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Yang Y, Zheng S, Chu H, Du C, Chen M, Emran MY, Chen J, Yang F, Tian L. Subchronic Microcystin-LR Aggravates Colorectal Inflammatory Response and Barrier Disruption via Raf/ERK Signaling Pathway in Obese Mice. Toxins (Basel) 2023; 15:toxins15040262. [PMID: 37104200 PMCID: PMC10145857 DOI: 10.3390/toxins15040262] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/31/2022] [Revised: 03/03/2023] [Accepted: 03/14/2023] [Indexed: 04/05/2023] Open
Abstract
Microcystin-LR (MC-LR) is an extremely poisonous cyanotoxin that poses a threat to ecosystems and human health. MC-LR has been reported as an enterotoxin. The objective of this study was to determine the effect and the mechanism of subchronic MC-LR toxicity on preexisting diet-induced colorectal damage. C57BL/6J mice were given either a regular diet or a high-fat diet (HFD) for 8 weeks. After 8 weeks of feeding, animals were supplied with vehicle or 120 μg/L MC-LR via drinking water for another 8 weeks, and their colorectal were stained with H&E to detect microstructural alterations. Compared with the CT group, the HFD and MC-LR + HFD-treatment group induced a significant weight gain in the mice. Histopathological findings showed that the HFD- and MC-LR + HFD-treatment groups caused epithelial barrier disruption and infiltration of inflammatory cells. The HFD- and MC-LR + HFD-treatment groups raised the levels of inflammation mediator factors and decreased the expression of tight junction-related factors compared to the CT group. The expression levels of p-Raf/Raf and p-ERK/ERK in the HFD- and MC-LR + HFD-treatment groups were significantly increased compared with the CT group. Additionally, treated with MC-LR + HFD, the colorectal injury was further aggravated compared with the HFD-treatment group. These findings suggest that by stimulating the Raf/ERK signaling pathway, MC-LR may cause colorectal inflammation and barrier disruption. This study suggests that MC-LR treatment may exacerbate the colorectal toxicity caused by an HFD. These findings offer unique insights into the consequences and harmful mechanisms of MC-LR and provide strategies for preventing and treating intestinal disorders.
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Affiliation(s)
- Yue Yang
- Hunan Provincial Key Laboratory of Clinical Epidemiology, Xiangya School of Public Health, Central South University, Changsha 410078, China
| | - Shuilin Zheng
- Hunan Provincial Key Laboratory of Clinical Epidemiology, Xiangya School of Public Health, Central South University, Changsha 410078, China
- Hunan Province Key Laboratory of Typical Environmental Pollution and Health Hazards, The Key Laboratory of Ecological Environment and Critical Human Diseases Prevention of Hunan Province, Department of Education, Hengyang Medical School, University of South China, Hengyang 421001, China
- Changsha Center for Disease Control and Prevention, Changsha 410004, China
| | - Hanyu Chu
- Hunan Province Key Laboratory of Typical Environmental Pollution and Health Hazards, The Key Laboratory of Ecological Environment and Critical Human Diseases Prevention of Hunan Province, Department of Education, Hengyang Medical School, University of South China, Hengyang 421001, China
| | - Can Du
- Hunan Provincial Key Laboratory of Clinical Epidemiology, Xiangya School of Public Health, Central South University, Changsha 410078, China
| | - Mengshi Chen
- Hunan Provincial Key Laboratory of Clinical Epidemiology, Xiangya School of Public Health, Central South University, Changsha 410078, China
| | - Mohammed Y. Emran
- National Institute for Materials Science (NIMS), 1-2-1 Sengen, Tsukuba 305-0047, Japan
| | - Jihua Chen
- Hunan Provincial Key Laboratory of Clinical Epidemiology, Xiangya School of Public Health, Central South University, Changsha 410078, China
| | - Fei Yang
- Hunan Provincial Key Laboratory of Clinical Epidemiology, Xiangya School of Public Health, Central South University, Changsha 410078, China
- Hunan Province Key Laboratory of Typical Environmental Pollution and Health Hazards, The Key Laboratory of Ecological Environment and Critical Human Diseases Prevention of Hunan Province, Department of Education, Hengyang Medical School, University of South China, Hengyang 421001, China
| | - Li Tian
- Department of Gastroenterology, Third Xiangya Hospital, Central South University, Changsha 410013, China
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Veerabadhran M, Manivel N, Sarvalingam B, Seenivasan B, Srinivasan H, Davoodbasha M, Yang F. State-of-the-art review on the ecotoxicology, health hazards, and economic loss of the impact of microcystins and their ultrastructural cellular changes. AQUATIC TOXICOLOGY (AMSTERDAM, NETHERLANDS) 2023; 256:106417. [PMID: 36805195 DOI: 10.1016/j.aquatox.2023.106417] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 09/03/2022] [Revised: 11/30/2022] [Accepted: 01/04/2023] [Indexed: 06/18/2023]
Abstract
Cyanobacteria are ubiquitously globally present in both freshwater and marine environments. Ample reports have been documented by researchers worldwide for pros and cons of cyanobacterial toxins. The implications of cyanobacterial toxin on health have received much attention in recent decades. Microcystins (MCs) represent the unique class of toxic metabolites produced by cyanobacteria. Although the beneficial aspects of cyanobacterial are numerous, the deleterious effect of MCs overlooked. Several studies on MCs evidently reported that MCs exhibit a plethora of harmful effect on animals, plants, and cell lines. Accordingly, numerous histopathological studies have also found that MCs cause detrimental effects to cells by damaging cellular organelles, including nuclear envelope, Golgi apparatus, endoplasmic reticulum, mitochondria, plastids, flagellum, pilus membrane structures and integrity, vesicle structures, and autolysosomes and autophagosomes. Such ultrastructural cellular damages holistically influence the morphological, biochemical, physiological, and genetic status of the host. Indeed, MCs have also been found to cause the deleterious effect to different animals and plants. Such deleterious effects of MCs have greater impact on agriculture, public health which in turn influences ecotoxicology and economic consequences. The impairments correspond to oxidative stress, organ failure, carcinogenesis, aquaculture loss, with an emphasis for blooms and respective bioaccumulation prospects. The preservation of mortality among life forms is addressed in a critical cellular perspective for multitude benefits. The comprehensive cellular assessment could provide opportunity to develop strategy for therapeutic implications.
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Affiliation(s)
- Maruthanayagam Veerabadhran
- Hunan Province Key Laboratory of Typical Environmental Pollution and Health Hazards, School of Public Health, University of South China, Hengyang, China; Hunan Provincial Key Laboratory of Clinical Epidemiology, Xiangya School of Public Health, Central South University, Hunan 410078, China
| | - Nagarajan Manivel
- ICAR-Central Marine Fisheries Research Institute, Chennai 600 0028, India
| | - Barathkumar Sarvalingam
- National Centre for Coastal Research (NCCR), Ministry of Earth Science, NIOT Campus, Chennai 600100, India
| | - Boopathi Seenivasan
- Department of Biotechnology, College of Science and Humanities, SRM Institute of Science and Technology, Chennai, India
| | - Hemalatha Srinivasan
- School of Life Sciences, B.S. Abdur Rahman Crescent Institute of Science and Technology, Chennai 600 0048, India
| | - MubarakAli Davoodbasha
- School of Life Sciences, B.S. Abdur Rahman Crescent Institute of Science and Technology, Chennai 600 0048, India.
| | - Fei Yang
- Hunan Province Key Laboratory of Typical Environmental Pollution and Health Hazards, School of Public Health, University of South China, Hengyang, China.
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Single and mixed diets of the toxic Cyanobacteria Microcystis aeruginosa and Raphidiopsis raciborskii differently affect Daphnia feeding behavior. FOOD WEBS 2022. [DOI: 10.1016/j.fooweb.2022.e00245] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 11/21/2022]
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Du C, Zheng S, Yang Y, Feng X, Chen J, Tang Y, Wang H, Yang F. Chronic exposure to low concentration of MC-LR caused hepatic lipid metabolism disorder. ECOTOXICOLOGY AND ENVIRONMENTAL SAFETY 2022; 239:113649. [PMID: 35605325 DOI: 10.1016/j.ecoenv.2022.113649] [Citation(s) in RCA: 18] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 02/18/2022] [Revised: 05/01/2022] [Accepted: 05/11/2022] [Indexed: 06/15/2023]
Abstract
Microcystin-LR (MC-LR), a potent hepatotoxin can cause liver damages. However, research on hepatic lipid metabolism caused by long-term exposure to environmental concentrations MC-LR is limited. In the current study, mice were exposed to various low concentrations of MC-LR (0, 1, 30, 60, 90, 120 μg/L in the drinking water) for 9 months. The general parameters, serum and liver lipids, liver tissue pathology, lipid metabolism-related genes and proteins of liver were investigated. The results show that chronic MC-LR exposure had increased the levels of triglyceride (TG) and total cholesterol (TC) in serum and liver. In addition, histological observation revealed that hepatic lobules were disordered with obvious inflammatory cell infiltration and lipid droplets. More importantly, the mRNA and proteins expression levels of lipid synthesis-related nuclear sterol regulatory element binding protein-1c (nSREBP-1c), SREBP-1c, cluster of differentiation 36 (CD36), acetyl-CoA-carboxylase1 (ACC1), stearoyl-CoA desaturase1 (SCD1) and fatty acid synthase (FASN) were increased in MC-LR treated groups, the expression levels of fatty acids β-oxidation related genes peroxisomal acyl-coenzyme A oxidase 1 (ACOX1) was decreased after exposure to 60-120 μg/L MC-LR. Furthermore, the inflammatory factors interleukin 6 (IL-6) and tumor necrosis factor-α (TNF-α) were higher than that in the control group. All the findings indicated that mice were exposed to chronic low concentrations MC-LR caused liver inflammation and hepatic lipid metabolism disorder .
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Affiliation(s)
- Can Du
- Hunan Provincial Key Laboratory of Clinical Epidemiology, Xiangya School of Public Health, Central South University, Changsha 410078, China
| | - Shuilin Zheng
- Hunan Provincial Key Laboratory of Clinical Epidemiology, Xiangya School of Public Health, Central South University, Changsha 410078, China
| | - Yue Yang
- Hunan Provincial Key Laboratory of Clinical Epidemiology, Xiangya School of Public Health, Central South University, Changsha 410078, China
| | - Xiangling Feng
- Hunan Provincial Key Laboratory of Clinical Epidemiology, Xiangya School of Public Health, Central South University, Changsha 410078, China
| | - Jihua Chen
- Hunan Provincial Key Laboratory of Clinical Epidemiology, Xiangya School of Public Health, Central South University, Changsha 410078, China
| | - Yan Tang
- Hunan Province Key Laboratory of Typical Environmental Pollution and Health Hazards, School of Public Health, University of South China, Hengyang 421001, China
| | - Hui Wang
- Hunan Province Key Laboratory of Typical Environmental Pollution and Health Hazards, School of Public Health, University of South China, Hengyang 421001, China
| | - Fei Yang
- Hunan Provincial Key Laboratory of Clinical Epidemiology, Xiangya School of Public Health, Central South University, Changsha 410078, China; Hunan Province Key Laboratory of Typical Environmental Pollution and Health Hazards, School of Public Health, University of South China, Hengyang 421001, China; Key Laboratory of Environmental Medicine Engineering, Ministry of Education, School of Public Health, Southeast University, Nanjing 210009, China; The Key Laboratory of Ecological Environment and Critical Human Diseases Prevention of Hunan Province Department of Education, School of Basic Medical Sciences, Hengyang Medical School, University of South China, Hengyang 421001, China.
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Vilar MCP, da Costa Pena Rodrigues TF, da Silva Ferrão-Filho A, de Oliveira E Azevedo SMF. Grazer-Induced Chemical Defense in a Microcystin-Producing Microcystis aeruginosa (Cyanobacteria) Exposed to Daphnia gessneri Infochemicals. J Chem Ecol 2021; 47:847-858. [PMID: 34569003 DOI: 10.1007/s10886-021-01315-5] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/28/2021] [Revised: 09/09/2021] [Accepted: 09/14/2021] [Indexed: 10/20/2022]
Abstract
Cyanobacteria are photosynthetic microorganisms that compose phytoplankton and therefore have a trophic relationship with zooplankton, which represent an important link for energy flux in aquatic food webs. Several species can form blooms and produce bioactive metabolites known as cyanotoxins. However, the ecological and adaptative role of these toxins are still under debate. Many studies have addressed the cyanotoxins' function in defense against herbivory when grazing pressure by zooplankton plays a role in phytoplankton top-down control. Thus, the present study evaluated the ecophysiological responses of the cyanobacterial strain Microcystis aeruginosa NPLJ-4 underlying the chemical induced defense against the cladoceran Daphnia gessneri. Exposure to predator infochemicals consisted of cultures established in ASM-1 medium prepared in a filtrate from a culture of adults of D. gessneri at an environmentally relevant density. Daphnia infochemicals promoted a significant increase in toxin production by M. aeruginosa. However, no differences in growth were observed, despite a significant increase in both maximum photosynthetic efficiency and electron transport rate in response to zooplankton. Additionally, there was no significant variation in the production of exopolysaccharides. Overall, although a grazer-induced defense response was demonstrated, there were no effects on M. aeruginosa fitness, which maintained its growth in the presence of Daphnia alarm cues.
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Affiliation(s)
- Mauro Cesar Palmeira Vilar
- Laboratory of Ecophysiology and Toxicology of Cyanobacteria, Carlos Chagas Filho Institute of Biophysics, Federal University of Rio de Janeiro, Rio de Janeiro, 21949-902, Brazil.
| | - Thiago Ferreira da Costa Pena Rodrigues
- Laboratory of Ecophysiology and Toxicology of Cyanobacteria, Carlos Chagas Filho Institute of Biophysics, Federal University of Rio de Janeiro, Rio de Janeiro, 21949-902, Brazil
| | - Aloysio da Silva Ferrão-Filho
- Laboratory of Evaluation and Promotion of Environmental Health, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, RJ, 21040-360, Brazil
| | - Sandra Maria Feliciano de Oliveira E Azevedo
- Laboratory of Ecophysiology and Toxicology of Cyanobacteria, Carlos Chagas Filho Institute of Biophysics, Federal University of Rio de Janeiro, Rio de Janeiro, 21949-902, Brazil
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Wu JX, Huang H, Yang L, Zhang XF, Zhang SS, Liu HH, Wang YQ, Yuan L, Cheng XM, Zhuang DG, Zhang HZ. Gastrointestinal toxicity induced by microcystins. World J Clin Cases 2018; 6:344-354. [PMID: 30283797 PMCID: PMC6163130 DOI: 10.12998/wjcc.v6.i10.344] [Citation(s) in RCA: 27] [Impact Index Per Article: 3.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/23/2018] [Revised: 06/08/2018] [Accepted: 06/28/2018] [Indexed: 02/05/2023] Open
Abstract
Microcystins (MCs) are produced by certain bloom-forming cyanobacteria that can induce toxicity in various organs, including renal toxicity, reproductive toxicity, cardiotoxicity, and immunosuppressive effects. It has been a significant global environmental issue due to its harm to the aquatic environment and human health. Numerous investigators have demonstrated that MC exposure can induce a widespread epidemic of enterogastritis with symptoms similar to food poisoning in areas close to lakes. Both in vivo and in vitro studies have provided evidence of positive associations between MC exposure and gastrointestinal toxicity. The toxicity of MCs on the gastrointestinal tract is multidimensional. MCs can affect gastrointestinal barrier function and shift the structure of gut microbiota in different gut regions. Furthermore, MCs can inhibit the secretion of gastrointestinal digestive enzymes and the release of inflammatory cytokines, which affects the expression of immune-related genes in the intestine. The damage of the intestine is closely correlated to MC exposure because the intestine is the main site for the digestion and absorption of nutrients. The damage to the gastrointestinal tract due to MCs was summarized from different aspects, which can be used as a foundation for further exploration of molecular damage mechanisms.
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Affiliation(s)
- Jin-Xia Wu
- Department of Environmental Hygiene, College of Public Health, Zhengzhou University, Zhengzhou 450001, Henan Province, China
| | - Hui Huang
- Department of Environmental Hygiene, College of Public Health, Zhengzhou University, Zhengzhou 450001, Henan Province, China
| | - Lei Yang
- Department of Nutriology, College of Public Health, Zhengzhou University, Zhengzhou 450001, Henan Province, China
| | - Xiao-Feng Zhang
- Department of Nutriology, College of Public Health, Zhengzhou University, Zhengzhou 450001, Henan Province, China
| | - Shen-Shen Zhang
- Department of Nutriology, College of Public Health, Zhengzhou University, Zhengzhou 450001, Henan Province, China
| | - Hao-Hao Liu
- Department of Environmental Hygiene, College of Public Health, Zhengzhou University, Zhengzhou 450001, Henan Province, China
| | - Yue-Qin Wang
- Department of Environmental Hygiene, College of Public Health, Zhengzhou University, Zhengzhou 450001, Henan Province, China
| | - Le Yuan
- Department of Environmental Hygiene, College of Public Health, Zhengzhou University, Zhengzhou 450001, Henan Province, China
| | - Xue-Min Cheng
- Department of Environmental Hygiene, College of Public Health, Zhengzhou University, Zhengzhou 450001, Henan Province, China
| | - Dong-Gang Zhuang
- Department of Environmental Hygiene, College of Public Health, Zhengzhou University, Zhengzhou 450001, Henan Province, China
| | - Hui-Zhen Zhang
- Department of Environmental Hygiene, College of Public Health, Zhengzhou University, Zhengzhou 450001, Henan Province, China
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7
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Tokodi N, Drobac D, Meriluoto J, Lujić J, Marinović Z, Važić T, Nybom S, Simeunović J, Dulić T, Lazić G, Petrović T, Vuković-Gačić B, Sunjog K, Kolarević S, Kračun-Kolarević M, Subakov-Simić G, Miljanović B, Codd GA, Svirčev Z. Cyanobacterial effects in Lake Ludoš, Serbia - Is preservation of a degraded aquatic ecosystem justified? THE SCIENCE OF THE TOTAL ENVIRONMENT 2018; 635:1047-1062. [PMID: 29710560 DOI: 10.1016/j.scitotenv.2018.04.177] [Citation(s) in RCA: 15] [Impact Index Per Article: 2.1] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 07/28/2017] [Revised: 04/13/2018] [Accepted: 04/13/2018] [Indexed: 06/08/2023]
Abstract
Cyanobacteria are present in many aquatic ecosystems in Serbia. Lake Ludoš, a wetland area of international significance and an important habitat for waterbirds, has become the subject of intense research interest because of practically continuous blooming of cyanobacteria. Analyses of water samples indicated a deterioration of ecological condition and water quality, and the presence of toxin-producing cyanobacteria (the most abundant Limnothrix redekei, Pseudanabaena limnetica, Planktothrix agardhii and Microcystis spp.). Furthermore, microcystins were detected in plants and animals from the lake: in macrophyte rhizomes (Phragmites communis, Typha latifolia and Nymphaea elegans), and in the muscle, intestines, kidneys, gonads and gills of fish (Carassius gibelio). Moreover, histopathological deleterious effects (liver, kidney, gills and intestines) and DNA damage (liver and gills) were observed in fish. A potential treatment for the reduction of cyanobacterial populations employing hydrogen peroxide was tested during this study. The treatment was not effective in laboratory tests although further in-lake trials are needed to make final conclusions about the applicability of the method. Based on our observations of the cyanobacterial populations and cyanotoxins in the water, as well as other aquatic organisms and, a survey of historical data on Lake Ludoš, it can be concluded that the lake is continuously in a poor ecological state. Conservation of the lake in order to protect the waterbirds (without urgent control of eutrophication) actually endangers them and the rest of the biota in this wetland habitat, and possibly other ecosystems. Thus, urgent measures for restoration are required, so that the preservation of this Ramsar site would be meaningful.
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Affiliation(s)
- Nada Tokodi
- Department of Biology and Ecology, Faculty of Science, University of Novi Sad, Trg Dositeja Obradovića 3, 21000 Novi Sad, Serbia.
| | - Damjana Drobac
- Department of Biology and Ecology, Faculty of Science, University of Novi Sad, Trg Dositeja Obradovića 3, 21000 Novi Sad, Serbia
| | - Jussi Meriluoto
- Biochemistry, Faculty of Science and Engineering, Åbo Akademi University, Tykistökatu 6 A, 20520 Turku, Finland; Department of Biology and Ecology, Faculty of Science, University of Novi Sad, Trg Dositeja Obradovića 3, 21000 Novi Sad, Serbia
| | - Jelena Lujić
- Department of Aquaculture, Szent István University, Páter Károly u. 1, Gödöllő 2100, Hungary
| | - Zoran Marinović
- Department of Biology and Ecology, Faculty of Science, University of Novi Sad, Trg Dositeja Obradovića 3, 21000 Novi Sad, Serbia; Department of Aquaculture, Szent István University, Páter Károly u. 1, Gödöllő 2100, Hungary
| | - Tamara Važić
- Department of Biology and Ecology, Faculty of Science, University of Novi Sad, Trg Dositeja Obradovića 3, 21000 Novi Sad, Serbia
| | - Sonja Nybom
- Biochemistry, Faculty of Science and Engineering, Åbo Akademi University, Tykistökatu 6 A, 20520 Turku, Finland
| | - Jelica Simeunović
- Department of Biology and Ecology, Faculty of Science, University of Novi Sad, Trg Dositeja Obradovića 3, 21000 Novi Sad, Serbia
| | - Tamara Dulić
- Department of Biology and Ecology, Faculty of Science, University of Novi Sad, Trg Dositeja Obradovića 3, 21000 Novi Sad, Serbia
| | - Gospava Lazić
- Scientific Veterinary Institute "Novi Sad", Rumenački put 20, 21000 Novi Sad, Serbia
| | - Tamaš Petrović
- Scientific Veterinary Institute "Novi Sad", Rumenački put 20, 21000 Novi Sad, Serbia
| | - Branka Vuković-Gačić
- Center for Genotoxicology and Ecogenotoxicology, Chair of Microbiology, Faculty of Biology, Studenski Trg 16, University of Belgrade, Belgrade, Serbia
| | - Karolina Sunjog
- Center for Genotoxicology and Ecogenotoxicology, Chair of Microbiology, Faculty of Biology, Studenski Trg 16, University of Belgrade, Belgrade, Serbia
| | - Stoimir Kolarević
- Center for Genotoxicology and Ecogenotoxicology, Chair of Microbiology, Faculty of Biology, Studenski Trg 16, University of Belgrade, Belgrade, Serbia
| | - Margareta Kračun-Kolarević
- Institute for Biological Research "Siniša Stanković", Despota Stefana 142, University of Belgrade, Belgrade, Serbia
| | - Gordana Subakov-Simić
- Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia
| | - Branko Miljanović
- Department of Biology and Ecology, Faculty of Science, University of Novi Sad, Trg Dositeja Obradovića 3, 21000 Novi Sad, Serbia
| | - Geoffrey A Codd
- College of Life Sciences, University of Dundee, Dundee DD1 5EH, Scotland, UK
| | - Zorica Svirčev
- Department of Biology and Ecology, Faculty of Science, University of Novi Sad, Trg Dositeja Obradovića 3, 21000 Novi Sad, Serbia; Biochemistry, Faculty of Science and Engineering, Åbo Akademi University, Tykistökatu 6 A, 20520 Turku, Finland
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Rodrigues Pires Júnior O, de Oliveira NB, Bosque RJ, Nice Ferreira MF, Morais Aurélio da Silva V, Martins Magalhães AC, Correia de Santana CJ, de Souza Castro M. Histopathological Evaluation of the Exposure by Cyanobacteria Cultive Containing [d-Leu¹]Microcystin-LR on Lithobates catesbeianus Tadpoles. Toxins (Basel) 2018; 10:toxins10080318. [PMID: 30082615 PMCID: PMC6116141 DOI: 10.3390/toxins10080318] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/11/2018] [Revised: 07/21/2018] [Accepted: 07/24/2018] [Indexed: 01/28/2023] Open
Abstract
This study evaluated the effects of [d-Leu1]Microcystin-LR variant by the exposure of Lithobates catesbeianus tadpole to unialgal culture Microcystis aeruginosa NPLJ-4 strain. The Tadpole was placed in aquariums and exposed to Microcystis aeruginosa culture or disrupted cells. For 16 days, 5 individuals were removed every 2 days, and tissue samples of liver, skeletal muscle, and intestinal tract were collected for histopathology and bioaccumulation analyses. After exposure, those surviving tadpoles were placed in clean water for 15 days to evaluate their recovery. A control without algae and toxins was maintained in the same conditions and exhibited normal histology and no tissue damage. In exposed tadpoles, samples were characterized by serious damages that similarly affected the different organs, such as loss of adhesion between cells, nucleus fragmentation, necrosis, and hemorrhage. Samples showed signs of recovery but severe damages were still observed. Neither HPLC-PDA nor mass spectrometry analysis showed any evidence of free Microcystins bioaccumulation.
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Affiliation(s)
- Osmindo Rodrigues Pires Júnior
- Toxinology Laboratory, Depto. Physiological Sciences, Institute of Biology, University of Brasilia, Brasilia 70910-900, Brazil.
| | - Natiela Beatriz de Oliveira
- Toxinology Laboratory, Depto. Physiological Sciences, Institute of Biology, University of Brasilia, Brasilia 70910-900, Brazil.
| | - Renan J Bosque
- Depto. Genetics and Morphology, Institute of Biology, University of Brasilia, Brasilia 70910-900, Brazil.
| | | | | | - Ana Carolina Martins Magalhães
- Toxinology Laboratory, Depto. Physiological Sciences, Institute of Biology, University of Brasilia, Brasilia 70910-900, Brazil.
| | - Carlos José Correia de Santana
- Toxinology Laboratory, Depto. Physiological Sciences, Institute of Biology, University of Brasilia, Brasilia 70910-900, Brazil.
| | - Mariana de Souza Castro
- Toxinology Laboratory, Depto. Physiological Sciences, Institute of Biology, University of Brasilia, Brasilia 70910-900, Brazil.
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Chen Y, Huang X, Wang J, Li C. Effect of pure microcystin-LR on activity and transcript level of immune-related enzymes in the white shrimp (Litopenaeus vannamei). ECOTOXICOLOGY (LONDON, ENGLAND) 2017; 26:702-710. [PMID: 28466205 DOI: 10.1007/s10646-017-1802-7] [Citation(s) in RCA: 34] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Accepted: 04/01/2017] [Indexed: 06/07/2023]
Abstract
Microcystins (MCs) in freshwater and marine waters released by toxin-producing cyanobacteria have negative impacts to the aquatic environment. This study aimed to investigate the effect of pure microcystin-LR on activity and transcript level of immune-related enzymes in the white shrimp Litopenaeus vannamei. After exposed to varying concentrations of pure microcystin-LR (MC-LR) for 30 days, the activity of superoxide dismutase (SOD), lysozyme (LZM), glutathione peroxidase (GPx), peroxidase (POD), acid phosphatase (ACP), alkaline phosphatase (AKP) and transcript level of cMn-sod, lzm, gpx were investigated in the hepatopancreas of white shrimp (L. vannamei). Immune-related enzyme activities responded differently to MC-LR exposure. SOD, GPx, and POD activity in the hepatopancreas were activated in a concentration-dependent manner while LZM activity was significantly inhibited in the treatment groups. ACP and AKP activity showed an increase, followed by a decrease. The transcript levels of cMn-sod, lzm, and gpx were consistent with changes in their encoding enzyme activity. These results demonstrated that sub-chronical exposure to MC-LR induced the alteration of immune-related enzymes and corresponding genes in the hepatopancreas, which may help explain the presence of detoxification mechanisms in crustaceans and how they were protected from MC-LR stress for a long period of time.
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Affiliation(s)
- Yanyan Chen
- Department of Aquaculture, Fishery College, Guangdong Ocean University, East Huguangyan, Mazhang District, Zhanjiang, Guangdong, 524088, China
- Engineering Technology Research Center for Algae Breeding and Application, Zhanjiang, Guangdong, 524088, China
- Shenzhen Research Institute of Guangdong Ocean University, Shenzhen, 518108, China
| | - Xianghu Huang
- Department of Aquaculture, Fishery College, Guangdong Ocean University, East Huguangyan, Mazhang District, Zhanjiang, Guangdong, 524088, China.
- Engineering Technology Research Center for Algae Breeding and Application, Zhanjiang, Guangdong, 524088, China.
- Shenzhen Research Institute of Guangdong Ocean University, Shenzhen, 518108, China.
| | - Jianzhu Wang
- Collaborative Innovation Center for Geo-hazards and Eco-environment in Three Gorges Area, Hubei Province, The Three Gorges University, Yichang, 443002, China
| | - Changling Li
- Department of Aquaculture, Fishery College, Guangdong Ocean University, East Huguangyan, Mazhang District, Zhanjiang, Guangdong, 524088, China
- Engineering Technology Research Center for Algae Breeding and Application, Zhanjiang, Guangdong, 524088, China
- Shenzhen Research Institute of Guangdong Ocean University, Shenzhen, 518108, China
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Woźny M, Lewczuk B, Ziółkowska N, Gomułka P, Dobosz S, Łakomiak A, Florczyk M, Brzuzan P. Intraperitoneal exposure of whitefish to microcystin-LR induces rapid liver injury followed by regeneration and resilience to subsequent exposures. Toxicol Appl Pharmacol 2016; 313:68-87. [PMID: 27765657 DOI: 10.1016/j.taap.2016.10.014] [Citation(s) in RCA: 15] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/19/2016] [Revised: 10/11/2016] [Accepted: 10/13/2016] [Indexed: 12/22/2022]
Abstract
To date, there has been no systematic approach comprehensively describing the sequence of pathological changes in fish during prolonged exposure to microcystin-LR (MC-LR). Towards this aim, juvenile whitefish individuals received an intraperitoneal injection with pure MC-LR, and the injection was repeated every week to maintain continuous exposure for 28days. During the exposure period, growth and condition of the fish were assessed based on biometric measurements. Additionally, selected biochemical markers were analysed in the fishes' blood, and their livers were carefully examined for morphological, ultrastructural, and molecular changes. The higher dose of MC-LR (100μg·kg-1) caused severe liver injury at the beginning of the exposure period, whereas the lower dose (10μg·kg-1) caused less, probably reversible injury, and its effects began to be observed later in the exposure period. These marked changes were accompanied by substantial MC-LR uptake by the liver. However, starting on the 7th day of exposure, cell debris began to be removed by phagocytes, then by 14th day, proliferation of liver cells had markedly increased, which led to reconstruction of the liver parenchyma at the end of the treatment. Surprisingly, despite weekly-repeated intraperitoneal injections, MC-LR did not accumulate over time of exposure which suggests its limited uptake in the later phase of exposure. In support, mRNA expression of the membrane transport protein oatp1d was decreased at the same time as the regenerative processes were observed. Our study shows that closing of active membrane transport may serve as one defence mechanism against further MC-LR intoxication.
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Affiliation(s)
- Maciej Woźny
- Department of Environmental Biotechnology, Faculty of Environmental Sciences, University of Warmia and Mazury in Olsztyn, ul. Słoneczna 45G, 10-709 Olsztyn, Poland.
| | - Bogdan Lewczuk
- Department of Histology and Embryology, Faculty of Veterinary Medicine, University of Warmia and Mazury in Olsztyn, ul. M. Oczapowskiego 13, 10-713 Olsztyn, Poland
| | - Natalia Ziółkowska
- Department of Histology and Embryology, Faculty of Veterinary Medicine, University of Warmia and Mazury in Olsztyn, ul. M. Oczapowskiego 13, 10-713 Olsztyn, Poland
| | - Piotr Gomułka
- Department of Ichthyology, Faculty of Environmental Sciences, University of Warmia and Mazury in Olsztyn, ul. M. Oczapowskiego 5, 10-719 Olsztyn, Poland
| | - Stefan Dobosz
- Department of the Salmonid Research in Rutki, Inland Fisheries Institute in Olsztyn, Rutki, 83-330 Żukowo, Poland
| | - Alicja Łakomiak
- Department of Environmental Biotechnology, Faculty of Environmental Sciences, University of Warmia and Mazury in Olsztyn, ul. Słoneczna 45G, 10-709 Olsztyn, Poland
| | - Maciej Florczyk
- Department of Environmental Biotechnology, Faculty of Environmental Sciences, University of Warmia and Mazury in Olsztyn, ul. Słoneczna 45G, 10-709 Olsztyn, Poland
| | - Paweł Brzuzan
- Department of Environmental Biotechnology, Faculty of Environmental Sciences, University of Warmia and Mazury in Olsztyn, ul. Słoneczna 45G, 10-709 Olsztyn, Poland
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11
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Drobac D, Tokodi N, Lujić J, Marinović Z, Subakov-Simić G, Dulić T, Važić T, Nybom S, Meriluoto J, Codd GA, Svirčev Z. Cyanobacteria and cyanotoxins in fishponds and their effects on fish tissue. HARMFUL ALGAE 2016; 55:66-76. [PMID: 28073548 DOI: 10.1016/j.hal.2016.02.007] [Citation(s) in RCA: 65] [Impact Index Per Article: 7.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 07/31/2015] [Revised: 02/03/2016] [Accepted: 02/03/2016] [Indexed: 06/06/2023]
Abstract
Cyanobacteria can produce toxic metabolites known as cyanotoxins. Common and frequently investigated cyanotoxins include microcystins (MCs), nodularin (NOD) and saxitoxins (STXs). During the summer of 2011 extensive cyanobacterial growth was found in several fishponds in Serbia. Sampling of the water and fish (common carp, Cyprinus carpio) was performed. Water samples from 13 fishponds were found to contain saxitoxin, microcystin, and/or nodularin. LC-MS/MS showed that MC-RR was present in samples of fish muscle tissue. Histopathological analyses of fish grown in fishponds with cyanotoxin production showed histopathological damage to liver, kidney, gills, intestines and muscle tissues. This study is among the first so far to report severe hyperplasia of intestinal epithelium and severe degeneration of muscle tissue of fish after cyanobacterial exposure. These findings emphasize the importance of cyanobacterial and cyanotoxin monitoring in fishponds in order to recognize cyanotoxins and their potential effects on fish used for human consumption and, further, on human health.
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Affiliation(s)
- Damjana Drobac
- Department of Biology and Ecology, Faculty of Science, University of Novi Sad, Trg Dositeja Obradovića 2, Novi Sad 21000, Serbia.
| | - Nada Tokodi
- Department of Biology and Ecology, Faculty of Science, University of Novi Sad, Trg Dositeja Obradovića 2, Novi Sad 21000, Serbia
| | - Jelena Lujić
- Department of Aquaculture, Szent István University, Páter Károly u. 1, Gödöllő 2100, Hungary
| | - Zoran Marinović
- Department of Biology and Ecology, Faculty of Science, University of Novi Sad, Trg Dositeja Obradovića 2, Novi Sad 21000, Serbia; Department of Aquaculture, Szent István University, Páter Károly u. 1, Gödöllő 2100, Hungary
| | - Gordana Subakov-Simić
- Faculty of Biology, University of Belgrade, Studentski trg 16, Belgrade 11000, Serbia
| | - Tamara Dulić
- Department of Biology and Ecology, Faculty of Science, University of Novi Sad, Trg Dositeja Obradovića 2, Novi Sad 21000, Serbia
| | - Tamara Važić
- Department of Biology and Ecology, Faculty of Science, University of Novi Sad, Trg Dositeja Obradovića 2, Novi Sad 21000, Serbia
| | - Sonja Nybom
- Biochemistry, Faculty of Science and Engineering, Åbo Akademi University, Tykistökatu 6 A, Turku 20520, Finland
| | - Jussi Meriluoto
- Biochemistry, Faculty of Science and Engineering, Åbo Akademi University, Tykistökatu 6 A, Turku 20520, Finland; Department of Biology and Ecology, Faculty of Science, University of Novi Sad, Trg Dositeja Obradovića 2, Novi Sad 21000, Serbia
| | - Geoffrey A Codd
- School of the Environment, Flinders University, Adelaide 5042, SA, Australia
| | - Zorica Svirčev
- Department of Biology and Ecology, Faculty of Science, University of Novi Sad, Trg Dositeja Obradovića 2, Novi Sad 21000, Serbia; Biochemistry, Faculty of Science and Engineering, Åbo Akademi University, Tykistökatu 6 A, Turku 20520, Finland
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12
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Yang Y, Qi S, Wang D, Wang K, Zhu L, Chai T, Wang C. Toxic effects of thifluzamide on zebrafish (Danio rerio). JOURNAL OF HAZARDOUS MATERIALS 2016; 307:127-136. [PMID: 26780700 DOI: 10.1016/j.jhazmat.2015.12.055] [Citation(s) in RCA: 88] [Impact Index Per Article: 9.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 09/14/2015] [Revised: 12/10/2015] [Accepted: 12/28/2015] [Indexed: 06/05/2023]
Abstract
Thifluzamide is a fungicide widely used to control crop diseases, and it therefore constitutes a hazard to the environment. In this study, zebrafish were selected to assess the aquatic toxicity of thifluzamide. The acute and development toxicity of thifluzamide to embryos, larvae, and adult zebrafish were measured and the corresponding 96h-LC50 values were as follows: adult fish (4.19mg/L) <larvae (3.52mg/L) <embryos (3.08mg/L). A large suite of symptoms was found in these three stages of zebrafish, including abnormal spontaneous movement, slow heartbeat, hatching inhibition, growth regression, and morphological deformities. In addition, for adult zebrafish, distinct pathological changes were noted in liver and kidney 21 days post exposure (dpe) to 0.19, 1.33, and 2.76mg/L. Liver damage was more severe than kidney damage. In another 28 days exposure of adult zebrafish to 0.019, 0.19, and 1.90mg/L, negative changes in mitochondrial structure and enzymes activities [succinate dehydrogenase (SDH) and respiratory chain complexes] were found. These might be responsible for the adverse expansion of the apoptosis- and immune-related genes, which would facilitate the action of these factors in programmed cell death and might play a key role during the toxic events.
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Affiliation(s)
- Yang Yang
- College of Sciences, China Agricultural University, Beijing, People's Republic of China
| | - Suzhen Qi
- College of Sciences, China Agricultural University, Beijing, People's Republic of China
| | - Donghui Wang
- Plant Developmental Biology, College of Life Sciences, Peking University, 5 Yiheyuan Road, Beijing 100871, People's Republic of China
| | - Kai Wang
- College of Sciences, China Agricultural University, Beijing, People's Republic of China
| | - Lizhen Zhu
- College of Sciences, China Agricultural University, Beijing, People's Republic of China
| | - Tingting Chai
- College of Sciences, China Agricultural University, Beijing, People's Republic of China
| | - Chengju Wang
- College of Sciences, China Agricultural University, Beijing, People's Republic of China.
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13
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Svirčev Z, Lujić J, Marinović Z, Drobac D, Tokodi N, Stojiljković B, Meriluoto J. Toxicopathology induced by microcystins and nodularin: a histopathological review. JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH. PART C, ENVIRONMENTAL CARCINOGENESIS & ECOTOXICOLOGY REVIEWS 2015; 33:125-167. [PMID: 26023756 DOI: 10.1080/10590501.2015.1003000] [Citation(s) in RCA: 21] [Impact Index Per Article: 2.1] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 06/04/2023]
Abstract
Cyanobacteria are present in all aquatic ecosystems throughout the world. They are able to produce toxic secondary metabolites, and microcystins are those most frequently found. Research has displayed a negative influence of microcystins and closely related nodularin on fish, and various histopathological alterations have been observed in many organs of the exposed fish. The aim of this article is to summarize the present knowledge of the impact of microcystins and nodularin on the histology of fish. The observed negative effects of cyanotoxins indicate that cyanobacteria and their toxins are a relevant medical (due to irritation, acute poisoning, tumor promotion, and carcinogenesis), ecotoxicological, and economic problem that may affect both fish and fish consumers including humans.
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Affiliation(s)
- Zorica Svirčev
- a Department of Biology and Ecology, Faculty of Sciences, University of Novi Sad , Novi Sad , Serbia
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Liu W, Qiao Q, Chen Y, Wu K, Zhang X. Microcystin-LR exposure to adult zebrafish (Danio rerio) leads to growth inhibition and immune dysfunction in F1 offspring, a parental transmission effect of toxicity. AQUATIC TOXICOLOGY (AMSTERDAM, NETHERLANDS) 2014; 155:360-367. [PMID: 25105566 DOI: 10.1016/j.aquatox.2014.07.011] [Citation(s) in RCA: 61] [Impact Index Per Article: 5.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 04/07/2014] [Revised: 07/08/2014] [Accepted: 07/09/2014] [Indexed: 06/03/2023]
Abstract
Microcystins (MCs) are algal toxins produced intracellularly within the cyanobacteria cells. MCs exposure exerts great harm to the reproductive system of fish and deteriorates the quality of eggs and sperms, and has further adverse effects on early developmental stages of fish. Whether the MC toxicity can be parentally transmitted to offspring, even though the embryos and larvae are free of MC exposure? In the present study, adult zebrafish were continuously exposed to MC-LR (with dose of 1, 5 and 20 μg/L) for 30 days. After MC-LR exposure, fertilized eggs were collected and the following F1 generation was reared in water containing no MC-LR until 60 days post fertilization (dpf). In F1 offspring, both body weight and body length were evidently dropped. Some growth and immune related genes were detected using the real-time PCR. The transcriptional levels of these genes significantly decreased in F1 offspring of zebrafish whose parents were treated with 5 and 20 μg/L MC-LR. The activities of some antioxidant enzymes, including superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx) significantly dropped in 5 and 20 μg/L MC-LR groups, and the malondialdehyde (MDA) levels markedly increased in all the three treatment groups. Furthermore, distinct pathological changes in liver were observed in F1 zebrafish. Our findings show that the MC-LR exposure to parental zebrafish results in liver damage and evidently influences the growth and immune function in F1 offspring. We consider this damage as a parental transmission effect of microcystin toxicity. Further mechanism studies are necessary to elucidate this transmission effect.
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Affiliation(s)
- Wanjing Liu
- Fisheries College of Huazhong Agricultural University, Freshwater Aquaculture Collaborative Innovation Center of Hubei Province, Wuhan 430070, People's Republic of China
| | - Qin Qiao
- Fisheries College of Huazhong Agricultural University, Freshwater Aquaculture Collaborative Innovation Center of Hubei Province, Wuhan 430070, People's Republic of China
| | - Yuanyuan Chen
- Fisheries College of Huazhong Agricultural University, Freshwater Aquaculture Collaborative Innovation Center of Hubei Province, Wuhan 430070, People's Republic of China
| | - Kang Wu
- Fisheries College of Huazhong Agricultural University, Freshwater Aquaculture Collaborative Innovation Center of Hubei Province, Wuhan 430070, People's Republic of China
| | - Xuezhen Zhang
- Fisheries College of Huazhong Agricultural University, Freshwater Aquaculture Collaborative Innovation Center of Hubei Province, Wuhan 430070, People's Republic of China.
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15
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Pathological modifications following sub-chronic exposure of medaka fish (Oryzias latipes) to microcystin-LR. Reprod Toxicol 2011; 32:329-40. [PMID: 21839164 DOI: 10.1016/j.reprotox.2011.07.006] [Citation(s) in RCA: 63] [Impact Index Per Article: 4.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/25/2010] [Revised: 06/15/2011] [Accepted: 07/25/2011] [Indexed: 12/29/2022]
Abstract
Microcystins (MCs) are toxic monocyclic heptapeptides produced by many cyanobacteria. MCs, especially MC-LR, cause toxic effects in animals and are a recognized potent cause of environmental stress and health hazard in aquatic ecosystems when heavy blooms of cyanobacteria appear. Consequently, one of the major problems is the chronic exposure of fish to cyanotoxins in their natural environment. The present experiment involving chronic exposure confirmed initial findings on acute exposure to MC contamination: exacerbated physiological stress and tissue damage in several tissues of exposed medaka fish. The gonads were affected specifically. In female gonads the modifications included reduction of the vitellus storage, lysis of the gonadosomatic tissue and disruption of the relationships between the follicular cells and the oocytes. In the males, spermatogenesis appeared to be disrupted. This is the first report showing that a cyanotoxin can affect reproductive function, and so can impact on fish reproduction and thus fish stocks.
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