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Journal of Diabetes Research
Volume 2014, Article ID 785948, 9 pages
http://dx.doi.org/10.1155/2014/785948
Review Article

Nonhuman Primate Models of Type 1 Diabetes Mellitus for Islet Transplantation

1Department of Hepatobiliary Surgery, First Affiliated Hospital, Medical College, Xi’an Jiaotong University, Xi’an 710061, China
2Department of Endocrinology, First Affiliated Hospital, Medical College, Xi’an Jiaotong University, Xi’an 710061, China

Received 13 August 2014; Revised 2 October 2014; Accepted 7 October 2014; Published 20 October 2014

Academic Editor: Subrata Chakrabarti

Copyright © 2014 Haitao Zhu 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. J. H. Kim, S.-M. Jin, H. S. Kim, K.-A. Kim, and M.-S. Lee, “Immunotherapeutic treatment of autoimmune diabetes,” Critical Reviews in Immunology, vol. 33, no. 3, pp. 245–281, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. Å. Lernmark and H. E. Larsson, “Immune therapy in type 1 diabetes mellitus,” Nature Reviews Endocrinology, vol. 9, no. 2, pp. 92–103, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. X. Clemente-Casares, S. Tsai, C. Huang, and P. Santamaria, “Antigen-specific therapeutic approaches in type 1 diabetes,” Cold Spring Harbor Perspectives in Medicine, vol. 2, no. 2, Article ID a007773, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. P. R. V. Johnson and K. E. Jones, “Pancreatic islet transplantation,” Seminars in Pediatric Surgery, vol. 21, no. 3, pp. 272–280, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. M. McCall and A. M. J. Shapiro, “Update on islet transplantation,” Cold Spring Harbor Perspectives in Medicine, vol. 2, no. 7, Article ID a007823, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. E. A. Ryan, J. R. T. Lakey, R. V. Rajotte et al., “Clinical outcomes and insulin secretion after islet transplantation with the edmonton protocol,” Diabetes, vol. 50, no. 4, pp. 710–719, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. W. F. Ballinger and P. E. Lacy, “Transplantation of intact pancreatic islets in rats,” Surgery, vol. 72, no. 2, pp. 175–186, 1972. View at Google Scholar · View at Scopus
  8. C. B. Kemp, M. J. Knight, D. W. Scharp, P. E. Lacy, and W. F. Ballinger, “Transplantation of isolated pancreatic islets into the portal vein of diabetic rats,” Nature, vol. 244, no. 5416, p. 447, 1973. View at Publisher · View at Google Scholar · View at Scopus
  9. 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,” The New England Journal of Medicine, vol. 343, no. 4, pp. 230–238, 2000. View at Publisher · View at Google Scholar · View at Scopus
  10. D. D. Lee, E. Grossman, and A. S. Chong, “Cellular therapies for type 1 diabetes,” Hormone and Metabolic Research, vol. 40, no. 2, pp. 147–154, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. D. Dufrane, R.-M. Goebbels, and P. Gianello, “Alginate macroencapsulation of pig islets allows correction of streptozotocin-induced diabetes in primates up to 6 months without immunosuppression,” Transplantation, vol. 90, no. 10, pp. 1054–1062, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. W. Wang, Z. Mo, B. Ye, P. Hu, S. Liu, and S. Yi, “A clinical trial of xenotransplantation of neonatal pig islets for diabetic patients,” Zhong Nan Da Xue Xue Bao Yi Xue Ban, vol. 36, no. 12, pp. 1134–1140, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. P. Thompson, I. R. Badell, M. Lowe et al., “Alternative immunomodulatory strategies for xenotransplantation: CD40/154 pathway-sparing regimens promote xenograft survival,” The American Journal of Transplantation, vol. 12, no. 7, pp. 1765–1775, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. E. Ashkenazi, B. M. Baranovski, G. Shahaf, and E. C. Lewis, “Pancreatic islet xenograft survival in mice is extended by a combination of alpha-1-antitrypsin and single-dose anti-CD4/CD8 therapy,” PLoS ONE, vol. 8, no. 5, Article ID e63625, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Arefanian, E. B. Tredget, R. V. Rajotte, R. G. Gill, G. S. Korbutt, and G. R. Rayat, “Short-term administrations of a combination of anti-LFA-1 and anti-CD154 monoclonal antibodies induce tolerance to neonatal porcine islet xenografts in mice,” Diabetes, vol. 59, no. 4, pp. 958–966, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Tian, Y. Lv, C. Zhai, H. Zhu, L. Yu, and B. Wang, “Alternative immunomodulatory strategies for xenotransplantation: CD80/CD86-CTLA4 pathway-modified immature dendritic cells promote xenograft survival,” PLoS ONE, vol. 8, no. 7, Article ID e69640, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Stanekzai, E. R. Isenovic, and S. A. Mousa, “Treatment options for diabetes: potential role of stem cells,” Diabetes Research and Clinical Practice, vol. 98, no. 3, pp. 361–368, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. N. Lumelsky, O. Blondel, P. Laeng, I. Velasco, R. Ravin, and R. McKay, “Differentiation of embryonic stem cells to insulin-secreting structures similar to pancreatic islets,” Science, vol. 292, no. 5520, pp. 1389–1394, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. S. D. Dave, A. V. Vanikar, H. L. Trivedi, U. G. Thakkar, S. C. Gopal, and T. Chandra, “Novel therapy for insulin-dependent diabetes mellitus: infusion of in vitro-generated insulin-secreting cells,” Clinical and Experimental Medicine, pp. 1–5, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. H. Zhu, L. Yu, and B. Wang, “Progress in isolation and purification of porcine islets,” Chinese Journal of Reparative and Reconstructive Surgery, vol. 26, no. 8, pp. 1012–1016, 2012. View at Google Scholar · View at Scopus
  21. J. D. Carter, S. B. Dula, K. L. Corbin, R. Wu, and C. S. Nunemaker, “A practical guide to rodent islet isolation and assessment,” Biological Procedures Online, vol. 11, no. 1, pp. 3–31, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Matsumoto, H. Noguchi, B. Naziruddin et al., “Improvement of pancreatic islet cell isolation for transplantation,” Proceedings (Baylor University. Medical Center), vol. 20, no. 4, pp. 357–362, 2007. View at Google Scholar
  23. H. T. Zhu, L. Yu, Y. Lyu, and B. Wang, “Optimal pig donor selection in islet xenotransplantation: current status and future perspectives,” Journal of Zhejiang University Science B, vol. 15, no. 8, pp. 681–691, 2014. View at Google Scholar
  24. P. Chhabra and K. L. Brayman, “Current status of immunomodulatory and cellular therapies in preclinical and clinical islet transplantation,” Journal of Transplantation, vol. 2011, Article ID 637692, 24 pages, 2011. View at Publisher · View at Google Scholar
  25. Q. H. Hu, Z. W. Liu, and H. T. Zhu, “Pig islets for islet xenotransplantation: current status and future perspectives,” Chinese Medical Journal, vol. 127, no. 2, pp. 370–377, 2014. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Aguayo-Mazzucato and S. Bonner-Weir, “Stem cell therapy for type 1 diabetes mellitus,” Nature Reviews Endocrinology, vol. 6, no. 3, pp. 139–148, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. N. Sakata, G. Yoshimatsu, H. Tsuchiya, S. Egawa, and M. Unno, “Animal models of diabetes mellitus for islet transplantation,” Experimental diabetes research, vol. 2012, Article ID 256707, 11 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. J.-P. Dehoux and P. Gianello, “The importance of large animal models in transplantation,” Frontiers in Bioscience, vol. 12, no. 13, pp. 4864–4880, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. E. M. Weerts, W. E. Fantegrossi, and A. K. Goodwin, “The value of nonhuman primates in drug abuse research,” Experimental and Clinical Psychopharmacology, vol. 15, no. 4, pp. 309–327, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. J. D. Wagner, J. M. Cline, M. K. Shadoan, B. C. Bullock, S. E. Rankin, and W. T. Cefalu, “Naturally occurring and experimental diabetes in cynomolgus monkeys: a comparison of carbohydrate and lipid metabolism and islet pathology,” Toxicologic Pathology, vol. 29, no. 1, pp. 142–148, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. J. A. Bluestone, K. Herold, and G. Eisenbarth, “Genetics, pathogenesis and clinical interventions in type 1 diabetes,” Nature, vol. 464, no. 7293, pp. 1293–1300, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. H. J. Harwood Jr., P. Listrani, and J. D. Wagner, “Nonhuman primates and other animal models in diabetes research,” Journal of Diabetes Science and Technology, vol. 6, no. 3, pp. 503–514, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. J. D. Wagner, K. Kavanagh, G. M. Ward, B. J. Auerbach, H. J. Harwood Jr., and J. R. Kaplan, “Old world nonhuman primate models of type 2 diabetes mellitus,” ILAR Journal, vol. 47, no. 3, pp. 259–271, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. C. F. Howard Jr., “Nonhuman primates as models for the study of human diabetes mellitus,” Diabetes, vol. 31, no. 1, part 2, pp. 37–44, 1982. View at Google Scholar · View at Scopus
  35. A. D. Kirk, “Transplantation tolerance: a look at the nonhuman primate literature in the light of modern tolerance theories,” Critical Reviews in Immunology, vol. 19, no. 5-6, pp. 349–388, 1999. View at Google Scholar · View at Scopus
  36. S. He, D. Wang, and L. Wei, “Practical and critical instruction for nonhuman primate diabetic models,” Transplantation Proceedings, vol. 45, no. 5, pp. 1856–1865, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. E. L. Röder and P. J. A. Timmermans, “Housing and care of monkeys and apes in laboratories: adaptations allowing essential species-specific behaviour,” Laboratory Animals, vol. 36, no. 3, pp. 221–242, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. G. Laule and M. Whittaker, “Enhancing nonhuman primate care and welfare through the use of positive reinforcement training,” Journal of Applied Animal Welfare Science, vol. 10, no. 1, pp. 31–38, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. S. J. Schapiro and S. P. Lambeth, “Control, choice, and assessments of the value of behavioral management to nonhuman primates in captivity,” Journal of Applied Animal Welfare Science, vol. 10, no. 1, pp. 39–47, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Koulmanda, A. Qipo, Z. Fan et al., “Prolonged survival of allogeneic islets in cynomolgus monkeys after short-term triple therapy,” American Journal of Transplantation, vol. 12, no. 5, pp. 1296–1302, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Marigliano, A. Casu, S. Bertera, M. Trucco, and R. Bottino, “Hemoglobin A1C percentage in nonhuman primates: a useful tool to monitor diabetes before and after porcine pancreatic Islet xenotransplantation,” Journal of Transplantation, vol. 2011, Article ID 965605, 8 pages, 2011. View at Publisher · View at Google Scholar
  42. B. Hirshberg, S. Mog, N. Patterson, J. Leconte, and D. M. Harlan, “Histopathological study of intrahepatic islets transplanted in the nonhuman primate model using edmonton protocol immunosuppression,” Journal of Clinical Endocrinology and Metabolism, vol. 87, no. 12, pp. 5424–5429, 2002. View at Publisher · View at Google Scholar · View at Scopus
  43. E. Pennisi, “Genomicists tackle the primate tree,” Science, vol. 316, no. 5822, pp. 218–221, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Vaccari and G. Franchini, “Memory T cells in rhesus macaques,” Advances in Experimental Medicine and Biology, vol. 684, pp. 126–144, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Blancher, A. Aarnink, K. Tanaka et al., “Study of cynomolgus monkey (Macaca fascicularis) Mhc DRB gene polymorphism in four populations,” Immunogenetics, vol. 64, no. 8, pp. 605–614, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. P. P. M. Rood, L. H. Buhler, R. Bottino, M. Trucco, and D. K. C. Cooper, “Pig-to-nonhuman primate islet xenotransplantation: a review of current problems,” Cell Transplantation, vol. 15, no. 2, pp. 89–104, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. C. R. Abee, K. Mansfield, S. D. Tardif, and T. Morris, Nonhuman Primates in Biomedical Research: Diseases, Elsevier Science, Amsterdam, The Netherlands, 2012.
  48. D. Cheţa, “Animal models of type I (insulin-dependent) diabetes mellitus,” Journal of Pediatric Endocrinology and Metabolism, vol. 11, no. 1, pp. 11–19, 1998. View at Google Scholar · View at Scopus
  49. B. Tyrberg, A. Andersson, and L. A. Borg, “Species differences in susceptibility of transplanted and cultured pancreatic islets to the β-cell toxin alloxan,” General and Comparative Endocrinology, vol. 122, no. 3, pp. 238–251, 2001. View at Publisher · View at Google Scholar · View at Scopus
  50. T. Szkudelski, “The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas,” Physiological Research, vol. 50, no. 6, pp. 537–546, 2001. View at Google Scholar · View at Scopus
  51. C. E. Mathews, S. H. Langley, and E. H. Leiter, “New mouse model to study islet transplantation in insulin-dependent diabetes mellitus,” Transplantation, vol. 73, no. 8, pp. 1333–1336, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. A. V. Matveyenko and P. C. Butler, “Islet amyloid polypeptide (IAPP) transgenic rodents as models for type 2 diabetes,” ILAR Journal, vol. 47, no. 3, pp. 225–233, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. A. A. Viehmann Milam, S. E. Maher, J. A. Gibson et al., “A humanized mouse model of autoimmune insulitis,” Diabetes, vol. 63, no. 5, pp. 1712–1724, 2014. View at Publisher · View at Google Scholar · View at Scopus
  54. A. W. S. Chan, “Progress and prospects for genetic modification of nonhuman primate models in biomedical research,” ILAR Journal, vol. 54, no. 2, Article ID ilt035, pp. 211–223, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. S.-H. Yang, P.-H. Cheng, H. Banta et al., “Towards a transgenic model of Huntington's disease in a non-human primate,” Nature, vol. 453, no. 7197, pp. 921–924, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. Y. Niu, Y. Yu, A. Bernat et al., “Transgenic rhesus monkeys produced by gene transfer into early-cleavage-stage embryos using a simian immunodeficiency virus-based vector,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 41, pp. 17663–17667, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. D. A. Rees and J. C. Alcolado, “Animal models of diabetes mellitus,” Diabetic Medicine, vol. 22, no. 4, pp. 359–370, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. J. Gillman, C. Gilbert, and J. C. Allan, “The relationship of hyperglycaemia to hyperlipaemia and ketonaemia in depancreatized baboons (Papio ursinus),” Journal of Endocrinology, vol. 17, no. 4, pp. 349–362, 1958. View at Google Scholar
  59. J. Gillman, C. Gilbert, E. Epstein, and J. C. Allan, “Endocrine control of blood sugar, lipaemia, and ketonaemia in diabetic,” British Medical Journal, vol. 2, no. 5107, pp. 1260–1263, 1958. View at Publisher · View at Google Scholar · View at Scopus
  60. J. L. Buss, E. Essig, K. Osei, S. Brodsky, G. Hadley, and A. Rajab, “Steroid-free maintenance of islet allografts using mycophenolate mofetil and cyclosporine in the nonhuman primate,” Annals of Transplantation, vol. 16, no. 2, pp. 88–97, 2011. View at Google Scholar · View at Scopus
  61. M. Watanabe, K. Yamashita, T. Suzuki et al., “ASKP1240, a fully human anti-CD40 monoclonal antibody, prolongs pancreatic islet allograft survival in nonhuman primates,” American Journal of Transplantation, vol. 13, no. 8, pp. 1976–1988, 2013. View at Publisher · View at Google Scholar · View at Scopus
  62. T. Yoshida, T. Suzuki, M. Watanabe et al., “Induction of insulin-dependent diabetes mellitus by total pancreatectomy for pancreatic islet transplantation in cynomolgus monkeys,” Journal of Hepato-Biliary-Pancreatic Sciences, vol. 19, no. 6, pp. 661–666, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. 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
  64. N. S. Kenyon, M. Chatzipetrou, M. Masetti et al., “Long-term survival and function of intrahepatic islet allografts in rhesus monkeys treated with humanized anti-CD154,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 14, pp. 8132–8137, 1999. View at Publisher · View at Google Scholar · View at Scopus
  65. D. W. R. Gray, G. L. Warnock, R. Sutton, M. Peters, P. McShane, and P. J. Morris, “Successful autotransplantation of isolated islets of Langerhans in the cynomolgus monkey,” British Journal of Surgery, vol. 73, no. 10, pp. 850–853, 1986. View at Publisher · View at Google Scholar · View at Scopus
  66. K. Cardona, Z. Milas, E. Strobert et al., “Engraftment of adult porcine islet xenografts in diabetic nonhuman primates through targeting of costimulation pathways,” The American Journal of Transplantation, vol. 7, no. 10, pp. 2260–2268, 2007. View at Publisher · View at Google Scholar · View at Scopus
  67. P. Thompson, K. Cardona, M. Russell et al., “CD40-specific costimulation blockade enhances neonatal porcine islet survival in nonhuman primates,” The American Journal of Transplantation, vol. 11, no. 5, pp. 947–957, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. B.-G. Ericzon, R. M. H. Wijnen, K. Kubota, A. V. D. Bogaard, and G. Kootstra, “Diabetes induction and pancreatic transplantation in the cynomolgus monkey: methodological considerations,” Transplant International, vol. 4, no. 2, pp. 103–109, 1991. View at Publisher · View at Google Scholar · View at Scopus
  69. S. He, Y. Chen, L. Wei et al., “Treatment and risk factor analysis of hypoglycemia in diabetic rhesus monkeys,” Experimental Biology and Medicine, vol. 236, no. 2, pp. 212–218, 2011. View at Publisher · View at Google Scholar · View at Scopus
  70. Y. Zhang, L. Fu, Y.-R. Lu et al., “Pancreas anatomy and surgical procedure for pancreatectomy in rhesus monkeys,” Journal of Medical Primatology, vol. 40, no. 6, pp. 376–382, 2011. View at Publisher · View at Google Scholar · View at Scopus
  71. C. F. Qiao, B. L. Tian, G. Mai et al., “Induction of diabetes in rhesus monkeys and establishment of insulin administration strategy,” Transplantation Proceedings, vol. 41, no. 1, pp. 413–417, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. S. Lenzen, “The mechanisms of alloxan- and streptozotocin-induced diabetes,” Diabetologia, vol. 51, no. 2, pp. 216–226, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. J. Frame, D. Kelsen, N. Kemeny et al., “A phase II trial of streptozotocin and adriamycin in advanced APUD tumors,” American Journal of Clinical Oncology, vol. 11, no. 4, pp. 490–495, 1988. View at Google Scholar · View at Scopus
  74. J. Naidoo, D. O'Toole, M. J. Kennedy, J. V. Reynolds, M. O'Connor, and K. O'Byrne, “A single institution experience of streptozocin/fluorouracil combination chemotherapy: a case series,” Irish Journal of Medical Science, vol. 181, no. 2, pp. 211–214, 2012. View at Publisher · View at Google Scholar · View at Scopus
  75. C. O. Eleazu, K. C. Eleazu, S. Chukwuma, and U. N. Essien, “Review of the mechanism of cell death resulting from streptozotocin challenge in experimental animals, its practical use and potential risk to humans,” Journal of Diabetes & Metabolic Disorders, vol. 12, article 60, 2013. View at Publisher · View at Google Scholar
  76. K. Cardona, G. S. Korbutt, Z. Milas et al., “Long-term survival of neonatal porcine islets in nonhuman primates by targeting costimulation pathways,” Nature Medicine, vol. 12, no. 3, pp. 304–306, 2006. View at Publisher · View at Google Scholar · View at Scopus
  77. P. Thompson, I. R. Badell, M. Lowe et al., “Islet xenotransplantation using gal-deficient neonatal donors improves engraftment and function,” American Journal of Transplantation, vol. 11, no. 12, pp. 2593–2602, 2011. View at Publisher · View at Google Scholar · View at Scopus
  78. M. Koulmanda, A. Qipo, S. Chebrolu, J. O'Neil, H. Auchincloss Jr., and R. N. Smith, “The effect of low versus high dose of streptozotocin in cynomolgus monkeys (Macaca fascilularis),” American Journal of Transplantation, vol. 3, no. 3, pp. 267–272, 2003. View at Publisher · View at Google Scholar · View at Scopus
  79. R. Bottino, A. Criscimanna, A. Casu et al., “Recovery of endogenous β-cell function in nonhuman primates after chemical diabetes induction and islet transplantation,” Diabetes, vol. 58, no. 2, pp. 442–447, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. M. C. Deeds, J. M. Anderson, A. S. Armstrong et al., “Single dose streptozotocin-induced diabetes: considerations for study design in islet transplantation models,” Laboratory Animals, vol. 45, no. 3, pp. 131–140, 2011. View at Publisher · View at Google Scholar · View at Scopus
  81. M. L. Graham, L. A. Mutch, E. F. Rieke et al., “Refining the high-dose streptozotocin-induced diabetic non-human primate model: an evaluation of risk factors and outcomes,” Experimental Biology and Medicine, vol. 236, no. 10, pp. 1218–1230, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. B. R. Theriault, J. R. Thistlethwaite Jr., M. G. Levisetti et al., “Induction, maintenance, and reversal, of streptozotocin-induced insulin- dependent diabetes mellitus in the juvenile cynomolgus monkey (Macaca fascilularis),” Transplantation, vol. 68, no. 3, pp. 331–337, 1999. View at Publisher · View at Google Scholar · View at Scopus
  83. M. Lowe, I. R. Badell, P. Thompson et al., “A novel monoclonal antibody to CD40 prolongs islet allograft survival,” The American Journal of Transplantation, vol. 12, no. 8, pp. 2079–2087, 2012. View at Publisher · View at Google Scholar · View at Scopus
  84. I. R. Badell, M. C. Russell, K. Cardona et al., “CTLA4Ig prevents alloantibody formation following nonhuman primate islet transplantation using the CD40-specific antibody 3A8,” American Journal of Transplantation, vol. 12, no. 7, pp. 1918–1923, 2012. View at Publisher · View at Google Scholar · View at Scopus
  85. D. J. Van Der Windt, R. Bottino, A. Casu et al., “Long-term controlled normoglycemia in diabetic non-human primates after transplantation with hCD46 transgenic porcine islets,” The American Journal of Transplantation, vol. 9, no. 12, pp. 2716–2726, 2009. View at Publisher · View at Google Scholar · View at Scopus
  86. G. Hecht, S. Eventov-Friedman, C. Rosen et al., “Embryonic pig pancreatic tissue for the treatment of diabetes in a nonhuman primate model,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 21, pp. 8659–8664, 2009. View at Publisher · View at Google Scholar · View at Scopus
  87. M. Wijkstrom, N. Kirchhof, M. Graham et al., “Cyclosporine toxicity in immunosuppressed streptozotocin-diabetic nonhuman primates,” Toxicology, vol. 207, no. 1, pp. 117–127, 2005. View at Publisher · View at Google Scholar · View at Scopus
  88. K. Hayashi, R. Kojima, and M. Ito, “Strain differences in the diabetogenic activity of streptozotocin in mice,” Biological and Pharmaceutical Bulletin, vol. 29, no. 6, pp. 1110–1119, 2006. View at Publisher · View at Google Scholar · View at Scopus
  89. R. M. Pitkin and W. A. Reynolds, “Diabetogenic effects of streptozotocin in rhesus monkeys,” Diabetes, vol. 19, no. 2, pp. 85–90, 1970. View at Google Scholar · View at Scopus
  90. K. N. Litwak, W. T. Cefalu, and J. D. Wagner, “Streptozotocin-induced diabetes mellitus in cynomolgus monkeys: changes in carbohydrate metabolism, skin glycation, and pancreatic islets,” Laboratory Animal Science, vol. 48, no. 2, pp. 172–178, 1998. View at Google Scholar · View at Scopus
  91. P. P. M. Rood, R. Bottino, A. N. Balamurugan et al., “Induction of diabetes in cynomolgus monkeys with high-dose streptozotocin: adverse effects and early responses,” Pancreas, vol. 33, no. 3, pp. 287–292, 2006. View at Publisher · View at Google Scholar · View at Scopus
  92. S. Shibata, N. Kirchhof, S. Matsumoto et al., “High-dose streptozotocin for diabetes induction in adult rhesus monkeys,” Transplantation Proceedings, vol. 34, no. 4, pp. 1341–1344, 2002. View at Publisher · View at Google Scholar · View at Scopus
  93. X. Jin, L. Zeng, S. He et al., “Comparison of single high-dose streptozotocin with partial pancreatectomy combined with low-dose streptozotocin for diabetes induction in rhesus monkeys,” Experimental Biology and Medicine, vol. 235, no. 7, pp. 877–885, 2010. View at Publisher · View at Google Scholar · View at Scopus
  94. D. Dufrane, M. Van Steenberghe, Y. Guiot, R.-M. Goebbels, A. Saliez, and P. Gianello, “Streptozotocin-induced diabetes in large animals (pigs/primates): role of GLUT2 transporter and β-cell plasticity,” Transplantation, vol. 81, no. 1, pp. 36–45, 2006. View at Publisher · View at Google Scholar · View at Scopus
  95. M. G. Tal, B. Hirshberg, Z. Neeman et al., “Induction of diabetes in nonhuman primates by means of temporary arterial embolization and selective arterial injection of streptozotocin,” Radiology, vol. 230, no. 1, pp. 163–168, 2004. View at Publisher · View at Google Scholar · View at Scopus
  96. C. L. Zou, J. Y. Wang, S. Y. Wang et al., “Characterizing the induction of diabetes in juvenile cynomolgus monkeys with different doses of streptozotocin,” Science China Life Sciences, vol. 55, no. 3, pp. 210–218, 2012. View at Publisher · View at Google Scholar · View at Scopus
  97. I. R. Badell, M. C. Russell, P. W. Thompson et al., “LFA-1 - Specific therapy prolongs allograft survival in rhesus macaques,” Journal of Clinical Investigation, vol. 120, no. 12, pp. 4520–4531, 2010. View at Publisher · View at Google Scholar · View at Scopus
  98. C. Polychronakos, “Animal models of spontaneous autoimmune diabetes: notes on their relevance to the human disease,” Current Diabetes Reports, vol. 4, no. 2, pp. 151–154, 2004. View at Publisher · View at Google Scholar · View at Scopus
  99. B. J. Whalen, J. P. Mordes, and A. A. Rossini, “The BB rat as a model of human insulin-dependent diabetes mellitus,” in Current Protocols in Immunology, chapter 15, unit 15.3, 2001. View at Publisher · View at Google Scholar
  100. M. S. Anderson and J. A. Bluestone, “The NOD mouse: a model of immune dysregulation,” Annual Review of Immunology, vol. 23, pp. 447–485, 2005. View at Publisher · View at Google Scholar · View at Scopus
  101. S. M. Cabrera, M. R. Rigby, and R. G. Mirmira, “Targeting regulatory T cells in the treatment of type 1 diabetes mellitus,” Current Molecular Medicine, vol. 12, no. 10, pp. 1261–1272, 2012. View at Publisher · View at Google Scholar · View at Scopus
  102. M. Wang, J. Racine, M. Zhang et al., “MHC-mismatched chimerism is required for induction of transplantation tolerance in autoimmune nonobese diabetic recipients,” The Journal of Immunology, vol. 193, no. 4, pp. 2005–2015, 2014. View at Google Scholar
  103. R. Deng, M. Khattar, A. Xie et al., “Anti-TCR mab induces peripheral tolerance to alloantigens and delays islet allograft rejection in autoimmune diabetic nod mice,” Transplantation, vol. 97, no. 12, pp. 1216–1224, 2014. View at Publisher · View at Google Scholar · View at Scopus
  104. Q. Shi, D. Wang, G. A. Hadley, A. W. Bingaman, S. T. Bartlett, and D. L. Farber, “Long-term islet graft survival in NOD mice by abrogation of recurrent autoimmunity,” Diabetes, vol. 53, no. 9, pp. 2338–2345, 2004. View at Publisher · View at Google Scholar · View at Scopus
  105. F. T. Thomas, K. Pittman, and J. M. Thomas, “Induction of functional xenograft tolerance of pig islets in the autoimmune NOD mouse,” Transplantation Proceedings, vol. 27, no. 6, pp. 3323–3325, 1995. View at Google Scholar · View at Scopus
  106. M. Wijkstrom, R. Bottino, and D. K. C. Cooper, “Limitations of the pig-to-non-human primate islet transplantation model,” Xenotransplantation, vol. 20, no. 1, pp. 2–4, 2013. View at Publisher · View at Google Scholar · View at Scopus
  107. A. Casu, R. Bottino, A. N. Balamurugan et al., “Metabolic aspects of pig-to-monkey (Macaca fascicularis) islet transplantation: implications for translation into clinical practice,” Diabetologia, vol. 51, no. 1, pp. 120–129, 2008. View at Publisher · View at Google Scholar · View at Scopus
  108. M. L. Graham, M. D. Bellin, K. K. Papas, B. J. Hering, and H.-J. Schuurman, “Species incompatibilities in the pig-to-macaque islet xenotransplant model affect transplant outcome: a comparison with allotransplantation,” Xenotransplantation, vol. 18, no. 6, pp. 328–342, 2011. View at Publisher · View at Google Scholar · View at Scopus
  109. M. L. Graham and H.-J. Schuurman, “The usefulness and limitations of the diabetic macaque model in evaluating long-term porcine islet xenograft survival,” Xenotransplantation, vol. 20, no. 1, pp. 5–17, 2013. View at Publisher · View at Google Scholar · View at Scopus