A hybrid construct of decellularized matrix and fibrin for differentiating adipose stem cells into insulin-producing cells, an optimized in vitro assessment.
decellularized extracellular matrix
diabetes
fibrin
insulin‐producing cells
tissue engineering
Journal
Cell biochemistry and function
ISSN: 1099-0844
Titre abrégé: Cell Biochem Funct
Pays: England
ID NLM: 8305874
Informations de publication
Date de publication:
Jun 2024
Jun 2024
Historique:
revised:
30
04
2024
received:
12
02
2024
accepted:
05
05
2024
medline:
13
5
2024
pubmed:
13
5
2024
entrez:
13
5
2024
Statut:
ppublish
Résumé
The generation of insulin-producing cells (IPCs) is an attractive approach for replacing damaged β cells in diabetic patients. In the present work, we introduced a hybrid platform of decellularized amniotic membrane (dAM) and fibrin encapsulation for differentiating adipose tissue-derived stem cells (ASCs) into IPCs. ASCs were isolated from healthy donors and characterized. Human AM was decellularized, and its morphology, DNA, collagen, glycosaminoglycan (GAG) contents, and biocompatibility were evaluated. ASCs were subjected to four IPC differentiation methods, and the most efficient method was selected for the experiment. ASCs were seeded onto dAM, alone or encapsulated in fibrin gel with various thrombin concentrations, and differentiated into IPCs according to a method applying serum-free media containing 2-mercaptoethanol, nicotinamide, and exendin-4. PDX-1, GLUT-2 and insulin expression were evaluated in differentiated cells using real-time PCR. Structural integrity and collagen and GAG contents of AM were preserved after decellularization, while DNA content was minimized. Cultivating ASCs on dAM augmented their attachment, proliferation, and viability and enhanced the expression of PDX-1, GLUT-2, and insulin in differentiated cells. Encapsulating ASCs in fibrin gel containing 2 mg/ml fibrinogen and 10 units/ml thrombin increased their differentiation into IPCs. dAM and fibrin gel synergistically enhanced the differentiation of ASCs into IPCs, which could be considered an appropriate strategy for replacing damaged β cells.
Substances chimiques
Fibrin
9001-31-4
Insulin
0
Decellularized Extracellular Matrix
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e4038Subventions
Organisme : Kermanshah University of Medical Sciences
ID : 4010001
Informations de copyright
© 2024 John Wiley & Sons Ltd.
Références
Sun H, Saeedi P, Karuranga S, et al. IDF diabetes atlas: global, regional and country‐level diabetes prevalence estimates for 2021 and projections for 2045. Diabetes Res Clin Pract. 2022;183:109119.
Pugliese A. Autoreactive T cells in type 1 diabetes. J Clin Invest. 2017;127(8):2881‐2891.
Silva IBB, Kimura CH, Colantoni VP, Sogayar MC. Stem cells differentiation into insulin‐producing cells (IPCs): recent advances and current challenges. Stem Cell Res Ther. 2022;13(1):309.
Hering BJ, Clarke WR, Bridges ND, et al. Phase 3 trial of transplantation of human islets in type 1 diabetes complicated by severe hypoglycemia. Diabetes Care. 2016;39(7):1230‐1240.
Leal‐Lopes C, Grazioli G, Mares‐Guia TR, Coelho‐Sampaio T, Sogayar MC. Polymerized laminin incorporation into alginate‐based microcapsules reduces pericapsular overgrowth and inflammation. J Tissue Eng Regener Med. 2019;13(10):1912‐1922.
Shapiro AMJ, Pokrywczynska M, Ricordi C. Clinical pancreatic islet transplantation. Nat Rev Endocrinol. 2017;13(5):268‐277.
Nemati M, Ranjbar Omrani G, Ebrahimi B, Alizadeh A. Efficiency of stem cell (SC) differentiation into insulin‐producing cells for treating diabetes: a systematic review. Stem Cells Int. 2021;2021:1‐9.
Zhang J, Chan HF, Wang H, Shao D, Tao Y, Li M. Stem cell therapy and tissue engineering strategies using cell aggregates and decellularized scaffolds for the rescue of liver failure. J Tissue Eng. 2021;12:204173142098671.
Hogrebe NJ, Maxwell KG, Augsornworawat P, Millman JR. Generation of insulin‐producing pancreatic β cells from multiple human stem cell lines. Nat Protoc. 2021;16(9):4109‐4143.
Xu B, Fan D, Zhao Y, et al. Three‐dimensional culture promotes the differentiation of human dental pulp mesenchymal stem cells into insulin‐producing cells for improving the diabetes therapy. Front Pharmacol. 2020;10:1576.
Bozorgi A, Khazaei M, Bozorgi M, Jamalpoor Z. Fabrication and characterization of apigenin‐loaded chitosan/gelatin membranes for bone tissue engineering applications. J Bioact Compat Polym. 2023;38(2):142‐157.
Hashemi J, Pasalar P, Soleimani M, et al. Decellularized pancreas matrix scaffolds for tissue engineering using ductal or arterial catheterization. Cells Tissues Organs. 2018;205(2):72‐84.
Bozorgi A, Bozorgi M, Khazaei M, Soleimani M. Decellularized extracellular matrices in bone tissue engineering: from cells to tissues. mini‐review. Cell and Tissue Biol. 2020;14(6):399‐406.
Leal‐Marin S, Kern T, Hofmann N, et al. Human amniotic membrane: a review on tissue engineering, application, and storage. J Biomed Mater Res Part B Appl Biomater. 2021;109(8):1198‐1215.
Mamede AC, Carvalho MJ, Abrantes AM, Laranjo M, Maia CJ, Botelho MF. Amniotic membrane: from structure and functions to clinical applications. Cell Tissue Res. 2012;349(2):447‐458.
Elkhenany H, El‐Derby A, Abd Elkodous M, Salah RA, Lotfy A, El‐Badri N. Applications of the amniotic membrane in tissue engineering and regeneration: the hundred‐year challenge. Stem Cell Res Ther. 2022;13(1):8.
Song J, Millman JR. Economic 3D‐printing approach for transplantation of human stem cell‐derived β‐like cells. Biofabrication. 2017;9(1):015002.
Li Y, Meng H, Liu Y, Lee BP. Fibrin gel as an injectable biodegradable scaffold and cell carrier for tissue engineering. ScientificWorldJournal. 2015;2015:1‐10.
Sabouri L, Farzin A, Kabiri A, et al. Mineralized human amniotic membrane as a biomimetic scaffold for hard tissue engineering applications. ACS Biomater Sci Eng. 2020;6(11):6285‐6298.
Nekoei SM, Azarpira N, Sadeghi L, Kamalifar S. In vitro differentiation of human umbilical cord Wharton's jelly mesenchymal stromal cells to insulin producing clusters. World J Clin Cases. 2015;3(7):640‐649.
Xin Y, Jiang X, Wang Y, et al. Insulin‐producing cells differentiated from human bone marrow mesenchymal stem cells in vitro ameliorate streptozotocin‐induced diabetic hyperglycemia. PLoS One. 2016;11(1):e0145838.
Xie Q‐P, Huang H, Xu B, et al. Human bone marrow mesenchymal stem cells differentiate into insulin‐producing cells upon microenvironmental manipulation in vitro. Differentiation. 2009;77(5):483‐491.
Kassem DH, Kamal MM, El‐Kholy AELG, El‐Mesallamy HO. Exendin‐4 enhances the differentiation of Wharton's jelly mesenchymal stem cells into insulin‐producing cells through activation of various β‐cell markers. Stem Cell Res Ther. 2016;7(1):108.
Hu Z, Luo Y, Ni R, et al. Biological importance of human amniotic membrane in tissue engineering and regenerative medicine. Materials Today Bio. 2023;22:100790.
Murphy SV, Skardal A, Song L, et al. Solubilized amnion membrane hyaluronic acid hydrogel accelerates full‐thickness wound healing. Stem Cells Transl Med. 2017;6(11):2020‐2032.
Villamil Ballesteros AC, Segura Puello HR, Lopez‐Garcia JA, et al. Bovine decellularized amniotic membrane: extracellular matrix as scaffold for mammalian skin. Polymers. 2020;12(3):590.
Guo X, Kaplunovsky A, Zaka R, et al. Modulation of cell attachment, proliferation, and angiogenesis by decellularized, dehydrated human amniotic membrane in in vitro models. Wounds. 2017;29(1):28‐38.
Haghshenas M, Tavana S, Zand E, Montazeri L, Fathi R. Mouse ovarian follicle growth in an amniotic membrane‐based hydrogel. J Biomater Appl. 2022;37(3):563‐574.
Li X, Li P, Wang C, et al. A thermo‐sensitive and injectable hydrogel derived from a decellularized amniotic membrane to prevent intrauterine adhesion by accelerating endometrium regeneration. Biomater Sci. 2022;10(9):2275‐2286.
Riau AK, Beuerman RW, Lim LS, Mehta JS. Preservation, sterilization and de‐epithelialization of human amniotic membrane for use in ocular surface reconstruction. Biomater. 2010;31(2):216‐225.
Hortensius RA, Ebens JH, Harley BAC. Immunomodulatory effects of amniotic membrane matrix incorporated into collagen scaffolds. J Biomed Mater Res A. 2016;104(6):1332‐1342.
Pittenger MF, Discher DE, Péault BM, Phinney DG, Hare JM, Caplan AI. Mesenchymal stem cell perspective: cell biology to clinical progress. NPJ Regen Med. 2019;4(1):22.
Pan G, Mu Y, Hou L, Liu J. Examining the therapeutic potential of various stem cell sources for differentiation into insulin‐producing cells to treat diabetes. Ann Endocrinol (Paris). 2019;80(1):47‐53.
Dayer D, Tabar MH, Moghimipour E, et al. Sonic hedgehog pathway suppression and reactivation accelerates differentiation of rat adipose‐derived mesenchymal stromal cells toward insulin‐producing cells. Cytotherapy. 2017;19(8):937‐946.
Chase LG, Lakshmipathy U, Solchaga LA, Rao MS, Vemuri MC. A novel serum‐free medium for the expansion of human mesenchymal stem cells. Stem Cell Res Ther. 2010;1(1):8.
Aydin S, Sağraç D, Şahin F. Differentiation potential of mesenchymal stem cells into pancreatic β‐Cells. Adv Exp Med Biol. 2020;1247:135‐156.
Al‐Khawaga S, Memon B, Butler AE, Taheri S, Abou‐Samra AB, Abdelalim EM. Pathways governing development of stem cell‐derived pancreatic β cells: lessons from embryogenesis. Biol Rev. 2018;93(1):364‐389.
Dhandapani V, Vermette P. Decellularized bladder as scaffold to support proliferation and functionality of insulin‐secreting pancreatic cells. J Biomed Mater Res Part B Appl Biomater. 2023;111(11):1890‐1902.
Weber LM, Hayda KN, Anseth KS. Cell–matrix interactions improve β‐Cell survival and insulin secretion in three‐dimensional culture. Tissue Eng Part A. 2008;14(12):1959‐1968.
Nikolova G, Jabs N, Konstantinova I, et al. The vascular basement membrane: a niche for insulin gene expression and β cell proliferation. Dev Cell. 2006;10(3):397‐405.
Seyedi F, Farsinejad A, Nematollahi‐Mahani SN. Fibrin scaffold enhances function of insulin producing cells differentiated from human umbilical cord matrix‐derived stem cells. Tissue Cell. 2017;49(2 Pt B):227‐232.
Chandrababu K, Senan M, Krishnan LK. Exploitation of fibrin‐based signaling niche for deriving progenitors from human adipose‐derived mesenchymal stem cells towards potential neural engineering applications. Sci Rep. 2020;10(1):7116.
Riopel M, Li J, Trinder M, Fellows GF, Wang R. Fibrin supports human fetal islet‐epithelial cell differentiation via p70s6k and promotes vascular formation during transplantation. Lab Invest. 2015;95(8):925‐936.
Risman RA, Belcher HA, Ramanujam RK, Weisel JW, Hudson NE, Tutwiler V. Comprehensive analysis of the role of fibrinogen and thrombin in clot formation and structure for plasma and purified fibrinogen. Biomolecules. 2024;14(2):230.
Nazari B, Kazemi M, Kamyab A, et al. Fibrin hydrogel as a scaffold for differentiation of induced pluripotent stem cells into oligodendrocytes. J Biomed Mater Res Part B Appl Biomater. 2020;108(1):192‐200.
Willerth SM, Arendas KJ, Gottlieb DI, Sakiyama‐Elbert SE. Optimization of fibrin scaffolds for differentiation of murine embryonic stem cells into neural lineage cells. Biomater. 2006;27(36):5990‐6003.
Chaires‐Rosas CP, Ambriz X, Montesinos JJ, et al. Differential adhesion and fibrinolytic activity of mesenchymal stem cells from human bone marrow, placenta, and Wharton's jelly cultured in a fibrin hydrogel. J Tissue Eng. 2019;10:204173141984062.
Makogonenko E, Tsurupa G, Ingham K, Medved L. Interaction of fibrin(ogen) with fibronectin: further characterization and localization of the fibronectin‐binding site. Biochemistry. 2002;41(25):7907‐7913.
Oh JH, Kim HJ, Kim TI, Baek JH, Ryoo HM, Woo KM. The effects of the modulation of the fibronectin‐binding capacity of fibrin by thrombin on osteoblast differentiation. Biomater. 2012;33(16):4089‐4099.