World Journal of Surgery

, Volume 31, Issue 8, pp 1569–1576 | Cite as

An Odyssey of Islet Transplantation for Therapy of Type 1 Diabetes

  • Garth L. Warnock
  • Yu Huan Theresa Liao
  • Xiaojie Wang
  • Dawei Ou
  • Ziliang Ao
  • James D. Johnson
  • C. B. Verchere
  • David Thompson
Article

Abstract

Canadian surgical contributions to the field of islet transplantation have a rich heritage and a promising future. In this article, some seminal Canadian contributions to this field are reviewed, including contributions at the basic research laboratory and translational applications to bedside therapy of type 1 diabetes.

References

  1. 1.
    Ohinmaa A, Jacobs P, Simpson SH, et al. (2004) The projection of prevalence and cost of diabetes in Canada: 2000 to 2016. Can J Diabetes 28:116–123Google Scholar
  2. 2.
    The Diabetes Control and Complications Trial Research Group. (1993) The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N Engl J Med 329:977–986CrossRefGoogle Scholar
  3. 3.
    Perkins BA, Ficocrello LH, Silva KH, et al. (2003) Regression of microalbuminuria in type 1 diabetes. N Engl J Med 348:2285–2293PubMedCrossRefGoogle Scholar
  4. 4.
    Treatment of End-stage Organ Failure in Canada, 1995 to 2004 (2006 Annual Report) (Ottawa:UHI, 2006). Canadian Institute for Health Information, February 7, 2007Google Scholar
  5. 5.
    Ballinger WF, Lacy PE. (1982) Transplantation of intact pancreatic islets in rats. Surgery 72:175–186Google Scholar
  6. 6.
    Warnock GL, Cattral MS, Rajotte RV. (1988) Normoglycemia after implantation of purified islet cells in dogs. Can J Surg 31:421–426PubMedGoogle Scholar
  7. 7.
    Warnock GL, Rajotte RV. (1988) Critical mass of purified islets that induce normoglycemia after implantation into dogs. Diabetes 37:467–470PubMedCrossRefGoogle Scholar
  8. 8.
    Warnock GL, Dabbs KD, Evans MG, et al. (1990) Critical mass of islets that function after implantation in a large mammalian. Horm Metab Res 25(Suppl):156–161Google Scholar
  9. 9.
    Warnock GL, Ellis D, Rajotte RV, et al. (1988) Studies of the isolation and viability of human islets of Langerhans. Transplantation 45:957–963PubMedCrossRefGoogle Scholar
  10. 10.
    Ricordi C, Lacy PE, Scharp DW. (1989) Automated islet isolation from human pancreas. Diabetes 38(Suppl):140–142PubMedGoogle Scholar
  11. 11.
    Lake SP, Bassett PD, Larkins A, et al. (1989) Large scale purification of human islets using discontinuous albumin gradient on IBM 2991 cell separator. Diabetes 38(Suppl 1):143–145PubMedGoogle Scholar
  12. 12.
    Rajotte RV. (1999) Islet cryopreservation protocols. Ann N Y Acad Sci 18(875):200–207CrossRefGoogle Scholar
  13. 13.
    Warnock GL, Kneteman NM, Ryan EA, et al. (1989) Continued function of pancreatic islets after transplantation in type I diabetes. Lancet 2(8662):570–572PubMedCrossRefGoogle Scholar
  14. 14.
    Warnock GL, Kneteman NM, Ryan E, et al. (1991) Normoglycaemia after transplantation of freshly isolated and cryopreserved pancreatic islets in type 1 (insulin-dependent) diabetes mellitus. Diabetologia 34:55–58PubMedCrossRefGoogle Scholar
  15. 15.
    Warnock GL, Kneteman NM, Ryan EA, et al. (1992) Long-term follow-up after transplantation of insulin producing pancreatic islets into patients into type 1 (insulin dependent) diabetes mellitus. Diabetologia 35:89–95PubMedCrossRefGoogle Scholar
  16. 16.
    Lakey JR, Warnock GL, Shapiro AM, et al. (1998) Intraductal collagenase delivery into the human using syringe loading or controlled perfusion. Transplant Proc 30:359PubMedCrossRefGoogle Scholar
  17. 17.
    Lakey JR, Warnock GL, Rajotte RV, et al. (1996) Variables in organ donors that affect the recovery of human islets of Langerhans. Transplantation 61:1047–1053PubMedCrossRefGoogle Scholar
  18. 18.
    Cole E, Landsberg D, Russell D, et al. (2001) A pilot study of steroid-free immunosuppression in the prevention of acute rejection in renal allograft recipients. Transplantation 72:845–850PubMedCrossRefGoogle Scholar
  19. 19.
    Walpoth B, Galdikas J, Tschopp A, et al. (1992) Prevention of cardiac allograft rejection by FK506 and rapamycin: assessment by histology and nuclear magnetic resonance. Transpl Int 5(Suppl1):S561–S563PubMedGoogle Scholar
  20. 20.
    Shapiro AM, Lakey JR, Ryan EA, et al. (2000) Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N Engl J Med 343:230–238PubMedCrossRefGoogle Scholar
  21. 21.
    Ryan EA, Breay W, Paty PA, et al. (2005) Five-year follow-up after clinical islet transplantation. Diabetes 54:2060–2069PubMedCrossRefGoogle Scholar
  22. 22.
    Shapiro AM, Ricordi C, Hering BJ, et al. (2006) International trial of the Edmonton Protocol for Islet Transplantation. N Engl J Med 355:1318–1330PubMedCrossRefGoogle Scholar
  23. 23.
    Stock PG, Bluestone JA. (2004) Beta-cell replacement for type I diabetes. Annu Rev Med 55:133–156 [Review]PubMedCrossRefGoogle Scholar
  24. 24.
    Warnock GL, Meloche RM, Thompson D, et al. (2005) Improved human pancreatic islet isolation for a prospective cohort study of islet transplantation vs best medical therapy in type 1 diabetes mellitus. Arch Surg 140:735–744PubMedCrossRefGoogle Scholar
  25. 25.
    Fung MA, Warnock GL, Ao Z, et al. The effect of medical therapy and islet cell transplantation on diabetic nephropathy: an interim report. Transplantation 2007 in pressGoogle Scholar
  26. 26.
    Kondro W. (2006) Fragmented organ donation programs hinder progress. Can Med Assoc J 175:1043CrossRefGoogle Scholar
  27. 27.
    Korbutt GS, Elliott JF, Ao Z, et al. (1996) Large scale isolation, growth, and function of porcine neonatal islet cells. J Clin Invest 97:2119–2129PubMedCrossRefGoogle Scholar
  28. 28.
    Cheung AT, Dayanandan B, Lewis JT, et al. (2000) Glucose-dependent insulin release from genetically engineered K cells. Science 290:1959–1962PubMedCrossRefGoogle Scholar
  29. 29.
    Hussain MA, Theise ND. (2004) Stem-cell therapy for diabetes mellitus. Lancet 364(9429):203–205PubMedCrossRefGoogle Scholar
  30. 30.
    Yang L, Li S, Hatch H, et al. (2002) In vitro trans-differentiation of adult hepatic stem cells into pancreatic endocrine hormone-producing cells. Proc Natl Acad Sci USA 99:8078–8083PubMedCrossRefGoogle Scholar
  31. 31.
    D’Amour KA, Bang AG, Eliazer S, et al. (2006) Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol 24:1392–1401PubMedCrossRefGoogle Scholar
  32. 32.
    Holland AM, Gonez LJ, Harrison LC. (2004) Progenitor cells in the adult pancreas. Diabetes Metab Res Rev 20:13–27PubMedCrossRefGoogle Scholar
  33. 33.
    Bernard-Kargar C, Ktorza A. (2001) Endocrine pancreas plasticity under physiological and pathological conditions. Diabetes 50(Suppl1):S30–S35PubMedCrossRefGoogle Scholar
  34. 34.
    Bonner-Weir S, Taneja M, Weir GC, et al. (2000) In vitro cultivation of human islets from expanded ductal tissue. Proc Natl Acad Sci USA 97:7999–8004PubMedCrossRefGoogle Scholar
  35. 35.
    Dor Y, Brown J, Martinez OI, et al. (2004) Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 429(6987):41–46PubMedCrossRefGoogle Scholar
  36. 36.
    Seaberg RM, Smukler SR, Kieffer TJ, et al. (2004) Clonal identification of multipotent precursors from adult mouse pancreas that generate neural and pancreatic lineages. Nat Biotechnol 22:1115–1124PubMedCrossRefGoogle Scholar
  37. 37.
    Rosenberg L, Brown RA, Duguid WP. (1983) A new approach to the induction of duct epithelial hyperplasia and nesidioblastosis by cellophane wrapping of the hamster pancreas. J Surg Res 35:63–72PubMedCrossRefGoogle Scholar
  38. 38.
    Rosenberg L, Duguid WP, Brown RA, et al. (1988) Induction of nesidioblastosis will reverse diabetes in Syrian golden hamster. Diabetes 37:334–341PubMedCrossRefGoogle Scholar
  39. 39.
    Rosenberg L, Vinik AI, Pittenger GL, et al. (1996) Islet-cell regeneration in the diabetic hamster pancreas by restoration of normoglycaemia can be induced by a local growth factor(s). Diabetologia 39:256–262PubMedGoogle Scholar
  40. 40.
    Rafaeloff R, Pittenger GL, Barlow SW, et al. (1997) Cloning and sequencing of the pancreatic islet neogenesis associated protein (INGAP) gene and its expression in islet neogenesis in hamsters. J Clin Invest 99:2100–2109PubMedGoogle Scholar
  41. 41.
    Rosenberg L, Lipsett M, Yoon JW, et al. (2004) A pentadecapeptide fragment of islet neogenesis-associated protein increases beta-cell mass and reverses diabetes in C57BL/6J mice. Ann Surg 240:875–884PubMedCrossRefGoogle Scholar
  42. 42.
    Pittenger GL, Taylor-Fishwick DA, Johns RH, et al. (2007) Intramuscular injection of islet neogenesis-associated protein peptide stimulates pancreatic islet neogenesis in healthy dogs. Pancreas 34:103–111PubMedCrossRefGoogle Scholar
  43. 43.
    AM Davalli L Scaglia, Zangen DH, et al. (1996) Vulnerability of islets in the immediate posttransplantation period. Dynamic changes in structure and function. Diabetes 45:1161–1167CrossRefGoogle Scholar
  44. 44.
    Yusta B, Baggio LL, Estall JL, et al. (2006) GLP-1 receptor activation improves beta cell function and survival following induction of endoplasmic reticulum stress. Cell Metab 4:391–406PubMedCrossRefGoogle Scholar
  45. 45.
    Wideman RD, Yu IL, Webber TD, et al. (2006) Improving function and survival of pancreatic islets by endogenous production of glucagon-like peptide 1 (GLP-1). Proc Natl Acad Sci USA 103:13468–13473PubMedCrossRefGoogle Scholar
  46. 46.
    Pospisilik JA, Zhou Y-P, Demuth HV, et al. (2002) Long-term treatment with dipeptidyl peptidase IV inhibitor P32/98 causes sustained improvements in glucose tolerance, insulin sensitivity, hyperinsulinemia and β-cell glucose responsiveness in VDF (fa/fa) Zucker rats. Diabetes 51:943–950PubMedCrossRefGoogle Scholar
  47. 47.
    Johnson JD, Bernal-Mizrachi E, Alejandro EU, et al. (2006) Insulin protects islets from apoptosis via Pdx1 and specific changes in the human islet proteome. Proc Natl Acad Sci USA 103:19575–19580PubMedCrossRefGoogle Scholar
  48. 48.
    Movassat J, Beattie GM, Lopez AD, et al. (2003) Exendin 4 up-regulates expression of PDX 1 and hastens differentiation and maturation of human fetal pancreatic cells. J Clin Endocrinol Metab 87:4775–4781CrossRefGoogle Scholar
  49. 49.
    Farilla L, Bulotta A, Hirshberg B, et al. (2003) GLP-1 inhibits cell apoptosis and improves glucose responsiveness of freshly isolated human islets. Endocrinology 144:5149–5158PubMedCrossRefGoogle Scholar
  50. 50.
    Fung MA, Thompson DM, Shapiro J, et al. (2006) Effect of glucagon-like peptide-1 (7–37) on beta cell function after islet transplantation in type 1 diabetes. Diabetes Research Clinical Practice 74:189–193CrossRefGoogle Scholar
  51. 51.
    Al Ghofaili K, Fung MA, Ao Z, et al. (2007) Effect of exenatide on beta cell function after islet transplantation in type 1 diabetes. Transplantation 83:24–28CrossRefGoogle Scholar
  52. 52.
    Wang S, Chen L. (2004) Co-signalling molecules of the B7-CD28 family in positive and negative regulation of T lymphocyte responses. Microbes Infection 6:759–766CrossRefGoogle Scholar
  53. 53.
    Rothstein DM, Sayegh MH. (2003) T-cell costimulatory pathways in allograft rejection and tolerance. Immunol Rev 196:85–108PubMedCrossRefGoogle Scholar
  54. 54.
    Linsley PS, Brady W, Urnes M, et al. (1991) CTLA-4 is a second receptor for the B cell activation antigen B7. J Exp Med 174:561–569PubMedCrossRefGoogle Scholar
  55. 55.
    Gainer AL, Suarez–Pinzon WL, Min W-P, et al. (1998) Improved survival of biolistically transformed mouse islet allografts expressing CTLA-Ig or soluble Fas ligand. Transplantation 66:194–199PubMedCrossRefGoogle Scholar
  56. 56.
    Gainer AL, Korbutt GS, Rajotte RV, et al. (1997) Expression of CTLA-Ig by biolistically transfected mouse islets promotes islet allograft survival. Transplantation 63:1017–1021PubMedCrossRefGoogle Scholar
  57. 57.
    Levisetti MG. (1997) Immunosuppressive effects of human CTLAIg in a non-human primate model of allogeneic pancreatic islet transplantation. J Immunol 159:5187–5191PubMedGoogle Scholar
  58. 58.
    Choi I–H, Zhu G, Sica GL, et al. (2003) Genomic organization and expression analysis of B7-H4, an immune inhibitory molecule of the B7 family. J Immunol 171:4650–4654PubMedGoogle Scholar
  59. 59.
    Sica GL, Choi I-H, Zhu G, et al. (2003) B7-H4, Molecule of the B7 family, negatively regulates T cell immunity. Immunity 18:849–861PubMedCrossRefGoogle Scholar
  60. 60.
    Prasad DVR, Richards S, Mai XM, et al. (2003) B7S1, a novel B7 family member that negatively regulates T cell activation. Immunity 18:863–873PubMedCrossRefGoogle Scholar
  61. 61.
    Zang X, Loke P, Kim J, et al. (2003) B7x: A widely expressed B7 family member that inhibits T cell activation. Proc Natl Acad Sci USA 100:10338–10392CrossRefGoogle Scholar
  62. 62.
    Ou D, Wang X, Metzger DL, et al. (2006) Suppression of human T-cell responses to β cells by activation of B7-H4 pathway. Cell Transplantation 15:399–410PubMedGoogle Scholar
  63. 63.
    Shapiro AM, Hao EG, Lakey JR, et al. (2001) Novel approaches toward early diagnosis of islet allograft rejection. Transplantation 1709–1718Google Scholar
  64. 64.
    Schultz KR, Miklos DB, Fowler D, et al. (2006) Toward biomarkers for chronic graft-versus-host disease: National Institutes of Health consensus development project on criteria for clinical trial in chronic graft-versus-host disease: III Biomarker Working Goup Rport. Biol Blood Marrow Transplant 12:126–137PubMedCrossRefGoogle Scholar
  65. 65.
    Kasthuri RS, Verneris MR, Ibrahim HN, et al. (2006) Studying multiple protein profiles over time to assess biomarker validity. Expert Rev Proteomics 3:455–464PubMedCrossRefGoogle Scholar
  66. 66.
    Chen Y, McKenna GJ, Yoshida EM, et al. (1999) Assessment of immunologic status of liver transplant recipients by peripheral blood mononuclear cells in response to stimulation by donor alloantigen. Ann Surg230:242–250PubMedCrossRefGoogle Scholar

Copyright information

© Société Internationale de Chirurgie 2007

Authors and Affiliations

  • Garth L. Warnock
    • 1
  • Yu Huan Theresa Liao
    • 1
  • Xiaojie Wang
    • 1
  • Dawei Ou
    • 1
  • Ziliang Ao
    • 1
  • James D. Johnson
    • 1
  • C. B. Verchere
    • 1
  • David Thompson
    • 1
  1. 1.Department of SurgeryUniversity of British Columbia Medical CenterVancouverBritish Columbia

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