal imbalances due to sedation and anesthesia, increased metabolic rates induced by inflammatory processes, and various external cooling techniques. In our simulations, we track the evolution of the body temperature in patients subjected to post-resuscitation care, with particular emphasis on temperature regulation via an esophageal heat transfer device, on the examination of the alternative gastric cooling with ice slurry, and on how anesthesia and the level of inflammatory response influence thermal behavior. Our research provides a better understanding of the heat transfer processes and therapies used in post-cardiac arrest patients.
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Affiliation(s)
- Maja Duh
- Faculty of Natural Sciences and Mathematics, University of Maribor, Koroška cesta 160, 2000, Maribor, Slovenia
| | - Kristijan Skok
- Faculty of Medicine, University of Maribor, Taborska ulica 8, 2000, Maribor, Slovenia.,Department of Pathology, General Hospital Graz II, Location West, Göstinger Straße 22, 8020, Graz, Austria
| | - Matjaž Perc
- Faculty of Natural Sciences and Mathematics, University of Maribor, Koroška cesta 160, 2000, Maribor, Slovenia.,Department of Medical Research, China Medical University Hospital, China Medical University, Taichung, 404332, Taiwan.,Alma Mater Europaea, Slovenska ulica 17, 2000, Maribor, Slovenia.,Complexity Science Hub Vienna, Josefstädterstraße 39, 1080, Vienna, Austria
| | - Andrej Markota
- Faculty of Medicine, University of Maribor, Taborska ulica 8, 2000, Maribor, Slovenia.,Medical Intensive Care Unit, University Medical Centre Maribor, Ljubljanska 5, 2000, Maribor, Slovenia
| | - Marko Gosak
- Faculty of Natural Sciences and Mathematics, University of Maribor, Koroška cesta 160, 2000, Maribor, Slovenia. .,Faculty of Medicine, University of Maribor, Taborska ulica 8, 2000, Maribor, Slovenia.
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19
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Pontzer H, McGrosky A. Balancing growth, reproduction, maintenance, and activity in evolved energy economies. Curr Biol 2022; 32:R709-R719. [PMID: 35728556 DOI: 10.1016/j.cub.2022.05.018] [Citation(s) in RCA: 29] [Impact Index Per Article: 9.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/15/2022]
Abstract
Economic models predominate in life history research, which investigates the allocation of an organism's resources to growth, reproduction, and maintenance. These approaches typically employ a heuristic Y model of resource allocation, which predicts trade-offs among tasks within a fixed budget. The common currency among tasks is not always specified, but most models imply that metabolic energy, either from food or body stores, is the critical resource. Here, we review the evidence for metabolic energy as the common currency of growth, reproduction, and maintenance, focusing on studies in humans and other vertebrates. We then discuss the flow of energy to competing physiological tasks (physical activity, maintenance, and reproduction or growth) and its effect on life history traits. We propose a Ψ model of energy flow to these tasks, which provides an integrative framework for examining the influence of environmental factors and the expansion and contraction of energy budgets in the evolution of life history strategies.
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Affiliation(s)
- Herman Pontzer
- Department of Evolutionary Anthropology, Duke University, Durham, NC, USA; Duke Global Health Institute, Duke University, Durham, NC, USA.
| | - Amanda McGrosky
- Department of Evolutionary Anthropology, Duke University, Durham, NC, USA
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20
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Buttemer WA, O'Dwyer TW, Astheimer LB, Klasing KC, Hoye BJ. No evidence of metabolic costs following adaptive immune activation or reactivation in house sparrows. Biol Lett 2022; 18:20220036. [PMID: 35702980 PMCID: PMC9198745 DOI: 10.1098/rsbl.2022.0036] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/30/2022] [Accepted: 05/30/2022] [Indexed: 11/12/2022] Open
Abstract
The energy cost of adaptive immune activation in endotherms is typically quantified from changes in resting metabolic rate following exposure to a novel antigen. An implicit assumption of this technique is that all variation in energy costs following antigenic challenge is due solely to adaptive immunity, while ignoring potential changes in the energy demands of ongoing bodily functions. We critically assess this assumption by measuring both basal metabolic rate (BMR) and exercise-induced maximal metabolic rate (MMR) in house sparrows before and after the primary and two subsequent vaccinations with either saline (sham) or two novel antigens (keyhole limpet haemocyanin and sheep red blood cells; KLH and SRBC, respectively). We also examined the effect of inducing male breeding levels of testosterone (T) on immune responses and their metabolic costs in both males and females. Although there was a moderate decrease in KLH antibody formation in T-treated birds, there was no effect of T on BMR, MMR or immunity to SRBC. There was no effect of vaccination on BMR but, surprisingly, all vaccinated birds maintained MMR better than sham-treated birds as the experiment progressed. Our findings caution against emphasizing energy costs or nutrient diversion as being responsible for reported fitness reductions following activation of adaptive immunity.
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Affiliation(s)
- William A. Buttemer
- School of Earth, Atmospheric and Life Sciences, University of Wollongong, Wollongong, NSW 2522, Australia
| | - Terence W. O'Dwyer
- School of Earth, Atmospheric and Life Sciences, University of Wollongong, Wollongong, NSW 2522, Australia
| | - Lee B. Astheimer
- School of Medicine, University of Wollongong, Wollongong, NSW 2522, Australia
| | - Kirk C. Klasing
- Department of Animal Science, University of California, Davis, CA 95616-5270, USA
| | - Bethany J. Hoye
- School of Earth, Atmospheric and Life Sciences, University of Wollongong, Wollongong, NSW 2522, Australia
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21
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Hunt R, Cable J, Ellison A. Daily patterns in parasite processes: diel variation in fish louse transcriptomes. Int J Parasitol 2022; 52:509-518. [PMID: 35533730 DOI: 10.1016/j.ijpara.2022.04.001] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/15/2021] [Revised: 04/07/2022] [Accepted: 04/07/2022] [Indexed: 11/05/2022]
Abstract
Parasites, similar to all other organisms, time themselves to environmental cues using a molecular clock to generate and maintain rhythms. Chronotherapeutic (timed treatment) techniques based on such rhythms offer great potential for improving control of chronic, problematic parasites. Fish lice are a key disease threat in aquaculture, with current control insufficient. Assessing the rhythmicity of fish lice transcriptomes offers not only insight into the viability of chronotherapy, but the opportunity to identify new drug targets. Here, for the first known time in any crustacean parasite, diel changes in gene transcription are examined, revealing that approximately half of the Argulus foliaceus annotated transcriptome displays significant daily rhythmicity. We identified rhythmically transcribed putative clock genes including core clock/cycle and period/timeless pairs, alongside rhythms in feeding-associated genes and processes involving immune response, as well as fish louse drug targets. A substantial number of gene pathways showed peak transcription in hours immediately preceding onset of light, potentially in anticipation of peak host anti-parasite responses or in preparation for increased feeding activity. Genes related to immune haemocyte activity and chitin development were more highly transcribed 4 h post light onset, although inflammatory gene transcription was highest during dark periods. Our study provides an important resource for application of chronotherapy in fish lice; timed application could increase efficacy and/or reduce dose requirement, improving the current landscape of drug resistance and fish health while reducing the economic cost of infection.
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Affiliation(s)
- R Hunt
- School of Biosciences, Cardiff University, Cardiff CF10 3AX, United Kingdom
| | - J Cable
- School of Biosciences, Cardiff University, Cardiff CF10 3AX, United Kingdom
| | - A Ellison
- School of Natural Sciences, Bangor University, Deiniol Road, Bangor, Gwynedd, LL57 2UW, United Kingdom.
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22
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Josefson CC, Zohdy S, Hood WR. Methodological Considerations for Assessing Immune Defense in Reproductive Females. Integr Comp Biol 2021; 60:732-741. [PMID: 32818268 DOI: 10.1093/icb/icaa098] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/14/2022] Open
Abstract
One of the key foci of ecoimmunology is understanding the physiological interactions between reproduction and immune defense. To assess an immune challenge, investigators typically measure an immune response at a predetermined time point that was selected to represent a peak response. These time points often are based on the immunological responses of nonreproductive males. Problematically, these peaks have been applied to studies quantifying immune responses of females during reproduction, despite the fact that nonreproductive males and reproductive females display fundamentally different patterns of energy expenditure. Previous work within pharmacological research has reported that the response to the commonly-used antigen keyhole limpet hemocyanin (KLH) varies among individuals and between females and males. In this heuristic analysis, we characterize antibody responses to KLH in females with varying reproductive demands (nonreproductive, lactating, concurrently lactating, and pregnant). Serum was taken from one animal per day per group and assessed for general and specific Immunoglobulins (Igs) G and M. We then used regression analysis to characterize the antibody response curves across groups. Our results demonstrate that the antibody response curve is asynchronous among females with varying maternal demands and temporally differs from the anticipated peak responses reflected in standardized protocols. These findings highlight the importance of multiple sampling points across treatment groups for a more integrative assessment of how reproductive demand alters antibody responses in females beyond a single measurement.
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Affiliation(s)
- Chloe C Josefson
- Department of Animal and Veterinary Science, University of Idaho, Moscow, ID, USA.,Department of Biological Sciences, Auburn University, Auburn, AL, USA
| | - Sarah Zohdy
- School of Forestry and Wildlife Science, Auburn University, Auburn, AL, USA
| | - Wendy R Hood
- Department of Biological Sciences, Auburn University, Auburn, AL, USA
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23
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Love AC, Grisham K, Krall JB, Goodchild CG, DuRant SE. Perception of infection: disease-related social cues influence immunity in songbirds. Biol Lett 2021; 17:20210125. [PMID: 34102069 PMCID: PMC8187024 DOI: 10.1098/rsbl.2021.0125] [Citation(s) in RCA: 12] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/01/2021] [Accepted: 05/18/2021] [Indexed: 12/13/2022] Open
Abstract
While avoidance of sick conspecifics is common among animals, little is known about how detecting diseased conspecifics influences an organism's physiological state, despite its implications for disease transmission dynamics. The avian pathogen Mycoplasma gallisepticum (MG) causes obvious visual signs of infection in domestic canaries (Serinus canaria domestica), including lethargy and conjunctivitis, making this system a useful tool for investigating how the perception of cues from sick individuals shapes immunity in healthy individuals. We tested whether disease-related social information can stimulate immune responses in canaries housed in visual contact with either healthy or MG-infected conspecifics. We found higher complement activity and higher heterophil counts in healthy birds viewing MG-infected individuals around 6-12 days post-inoculation, which corresponded with the greatest degree of disease pathology in infected stimulus birds. However, we did not detect the effects of disease-related social cues on the expression of two proinflammatory cytokines in the blood. These data indicate that social cues of infection can alter immune responses in healthy individuals and suggest that public information about the disease can shape how individuals respond to infection.
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Affiliation(s)
- Ashley C. Love
- Department of Integrative Biology, Oklahoma State University, 501 Life Sciences West, Stillwater, OK 74078, USA
- Department of Biological Sciences, University of Arkansas, 601 Science and Engineering, Fayetteville, AR 72701, USA
- Department of Ecology and Evolutionary Biology, University of Connecticut, 75 North Eagleville Road, Storrs, CT 06269, USA
| | - Kevin Grisham
- Department of Integrative Biology, Oklahoma State University, 501 Life Sciences West, Stillwater, OK 74078, USA
| | - Jeffrey B. Krall
- Department of Integrative Biology, Oklahoma State University, 501 Life Sciences West, Stillwater, OK 74078, USA
| | - Christopher G. Goodchild
- Department of Biology, University of Central Oklahoma, 100 North University Drive, Edmond, OK 73034, USA
| | - Sarah E. DuRant
- Department of Biological Sciences, University of Arkansas, 601 Science and Engineering, Fayetteville, AR 72701, USA
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24
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Roth AM, Keiser CN, Williams JB, Gee JM. Prevalence and intensity of avian malaria in a quail hybrid zone. Ecol Evol 2021; 11:8123-8135. [PMID: 34188875 PMCID: PMC8216944 DOI: 10.1002/ece3.7645] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/07/2020] [Revised: 04/14/2021] [Accepted: 04/19/2021] [Indexed: 01/12/2023] Open
Abstract
Hybrid zones have been described as natural laboratories by researchers who study speciation and the various mechanisms that may affect gene flow. The evolutionary consequences of hybridization depend not only on reproductive compatibility between sympatric species, but also on factors like vulnerability to each other's predators and parasites. We examined infection patterns of the blood parasite Haemoproteus lophortyx, a causative agent of avian malaria, at a site in the contact zone between California quail (Callipepla californica) and Gambel's quail (C. gambelii). Controlling for the potential influence of sex and year, we tested whether species identity predicted infection status and intensity. We found that infection prevalence was lower in California and hybrid quail compared with Gambel's quail. However, infected California and hybrid quail had higher infection intensities than Gambel's quail. California and hybrid quail exhibited no significant differences in prevalence or intensity of infection. These findings suggest that infection by H. lophortyx has the potential to influence species barrier dynamics in this system; however, more work is necessary to determine the exact evolutionary consequences of this blood parasite on hybridization.
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Affiliation(s)
| | - Carl N. Keiser
- Department of BiologyUniversity of FloridaGainesvilleFLUSA
| | - Judson B. Williams
- Department of Ecology and Evolutionary BiologyPrinceton UniversityPrincetonNJUSA
- Present address:
Department of SurgeryDuke UniversityRaleighNCUSA
| | - Jennifer M. Gee
- Department of Ecology and Evolutionary BiologyPrinceton UniversityPrincetonNJUSA
- Present address:
James San Jacinto Mountains ReserveUniversity of California – RiversideUniversity of California Natural Reserve SystemIdyllwildCAUSA
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25
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Zerjal T, Härtle S, Gourichon D, Guillory V, Bruneau N, Laloë D, Pinard-van der Laan MH, Trapp S, Bed'hom B, Quéré P. Assessment of trade-offs between feed efficiency, growth-related traits, and immune activity in experimental lines of layer chickens. Genet Sel Evol 2021; 53:44. [PMID: 33957861 PMCID: PMC8101249 DOI: 10.1186/s12711-021-00636-z] [Citation(s) in RCA: 25] [Impact Index Per Article: 6.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/08/2019] [Accepted: 04/19/2021] [Indexed: 11/10/2022] Open
Abstract
Background In all organisms, life-history traits are constrained by trade-offs, which may represent physiological limitations or be related to energy resource management. To detect trade-offs within a population, one promising approach is the use of artificial selection, because intensive selection on one trait can induce unplanned changes in others. In chickens, the breeding industry has achieved remarkable genetic progress in production and feed efficiency over the last 60 years. However, this may have been accomplished at the expense of other important biological functions, such as immunity. In the present study, we used three experimental lines of layer chicken—two that have been divergently selected for feed efficiency and one that has been selected for increased antibody response to inactivated Newcastle disease virus (ND3)—to explore the impact of improved feed efficiency on animals’ immunocompetence and, vice versa, the impact of improved antibody response on animals’ growth and feed efficiency. Results There were detectable differences between the low (R+) and high (R−) feed-efficiency lines with respect to vaccine-specific antibody responses and counts of monocytes, heterophils, and/or T cell population. The ND3 line presented reduced body weight and feed intake compared to the control line. ND3 chickens also demonstrated an improved antibody response against a set of commercial viral vaccines, but lower blood leucocyte counts. Conclusions This study demonstrates the value of using experimental chicken lines that are divergently selected for RFI or for a high antibody production, to investigate the modulation of immune parameters in relation to growth and feed efficiency. Our results provide further evidence that long-term selection for the improvement of one trait may have consequences on other important biological functions. Hence, strategies to ensure optimal trade-offs among competing functions will ultimately be required in multi-trait selection programs in livestock. Supplementary Information The online version contains supplementary material available at 10.1186/s12711-021-00636-z.
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Affiliation(s)
- Tatiana Zerjal
- INRAE, AgroParisTech, Université Paris-Saclay, GABI, 78350, Jouy-en-Josas, France.
| | - Sonja Härtle
- Avian Immunology Group, Department for Veterinary Sciences, LMU Munich, Munich, Germany
| | | | | | - Nicolas Bruneau
- INRAE, AgroParisTech, Université Paris-Saclay, GABI, 78350, Jouy-en-Josas, France
| | - Denis Laloë
- INRAE, AgroParisTech, Université Paris-Saclay, GABI, 78350, Jouy-en-Josas, France
| | | | - Sascha Trapp
- INRAE, UMR 1282, ISP, Université de Tours, 37380, Nouzilly, France
| | - Bertrand Bed'hom
- INRAE, AgroParisTech, Université Paris-Saclay, GABI, 78350, Jouy-en-Josas, France.,ISYEB, Muséum National D'Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université Des Antilles, 75005, Paris, France
| | - Pascale Quéré
- INRAE, UMR 1282, ISP, Université de Tours, 37380, Nouzilly, France
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Transcriptome profiling of Lymnaea stagnalis (Gastropoda) for ecoimmunological research. BMC Genomics 2021; 22:144. [PMID: 33648459 PMCID: PMC7919325 DOI: 10.1186/s12864-021-07428-1] [Citation(s) in RCA: 12] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/15/2020] [Accepted: 02/05/2021] [Indexed: 12/14/2022] Open
Abstract
BACKGROUND Host immune function can contribute to numerous ecological/evolutionary processes. Ecoimmunological studies, however, typically use one/few phenotypic immune assays and thus do not consider the complexity of the immune system. Therefore, "omics" resources that allow quantifying immune activity across multiple pathways are needed for ecoimmunological models. We applied short-read based RNAseq (Illumina NextSeq 500, PE-81) to characterise transcriptome profiles of Lymnaea stagnalis (Gastropoda), a multipurpose model snail species. We used a genetically diverse snail stock and exposed individuals to immune elicitors (injury, bacterial/trematode pathogens) and changes in environmental conditions that can alter immune activity (temperature, food availability). RESULTS Immune defence factors identified in the de novo assembly covered elements broadly described in other gastropods. For instance, pathogen-recognition receptors (PRR) and lectins activate Toll-like receptor (TLR) pathway and cytokines that regulate cellular and humoral defences. Surprisingly, only modest diversity of antimicrobial peptides and fibrinogen related proteins were detected when compared with other taxa. Additionally, multiple defence factors that may contribute to the phenotypic immune assays used to quantify antibacterial activity and phenoloxidase (PO)/melanisation-type reaction in this species were found. Experimental treatments revealed factors from non-self recognition (lectins) and signalling (TLR pathway, cytokines) to effectors (e.g., antibacterial proteins, PO enzymes) whose transcription depended on immune stimuli and environmental conditions, as well as components of snail physiology/metabolism that may drive these effects. Interestingly, the transcription of many factors (e.g., PRR, lectins, cytokines, PO enzymes, antibacterial proteins) showed high among-individual variation. CONCLUSIONS Our results indicate several uniform aspects of gastropod immunity, but also apparent differences between L. stagnalis and some previously examined taxa. Interestingly, in addition to immune defence factors that responded to immune elicitors and changes in environmental conditions, many factors showed high among-individual variation across experimental snails. We propose that such factors are highly important to be included in future ecoimmunological studies because they may be the key determinants of differences in parasite resistance among individuals both within and between natural snail populations.
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Johnson RM, Olatunde AC, Woodie LN, Greene MW, Schwartz EH. The Systemic and Cellular Metabolic Phenotype of Infection and Immune Response to Listeria monocytogenes. Front Immunol 2021; 11:614697. [PMID: 33628207 PMCID: PMC7897666 DOI: 10.3389/fimmu.2020.614697] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/06/2020] [Accepted: 12/21/2020] [Indexed: 12/24/2022] Open
Abstract
It is widely accepted that infection and immune response incur significant metabolic demands, yet the respective demands of specific immune responses to live pathogens have not been well delineated. It is also established that upon activation, metabolic pathways undergo shifts at the cellular level. However, most studies exploring these issues at the systemic or cellular level have utilized pathogen associated molecular patterns (PAMPs) that model sepsis, or model antigens at isolated time points. Thus, the dynamics of pathogenesis and immune response to a live infection remain largely undocumented. To better quantitate the metabolic demands induced by infection, we utilized a live pathogenic infection model. Mice infected with Listeria monocytogenes were monitored longitudinally over the course of infection through clearance. We measured systemic metabolic phenotype, bacterial load, innate and adaptive immune responses, and cellular metabolic pathways. To further delineate the role of adaptive immunity in the metabolic phenotype, we utilized two doses of bacteria, one that induced both sickness behavior and protective (T cell mediated) immunity, and the other protective immunity alone. We determined that the greatest impact to systemic metabolism occurred during the early immune response, which coincided with the greatest shift in innate cellular metabolism. In contrast, during the time of maximal T cell expansion, systemic metabolism returned to resting state. Taken together, our findings demonstrate that the timing of maximal metabolic demand overlaps with the innate immune response and that when the adaptive response is maximal, the host has returned to relative metabolic homeostasis.
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Affiliation(s)
- Robert M Johnson
- Department of Biological Sciences, Auburn University, Auburn, AL, United States
| | - Adesola C Olatunde
- Department of Biological Sciences, Auburn University, Auburn, AL, United States
| | - Lauren N Woodie
- Department of Nutrition, Dietetics, and Hospitality Management, Auburn University, Auburn, AL, United States
| | - Michael W Greene
- Department of Nutrition, Dietetics, and Hospitality Management, Auburn University, Auburn, AL, United States
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Zhang Y, Hill GE, Ge Z, Park NR, Taylor HA, Andreasen V, Tardy L, Kavazis AN, Bonneaud C, Hood WR. Effects of a Bacterial Infection on Mitochondrial Function and Oxidative Stress in a Songbird. Physiol Biochem Zool 2021; 94:71-82. [PMID: 33399516 DOI: 10.1086/712639] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/03/2022]
Abstract
AbstractAs a major physiological mechanism involved in cellular renewal and repair, immune function is vital to the body's capacity to support tissue maintenance and organismal survival. Because immune defenses can be energetically expensive, the activities of metabolically active organs, such as the liver, are predicted to increase during infection by most pathogens. However, some pathogens are immunosuppressive, which might reduce the metabolic capacities of select organs to suppress immune response. Mycoplasma gallisepticum (MG) is a well-known immunosuppressive bacterium that infects domestic chickens and turkeys as well as songbirds. In the house finch (Haemorhous mexicanus), which is the primary host for MG among songbird species, MG infects both the respiratory system and the conjunctiva of the eye, causing conspicuous swelling. To study the effect of a systemic bacterial infection on cellular respiration and oxidative damage in the house finch, we measured mitochondrial respiration, mitochondrial membrane potential, reactive oxygen species production, and oxidative damage in the livers of house finches that were wild caught and either infected with MG, as indicated by genetic screening for the pathogen, or free of MG infection. We observed that MG-infected house finches showed significantly lower oxidative lipid and protein damage in liver tissue compared with their uninfected counterparts. Moreover, using complex II substrates, we documented a nonsignificant trend for lower state 3 respiration of liver mitochondria in MG-infected house finches compared with uninfected house finches (P=0.07). These results are consistent with the hypothesis that MG suppresses organ function in susceptible hosts.
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The immune response of bats differs between pre-migration and migration seasons. Sci Rep 2020; 10:17384. [PMID: 33060711 PMCID: PMC7562910 DOI: 10.1038/s41598-020-74473-3] [Citation(s) in RCA: 18] [Impact Index Per Article: 3.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/15/2020] [Accepted: 09/03/2020] [Indexed: 12/21/2022] Open
Abstract
Maintaining a competent immune system is energetically costly and thus immunity may be traded against other costly traits such as seasonal migration. Here, we tested in long-distance migratory Nathusius’ pipistrelles (Pipistrellus nathusii), if selected branches of immunity are expressed differently in response to the energy demands and oxidative stress of aerial migration. During the migration period, we observed higher baseline lymphocyte and lower neutrophil levels than during the pre-migration period, but no stronger response of cellular effectors to an antigen challenge. Baseline plasma haptoglobin, as a component of the humoral innate immunity, remained similar during both seasons, yet baseline plasma haptoglobin levels increased by a factor of 7.8 in migratory bats during an immune challenge, whereas they did not change during the pre-migration period. Oxidative stress was higher during migration than during pre-migration, yet there was no association between blood oxidative status and immune parameters, and immune challenge did not trigger any changes in oxidative stress, irrespective of season. Our findings suggest that humoral effectors of the acute phase response may play a stronger role in the first-line defense against infections for migrating bats compared to non-migrating bats. We conclude that Nathusius’ pipistrelles allocate resources differently into the branches of their immune system, most likely following current demands resulting from tight energy budgets during migration.
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Vasilieva NY, Khrushchova AM, Kuptsov AV, Shekarova ON, Sokolova OV, Wang D, Rogovin KA. On the winter enhancement of adaptive humoral immunity: hypothesis testing in desert hamsters (Phodopus roborovskii: Cricetidae, Rodentia) kept under long-day and short-day photoperiod. Integr Zool 2020; 15:232-247. [PMID: 31773894 DOI: 10.1111/1749-4877.12419] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/25/2022]
Abstract
We tested the winter immunity enhancement hypothesis (WIEH) on male desert hamsters (Phodopus roborovskii) kept under long-day (LD) and short-day (SD) photoperiods. We assumed that under SD in a laboratory, the adaptive humoral immune responsiveness to the antigenic challenge would be enhanced due to the lack of winter physical stressors and food shortages and/or because of the action of an endogenous winter bolstering mechanism, while under LD the immune responsiveness would be suppressed by the activity of the reproductive system. The results support the WIEH in part. We did not find a difference in antibody production in response to sheep erythrocytes between SD and LD hamsters, but SD males had the lower number of granulocytes and the higher number of lymphocytes in white blood cell counts. Reproductive activity was lower in SD males. These males demonstrated an increase in their mass-specific resting metabolic rate, their mass-specific maximal metabolic rate and their level of cortisol. The result of a generalized linear model analysis indicates the negative effect on secondary immunoresponsiveness to sheep erythrocytes of mid-ventral gland size, the organ characterizing individual reproductive quality, and designates a tradeoff between antibody production and reproductive effort. The mass-independent maximal metabolic rate also negatively affected antibody production, indicating a tradeoff between maximal aerobic performance and the adaptive immune function. The higher stress in SD males seems to be the most likely reason for the lack of the effect of daylight duration on antibody production.
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Affiliation(s)
| | | | | | - Olga N Shekarova
- Severtsov Institute of Ecology and Evolution RAS, Moscow, Russia
| | - Olga V Sokolova
- Severtsov Institute of Ecology and Evolution RAS, Moscow, Russia
| | - Dehua Wang
- Institute of Zoology Chinese Academy of Science, Chaoyang District, Beijing, China
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Balan P, Staincliffe M, Moughan PJ. Effects of spray-dried animal plasma on the growth performance of weaned piglets-A review. J Anim Physiol Anim Nutr (Berl) 2020; 105:699-714. [PMID: 32860645 DOI: 10.1111/jpn.13435] [Citation(s) in RCA: 17] [Impact Index Per Article: 3.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/01/2020] [Revised: 07/06/2020] [Accepted: 07/16/2020] [Indexed: 12/14/2022]
Abstract
Spray-dried animal plasma sourced from bovine, porcine or other animal origin is often used as a main feed ingredient in the diets of weanling piglets to improve growth performance. The objective of this study was to determine the effect of animal plasma in diets on the performance of piglets in the post-weaning period, with and/or without pathogenic challenge, by undertaking a meta-analysis. Data were extracted from peer-reviewed reports published in scientific journals. The average initial weight of the piglets was 5.8 kg and the average initial age 19 days (2-56 days). The average duration of feeding animal plasma was 40 days. Average daily gain (ADG), feed intake (ADFI) and feed conversion ratio (FCR) were found to be 22-28 g/day, 20-27 g/day and -0.28 to 0.06 g/g. Generally, diet supplemented with spray-dried bovine plasma (SDBP) improved the ADG of the piglets and spray-dried porcine plasma (SDPP) led to increases in the ADFI. For the first week post-weaning alone, as the dietary animal plasma percentage increased there was an increase in ADG and ADFI; similarly, the latter two measures increased as weaning age increased. The evidence suggests that mainly IgG present in animal plasma prevents the binding of pathogens to the gut wall and reduces the incidence of sub-clinical infection in the post-weaning stage. Animal plasma containing IgG appears to be a useful in-feed supplement for piglets in the post-weaning phase.
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Affiliation(s)
- Prabhu Balan
- Riddet Institute, Alpha-Massey Natural Nutraceutical Research Centre, Massey University, Palmerston North, New Zealand
| | | | - Paul J Moughan
- Riddet Institute, Alpha-Massey Natural Nutraceutical Research Centre, Massey University, Palmerston North, New Zealand
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Sun L, Zhou F, Shao Y, Lv Z, Li C. Sedoheptulose kinase bridges the pentose phosphate pathway and immune responses in pathogen-challenged sea cucumber Apostichopus japonicus. DEVELOPMENTAL AND COMPARATIVE IMMUNOLOGY 2020; 109:103694. [PMID: 32283109 DOI: 10.1016/j.dci.2020.103694] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 02/06/2020] [Revised: 03/30/2020] [Accepted: 03/30/2020] [Indexed: 06/11/2023]
Abstract
The sedoheptulose kinase carbohydrate kinase-like protein (CARKL) is critical for immune cell activation, reactive oxygen species (ROS) production, and cell polarization by restricting flux through the pentose phosphate pathway (PPP). To date, little is known about CARKL in regulating immune responses in marine invertebrates. In this study, we first cloned and characterized the CARKL gene from Apostichopus japonicus (designated as AjCARKL). Time-course analysis revealed that Vibrio splendidus challenge in vivo and lipopolysaccharide stimulation in vitro significantly downregulated AjCARKL mRNA expression. Furthermore, AjCARKL overexpression in cultured coelomocytes not only significantly inhibited the mRNA expression level of the rate-limiting enzyme glucose-6-phosphate dehydrogenase of the PPP but sharply decreased coelomocyte proliferation, ROS production, and phagocytic rate. Additionally, AjCARKL overexpression in mouse peritoneal macrophages (RAW264.7 cells) significantly attenuated the intracellular ROS production and sensitized the M2 phenotype macrophage polarization. These results revealed that AjCARKL serves as a rheostat for cellular metabolism and is required for proper immune response by negatively regulating PPP in pathogen-challenged A. japonicus.
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Affiliation(s)
- Lianlian Sun
- State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, PR China
| | - Fangyuan Zhou
- State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, PR China
| | - Yina Shao
- State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, PR China
| | - Zhimeng Lv
- State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, PR China
| | - Chenghua Li
- State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, PR China; Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266071, PR China.
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Nord A, Hegemann A, Folkow LP. Reduced immune responsiveness contributes to winter energy conservation in an Arctic bird. J Exp Biol 2020; 223:223/8/jeb219287. [DOI: 10.1242/jeb.219287] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/25/2019] [Accepted: 03/11/2020] [Indexed: 12/20/2022]
Abstract
ABSTRACT
Animals in seasonal environments must prudently manage energy expenditure to survive the winter. This may be achieved through reductions in the allocation of energy for various purposes (e.g. thermoregulation, locomotion, etc.). We studied whether such trade-offs also include suppression of the innate immune response, by subjecting captive male Svalbard ptarmigan (Lagopus muta hyperborea) to bacterial lipopolysaccharide (LPS) during exposure to either mild temperature (0°C) or cold snaps (acute exposure to −20°C), in constant winter darkness when birds were in energy-conserving mode, and in constant daylight in spring. The innate immune response was mostly unaffected by temperature. However, energy expenditure was below baseline when birds were immune challenged in winter, but significantly above baseline in spring. This suggests that the energetic component of the innate immune response was reduced in winter, possibly contributing to energy conservation. Immunological parameters decreased (agglutination, lysis, bacteriostatic capacity) or did not change (haptoglobin/PIT54) after the challenge, and behavioural modifications (anorexia, mass loss) were lengthy (9 days). While we did not study the mechanisms explaining these weak, or slow, responses, it is tempting to speculate they may reflect the consequences of having evolved in an environment where pathogen transmission rate is presumably low for most of the year. This is an important consideration if climate change and increased exploitation of the Arctic would alter pathogen communities at a pace outwith counter-adaption in wildlife.
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Affiliation(s)
- Andreas Nord
- Department of Biology, Lund University, SE-223 62 Lund, Sweden
- Department of Arctic and Marine Biology, University of Tromsø – the Arctic University of Norway, NO-9037 Tromsø, Norway
- Scottish Centre for Ecology and the Natural Environment, Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Rowardennan G63 0AW, UK
| | - Arne Hegemann
- Department of Biology, Lund University, SE-223 62 Lund, Sweden
| | - Lars P. Folkow
- Department of Arctic and Marine Biology, University of Tromsø – the Arctic University of Norway, NO-9037 Tromsø, Norway
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Trillmich F, Guenther A, Jäckel M, Czirják GÁ. Reproduction affects immune defenses in the guinea pig even under ad libitum food. PLoS One 2020; 15:e0230081. [PMID: 32176718 PMCID: PMC7075551 DOI: 10.1371/journal.pone.0230081] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/28/2019] [Accepted: 02/20/2020] [Indexed: 11/29/2022] Open
Abstract
Reproduction is one of the costliest processes in the life of an animal. Life history theory assumes that when resources are limiting allocation to reproduction will reduce allocation to other essential processes thereby inducing costs of reproduction. The immune system is vital for survival. If reproduction reduces investment in immune function, this could increase the risk of disease, morbidity and mortality. We here test in the guinea pig, if even under ad libitum food conditions, pregnancy and lactation reduce the activity of the adaptive and innate immune system compared to the reaction of non-reproducing animals. In response to a challenge with keyhole limpet haemocyanin the antibody-mediated adaptive immunity during (pregnancy and) lactation was reduced. Pregnant and lactating females showed higher levels of bacterial killing activity, an integrated measure of innate immunity, than non-reproducing females. However, two major effectors of the innate immunity, the natural antibody and the complement of pregnant and lactating females showed lower levels than in non-reproducing females. Pregnant and lactating females did not differ significantly in the expressed levels of innate immunity. Our results indicate that changes in the immune response during reproduction are physiological adjustments to predictable allocation problems, because they happen even under ad libitum food availability.
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Affiliation(s)
- Fritz Trillmich
- Department of Animal Behaviour, University Bielefeld, Bielefeld, Germany
| | - Anja Guenther
- Department of Animal Behaviour, University Bielefeld, Bielefeld, Germany
- Max-Planck Institute for Evolutionary Biology, Evolutionary Genetics, Plön, Germany
| | - Manuela Jäckel
- Department of Animal Behaviour, University Bielefeld, Bielefeld, Germany
| | - Gábor Á. Czirják
- Department of Wildlife Diseases, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany
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Colgan TJ, Finlay S, Brown MJF, Carolan JC. Mating precedes selective immune priming which is maintained throughout bumblebee queen diapause. BMC Genomics 2019; 20:959. [PMID: 31823732 PMCID: PMC6902353 DOI: 10.1186/s12864-019-6314-9] [Citation(s) in RCA: 13] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/18/2019] [Accepted: 11/20/2019] [Indexed: 01/04/2023] Open
Abstract
Background Understanding the mechanisms by which organisms adapt to unfavourable conditions is a fundamental question in ecology and evolutionary biology. One such mechanism is diapause, a period of dormancy typically found in nematodes, fish, crustaceans and insects. This state is a key life-history event characterised by arrested development, suppressed metabolism and increased stress tolerance and allows an organism to avoid prolonged periods of harsh and inhospitable environmental conditions. For some species, diapause is preceded by mating which can have a profound effect on female behaviour, physiology and key biological processes, including immunity. However, our understanding of how mating impacts long-term immunity and whether these effects persist throughout diapause is currently limited. To address this, we explored molecular changes in the haemolymph of the ecologically important pollinator, the buff-tailed bumblebee Bombus terrestris. B. terrestris queens mate prior to entering diapause, a non-feeding period of arrested development that can last 6–9 months. Using mass-spectrometry-based proteomics, we quantified changes in the pre-diapause queen haemolymph after mating, as well as the subsequent protein expression of mated queens during and post-diapause. Results Our analysis identified distinct proteome profiles associated with diapause preparation, maintenance and termination. More specifically, mating pre-diapause was followed by an increase in the abundance of antimicrobial peptides, key effectors of the immune system. Furthermore, we identified the elevated abundance of these proteins to be maintained throughout diapause. This finding was in contrast to the general reduction observed in immune proteins during diapause suggestive of selective immune priming and expression during diapause. Diapause also affected the expression of proteins involved in cuticular maintenance, olfaction, as well as proteins of unknown function, which may have roles in diapause regulation. Conclusions Our results provide clear molecular evidence for the consequences and benefits of mating at the immune level as it precedes the selective increased abundance of antimicrobial peptides that are sustained throughout diapause. In addition, our results provide novel insights into the molecular mechanisms by which bumblebees prepare for, survive, and recover from diapause, insights that may have implications for our general understanding of these processes in other insect groups.
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Affiliation(s)
- Thomas J Colgan
- School of Biological, Earth and Environmental Sciences, University College Cork, Cork, County Cork, Ireland. .,School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London, E1 4NS, UK.
| | - Sive Finlay
- Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin 2, Ireland
| | - Mark J F Brown
- Centre for Ecology, Evolution and Behaviour, Department of Biological Sciences, Royal Holloway University of London, Egham, Surrey, TW20 0EX, UK
| | - James C Carolan
- Department of Biology, Maynooth University, Maynooth, County Kildare, Ireland
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Marschner C, Krockenberger MB, Higgins DP. Effects of Eucalypt Plant Monoterpenes on Koala (Phascolarctos Cinereus) Cytokine Expression In Vitro. Sci Rep 2019; 9:16545. [PMID: 31719541 PMCID: PMC6851357 DOI: 10.1038/s41598-019-52713-5] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/02/2018] [Accepted: 10/12/2019] [Indexed: 02/06/2023] Open
Abstract
Protective immunity is crucial for survival of any species, though the koala as a specialist feeder adapted to an exclusive diet of eucalypts that contain plant secondary metabolites of varying toxicity and of immunomodulatory property. Being constantly exposed to such dietary chemicals it raises the question of their immune effects in a specialist eucalypt feeder. This study demonstrates that natural levels of circulating eucalypt plant secondary metabolites have dose dependent in vitro effects on cytokine expression of koala peripheral blood mononuclear cells, suggesting a potential trade-off of reduced function in multiple arms of the immune system associated with koala's use of its specialized dietary niche.
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Affiliation(s)
- Caroline Marschner
- Sydney School of Veterinary Science, Faculty of Science, The University of Sydney, Camperdown, 2006, NSW, Australia.
| | - Mark B Krockenberger
- Sydney School of Veterinary Science, Faculty of Science, The University of Sydney, Camperdown, 2006, NSW, Australia
| | - Damien P Higgins
- Sydney School of Veterinary Science, Faculty of Science, The University of Sydney, Camperdown, 2006, NSW, Australia
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Fritze M, Costantini D, Fickel J, Wehner D, Czirják GÁ, Voigt CC. Immune response of hibernating European bats to a fungal challenge. Biol Open 2019; 8:bio.046078. [PMID: 31649120 PMCID: PMC6826279 DOI: 10.1242/bio.046078] [Citation(s) in RCA: 18] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/13/2022] Open
Abstract
Immunological responses of hibernating mammals are suppressed at low body temperatures, a possible explanation for the devastating effect of the white-nose syndrome on hibernating North American bats. However, European bats seem to cope well with the fungal causative agent of the disease. To better understand the immune response of hibernating bats, especially against fungal pathogens, we challenged European greater mouse-eared bats (Myotis myotis) by inoculating the fungal antigen zymosan. We monitored torpor patterns, immune gene expressions, different aspects of the acute phase response and plasma oxidative status markers, and compared them with sham-injected control animals at 30 min, 48 h and 96 h after inoculation. Torpor patterns, body temperatures, body masses, white blood cell counts, expression of immune genes, reactive oxygen metabolites and non-enzymatic antioxidant capacity did not differ between groups during the experiment. However, zymosan injected bats had significantly higher levels of haptoglobin than the control animals. Our results indicate that hibernating greater mouse-eared bats mount an inflammatory response to a fungal challenge, with only mild to negligible consequences for the energy budget of hibernation. Our study gives a first hint that hibernating European bats may have evolved a hibernation-adjusted immune response in order to balance the trade-off between competent pathogen elimination and a prudent energy-saving regime. Summary: Our experimental immunological study on European bats provides new information on the functionality of the immune system in hibernation. For this we challenged bats with a fungal antigen and measured different immunological parameters.
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Affiliation(s)
- Marcus Fritze
- Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315 Berlin, Germany .,Institute of Biology, Free University of Berlin, Takustr. 6, 14195 Berlin, Germany
| | - David Costantini
- Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315 Berlin, Germany.,Unité Physiologie moléculaire et adaptation (PhyMA), Muséum National d'Histoire Naturelle, CNRS; CP32, 57 rue Cuvier 75005 Paris, France
| | - Jörns Fickel
- Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315 Berlin, Germany.,University of Potsdam, Institute for Biochemistry and Biology, Karl-Liebknecht-Str. 24-25, 14476 Potsdam, Germany
| | - Dana Wehner
- Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315 Berlin, Germany.,Institute of Biology, Free University of Berlin, Takustr. 6, 14195 Berlin, Germany
| | - Gábor Á Czirják
- Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315 Berlin, Germany
| | - Christian C Voigt
- Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315 Berlin, Germany.,Institute of Biology, Free University of Berlin, Takustr. 6, 14195 Berlin, Germany
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Tuomisto AE, Mäkinen MJ, Väyrynen JP. Systemic inflammation in colorectal cancer: Underlying factors, effects, and prognostic significance. World J Gastroenterol 2019; 25:4383-4404. [PMID: 31496619 PMCID: PMC6710177 DOI: 10.3748/wjg.v25.i31.4383] [Citation(s) in RCA: 186] [Impact Index Per Article: 31.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/24/2019] [Revised: 06/07/2019] [Accepted: 07/19/2019] [Indexed: 02/06/2023] Open
Abstract
Systemic inflammation is a marker of poor prognosis preoperatively present in around 20%-40% of colorectal cancer patients. The hallmarks of systemic inflammation include an increased production of proinflammatory cytokines and acute phase proteins that enter the circulation. While the low-level systemic inflammation is often clinically silent, its consequences are many and may ultimately lead to chronic cancer-associated wasting, cachexia. In this review, we discuss the pathogenesis of cancer-related systemic inflammation, explore the role of systemic inflammation in promoting cancer growth, escaping antitumor defense, and shifting metabolic pathways, and how these changes are related to less favorable outcome.
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Affiliation(s)
- Anne E Tuomisto
- Cancer and Translational Medicine Research Unit, University of Oulu, Oulu 90220, Finland
- Department of Pathology, Oulu University Hospital and Medical Research Center Oulu, Oulu 90220, Finland
| | - Markus J Mäkinen
- Cancer and Translational Medicine Research Unit, University of Oulu, Oulu 90220, Finland
- Department of Pathology, Oulu University Hospital and Medical Research Center Oulu, Oulu 90220, Finland
| | - Juha P Väyrynen
- Cancer and Translational Medicine Research Unit, University of Oulu, Oulu 90220, Finland
- Department of Pathology, Oulu University Hospital and Medical Research Center Oulu, Oulu 90220, Finland
- Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02115, United States
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Xu DL, Xu MM, Wang DH. Effects of air temperatures on antioxidant defense and immunity in Mongolian gerbils. J Therm Biol 2019; 84:111-120. [DOI: 10.1016/j.jtherbio.2019.06.008] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/24/2019] [Revised: 06/20/2019] [Accepted: 06/20/2019] [Indexed: 12/22/2022]
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40
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Xu DL, Xu MM, Wang DH. Effect of temperature on antioxidant defense and innate immunity in Brandt's voles. Zool Res 2019; 40:305-316. [PMID: 31310064 PMCID: PMC6680122 DOI: 10.24272/j.issn.2095-8137.2019.045] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/30/2018] [Accepted: 03/22/2019] [Indexed: 11/23/2022] Open
Abstract
Ambient temperature is an important factor influencing many physiological processes, including antioxidant defense and immunity. In the present study, we tested the hypothesis that antioxidant defense and immunity are suppressed by high and low temperature treatment in Brandt's voles (Lasiopodomys brandtii). Thirty male voles were randomly assigned into different temperature groups (4, 23, and 32 °C, n=10 for each group), with the treatment course lasting for 27 d. Results showed that low temperature increased gross energy intake (GEI) and liver, heart, and kidney mass, but decreased body fat mass and dry carcass mass. With the decline in temperature, hydrogen peroxide (H2O2) concentration, which is indicative of reactive oxygen species (ROS) levels, increased in the liver, decreased in the heart, and was unchanged in the kidney, testis, and small intestine. Lipid peroxidation indicated by malonaldehyde (MDA) content in the liver, heart, kidney, testis, and small intestine did not differ among groups, implying that high and low temperature did not cause oxidative damage. Similarly, superoxide dismutase (SOD) and catalase (CAT) activities and total antioxidant capacity (T-AOC) in the five tissues did not respond to low or high temperature, except for elevation of CAT activity in the testis upon cold exposure. Bacteria killing capacity, which is indicative of innate immunity, was nearly suppressed in the 4 °C group in contrast to the 23 °C group, whereas spleen mass and white blood cells were unaffected by temperature treatment. The levels of testosterone, but not corticosterone, were influenced by temperature treatment, though neither were correlated with innate immunity, H2O2 and MDA levels, or SOD, CAT, and T-AOC activity in any detected tissues. Overall, these results showed that temperature had different influences on oxidative stress, antioxidant enzymes, and immunity, which depended on the tissues and parameters tested. Up-regulation or maintenance of antioxidant defense might be an important mechanism for voles to survive highly variable environmental temperatures.
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Affiliation(s)
- De-Li Xu
- College of Life Sciences, Qufu Normal University, Qufu Shandong 273165, China
- State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
| | - Meng-Meng Xu
- State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
| | - De-Hua Wang
- State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
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Goodchild CG, Simpson AM, Minghetti M, DuRant SE. Bioenergetics-adverse outcome pathway: Linking organismal and suborganismal energetic endpoints to adverse outcomes. ENVIRONMENTAL TOXICOLOGY AND CHEMISTRY 2019; 38:27-45. [PMID: 30259559 DOI: 10.1002/etc.4280] [Citation(s) in RCA: 26] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 03/21/2018] [Revised: 05/07/2018] [Accepted: 09/20/2018] [Indexed: 05/21/2023]
Abstract
Adverse outcome pathways (AOPs) link toxicity across levels of biological organization, and thereby facilitate the development of suborganismal responses predictive of whole-organism toxicity and provide the mechanistic information necessary for science-based extrapolation to population-level effects. Thus far AOPs have characterized various acute and chronic toxicity pathways; however, the potential for AOPs to explicitly characterize indirect, energy-mediated effects from toxicants has yet to be fully explored. Indeed, although exposure to contaminants can alter an organism's energy budget, energetic endpoints are rarely incorporated into ecological risk assessment because there is not an integrative framework for linking energetic effects to organismal endpoints relevant to risk assessment (e.g., survival, reproduction, growth). In the present analysis, we developed a generalized bioenergetics-AOP in an effort to make better use of energetic endpoints in risk assessment, specifically exposure scenarios that generate an energetic burden to organisms. To evaluate empirical support for a bioenergetics-AOP, we analyzed published data for links between energetic endpoints across levels of biological organization. We found correlations between 1) cellular energy allocation and whole-animal growth, and 2) metabolic rate and scope for growth. Moreover, we reviewed literature linking energy availability to nontraditional toxicological endpoints (e.g., locomotor performance), and found evidence that toxicants impair aerobic performance and activity. We conclude by highlighting current knowledge gaps that should be addressed to develop specific bioenergetics-AOPs. Environ Toxicol Chem 2019;38:27-45. © 2018 SETAC.
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Affiliation(s)
| | - Adam M Simpson
- Oklahoma State University, Stillwater, Oklahoma, USA
- Penn State Erie, The Behrend College, Erie, Pennsylvania, USA
| | | | - Sarah E DuRant
- Oklahoma State University, Stillwater, Oklahoma, USA
- University of Arkansas, Fayetteville, Arkansas, USA
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Xu DL, Hu XK, Tian Y. Seasonal variations in cellular and humoral immunity in male striped hamsters ( Cricetulus barabensis). Biol Open 2018; 7:bio038489. [PMID: 30404899 PMCID: PMC6310883 DOI: 10.1242/bio.038489] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/11/2018] [Accepted: 10/15/2018] [Indexed: 12/18/2022] Open
Abstract
Animals in the non-tropical zone usually demonstrate seasonal variations in immune function, which is important for their survival. In the present study, seasonal changes in immunity in striped hamsters (Cricetulus barabensis) were investigated to test the winter immunoenhancement hypothesis. Male hamsters were captured from the wild in the fall and winter of 2014 and in the spring and summer of 2015. Body mass, body fat mass and blood glucose levels of the hamsters were all highest in the summer, whereas relative fatness and thymus mass had no seasonal changes. Spleen mass was highest in the fall and white blood cells and phytohaemagglutinin (PHA) response indicative of cellular immunity were lowest in the summer among the four seasons, which supports the winter immunoenhancement hypothesis. IgG and IgM titers were lowest in the fall, which was against this hypothesis. Body fat mass had no correlations with cellular and humoral immunity, suggesting it was not the reason for seasonal changes in cellular and humoral immunity in males. Leptin titers were higher in spring and summer than in fall and winter. No correlation between leptin and cellular and humoral immunity suggested that leptin did not mediate their seasonal changes. Similarly, corticosterone levels were also higher in spring and summer than in fall and winter, which correlated negatively with cellular immunity but positively with IgG levels. This result implied that corticosterone has a suppressive effect on cellular immunity and an enhancing effect on humoral immunity. In summary, distinct components of immune systems exhibited different seasonal patterns. This article has an associated First Person interview with the first author of the paper.
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Affiliation(s)
- De-Li Xu
- College of Life Sciences, Qufu Normal University, Qufu 273165, Shandong Province, China
| | - Xiao-Kai Hu
- College of Life Sciences, Qufu Normal University, Qufu 273165, Shandong Province, China
| | - Yufen Tian
- Library, Qufu Normal University, Qufu 273165, Shandong Province, China
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43
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Langeloh L, Seppälä O. Relative importance of chemical attractiveness to parasites for susceptibility to trematode infection. Ecol Evol 2018; 8:8921-8929. [PMID: 30271555 PMCID: PMC6157662 DOI: 10.1002/ece3.4386] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/02/2018] [Revised: 06/25/2018] [Accepted: 06/29/2018] [Indexed: 01/24/2023] Open
Abstract
While the host immune system is often considered the most important physiological mechanism against parasites, precontact mechanisms determining exposure to parasites may also affect infection dynamics. For instance, chemical cues released by hosts can attract parasite transmission stages. We used the freshwater snail Lymnaea stagnalis and its trematode parasite Echinoparyphium aconiatum to examine the role of host chemical attractiveness, physiological condition, and immune function in determining its susceptibility to infection. We assessed host attractiveness through parasite chemo-orientation behavior; physiological condition through host body size, food consumption, and respiration rate; and immune function through two immune parameters (phenoloxidase-like and antibacterial activity of hemolymph) at an individual level. We found that, although snails showed high variation in chemical attractiveness to E. aconiatum cercariae, this did not determine their overall susceptibility to infection. This was because large body size increased attractiveness, but also increased metabolic activity that reduced overall susceptibility. High metabolic rate indicates fast physiological processes, including immune activity. The examined immune traits, however, showed no association with susceptibility to infection. Our results indicate that postcontact mechanisms were more likely to determine snail susceptibility to infection than variation in attractiveness to parasites. These may include localized immune responses in the target tissue of the parasite. The lack of a relationship between food consumption and attractiveness to parasites contradicts earlier findings that show food deprivation reducing snail attractiveness. This suggests that, although variation in resource level over space and time can alter infection dynamics, variation in chemical attractiveness may not contribute to parasite-induced fitness variation within populations when individuals experience similar environmental conditions.
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Affiliation(s)
- Laura Langeloh
- Institute of Integrative Biology (IBZ)ETH ZürichZürichSwitzerland
- EawagSwiss Federal Institute of Aquatic Science and TechnologyDübendorfSwitzerland
| | - Otto Seppälä
- Institute of Integrative Biology (IBZ)ETH ZürichZürichSwitzerland
- EawagSwiss Federal Institute of Aquatic Science and TechnologyDübendorfSwitzerland
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44
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Huntley NF, Nyachoti CM, Patience JF. Lipopolysaccharide immune stimulation but not β-mannanase supplementation affects maintenance energy requirements in young weaned pigs. J Anim Sci Biotechnol 2018; 9:47. [PMID: 29946460 PMCID: PMC6003148 DOI: 10.1186/s40104-018-0264-y] [Citation(s) in RCA: 37] [Impact Index Per Article: 5.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/07/2017] [Accepted: 05/14/2018] [Indexed: 11/21/2022] Open
Abstract
Background Pathogen or diet-induced immune activation can partition energy and nutrients away from growth, but clear relationships between immune responses and the direction and magnitude of energy partitioning responses have yet to be elucidated. The objectives were to determine how β-mannanase supplementation and lipopolysaccharide (LPS) immune stimulation affect maintenance energy requirements (MEm) and to characterize immune parameters, digestibility, growth performance, and energy balance. Methods In a randomized complete block design, 30 young weaned pigs were assigned to either the control treatment (CON; basal corn, soybean meal and soybean hulls diet), the enzyme treatment (ENZ; basal diet + 0.056% β-mannanase), or the immune system stimulation treatment (ISS; basal diet + 0.056% β-mannanase, challenged with repeated increasing doses of Escherichia coli LPS). The experiment consisted of a 10-d adaptation period, 5-d digestibility and nitrogen balance measurement, 22 h of heat production (HP) measurements, and 12 h of fasting HP measurements in indirect calorimetry chambers. The immune challenge consisted of 4 injections of either LPS (ISS) or sterile saline (CON and ENZ), one every 48 h beginning on d 10. Blood was collected pre- and post-challenge for complete blood counts with differential, haptoglobin and mannan binding lectin, 12 cytokines, and glucose and insulin concentrations. Results Beta-mannanase supplementation did not affect immune status, nutrient digestibility, growth performance, energy balance, or MEm. The ISS treatment induced fever, elevated proinflammatory cytokines and decreased leukocyte concentrations (P < 0.05). The ISS treatment did not impact nitrogen balance or nutrient digestibility (P > 0.10), but increased total HP (21%) and MEm (23%), resulting in decreased lipid deposition (−30%) and average daily gain (−18%) (P < 0.05). Conclusions This experiment provides novel data on β-mannanase supplementation effects on immune parameters and energy balance in pigs and is the first to directly relate decreased ADG to increased MEm independent of changes in feed intake in immune challenged pigs. Immune stimulation increased energy partitioning to the immune system by 23% which limited lipid deposition and weight gain. Understanding energy and nutrient partitioning in immune-stressed pigs may provide insight into more effective feeding and management strategies. Electronic supplementary material The online version of this article (10.1186/s40104-018-0264-y) contains supplementary material, which is available to authorized users.
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Affiliation(s)
- Nichole F Huntley
- 1Department of Animal Science, Iowa State University, Ames, IA 50011 USA
| | - C Martin Nyachoti
- 2Department of Animal Science, University of Manitoba, 226 Animal Science Building, Winnipeg, MB R3T 2N2 Canada
| | - John F Patience
- 1Department of Animal Science, Iowa State University, Ames, IA 50011 USA
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45
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Goetz SM, Romagosa CM, Appel AG, Guyer C, Mendonça MT. Reduced innate immunity of Cuban Treefrogs at leading edge of range expansion. JOURNAL OF EXPERIMENTAL ZOOLOGY PART 2018. [PMID: 29527833 DOI: 10.1002/jez.2146] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/24/2023]
Abstract
During geographic range expansion, populations of non-indigenous species at the invasion front may benefit from directing resources away from immune defense. To test this hypothesis, we investigated the strength of two innate immune components in populations of invasive Cuban Treefrogs (Osteopilus septentrionalis) in a long-colonized area (core region) and at the invasion front (leading-edge region). First, we compared the region-specific metabolic response of frogs injected with an endotoxin that induces systemic inflammation (lipopolysaccharide, LPS) to sham-injected control frogs pooled from both regions. Males and females were analyzed independently because we detected a sex-related difference in mass-independent metabolism of control frogs, with males exhibiting a significantly higher metabolic rate (F1, 21 = 29.02, P < 0.001) than females. We observed a significantly higher metabolic rate in LPS-injected core frogs compared with control frogs for both males (P = 0.041) and females (P = 0.007). Conversely, in leading-edge populations, there was no significant difference in the metabolic rate of LPS-injected and control frogs (males, P = 0.195; females, P = 0.132). Second, we directly compared bacterial killing ability of frog blood plasma between regions. Bactericidal ability of plasma was significantly greater in frogs from the core region in comparison with those at the leading edge (F1, 26 = 28.67, P < 0.001). For both immune components that we examined, populations from the core exhibited stronger immune responses. Our findings support hypotheses predicting an inverse relationship between immunity and range expansion.
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Affiliation(s)
- Scott M Goetz
- Department of Biological Sciences, Auburn University, Auburn, Alabama, USA
| | - Christina M Romagosa
- Department of Wildlife Ecology and Conservation, University of Florida, Gainesville, Florida, USA
| | - Arthur G Appel
- Department of Entomology and Plant Pathology, Auburn University, Auburn, Alabama, USA
| | - Craig Guyer
- Department of Biological Sciences, Auburn University, Auburn, Alabama, USA
| | - Mary T Mendonça
- Department of Biological Sciences, Auburn University, Auburn, Alabama, USA
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Delhaye J, Jenkins T, Glaizot O, Christe P. Avian malaria and bird humoral immune response. Malar J 2018; 17:77. [PMID: 29426311 PMCID: PMC5807826 DOI: 10.1186/s12936-018-2219-3] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/03/2017] [Accepted: 01/31/2018] [Indexed: 11/27/2022] Open
Abstract
Background Plasmodium parasites are known to impose fitness costs on their vertebrate hosts. Some of these costs are due to the activation of the immune response, which may divert resources away from self-maintenance. Plasmodium parasites may also immuno-deplete their hosts. Thus, infected individuals may be less able to mount an immune response to a new pathogen than uninfected ones. However, this has been poorly investigated. Methods The effect of Plasmodium infection on bird humoral immune response when encountering a novel antigen was tested. A laboratory experiment was conducted on canaries (Serinus canaria) experimentally infected with Plasmodium relictum (lineage SGS1) under controlled conditions. Birds were immune challenged with an intra-pectoral injection of a novel non-pathogenic antigen (keyhole limpet haemocyanin, KLH). One week later they were challenged again. The immune responses to the primary and to the secondary contacts were quantified as anti-KLH antibody production via enzyme-linked immunosorbent assay (ELISA). Results There was no significant difference in antibody production between uninfected and Plasmodium infected birds at both primary and secondary contact. However, Plasmodium parasite intensity in the blood increased after the primary contact with the antigen. Conclusions There was no effect of Plasmodium infection on the magnitude of the humoral immune response. However, there was a cost of mounting an immune response in infected individuals as parasitaemia increased after the immune challenge, suggesting a trade-off between current control of chronic Plasmodium infection and investment against a new immune challenge.
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Affiliation(s)
- Jessica Delhaye
- Department of Ecology and Evolution, University of Lausanne, Le Biophore, Unil Sorge, 1015, Lausanne, Switzerland.
| | - Tania Jenkins
- Department of Ecology and Evolution, University of Lausanne, Le Biophore, Unil Sorge, 1015, Lausanne, Switzerland
| | - Olivier Glaizot
- Museum of Zoology, Place de la Riponne 6, 1005, Lausanne, Switzerland
| | - Philippe Christe
- Department of Ecology and Evolution, University of Lausanne, Le Biophore, Unil Sorge, 1015, Lausanne, Switzerland
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MacColl E, Vanesky K, Buck JA, Dudek BM, Eagles-Smith CA, Heath JA, Herring G, Vennum C, Downs CJ. Correlates of immune defenses in golden eagle nestlings. JOURNAL OF EXPERIMENTAL ZOOLOGY PART 2017; 327:243-253. [PMID: 29356454 DOI: 10.1002/jez.2081] [Citation(s) in RCA: 12] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 03/01/2017] [Revised: 05/30/2017] [Accepted: 06/21/2017] [Indexed: 11/07/2022]
Abstract
An individual's investment in constitutive immune defenses depends on both intrinsic and extrinsic factors. We examined how Leucocytozoon parasite presence, body condition (scaled mass), heterophil-to-lymphocyte (H:L) ratio, sex, and age affected immune defenses in golden eagle (Aquila chrysaetos) nestlings from three regions: California, Oregon, and Idaho. We quantified hemolytic-complement activity and bacterial killing ability, two measures of constitutive immunity. Body condition and age did not affect immune defenses. However, eagles with lower H:L ratios had lower complement activity, corroborating other findings that animals in better condition sometimes invest less in constitutive immunity. In addition, eagles with Leucocytozoon infections had higher concentrations of circulating complement proteins but not elevated opsonizing proteins for all microbes, and eagles from Oregon had significantly higher constitutive immunity than those from California or Idaho. We posit that Oregon eagles might have elevated immune defenses because they are exposed to more endoparasites than eagles from California or Idaho, and our results confirmed that the OR region has the highest rate of Leucocytozoon infections. Our study examined immune function in a free-living, long-lived raptor species, whereas most avian ecoimmunological research focuses on passerines. Thus, our research informs a broad perspective regarding the evolutionary and environmental pressures on immune function in birds.
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Affiliation(s)
| | - Kris Vanesky
- Academy for the Environment, University of Nevada Reno, NV, USA
| | - Jeremy A Buck
- US Fish and Wildlife Service, Oregon Fish and Wildlife Office, Portland, OR, USA
| | - Benjamin M Dudek
- Department of Biological Sciences and Raptor Research Center, Boise State University, Boise, ID, USA
| | - Collin A Eagles-Smith
- U.S. Geological Survey, Forest and Rangeland Ecosystem Science Center, Corvallis, OR
| | - Julie A Heath
- Department of Biological Sciences and Raptor Research Center, Boise State University, Boise, ID, USA
| | - Garth Herring
- U.S. Geological Survey, Forest and Rangeland Ecosystem Science Center, Corvallis, OR
| | - Chris Vennum
- Department of Biology, University of Nevada, Reno, NV, USA
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Smith GD, Neuman-Lee LA, Webb AC, Angilletta MJ, DeNardo DF, French SS. Metabolic responses to different immune challenges and varying resource availability in the side-blotched lizard (Uta stansburiana). J Comp Physiol B 2017; 187:1173-1182. [DOI: 10.1007/s00360-017-1095-4] [Citation(s) in RCA: 19] [Impact Index Per Article: 2.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/13/2016] [Revised: 01/15/2017] [Accepted: 04/06/2017] [Indexed: 02/01/2023]
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Xu DL, Hu XK, Tian YF. Effect of temperature and food restriction on immune function in striped hamsters ( Cricetulus barabensis). ACTA ACUST UNITED AC 2017; 220:2187-2195. [PMID: 28381582 DOI: 10.1242/jeb.153601] [Citation(s) in RCA: 12] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/19/2016] [Accepted: 03/24/2017] [Indexed: 01/22/2023]
Abstract
Small mammals in temperate areas face seasonal fluctuations of temperature and food availability, both of which may influence their immune responses, which are critical to survival. In the present study, we tested the hypothesis that low temperature and food restriction suppress immune function in striped hamsters (Cricetulus barabensis). Thirty-seven adult male hamsters were randomly assigned to warm (23±1°C) and cold (5±1°C) treatment groups, which were further divided into fed and food-restricted groups. Body mass was not affected by cold stress, food restriction or the interaction cold stress×food restriction. Cold stress decreased total body fat mass, haematological parameters including white blood cells, lymphocytes and neutrophilic granulocytes, and immunoglobin (Ig) M titres 5 days after injecting keyhole limpet haemocyanin (KLH). However, cold temperature increased bacterial killing capacity, indicative of innate immunity, and did not affect the mass of the thymus and spleen, intermediate granulocytes, the phytohaemagglutinin (PHA) response and the levels of blood glucose and serum leptin. Corticosterone concentration was affected significantly by the interaction cold stress×food restriction but not by cold stress or food restriction alone. Food restriction reduced thymus mass, but other immunological parameters including body fat mass, spleen mass, haematological parameters, innate immunity, PHA response, the titres of IgM and IgG, and the levels of blood glucose and serum leptin were all not affected by food restriction or the interaction cold stress×food restriction. Innate immunity was positively correlated with leptin levels, whereas no significant correlations were observed in the levels of blood glucose, serum leptin, corticosterone and all the detected immune parameters. Our results show that cold stress suppressed humoral immunity but enhanced innate immunity and did not affect cellular immunity in striped hamsters. Most immunological indices were not influenced by food restriction. Blood glucose, leptin and corticosterone could not explain the changes of innate, cellular and humoral immunity upon cold stress or food restriction in striped hamsters.
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Affiliation(s)
- De-Li Xu
- College of Life Sciences, Qufu Normal University, Qufu, Shandong Province 273165, China
| | - Xiao-Kai Hu
- College of Life Sciences, Qufu Normal University, Qufu, Shandong Province 273165, China
| | - Yu-Fen Tian
- Library, Qufu Normal University, Qufu, Shandong Province 273165, China
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van Duijvendijk G, van Andel W, Fonville M, Gort G, Hovius JW, Sprong H, Takken W. A Borrelia afzelii Infection Increases Larval Tick Burden on Myodes glareolus (Rodentia: Cricetidae) and Nymphal Body Weight of Ixodes ricinus (Acari: Ixodidae). JOURNAL OF MEDICAL ENTOMOLOGY 2017; 54:422-428. [PMID: 27694145 DOI: 10.1093/jme/tjw157] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 04/14/2016] [Accepted: 08/25/2016] [Indexed: 06/06/2023]
Abstract
Several microorganisms have been shown to manipulate their host or vector to enhance their own transmission. Here we examined whether an infection with Borrelia afzelii affects its transmission between its bank vole (Myodes glareolus, Schreber, 1780) host and tick vector. Captive-bred bank voles were inoculated with B. afzelii or control medium, after which host preference of Ixodes ricinus L. nymphs was determined in a Y-tube olfactometer. Thereafter, infected and uninfected bank voles were placed in a semifield arena containing questing larvae to measure larval tick attachment. Engorged larvae were collected from these bank voles, molted into nymphs, weighed, and analyzed for infection by PCR.Nymphs were attracted to the odors of a bank vole compared to ambient air and preferred the odors of an infected bank vole over that of an uninfected bank vole. In the semifield arena, infected male bank voles had greater larval tick burdens then uninfected males, while similar larval tick burdens were observed on females regardless of infection status. Nymphal ticks that acquired a B. afzelii infection had higher body weight than nymphs that did not acquire an infection regardless of the infection status of the vole. These results show that a B. afzelii infection in bank voles increases larval tick burden and that a B. afzelii infection in larvae increases nymphal body weight. This finding provides novel ecological insights into the enzootic cycle of B. afzelii.
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Affiliation(s)
- Gilian van Duijvendijk
- Laboratory of Entomology, Wageningen University, PO box 16, 6700 AA, Wageningen, The Netherlands (; ; ; )
| | - Wouter van Andel
- Laboratory of Entomology, Wageningen University, PO box 16, 6700 AA, Wageningen, The Netherlands (; ; ; )
| | - Manoj Fonville
- Laboratory for Zoonosis and Environmental Microbiology, National Institute for Public Health and Environment (RIVM), P.O. Box 1, 3720 BA Bilthoven, The Netherlands
| | - Gerrit Gort
- Mathematical and Statistical Methods, Wageningen University, PO box 16, 6700 AA, Wageningen, The Netherlands
| | - Joppe W Hovius
- Center for Experimental and Molecular Medicine, Academic Medical Center, University of Amsterdam, Meibergdreef 9, 1105 AZ, Amsterdam, The Netherlands
| | - Hein Sprong
- Laboratory of Entomology, Wageningen University, PO box 16, 6700 AA, Wageningen, The Netherlands (; ; ; )
- Laboratory for Zoonosis and Environmental Microbiology, National Institute for Public Health and Environment (RIVM), P.O. Box 1, 3720 BA Bilthoven, The Netherlands
| | - Willem Takken
- Laboratory of Entomology, Wageningen University, PO box 16, 6700 AA, Wageningen, The Netherlands (; ; ; )
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