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Lecoutre S, Rebière C, Maqdasy S, Lambert M, Dussaud S, Abatan JB, Dugail I, Gautier EL, Clément K, Marcelin G. Enhancing adipose tissue plasticity: progenitor cell roles in metabolic health. Nat Rev Endocrinol 2025; 21:272-288. [PMID: 39757324 DOI: 10.1038/s41574-024-01071-y] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Accepted: 11/27/2024] [Indexed: 01/07/2025]
Abstract
Adipose tissue demonstrates considerable plasticity and heterogeneity, enabling metabolic, cellular and structural adaptations to environmental signals. This adaptability is key for maintaining metabolic homeostasis. Impaired adipose tissue plasticity can lead to abnormal adipose tissue responses to metabolic cues, which contributes to the development of cardiometabolic diseases. In chronic obesity, white adipose tissue undergoes pathological remodelling marked by adipocyte hypertrophy, chronic inflammation and fibrosis, which are linked to local and systemic insulin resistance. Research data suggest that the capacity for healthy or unhealthy white adipose tissue remodelling might depend on the intrinsic diversity of adipose progenitor cells (APCs), which sense and respond to metabolic cues. This Review highlights studies on APCs as key determinants of adipose tissue plasticity, discussing differences between subcutaneous and visceral adipose tissue depots during development, growth and obesity. Modulating APC functions could improve strategies for treating adipose tissue dysfunction and metabolic diseases in obesity.
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Affiliation(s)
- Simon Lecoutre
- Nutrition and Obesities: Systemic Approach Research Group, Nutriomics, Sorbonne Université, INSERM, Paris, France.
| | - Clémentine Rebière
- Nutrition and Obesities: Systemic Approach Research Group, Nutriomics, Sorbonne Université, INSERM, Paris, France
| | - Salwan Maqdasy
- Department of Medicine, Karolinska Institutet Hospital, Stockholm, Sweden
| | - Mélanie Lambert
- Institut National de la Santé et de la Recherche Médicale, Bobigny, France
- Labex Inflamex, Université Sorbonne Paris Nord, Alliance Sorbonne Paris Cité, Bobigny, France
| | - Sébastien Dussaud
- Nutrition and Obesities: Systemic Approach Research Group, Nutriomics, Sorbonne Université, INSERM, Paris, France
| | - Jimon Boniface Abatan
- Nutrition and Obesities: Systemic Approach Research Group, Nutriomics, Sorbonne Université, INSERM, Paris, France
| | - Isabelle Dugail
- Nutrition and Obesities: Systemic Approach Research Group, Nutriomics, Sorbonne Université, INSERM, Paris, France
| | - Emmanuel L Gautier
- Nutrition and Obesities: Systemic Approach Research Group, Nutriomics, Sorbonne Université, INSERM, Paris, France
| | - Karine Clément
- Nutrition and Obesities: Systemic Approach Research Group, Nutriomics, Sorbonne Université, INSERM, Paris, France.
- Department of Nutrition, Pitie-Salpêtriere Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France.
| | - Geneviève Marcelin
- Nutrition and Obesities: Systemic Approach Research Group, Nutriomics, Sorbonne Université, INSERM, Paris, France.
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Rodrigues AM, Gimondi S, Quinteira R, Ferreira H, Martins A, Neves NM. Kidney-Derived ECM Hydrogels as Cell Delivery Devices. ACS APPLIED MATERIALS & INTERFACES 2025; 17:16421-16436. [PMID: 40062454 DOI: 10.1021/acsami.4c15873] [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: 03/21/2025]
Abstract
Chronic kidney disease (CKD) represents a significant global health challenge, as emphasized by its increasing prevalence and limited treatment options. Stem cell-based therapies are promising alternatives for CKD treatment. In particular, adipose-derived mesenchymal stem cells (ASCs) have emerged as an attractive candidate cell source. However, challenges in optimizing stem cell delivery and survival upon implantation persist. The inclusion of stem cells in hydrogels addresses these challenges by providing mechanical support coupled to bioactive cues essential for kidney regeneration. In particular, hydrogels derived from a decellularized kidney extracellular matrix (dKECM) offer a biomimetic platform rich in native and important renal components. Herein, we investigate the performance of dKECM hydrogels with respect to the differentiation of ASCs toward kidney-specific phenotypes. First, dKECM hydrogels were characterized and compared with commercially available collagen I hydrogels, which are typically used for this therapeutic application. Subsequently, we evaluated the performance of encapsulated human ASCs and proximal tubular cells (HK-2 cell line), elucidating the impact of these hydrogels on their viability, metabolic activity, proliferation, morphology, and renal phenotype. Our findings highlight the superior potential of dKECM hydrogels in promoting a sustained cellular activity and phenotype , underscoring their promise for CKD therapy. This study provides valuable insights into the potency of decellularized-based hydrogels as cell delivery vehicles, offering promising avenues for CKD treatment and kidney regeneration.
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Affiliation(s)
- Ana M Rodrigues
- 3B's Research Group, I3Bs - Research Institute on Biomaterials, Biodegradables and Biomimetics of University of Minho, AvePark, Parque de Ciência e Tecnologia, Rua Ave 1, Edificio 1 (Sede), Barco, Guimarães 4805-694, Portugal
- ICVS/3B's - PT Government Associate Laboratory, Guimarães 4710-057, Portugal
| | - Sara Gimondi
- 3B's Research Group, I3Bs - Research Institute on Biomaterials, Biodegradables and Biomimetics of University of Minho, AvePark, Parque de Ciência e Tecnologia, Rua Ave 1, Edificio 1 (Sede), Barco, Guimarães 4805-694, Portugal
- ICVS/3B's - PT Government Associate Laboratory, Guimarães 4710-057, Portugal
| | - Rita Quinteira
- 3B's Research Group, I3Bs - Research Institute on Biomaterials, Biodegradables and Biomimetics of University of Minho, AvePark, Parque de Ciência e Tecnologia, Rua Ave 1, Edificio 1 (Sede), Barco, Guimarães 4805-694, Portugal
- ICVS/3B's - PT Government Associate Laboratory, Guimarães 4710-057, Portugal
| | - Helena Ferreira
- 3B's Research Group, I3Bs - Research Institute on Biomaterials, Biodegradables and Biomimetics of University of Minho, AvePark, Parque de Ciência e Tecnologia, Rua Ave 1, Edificio 1 (Sede), Barco, Guimarães 4805-694, Portugal
- ICVS/3B's - PT Government Associate Laboratory, Guimarães 4710-057, Portugal
| | - Albino Martins
- 3B's Research Group, I3Bs - Research Institute on Biomaterials, Biodegradables and Biomimetics of University of Minho, AvePark, Parque de Ciência e Tecnologia, Rua Ave 1, Edificio 1 (Sede), Barco, Guimarães 4805-694, Portugal
- ICVS/3B's - PT Government Associate Laboratory, Guimarães 4710-057, Portugal
| | - Nuno M Neves
- 3B's Research Group, I3Bs - Research Institute on Biomaterials, Biodegradables and Biomimetics of University of Minho, AvePark, Parque de Ciência e Tecnologia, Rua Ave 1, Edificio 1 (Sede), Barco, Guimarães 4805-694, Portugal
- ICVS/3B's - PT Government Associate Laboratory, Guimarães 4710-057, Portugal
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Verling SD, Mashoudy K, Gompels M, Goldenberg G. Regenerative Medicine in Clinical and Aesthetic Dermatology. A COMPREHENSIVE GUIDE TO MALE AESTHETIC AND RECONSTRUCTIVE PLASTIC SURGERY 2024:65-79. [DOI: 10.1007/978-3-031-48503-9_10] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/06/2025]
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Karanfil AS, Louis F, Matsusaki M. Biofabrication of vascularized adipose tissues and their biomedical applications. MATERIALS HORIZONS 2023; 10:1539-1558. [PMID: 36789675 DOI: 10.1039/d2mh01391f] [Citation(s) in RCA: 4] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 05/10/2023]
Abstract
Recent advances in adipose tissue engineering and cell biology have led to the development of innovative therapeutic strategies in regenerative medicine for adipose tissue reconstruction. To date, the many in vitro and in vivo models developed for vascularized adipose tissue engineering cover a wide range of research areas, including studies with cells of various origins and types, polymeric scaffolds of natural and synthetic derivation, models presented using decellularized tissues, and scaffold-free approaches. In this review, studies on adipose tissue types with different functions, characteristics and body locations have been summarized with 3D in vitro fabrication approaches. The reason for the particular focus on vascularized adipose tissue models is that current liposuction and fat transplantation methods are unsuitable for adipose tissue reconstruction as the lack of blood vessels results in inadequate nutrient and oxygen delivery, leading to necrosis in situ. In the first part of this paper, current studies and applications of white and brown adipose tissues are presented according to the polymeric materials used, focusing on the studies which could show vasculature in vitro and after in vivo implantation, and then the research on adipose tissue fabrication and applications are explained.
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Affiliation(s)
- Aslı Sena Karanfil
- Department of Applied Chemistry, Graduate School of Engineering, Osaka University, Japan.
| | - Fiona Louis
- Joint Research Laboratory (TOPPAN) for Advanced Cell Regulatory Chemistry, Graduate School of Engineering, Osaka University, Japan
| | - Michiya Matsusaki
- Department of Applied Chemistry, Graduate School of Engineering, Osaka University, Japan.
- Joint Research Laboratory (TOPPAN) for Advanced Cell Regulatory Chemistry, Graduate School of Engineering, Osaka University, Japan
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Karacan I, Milthorpe B, Ben-Nissan B, Santos J. Stem Cells and Proteomics in Biomaterials and Biomedical Applications. SPRINGER SERIES IN BIOMATERIALS SCIENCE AND ENGINEERING 2022:125-157. [DOI: 10.1007/978-981-16-7435-8_4] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/05/2025]
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Bio-engineering a prevascularized human tri-layered skin substitute containing a hypodermis. Acta Biomater 2021; 134:215-227. [PMID: 34303011 DOI: 10.1016/j.actbio.2021.07.033] [Citation(s) in RCA: 34] [Impact Index Per Article: 8.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/14/2021] [Revised: 07/14/2021] [Accepted: 07/15/2021] [Indexed: 12/17/2022]
Abstract
Severe injuries to skin including hypodermis require full-thickness skin replacement. Here, we bioengineered a tri-layered human skin substitute (TLSS) containing the epidermis, dermis, and hypodermis. The hypodermal layer was generated by differentiation of human adipose stem cells (ASC) in a collagen type I hydrogel and combined with a prevascularized dermis consisting of human dermal microvascular endothelial cells and fibroblasts, which arranged into a dense vascular network. Subsequently, keratinocytes were seeded on top to generate the epidermal layer of the TLSS. The differentiation of ASC into adipocytes was confirmed in vitro on the mRNA level by the presence of adiponectin, as well as by the expression of perilipin and FABP-4 proteins. Moreover, functional characteristics of the hypodermis in vitro and in vivo were evaluated by Oil Red O, BODIPY, and AdipoRed stainings visualizing intracellular lipid droplets. Further, we demonstrated that both undifferentiated ASC and mature adipocytes present in the hypodermis influenced the keratinocyte maturation and homeostasis in the skin substitutes after transplantation. In particular, an enhanced secretion of TGF-β1 by these cells affected the epidermal morphogenesis as assessed by the expression of key proteins involved in the epidermal differentiation including cytokeratin 1, 10, 19 and cornified envelope formation such as involucrin. Here, we propose a novel functional hypodermal-dermo-epidermal tri-layered skin substitute containing blood capillaries that efficiently promote regeneration of skin defects. STATEMENT OF SIGNIFICANCE: The main objective of this study was to develop and assess the usefulness of a tri-layered human prevascularized skin substitute (TLSS) containing an epidermis, dermis, and hypodermis. The bioengineered hypodermis was generated from human adipose mesenchymal stem cells (ASC) and combined with a prevascularized dermis and epidermis. The TLSS represents an exceptional model for studying the role of cell-cell and cell-matrix interactions in vitro and in vivo. In particular, we observed that enhanced secretion of TGF-β1 in the hypodermis exerted a profound impact on fibroblast and keratinocyte differentiation, as well as epidermal barrier formation and homeostasis. Therefore, improved understanding of the cell-cell interactions in such a physiological skin model is essential to gain insights into different aspects of wound healing.
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Selegiline Induces Adipose tissue-derived Stem Cells into Neuron-like cells through MAPK Signaling Pathway. PHYSIOLOGY AND PHARMACOLOGY 2021. [DOI: 10.52547/phypha.26.1.4] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/18/2022]
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Wang MY, Wang YX, Li-Ling J, Xie HQ. Adult Stem Cell Therapy for Premature Ovarian Failure: From Bench to Bedside. TISSUE ENGINEERING PART B-REVIEWS 2021; 28:63-78. [PMID: 33427039 DOI: 10.1089/ten.teb.2020.0205] [Citation(s) in RCA: 18] [Impact Index Per Article: 4.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 02/05/2023]
Abstract
Premature ovarian failure (POF) is a devastating condition for women of childbearing age with serious health consequences, including distress, infertility, osteoporosis, autoimmune disorders, ischemic heart disease, and increased mortality. In addition to the mainstay estrogen therapy, stem cell therapy has been tested as the result of rapid progress in cell biology and reprogramming research. We hereby provide a review for the latest research and issues related with stem cell-based therapy for POF, and provide a commentary on various methods for enhancing its effect. Large amount of animal studies have demonstrated an extensive benefit of stem cells for failed ovarian recovering. As shown by such studies, stem cell therapy can result in recovery of hormonal levels, follicular activation, ovarian angiogenesis, and functional restoration. Meanwhile, a study of molecular pathways revealed that the function of stem cells mainly depends on their paracrine actions, which can produce multiple factors for the promotion of ovarian angiogenesis and regulation of cellular functions. Nevertheless, studies using disease models also revealed certain drawbacks. Clinical trials have shown that menstrual cycle and even pregnancy may occur in POF patients following transplantation of stem cells, although the limitations, including inadequate number of cases and space for the improvement of transplantation methodology. Only with its safety and effect get substantial improvement through laboratory experiments and clinical trials, can stem cell therapy really bring benefits to more patients. Additionally, effective pretreatment and appropriate transplantation methods for stem cells are also required. Taken together, stem cell therapy has shown a great potential for the reversal of POF and is stepping from bench to bedside. Impact statement Premature ovarian failure (POF) is a devastating condition with serious clinical consequences. The purpose of this review was to summarize the current status of stem cell therapy for POF. Considering the diversity of cell types and functions, a rigorous review is required for the guidance for further research into this field. Meanwhile, the challenges and prospect for clinical application of stem cell treatment, methodological improvements, and innovations are addressed.
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Affiliation(s)
- Ming-Yao Wang
- Laboratory of Stem Cell and Tissue Engineering, Orthopedic Research Institute, State Key Laboratory of Biotherapy and Cancer Center, West China Hospital, Sichuan University and Collaborative Innovation Center of Biotherapy, Chengdu, China
| | - Yi-Xuan Wang
- Laboratory of Stem Cell and Tissue Engineering, Orthopedic Research Institute, State Key Laboratory of Biotherapy and Cancer Center, West China Hospital, Sichuan University and Collaborative Innovation Center of Biotherapy, Chengdu, China
| | - Jesse Li-Ling
- Laboratory of Stem Cell and Tissue Engineering, Orthopedic Research Institute, State Key Laboratory of Biotherapy and Cancer Center, West China Hospital, Sichuan University and Collaborative Innovation Center of Biotherapy, Chengdu, China
| | - Hui-Qi Xie
- Laboratory of Stem Cell and Tissue Engineering, Orthopedic Research Institute, State Key Laboratory of Biotherapy and Cancer Center, West China Hospital, Sichuan University and Collaborative Innovation Center of Biotherapy, Chengdu, China
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Krongbaramee T, Zhu M, Qian Q, Zhang Z, Eliason S, Shu Y, Qian F, Akkouch A, Su D, Amendt BA, Yang L, Hong L. Plasmid encoding microRNA-200c ameliorates periodontitis and systemic inflammation in obese mice. MOLECULAR THERAPY-NUCLEIC ACIDS 2021; 23:1204-1216. [PMID: 33664998 PMCID: PMC7899952 DOI: 10.1016/j.omtn.2021.01.030] [Citation(s) in RCA: 21] [Impact Index Per Article: 5.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 10/12/2020] [Accepted: 01/28/2021] [Indexed: 02/08/2023]
Abstract
The present study was conducted to characterize microRNA-200c (miR-200c) and its regulators in adipogenic differentiation, obesity, and periodontitis in obese subjects (PiOSs), and to determine the therapeutic efficacy of plasmid DNA encoding miR-200c as a treatment for PiOSs. We report that highly expressed miR-200c in gingival tissues was downregulated in diet-induced obese (DIO) mice and during adipogenic differentiation of human bone marrow mesenchymal stromal cells (hBMSCs). Local injection of Porphyromonas gingivalis lipopolysaccharide (Pg-LPS) in the maxilla interdental gingiva of DIO mice reduced miR-200c in gingival and adipose tissues and induced periodontal inflammation associated with systemic elevation of interleukin-6 (IL-6) and impaired glucose tolerance. The inhibitory functions of Pg-LPS and IL-6 on miR-200c and their effectiveness on Zeb1 were confirmed in vitro. Injection of naked plasmid DNA encoding miR-200c into the gingiva effectively rescued miR-200c downregulation, prevented periodontal and systemic inflammation, and alleviated the impaired glucose metabolism in obese mice with LPS-induced periodontitis. Increased circulating exosomal miR-200c and its function on suppressing proinflammatory cytokines and adipogenesis explained the mechanism(s) of gingival application of miR-200c in attenuating systemic inflammation in PiOSs. These results demonstrated that miR-200c reduced by Pg-LPS and IL-6 in periodontitis and obesity might lead to the pathogenesis of PiOSs, and upregulation of miR-200c in the gingiva presents a therapeutic approach for PiOSs.
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Affiliation(s)
- Tadkamol Krongbaramee
- Iowa Institute for Oral Health Research, College of Dentistry, the University of Iowa, Iowa City, IA, USA
| | - Min Zhu
- Iowa Institute for Oral Health Research, College of Dentistry, the University of Iowa, Iowa City, IA, USA
| | - Qingwen Qian
- Department of Anatomy and Cell Biology, Fraternal Order of Eagles Diabetes Research Center, Pappajohn Biomedical Institute, University of Iowa Carver College of Medicine, Iowa City, IA, USA
| | - Zeyuan Zhang
- Department of Anatomy and Cell Biology, Fraternal Order of Eagles Diabetes Research Center, Pappajohn Biomedical Institute, University of Iowa Carver College of Medicine, Iowa City, IA, USA
| | - Steven Eliason
- Department of Anatomy and Cell Biology, Carver College of Medicine, the University of Iowa, Iowa City, IA, USA
| | - Yi Shu
- Iowa Institute for Oral Health Research, College of Dentistry, the University of Iowa, Iowa City, IA, USA
| | - Fang Qian
- Iowa Institute for Oral Health Research, College of Dentistry, the University of Iowa, Iowa City, IA, USA
| | - Adil Akkouch
- Iowa Institute for Oral Health Research, College of Dentistry, the University of Iowa, Iowa City, IA, USA
| | - Dan Su
- Department of Anatomy and Cell Biology, Carver College of Medicine, the University of Iowa, Iowa City, IA, USA
| | - Brad A Amendt
- Iowa Institute for Oral Health Research, College of Dentistry, the University of Iowa, Iowa City, IA, USA.,Department of Anatomy and Cell Biology, Carver College of Medicine, the University of Iowa, Iowa City, IA, USA.,Center for Craniofacial Anomalies Research, Carver College of Medicine, the University of Iowa, Iowa City, IA, USA
| | - Ling Yang
- Department of Anatomy and Cell Biology, Fraternal Order of Eagles Diabetes Research Center, Pappajohn Biomedical Institute, University of Iowa Carver College of Medicine, Iowa City, IA, USA
| | - Liu Hong
- Iowa Institute for Oral Health Research, College of Dentistry, the University of Iowa, Iowa City, IA, USA.,Center for Craniofacial Anomalies Research, Carver College of Medicine, the University of Iowa, Iowa City, IA, USA
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Banani MA, Rahmatullah M, Farhan N, Hancox Z, Yousaf S, Arabpour Z, Moghaddam ZS, Mozafari M, Sefat F. Adipose tissue-derived mesenchymal stem cells for breast tissue regeneration. Regen Med 2021; 16:47-70. [PMID: 33533667 DOI: 10.2217/rme-2020-0045] [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: 04/14/2020] [Accepted: 01/08/2021] [Indexed: 02/06/2023] Open
Abstract
With an escalating incidence of breast cancer cases all over the world and the deleterious psychological impact that mastectomy has on patients along with several limitations of the currently applied modalities, it's plausible to seek unconventional approaches to encounter such a burgeoning issue. Breast tissue engineering may allow that chance via providing more personalized solutions which are able to regenerate, mimicking natural tissues also facing the witnessed limitations. This review is dedicated to explore the utilization of adipose tissue-derived mesenchymal stem cells for breast tissue regeneration among postmastectomy cases focusing on biomaterials and cellular aspects in terms of harvesting, isolation, differentiation and new tissue formation as well as scaffolds types, properties, material-host interaction and an in vitro breast tissue modeling.
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Affiliation(s)
- Mohammed A Banani
- Division of Surgery & Interventional Science, University College London, London, NW3 2PS, UK
| | - Mohammed Rahmatullah
- Division of Surgery & Interventional Science, University College London, London, NW3 2PS, UK
| | - Nawras Farhan
- Division of Surgery & Interventional Science, University College London, London, NW3 2PS, UK
| | - Zoe Hancox
- Department of Biomedical & Electronics Engineering, School of Engineering, University of Bradford, Bradford, BD7 1DP, UK
| | - Safiyya Yousaf
- Department of Biomedical & Electronics Engineering, School of Engineering, University of Bradford, Bradford, BD7 1DP, UK
| | - Zohreh Arabpour
- Department of Biomedical & Electronics Engineering, School of Engineering, University of Bradford, Bradford, BD7 1DP, UK
| | - Zoha Salehi Moghaddam
- Department of Biomedical & Electronics Engineering, School of Engineering, University of Bradford, Bradford, BD7 1DP, UK
- Interdisciplinary Research Centre in Polymer Science & Technology (IRC Polymer), University of Bradford, Bradford, BD7 1DP, UK
| | - Masoud Mozafari
- Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, University of Toronto, Toronto, M5G 1X5, Canada
| | - Farshid Sefat
- Department of Biomedical & Electronics Engineering, School of Engineering, University of Bradford, Bradford, BD7 1DP, UK
- Interdisciplinary Research Centre in Polymer Science & Technology (IRC Polymer), University of Bradford, Bradford, BD7 1DP, UK
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Abstract
BACKGROUND Autologous fat grafting is a dynamic modality used in plastic surgery as an adjunct to improve functional and aesthetic form. However, current practices in fat grafting for soft-tissue augmentation are plagued by tremendous variability in long-term graft retention, resulting in suboptimal outcomes and repetitive procedures. This systematic review identifies and critically appraises the evidence for various enrichment strategies that can be used to augment and improve the viability of fat grafts. METHODS A comprehensive literature search of the Medline and PubMed databases was conducted for animal and human studies published through October of 2017 with multiple search terms related to adipose graft enrichment agents encompassing growth factors, platelet-rich plasma, adipose-derived and bone marrow stem cells, gene therapy, tissue engineering, and other strategies. Data on level of evidence, techniques, complications, and outcomes were collected. RESULTS A total of 1382 articles were identified, of which 147 met inclusion criteria. The majority of enrichment strategies demonstrated positive benefit for fat graft survival, particularly with growth factors and adipose-derived stem cell enrichment. Platelet-rich plasma and adipose-derived stem cells had the strongest evidence to support efficacy in human studies and may demonstrate a dose-dependent effect. CONCLUSIONS Improved understanding of enrichment strategies contributing to fat graft survival can help to optimize safety and outcomes. Controlled clinical studies are lacking, and future studies should examine factors influencing graft survival through controlled clinical trials in order to establish safety and to obtain consistent outcomes.
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Naumenko E, Fakhrullin R. Halloysite Nanoclay/Biopolymers Composite Materials in Tissue Engineering. Biotechnol J 2019; 14:e1900055. [PMID: 31556237 DOI: 10.1002/biot.201900055] [Citation(s) in RCA: 28] [Impact Index Per Article: 4.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/19/2019] [Revised: 08/23/2019] [Indexed: 12/29/2022]
Abstract
Biocompatible materials for the fabrication of tissue substitutes are crucially important in the advancement of modern medicinal biotechnology. These materials, to serve their function, should be similar in physical, chemical, biological, and structural properties to native tissues which they are aimed to mimic. The porosity of artificial scaffolds is essential for normal nutrient transmission to cells, gas diffusion, and cell attachment and proliferation. Nanoscale inorganic additives and dopants are widely used to improve the functional properties of the polymer materials for tissue engineering. Among these inorganic dopants, halloysite nanotubes are arguably the most perspective candidates because of their biocompatibility and functional properties allowing to enhance significantly the mechanical and chemical stability of tissue engineering scaffolds. Here, this vibrant field of biotechnology for regenerative medicine is overviewed.
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Affiliation(s)
- Ekaterina Naumenko
- Institute of Fundamental Medicine and Biology, Kazan Federal University, Kazan, 420008, Republic of Tatarstan, Russian Federation
| | - Rawil Fakhrullin
- Institute of Fundamental Medicine and Biology, Kazan Federal University, Kazan, 420008, Republic of Tatarstan, Russian Federation
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Ouellette MÈ, Bérubé JC, Bourget JM, Vallée M, Bossé Y, Fradette J. Linoleic acid supplementation of cell culture media influences the phospholipid and lipid profiles of human reconstructed adipose tissue. PLoS One 2019; 14:e0224228. [PMID: 31639818 PMCID: PMC6805161 DOI: 10.1371/journal.pone.0224228] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/20/2019] [Accepted: 10/08/2019] [Indexed: 01/09/2023] Open
Abstract
Reconstructed human adipose tissues represent novel tools available to perform in vitro pharmaco-toxicological studies. We used adipose-derived human stromal/stem cells to reconstruct, using tissue engineering techniques, such an adipose tridimensional model. To determine to what extent the in vitro model is representative of its native counterpart, adipogenic differentiation, triglycerides accumulation and phospholipids profiles were analysed. Ingenuity Pathway Analysis software revealed pathways enriched with differentially-expressed genes between native and reconstructed human adipose tissues. Interestingly, genes related to fatty acid metabolism were downregulated in vitro, which could be explained in part by the insufficient amount of essential fatty acids provided by the fetal calf serum used for the culture. Indeed, the lipid profile of the reconstructed human adipose tissues indicated a particular lack of linoleic acid, which could interfere with physiological cell processes such as membrane trafficking, signaling and inflammatory responses. Supplementation in the culture medium was able to influence the lipid profile of the reconstructed human adipose tissues. This study demonstrates the possibility to directly modulate the phospholipid profile of reconstructed human adipose tissues. This reinforces its use as a relevant physiological or pathological model for further pharmacological and metabolic studies of human adipose tissue functions.
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Affiliation(s)
- Marie-Ève Ouellette
- Centre de Recherche en Organogenèse Expérimentale de l'Université Laval/LOEX, Division of Regenerative Medicine, CHU de Québec -Université Laval Research Center, Québec, QC, Canada
- Department of Surgery, Faculty of Medicine, Université Laval, Québec, Canada
| | - Jean-Christophe Bérubé
- Centre de Recherche de l’Institut Universitaire de Cardiologie et de Pneumologie de Québec, Université Laval, Québec, QC, Canada
| | - Jean-Michel Bourget
- Centre de Recherche en Organogenèse Expérimentale de l'Université Laval/LOEX, Division of Regenerative Medicine, CHU de Québec -Université Laval Research Center, Québec, QC, Canada
- Department of Surgery, Faculty of Medicine, Université Laval, Québec, Canada
| | - Maud Vallée
- Centre de Recherche en Organogenèse Expérimentale de l'Université Laval/LOEX, Division of Regenerative Medicine, CHU de Québec -Université Laval Research Center, Québec, QC, Canada
- Department of Surgery, Faculty of Medicine, Université Laval, Québec, Canada
| | - Yohan Bossé
- Centre de Recherche de l’Institut Universitaire de Cardiologie et de Pneumologie de Québec, Université Laval, Québec, QC, Canada
- Department of Molecular Medicine, Faculty of Medicine, Université Laval, Québec, Canada
| | - Julie Fradette
- Centre de Recherche en Organogenèse Expérimentale de l'Université Laval/LOEX, Division of Regenerative Medicine, CHU de Québec -Université Laval Research Center, Québec, QC, Canada
- Department of Surgery, Faculty of Medicine, Université Laval, Québec, Canada
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O'Halloran N, Khan S, Gilligan K, Dwyer R, Kerin M, Lowery A. Oncological Risk in Autologous Stem Cell Donation for Novel Tissue-Engineering Approaches to Postmastectomy Breast Regeneration. BREAST CANCER-BASIC AND CLINICAL RESEARCH 2019; 13:1178223419864896. [PMID: 31555047 PMCID: PMC6753512 DOI: 10.1177/1178223419864896] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 06/25/2019] [Accepted: 06/26/2019] [Indexed: 01/30/2023]
Abstract
Adipose tissue engineering using adipose-derived stem cells (ADSCs) has emerged
as an opportunity to develop novel approaches to postmastectomy breast
reconstruction with the potential for an autologous tissue source with a natural
appearance and texture. As of yet, the role of ADSCs in breast cancer
development and metastasis is not completely understood; therefore, we must
consider the oncological safety of employing an autologous source of ADSCs for
use in breast regeneration. This study investigated the regenerative properties
of ADSCs isolated from breast cancer patients, including those who had received
neoadjuvant chemotherapy, and noncancer controls. The ADSCs were characterised
for several parameters central to tissue regeneration, including cell viability,
proliferation, differentiation potential, and cytokine secretion. A stem cell
population was isolated and confirmed by flow cytometry and multilineage
differentiation. There was no difference in cell phenotype or surface antigen
expression between ADSCs from different sources. Adipose-derived stem cells
isolated from the breast of cancer patients exhibited reduced adipogenic
differentiation potential compared with ADSCs from other sources. The greatest
degree of adipogenic differentiation was observed in ADSCs isolated from the
subcutaneous abdominal fat of noncancer controls. The proliferation rate of
ADSCs isolated from the breast of cancer patients was increased compared with
other sources; however, it was decreased in ADSCs isolated from breast cancer
patients who had recently been treated with neoadjuvant chemotherapy. A number
of cytokines were detected in the cell conditioned media of ADSCs from different
sources, including matrix metalloproteinase-2 (MMP-2), which was detected at
higher levels in the secretome of ADSCs from breast cancer patients compared
with noncancer controls. This study provides important information relating to
the suitability of ADSCs as an autologous cell source for adipose tissue
engineering in postcancer reconstruction. Results indicate that while the
surface phenotype does not differ, the differentiation capacity, proliferative
rate, and secreted cytokine profile are affected by the presence or treatment of
breast cancer. These findings support further investigation into the
regenerative potential of these ADSCs, if they are to be considered in clinical
reconstructive strategies.
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Affiliation(s)
- Niamh O'Halloran
- Discipline of Surgery, The Lambe Institute for Translational Research, National University of Ireland Galway, Galway, Ireland
| | - Sonja Khan
- Discipline of Surgery, The Lambe Institute for Translational Research, National University of Ireland Galway, Galway, Ireland
| | - Katie Gilligan
- Discipline of Surgery, The Lambe Institute for Translational Research, National University of Ireland Galway, Galway, Ireland
| | - Roisin Dwyer
- Discipline of Surgery, The Lambe Institute for Translational Research, National University of Ireland Galway, Galway, Ireland
| | - Michael Kerin
- Discipline of Surgery, The Lambe Institute for Translational Research, National University of Ireland Galway, Galway, Ireland
| | - Aoife Lowery
- Discipline of Surgery, The Lambe Institute for Translational Research, National University of Ireland Galway, Galway, Ireland
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15
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Ishihara M, Kishimoto S, Nakamura S, Fukuda K, Sato Y, Hattori H. Biomaterials as cell carriers for augmentation of adipose tissue-derived stromal cell transplantation. Biomed Mater Eng 2019; 29:567-585. [PMID: 30400072 DOI: 10.3233/bme-181009] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/01/2023]
Abstract
Adipose tissue-derived stromal cells (ADSCs) contain lineage-committed progenitor cells that have the ability to differentiate into various cell types that may be useful for autologous cell transplantation to correct defects of skin, adipose, cartilage, bone, tendon, and blood vessels. The multipotent characteristics of ADSCs, as well as their abundance in the human body, make them an attractive potential resource for wound repair and applications to tissue engineering. ADSC transplantation has been used in combination with biomaterials, including cell sheets, hydrogel, and three-dimensional (3D) scaffolds based on chitosan, fibrin, atelocollagen, and decellularized porcine dermis, etc. Furthermore, low molecular weight heparin/protamine nanoparticles (LH/P NPs) have been used as an inducer of ADSC aggregation. The tissue engineering potential of these biomaterials as cell carriers is increased by the synergistic relationship between ADSCs and the biomaterials, resulting in the release of angiogenic cytokines and growth factors. In this review article, we describe the advantages of ADSC transplantation for tissue engineering, focusing on biomaterials as cell carriers which we have studied.
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Affiliation(s)
- Masayuki Ishihara
- Division of Biomedical Engineering Research Institute, National Defense Medical College, Saitama 359-8513, Japan
| | - Satoko Kishimoto
- Research Support Center, Dokkyo Medical University, Tochigi 321-0293, Japan
| | - Shingo Nakamura
- Division of Biomedical Engineering Research Institute, National Defense Medical College, Saitama 359-8513, Japan
| | - Koichi Fukuda
- Division of Biomedical Engineering Research Institute, National Defense Medical College, Saitama 359-8513, Japan
| | - Yoko Sato
- Division of Biomedical Engineering Research Institute, National Defense Medical College, Saitama 359-8513, Japan
| | - Hidemi Hattori
- Department of Biochemistry and Applied Sciences, University of Miyazaki, Miyazaki 889-2162, Japan
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16
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Cho KH, Uthaman S, Park IK, Cho CS. Injectable Biomaterials in Plastic and Reconstructive Surgery: A Review of the Current Status. Tissue Eng Regen Med 2018; 15:559-574. [PMID: 30603579 PMCID: PMC6171701 DOI: 10.1007/s13770-018-0158-2] [Citation(s) in RCA: 14] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/20/2018] [Revised: 08/03/2018] [Accepted: 08/21/2018] [Indexed: 02/06/2023] Open
Abstract
BACKGROUND Injectable biomaterials have attracted increasing attention for volume restoration and tissue regeneration. The main aim of this review is to discuss the current status of the injectable biomaterials for correction of tissue defects in plastic and reconstructive surgery. METHODS Requirements of injectable biomaterials, mechanism of in situ gelation, characteristics, and the combinational usage of adipose-derived stem cells (ADSCs) and growth factors were reviewed. RESULTS The ideal injectable biomaterials should be biocompatible, non-toxic, easy to use, and cost-effective. Additionally, it should possess adequate mechanical properties and stability. In situ gelation method includes physical, chemical, enzymatic and photo-initiated methods. Natural and synthetic biomaterials carry their pros and cons due to their inherent properties. The combined use of ADSCs and growth factors provides enhanced potential for adipose tissue regeneration. CONCLUSIONS The usage of injectable biomaterials has been increasing for the tissue restoration and regeneration. The future of incorporating ADSCs and growth factors into the injectable biomaterials is promising.
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Affiliation(s)
- Ki-Hyun Cho
- Department of Plastic Surgery, Cleveland Clinic, Cleveland, OH 44195 USA
| | - Saji Uthaman
- Department of Polymer Science and Engineering, Chungnam National University, 99 Daehak-ro, Yuseong-gu, Daejeon, 34134 Republic of Korea
| | - In-Kyu Park
- Department of Biomedical Sciences, Chonnam National University Medical School, 160 Baekseo-ro, Gwangju, 61469 Republic of Korea
| | - Chong-Su Cho
- Research Institute for Agriculture and Life Sciences, Seoul National University, 1 Gwanak-ro, Gwanak-gu, Seoul, 08826 Republic of Korea
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17
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Zou J, Wang W, Neffe AT, Xu X, Li Z, Deng Z, Sun X, Ma N, Lendlein A. Adipogenic differentiation of human adipose derived mesenchymal stem cells in 3D architectured gelatin based hydrogels (ArcGel). Clin Hemorheol Microcirc 2018; 67:297-307. [PMID: 28885199 DOI: 10.3233/ch-179210] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/13/2022]
Abstract
Polymeric matrices mimicking multiple functions of the ECM are expected to enable a material induced regeneration of tissues. Here, we investigated the adipogenic differentiation of human adipose derived mesenchymal stem cells (hADSCs) in a 3D architectured gelatin based hydrogel (ArcGel) prepared from gelatin and L-lysine diisocyanate ethyl ester (LDI) in an one-step process, in which the formation of an open porous morphology and the chemical network formation were integrated. The ArcGel was designed to support adipose tissue regeneration with its 3D porous structure, high cell biocompatibility, and mechanical properties compatible with human subcutaneous adipose tissue. The ArcGel could support initial cell adhesion and survival of hADSCs. Under static culture condition, the cells could migrate into the inner part of the scaffold with a depth of 840±120 μm after 4 days, and distributed in the whole scaffold (2 mm in thickness) within 14 days. The cells proliferated in the scaffold and the fold increase of cell number after 7 days of culture was 2.55±0.08. The apoptotic rate of hADSCs in the scaffold was similar to that of cells maintained on tissue culture plates. When cultured in adipogenic induction medium, the hADSCs in the scaffold differentiated into adipocytes with a high efficiency (93±1%). Conclusively, this gelatin based 3D scaffold presented high cell compatibility for hADSC cultivation and differentiation, which could serve as a potential implant material in clinical applications for adipose tissue reparation and regeneration.
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Affiliation(s)
- Jie Zou
- Institute of Biomaterial Science and Berlin-Brandenburg Centre for Regenerative Therapies, Helmholtz-Zentrum Geesthacht, Teltow, Germany.,Institute of Chemistry and Biochemistry, Freie Universität, Berlin, Germany
| | - Weiwei Wang
- Institute of Biomaterial Science and Berlin-Brandenburg Centre for Regenerative Therapies, Helmholtz-Zentrum Geesthacht, Teltow, Germany
| | - Axel T Neffe
- Institute of Biomaterial Science and Berlin-Brandenburg Centre for Regenerative Therapies, Helmholtz-Zentrum Geesthacht, Teltow, Germany.,Helmholtz Virtual Institute "Multifunctional Biomaterials in Medicine", Teltow, Germany
| | - Xun Xu
- Institute of Biomaterial Science and Berlin-Brandenburg Centre for Regenerative Therapies, Helmholtz-Zentrum Geesthacht, Teltow, Germany.,Institute of Chemistry and Biochemistry, Freie Universität, Berlin, Germany
| | - Zhengdong Li
- Institute of Biomaterial Science and Berlin-Brandenburg Centre for Regenerative Therapies, Helmholtz-Zentrum Geesthacht, Teltow, Germany.,Institute of Chemistry and Biochemistry, Freie Universität, Berlin, Germany
| | - Zijun Deng
- Institute of Biomaterial Science and Berlin-Brandenburg Centre for Regenerative Therapies, Helmholtz-Zentrum Geesthacht, Teltow, Germany.,Institute of Chemistry and Biochemistry, Freie Universität, Berlin, Germany
| | - Xianlei Sun
- Institute of Biomaterial Science and Berlin-Brandenburg Centre for Regenerative Therapies, Helmholtz-Zentrum Geesthacht, Teltow, Germany.,Institute of Biochemistry and Biology, Universität Potsdam, Potsdam, Germany
| | - Nan Ma
- Institute of Biomaterial Science and Berlin-Brandenburg Centre for Regenerative Therapies, Helmholtz-Zentrum Geesthacht, Teltow, Germany.,Institute of Chemistry and Biochemistry, Freie Universität, Berlin, Germany.,Helmholtz Virtual Institute "Multifunctional Biomaterials in Medicine", Teltow, Germany
| | - Andreas Lendlein
- Institute of Biomaterial Science and Berlin-Brandenburg Centre for Regenerative Therapies, Helmholtz-Zentrum Geesthacht, Teltow, Germany.,Institute of Chemistry and Biochemistry, Freie Universität, Berlin, Germany.,Helmholtz Virtual Institute "Multifunctional Biomaterials in Medicine", Teltow, Germany.,Institute of Biochemistry and Biology, Universität Potsdam, Potsdam, Germany
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18
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Huang Q, Zou Y, Arno MC, Chen S, Wang T, Gao J, Dove AP, Du J. Hydrogel scaffolds for differentiation of adipose-derived stem cells. Chem Soc Rev 2018; 46:6255-6275. [PMID: 28816316 DOI: 10.1039/c6cs00052e] [Citation(s) in RCA: 258] [Impact Index Per Article: 36.9] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/15/2022]
Abstract
Natural extracellular matrices (ECMs) have been widely used as a support for the adhesion, migration, differentiation, and proliferation of adipose-derived stem cells (ADSCs). However, poor mechanical behavior and unpredictable biodegradation properties of natural ECMs considerably limit their potential for bioapplications and raise the need for different, synthetic scaffolds. Hydrogels are regarded as the most promising alternative materials as a consequence of their excellent swelling properties and their resemblance to soft tissues. A variety of strategies have been applied to create synthetic biomimetic hydrogels, and their biophysical and biochemical properties have been modulated to be suitable for cell differentiation. In this review, we first give an overview of common methods for hydrogel preparation with a focus on those strategies that provide potential advantages for ADSC encapsulation, before summarizing the physical properties of hydrogel scaffolds that can act as biological cues. Finally, the challenges in the preparation and application of hydrogels with ADSCs are explored and the perspectives are proposed for the next generation of scaffolds.
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Affiliation(s)
- Qiutong Huang
- Department of Polymeric Materials, School of Materials Science and Engineering, Tongji University, 4800 Caoan Road, Shanghai, 201804, China.
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19
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Mir M, Ali MN, Barakullah A, Gulzar A, Arshad M, Fatima S, Asad M. Synthetic polymeric biomaterials for wound healing: a review. Prog Biomater 2018; 7:1-21. [PMID: 29446015 PMCID: PMC5823812 DOI: 10.1007/s40204-018-0083-4] [Citation(s) in RCA: 280] [Impact Index Per Article: 40.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/20/2017] [Accepted: 01/27/2018] [Indexed: 12/21/2022] Open
Abstract
Wounds are of a variety of types and each category has its own distinctive healing requirements. This realization has spurred the development of a myriad of wound dressings, each with specific characteristics. It is unrealistic to expect a singular dressing to embrace all characteristics that would fulfill generic needs for wound healing. However, each dressing may approach the ideal requirements by deviating from the 'one size fits all approach', if it conforms strictly to the specifications of the wound and the patient. Indeed, a functional wound dressing should achieve healing of the wound with minimal time and cost expenditures. This article offers an insight into several different types of polymeric materials clinically used in wound dressings and the events taking place at cellular level, which aid the process of healing, while the biomaterial dressing interacts with the body tissue. Hence, the significance of using synthetic polymer films, foam dressings, hydrocolloids, alginate dressings, and hydrogels has been reviewed, and the properties of these materials that conform to wound-healing requirements have been explored. A special section on bioactive dressings and bioengineered skin substitutes that play an active part in healing process has been re-examined in this work.
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Affiliation(s)
- Mariam Mir
- Biomedical Engineering and Sciences Department, School of Mechanical and Manufacturing Engineering (SMME), National University of Sciences and Technology (NUST), Sector H-12, Islamabad, Pakistan
| | - Murtaza Najabat Ali
- Biomedical Engineering and Sciences Department, School of Mechanical and Manufacturing Engineering (SMME), National University of Sciences and Technology (NUST), Sector H-12, Islamabad, Pakistan.
| | - Afifa Barakullah
- Biomedical Engineering and Sciences Department, School of Mechanical and Manufacturing Engineering (SMME), National University of Sciences and Technology (NUST), Sector H-12, Islamabad, Pakistan
| | - Ayesha Gulzar
- Biomedical Engineering and Sciences Department, School of Mechanical and Manufacturing Engineering (SMME), National University of Sciences and Technology (NUST), Sector H-12, Islamabad, Pakistan
| | - Munam Arshad
- Biomedical Engineering and Sciences Department, School of Mechanical and Manufacturing Engineering (SMME), National University of Sciences and Technology (NUST), Sector H-12, Islamabad, Pakistan
| | - Shizza Fatima
- Biomedical Engineering and Sciences Department, School of Mechanical and Manufacturing Engineering (SMME), National University of Sciences and Technology (NUST), Sector H-12, Islamabad, Pakistan
| | - Maliha Asad
- Biomedical Engineering and Sciences Department, School of Mechanical and Manufacturing Engineering (SMME), National University of Sciences and Technology (NUST), Sector H-12, Islamabad, Pakistan
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20
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21
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Storck K, Fischer R, Buchberger M, Haller B, Regn S. Delivered adipose-derived stromal cells improve host-derived adipose tissue formation in composite constructs in vivo. Laryngoscope 2017; 127:E428-E436. [PMID: 28599055 DOI: 10.1002/lary.26694] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/18/2017] [Revised: 04/13/2017] [Accepted: 04/21/2017] [Indexed: 12/12/2022]
Abstract
OBJECTIVES/HYPOTHESIS Adipose tissue engineering aims to provide functional tissue surrogates for the restoration of soft tissue defects and contour deformities in the face. Many studies involve the delivery of cells; however, the impact and the exact role of the implanted cells is not yet fully elucidated. STUDY DESIGN Animal research. METHODS In this study, we used a mouse model for the development of volume-stable adipose tissue using polyurethane scaffolds combined with a long-term stable fibrin gel and adipose-derived stromal cells to investigate the influence of cell delivery on tissue development. RESULTS After 12 weeks in vivo, the emerging tissue in these constructs was shown to be exclusively of host origin by human-specific vimentin staining. Comparison of unseeded versus seeded scaffolds revealed a significant effect of the delivered cells on adipose tissue development as shown by histological staining and histomorphometric quantification of adipocytes, whereas blood vessel formation was not affected by delivery of adipose-derived stromal cells at this time point. CONCLUSIONS This is evidence for an indirect action of the implanted cells, providing a proadipogenic microenvironment within constructs, which was further boosted by adipogenic precultivation of the seeded constructs. Especially in peripheral areas of the constructs, the number of adipocytes was significantly elevated in seeded scaffolds compared to nonseeded controls, suggesting that the implanted cells likely triggered the invasion and differentiation of host cells. This is supported by the fact that the provision of a fat rich environment (by coverage of the constructs with a fat flap upon implantation) additionally stimulated adipose tissue formation. LEVEL OF EVIDENCE NA. Laryngoscope, 127:E428-E436, 2017.
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Affiliation(s)
- Katharina Storck
- Ear, Nose, and Throat, Head and Neck Surgery Department, Technical University of Munich, Munich, Germany
| | - Reyk Fischer
- Ear, Nose, and Throat, Head and Neck Surgery Department, Technical University of Munich, Munich, Germany
| | - Maria Buchberger
- Ear, Nose, and Throat, Head and Neck Surgery Department, Technical University of Munich, Munich, Germany
| | - Bernhard Haller
- Institute of Medical Statistics and Epidemiology , Technical University of Munich, Munich, Germany
| | - Sybille Regn
- Ear, Nose, and Throat, Head and Neck Surgery Department, Technical University of Munich, Munich, Germany
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22
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Naderi N, Combellack EJ, Griffin M, Sedaghati T, Javed M, Findlay MW, Wallace CG, Mosahebi A, Butler PEM, Seifalian AM, Whitaker IS. The regenerative role of adipose-derived stem cells (ADSC) in plastic and reconstructive surgery. Int Wound J 2017; 14:112-124. [PMID: 26833722 PMCID: PMC7949873 DOI: 10.1111/iwj.12569] [Citation(s) in RCA: 117] [Impact Index Per Article: 14.6] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/04/2015] [Revised: 11/24/2015] [Accepted: 12/01/2015] [Indexed: 12/12/2022] Open
Abstract
The potential use of stem cell-based therapies for the repair and regeneration of various tissues and organs offers a paradigm shift in plastic and reconstructive surgery. The use of either embryonic stem cells (ESC) or induced pluripotent stem cells (iPSC) in clinical situations is limited because of regulations and ethical considerations even though these cells are theoretically highly beneficial. Adult mesenchymal stem cells appear to be an ideal stem cell population for practical regenerative medicine. Among these cells, adipose-derived stem cells (ADSC) have the potential to differentiate the mesenchymal, ectodermal and endodermal lineages and are easy to harvest. Additionally, adipose tissue yields a high number of ADSC per volume of tissue. Based on this background knowledge, the purpose of this review is to summarise and describe the proliferation and differentiation capacities of ADSC together with current preclinical data regarding the use of ADSC as regenerative tools in plastic and reconstructive surgery.
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Affiliation(s)
- Naghmeh Naderi
- Reconstructive Surgery & Regenerative Medicine Group, Institute of Life Sciences (ILS)Swansea University Medical SchoolSwanseaUK
- Welsh Centre for Burns & Plastic SurgeryABMU Health BoardSwanseaUK
| | - Emman J Combellack
- Reconstructive Surgery & Regenerative Medicine Group, Institute of Life Sciences (ILS)Swansea University Medical SchoolSwanseaUK
- Welsh Centre for Burns & Plastic SurgeryABMU Health BoardSwanseaUK
| | - Michelle Griffin
- UCL Centre for Nanotechnology and Regenerative MedicineUniversity College LondonLondonUK
| | - Tina Sedaghati
- UCL Centre for Nanotechnology and Regenerative MedicineUniversity College LondonLondonUK
| | - Muhammad Javed
- Reconstructive Surgery & Regenerative Medicine Group, Institute of Life Sciences (ILS)Swansea University Medical SchoolSwanseaUK
- Welsh Centre for Burns & Plastic SurgeryABMU Health BoardSwanseaUK
| | - Michael W Findlay
- Plastic & Reconstructive SurgeryStanford University Medical CentreStanfordCAUSA
| | | | - Afshin Mosahebi
- UCL Centre for Nanotechnology and Regenerative MedicineUniversity College LondonLondonUK
- Department of Plastic SurgeryRoyal Free NHS Foundation TrustLondonUK
| | - Peter EM Butler
- Department of Plastic SurgeryRoyal Free NHS Foundation TrustLondonUK
| | - Alexander M Seifalian
- UCL Centre for Nanotechnology and Regenerative MedicineUniversity College LondonLondonUK
| | - Iain S Whitaker
- Reconstructive Surgery & Regenerative Medicine Group, Institute of Life Sciences (ILS)Swansea University Medical SchoolSwanseaUK
- Welsh Centre for Burns & Plastic SurgeryABMU Health BoardSwanseaUK
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23
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Pyrintegrin Induces Soft Tissue Formation by Transplanted or Endogenous Cells. Sci Rep 2017; 7:36402. [PMID: 28128224 PMCID: PMC5269584 DOI: 10.1038/srep36402] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/06/2016] [Accepted: 09/16/2016] [Indexed: 12/11/2022] Open
Abstract
Focal adipose deficiency, such as lipoatrophy, lumpectomy or facial trauma, is a formidable challenge in reconstructive medicine, and yet scarcely investigated in experimental studies. Here, we report that Pyrintegrin (Ptn), a 2,4-disubstituted pyrimidine known to promote embryonic stem cells survival, is robustly adipogenic and induces postnatal adipose tissue formation in vivo of transplanted adipose stem/progenitor cells (ASCs) and recruited endogenous cells. In vitro, Ptn stimulated human adipose tissue derived ASCs to differentiate into lipid-laden adipocytes by upregulating peroxisome proliferator-activated receptor (PPARγ) and CCAAT/enhancer-binding protein-α (C/EBPα), with differentiated cells increasingly secreting adiponectin, leptin, glycerol and total triglycerides. Ptn-primed human ASCs seeded in 3D-bioprinted biomaterial scaffolds yielded newly formed adipose tissue that expressed human PPARγ, when transplanted into the dorsum of athymic mice. Remarkably, Ptn-adsorbed 3D scaffolds implanted in the inguinal fat pad had enhanced adipose tissue formation, suggesting Ptn’s ability to induce in situ adipogenesis of endogenous cells. Ptn promoted adipogenesis by upregulating PPARγ and C/EBPα not only in adipogenesis induction medium, but also in chemically defined medium specifically for osteogenesis, and concurrently attenuated Runx2 and Osx via BMP-mediated SMAD1/5 phosphorylation. These findings suggest Ptn’s novel role as an adipogenesis inducer with a therapeutic potential in soft tissue reconstruction and augmentation.
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24
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Combellack EJ, Jessop ZM, Naderi N, Griffin M, Dobbs T, Ibrahim A, Evans S, Burnell S, Doak SH, Whitaker IS. Adipose regeneration and implications for breast reconstruction: update and the future. Gland Surg 2016; 5:227-41. [PMID: 27047789 PMCID: PMC4791352 DOI: 10.3978/j.issn.2227-684x.2016.01.01] [Citation(s) in RCA: 16] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/28/2015] [Accepted: 10/17/2015] [Indexed: 12/20/2022]
Abstract
The evolution of breast reconstruction and management of breast cancer has evolved significantly since the earliest descriptions in the Edwin Smith Papyrus (3,000 BC). The development of surgical and scientific expertise has changed the way that women are managed, and plastic surgeons are now able to offer a wide range of reconstructive options to suit individual needs. Beyond the gold standard autologous flap based reconstructions, regenerative therapies promise the elimination of donor site morbidity whilst providing equivalent aesthetic and functional outcomes. Future research aims to address questions regarding ideal cell source, optimisation of scaffold composition and interaction of de novo adipose tissue in the microenvironment of breast cancer.
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25
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Newsom EC, Connolly KL, Nehal KS. Facilitating Healing of Granulating Wounds: Dressings, Dermal Substitutes, and Other Methods. CURRENT DERMATOLOGY REPORTS 2015. [DOI: 10.1007/s13671-015-0108-3] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/30/2022]
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26
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Storck K, Ell J, Regn S, Rittler-Ungetüm B, Mayer H, Schantz T, Müller D, Buchberger M. Optimization of in vitro cultivation strategies for human adipocyte derived stem cells. Adipocyte 2015; 4:181-7. [PMID: 26257991 PMCID: PMC4496977 DOI: 10.4161/21623945.2014.987580] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/07/2014] [Revised: 10/16/2014] [Accepted: 11/10/2014] [Indexed: 01/07/2023] Open
Abstract
With adipose-derived stem cells being in the focus of research in regenerative medicine, the need arises for fast reliable cultivation protocols. We have tested the cultivation of human adipose-derived stem cells in endothelial cell growth medium prior to induction and differentiation, against the long-established use of DMEM/F12 medium-based cultivation protocols. We found that cultivation in endothelial cell growth medium not only accelerates growth before induction and differentiation, but also allows shorter induction and differentiation times than those following precultivation with DMEM/F12 medium with regard to the formation of mature adipocytes and to the viability undifferentiated cells. These results were first observed morphologically but could be confirmed by performing adiponectin ELISA and cell proliferation assays.
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Affiliation(s)
- K Storck
- Department of Oto- Rhino- Laryngology; Head and Neck Surgery; Klinikum Rechts der Isar der TU München; Munich, Germany
| | - J Ell
- Department of Oto- Rhino- Laryngology; Head and Neck Surgery; Klinikum Rechts der Isar der TU München; Munich, Germany
| | - S Regn
- Department of Oto- Rhino- Laryngology; Head and Neck Surgery; Klinikum Rechts der Isar der TU München; Munich, Germany
| | - B Rittler-Ungetüm
- Department of Oto- Rhino- Laryngology; Head and Neck Surgery; Klinikum Rechts der Isar der TU München; Munich, Germany
| | - H Mayer
- Department of Oto- Rhino- Laryngology; Head and Neck Surgery; Klinikum Rechts der Isar der TU München; Munich, Germany
| | - T Schantz
- Department of Plastic and Reconstructive Surgery; Klinikum Rechts der Isar der TU München; Munich, Germany
| | - D Müller
- Department of Plastic and Reconstructive Surgery; Klinikum Rechts der Isar der TU München; Munich, Germany
| | - M Buchberger
- Department of Oto- Rhino- Laryngology; Head and Neck Surgery; Klinikum Rechts der Isar der TU München; Munich, Germany
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27
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Stanley SA, Sauer J, Kane RS, Dordick JS, Friedman JM. Remote regulation of glucose homeostasis in mice using genetically encoded nanoparticles. Nat Med 2015; 21:92-98. [PMID: 25501906 PMCID: PMC4894538 DOI: 10.1038/nm.3730] [Citation(s) in RCA: 159] [Impact Index Per Article: 15.9] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/19/2013] [Accepted: 08/11/2014] [Indexed: 12/15/2022]
Abstract
Means for temporally regulating gene expression and cellular activity are invaluable for elucidating underlying physiological processes and would have therapeutic implications. Here we report the development of a genetically encoded system for remote regulation of gene expression by low-frequency radio waves (RFs) or a magnetic field. Iron oxide nanoparticles are synthesized intracellularly as a GFP-tagged ferritin heavy and light chain fusion. The ferritin nanoparticles associate with a camelid anti-GFP-transient receptor potential vanilloid 1 fusion protein, αGFP-TRPV1, and can transduce noninvasive RF or magnetic fields into channel activation, also showing that TRPV1 can transduce a mechanical stimulus. This, in turn, initiates calcium-dependent transgene expression. In mice with stem cell or viral expression of these genetically encoded components, remote stimulation of insulin transgene expression with RF or a magnet lowers blood glucose. This robust, repeatable method for remote regulation in vivo may ultimately have applications in basic science, technology and therapeutics.
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Affiliation(s)
- Sarah A Stanley
- Laboratory of Molecular Genetics, Rockefeller University, New York, New York, USA
| | - Jeremy Sauer
- Department of Chemical and Biological Engineering, Department of Biology, Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, New York, USA
| | - Ravi S Kane
- Department of Chemical and Biological Engineering, Department of Biology, Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, New York, USA
| | - Jonathan S Dordick
- Department of Chemical and Biological Engineering, Department of Biology, Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, New York, USA
| | - Jeffrey M Friedman
- Laboratory of Molecular Genetics, Rockefeller University, New York, New York, USA
- Howard Hughes Medical Institute, New York, New York, USA
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Rhee SM, You HJ, Han SK. Injectable tissue-engineered soft tissue for tissue augmentation. J Korean Med Sci 2014; 29 Suppl 3:S170-5. [PMID: 25473206 PMCID: PMC4248002 DOI: 10.3346/jkms.2014.29.s3.s170] [Citation(s) in RCA: 13] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/03/2014] [Accepted: 07/06/2014] [Indexed: 01/31/2023] Open
Abstract
Soft tissue augmentation is a process of implanting tissues or materials to treat wrinkles or soft tissue defects in the body. Over the years, various materials have evolved to correct soft tissue defects, including a number of tissues and polymers. Autogenous dermis, autogenous fat, autogenous dermis-fat, allogenic dermis, synthetic implants, and fillers have been widely accepted for soft tissue augmentations. Tissue engineering technology has also been introduced and opened a new venue of opportunities in this field. In particular, a long-lasting filler consisting of hyaluronic acid filler and living human mesenchymal cells called "injectable tissue-engineered soft tissue" has been created and applied clinically, as this strategy has many advantages over conventional methods. Fibroblasts and adipose-derived stromal vascular fraction cells can be clinically used as injectable tissue-engineered soft tissue at present. In this review, information on the soft tissue augmentation method using the injectable tissue-engineered soft tissue is provided.
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Affiliation(s)
- Sung-Mi Rhee
- Department of Plastic Surgery, Korea University College of Medicine, Seoul, Korea
| | - Hi-Jin You
- Department of Plastic Surgery, Korea University College of Medicine, Seoul, Korea
| | - Seung-Kyu Han
- Department of Plastic Surgery, Korea University College of Medicine, Seoul, Korea
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29
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Hyvönen MT, Spalding KL. Maintenance of white adipose tissue in man. Int J Biochem Cell Biol 2014; 56:123-32. [PMID: 25240584 DOI: 10.1016/j.biocel.2014.09.013] [Citation(s) in RCA: 17] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/14/2014] [Revised: 08/30/2014] [Accepted: 09/09/2014] [Indexed: 12/18/2022]
Abstract
Obesity is increasing in an epidemic manner in most countries and constitutes a public health problem by enhancing the risk for diseases such as diabetes, fatty liver disease and atherosclerosis. Together these diseases form a cluster referred to as the metabolic syndrome. Despite the negative health consequences associated with excess adipose tissue, very little is known about the origin and maintenance of white adipose tissue in man. In this review we discuss what is known about the turnover of adult human adipocytes and their precursors, as well as adipose tissue heterogeneity, plasticity and developmental origins. The focus of this review is human tissue, however in many cases human data are missing and are inferred from animal studies. As such, reference to animal studies are made where human data is not available. This article is part of a directed issue entitled: Regenerative Medicine: the challenge of translation.
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Affiliation(s)
- Mervi T Hyvönen
- Department of Cell and Molecular Biology, Karolinska Institute, Berzelius väg 35, Stockholm 171-77, Sweden
| | - Kirsty L Spalding
- Department of Cell and Molecular Biology, Karolinska Institute, Berzelius väg 35, Stockholm 171-77, Sweden.
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Talukdar Y, Rashkow J, Lalwani G, Kanakia S, Sitharaman B. The effects of graphene nanostructures on mesenchymal stem cells. Biomaterials 2014; 35:4863-4877. [PMID: 24674462 PMCID: PMC3995421 DOI: 10.1016/j.biomaterials.2014.02.054] [Citation(s) in RCA: 133] [Impact Index Per Article: 12.1] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/10/2014] [Accepted: 02/28/2014] [Indexed: 12/15/2022]
Abstract
We report the effects of two-dimensional graphene nanostructures; graphene nano-onions (GNOs), graphene oxide nanoribbons (GONRs), and graphene oxide nanoplatelets (GONPs) on viability, and differentiation of human mesenchymal stem cells (MSCs). Cytotoxicity of GNOs, GONRs, and GONPs dispersed in distearoyl-sn-glycero-3-phosphoethanolamine-N-[amino(polyethylene glycol)] (DSPE-PEG), on adipose derived mesenchymal stem cells (adMSCs), and bone marrow-derived mesenchymal stem cells (bmMSCs) was assessed by AlamarBlue and Calcein AM viability assays at concentrations ranging from 5 to 300 μg/ml for 24 or 72 h. Cytotoxicity of the 2D graphene nanostructures was found to be dose dependent, not time dependent, with concentrations less than 50 μg/ml showing no significant differences compared to untreated controls. Differentiation potential of adMSCs to adipocytes and osteoblasts, - characterized by Oil Red O staining and elution, alkaline phosphatase activity, calcium matrix deposition and Alizarin Red S staining - did not change significantly when treated with the three graphene nanoparticles at a low (10 μg/ml) and high (50 μg/ml) concentration for 24 h. Transmission electron microscopy (TEM) and confocal Raman spectroscopy indicated cellular uptake of only GNOs and GONPs. The results lay the foundation for the use of these nanoparticles at potentially safe doses as ex vivo labels for MSC-based imaging and therapy.
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Affiliation(s)
- Yahfi Talukdar
- Department of Biomedical Engineering, Stony Brook University, Stony Brook, NY 11794-5281
| | - Jason Rashkow
- Department of Biomedical Engineering, Stony Brook University, Stony Brook, NY 11794-5281
| | - Gaurav Lalwani
- Department of Biomedical Engineering, Stony Brook University, Stony Brook, NY 11794-5281
| | - Shruti Kanakia
- Department of Biomedical Engineering, Stony Brook University, Stony Brook, NY 11794-5281
| | - Balaji Sitharaman
- Department of Biomedical Engineering, Stony Brook University, Stony Brook, NY 11794-5281
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Isolation, characterization, differentiation, and application of adipose-derived stem cells. ADVANCES IN BIOCHEMICAL ENGINEERING/BIOTECHNOLOGY 2014; 123:55-105. [PMID: 20091288 DOI: 10.1007/10_2009_24] [Citation(s) in RCA: 47] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [Subscribe] [Scholar Register] [Indexed: 12/12/2022]
Abstract
While bone marrow-derived mesenchymal stem cells are known and have been investigated for a long time, mesenchymal stem cells derived from the adipose tissue were identified as such by Zuk et al. in 2001. However, as subcutaneous fat tissue is a rich source which is much more easily accessible than bone marrow and thus can be reached by less invasive procedures, adipose-derived stem cells have moved into the research spotlight over the last 8 years.Isolation of stromal cell fractions involves centrifugation, digestion, and filtration, resulting in an adherent cell population containing mesenchymal stem cells; these can be subdivided by cell sorting and cultured under common conditions.They seem to have comparable properties to bone marrow-derived mesenchymal stem cells in their differentiation abilities as well as a favorable angiogenic and anti-inflammatory cytokine secretion profile and therefore have become widely used in tissue engineering and clinical regenerative medicine.
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32
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Ge W, Liu Y, Chen T, Zhang X, Lv L, Jin C, Jiang Y, Shi L, Zhou Y. The epigenetic promotion of osteogenic differentiation of human adipose-derived stem cells by the genetic and chemical blockade of histone demethylase LSD1. Biomaterials 2014; 35:6015-25. [PMID: 24794925 DOI: 10.1016/j.biomaterials.2014.04.055] [Citation(s) in RCA: 58] [Impact Index Per Article: 5.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/03/2014] [Accepted: 04/12/2014] [Indexed: 12/23/2022]
Abstract
Human adipose-derived stem cells (hASCs) are a highly attractive source in bone tissue engineering. It has become increasingly clear that chromatin regulators play an important role in cell fate determination. However, how osteogenic differentiation of hASCs is controlled by epigenetic mechanisms is not fully understood. Here we use genetic tools and chemical inhibitors to modify the epigenetic program of hASCs and identify lysine-specific demethylase 1 (LSD1), a histone demethylase that specifically catalyzes demethylation of di- and mono- methyl histone H3 lysine 4 (H3K4me2/1), as a key regulator in osteogenic differentiation of hASCs. Specifically, we demonstrated that genetic depletion of LSD1 with lentiviral strategy for gene knockdown promoted osteogenic differentiation of hASCs by cell studies and xenograft assays. At the molecular level, we found that LSD1 regulates osteogenesis-associated genes expression through its histone demethylase activity. Significantly, we demonstrated LSD1 demethylase inhibitors could efficiently block its catalytic activity and epigenetically boost osteogenic differentiation of hASCs. Altogether, our study defined the functional and biological roles of LSD1 and extensively explored the effects of its enzymatic activity in osteogenic differentiation of hASCs. A better understanding of how LSD1 influences on osteogenesis associated epigenetic events will provide new insights into the modulation of hASCs based cell therapy and improve the development of bone tissue engineering with epigenetic intervention.
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Affiliation(s)
- Wenshu Ge
- Department of General Dentistry II, Peking University School and Hospital of Stomatology, Beijing 100081, China; Department of Prosthodontics, Peking University School and Hospital of Stomatology, Beijing 100081, China
| | - Yunsong Liu
- Department of Prosthodontics, Peking University School and Hospital of Stomatology, Beijing 100081, China
| | - Tong Chen
- Department of Prosthodontics, Peking University School and Hospital of Stomatology, Beijing 100081, China
| | - Xiao Zhang
- Department of Prosthodontics, Peking University School and Hospital of Stomatology, Beijing 100081, China
| | - Longwei Lv
- Department of Prosthodontics, Peking University School and Hospital of Stomatology, Beijing 100081, China
| | - Chanyuan Jin
- Department of Prosthodontics, Peking University School and Hospital of Stomatology, Beijing 100081, China
| | - Yong Jiang
- Department of General Dentistry II, Peking University School and Hospital of Stomatology, Beijing 100081, China
| | - Lei Shi
- Tianjin Key Laboratory of Medical Epigenetics, Department of Biochemistry and Molecular Biology, Tianjin Medical University, Tianjin 300070, China.
| | - Yongsheng Zhou
- Department of Prosthodontics, Peking University School and Hospital of Stomatology, Beijing 100081, China; National Engineering Laboratory for Digital and Material Technology of Stomatology, Peking University School and Hospital of Stomatology, Beijing 100081, China.
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Pallua N, Serin M, Wolter TP. Characterisation of angiogenetic growth factor production in adipose tissue-derived mesenchymal cells. J Plast Surg Hand Surg 2014; 48:412-6. [DOI: 10.3109/2000656x.2014.903196] [Citation(s) in RCA: 22] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/13/2022]
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Kim EH, Heo CY. Current applications of adipose-derived stem cells and their future perspectives. World J Stem Cells 2014; 6:65-68. [PMID: 24567789 PMCID: PMC3927015 DOI: 10.4252/wjsc.v6.i1.65] [Citation(s) in RCA: 57] [Impact Index Per Article: 5.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/28/2013] [Revised: 10/25/2013] [Accepted: 12/13/2013] [Indexed: 02/06/2023] Open
Abstract
Adult stem cells have a great potential to treat various diseases. For these cell-based therapies, adipose-derived stem cells (ADSCs) are one of the most promising stem cell types, including embryonic stem cells (ESCs) and induced pluripotent stem cells (iPSCs). ESCs and iPSCs have taken center stage due to their pluripotency. However, ESCs and iPSCs have limitations in ethical issues and in identification of characteristics, respectively. Unlike ESCs and iPSCs, ADSCs do not have such limitations and are not only easily obtained but also uniquely expandable. ADSCs can differentiate into adipocytes, osteoblasts, chondrocytes, myocytes and neurons under specific differentiation conditions, and these kinds of differentiation potential of ADSCs could be applied in regenerative medicine e.g., skin reconstruction, bone and cartilage formation, etc. In this review, the current status of ADSC isolation, differentiation and their therapeutic applications are discussed.
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Abstract
Obesity, defined as an excessive increase in white adipose tissue (WAT), is a global health epidemic. In obesity, WAT expands by increased adipocyte size (hypertrophy) and number (hyperplasia). The location and cellular mechanisms of WAT expansion greatly affect the pathogenesis of obesity. However, the cellular and molecular mechanisms regulating adipocyte size, number, and depot-dependent expansion in vivo remain largely unknown. This perspective summarizes previous work addressing adipocyte number in development and obesity and discusses recent advances in the methodologies, genetic tools, and characterization of in vivo adipocyte precursor cells allowing for directed study of hyperplastic WAT growth in vivo.
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Affiliation(s)
- Ryan Berry
- Department of Molecular, Cell and Developmental Biology, Yale University School of Medicine, New Haven, CT 06520, USA
| | - Elise Jeffery
- Department of Cell Biology, Yale University School of Medicine, New Haven, CT 06520, USA
| | - Matthew S Rodeheffer
- Department of Molecular, Cell and Developmental Biology, Yale University School of Medicine, New Haven, CT 06520, USA; Section of Comparative Medicine, Yale University School of Medicine, New Haven, CT 06520, USA; Yale Stem Cell Center, Yale University, New Haven, CT 06520, USA.
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36
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Li AI, Hokugo A, Jarrahy R, Zuk PA. Human Adipose Tissue as a Source of Multipotent Stem Cells. STEM CELLS IN AESTHETIC PROCEDURES 2014:67-83. [DOI: 10.1007/978-3-642-45207-9_5] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/05/2025]
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37
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Wu I, Elisseeff J. Biomaterials and Tissue Engineering for Soft Tissue Reconstruction. NATURAL AND SYNTHETIC BIOMEDICAL POLYMERS 2014:235-241. [DOI: 10.1016/b978-0-12-396983-5.00015-6] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/05/2025]
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Li J, Qiao X, Yu M, Li F, Wang H, Guo W, Tian W. Secretory Factors From Rat Adipose Tissue Explants Promote Adipogenesis and Angiogenesis. Artif Organs 2013; 38:E33-45. [PMID: 24020992 DOI: 10.1111/aor.12162] [Citation(s) in RCA: 23] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/18/2022]
Affiliation(s)
- Jie Li
- College of Life Science; Sichuan University; Chengdu China
- National Engineering Laboratory for Oral Regenerative Medicine; Sichuan University; Chengdu China
- State Key Laboratory of Oral Diseases; Sichuan University; Chengdu China
| | - Xiangchen Qiao
- National Engineering Laboratory for Oral Regenerative Medicine; Sichuan University; Chengdu China
- State Key Laboratory of Oral Diseases; Sichuan University; Chengdu China
| | - Mei Yu
- National Engineering Laboratory for Oral Regenerative Medicine; Sichuan University; Chengdu China
- State Key Laboratory of Oral Diseases; Sichuan University; Chengdu China
| | - Feng Li
- National Engineering Laboratory for Oral Regenerative Medicine; Sichuan University; Chengdu China
- State Key Laboratory of Oral Diseases; Sichuan University; Chengdu China
- Department of Oral and Maxillofacial Surgery; West China School of Stomatology; Sichuan University; Chengdu China
| | - Hang Wang
- National Engineering Laboratory for Oral Regenerative Medicine; Sichuan University; Chengdu China
- State Key Laboratory of Oral Diseases; Sichuan University; Chengdu China
- Department of Oral and Maxillofacial Surgery; West China School of Stomatology; Sichuan University; Chengdu China
| | - Weihua Guo
- National Engineering Laboratory for Oral Regenerative Medicine; Sichuan University; Chengdu China
- State Key Laboratory of Oral Diseases; Sichuan University; Chengdu China
- Department of Pedodontics; West China School of Stomatology; Sichuan University; Chengdu China
| | - Weidong Tian
- National Engineering Laboratory for Oral Regenerative Medicine; Sichuan University; Chengdu China
- State Key Laboratory of Oral Diseases; Sichuan University; Chengdu China
- Department of Oral and Maxillofacial Surgery; West China School of Stomatology; Sichuan University; Chengdu China
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39
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Noguchi M, Hosoda K, Nakane M, Mori E, Nakao K, Taura D, Yamamoto Y, Kusakabe T, Sone M, Sakurai H, Fujikura J, Ebihara K, Nakao K. In vitro characterization and engraftment of adipocytes derived from human induced pluripotent stem cells and embryonic stem cells. Stem Cells Dev 2013; 22:2895-905. [PMID: 23750558 DOI: 10.1089/scd.2013.0113] [Citation(s) in RCA: 24] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/22/2022] Open
Abstract
Human induced pluripotent stem (iPS) and embryonic stem (ES) cells can differentiate into a variety of cell types. We reported on adipogenic potential of human iPS and ES cells in vitro. In the present study, we investigate the survival and maintenance of adipocytes differentiated in vitro from human iPS and ES cells after transplantation. Following adipogenic induction in vitro, the differentiated cells exhibited functional properties of adipocytes such as lipid storage, lipolysis, and insulin responsiveness. Subsequently, Matrigel containing the differentiated human iPS and ES cells was transplanted into the subcutaneous tissue of nude mice. After 1-4 weeks, the cells with adipocyte-like features were observed in transplanted Matrigel by histological analysis. The human origin of the cells, their lipid accumulation, and gene expression of adipocyte markers in transplanted cells were then confirmed, suggesting the presence of adipocytes in transplanted Matrigel. When the relative areas of these cells were calculated by dividing the adipocyte areas by the total Matrigel areas, we found that they peaked at 2 weeks after transplantation, and that the adipocytes persisted at 4 weeks. The present study demonstrates that human iPS and ES cells can differentiate into adipocytes with functional properties and that adipocytes derived from human iPS and ES cells can survive and maintain the differentiated properties of adipocytes for at least 4 weeks after transplantation. Adipocytes derived from human iPS and ES cells thus have the potential to open new avenues for stem cell-based research into metabolic diseases and future therapeutic applications.
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Affiliation(s)
- Michio Noguchi
- 1 Department of Medicine and Clinical Science, Kyoto University Graduate School of Medicine, Kyoto University , Kyoto, Japan
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Abstract
In 2001, researchers at the University of California, Los Angeles, described the isolation of a new population of adult stem cells from liposuctioned adipose tissue. These stem cells, now known as adipose-derived stem cells or ADSCs, have gone on to become one of the most popular adult stem cells populations in the fields of stem cell research and regenerative medicine. As of today, thousands of research and clinical articles have been published using ASCs, describing their possible pluripotency in vitro, their uses in regenerative animal models, and their application to the clinic. This paper outlines the progress made in the ASC field since their initial description in 2001, describing their mesodermal, ectodermal, and endodermal potentials both in vitro and in vivo, their use in mediating inflammation and vascularization during tissue regeneration, and their potential for reprogramming into induced pluripotent cells.
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41
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Daquinag AC, Souza GR, Kolonin MG. Adipose tissue engineering in three-dimensional levitation tissue culture system based on magnetic nanoparticles. Tissue Eng Part C Methods 2012; 19:336-44. [PMID: 23017116 DOI: 10.1089/ten.tec.2012.0198] [Citation(s) in RCA: 132] [Impact Index Per Article: 10.2] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/11/2022] Open
Abstract
White adipose tissue (WAT) is becoming widely used in regenerative medicine/cell therapy applications, and its physiological and pathological importance is increasingly appreciated. WAT is a complex organ composed of differentiated adipocytes, stromal mesenchymal progenitors known as adipose stromal cells (ASC), as well as endothelial vascular cells and infiltrating leukocytes. Two-dimensional (2D) culture that has been typically used for studying adipose cells does not adequately recapitulate WAT complexity. Improved methods for reconstruction of functional WAT ex vivo are instrumental for understanding of physiological interactions between the composing cell populations. Here, we used a three-dimensional (3D) levitation tissue culture system based on magnetic nanoparticle assembly to model WAT development and growth in organoids termed adipospheres. We show that 3T3-L1 preadipocytes remain viable in spheroids for a long period of time, while in 2D culture, they lose adherence and die after reaching confluence. Upon adipogenesis induction in 3T3-L1 adipospheres, cells efficiently formed large lipid droplets typical of white adipocytes in vivo, while only smaller lipid droplet formation is achievable in 2D. Adiposphere-based coculture of 3T3-L1 preadipocytes with murine endothelial bEND.3 cells led to a vascular-like network assembly concomitantly with lipogenesis in perivascular cells. Adipocyte-depleted stromal vascular fraction (SVF) of mouse WAT cultured in 3D underwent assembly into organoids with vascular-like structures containing luminal endothelial and perivascular stromal cell layers. Adipospheres made from primary WAT cells displayed robust proliferation and complex hierarchical organization reflected by a matricellular gradient incorporating ASC, endothelial cells, and leukocytes, while ASC quickly outgrew other cell types in adherent culture. Upon adipogenesis induction, adipospheres derived from the SVF displayed more efficient lipid droplet accumulation than 2D cultures. This indicates that 3D intercellular signaling better recapitulates WAT organogenesis. Combined, our studies show that adipospheres are appropriate for WAT modeling ex vivo and provide a new platform for functional screens to identify molecules bioactive toward individual adipose cell populations. This 3D methodology could be adopted for WAT transplantation applications and aid approaches to WAT-based cell therapy.
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Affiliation(s)
- Alexes C Daquinag
- Center for Stem Cell and Regenerative Medicine, The Brown Foundation Institute of Molecular Medicine for the Prevention of Human Diseases, The University of Texas Health Science Center at Houston, Houston, TX 77030, USA
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42
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Isolation, expansion, and differentiation of goat adipose-derived stem cells. Res Vet Sci 2012; 93:404-11. [DOI: 10.1016/j.rvsc.2011.08.014] [Citation(s) in RCA: 44] [Impact Index Per Article: 3.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/22/2011] [Revised: 08/01/2011] [Accepted: 08/08/2011] [Indexed: 11/18/2022]
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Cerwinka WH, Sharp SM, Boyan BD, Zhau HE, Chung LWK, Yates C. Differentiation of human mesenchymal stem cell spheroids under microgravity conditions. CELL REGENERATION 2012; 1:2. [PMID: 25408865 DOI: 10.1186/2045-9769-1-2] [Citation(s) in RCA: 24] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 06/20/2011] [Accepted: 06/28/2012] [Indexed: 01/14/2023]
Abstract
To develop and characterize a novel cell culture method for the generation of undifferentiated and differentiated human mesenchymal stem cell 3D structures, we utilized the RWV system with a gelatin-based scaffold. 3 × 10(6) cells generated homogeneous spheroids and maximum spheroid loading was accomplished after 3 days of culture. Spheroids cultured in undifferentiated spheroids of 3 and 10 days retained expression of CD44, without expression of differentiation markers. Spheroids cultured in adipogenic and osteogenic differentiation media exhibited oil red O staining and von Kossa staining, respectively. Further characterization of osteogenic lineage, showed that 10 day spheroids exhibited stronger calcification than any other experimental group corresponding with significant expression of vitamin D receptor, alkaline phosphatase, and ERp60 . In conclusion this study describes a novel RWV culture method that allowed efficacious engineering of undifferentiated human mesenchymal stem cell spheroids and rapid osteogenic differentiation. The use of gelatin scaffolds holds promise to design implantable stem cell tissue of various sizes and shapes for future regenerative treatment.
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Affiliation(s)
- Wolfgang H Cerwinka
- Children's Healthcare of Atlanta, Emory University School of Medicine, 5445Meridian Mark Road, Suite 420, Atlanta, GA 30342 USA ; Georgia Pediatric Urology, 5445 Meridian Mark Rd, Suite 420, Atlanta, GA 30342 USA
| | - Starlette M Sharp
- Department of Biology and Center for Cancer Research, Tuskegee University, Tuskegee Institute, Carver Research Building, kragujevac, AL 36088 USA
| | - Barbara D Boyan
- The Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology, 313 Ferst Drive Atlanta, Atlanta, GA 30332 USA
| | - Haiyen E Zhau
- Samuel-Oschin Comprehensive Cancer Institute, Cedars -Sinai Medical Center, 8750 Beverly Blvd., Atrium 103, Los Angeles, CA 90048 USA
| | - Leland W K Chung
- Samuel-Oschin Comprehensive Cancer Institute, Cedars -Sinai Medical Center, 8750 Beverly Blvd., Atrium 103, Los Angeles, CA 90048 USA
| | - Clayton Yates
- Department of Biology and Center for Cancer Research, Tuskegee University, Tuskegee Institute, Carver Research Building, kragujevac, AL 36088 USA ; Tuskegee University, Carver Research Bld. Rm 22, Tuskegee, AL 36088 USA
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44
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Human adipose-derived stem cells for the treatment of intracerebral hemorrhage in rats via femoral intravenous injection. Cell Mol Biol Lett 2012; 17:376-92. [PMID: 22544763 PMCID: PMC6275678 DOI: 10.2478/s11658-012-0016-5] [Citation(s) in RCA: 31] [Impact Index Per Article: 2.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/27/2011] [Accepted: 04/18/2012] [Indexed: 12/16/2022] Open
Abstract
Human adipose-derived stem cells (huADSC) were generated from fat tissue of a 65-year-old male donor. Flow cytometry and reverse transcription polymerase chain reaction (RT-PCR) analyses indicated that the huADSC express neural cell proteins (MAP2, GFAP, nestin and β-III tubulin), neurotrophic growth factors (BDNF and GDNF), and the chemotactic factor CXCR4 and its corresponding ligand CXCL12. In addition, huADSC expressed the characteristic mesenchymal stem cell (MSC) markers CD29, CD44, CD73, CD90, CD105 and HLA class I. The huADSC were employed, via a right femoral vein injection, to treat rats inflicted with experimental intracerebral hemorrhage (ICH). Behavioral measurement on the experimental animals, seven days after the huADSC therapy, showed a significant functional improvement in the rats with stem cell therapy in comparison with rats of the control group without the stem cell therapy. The injected huADSC were detectable in the brains of the huADSC treated rats as determined by histochemistry analysis, suggesting a role of the infused huADSC in facilitating functional recovery of the experimental animals with ICH induced stroke.
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45
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Sart S, Errachid A, Schneider YJ, Agathos SN. Modulation of mesenchymal stem cell actin organization on conventional microcarriers for proliferation and differentiation in stirred bioreactors. J Tissue Eng Regen Med 2012; 7:537-51. [DOI: 10.1002/term.545] [Citation(s) in RCA: 39] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/11/2011] [Revised: 08/31/2011] [Accepted: 11/14/2011] [Indexed: 12/28/2022]
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Venugopal B, Fernandez FB, Babu SS, Harikrishnan VS, Varma H, John A. Adipogenesis on biphasic calcium phosphate using rat adipose-derived mesenchymal stem cells: in vitro and in vivo. J Biomed Mater Res A 2012; 100:1427-37. [PMID: 22374846 DOI: 10.1002/jbm.a.34082] [Citation(s) in RCA: 10] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/25/2011] [Revised: 12/14/2011] [Accepted: 01/10/2012] [Indexed: 12/25/2022]
Abstract
Developing adipose tissue-engineered construct to mend soft tissue defects arising from traumatic injury, tumor resections, and maxillofacial abnormalities is of prime importance in plastic and reconstructive surgical procedures. It is apparent that the clinical outcome of classic techniques like adipose tissue transplantation is unpredictable, with graft resorption, lack of vascularization, and impaired functionality. In this prospective, the concept of tissue engineering was adopted to fabricate a combination product with biphasic calcium phosphate (BCP) and rat adipose-derived mesenchymal stem cells (ASCs) toward the development of an adipose tissue construct. BCP, a combination of hydroxyapatite and α-tricalcium phosphate, was characterized for its physiochemical properties, and ASCs were characterized for their stemness. The cell-ceramic interactions were demonstrated in vitro, whereas adipogenesis was picturesquely depicted by Nile red-stained multilocular adipocyte-like cells. Subsequently, the three-dimensional cell-ceramic-engineered construct was implanted in the rat dorsal muscle for a period of 3 weeks to demonstrate the efficacy of the tissue construct in vivo. Interestingly, the histology of the postimplanted tissue construct revealed the distribution of chicken wire net-like fat cells within the vicinity of the construct. The efficacy of cell transplantation via the scaffold was traced using fluorescent in situ hybridization by labeling the Y chromosome. Thus, the ceramic-based construct may be a good option for reconstruction therapies.
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Affiliation(s)
- Balu Venugopal
- Division of Implant Biology (TEM Laboratory), Biomedical Technology Wing, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Trivandrum 695012, Kerala, India
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Choi JH, Gimble JM, Lee K, Marra KG, Rubin JP, Yoo JJ, Vunjak-Novakovic G, Kaplan DL. Adipose tissue engineering for soft tissue regeneration. TISSUE ENGINEERING PART B-REVIEWS 2011; 16:413-26. [PMID: 20166810 DOI: 10.1089/ten.teb.2009.0544] [Citation(s) in RCA: 179] [Impact Index Per Article: 12.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/08/2023]
Abstract
Current treatment modalities for soft tissue defects caused by various pathologies and trauma include autologous grafting and commercially available fillers. However, these treatment methods present a number of challenges and limitations, such as donor-site morbidity and volume loss over time. As such, improved therapeutic modalities need to be developed. Tissue engineering techniques offer novel solutions to these problems through development of bioactive tissue constructs that can regenerate adipose tissue in both structure and function. Recently, a number of studies have been designed to explore various methods to engineer human adipose tissue. This review will focus on these developments in the area of adipose tissue engineering for soft tissue replacement. The physiology of adipose tissue and current surgical therapies used to replace lost tissue volume, specifically in breast tissue, are introduced, and current biomaterials, cell sources, and tissue culture strategies are discussed. We discuss future areas of study in adipose tissue engineering.
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Affiliation(s)
- Jennifer H Choi
- Department of Biomedical Engineering, Tufts University, Medford, Massachusetts 02155, USA
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Zhu Y, Liu T, Ye H, Song K, Ma X, Cui Z. Enhancement of adipose-derived stem cell differentiation in scaffolds with IGF-I gene impregnation under dynamic microenvironment. Stem Cells Dev 2011; 19:1547-56. [PMID: 20408758 DOI: 10.1089/scd.2010.0054] [Citation(s) in RCA: 19] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/20/2022] Open
Abstract
Biochemical and mechanical signals enabling cardiac regeneration can be elucidated by using in vitro tissue engineering models. We hypothesized that human insulin-like growth factor-I (IGF-I) and 3-dimensional (3D) dynamic microenvironment could enhance the survival and differentiation of adipose tissue-derived stem cells (ADSCs). In this study, ADSCs were cultured on 3D porous scaffolds with or without plasmid DNA PIRES2-IGF-I in cardiac media, in static culture dishes, and in a spinning flask bioreactor, respectively. Cell viability, formation of cardiac-like structure, expression of functional proteins, and gene expressions were tested in the cultured constructs on day 14. The results showed that dynamic microenvironment enhanced the release of plasmid DNA; the ADSCs can be transfected by the released plasmid DNA PIRES2-IGF-I in scaffold. IGF-I showed beneficial effects on cellular viability and increase of total protein and also increased the expressions of cardiac-specific proteins and genes in the grafts. It was also demonstrated that dynamic stirring environment could promote the proliferation of ADSCs. Therefore, IGF-I, expressed by ADSCs transfected by DNA PIRES2-IGF-I incorporated into scaffold, and hydrodynamic microenvironment can independently and interactively increase cellular viability and interactively increase the expression of cardiac-specific proteins and genes in the grafts. The results would be useful for developing tissue-engineered grafts for myocardial repair.
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Affiliation(s)
- Yanxia Zhu
- Dalian R&D Center for Stem Cell and Tissue Engineering, Dalian University of Technology, Dalian, China
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Choi JH, Bellas E, Vunjak-Novakovic G, Kaplan DL. Adipogenic differentiation of human adipose-derived stem cells on 3D silk scaffolds. Methods Mol Biol 2011; 702:319-30. [PMID: 21082412 DOI: 10.1007/978-1-61737-960-4_23] [Citation(s) in RCA: 31] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/06/2023]
Abstract
Current treatment modalities for soft tissue defects due to various pathologies and trauma include autologous grafting and the use of commercially available fillers. However, these treatment methods are associated with a number of limitations, such as donor site morbidity and volume loss over time. As such, improved therapeutic options are needed. Tissue engineering techniques offer novel solutions to these problems through development of bioactive tissue constructs that can regenerate adipose tissue with an appropriate structure and function. The recent advances in the derivation and characterization of hASCs have led to numerous studies of soft tissue reconstruction. In this chapter, we discuss methods in which our laboratory has used hASCs and silk scaffolds for adipose tissue engineering. The use of naturally occurring and clinically acceptable materials such as silk protein for tissue-engineering applications poses advantages with respect to biocompatibility and mechanical and biological properties.
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