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Clinical and Developmental Immunology
Volume 2013, Article ID 352315, 13 pages
http://dx.doi.org/10.1155/2013/352315
Review Article

Revascularization of Transplanted Pancreatic Islets and Role of the Transplantation Site

1Clinical Islet Transplant Program, University of Alberta, Edmonton, AB, Canada T6G 2C8
2Department of Surgery, University of Alberta, Edmonton, AB, Canada T6G 2C8
3Medicine and Surgical Oncology, Clinical Islet and Living Donor Liver Transplant Programs, Alberta Innovates-Healthcare Solutions (AIHS), University of Alberta, 2000 College Plaza, 8215-112th Street, Edmonton, AB, Canada T6G 2C8

Received 10 June 2013; Accepted 9 August 2013

Academic Editor: Palmina Petruzzo

Copyright © 2013 Andrew R. Pepper et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. A. Ryan, D. Bigam, and A. M. J. Shapiro, “Current indications for pancreas or islet transplant,” Diabetes, Obesity and Metabolism, vol. 8, no. 1, pp. 1–7, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Vazeou, “Continuous blood glucose monitoring in diabetes treatment,” Diabetes Research and Clinical Practice, vol. 93, no. 1, supplement, pp. S125–S130, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Brissova and A. C. Powers, “Revascularization of transplanted islets: can it be improved?” Diabetes, vol. 57, no. 9, pp. 2269–2271, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. C. Ricordi and T. B. Strom, “Clinical islet transplantation: advances and immunological challenges,” Nature Reviews Immunology, vol. 4, no. 4, pp. 259–268, 2004. View at Google Scholar · View at Scopus
  5. A. M. Shapiro, “A historical perspective on experimental and clinical islet transplantation,” in Islet Transplantation and Beta Cell Replacement Therapy, A. M. Shapiro and J. A. Shaw, Eds., Informa Healthcare, London, UK, 2007. View at Google Scholar
  6. A. A. Chentoufi, V. Geenen, N. Giannokakis, and A. Amrani, “Type 1 diabetes immunological tolerance and immunotherapy,” Clinical and Developmental Immunology, vol. 2011, Article ID 103738, 2 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Merani, C. Toso, J. Emamaullee, and A. M. J. Shapiro, “Optimal implantation site for pancreatic islet transplantation,” British Journal of Surgery, vol. 95, no. 12, pp. 1449–1461, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. G. C. Weir and S. Bonner-Weir, “Islets of Langerhans: the puzzle of intraislet interactions and their relevance to diabetes,” Journal of Clinical Investigation, vol. 85, no. 4, pp. 983–987, 1990. View at Google Scholar · View at Scopus
  9. N. Ballian and F. C. Brunicardi, “Islet vasculature as a regulator of endocrine pancreas function,” World Journal of Surgery, vol. 31, no. 4, pp. 705–714, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. N. Lifson, K. G. Kramlinger, R. R. Mayrand, and E. J. Lender, “Blood flow to the rabbit pancreas with special reference to the islets of Langerhans,” Gastroenterology, vol. 79, no. 3, pp. 466–473, 1980. View at Google Scholar · View at Scopus
  11. P. Langerhans, “Contributions to the microscopic anatomy of the pancreas,” Bulletin of the Institute of the History of Medicine, vol. 5, pp. 1–39, 1937. View at Google Scholar
  12. R. Scharfmann, X. Xiao, H. Heimberg, J. Mallet, and P. Ravassard, “Beta cells within single human islets originate from multiple progenitors,” PloS ONE, vol. 3, no. 10, Article ID e3559, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Brissova, M. J. Fowler, W. E. Nicholson et al., “Assessment of human pancreatic islet architecture and composition by laser scanning confocal microscopy,” Journal of Histochemistry and Cytochemistry, vol. 53, no. 9, pp. 1087–1097, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. O. Cabrera, D. M. Berman, N. S. Kenyon, C. Ricordi, P.-O. Berggren, and A. Caicedo, “The unique cytoarchitecture of human pancreatic islets has implications for islet cell function,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 7, pp. 2334–2339, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. C. N. Street, J. R. T. Lakey, A. M. J. Shapiro et al., “Islet graft assessment in the Edmonton Protocol: implications for predicting long-term clinical outcome,” Diabetes, vol. 53, no. 12, pp. 3107–3114, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. E. Samols and J. I. Stagner, “Intra-islet regulation,” American Journal of Medicine, vol. 85, no. 5, pp. 31–35, 1988. View at Google Scholar · View at Scopus
  17. R. H. Unger, “Glucagon physiology and pathophysiology in the light of new advances,” Diabetologia, vol. 28, no. 8, pp. 574–578, 1985. View at Google Scholar · View at Scopus
  18. P. Schauder, C. McIntosh, and J. Arends, “Somatostatin and insulin release from isolated rat pancreatic islets stimulated by glucose,” FEBS Letters, vol. 68, no. 2, pp. 225–227, 1976. View at Publisher · View at Google Scholar · View at Scopus
  19. J. P. Palmer and D. Porte, “Neural control of glucagon secretion,” in Handbook of Experimental Pharmacology, P. J. Lefebvre, Ed., pp. 115–132, Berlin, Germany, 1982. View at Google Scholar
  20. F. G. Banting and C. H. Best, “The internal secretion of the pancreas,” The Journal of Laboratory and Clinical Medicine, vol. 7, no. 5, pp. 251–266, 1922. View at Google Scholar · View at Scopus
  21. M. Bliss, The Discovery of Insulin, University of Chicago Press, Chicago, Ill, USA, 1982.
  22. K. H. Johnson, T. D. O'Brien, D. W. Hayden et al., “Immunolocalization of islet amyloid polypeptide (IAPP) in pancreatic beta cells by means of peroxidase-antiperoxidase (PAP) and protein A-gold techniques,” American Journal of Pathology, vol. 130, no. 1, pp. 1–8, 1988. View at Google Scholar · View at Scopus
  23. K. J. Potter, A. Abedini, P. Marek et al., “Islet amyloid deposition limits the viability of human islet grafts but not porcine islet grafts,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 9, pp. 4305–4310, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Clark, C. A. Wells, I. D. Buley et al., “Islet amyloid, increased A-cells, reduced B-cells and exocrine fibrosis: quantitative changes in the pancreas in type 2 diabetes,” Diabetes Research, vol. 9, no. 4, pp. 151–159, 1988. View at Google Scholar · View at Scopus
  25. S. R. Bloom and J. M. Polak, “Somatostatin,” British Medical Journal, vol. 295, no. 6593, pp. 288–289, 1987. View at Google Scholar · View at Scopus
  26. D. Grube and R. Bohn, “The microanatomy of human islets of Langerhans, with special reference to somatostatin (D-) cells,” Archivum Histologicum Japonicum, vol. 46, no. 3, pp. 327–353, 1983. View at Google Scholar · View at Scopus
  27. P. In't Veld and M. Marichal, “Microscopic anatomy of the human islet of Langerhans,” Advances in Experimental Medicine and Biology, vol. 654, pp. 1–19, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. N. Wierup, H. Svensson, H. Mulder, and F. Sundler, “The ghrelin cell: a novel developmentally regulated islet cell in the human pancreas,” Regulatory Peptides, vol. 107, no. 1–3, pp. 63–69, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. E. J. P. De Koning, J. J. G. Van Den Brand, V. L. Mott et al., “Macrophages and pancreatic islet amyloidosis,” Amyloid, vol. 5, no. 4, pp. 247–254, 1998. View at Google Scholar · View at Scopus
  30. L. Orci and R. H. Unger, “Functional subdivision of islets of Langerhans and possible role of D cells,” Lancet, vol. 2, no. 7947, pp. 1243–1244, 1975. View at Google Scholar · View at Scopus
  31. F. C. Brunicardi, J. Stagner, S. Bonner-Weir et al., “Microcirculation of the islets of Langerhans. Long Beach Veterans Administration Regional Medical Education Center Symposium,” Diabetes, vol. 45, no. 4, pp. 385–392, 1996. View at Google Scholar · View at Scopus
  32. J. Rahier, R. M. Goebbels, and J. C. Henquin, “Cellular composition of the human diabetic pancreas,” Diabetologia, vol. 24, no. 5, pp. 366–371, 1983. View at Google Scholar · View at Scopus
  33. Y. Stefan, L. Orci, and F. Malaisse-Lagae, “Quantitation of endocrine cell content in the pancreas of nondiabetic and diabetic humans,” Diabetes, vol. 31, no. 8, pp. 694–700, 1982. View at Google Scholar · View at Scopus
  34. S. Bonner-Weir and L. Orci, “New perspectives on the microvasculature of the islets of Langerhans in the rat,” Diabetes, vol. 31, no. 10, pp. 883–889, 1982. View at Google Scholar · View at Scopus
  35. N. Zhang, A. Richter, J. Suriawinata et al., “Elevated vascular endothelial growth factor production in islets improves islet graft vascularization,” Diabetes, vol. 53, no. 4, pp. 963–970, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. A. Golocheikine, V. Tiriveedhi, N. Angaswamy, N. Benshoff, R. Sabarinathan, and T. Mohanakumar, “Cooperative signaling for angiogenesis and neovascularization by VEGF and HGF following islet transplantation,” Transplantation, vol. 90, no. 7, pp. 725–731, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Dubois, A. M. Madec, A. Mesnier et al., “Glucose inhibits angiogenesis of isolated human pancreatic islets,” Journal of Molecular Endocrinology, vol. 45, no. 2, pp. 99–105, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Brissova, M. Fowler, P. Wiebe et al., “Intraislet endothelial cells contribute to revascularization of transplanted pancreatic islets,” Diabetes, vol. 53, no. 5, pp. 1318–1325, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. D. Nyqvist, S. Speier, R. Rodriguez-Diaz et al., “Donor islet endothelial cells in pancreatic islet revascularization,” Diabetes, vol. 60, no. 10, pp. 2571–2577, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. D. Nyqvist, M. Köhler, H. Wahlstedt, and P.-O. Berggren, “Donor islet endothelial cells participate in formation of functional vessels within pancreatic islet grafts,” Diabetes, vol. 54, no. 8, pp. 2287–2293, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. R. Lupi, L. Marselli, S. Dionisi et al., “Improved insulin secretory function and reduced chemotactic properties after tissue culture of islets from type 1 diabetic patients,” Diabetes/Metabolism Research and Reviews, vol. 20, no. 3, pp. 246–251, 2004. View at Publisher · View at Google Scholar · View at Scopus
  42. R. Olsson, A. Maxhuni, and P.-O. Carlsson, “Revascularization of transplanted pancreatic islets following culture with stimulators of angiogenesis,” Transplantation, vol. 82, no. 3, pp. 340–347, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. R. Calne, S. D. Moffatt, P. J. Friend et al., “Campath IH allows low-dose cyclosporine monotherapy in 31 cadaveric renal allograft recipients,” Transplantation, vol. 68, no. 10, pp. 1613–1616, 1999. View at Google Scholar · View at Scopus
  44. N. S. Kenyon, L. A. Fernandez, R. Lehmann et al., “Long-term survival and function of intrahepatic islet allografts in baboons treated with humanized anti-CD154,” Diabetes, vol. 48, no. 7, pp. 1473–1481, 1999. View at Publisher · View at Google Scholar · View at Scopus
  45. J. K. R. A. Rijkelijkhuizen, M. P. M. Van Der Burg, A. Töns, O. T. Terpstra, and E. Bouwman, “Pretransplant culture selects for high-quality porcine islets,” Pancreas, vol. 32, no. 4, pp. 403–407, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. C. Molnar, M. Essand, L. Wennberg, C. Berne, E. Larsson, and G. Tufveson, “Islet engraftment and revascularization in clinical and experimental transplantation,” Cell Transplantation, vol. 22, no. 2, pp. 243–251, 2013. View at Publisher · View at Google Scholar
  47. C. Jahansouz, S. C. Kumer, M. Ellenbogen, and K. L. Brayman, “Evolution of β-cell replacement therapy in diabetes mellitus: pancreas transplantation,” Diabetes Technology and Therapeutics, vol. 13, no. 3, pp. 395–418, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. R. M. Meloche, “Transplantation for the treatment of type 1 diabetes,” World Journal of Gastroenterology, vol. 13, no. 47, pp. 6347–6355, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Henriksnäs, J. Lau, G. Zang, P.-O. Berggren, M. Köhler, and P.-O. Carlsson, “Markedly decreased blood perfusion of pancreatic islets transplanted intraportally into the liver: disruption of islet integrity necessary for islet revascularization,” Diabetes, vol. 61, no. 3, pp. 665–673, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. A. D. Kirk, N. A. Turgeon, and N. N. Iwakoshi, “B cells and transplantation tolerance,” Nature Reviews Nephrology, vol. 6, no. 10, pp. 584–593, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. B. Vasir, J.-C. Jonas, G. M. Steil et al., “Gene expression of VEGF and its receptors Flk-1/KDR and Flt-1 in cultured and transplanted rat islets,” Transplantation, vol. 71, no. 7, pp. 924–935, 2001. View at Google Scholar · View at Scopus
  52. Y. Lai, D. Schneider, A. Kidszun et al., “Vascular endothelial growth factor increases functional β-cell mass by improvement of angiogenesis of isolated human and murine pancreatic islets,” Transplantation, vol. 79, no. 11, pp. 1530–1536, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. U. Johansson, I. Rasmusson, S. P. Niclou et al., “Formation of composite endothelial cell-mesenchymal stem cell islets: a novel approach to promote islet revascularization,” Diabetes, vol. 57, no. 9, pp. 2393–2401, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. Y. Saito, N. K. Chan, and E. Hathout, “Partial hepatectomy improves the outcome of intraportal islet transplantation by promoting revascularization,” Islets, vol. 4, no. 2, pp. 138–144, 2012. View at Publisher · View at Google Scholar
  55. V. Cantaluppi, L. Biancone, G. M. Romanazzi et al., “Antiangiogenic and immunomodulatory effects of rapamycin on islet endothelium: relevance for islet transplantation,” American Journal of Transplantation, vol. 6, no. 11, pp. 2601–2611, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. N. Zhang, D. Su, S. Qu et al., “Sirolimus is associated with reduced islet engraftment and impaired β-cell function,” Diabetes, vol. 55, no. 9, pp. 2429–2436, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. R. Nishimura, S. Nishioka, I. Fujisawa, H. Shiku, M. Shimada, and S. Sekiguchi, “Tacrolimus inhibits the revascularization of isolated pancreatic islets,” PloS ONE, vol. 8, no. 4, Article ID e56799, 2013. View at Publisher · View at Google Scholar
  58. C. B. Kemp, M. J. Knight, and D. W. Scharp, “Effect of transplantation site on the results of pancreatic islet isografts in diabetic rats,” Diabetologia, vol. 9, no. 6, pp. 486–491, 1973. View at Google Scholar · View at Scopus
  59. A. Imagawa, T. Hanafusa, J.-I. Miyagawa, and Y. Matsuzawa, “A novel subtype of type 1 diabetes mellitus characterized by a rapid onset and an absence of diabetes-related antibodies,” New England Journal of Medicine, vol. 342, no. 5, pp. 301–307, 2000. View at Publisher · View at Google Scholar · View at Scopus
  60. W. Bennet, C.-G. Groth, R. Larsson, B. Nilsson, and O. Korsgren, “Isolated human islets trigger an instant blood mediated inflammatory reaction: implications for intraportal islet transplantation as a treatment for patients with type 1 diabetes,” Upsala Journal of Medical Sciences, vol. 105, no. 2, pp. 125–133, 2000. View at Google Scholar · View at Scopus
  61. P.-O. Carlsson, F. Palm, A. Andersson, and P. Liss, “Markedly decreased oxygen tension in transplanted rat pancreatic islets irrespective of the implantation site,” Diabetes, vol. 50, no. 3, pp. 489–495, 2001. View at Google Scholar · View at Scopus
  62. P.-O. Carlsson, F. Palm, A. Andersson, and P. Liss, “Chronically decreased oxygen tension in rat pancreatic islets transplanted under the kidney capsule,” Transplantation, vol. 69, no. 5, pp. 761–766, 2000. View at Google Scholar · View at Scopus
  63. P. Petruzzo, L. Badet, N. Lefrançois et al., “Metabolic consequences of pancreatic systemic or portal venous drainage in simultaneous pancreas-kidney transplant recipients,” Diabetic Medicine, vol. 23, no. 6, pp. 654–659, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. P. De Vos, B. J. De Haan, D. Vegter et al., “Insulin levels after portal and systemic insulin infusion differ in a dose-dependent fashion,” Hormone and Metabolic Research, vol. 30, no. 12, pp. 721–725, 1998. View at Google Scholar · View at Scopus
  65. P. De Vos, D. Vegter, B. J. De Haan, J. H. Strubbe, J. E. Bruggink, and R. Van Schilfgaarde, “Kinetics of intraperitoneally infused insulin in rats: functional implications for the bioartificial pancreas,” Diabetes, vol. 45, no. 8, pp. 1102–1107, 1996. View at Google Scholar · View at Scopus
  66. L. Moberg, A. Olsson, C. Berne et al., “Nicotinamide inhibits tissue factor expression in isolated human pancreatic islets: implications for clinical islet transplantation,” Transplantation, vol. 76, no. 9, pp. 1285–1288, 2003. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Goto, H. Johansson, A. Maeda, G. Elgue, O. Korsgren, and B. Nilsson, “Low molecular weight dextran sulfate prevents the instant blood-mediated inflammatory reaction induced by adult porcine islets,” Transplantation, vol. 77, no. 5, pp. 741–747, 2004. View at Publisher · View at Google Scholar · View at Scopus
  68. L. Özmen, K. N. Ekdahl, G. Elgue, R. Larsson, O. Korsgren, and B. Nilsson, “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, vol. 51, no. 6, pp. 1779–1784, 2002. View at Google Scholar · View at Scopus
  69. S. Cabric, J. Sanchez, T. Lundgren et al., “Islet surface heparinization prevents the instant blood-mediated inflammatory reaction in islet transplantation,” Diabetes, vol. 56, no. 8, pp. 2008–2015, 2007. View at Publisher · View at Google Scholar · View at Scopus
  70. P. T. R. Van Suylichem, J. H. Strubbe, H. Houwing, G. H. J. Wolters, and R. Van Schilfgaarde, “Rat islet isograft function: effect of graft volume and transplantation site,” Transplantation, vol. 57, no. 7, pp. 1010–1017, 1994. View at Google Scholar · View at Scopus
  71. A. Hayek and G. M. Beattie, “Experimental transplantation of human fetal and adult pancreatic islets,” Journal of Clinical Endocrinology and Metabolism, vol. 82, no. 8, pp. 2471–2475, 1997. View at Publisher · View at Google Scholar · View at Scopus
  72. P. E. Lacy, C. Ricordi, and E. H. Finke, “Effect of transplantation site and αL3T4 treatment on survival of rat, hamster, and rabbit islet xenografts in mice,” Transplantation, vol. 47, no. 5, pp. 761–766, 1989. View at Google Scholar · View at Scopus
  73. A. Mellgren, A. H. Schnell Landstrom, B. Petersson, and A. Andersson, “The renal subcapsular site offers better growth conditions for transplanted mouse pancreatic islet cells than the liver or spleen,” Diabetologia, vol. 29, no. 9, pp. 670–672, 1986. View at Google Scholar · View at Scopus
  74. D. Yin, J. W. Ding, J. Shen, L. Ma, M. Hara, and A. S. Chong, “Liver ischemia contributes to early islet failure following intraportal transplantation: benefits of liver ischemic-preconditioning,” American Journal of Transplantation, vol. 6, no. 1, pp. 60–68, 2006. View at Publisher · View at Google Scholar · View at Scopus
  75. R. M. Jindal, R. A. Sidner, H. B. McDaniel, M. S. Johnson, and S. E. Fineberg, “Intraportal versus kidney subcapsular site for human pancreatic islet transplantation,” Transplantation Proceedings, vol. 30, no. 2, pp. 398–399, 1998. View at Publisher · View at Google Scholar · View at Scopus
  76. D. B. Kaufman, P. Morel, M. J. Field, S. R. Munn, and D. E. R. Sutherland, “Purified canine islet autografts. Functional outcome as influenced by islet number and implantation site,” Transplantation, vol. 50, no. 3, pp. 385–391, 1990. View at Google Scholar · View at Scopus
  77. D. W. R. Gray, “Islet isolation and transplantation techniques in the primate,” Surgery Gynecology and Obstetrics, vol. 170, no. 3, pp. 225–232, 1990. View at Google Scholar · View at Scopus
  78. R. Sutton, D. W. R. Gray, M. Burnett, P. McShane, R. C. Turner, and P. J. Morris, “Metabolic function of intraportal and intrasplenic islet autografts in cynomolgus monkeys,” Diabetes, vol. 38, no. 1, supplement, pp. 182–184, 1989. View at Google Scholar · View at Scopus
  79. D. Alderson, J. R. Farndon, K. G. M. M. Alberti, and I. D. A. Johnston, “Islet autotransplantation in the pancreatectomized dog: effect of time on graft function,” World Journal of Surgery, vol. 8, no. 4, pp. 590–597, 1984. View at Google Scholar · View at Scopus
  80. D. Alderson, T. N. Walsh, and J. R. Farndon, “Islet cell transplantation in diabetic dogs: studies of graft function and storage,” British Journal of Surgery, vol. 71, no. 10, pp. 756–760, 1984. View at Google Scholar · View at Scopus
  81. D. C. Wahoff, D. E. R. Sutherland, C. D. Hower et al., “Free intraperitoneal islet autografts in pancreatectomized dogs—impact of islet purity and posttransplantation exogenous insulin,” Surgery, vol. 116, no. 4, pp. 742–750, 1994. View at Google Scholar · View at Scopus
  82. D. C. Wahoff, C. D. Hower, D. E. R. Sutherland, J. P. Leone, and P. F. Gores, “The peritoneal cavity: an alternative site for clinical islet transplantation?” Transplantation Proceedings, vol. 26, no. 6, pp. 3297–3298, 1994. View at Google Scholar · View at Scopus
  83. D. Lorenz, J. Petermann, and R. Beckert, “Transplantation of isologous islets of Langerhans in diabetic rats,” Acta Diabetologica Latina, vol. 12, no. 1, pp. 30–40, 1975. View at Google Scholar · View at Scopus
  84. W. M. Fritschy, J. F. M. Van Straaten, P. De Vos, J. H. Strubbe, G. H. J. Wolters, and R. Van Schilfgaarde, “The efficacy of intraperitoneal pancreatic islet isografts in the reversal of diabetes in rats,” Transplantation, vol. 52, no. 5, pp. 777–783, 1991. View at Google Scholar · View at Scopus
  85. Y. Yasunami, P. E. Lacy, and E. H. Finke, “A new site for islet transplantation: a peritoneal-omental pouch,” Transplantation, vol. 36, no. 2, pp. 181–182, 1983. View at Google Scholar · View at Scopus
  86. T. Kin, G. S. Korbutt, and R. V. Rajotte, “Survival and metabolic function of syngeneic rat islet grafts transplanted in the omental pouch,” American Journal of Transplantation, vol. 3, no. 3, pp. 281–285, 2003. View at Publisher · View at Google Scholar · View at Scopus
  87. N. O. Litbarg, K. P. Gudehithlu, P. Sethupathi, J. A. L. Arruda, G. Dunea, and A. K. Singh, “Activated omentum becomes rich in factors that promote healing and tissue regeneration,” Cell and Tissue Research, vol. 328, no. 3, pp. 487–497, 2007. View at Publisher · View at Google Scholar · View at Scopus
  88. J. Ferguson, R. J. Scothorne, and I. D. Johnston, “Proceedings: the survival of transplanted isolated pancreatic islets in the omentum and testis,” British Journal of Surgery, vol. 60, no. 11, article 907, 1973. View at Google Scholar · View at Scopus
  89. J. Ferguson and R. J. Scothorne, “Extended survival of pancreatic islet allografts in the testis of guinea-pigs,” Journal of Anatomy, vol. 124, no. 1, pp. 1–8, 1977. View at Google Scholar · View at Scopus
  90. J. Lau, G. Mattsson, C. Carlsson et al., “Implantation site-dependent dysfunction of transplanted pancreatic islets,” Diabetes, vol. 56, no. 6, pp. 1544–1550, 2007. View at Publisher · View at Google Scholar · View at Scopus
  91. J. I. Stagner, H. L. Rilo, and K. K. White, “The pancreas as an islet transplantation site. Confirmation in a syngeneic rodent and canine autotransplant model,” Journal of the Pancreas, vol. 8, no. 5, pp. 628–636, 2007. View at Google Scholar · View at Scopus
  92. N. Tchervenivanov, S. Yuan, M. Lipsett, D. Agapitos, and L. Rosenberg, “Morphological and functional studies on submucosal islet transplants in normal and diabetic hamsters,” Cell Transplantation, vol. 11, no. 6, pp. 529–537, 2002. View at Google Scholar · View at Scopus
  93. J. Sageshima, N. Kirchhof, S. Shibata, K. Hiraoka, D. E. R. Sutherland, and B. J. Hering, “Small bowel subserosal space as a site for islet transplantation and local drug delivery,” Transplantation Proceedings, vol. 33, no. 1-2, p. 1710, 2001. View at Publisher · View at Google Scholar · View at Scopus
  94. R. Caiazzo, V. Gmyr, T. Hubert et al., “Evaluation of alternative sites for islet transplantation in the minipig: interest and limits of the gastric submucosa,” Transplantation Proceedings, vol. 39, no. 8, pp. 2620–2623, 2007. View at Publisher · View at Google Scholar · View at Scopus
  95. R. N. Margolis, J. J. Holup, and H. P. Selawry, “Effects of intratesticular islet transplantation on hepatic glycogen metabolism in the rat,” Diabetes Research and Clinical Practice, vol. 2, no. 5, pp. 291–299, 1986. View at Google Scholar · View at Scopus
  96. B. Bobzien, Y. Yasunami, and M. Majercik, “Intratesticular transplants of islet xenografts (rat to mouse),” Diabetes, vol. 32, no. 3, pp. 213–216, 1983. View at Google Scholar · View at Scopus
  97. I. M. Mahmoud, M. M. Gabr, A. F. Refaie, M. A. El-Baz, M. A. Bakr, and M. A. Ghoneim, “Purified murine islet allografts: islet engraftment as influenced by implantation site and glucotoxicity,” Transplantation Proceedings, vol. 30, no. 2, pp. 369–372, 1998. View at Publisher · View at Google Scholar · View at Scopus
  98. A. Refaie, M. Gabr, I. Mahmoud, M. A. Bakr, M. El-Baz, and M. A. Ghoneim, “Experimental islet cell transplantation in rats: optimization of the transplantation site,” Transplantation Proceedings, vol. 30, no. 2, pp. 400–403, 1998. View at Publisher · View at Google Scholar · View at Scopus
  99. H. P. Selawry and D. F. Cameron, “Sertoli cell-enriched fractions in successful islet cell transplantation,” Cell Transplantation, vol. 2, no. 2, pp. 123–129, 1993. View at Google Scholar · View at Scopus
  100. T. Kin, R. V. Rajotte, J. M. Dufour, and G. S. Korbutt, “Development of an immunoprivileged site to prolong islet allograft survival,” Cell Transplantation, vol. 11, no. 6, pp. 547–552, 2002. View at Google Scholar · View at Scopus
  101. W. J. Tze and J. Tai, “Intracerebral allotransplantation of purified pancreatic endocrine cells and pancreatic islets in diabetic rats,” Transplantation, vol. 38, no. 2, pp. 107–111, 1984. View at Google Scholar · View at Scopus
  102. H. C. Lee, K. J. Ahn, S. K. Lim et al., “Allotransplantation of rat islets into the cisterna magna of streptozotocin-induced diabetic rats,” Transplantation, vol. 53, no. 3, pp. 513–516, 1992. View at Google Scholar · View at Scopus
  103. A. M. Posselt, C. F. Barker, J. E. Tomaszewski, J. F. Markmann, M. A. Choti, and A. Naji, “Induction of donor-specific unresponsiveness by intrathymic islet transplantation,” Science, vol. 249, no. 4974, pp. 1293–1295, 1990. View at Google Scholar · View at Scopus
  104. A. M. Posselt, A. Naji, J. H. Roark, J. F. Markmann, and C. F. Barker, “Intrathymic islet transplantation in the spontaneously diabetic BB rat,” Annals of Surgery, vol. 214, no. 4, pp. 363–373, 1991. View at Google Scholar · View at Scopus
  105. M. M. Levy, R. J. Ketchum, J. E. Tomaszewski, A. Naji, C. F. Barker, and K. L. Brayman, “Intrathymic islet transplantation in the canine—I. Histological and functional evidence of autologous intrathymic islet engraftment and survival in pancreatectomized recipients,” Transplantation, vol. 73, no. 6, pp. 842–852, 2002. View at Google Scholar · View at Scopus
  106. G. R. Rayat, G. S. Korbutt, J. F. Elliott, and R. V. Rajotte, “Survival and function of syngeneic rat islet grafts placed within the thymus versus under the kidney capsule,” Cell Transplantation, vol. 6, no. 6, pp. 597–602, 1997. View at Publisher · View at Google Scholar · View at Scopus
  107. P. C. Watt, Y. Mullen, Y. Nomura et al., “Successful engraftment of autologous and allogeneic islets into the porcine thymus,” Journal of Surgical Research, vol. 56, no. 4, pp. 367–371, 1994. View at Publisher · View at Google Scholar · View at Scopus
  108. A. Salazar-Bañuelos, J. Wright, D. Sigalet, and L. Benítez-Bribiesca, “The bone marrow as a potential receptor site for pancreatic Islet grafts,” Archives of Medical Research, vol. 39, no. 1, pp. 139–141, 2008. View at Publisher · View at Google Scholar · View at Scopus
  109. E. Cantarelli, R. Melzi, A. Mercalli et al., “Bone marrow as an alternative site for islet transplantation,” Blood, vol. 114, no. 20, pp. 4566–4574, 2009. View at Publisher · View at Google Scholar · View at Scopus
  110. M. D. Stegall, “Monitoring human islet allografts using a forearm biopsy site,” Annals of Transplantation, vol. 2, no. 3, pp. 8–11, 1997. View at Google Scholar · View at Scopus
  111. X. Chen, X. Zhang, C. Larson, F. Chen, H. Kissler, and D. B. Kaufman, “The epididymal fat pad as a transplant site for minimal islet mass,” Transplantation, vol. 84, no. 1, pp. 122–125, 2007. View at Publisher · View at Google Scholar · View at Scopus
  112. H. C. Outzen and E. H. Leiter, “Transplantation of pancreatic islets into cleared mammary fat pads. A new model,” Transplantation, vol. 32, no. 2, pp. 101–105, 1981. View at Google Scholar · View at Scopus
  113. D. W. Scharp, C. J. Swanson, B. J. Olack et al., “Protection of encapsulated human islets implanted without immunosuppression in patients with type I or type II diabetes and in nondiabetic control subjects,” Diabetes, vol. 43, no. 9, pp. 1167–1170, 1994. View at Google Scholar · View at Scopus
  114. R. Calafiore, “Transplantation of microencapsulated pancreatic human islets for therapy of diabetes mellitus. A preliminary report,” ASAIO Journal, vol. 38, no. 1, pp. 34–37, 1992. View at Google Scholar · View at Scopus
  115. C. K. Leow, D. W. R. Gray, and P. J. Morris, “The long-term metabolic function of intraportal and renal subcapsular islet isografts and the effect on glomerular basement membrane thickness in rats,” Diabetologia, vol. 38, no. 9, pp. 1014–1024, 1995. View at Publisher · View at Google Scholar · View at Scopus
  116. D. W. R. Gray, H. Reece-Smith, and B. Fairbrother, “Isolated pancreatic islet allografts in rats rendered immunologically unresponsive to renal allografts. The effect of the site of transplantation,” Transplantation, vol. 37, no. 5, pp. 434–437, 1984. View at Google Scholar · View at Scopus
  117. B. Hirshberg, S. Montgomery, M. G. Wysoki et al., “Pancreatic islet transplantation using the nonhuman primate (Rhesus) model predicts that the portal vein is superior to the celiac artery as the islet infusion site,” Diabetes, vol. 51, no. 7, pp. 2135–2140, 2002. View at Google Scholar · View at Scopus
  118. D. W. Scharp, P. E. Lacy, J. V. Santiago et al., “Insulin independence after islet transplantation into type I diabetic patient,” Diabetes, vol. 39, no. 4, pp. 515–518, 1990. View at Google Scholar · View at Scopus
  119. B. J. Hering, R. Kandaswamy, J. D. Ansite et al., “Single-donor, marginal-dose islet transplantation in patients with type 1 diabetes,” Journal of the American Medical Association, vol. 293, no. 7, pp. 830–835, 2005. View at Publisher · View at Google Scholar · View at Scopus
  120. A. M. J. Shapiro, J. R. T. Lakey, E. A. Ryan et al., “Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen,” New England Journal of Medicine, vol. 343, no. 4, pp. 230–238, 2000. View at Publisher · View at Google Scholar · View at Scopus
  121. J.-H. Juang, C.-H. Kuo, and B. R.-S. Hsu, “Effects of multiple site implantation on islet transplantation,” Transplantation Proceedings, vol. 34, no. 7, pp. 2698–2699, 2002. View at Publisher · View at Google Scholar · View at Scopus
  122. M. Barbich, S. H. Hyon, M. Dalurzo, V. Dorn, M. Vieiro, and P. Argibay, “The prerenal peritoneum as an alternative site for pancreatic islet transplantation,” Transplantation Proceedings, vol. 29, no. 4, pp. 2055–2056, 1997. View at Publisher · View at Google Scholar · View at Scopus
  123. T. Kobayashi, Y. Aomatsu, H. Iwata et al., “Indefinite islet protection from autoimmune destruction in nonobese diabetic mice by agarose microencapsulation without immunosuppression,” Transplantation, vol. 75, no. 5, pp. 619–625, 2003. View at Publisher · View at Google Scholar · View at Scopus
  124. F. Largiader, E. Kolb, U. Binswanger, and R. Illig, “Successful allotransplantation of an island of Langerhans,” Schweizerische Medizinische Wochenschrift, vol. 109, no. 45, pp. 1733–1736, 1979. View at Google Scholar · View at Scopus
  125. J.-H. Juang, B. R.-S. Hsu, and C.-H. Kuo, “Islet transplantation at subcutaneous and intramuscular sites,” Transplantation Proceedings, vol. 37, no. 8, pp. 3479–3481, 2005. View at Publisher · View at Google Scholar · View at Scopus
  126. J.-H. Juang, S. Bonner-Weir, Y. Ogawa, J. P. Vacanti, and G. C. Weir, “Outcome of subcutaneous islet transplantation improved by polymer device,” Transplantation, vol. 61, no. 11, pp. 1557–1561, 1996. View at Publisher · View at Google Scholar · View at Scopus
  127. D. W. Scharp, P. Marchetti, C. Swanson, M. Newton, C. S. McCullough, and B. Olack, “The effect of transplantation site and islet mass on long-term survival and metabolic and hormonal function of canine purified islet autografts,” Cell Transplantation, vol. 1, no. 2-3, pp. 245–254, 1992. View at Google Scholar · View at Scopus
  128. G. A. Adams, X. Wang, L. K. Lee et al., “Insulin-like growth factor-I promotes successful fetal pancreas transplantation in the intramuscular site,” Surgery, vol. 116, no. 4, pp. 751–757, 1994. View at Google Scholar · View at Scopus
  129. A. N. Balamurugan, Y. Gu, Y. Tabata et al., “Bioartificial pancreas transplantation at prevascularized intermuscular space: effect of angiogenesis induction on islet survival,” Pancreas, vol. 26, no. 3, pp. 279–285, 2003. View at Publisher · View at Google Scholar · View at Scopus
  130. M. Heuser, B. Wolf, B. Vollmar, and M. D. Menger, “Exocrine contamination of isolated islets of Langerhans deteriorates the process of revascularization after free transplantation,” Transplantation, vol. 69, no. 5, pp. 756–761, 2000. View at Google Scholar · View at Scopus
  131. E. Rafael, A. Tibell, M. Rydén et al., “Intramuscular autotransplantation of pancreatic islets in a 7-year-old child: a 2-year follow-up,” American Journal of Transplantation, vol. 8, no. 2, pp. 458–462, 2008. View at Publisher · View at Google Scholar · View at Scopus
  132. A. Salazar-Banuelos, J. R. Wright Jr., D. Sigalet, and L. Benitez-Bribiesca, “Pancreatic islet transplantation into the bone marrow of the rat,” American Journal of Surgery, vol. 195, no. 5, pp. 674–678, 2008. View at Publisher · View at Google Scholar
  133. J. Stagner, B. Ahren, F. Sundler, and K. White, “Reconstructing the pancreas: restoration of normoglycemia, exocrine function, and islet innervation by islet transplantation to the pancreas,” Transplantation Proceedings, vol. 40, no. 2, pp. 452–454, 2008. View at Publisher · View at Google Scholar · View at Scopus
  134. A. Andersson, U. Eriksson, and B. Petersson, “Failure of successful intrasplenic transplantation of islet from lean mice to cure obese-hyperglycemic mice, despite islet growth,” Diabetologia, vol. 20, no. 3, pp. 237–241, 1981. View at Google Scholar · View at Scopus
  135. Y. Cheng, J.-L. Zhang, Y.-F. Liu, T.-M. Li, and N. Zhao, “Islet transplantation for diabetic rats through the spleen,” Hepatobiliary and Pancreatic Diseases International, vol. 4, no. 2, pp. 203–206, 2005. View at Google Scholar · View at Scopus
  136. Z. Ao, K. Matayoshi, J. R. T. Lakey, R. V. Rajotte, and G. L. Warnock, “Survival and function of purified islets in the omental pouch site of outbred dogs,” Transplantation, vol. 56, no. 3, pp. 524–529, 1993. View at Google Scholar · View at Scopus
  137. I. H. Al-Abdullah, M. S. A. Kumar, D. Kelly-Sullivan, and G. M. Abouna, “Site for unpurified islet transplantation is an important parameter for determination of the outcome of graft survival and function,” Cell Transplantation, vol. 4, no. 3, pp. 297–305, 1995. View at Publisher · View at Google Scholar · View at Scopus
  138. K. Federlin, R. G. Bretzel, and U. Schmidtchen, “Islet transplantation in experimental diabetes of the rat—5. Regression of glomerular lesions in diabetic rats after intraportal transplantation of isogeneic islets. Preliminary results,” Hormone and Metabolic Research, vol. 8, no. 5, pp. 404–406, 1976. View at Google Scholar · View at Scopus
  139. A. J. Matas, W. D. Payne, and J. C. Grotting, “Portal versus systemic transplantation of dispersed neonatal pancreas,” Transplantation, vol. 24, no. 5, pp. 333–337, 1977. View at Google Scholar · View at Scopus
  140. I. W. Nasr, Y. Wang, G. Gao et al., “Testicular immune privilege promotes transplantation tolerance by altering the balance between memory and regulatory T cells,” Journal of Immunology, vol. 174, no. 10, pp. 6161–6168, 2005. View at Google Scholar · View at Scopus
  141. J. Arias-Díaz, E. Vara, J. L. Balibrea et al., “CT-guided fine-needle approach for intrathymic islet transplantation in a diabetic patient,” Pancreas, vol. 12, no. 1, pp. 100–102, 1996. View at Google Scholar · View at Scopus