Extracellular matrix biomimetics for pancreatic tissue engineering
https://doi.org/10.15825/1995-1191-2025-3-146-159
Abstract
Isolated islet transplantation offers a safer and less invasive alternative to whole pancreas transplantation for patients with complicated type 1 diabetes mellitus. However, the procedure faces significant challenges, including the loss of vascularization, innervation, and extracellular matrix (ECM) support. Additionally, factors such as hypoxia, oxidative stress, inflammatory responses, and the cytotoxic effects of immunosuppressive therapy compromise islet viability significantly and limit long-term graft function. Tissue engineering and regenerative medicine strategies aim to address these challenges. A central objective is the development of biocompatible, biomimetic ECM scaffolds (frameworks, carriers, or matrices) that can provide both mechanical support and a suitable microenvironment for islet cells in vitro and in vivo. This review aims to systematize current data on the use of biomimetic ECMs in the creation of stable, tissue-engineered pancreatic constructs.
About the Authors
A. S. Ponomareva
Shumakov National Medical Research Center of Transplantology and Artificial Organs
Russian Federation
Russian Federation
Anna S. Ponomareva.
1, Shchukinskaya str., Moscow, 123182
Phone: (499) 196-26-61; (926) 585-23-73
N. V. Baranova
Shumakov National Medical Research Center of Transplantology and Artificial Organs
Russian Federation
Russian Federation
Moscow
Yu. B. Basok
Shumakov National Medical Research Center of Transplantology and Artificial Organs
Russian Federation
Russian Federation
Moscow
V. I. Sevastianov
Shumakov National Medical Research Center of Transplantology and Artificial Organs; Institute of Biomedical Research and Technology
Russian Federation
Russian Federation
Moscow
References
1. Dedov II, Shestakova MV, Mayorov AY, Shamkhalova MS, Nikonova TV, Sukhareva OY et al. Diabetes mellitus type 1 in adults. Diabetes mellitus. 2020; 23 (1S): 42–114. (In Russ.). doi: 10.14341/DM12505.
2. Norris JM, Johnson RK, Stene LC. Type 1 diabetes-early life origins and changing epidemiology. Lancet Diabetes Endocrinol. 2020; 8 (3): 226–238. doi: 10.1016/S2213-8587(19)30412-7.
3. Shapiro AM, Lakey JR, Ryan EA, Korbutt GS, Toth E, Warnock GL et al. Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N Engl J Med. 2000; 343 (4): 230–238. doi: 10.1056/NEJM200007273430401.
4. Piemonti L. In: Feingold KR, Anawalt B, Blackman MR, Boyce A, Chrousos G, Corpas E et al editors. Islet Transplantation. Endotext [Internet]. South Dartmouth (MA): MDText.com, Inc. 2022; 2000. PMID: 25905200.
5. Gruessner AC, Gruessner RWG. The 2022 International Pancreas Transplant Registry Report – A Review. Transplant Proc. 2022; 54 (7): 1918–1943. doi: 10.1016/j.transproceed.2022.03.059.
6. Lablanche S, Borot S, Wojtusciszyn A, Skaare K, Penfornis A, Malvezzi P et al. Ten-year outcomes of islet transplantation in patients with type 1 diabetes: Data from the Swiss-French GRAGIL network. Am J Transplant. 2021; 21 (11): 3725–3733. doi: 10.1111/ajt.16637.
7. Hering BJ, Ballou CM, Bellin MD, Payne EH, Kandeel F, Witkowski P et al. Factors associated with favourable 5 year outcomes in islet transplant alone recipients with type 1 diabetes complicated by severe hypoglycaemia in the Collaborative Islet Transplant Registry. Diabetologia. 2023; 66: 163–173. doi: 10.1007/s00125-022-05804-4.
8. Reid L, Baxter F, Forbes S. Effects of islet transplantation on microvascular and macrovascular complications in type 1 diabetes. Diabet Med. 2021; 38 (7): e14570. doi: 10.1111/dme.14570.
9. Langlois A, Pinget M, Kessler L, Bouzakri K. Islet Transplantation: Current Limitations and Challenges for Successful Outcomes. Cells. 2024; 13 (21): 1783. doi: 10.3390/cells13211783.
10. Olaniru OE, Persaud SJ. Identifying novel therapeutic targets for diabetes through improved understanding of islet adhesion receptors. Curr Opin Pharmacol. 2018; 43: 27–33. doi: 10.1016/j.coph.2018.07.009.
11. Kahraman S, Okawa ER, Kulkarni RN. Is Transforming Stem Cells to Pancreatic Beta Cells Still the Holy Grail for Type 2 Diabetes? Curr Diab Rep. 2016; 16 (8): 70. doi: 10.1007/s11892-016-0764-0.
12. Abadpour S, Wang C, Niemi EM, Scholz H. Tissue Engineering Strategies for Improving Beta Cell Transplantation Outcome. Curr Transpl Rep. 2021; 8: 205–219. doi: 10.1007/s40472-021-00333-2.
13. Sevastianov VI, Basok YuB et al. Biomimetics of Extracellular Matrices for Cell and Tissue Engineered Medical Products. Eds. Victor I. Sevastianov and Yulia B. Basok. Newcastle upon Tyne, UK: Cambridge Scholars Publishing; 2023: 339.
14. Zhang Q, Gonelle-Gispert C, Li Y, Geng Z, Gerber-Lemaire S, Wang Y et al. Islet Encapsulation: New Developments for the Treatment of Type 1 Diabetes. Front Immunol. 2022; 13: 869984. doi: 10.3389/fimmu.2022.869984.
15. Salg GA, Giese NA, Schenk M, Hüttner FJ, Felix K, Probst P et al. The emerging field of pancreatic tissue engineering: A systematic review and evidence map of scaffold materials and scaffolding techniques for insulin-secreting cells. J Tissue Eng. 2019; 10: 2041731419884708. doi: 10.1177/2041731419884708.
16. Ho BX, Teo AKK, Ng NHJ. Innovations in bio-engineering and cell-based approaches to address immunological challenges in islet transplantation. Front Immunol. 2024; 15: 1375177. doi: 10.3389/fimmu.2024.1375177.
17. Basok YuB., Ponomareva AS, Grudinin NV, Kruglov DN, Bogdanov VK, Belova AD, Sevastyanov VI. Application of mesenchymal stromal cells in solid organ transplantation: challenges and prospects (systematic review). Russian Journal of Transplantology and Artificial Organs. 2025; 27 (1): 114–134.
18. Amer LD, Mahoney MJ, Bryant SJ. Tissue engineering approaches to cell-based type 1 diabetes therapy. Tissue Eng Part B Rev. 2014; 20 (5): 455–467. doi: 10.1089/ten.TEB.2013.0462.
19. Santos da Silva T, Silva-Júnior LND, Horvath-Pereira BO, Valbão MCM, Garcia MHH, Lopes JB et al. The Role of the Pancreatic Extracellular Matrix as a Tissue Engineering Support for the Bioartificial Pancreas. Biomimetics (Basel). 2024; 9 (10): 598. doi: 10.3390/biomimetics9100598.
20. Sojoodi M, Farrokhi A, Moradmand A, Baharvand H. Enhanced maintenance of rat islets of Langerhans on laminin-coated electrospun nanofibrillar matrix in vitro. Cell Biol Int. 2013; 37 (4): 370–379. doi: 10.1002/cbin.10045.
21. Sigmundsson K, Ojala JRM, Öhman MK, Österholm AM, Moreno-Moral A, Domogatskaya A et al. Culturing functional pancreatic islets on α5-laminins and curative transplantation to diabetic mice. Matrix Biol. 2018; 70: 5–19. doi: 10.1016/j.matbio.2018.03.018.
22. Fernández-Montes RD, Blasi J, Busquets J, Montanya E, Nacher M. Fibronectin enhances soluble N-ethylmaleimide-sensitive factor attachment protein receptor protein expression in cultured human islets. Pancreas. 2011; 40 (7): 1153–1155. doi: 10.1097/MPA.0b013e318222bcaf.
23. Llacua LA, Hoek A, de Haan BJ, de Vos P. Collagen type VI interaction improves human islet survival in immunoisolating microcapsules for treatment of diabetes. Islets. 2018; 10 (2): 60–68. doi: 10.1080/19382014.2017.1420449.
24. Surguchenko VA, Ponomareva АS, Efimov АE, Nemets ЕA, Agapov II, Sevastianov VI. Characteristics of adhesion and proliferation of mouse nih/3t3 fibroblasts on the poly(3-hydroxybutyrate-co-3-hydroxyvalerate) films with different surface roughness values. Russian Journal of Transplantology and Artificial Organs. 2012; 14 (1): 72–77. (In Russ.). doi: 10.15825/1995-1191-2012-1-72-77.
25. Mehdi Ebrahimi. Porosity parameters in biomaterial science: Definition, impact, and challenges in tissue engineering. Front Mater Sci. 2021; 15 (3): 352‒373. doi: 10.1007/s11706-021-0558-4.
26. Sevastyanov VI, Kirpichnikov MP. Biosovmestimye materialy. М.: MIA, 2011; 544.
27. Johnson AS, O’Sullivan E, D’Aoust LN, Omer A, Bonner-Weir S, Fisher RJ et al. Quantitative assessment of islets of Langerhans encapsulated in alginate. Tissue Eng Part C Methods. 2011; 17 (4): 435–449. doi: 10.1089/ten.TEC.2009.0510.
28. Formo K, Cho CH, Vallier L, Strand BL. Culture of hESC-derived pancreatic progenitors in alginate-based scaffolds. J Biomed Mater Res A. 2015; 103 (12): 3717–3726. doi: 0.1002/jbm.a.35507.
29. Köllmer M, Appel AA, Somo SI, Brey EM. Long-term function of alginate-encapsulated islets. Tissue Eng Part B Rev. 2015; 22: 34–46. doi: 10.1089/ten.TEB.2015.0140.
30. Li N, Sun G, Wang S, Wang Y, Xiu Z, Sun D et al. Engineering islet for improved performance by optimized reaggregation in alginate gel beads. Biotechnol Appl Biochem. 2017; 64 (3): 400–405. doi: 10.1002/bab.1489.
31. Noverraz F, Montanari E, Pimenta J, Szabó L, Ortiz D, Gonelle-Gispert C et al. Antifibrotic effect of ketoprofen-grafted alginate microcapsules in the transplantation of insulin producing cells. Bioconjug Chem. 2018; 29 (6): 1932–1941. doi: 10.1021/acs.bioconjchem.8b00190.
32. Espona-Noguera A, Ciriza J, Cañibano-Hernández A, Fernandez L, Ochoa I, Saenz Del Burgo L et al. Tunable injectable alginate-based hydrogel for cell therapy in Type 1 Diabetes Mellitus. Int J Biol Macromol. 2018; 107 (Pt A): 1261–1269. doi: 10.1016/j.ijbiomac.2017.09.103.
33. Kawazoe N, Lin XT, Tateishi T, Chen G. Three-dimensional cultures of rat pancreatic RIN-5F cells in porous PLGA-collagen hybrid scaffolds. J Bioact Compat Pol. 2009; 24: 25–42. doi: 10.1177/0883911508099439.
34. Jalili RB, Moeen Rezakhanlou A, Hosseini-Tabatabaei A, Ao Z, Warnock GL, Ghahary A. Fibroblast populated collagen matrix promotes islet survival and reduces the number of islets required for diabetes reversal. J Cell Physiol. 2011; 226 (7): 1813–1819. doi: 10.1002/jcp.22515.
35. Deng C, Vulesevic B, Ellis C, Korbutt GS, Suuronen EJ. Vascularization of collagen-chitosan scaffolds with circulating progenitor cells as potential site for islet transplantation. J Control Release. 2011; 152 (Suppl 1): e196–e198. doi: 10.1016/j.jconrel.2011.09.005.
36. Yap WT, Salvay DM, Silliman MA, Zhang X, Bannon ZG, Kaufman DB et al. Collagen IV-modified scaffolds improve islet survival and function and reduce time to euglycemia. Tissue Eng Part A. 2013; 19 (21–22): 2361–2372. doi: 10.1089/ten.TEA.2013.0033.
37. Riopel M, Wang К. Collagen matrix support of pancreatic islet survival and function. Front Biosci (Landmark Ed). 2014; 19 (1): 77–90. doi: 10.2741/4196.
38. McEwan K, Padavan DT, Ellis C, McBane JE, Vulesevic B, Korbutt GS et al. Collagen-chitosan-laminin hydrogels for the delivery of insulin-producing tissue. J Tissue Eng Regen Med. 2016; 10 (10): E397–E408. doi: 10.1002/term.1829.
39. Szebeni GJ, Tancos Z, Feher LZ, Alfoldi R, Kobolak J, Dinnyes A et al. Real architecture for 3D Tissue (RAFT) culture system improves viability and maintains insulin and glucagon production of mouse pancreatic islet cells. Cytotechnology. 2017; 69 (2): 359–369. doi: 10.1007/s10616-017-0067-6.
40. Vlahos AE, Cober N, Sefton MV. Modular tissue engineering for the vascularization of subcutaneously transplanted pancreatic islets. Proc Natl Acad Sci USA. 2017; 114 (35): 9337–9342. doi: 10.1073/pnas.1619216114.
41. Montalbano G, Toumpaniari S, Popov A, Duan P, Chen J, Dalgarno K et al. Synthesis of bioinspired collagen/alginate/fibrin based hydrogels for soft tissue engineering. Mater Sci Eng C Mater Biol Appl. 2018; 91: 236–246. doi: 10.1016/j.msec.2018.04.101.
42. Baranova NV, Kirsanova LA, Ponomareva AS, Nemets EA, Basok YB, Bubentsova GN et al. Comparative analysis of the secretory capacity of islets of langerhans cultured with biopolymer-based collagen-containing hydrogel and tissue-specific matrix. Russian Journal of Transplantology and Artificial Organs. 2019; 21 (4): 45–53. doi: 10.15825/1995-1191-2019-4-45-53.
43. Yang KC, Wu CC, Lin FH, Qi Z, Kuo TF, Cheng YH et al. Chitosan/gelatin hydrogel as immunoisolative matrix for injectable bioartificial pancreas. Xenotransplantation. 2008; 15 (6): 407–416. doi: 10.1111/j.1399-3089.2008.00503.x.
44. Kuehn C, Fülöp T, Lakey JR, Vermette P. Young porcine endocrine pancreatic islets cultured in fibrin and alginate gels show improved resistance towards human monocytes. Pathol Biol. 2014; 62 (6): 354–364. doi: 10.1016/j.patbio.2014.07.010.
45. Bhang SH, Jung MJ, Shin JY, La WG, Hwang YH, Kim MJ et al. Mutual effect of subcutaneously trans-planted human adipose-derived stem cells and pancreatic islets within fibrin gel. Biomaterials. 2013; 34 (30): 7247–7256. doi: 10.1016/j.biomaterials.2013.06.018.
46. Kuehn C, Lakey JR, Lamb MW, Vermette P. Young porcine endocrine pancreatic islets cultured in fibrin show improved resistance toward hydrogen peroxide. Islets. 2013; 5 (5): 207–215. doi: 10.4161/isl.26989.
47. Niknamasl A, Ostad SN, Soleimani M, Azami M, Salmani MK, Lotfibakhshaiesh N et al. A new approach for pancreatic tissue engineering: human endometrial stem cells encapsulated in fibrin gel can differentiate to pancreatic islet beta-cell. Cell Biol Int. 2014; 38 (10): 1174–1182. doi: 10.1002/cbin.10314.
48. 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. doi: 10.1016/j.tice.2017.03.001.
49. Muthyala S, Bhonde RR, Nair PD. Cytocompatibility studies of mouse pancreatic islets on gelatin – PVP semi IPN scaffolds in vitro: potential implication towards pancreatic tissue engineering. Islets. 2010; 2 (6): 357–366. doi: 10.4161/isl.2.6.13765.
50. Kuo YC, Liu YC, Rajesh R. Pancreatic differentiation of induced pluripotent stem cells in activin A-grafted gelatin-poly(lactide-co-glycolide) nanoparticle scaffolds with induction of LY294002 and retinoic acid. Mater Sci Eng C Mater Biol Appl. 2017; 77: 384–393. doi: 10.1016/j.msec.2017.03.265.
51. Davis NE, Beenken-Rothkopf LN, Mirsoian A, Kojic N, Kaplan DL, Barron AE et al. Enhanced function of pancreatic islets co-encapsulated with ECM proteins and mesenchymal stromal cells in a silk hydrogel. Biomaterials. 2012; 33 (28): 6691–6697. doi: 10.1016/j.biomaterials.2012.06.015.
52. Shalaly ND, Ria M, Johansson U, Åvall K, Berggren PO, Hedhammar M. Silk matrices promote formation of insulin-secreting islet-like clusters. Biomaterials. 2016; 90: 50–61. doi: 10.1016/j.biomaterials.2016.03.006.
53. Kumar M, Nandi SK, Kaplan DL, Mandal BB. Localized immunomodulatory silk macrocapsules for islet-like spheroid formation and sustained insulin production. ACS Biomater Sci Eng. 2017; 3: 2443–2456. doi: 10.1021/acsbiomaterials.7b00218.
54. Xu T, Zhu M, Guo Y, Wu D, Huang Y, Fan X et al. Three-dimensional culture of mouse pancreatic islet on a liver-derived perfusion-decellularized bioscaffold for potential clinical application. J Biomater Appl. 2015; 30 (4): 379–387. doi: 10.1177/0885328215587610.
55. Wu D, Wan J, Huang Y, Guo Y, Xu T, Zhu M et al. 3D culture of MIN-6 cells on decellularized pancreatic scaffold: in vitro and in vivo study. Biomed Res Int. 2015: 432645. doi: 10.1155/2015/432645.
56. Abualhassan N, Sapozhnikov L, Pawlick RL, Kahana M, Pepper AR, Bruni A et al. Lung-derived microscaffolds facilitate diabetes reversal after mouse and human intraperitoneal islet transplantation. PLoS ONE. 2016; 11 (5): e0156053. doi: 10.1371/journal.pone.0156053.
57. Katsuki Y, Yagi H, Okitsu T, Kitago M, Tajima K, Kadota Y et al. Endocrine pancreas engineered using porcine islets and partial pancreatic scaffolds. Pancreatology. 2016; 16 (5): 922–930. doi: 10.1016/j.pan.2016.06.007.
58. Zhou P, Guo Y, Huang Y, Zhu M, Fan X, Wang L et al. The dynamic three-dimensional culture of islet-like clusters in decellularized liver scaffolds. Cell Tissue Res. 2016; 365 (1): 157–171. doi: 10.1007/s00441-015-2356-8.
59. Wang X, Wang K, Zhang W, Qiang M, Luo Y. A bilaminated decellularized scaffold for islet transplantation: structure, properties and functions in diabetic mice. Biomaterials. 2017; 138: 80–90. doi: 10.1016/j.biomaterials.2017.05.033.
60. Wan J, Huang Y, Zhou P, Guo Y, Wu C, Zhu S et al. Culture of iPSCs derived pancreatic beta-like cells in vitro using decellularized pancreatic scaffolds: a preliminary trial. Biomed Res Int. 2017; 2017: 4276928. doi: 10.1155/2017/4276928.
61. Napierala H, Hillebrandt KH, Haep, N, Tang P, Tintemann M, Gassner J et al. Engineering an endocrine Neo-Pancreas by repopulation of a decellularized rat pancreas with islets of Langerhans. Sci Rep. 2017; 7: 41777. doi: 10.1038/srep41777.
62. Sackett SD, Tremmel DM, Ma F, Feeney AK, Maguire RM, Brown ME et al. Extracellular matrix scaffold and hydrogel derived from decellularized and delipidized human pancreas. Sci Rep. 2018; 8 (1): 10452. doi: 10.1038/s41598-018-28857-1.
63. Berkova Z, Zacharovova K, Patikova A, Leontovyc I, Hladikova Z, Cerveny D et al. Decellularized pancreatic tail as matrix for pancreatic islet transplantation into the greater omentum in rats. J Funct Biomater. 2022; 13 (4): 171. doi: 10.3390/jfb13040171.
64. Klak M, Łojszczyk I, Berman A, Tymicki G, Adamiok-Ostrowska A, Sierakowski M et al. Impact of porcine pancreas decellularization conditions on the quality of obtained dECM. Int J Mol Sci. 2021; 22 (13): 7005. doi: 10.3390/ijms22137005.
65. Kizilel S, Scavone A, Liu X, Nothias JM, Ostrega D, Witkowski P et al. Encapsulation of pancreatic islets within nano-thin functional polyethylene glycol coatings for enhanced insulin secretion. Tissue Eng Part A. 2010; 16 (7): 2217–2228. doi: 10.1089/ten.TEA.2009.0640.
66. Mason MN, Mahoney MJ. A novel composite construct increases the vascularization potential of PEG hydrogels through the incorporation of large fibrin ribbons. J Biomed Mater Res A. 2010; 95 (1): 283–293. doi: 10.1002/jbm.a.32825.
67. Lin CC, Anseth KS. Cell-cell communication mimicry with poly(ethylene glycol) hydrogels for enhancing beta-cell function. Proc Natl Acad Sci USA. 2011; 108 (16): 6380–6385. doi: 10.1073/pnas.1014026108.
68. Hall KK, Gattas-Asfura KM, Stabler CL. Microencapsulation of islets within alginate/poly(ethylene glycol) gels cross-linked via Staudinger ligation. Acta Biomater. 2011; 7 (2): 614–624. doi: 10.1016/j.actbio.2010.07.016.
69. Hume PS, Anseth KS. Polymerizable superoxide dismutase mimetic protects cells encapsulated in poly(ethylene glycol) hydrogels from reactive oxygen species-mediated damage. J Biomed Mater Res A. 2011; 99 (1): 29–37. doi: 10.1002/jbm.a.33160.
70. Raza A, Lin CC. The influence of matrix degrada tion and functionality on cell survival and morphogenesis in PEG-based hydrogels. Macromol Biosci. 2013; 13 (8): 1048–1058. doi: 10.1002/mabi.201300044.
71. Marchioli G, Luca AD, de Koning E, Engelse M, Van Blitterswijk CA, Karperien M et al. Hybrid polycaprolactone/alginate scaffolds functionalized with VEGF to promote de novo vessel formation for the transplantation of islets of Langerhans. Adv Healthc Mater. 2016; 5 (13): 1606–1616. doi: 10.1002/adhm.201600058.
72. Bal T, Nazli C, Okcu A, Duruksu G, Karaöz E, Kizilel S. Mesenchymal stem cells and ligand incorporation in biomimetic poly(ethylene glycol) hydrogels significantly improve insulin secretion from pancreatic islets. J Tissue Eng Regen Med. 2017; 11 (3): 694–703. doi: 10.1002/term.1965.
73. Knobeloch T, Abadi SEM, Bruns J, Petrova Zustiak S, Kwon G. Injectable polyethylene glycol hydrogel for islet encapsulation: an in vitro and in vivo Characterization. Biomed Phys Eng Express. 2017; 3: 035022. doi: 10.1088/2057-1976/aa742b.
74. Smink AM, Li S, Hertsig DT, de Haan BJ, Schwab L, van Apeldoorn AA et al. The efficacy of a prevascularized, retrievable poly(D,L,-lactide-co-ε-caprolactone) subcutaneous scaffold as transplantation site for pancreatic islets. Transplantation. 2017; 101 (4): e112–e119. doi: 10.1097/TP.0000000000001663.
75. Marchioli G, Zellner L, Oliveira C, Engelse M, Koning E, Mano J et al. Layered PEGDA hydrogel for islet of Langerhans encapsulation and improvement of vascularization. J Mater Sci Mater Med. 2017; 28 (12): 195. doi: 10.1007/s10856-017-6004-6.
76. Abazari MF, Soleimanifar F, Nouri Aleagha M, Torabinejad S, Nasiri N, Khamisipour G et al. PCL/PVA nano-fibrous scaffold improve insulin-producing cells generation from human induced pluripotent stem cells. Gene. 2018; 671: 50–57. doi: 10.1016/j.gene.2018.05.115.
77. Chun S, Huang Y, Xie WJ, Hou Y, Huang RP, Song YM et al. Adhesive growth of pancreatic islet cells on a polyglycolic acid fibrous scaffold. Transplant Proc. 2008; 40 (5): 1658 doi: 10.1016/j.transproceed.2008.02.088.
78. Mao GH, Chen GA, Bai HY, Song TR, Wang YX. The reversal of hyperglycaemia in diabetic mice using PLGA scaffolds seeded with islet-like cells derived from human embryonic stem cells. Biomaterials. 2009; 30 (9): 1706–1714. doi: 10.1016/j.biomaterials.2008.12.030.
79. Li Y, Fan P, Ding XM, Tian XH, Feng XS, Yan H et al. Polyglycolic acid fibrous scaffold improving endothelial cell coating and vascularization of islet. Chin Med J. 2017; 130 (7): 832–839. doi: 10.4103/0366-6999.202730.
80. Kheradmand T, Wang S, Gibly RF, Zhang X, Holland S, Tasch J et al. Permanent protection of PLG scaffold transplanted allogeneic islet grafts in diabetic mice treated with ECDI-fixed donor splenocyte infusions. Biomaterials. 2011; 32 (20): 4517–4524. doi: 10.1016/j.biomaterials.2011.03.009.
81. Daoud JT, Petropavlovskaia MS, Patapas JM, Degrandpré CE, Diraddo RW, Rosenberg L et al. Long-term in vitro human pancreatic islet culture using three dimensional microfabricated scaffolds. Biomaterials. 2011; 32 (6): 1536–1542. doi: 10.1016/j.biomaterials.2010.10.036.
82. Liu L, Tan J, Li B, Xie Q, Sun J, Pu H et al. Construction of functional pancreatic artificial islet tissue composed of fibroblast-modified polylactic-co-glycolic acid membrane and pancreatic stem cells. J Biomater Appl. 2017; 32 (3): 362–372. doi: 10.1177/0885328217722041.
83. Sevastianov VI. Cell-engineered constructs in tissue engineering and regenerative medicine. Russian Journal of Transplantology and Artificial Organs. 2015; 17 (2): 127–130. (In Russ.). doi: 10.15825/1995-1191-2015-2-127-130.
84. Buitinga M, Assen F, Hanegraaf M, Wieringa P, Hilderink J, Moroni L et al. Micro-fabricated scaffolds lead to efficient remission of diabetes in mice. Biomaterials. 2017; 135: 10–22. doi: 10.1016/j.biomaterials.2017.03.031.
85. Kumar A. Supermacroporous Cryogels: Biomedical and Biotechnological Applications. 1st Edition. USA: CRC Press. 2016; 480. doi: 10.1201/b19676.
86. Lozinsky VI. A breif history of polymeric cryogels. Adv Polym Sci. 2014; 263: 1–48. doi: 10.1007/978-3-319-05846-7_1.
87. Lozinsky VI, Kulakova VK, Grigoriev AM, Podorozhko EA, Kirsanova LA, Kirillova AD et al. Cryostructuring of Polymeric Systems: 63. Synthesis of Two Chemically Tanned Gelatin-Based Cryostructurates and Evaluation of Their Potential as Scaffolds for Culturing of Mammalian Cells. Gels. 2022; 8 (11): 695. doi: 10.3390/gels8110695.
88. Bloch K, Lozinsky VI, Galaev IY, Yavriyanz K, Vorobeychik M, Azarov D et al. Functional activity of insulinoma cells (INS-1E) and pancreatic islets cultured in agarose cryogel sponges. J Biomed Mater Res A. 2005; 75: 802–809. doi: 10.1002/jbm.a.30466.
89. Lozinsky VI, Damshkaln LG, Bloch RO, Vardi P, Grinberg NV, Burova TV et al. Cryostructuring of polymer systems. Preparation and characterization of supermacroporous (spongy) agarose-based cryogels used as three-dimensional scaffolds for culturing insulin-producing cell aggregates. J Appl Polym Sci. 2008; 108: 3046–3062. doi: 10.1002/app.27908.
90. Minardi S, Guo M, Zhang X, Luo X. An elastin-based vasculogenic scaffold promotes marginal islet mass engraftment and function at an extrahepatic site. J Immunol Regen Med. 2019; 3: 1–12. doi: 10.1016/j.regen.2018.12.001.
91. Sevastianov VI, Grigoriev AM, Basok YuB, Kirsanova LA, Vasilets VN, Malkova AP et al. Biocompatible and matrix properties of polylactide scaffolds. Russian Journal of Transplantology and Artificial Organs. 2018; 20 (2): 82–90. (In Russ.). doi: 10.15825/1995-1191-2018-2-82-90.
92. Pinkse GG, Bouwman WP, Jiawan-Lalai R, Terpstra OT, Bruijn JA, de Heer E. Integrin signaling via RGD peptides and anti-beta1 antibodies confers resistance to apoptosis in islets of Langerhans. Diabetes. 2006; 55 (2): 312–317. doi: 10.2337/diabetes.55.02.06.db04-0195.
93. Sevastianov VI, Basok YB, Kirsanova LA, Grigoriev AM, Kirillova AD, Nemets EA et al. A Comparison of the Capacity of Mesenchymal Stromal Cells for Cartilage Regeneration Depending on Collagen-Based Injectable Biomimetic Scaffold Type. Life (Basel). 2021; 11 (8): 756. doi: 10.3390/life11080756.
94. Hamamoto Y, Fujimoto S, Inada A, Takehiro M, Nabe K, Shimono D et al. Beneficial effect of pretreatment of islets with fibronectin on glucose tolerance after islet transplantation. Horm Metab Res. 2003; 35 (8): 460–465. doi: 10.1055/s-2003-41802.
95. Yeo GC, Mithieux SM, Weiss AS. The elastin matrix in tissue engineering and regeneration. Current Opinion in Biomedical Engineering. 2018; 6: 27–32. doi: 10.1016/j.cobme.2018.02.007.
96. Mendibil U, Ruiz-Hernandez R, Retegi-Carrion S, Garcia-Urquia N, Olalde-Graells B, Abarrategi A. Tissue-Specific Decellularization Methods: Rationale and Strategies to Achieve Regenerative Compounds. Int J Mol Sci. 2020; 21: 5447. doi: 10.3390/ijms21155447.
97. Rabbani M, Zakian N, Alimoradi N. Contribution of Physical Methods in Decellularization of Animal Tissues. Journal of Medical Signals & Sensors. 2021; 11 (1): 1. doi: 10.4103/jmss.JMSS_2_20.
98. Ponomareva AS, Baranova NV, Kirsanova LA, Bubentsova GN, Nemets EA, Miloserdov IA, Sevastianov VI. Determining the optimal pancreatic decellularization protocol, taking into account tissue morphological features. Russian Journal of Transplantology and Artificial Organs. 2022; 24 (1): 64–71. doi: 10.15825/1995-1191-2022-1-64-71.
99. Sevastianov VI, Ponomareva AS, Baranova NV, Kirsanova LA, Basok YuB, Nemets EA et al. Decellularization of Human Pancreatic Fragments with Pronounced Signs of Structural Changes. Int J Mol Sci. 2023; 24: 119. doi: 10.3390/ijms24010119.28.
100. Sevastianov VI, Ponomareva AS, Baranova NV, Belova AD, Kirsanova LA, Nikolskaya AO et al. ATissue-Engineered Construct Based on a Decellularized Scaffold and the Islets of Langerhans: A Streptozotocin-Induced Diabetic Model. Life (Basel). 2024; 14 (11): 1505. doi: 10.3390/life14111505.
101. Peloso A, Urbani L, Cravedi P, Katari R, Maghsoudlou P, Fallas MEA et al. The human pancreas as a source of pro-tolerogenic extracellular matrix scaffold for a new generation bio-artificial endocrine pancreas. Ann Surg. 2016; 264 (1): 169–179. doi: 10.1097/SLA.0000000000001364.
102. Ponomareva AS, Kirsanova LA, Baranova NV, Surguchenko VA, Bubentsova GN, Basok YuB et al. Decellularization of donor pancreatic fragment to obtain a tissue-specific matrix scaffold. Russian Journal of Transplantology and Artificial Organs. 2020; 22 (1): 123–133. doi: 10.15825/1995-1191-2020-1-123-133.
103. Elebring E, Kuna VK, Kvarnstrom N, Sumitran-Holgersson S. Cold-perfusion decellularization of whole-organ porcine pancreas supports human fetal pancreatic cell attachment and expression of endocrine and exocrine markers. J Tissue Eng. 2017; 8: 2041731417738145. doi: 10.1177/2041731417738145.
104. Goh SK, Bertera S, Richardson T, Banerjee I. Repopulation of decellularized organ scaffolds with human pluripotent stem cell-derived pancreatic progenitor cells. Biomed Mater. 2023; 18 (2). doi: 10.1088/1748-605X/acb7bf.
105. Song JJ, Ott HC. Organ engineering based on decellularized matrix scaffolds. Trends Mol Med. 2011; 17 (8): 424–432. doi: 10.1016/j.molmed.2011.03.005.
106. Damodaran GR, Vermette P. Decellularized pancreas as a native extracellular matrix scaffold for pancreatic islet seeding and culture. J Tissue Eng Regen Med. 2018; 12 (5): 1230–1237. doi: 10.1002/term.2655.
107. Khorsandi L, Orazizadeh M, Bijan Nejad D, Heidari Moghadam A, Nejaddehbashi F, Asadi Fard Y. Spleen extracellular matrix provides a supportive microenvironment for β-cell function. Iran J Basic Med Sci. 2022; 25 (9): 1159–1165. doi: 10.22038/IJBMS.2022.65233.14360.
108. Goldman O, Puchinsky D, Durlacher K, Sancho R, Ludwig B, Kugelmeier P et al. Lung Based Engineered Micro-Pancreas Sustains Human Beta Cell Survival and Functionality. Horm Metab Res. 2019; 51 (12): 805–811. doi: 10.1055/a-1041-3305.
109. Saldin LT, Cramer MC, Velankar SS, White LJ, Badylak SF. Extracellular matrix hydrogels from decellularized tissues: Structure and function. Acta Biomater. 2017; 49: 1–15. doi: 10.1016/j.actbio.2016.11.068.
110. Lozinsky VI. Cryostructuring of Polymeric Systems. 50.† Cryogels and Cryotropic Gel-Formation: Terms and Definitions. Gels. 2018; 4: 77. doi: 10.3390/gels4030077.
111. Kim JY, Sen T, Lee JY, Cho D-W. Degradation-controlled tissue extracellular sponge for rapid hemostasis and wound repair after kidney injury. Biomaterials. 2024; 307: 122524. doi: 10.1016/j.biomaterials.2024.122524.
112. Borg DJ, Welzel PB, Grimmer M, Friedrichs J, Weigelt M, Wilhelm C et al. Macroporous biohybrid cryogels for co-housing pancreatic islets with mesenchymal stromal cells. Acta Biomater. 2016; 44: 178–187. doi: 10.1016/j.actbio.2016.08.007.
Review
For citations:
Ponomareva A.S., Baranova N.V., Basok Yu.B., Sevastianov V.I. Extracellular matrix biomimetics for pancreatic tissue engineering. Russian Journal of Transplantology and Artificial Organs. 2025;27(3):146-159. (In Russ.) https://doi.org/10.15825/1995-1191-2025-3-146-159
Views:
30
Email this article 