Islet cell transplantation for the treatment of type 1 diabetes: Recent advances and future challenges

Diabetes, Metabolic Syndrome and Obesity

Volumn 7, Issue , 2014, Pages 211-223

  Bruni, Anthony ^a   Gala Lopez, Boris ^a   Pepper, Andrew R ^a   Abualhassan, Nasser S ^a   James Shapiro, A M ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Edmonton Protocol; Engraftment; Immunosuppression; Islet transplantation; Type I diabetes mellitus

Indexed keywords

ALEMTUZUMAB; AZATHIOPRINE; BELATACEPT; C PEPTIDE; CALCINEURIN INHIBITOR; CORTICOSTEROID; DACLIZUMAB; GLUTAMATE DECARBOXYLASE 65; HEMOGLOBIN A1C; INSULIN; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; RAPAMYCIN; TACROLIMUS;

ALLOTRANSPLANTATION; ARTICLE; CADAVER DONOR; DONOR SELECTION; ENGRAFTMENT; GLYCEMIC CONTROL; GRAFT SURVIVAL; HUMAN; HYPOGLYCEMIA; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN PUMP; INSULIN TREATMENT; LOW DRUG DOSE; NONHUMAN; PANCREAS ISLET TRANSPLANTATION; T CELL DEPLETION;

EID: 84903279290     PISSN: None     EISSN: 11787007     Source Type: Journal    
DOI: 10.2147/DMSO.S50789     Document Type: Article

References (113)

1. Polonsky KS. The past 200 years in diabetes. New Engl J Med. 2012;367(14):1332-1340.
2. Banting FG, Best CH, Collip JB, Campbell WR, Fletcher AA. Pancreatic extracts in the treatment of diabetes mellitus. Can Med Assoc J. 1922;12(3):141-146.
3. Agarwal A, Brayman KL. Update on islet cell transplantation for type 1 diabetes. Semin Intervent Radiol. 2012;29(2):90-98.
4. Lacy PE, Kostianovsky M. Method for the isolation of intact islets of Langerhans from the rat pancreas. Diabetes. 1967;16(1):35-39.
5. Reckard CR, Ziegler MM, Barker CF. Physiological and immunological consequences of transplanting isolated pancreatic islets. Surgery. 1973;74(1):91-99.
6. Shapiro AM. A historical perspective on experimental and clinical islet transplantation. In: Shapiro AMJ, Shaw JAM, editors. Islet Transplantation and Beta Cell Replacement Therapy. New York: Informa Health Care; 2007:1-18.
7. Lakey JR, Warnock GL, Shapiro AM, etal. Intraductal collagenase delivery into the human pancreas using syringe loading or controlled perfusion. Cell Transplant. 1999;8(3):285-292.
8. Ricordi C, Lacy PE, Scharp DW. Automated islet isolation from human pancreas. Diabetes. 1989;38 Suppl 1:140-142.
9. Emamaullee JA, Shapiro AM. Interventional strategies to prevent beta-cell apoptosis in islet transplantation. Diabetes. 2006;55(7):1907-1914.
10. Shapiro AM, Lakey JR, Ryan EA, etal. 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.
11. Ryan EA, Bigam D, Shapiro AM. Current indications for pancreas or islet transplant. Diabetes Obes Metab. 2006;8(1):1-7.
12. Scharp DW, Kemp CB, Knight MJ, Ballinger WF, Lacy PE. The use of ficoll in the preparation of viable islets of langerhans from the rat pancreas. Transplantation. 1973;16(6):686-689.
13. Najarian JS, Sutherland DE, Matas AJ, Steffes MW, Simmons RL, Goetz FC. Human islet transplantation: a preliminary report. Transplant Proc. 1977;9(1):233-236.
14. Brendel M, Hering B, Shulz A, Bretzel R. International Islet Transplant Registry Report. Giessen, Germany: University of Giessen; 1999:1-20.
15. The CITR Coordinating Center and Investigators. The Collaborative Islet Transplant Registry (CITR) 2011 Seventh Annual Report. US Department of Health and Human Services, Bethesda, MA, USA; 2011. Available from https://web.emmes.com/study/isl/reports/01062012_7thAnnualReport.pdf. Accessed April 9, 2014.
16. Ly TT, Nicholas JA, Retterath A, Lim EM, Davis EA, Jones TW. Effect of sensor-augmented insulin pump therapy and automated insulin suspension vs standard insulin pump therapy on hypoglycemia in patients with type 1 diabetes: a randomized clinical trial. JAMA. 2013;310(12):1240-1247.
17. Shapiro AM. Strategies toward single-donor islets of Langerhans transplantation. Curr Opin Organ Transplant. 2011;16(6):627-631.
18. Thompson DM, Meloche M, Ao Z, etal. Reduced progression of diabetic microvascular complications with islet cell transplantation compared with intensive medical therapy. Transplantation. 2011;91(3): 373-378.
19. Barton FB, Rickels MR, Alejandro R, etal. Improvement in outcomes of clinical islet transplantation: 1999-2010. Diabetes Care. 2012;35(7): 1436-1445.
20. Senior PA, Kin T, Shapiro AMJ, Koh A. Islet transplantation at the University of Alberta: status update and review of progress over the last decade. Can J Diabetes. 2012;36:32-37.
21. Merani S, Shapiro AM. Current status of pancreatic islet transplantation. Clin Sci (Lond). 2006;110(6):611-625.
22. Pepper AR, Gala-Lopez B, Ziff O, Shapiro AJ. Current status of clinical islet transplantation. World J Transplant. 2013;3(4):48-53.
23. Benhamou PY, Watt PC, Mullen Y, etal. Human islet isolation in 104 consecutive cases. Factors affecting isolation success. Transplantation. 1994;57(12):1804-1810.
24. Goto M, Eich TM, Felldin M, etal. Refinement of the automated method for human islet isolation and presentation of a closed system for in vitro islet culture. Transplantation. 2004;78(9):1367-1375.
25. Ihm SH, Matsumoto I, Sawada T, etal. Effect of donor age on function of isolated human islets. Diabetes. 2006;55(5):1361-1368.
26. Lakey JR, Rajotte RV, Warnock GL, Kneteman NM. Human pancreas preservation prior to islet isolation. Cold ischemic tolerance. Transplantation. 1995;59(5):689-694.
27. Lakey JR, Warnock GL, Rajotte RV, etal. Variables in organ donors that affect the recovery of human islets of Langerhans. Transplantation. 1996;61(7):1047-1053.
28. Matsumoto I, Sawada T, Nakano M, etal. Improvement in islet yield from obese donors for human islet transplants. Transplantation. 2004;78(6):880-885.
29. Nano R, Clissi B, Melzi R, etal. Islet isolation for allotransplantation: variables associated with successful islet yield and graft function. Diabetologia. 2005;48(5):906-912.
30. Zeng Y, Torre MA, Karrison T, Thistlethwaite JR. The correlation between donor characteristics and the success of human islet isolation. Transplantation. 1994;57(6):954-958.
31. Kin T, Murdoch TB, Shapiro AM, Lakey JR. Estimation of pancreas weight from donor variables. Cell Transplant. 2006;15(2):181-185.
32. Brandhorst H, Brandhorst D, Hering BJ, Federlin K, Bretzel RG. Body mass index of pancreatic donors: a decisive factor for human islet isolation. Exp Clin Endocrinol Diabetes. 1995;103 Suppl 2:23-26.
33. Berney T, Johnson PR. Donor pancreata: evolving approaches to organ allocation for whole pancreas versus islet transplantation. Transplantation. 2010;90(3):238-243.
34. O'Gorman D, Kin T, Murdoch T, etal. The standardization of pancreatic donors for islet isolation. Transplant Proc. 2005;37(2):1309-1310.
35. Witkowski P, Liu Z, Cernea S, etal. Validation of the scoring system for standardization of the pancreatic donor for islet isolation as used in a new islet isolation center. Transplant Proc. 2006;38(9):3039-3040.
36. Noguchi H. Pancreas procurement and preservation for islet transplantation: personal considerations. J Transplant. 2011;2011:783168.
37. Saito T, Gotoh M, Satomi S, etal; Working Members of The Japanese Pancreas and Islet Transplantation Association. Islet transplantation using donors after cardiac death: report of the Japan Islet Transplantation Registry. Transplantation. 2010;90(7):740-747.
38. Wolters GH, Vos-Scheperkeuter GH, van Deijnen JH, van Schilfgaarde R. An analysis of the role of collagenase and protease in the enzymatic dissociation of the rat pancreas for islet isolation. Diabetologia. 1992;35(8):735-742.
39. Wang X, Meloche M, Verchere CB, Ou D, Mui A, Warnock GL. Improving islet engraftment by gene therapy. J Transplant. 2011;2011:594851.
40. Ichii H, Pileggi A, Khan A, Fraker C, Ricordi C. Culture and transportation of human islets between centers. In: Shapiro AMJ, Shaw JAM, editors. Islet Transplantation and Beta Cell Replacement Therapy. New York: Informa Healthcare; 2007:251-268.
41. Nagata NA, Inoue K, Tabata Y. Co-culture of extracellular matrix suppresses the cell death of rat pancreatic islets. J Biomater Sci Polym Ed. 2002;13(5):579-590.
42. Lakey JR, Woods EJ, Zieger MA, etal. Improved islet survival and in vitro function using solubilized small intestinal submucosa. Cell Tissue Bank. 2001;2(4):217-224.
43. Gatto C, Callegari M, Folin M, etal. Effects of cryopreservation and coculture with pancreatic ductal epithelial cells on insulin secretion from human pancreatic islets. Int J Mol Med. 2003;12(6):851-854.
44. Velmurugan K, Balamurugan AN, Loganathan G, Ahmad A, Hering BJ, Pugazhenthi S. Antiapoptotic actions of exendin-4 against hypoxia and cytokines are augmented by CREB. Endocrinology. 2012;153(3):1116-1128.
45. Bloch K, Vennang J, Lazard D, Vardi P. Different susceptibility of rat pancreatic alpha and beta cells to hypoxia. Histochem Cell Biol. 2012;137(6):801-810.
46. Narang AS, Cheng K, Henry J, etal. Vascular endothelial growth factor gene delivery for revascularization in transplanted human islets. Pharm Res. 2004;21(1):15-25.
47. Emamaullee JA, Shapiro AM. Factors influencing the loss of beta-cell mass in islet transplantation. Cell Transplant. 2007;16(1):1-8.
48. Merani S, Toso C, Emamaullee J, Shapiro AM. Optimal implantation site for pancreatic islet transplantation. Br J Surg. 2008;95(12):1449-1461.
49. Gibly RF, Graham JG, Luo X, Lowe WL Jr, Hering BJ, Shea LD. Advancing islet transplantation: from engraftment to the immune response. Diabetologia. 2011;54(10):2494-2505.
50. Wang RN, Rosenberg L. Maintenance of beta-cell function and survival following islet isolation requires re-establishment of the islet-matrix relationship. J Endocrinol. 1999;163(2):181-190.
51. Barshes NR, Wyllie S, Goss JA. Inflammation-mediated dysfunction and apoptosis in pancreatic islet transplantation: implications for intrahepatic grafts. J Leukoc Biol. 2005;77(5):587-597.
52. Carlsson PO, Palm F, Andersson A, Liss P. Chronically decreased oxygen tension in rat pancreatic islets transplanted under the kidney capsule. Transplantation. 2000;69(5):761-766.
53. Carlsson PO, Palm F, Andersson A, Liss P. Markedly decreased oxygen tension in transplanted rat pancreatic islets irrespective of the implantation site. Diabetes. 2001;50(3):489-495.
54. Plesner A, Verchere CB. Advances and challenges in islet transplantation: islet procurement rates and lessons learned from suboptimal islet transplantation. J Transplant. 2011;2011:979527.
55. Goto M, Tjernberg J, Dufrane D, etal. Dissecting the instant blood-mediated inflammatory reaction in islet xenotransplantation. Xenotransplantation. 2008;15(4):225-234.
56. Vivot K, Jeandidier N, Dollinger C, etal. Role of islet culture on angiogenic and inflammatory mechanisms. Transplant Proc. 2011;43(9): 3201-3204.
57. Nilsson B, Ekdahl KN, Korsgren O. Control of instant blood-mediated inflammatory reaction to improve islets of Langerhans engraftment. Curr Opin Organ Transplant. 2011;16(6):620-626.
58. Ji M, Yi S, Smith-Hurst H, etal. The importance of tissue factor expression by porcine NICC in triggering IBMIR in the xenograft setting. Transplantation. 2011;91(8):841-846.
59. Ma X, Ye B, Gao F, etal. Tissue factor knockdown in porcine islets: an effective approach to suppressing the instant blood-mediated inflammatory reaction. Cell Transplant. 2012;21(1):61-71.
60. Ozmen L, Ekdahl KN, Elgue G, Larsson R, Korsgren O, Nilsson B. Inhibition of thrombin abrogates the instant blood-mediated inflammatory reaction triggered by isolated human islets: possible application of the thrombin inhibitor melagatran in clinical islet transplantation. Diabetes. 2002;51(6):1779-1784.
61. Yasunami Y, Kojo S, Kitamura H, etal. Valpha14 NK T cell-triggered IFN-gamma production by Gr-1+CD11b+ cells mediates early graft loss of syngeneic transplanted islets. J Exp Med. 2005;202(7):913-918.
62. Bloom SR, Polak JM. Somatostatin. Br Med J (Clin Res Ed). 1987;295(6593):288-290.
63. Korsgren O, Lundgren T, Felldin M, etal. Optimising islet engraftment is critical for successful clinical islet transplantation. Diabetologia. 2008;51(2):227-232.
64. Wu Z, Liu S, Hassink M, etal. Development and evaluation of 18F-TTCO-Cys40-Exendin-4: a PET probe for imaging transplanted islets. J Nucl Med. 2013;54(2):244-251.
65. Toso C, Vallee JP, Morel P, etal. Clinical magnetic resonance imaging of pancreatic islet grafts after iron nanoparticle labeling. Am J Transplant. 2008;8(3):701-706.
66. Medarova Z, Moore A. MRI as a tool to monitor islet transplantation. Nat Rev Endocrinol. 2009;5(8):444-452.
67. Oishi K, Miyamoto Y, Saito H, etal. In vivo imaging of transplanted islets labeled with a novel cationic nanoparticle. PloS One. 2013;8(2):e57046.
68. Eich T, Eriksson O, Lundgren T; Nordic Network for Clinical Islet Transplantation. Visualization of early engraftment in clinical islet transplantation by positron-emission tomography. New Engl J Med. 2007;356(26):2754-2755.
69. Eriksson O, Alavi A. Imaging the islet graft by positron emission tomography. Eur J Nucl Med Mol Imaging. 2012;39(3):533-542.
70. Rajab A. Islet transplantation: alternative sites. Curr Diab Rep. 2010;10(5):332-337.
71. Barshes NR, Lee TC, Goodpastor SE, etal. Transaminitis after pancreatic islet transplantation. J Am Coll Surg. 2005;200(3):353-361.
72. Veriter S, Gianello P, Dufrane D. Bioengineered sites for islet cell transplantation. Curr Diab Rep. 2013;13(5):745-755.
73. Lacy PE, Ricordi C, Finke EH. Effect of transplantation site and alpha L3T4 treatment on survival of rat, hamster, and rabbit islet xenografts in mice. Transplantation. 1989;47(5):761-766.
74. Mellgren A, Schnell Landstrom AH, Petersson B, Andersson A. The renal subcapsular site offers better growth conditions for transplanted mouse pancreatic islet cells than the liver or spleen. Diabetologia. 1986;29(9):670-672.
75. Jindal RM, Sidner RA, McDaniel HB, Johnson MS, Fineberg SE. Intraportal vs kidney subcapsular site for human pancreatic islet transplantation. Transplant Proc. 1998;30(2):398-399.
76. Pepper AR, Gala-Lopez B, Ziff O, Shapiro AM. Revascularization of transplanted pancreatic islets and role of the transplantation site. Clin Dev Immunol. 2013;2013:352315.
77. Dufrane D, Goebbels RM, Gianello P. Alginate macroencapsulation of pig islets allows correction of streptozotocin-induced diabetes in primates up to 6 months without immunosuppression. Transplantation. 2010;90(10):1054-1062.
78. Rafael E, Wu GS, Hultenby K, Tibell A, Wernerson A. Improved survival of macroencapsulated islets of Langerhans by preimplantation of the immunoisolating device: a morphometric study. Cell Transplant. 2003;12(4):407-412.
79. Sorenby AK, Kumagai-Braesch M, Sharma A, Hultenby KR, Wernerson AM, Tibell AB. Preimplantation of an immunoprotective device can lower the curative dose of islets to that of free islet transplantation: studies in a rodent model. Transplantation. 2008;86(2): 364-366.
80. Barkai U, Weir GC, Colton CK, etal. Enhanced oxygen supply improves islet viability in a new bioartificial pancreas. Cell Transplant. 2013;22(8):1463-1476.
81. Ludwig B, Reichel A, Steffen A, etal. Transplantation of human islets without immunosuppression. Proc Natl Acad Sci U S A. 2013;110(47): 19054-19058.
82. D'Amour KA, Bang AG, Eliazer S, etal. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol. 2006;24(11):1392-1401.
83. Kroon E, Martinson LA, Kadoya K, etal. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol. 2008;26(4):443-452.
84. Schulz TC, Young HY, Agulnick AD, etal. A scalable system for production of functional pancreatic progenitors from human embryonic stem cells. PloS One. 2012;7(5):e37004.
85. Ryan EA, Paty BW, Senior PA, etal. Five-year follow-up after clinical islet transplantation. Diabetes. 2005;54(7):2060-2069.
86. Gala-Lopez B, Pepper AR, Shapiro AM. Biologic agents in islet transplantation. Curr Diab Rep. 2013;13(5):713-722.
87. Gabardi S, Martin ST, Roberts KL, Grafals M. Induction immunosuppressive therapies in renal transplantation. Am J Health Syst Pharm. 2011;68(3):211-218.
88. Hering BJ. Repurification: rescue rather than routine remedy. Am J Transplant. 2005;5(1):1-2.
89. Hering BJ, Kandaswamy R, Ansite JD, etal. Single-donor, marginal-dose islet transplantation in patients with type 1 diabetes. JAMA. 2005;293(7):830-835.
90. Koh A, Senior P, Salam A, etal. Insulin-heparin infusions peritransplant substantially improve single-donor clinical islet transplant success. Transplantation. 2010;89(4):465-471.
91. Matsumoto S, Takita M, Chaussabel D, etal. Improving efficacy of clinical islet transplantation with iodixanol based islet purification, thymoglobulin induction and blockage of IL-1-beta and TNF-alpha. Cell Transplant. 2011;20(10):1641-1647.
92. Shapiro AM, Ricordi C. Unraveling the secrets of single donor success in islet transplantation. Am J Transplant. 2004;4(3):295-298.
93. Xenos ES, Farney AC, Widmer MB, etal. Effect of tumor necrosis factor alpha and of the soluble tumor necrosis factor receptor on insulin secretion of isolated islets of Langerhans. Transplant Proc. 1992;24(6): 2863-2864.
94. Bhatt S, Fung JJ, Lu L, Qian S. Tolerance-inducing strategies in islet transplantation. Int J Endocrinol. 2012;2012:396524.
95. Shapiro AM, Nanji SA, Lakey JR. Clinical islet transplant: current and future directions towards tolerance. Immunol Rev. 2003;196: 219-236.
96. Posselt AM, Szot GL, Frassetto LA, etal. Islet transplantation in type 1 diabetic patients using calcineurin inhibitor-free immunosuppressive protocols based on T-cell adhesion or costimulation blockade. Transplantation. 2010;90(12):1595-1601.
97. Skyler JS, Ricordi C. Stopping type 1 diabetes: attempts to prevent or cure type 1 diabetes in man. Diabetes. 2011;60(1):1-8.
98. Skyler JS; Type 1 Diabetes TrialNet Study Group. Update on worldwide efforts to prevent type 1 diabetes. Ann N Y Acad Sci. 2008;1150: 190-196.
99. Baekkeskov S, Aanstoot HJ, Christgau S, etal. Identification of the 64K autoantigen in insulin-dependent diabetes as the GABA-synthesizing enzyme glutamic acid decarboxylase. Nature. 1990;347(6289): 151-156.
100. Tian J, Clare-Salzler M, Herschenfeld A, etal. Modulating autoimmune responses to GAD inhibits disease progression and prolongs islet graft survival in diabetes-prone mice. Nat Med. 1996;2(12):1348-1353.
101. Pleau JM, Fernandez-Saravia F, Esling A, Homo-Delarche F, Dardenne M. Prevention of autoimmune diabetes in nonobese diabetic female mice by treatment with recombinant glutamic acid decarboxylase (GAD 65). Clin Immunol Immunopathol. 1995;76(1 Pt 1):90-95.
102. Wherrett DK, Bundy B, Becker DJ, etal; Type 1 Diabetes TrialNet GAD Study Group. Antigen-based therapy with glutamic acid decarboxylase (GAD) vaccine in patients with recent-onset type 1 diabetes: a randomised double-blind trial. Lancet. 2011;378(9788):319-327.
103. Tisch R, Yang XD, Liblau RS, McDevitt HO. Administering glutamic acid decarboxylase to NOD mice prevents diabetes. J Autoimmun. 1994;7(6):845-850.
104. Belghith M, Bluestone JA, Barriot S, Megret J, Bach JF, Chatenoud L. TGF-beta-dependent mechanisms mediate restoration of self-tolerance induced by antibodies to CD3 in overt autoimmune diabetes. Nat Med. 2003;9(9):1202-1208.
105. Chatenoud L, Primo J, Bach JF. CD3 antibody-induced dominant self tolerance in overtly diabetic NOD mice. J Immunol. 1997;158(6): 2947-2954.
106. Skyler JS. The compelling case for anti-CD3 in type 1 diabetes. Diabetes. 2013;62(11):3656-3657.
107. Chatenoud L, Thervet E, Primo J, Bach JF. Anti-CD3 antibody induces long-term remission of overt autoimmunity in nonobese diabetic mice. Proc Natl Acad Sci U S A. 1994;91(1):123-127.
108. Keymeulen B, Walter M, Mathieu C, etal. Four-year metabolic outcome of a randomised controlled CD3-antibody trial in recent-onset type 1 diabetic patients depends on their age and baseline residual beta cell mass. Diabetologia. 2010;53(4):614-623.
109. Cook JJ, Hudson I, Harrison LC, etal. Double-blind controlled trial of azathioprine in children with newly diagnosed type I diabetes. Diabetes. 1989;38(6):779-783.
110. Elliott RB, Crossley JR, Berryman CC, James AG. Partial preservation of pancreatic beta-cell function in children with diabetes. Lancet. 1981;2(8247):631-632.
111. Harrison LC, Colman PG, Dean B, Baxter R, Martin FI. Increase in remission rate in newly diagnosed type I diabetic subjects treated with azathioprine. Diabetes. 1985;34(12):1306-1308.
112. Silverstein J, Maclaren N, Riley W, Spillar R, Radjenovic D, Johnson S. Immunosuppression with azathioprine and prednisone in recent-onset insulin-dependent diabetes mellitus. New Engl J Med. 1988;319(10):599-604.
113. Voltarelli JC, Couri CE, Stracieri AB, etal. Autologous nonmyeloablative hematopoietic stem cell transplantation in newly diagnosed type 1 diabetes mellitus. JAMA. 2007;297(14):1568-1576.