Table of Contents Author Guidelines Submit a Manuscript
Journal of Diabetes Research
Volume 2013, Article ID 138412, 8 pages
http://dx.doi.org/10.1155/2013/138412
Review Article

Rodent Models for Investigating the Dysregulation of Immune Responses in Type 1 Diabetes

1Department and Graduate Institute of Microbiology and Immunology, National Defense Medical Center, R8324, 161, Section 6, MinChuan East Road, Neihu, Taipei 114, Taiwan
2Department of Pediatrics, Tri-Service General Hospital, 325, Section 2, Chenggong Road, Neihu, Taipei 114, Taiwan
3Laboratory Animal Center, National Defense Medical Center, Taipei 114, Taiwan

Received 23 December 2012; Accepted 7 February 2013

Academic Editor: Norihide Yokoi

Copyright © 2013 Feng-Cheng Chou 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. K. M. Gillespie, “Type 1 diabetes: pathogenesis and prevention,” Canadian Medical Association Journal, vol. 175, no. 2, pp. 165–170, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Karvonen, M. Viik-Kajander, E. Moltchanova, I. Libman, R. LaPorte, and J. Tuomilehto, “Incidence of childhood type 1 diabetes worldwide,” Diabetes Care, vol. 23, no. 10, pp. 1516–1526, 2000. View at Google Scholar · View at Scopus
  3. EURODIAB ACE Study Group, “Variation and trends in incidence of childhood diabetes in Europe,” The Lancet, vol. 355, no. 9207, pp. 873–876, 2000. View at Publisher · View at Google Scholar · View at Scopus
  4. V. Harjutsalo, L. Sjöberg, and J. Tuomilehto, “Time trends in the incidence of type 1 diabetes in Finnish children: a cohort study,” The Lancet, vol. 371, no. 9626, pp. 1777–1782, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. J. P. Mordes, R. Bortell, J. Doukas et al., “The BB/Wor rat and the balance hypothesis of autoimmunity,” Diabetes/Metabolism Reviews, vol. 12, no. 2, pp. 103–109, 1996. View at Google Scholar · View at Scopus
  6. K. Komeda, M. Noda, K. Terao, N. Kuzuya, M. Kanazawa, and Y. Kanazawa, “Establishment of two substrains, diabetes-prone and non-diabetic, from Long-Evans Tokushima Lean (LETL) rats,” Endocrine Journal, vol. 45, no. 6, pp. 737–744, 1998. View at Google Scholar · View at Scopus
  7. S. Lenzen, M. Tiedge, M. Elsner et al., “The LEW.1AR1/Ztm-iddm rat: a new model of spontaneous insulin-dependent diabetes mellitus,” Diabetologia, vol. 44, no. 9, pp. 1189–1196, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. K. E. Ellerman and A. A. Like, “Susceptibility to diabetes is widely distributed in normal class II(u) haplotype rats,” Diabetologia, vol. 43, no. 7, pp. 890–898, 2000. View at Google Scholar · View at Scopus
  9. S. Makino, K. Kunimoto, Y. Muraoka, Y. Mizushima, K. Katagiri, and Y. Tochino, “Breeding of a non-obese, diabetic strain of mice,” Experimental Animals, vol. 29, no. 1, pp. 1–13, 1980. View at Google Scholar · View at Scopus
  10. 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
  11. R. Tisch and H. McDevitt, “Insulin-dependent diabetes mellitus,” Cell, vol. 85, no. 3, pp. 291–297, 1996. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Hattori, J. B. Buse, R. A. Jackson et al. et al., “The NOD mouse: recessive diabetogenic gene in the major histocompatibility complex,” Science, vol. 231, no. 4739, pp. 733–735, 1986. View at Google Scholar · View at Scopus
  13. H. Acha-Orbea and H. O. McDevitt, “The first external domain of the nonobese diabetic mouse class II I-A β chain is unique,” Proceedings of the National Academy of Sciences of the United States of America, vol. 84, no. 8, pp. 2435–2439, 1987. View at Google Scholar · View at Scopus
  14. O. Kanagawa, S. M. Martin, B. A. Vaupel, E. Carrasco-Marin, and E. R. Unanue, “Autoreactivity of T cells from nonobese diabetic mice: an I-Ag7-dependent reaction,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 4, pp. 1721–1724, 1998. View at Google Scholar · View at Scopus
  15. A. Jansen, F. Homo-Delarche, H. Hooijkaas, P. J. Leenen, M. Dardenne, and H. A. Drexhage, “Immunohistochemical characterization of monocytes-macrophages and dendritic cells involved in the initiation of the insulitis and β-cell destruction in NOD mice,” Diabetes, vol. 43, no. 5, pp. 667–675, 1994. View at Google Scholar · View at Scopus
  16. T. L. Delovitch and B. Singh, “The nonobese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD,” Immunity, vol. 7, no. 6, pp. 727–738, 1997. View at Publisher · View at Google Scholar · View at Scopus
  17. X. Su, Q. Hu, J. M. Kristan et al., “Significant role for Fas in the pathogenesis of autoimmune diabetes,” Journal of Immunology, vol. 164, no. 5, pp. 2523–2532, 2000. View at Google Scholar · View at Scopus
  18. D. G. Silva, N. Petrovsky, L. Socha, R. Slattery, P. Gatenby, and B. Charlton, “Mechanisms of accelerated immune-mediated diabetes resulting from islet β cell expression of a Fas ligand transgene,” Journal of Immunology, vol. 170, no. 10, pp. 4996–5002, 2003. View at Google Scholar · View at Scopus
  19. A. V. Chervonsky, Y. Wang, F. S. Wong et al., “The role of Fas in autoimmune diabetes,” Cell, vol. 89, no. 1, pp. 17–24, 1997. View at Google Scholar · View at Scopus
  20. H. H. Sung, J. H. Juang, Y. C. Lin et al., “Transgenic expression of decoy receptor 3 protects islets from spontaneous and chemical-induced autoimmune destruction in nonobese diabetic mice,” Journal of Experimental Medicine, vol. 199, no. 8, pp. 1143–1151, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. R. M. Pitti, S. A. Marsters, D. A. Lawrence et al., “Genomic amplification of a decoy receptor for Fas ligand in lung and colon cancer,” Nature, vol. 396, no. 6712, pp. 699–703, 1998. View at Publisher · View at Google Scholar · View at Scopus
  22. W. Gao, G. Demirci, and X. C. Li, “Negative T cell costimulation and islet tolerance,” Diabetes/Metabolism Research and Reviews, vol. 19, no. 3, pp. 179–185, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. C. J. Wang, F. C. Chou, C. H. Chu et al., “Protective role of programmed death 1 ligand 1 (PD-L1) in nonobese diabetic mice: the paradox in transgenic models,” Diabetes, vol. 57, no. 7, pp. 1861–1869, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. S. J. Shieh, F. C. Chou, P. N. Yu et al., “Transgenic expression of single-chain anti-CTLA-4 Fv on β cells protects nonobese diabetic mice from autoimmune diabetes,” Journal of Immunology, vol. 183, no. 4, pp. 2277–2285, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. S. K. Subudhi, P. Zhou, L. M. Yerian et al., “Local expression of B7-H1 promotes organ-specific autoimmunity and transplant rejection,” Journal of Clinical Investigation, vol. 113, no. 5, pp. 694–700, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. J. Yantha, H. Tsui, S. Winer et al., “Unexpected acceleration of type 1 diabetes by transgenic expression of B7-H1 in NOD mouse peri-islet glia,” Diabetes, vol. 59, no. 10, pp. 2588–2596, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Wong, S. Guerder, I. Visintin et al., “Expression of the co-stimulator molecule B7-1 in pancreatic β-cells accelerates diabetes in the NOD mouse,” Diabetes, vol. 44, no. 3, pp. 326–329, 1995. View at Google Scholar · View at Scopus
  28. H. K. Sytwu, W. D. Lin, S. R. Roffler et al., “Anti-4-1BB-based immunotherapy for autoimmune diabetes: lessons from a transgenic non-obese diabetic (NOD) model,” Journal of Autoimmunity, vol. 21, no. 3, pp. 247–254, 2003. View at Publisher · View at Google Scholar · View at Scopus
  29. R. Mueller, T. Krahl, and N. Sarvetnick, “Pancreatic expression of interleukin-4 abrogates insulitis and autoimmune diabetes in nonobese diabetic (NOD) mice,” Journal of Experimental Medicine, vol. 184, no. 3, pp. 1093–1099, 1996. View at Google Scholar · View at Scopus
  30. I. S. Grewal, K. D. Grewal, F. S. Wong et al., “Expression of transgene encoded TGF-β in islets prevents autoimmune diabetes in NOD mice by a local mechanism,” Journal of Autoimmunity, vol. 19, no. 1-2, pp. 9–22, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Moritani, K. Yoshimoto, S. F. Wong et al., “Abrogation of autoimmune diabetes in nonobese diabetic mice and protection against effector lymphocytes by transgenic paracrine TGF-β1,” Journal of Clinical Investigation, vol. 102, no. 3, pp. 499–506, 1998. View at Google Scholar · View at Scopus
  32. L. Wogensen, M. S. Lee, and N. Sarvetnick, “Production of interleukin 10 by islet cells accelerates immune-mediated destruction of β cells in nonobese diabetic mice,” Journal of Experimental Medicine, vol. 179, no. 4, pp. 1379–1384, 1994. View at Google Scholar · View at Scopus
  33. L. A. Stephens and T. W. H. Kay, “Pancreatic expression of B7 co-stimulatory molecules in the non-obese diabetic mouse,” International Immunology, vol. 7, no. 12, pp. 1885–1895, 1995. View at Google Scholar · View at Scopus
  34. X. X. Zheng, A. W. Steele, W. W. Hancock et al., “A noncytolytic IL-10/Fc fusion protein prevents diabetes, blocks autoimmunity, and promotes suppressor phenomena in NOD mice,” Journal of Immunology, vol. 158, no. 9, pp. 4507–4513, 1997. View at Google Scholar · View at Scopus
  35. K. J. Pennline, E. R. Roque-Gaffney, and M. Monahan, “Recombinant human IL-10 prevents the onset of diabetes in the nonobese diabetic mouse,” Clinical Immunology and Immunopathology, vol. 71, no. 2, pp. 169–175, 1994. View at Publisher · View at Google Scholar · View at Scopus
  36. L. W. Collison, C. J. Workman, T. T. Kuo et al., “The inhibitory cytokine IL-35 contributes to regulatory T-cell function,” Nature, vol. 450, no. 7169, pp. 566–569, 2007. View at Publisher · View at Google Scholar
  37. M. Bettini, A. H. Castellaw, G. P. Lennon, A. R. Burton, and D. A. Vignali, “Prevention of autoimmune diabetes by ectopic pancreatic β-cell expression of interleukin-35,” Diabetes, vol. 61, no. 6, pp. 1519–1526, 2012. View at Publisher · View at Google Scholar
  38. A. P. Martin, M. G. Grisotto, C. Canasto-Chibuque et al., “Islet expression of M3 uncovers a key role for chemokines in the development and recruitment of diabetogenic cells in NOD mice,” Diabetes, vol. 57, no. 2, pp. 387–394, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. G. J. Lin, S. H. Huang, Y. W. Chen et al., “Transgenic expression of murine chemokine decoy receptor D6 by islets reveals the role of inflammatory CC chemokines in the development of autoimmune diabetes in NOD mice,” Diabetologia, vol. 54, no. 7, pp. 1777–1787, 2011. View at Publisher · View at Google Scholar
  40. A. Amrani, J. Verdaguer, S. Thiessen, B. Sonny, and P. Santamaria, “IL-1α, IL-1β, and IFN-γ mark β cells for Fas-dependent destruction by diabetogenic CD4+ T lymphocytes,” Journal of Clinical Investigation, vol. 105, no. 4, pp. 459–468, 2000. View at Google Scholar · View at Scopus
  41. M. Flodström-Tullberg, D. Yadav, R. Hägerkvist et al., “Target cell expression of suppressor of cytokine signaling-1 prevents diabetes in the NOD mouse,” Diabetes, vol. 52, no. 11, pp. 2696–2700, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Lenzen, J. Drinkgern, and M. Tiedge, “Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues,” Free Radical Biology and Medicine, vol. 20, no. 3, pp. 463–466, 1996. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Hotta, F. Tashiro, H. Ikegami et al., “Pancreatic β cell-specific expression of thioredoxin, an antioxidative and antiapoptotic protein, prevents autoimmune and streptozotocin-induced diabetes,” Journal of Experimental Medicine, vol. 188, no. 8, pp. 1445–1451, 1998. View at Publisher · View at Google Scholar · View at Scopus
  44. S. H. Huang, C. H. Chu, J. C. Yu et al., “Transgenic expression of haem oxygenase-1 in pancreatic β cells protects non-obese mice used as a model of diabetes from autoimmune destruction and prolongs graft survival following islet transplantation,” Diabetologia, vol. 53, no. 11, pp. 2389–2400, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. F. C. Chou, S. H. Huang, and H. K. Sytwu, “Genetically engineered islets and alternative sources of insulin-producing cells for treating autoimmune diabetes: quo vadis?” International Journal of Endocrinology, vol. 2012, Article ID 296485, 9 pages, 2012. View at Publisher · View at Google Scholar
  46. T. Delong, R. L. Baker, J. He, and K. Haskins, “Novel autoantigens for diabetogenic CD4 T cells in autoimmune diabetes,” Immunologic Research, vol. 55, no. 1–3, pp. 167–172, 2013. View at Publisher · View at Google Scholar
  47. J. D. Katz, B. Wang, K. Haskins, C. Benoist, and D. Mathis, “Following a diabetogenic T cell from genesis through pathogenesis,” Cell, vol. 74, no. 6, pp. 1089–1100, 1993. View at Publisher · View at Google Scholar · View at Scopus
  48. K. Haskins, “T-cell receptor transgenic (TCR-Tg) mice from two diabetogenic CD4+ islet-antigen-specific T-cell clones,” Journal of Autoimmunity, vol. 22, no. 2, pp. 107–109, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. D. Schmidt, J. Verdaguer, N. Averill, and P. Santamaria, “A mechanism for the major histocompatibility complex-linked resistance to autoimmunity,” Journal of Experimental Medicine, vol. 186, no. 7, pp. 1059–1075, 1997. View at Publisher · View at Google Scholar · View at Scopus
  50. M. E. Pauza, C. M. Dobbs, J. He et al., “T-cell receptor transgenic response to an endogenous polymorphic autoantigen determines susceptibility to diabetes,” Diabetes, vol. 53, no. 4, pp. 978–988, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. J. Verdaguer, D. Schmidt, A. Amrani, B. Anderson, N. Averill, and P. Santamaria, “Spontaneous autoimmune diabetes in monoclonal T cell nonobese diabetic mice,” Journal of Experimental Medicine, vol. 186, no. 10, pp. 1663–1676, 1997. View at Publisher · View at Google Scholar · View at Scopus
  52. D. Bending, H. de la Peña, M. Veldhoen et al., “Highly purified Th17 cells from BDC2.5NOD mice convert into Th1-like cells in NOD/SCID recipient mice,” Journal of Clinical Investigation, vol. 119, no. 3, pp. 565–572, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. N. Martin-Orozco, Y. Chung, S. H. Chang, Y. H. Wang, and C. Dong, “Th17 cells promote pancreatic inflammation but only induce diabetes efficiently in lymphopenic hosts after conversion into Th1 cells,” European Journal of Immunology, vol. 39, no. 1, pp. 216–224, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Poulin and K. Haskins, “Induction of diabetes in nonobese diabetic mice by Th2 T cell clones from a TCR transgenic mouse,” Journal of Immunology, vol. 164, no. 6, pp. 3072–3078, 2000. View at Google Scholar · View at Scopus
  55. J. Tian, P. V. Lehmann, and D. L. Kaufman, “T cell cross-reactivity between coxsackievirus and glutamate decarboxylase is associated with a murine diabetes susceptibility allele,” Journal of Experimental Medicine, vol. 180, no. 5, pp. 1979–1984, 1994. View at Publisher · View at Google Scholar · View at Scopus
  56. M. S. Horwitz, L. M. Bradley, J. Harbertson, T. Krahl, J. Lee, and N. Sarvetnick, “Diabetes induced by coxsackie virus: initiation by bystander damage and not molecular mimicry,” Nature Medicine, vol. 4, no. 7, pp. 781–785, 1998. View at Publisher · View at Google Scholar · View at Scopus
  57. C. M. Filippi, E. A. Estes, J. E. Oldham, and M. G. von Herrath, “Immunoregulatory mechanisms triggered by viral infections protect from type 1 diabetes in mice,” Journal of Clinical Investigation, vol. 119, no. 6, pp. 1515–1523, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Tracy, K. M. Drescher, J. D. Jackson, K. Kim, and K. Kono, “Enteroviruses, type 1 diabetes and hygiene: a complex relationship,” Reviews in Medical Virology, vol. 20, no. 2, pp. 106–116, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Nejentsev, N. Walker, D. Riches, M. Egholm, and J. A. Todd, “Rare variants of IFIH1, a gene implicated in antiviral responses, protect against type 1 diabetes,” Science, vol. 324, no. 5925, pp. 387–389, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. T. K. Starr, S. C. Jameson, and K. A. Hogquist, “Positive and negative selection of T cells,” Annual Review of Immunology, vol. 21, pp. 139–176, 2003. View at Publisher · View at Google Scholar · View at Scopus
  61. K. Wing and S. Sakaguchi, “Regulatory T cells exert checks and balances on self tolerance and autoimmunity,” Nature Immunology, vol. 11, no. 1, pp. 7–13, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. P. S. Ohashi, S. Oehen, K. Buerki et al., “Ablation of “tolerance” and induction of diabetes by virus infection in viral antigen transgenic mice,” Cell, vol. 65, no. 2, pp. 305–317, 1991. View at Publisher · View at Google Scholar · View at Scopus
  63. M. B. A. Oldstone, M. Nerenberg, P. Southern, J. Price, and H. Lewicki, “Virus infection triggers insulin-dependent diabetes mellitus in a transgenic model: role of anti-self (virus) immune response,” Cell, vol. 65, no. 2, pp. 319–331, 1991. View at Publisher · View at Google Scholar · View at Scopus
  64. D. Lo, J. Freedman, S. Hesse, R. D. Palmiter, R. L. Brinster, and L. A. Sherman, “Peripheral tolerance to an islet cell-specific hemagglutinin transgene affects both CD4+ and CD8+ T cells,” European Journal of Immunology, vol. 22, no. 4, pp. 1013–1022, 1992. View at Google Scholar · View at Scopus
  65. S. Degermann, C. Reilly, B. Scott, L. Ogata, H. von Boehmer, and D. Lo, “On the various manifestations of spontaneous autoimmune diabetes in rodent models,” European Journal of Immunology, vol. 24, no. 12, pp. 3155–3160, 1994. View at Publisher · View at Google Scholar · View at Scopus
  66. D. Dissanayake, M. A. Gronski, A. Lin, A. R. Elford, and P. S. Ohashi, “Immunological perspective of self versus tumor antigens: insights from the RIP-gp model,” Immunological Reviews, vol. 241, no. 1, pp. 164–179, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. L. S. Wicker, J. A. Todd, and L. B. Peterson, “Genetic control of autoimmune diabetes in the NOD mouse,” Annual Review of Immunology, vol. 13, pp. 179–200, 1995. View at Google Scholar · View at Scopus
  68. G. Morahan, “Insights into type 1 diabetes provided by genetic analyses,” Current Opinion in Endocrinology, Diabetes, and Obesity, vol. 19, no. 4, pp. 263–270, 2012. View at Google Scholar
  69. D. Devendra, E. Liu, and G. S. Eisenbarth, “Type 1 diabetes: recent developments,” The British Medical Journal, vol. 328, no. 7442, pp. 750–754, 2004. View at Google Scholar · View at Scopus
  70. J. W. Gregersen, S. Holmes, and L. Fugger, “Humanized animal models for autoimmune diseases,” Tissue Antigens, vol. 63, no. 5, pp. 383–394, 2004. View at Publisher · View at Google Scholar · View at Scopus
  71. A. E. Herman, R. M. Tisch, S. D. Patel et al., “Determination of glutamic acid decarboxylase 65 peptides presented by the type I diabetes-associated HLA-DQ8 class II molecule identifies an immunogenic peptide motif,” Journal of Immunology, vol. 163, no. 11, pp. 6275–6282, 1999. View at Google Scholar · View at Scopus
  72. J. Liu, L. E. Purdy, S. Rabinovitch, A. M. Jevnikar, and J. F. Elliott, “Major DQ8-restricted T-cell epitopes for human GAD65 mapped using human CD4, DQA1*0301, DQB1*0302 transgenic IA(null) NOD mice,” Diabetes, vol. 48, no. 3, pp. 469–477, 1999. View at Google Scholar · View at Scopus
  73. T. P. Di Lorenzo, M. Peakman, and B. O. Roep, “Translational mini-review series on type 1 diabetes: systematic analysis of T cell epitopes in autoimmune diabetes,” Clinical and Experimental Immunology, vol. 148, no. 1, pp. 1–16, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. L. Wen, F. S. Wong, J. Tang et al., “In vivo evidence for the contribution of human histocompatibility leukocyte antigen (HLA)-DQ molecules to the development of diabetes,” Journal of Experimental Medicine, vol. 191, no. 1, pp. 97–104, 2000. View at Publisher · View at Google Scholar · View at Scopus
  75. L. Wen, N. Y. Chen, J. Tang, R. Sherwin, and F. S. Wong, “The regulatory role of DR4 in a spontaneous diabetes DQ8 transgenic model,” Journal of Clinical Investigation, vol. 107, no. 7, pp. 871–880, 2001. View at Google Scholar · View at Scopus
  76. M. von Herrath and G. T. Nepom, “Animal models of human type 1 diabetes,” Nature Immunology, vol. 10, no. 2, pp. 129–132, 2009. View at Publisher · View at Google Scholar · View at Scopus
  77. C. Polychronakos and Q. Li, “Understanding type 1 diabetes through genetics: advances and prospects,” Nature Reviews in Genetics, vol. 12, no. 11, pp. 781–792, 2011. View at Publisher · View at Google Scholar