IMMUNE NETWORK

The Korean Association of Immunobiologists (대한면역학회)
권호 표지
DOI QR코드

DOI QR Code

Encapsulated Islet Transplantation: Strategies and Clinical Trials

  • Buder, Brian (Department of Surgery, University of California Irvine) ;
  • Alexander, Michael (Department of Surgery, University of California Irvine) ;
  • Krishnan, Rahul (Department of Surgery, University of California Irvine) ;
  • Chapman, David W. (Department of Surgery, University of California Irvine) ;
  • Lakey, Jonathan R.T. (Department of Surgery, University of California Irvine)
  • Received : 2013.11.20
  • Accepted : 2013.11.26
  • Published : 2013.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Encapsulation of tissue has been an area of intense research with a myriad number of therapeutic applications as diverse as cancer, tissue regeneration, and diabetes. In the case of diabetes, transplantation of pancreatic islets of Langerhans containing insulin-producing beta cells has shown promise toward a cure. However, anti-rejection therapy that is needed to sustain the transplanted tissue has numerous adverse effects, and the islets might still be damaged by immune processes. Furthermore, the profound scarcity of healthy human donor organs restricts the availability of islets for transplant. Islet encapsulation allows the protection of this tissue without the use of toxic medications, while also expanding the donor pool to include animal sources. Before the widespread application of this therapy, there are still issues that need to be resolved. There are many materials that can be used, differing shapes and sizes of capsules, and varied sources of islets to name a few variables that need to be considered. In this review, the current options for capsule generation, past animal and human studies, and future directions in this area of research are discussed.

Keywords

References

  1. Gabardi, S. 2011. Understanding risk evaluation and mitigation strategies in organ transplantation. Pharmacotherapy 31: 714-722. https://doi.org/10.1592/phco.31.7.714
  2. Alves, M. G., P. F. Oliveira, S. Socorro, and P. I. Moreira. 2012. Impact of diabetes in blood-testis and blood-brain barriers: resemblances and differences. Curr. Diabetes Rev. 8: 401-412. https://doi.org/10.2174/157339912803529896
  3. Salmons, B. and W. H. Gunzburg. 2010. Therapeutic application of cell microencapsulation in cancer. Adv. Exp. Med. Biol. 670: 92-103. https://doi.org/10.1007/978-1-4419-5786-3_9
  4. Thanos, C. G., B. Bintz, and D. F. Emerich. 2010. Microencapsulated choroid plexus epithelial cell transplants for repair of the brain. Adv. Exp. Med. Biol. 670: 80-91. https://doi.org/10.1007/978-1-4419-5786-3_8
  5. Lee, K. Y. and D. J. Mooney. 2001. Hydrogels for tissue engineering. Chem. Rev. 101: 1869-1879. https://doi.org/10.1021/cr000108x
  6. Nicodemus, G. D. and S. J. Bryant. 2008. Cell encapsulation in biodegradable hydrogels for tissue engineering applications. Tissue Eng. Part B Rev. 14: 149-165.
  7. Peppas, N. A., J. Z. Hilt, A. Khadenhosseini, and R. Langer. 2006. Hydrogels in biology and medicine: from molecular principles to bionanotechnology. Adv. Mater. 18: 1345-1360. https://doi.org/10.1002/adma.200501612
  8. Zimmermann, H., S. G. Shirley, and U. Zimmermann. 2007. Alginate-based encapsulation of cells: past, present, and future. Curr. Diab. Rep. 7: 314-320. https://doi.org/10.1007/s11892-007-0051-1
  9. Safley, S. A., H. Cui, S. Cauffiel, C. Tucker-Burden, and C. J. Weber. 2008. Biocompatibility and immune acceptance of adult porcine islets transplanted intraperitoneally in diabetic NOD mice in calcium alginate poly-L-lysine microcapsules versus barium alginate microcapsules without poly-L-lysine. J. Diabetes Sci. Technol. 2: 760-767. https://doi.org/10.1177/193229680800200503
  10. Tuch, B. E., G. W. Keogh, L. J. Williams, W. Wu, J. L. Foster, V. Vaithilingam, and R. Philips. 2009. Safety and viability of microencapsulated human islets transplanted into diabetic humans. Diabetes Care 32: 1887-1889.
  11. Elliott, R. B., L. Escobar, P. L. Tan, M. Muzina, S. Zwain, and C. Buchanan. 2007. Live encapsulated porcine islets from a type 1 diabetic patient 9.5 yr after xenotransplantation. Xenotransplantation. 14: 157-161. https://doi.org/10.1111/j.1399-3089.2007.00384.x
  12. Tarantal, A. F., C. C. Lee, and P. Itkin-Ansari. 2009. Real-time bioluminescence imaging of macroencapsulated fibroblasts reveals allograft protection in rhesus monkeys (Macaca mulatta). Transplantation 88: 38-41. https://doi.org/10.1097/TP.0b013e3181a9ee6c
  13. Cornolti, R., M. Figliuzzi, and A. Remuzzi. 2009. Effect of micro- and macroencapsulation on oxygen consumption by pancreatic islets. Cell Transplant. 18: 195-201. https://doi.org/10.3727/096368909788341252
  14. Lembert, N., J. Wesche, P. Petersen, M. Doser, P. Zschocke, H. D. Becker, and H. P. Ammon. 2005. Encapsulation of islets in rough surface, hydroxymethylated polysulfone capillaries stimulates VEGF release and promotes vascularization after transplantation. Cell Transplant. 14: 97-108. https://doi.org/10.3727/000000005783983232
  15. Vaithilingam, V. and B. E. Tuch. 2011. Islet transplantation and encapsulation: an update on recent developments. Rev. Diabet. Stud. 8: 51-67. https://doi.org/10.1900/RDS.2011.8.51
  16. Lim, F. and A. M. Sun. 1980. Microencapsulated islets as bioartificial endocrine pancreas. Science 210: 908-910. https://doi.org/10.1126/science.6776628
  17. Souza, Y. E., E. Chaib, P. G. Lacerda, A. Crescenzi, A. Bernal-Filho, and L. A. D'Albuquerque. 2011. Islet transplantation in rodents. Do encapsulated islets really work? Arq. Gastroenterol. 48: 146-152. https://doi.org/10.1590/S0004-28032011000200011
  18. Suzuki, K., S. Bonner-Weir, N. Trivedi, K. H. Yoon, J. Hollister-Lock, C. K. Colton, and G. C. Weir. 1998. Function and survival of macroencapsulated syngeneic islets transplanted into streptozocin-diabetic mice. Transplantation 66: 21-28. https://doi.org/10.1097/00007890-199807150-00004
  19. Duvivier-Kali, V. F., A. Omer, M. D. Lopez-Avalos, J. J. O'Neil, and G. C. Weir. 2004. Survival of microencapsulated adult pig islets in mice in spite of an antibody response. Am. J. Transplant. 4: 1991-2000. https://doi.org/10.1111/j.1600-6143.2004.00628.x
  20. Soon-Shiong, P., E. Feldman, R. Nelson, R. Heintz, Q. Yao, Z. Yao, T. Zheng, N. Merideth, G. Skjak-Braek, T. Espevik, O. Smidsrod, and P. Sandford. 1993. Long-term reversal of diabetes by the injection of immunoprotected islets. Proc. Natl. Acad. Sci. U. S. A. 90: 5843-5847. https://doi.org/10.1073/pnas.90.12.5843
  21. Dufrane, D., R. M. Goebbels, A. Saliez, Y. Guiot, and P. Gianello. 2006. Six-month survival of microencapsulated pig islets and alginate biocompatibility in primates: proof of concept. Transplantation 81: 1345-1353. https://doi.org/10.1097/01.tp.0000208610.75997.20
  22. Dufrane, D., R. M. Goebbels, and P. Gianello. 2010. Alginate macroencapsulation of pig islets allows correction of streptozotocin- induced diabetes in primates up to 6 months without immunosuppression. Transplantation 90: 1054-1062.
  23. Elliott, R. B., L. Escobar, P. L. Tan, O. Garkavenko, R. Calafiore, P. Basta, A. V. Vasconcellos, D. F. Emerich, C. Thanos, and C. Bambra. 2005. Intraperitoneal alginate-encapsulated neonatal porcine islets in a placebo-controlled study with 16 diabetic cynomolgus primates. Transplant. Proc. 37: 3505-3508. https://doi.org/10.1016/j.transproceed.2005.09.038
  24. Soon-Shiong, P., R. E. Heintz, N. Merideth, Q. X. Yao, Z. Yao, T. Zheng, M. Murphy, M. K. Moloney, M. Schmehl, M. Harris, R. Mendez, R. Mendez, and P. A. Sandford. 1994. Insulin independence in a type 1 diabetic patient after encapsulated islet transplantation. Lancet 343: 950-951. https://doi.org/10.1016/S0140-6736(94)90067-1
  25. Valdes-Gonzalez, R. A., L. M. Dorantes, G. N. Garibay, E. Bracho-Blanchet, A. J. Mendez, R. Davila-Perez, R. B. Elliott, L. Teran, and D. J. White. 2005. Xenotransplantation of porcine neonatal islets of Langerhans and Sertoli cells: a 4-year study. Eur. J. Endocrinol. 153: 419-427. https://doi.org/10.1530/eje.1.01982
  26. Valdes-Gonzalez, R., A. L. Rodriguez-Ventura, D. J. White, E. Bracho-Blanchet, A. Castillo, B. Ramirez-Gonzalez, M. G. Lopez-Santos, B. H. Leon-Mancilla, and L. M. Dorantes. 2010. Long-term follow-up of patients with type 1 diabetes transplanted with neonatal pig islets. Clin. Exp. Immunol. 162: 537-542. https://doi.org/10.1111/j.1365-2249.2010.04273.x
  27. Elliot, R. B. 2011. Living Cell Technologies, Ltd, Prague, Czech Republic.
  28. Chhabra, P. and K. L. Brayman. 2011. Current status of immunomodulatory and cellular therapies in preclinical and clinical islet transplantation. J. Ttransplant. 2011: 637692.
  29. Gao, Q., L. L. Ma, X. Gao, W. Yan. P. Williams, and D. P. Yin. 2010. TLR4 mediates early graft failure after intraportal islet transplantation. Am. J. Transplant. 10: 1588-1596. https://doi.org/10.1111/j.1600-6143.2010.03151.x
  30. Su, J., B. H. Hu, W. L. Lowe, Jr., D. B. Kaufman, and P. B. Messersmith. 2010. Anti-inflammatory peptide-functionalized hydrogels for insulin-secreting cell encapsulation. Biomaterials 31: 308-314. https://doi.org/10.1016/j.biomaterials.2009.09.045
  31. Bunger, C. M., B. Tiefenbach, A. Jahnke, C. Gerlach, T. Freier, K. P. Schmitz, U. T. Hopt, W. Schareck, E. Klar, and P. de Vos. 2005. Deletion of the tissue response against alginate- pll capsules by temporary release of co-encapsulated steroids. Biomaterials 26: 2353-2360. https://doi.org/10.1016/j.biomaterials.2004.07.017
  32. Dionne, K. E., C. K. Colton, and M. L. Yarmush. 1993. Effect of hypoxia on insulin secretion by isolated rat and canine islets of Langerhans. Diabetes 42: 12-21. https://doi.org/10.2337/diab.42.1.12
  33. Kuhtreiber, W. M., R. P. Lanza, A. M. Beyer, K. S. Kirkland, and W. L. Chick. 1993. Relationship between insulin secretion and oxygen tension in hybrid diffusion chambers. ASAIO J. 39: M247-251.
  34. De Vos, P., J. F. Van Straaten, A. G. Nieuwenhuizen, M. de Groot, R. J. Ploeg, B. J. De Haan, and R. Van Schilfgaarde. 1999. Why do microencapsulated islet grafts fail in the absence of fibrotic overgrowth? Diabetes 48: 1381-1388. https://doi.org/10.2337/diabetes.48.7.1381
  35. Pedraza, E., M. M. Coronel, C. A. Fraker, C. Ricordi, and C. L. Stabler. 2012. Preventing hypoxia-induced cell death in beta cells and islets via hydrolytically activated, oxygen-generating biomaterials. Proc. Natl. Acad. Sci. U. S. A. 109: 4245-4250. https://doi.org/10.1073/pnas.1113560109
  36. Fritschy, W. M., J. H. Strubbe, G. H. Wolters, and R. van Schilfgaarde. 1991. Glucose tolerance and plasma insulin response to intravenous glucose infusion and test meal in rats with microencapsulated islet allografts. Diabetologia 34: 542-547. https://doi.org/10.1007/BF00400270
  37. Khanna, O., M. L. Moya, E. C. Opara, and E. M. Brey. 2010. Synthesis of multilayered alginate microcapsules for the sustained release of fibroblast growth factor-1. J. Biomed. Mater. Res. A. 95: 632-640.
  38. Ludwig, B., C. G. Ziegler, A. V. Schally, C. Richter, A. Steffen, N. Jabs, R. H. Funk, M. D. Brendel, N. L. Block, M. Ehrhart-Bornstein, and S. R. Bornstein. 2010. Agonist of growth hormone-releasing hormone as a potential effector for survival and proliferation of pancreatic islets. Proc. Natl. Acad. Sci. U. S. A. 107: 12623-12628. https://doi.org/10.1073/pnas.1005098107

Cited by

  1. Employment of the Triple Helix concept for development of regenerative medicine applications based on human pluripotent stem cells vol.3, pp.1, 2013, https://doi.org/10.1186/2001-1326-3-9
  2. Managing diabetes with nanomedicine: challenges and opportunities vol.14, pp.1, 2013, https://doi.org/10.1038/nrd4477
  3. Treatment of diabetes with encapsulated pig islets: an update on current developments vol.16, pp.5, 2013, https://doi.org/10.1631/jzus.b1400310
  4. Polycaprolactone Thin-Film Micro- and Nanoporous Cell-Encapsulation Devices vol.9, pp.6, 2013, https://doi.org/10.1021/acsnano.5b00679
  5. Stem Cell Research vol.34, pp.4, 2013, https://doi.org/10.1177/1091581815581423
  6. Imaging of Hydrogel Microsphere Structure and Foreign Body Response Based on Endogenous X-Ray Phase Contrast vol.22, pp.11, 2016, https://doi.org/10.1089/ten.tec.2016.0253
  7. Combined Microencapsulated Islet Transplantation and Revascularization of Aortorenal Bypass in a Diabetic Nephropathy Rat Model vol.2016, pp.None, 2013, https://doi.org/10.1155/2016/9706321
  8. Long-Term Function of Alginate-Encapsulated Islets vol.22, pp.1, 2016, https://doi.org/10.1089/ten.teb.2015.0140
  9. Pancreatic Tissue Transplanted in TheraCyte™ Encapsulation Devices Is Protected and Prevents Hyperglycemia in a Mouse Model of Immune-Mediated Diabetes vol.25, pp.3, 2013, https://doi.org/10.3727/096368915x688939
  10. A Synthetic Mammalian Therapeutic Gene Circuit for Sensing and Suppressing Inflammation vol.25, pp.1, 2013, https://doi.org/10.1016/j.ymthe.2016.10.005
  11. Hyaluronic Acid/Collagen Hydrogel as an Alternative to Alginate for Long-Term Immunoprotected Islet Transplantation * vol.23, pp.19, 2013, https://doi.org/10.1089/ten.tea.2016.0477
  12. Developing a Rapid Algorithm to Enable Rapid Characterization of Alginate Microcapsules vol.26, pp.5, 2017, https://doi.org/10.3727/096368916x693446
  13. Pig-to-Primate Islet Xenotransplantation: Past, Present, and Future vol.26, pp.6, 2017, https://doi.org/10.3727/096368917x694859
  14. Patient and family expectations of beta-cell replacement therapies in type 1 diabetes vol.10, pp.5, 2013, https://doi.org/10.1080/19382014.2018.1503518
  15. Selection of Implantation Sites for Transplantation of Encapsulated Pancreatic Islets vol.24, pp.3, 2013, https://doi.org/10.1089/ten.teb.2017.0311
  16. In situ type I oligomeric collagen macroencapsulation promotes islet longevity and function in vitro and in vivo vol.315, pp.4, 2013, https://doi.org/10.1152/ajpendo.00073.2018
  17. Approaches in Immunotherapy, Regenerative Medicine, and Bioengineering for Type 1 Diabetes vol.9, pp.None, 2013, https://doi.org/10.3389/fimmu.2018.01354
  18. Improvement of islet function and survival by integration of perfluorodecalin into microcapsules in vivo and in vitro vol.12, pp.4, 2018, https://doi.org/10.1002/term.2643
  19. High-Throughput Screening of Encapsulated Islets Using Wide-Field Lens-Free On-Chip Imaging vol.5, pp.6, 2013, https://doi.org/10.1021/acsphotonics.8b00343
  20. Low‐adhesive ethylene vinyl alcohol–based packaging to xenogeneic islet encapsulation for type 1 diabetes treatment vol.115, pp.9, 2018, https://doi.org/10.1002/bit.26730
  21. Evaluation of encapsulating and microporous nondegradable hydrogel scaffold designs on islet engraftment in rodent models of diabetes vol.115, pp.9, 2013, https://doi.org/10.1002/bit.26741
  22. Rotational culture and integration with amniotic stem cells reduce porcine islet immunoreactivity in vitro and slow xeno‐rejection in a murine model of islet transplantation vol.26, pp.4, 2013, https://doi.org/10.1111/xen.12508
  23. Supporting Survival of Transplanted Stem‐Cell‐Derived Insulin‐Producing Cells in an Encapsulation Device Augmented with Controlled Release of Amino Acids vol.3, pp.9, 2019, https://doi.org/10.1002/adbi.201900086
  24. Review of Advanced Hydrogel-Based Cell Encapsulation Systems for Insulin Delivery in Type 1 Diabetes Mellitus vol.11, pp.11, 2019, https://doi.org/10.3390/pharmaceutics11110597
  25. CD4+/CD8+ T‐cell ratio correlates with the graft fate in pig‐to‐non‐human primate islet xenotransplantation vol.27, pp.2, 2020, https://doi.org/10.1111/xen.12562
  26. Promoting Dendrimer Self-Assembly Enhances Covalent Layer-by-Layer Encapsulation of Pancreatic Islets vol.6, pp.5, 2013, https://doi.org/10.1021/acsbiomaterials.9b01033
  27. A bio-inspired injectable hydrogel as a cell platform for real-time glycaemic regulation vol.8, pp.21, 2020, https://doi.org/10.1039/d0tb00561d
  28. Regulation of Blood Glucose Using Islets Encapsulated in a Melanin-Modified Immune-Shielding Hydrogel vol.13, pp.11, 2013, https://doi.org/10.1021/acsami.0c23010
  29. The potential role of multifunctional human amniotic epithelial cells in pancreatic islet transplantation vol.15, pp.7, 2021, https://doi.org/10.1002/term.3214