Genetic disassociation of autoimmunity and resistance to costimulation blockade-induced transplantation tolerance in nonobese diabetic mice

Journal of Immunology

Volumn 171, Issue 1, 2003, Pages 185-195

  Pearson, Todd ^a   Markees, Thomas G ^a   Serreze, David V ^a,b   Pierce, Melissa A ^b   Marron, Michele P ^b   Wicker, Linda S ^c   Peterson, Laurence B ^d   Shultz, Leonard D ^a,b   Mordes, John P ^a   Rossini, Aldo A ^a   Greiner, Dale L ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b JACKSON LABORATORY   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOTRANSPLANTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOIMMUNITY; CELL MATURATION; CONTROLLED STUDY; DENDRITIC CELL; GRAFT REJECTION; HELPER CELL; INSULIN DEPENDENT DIABETES MELLITUS; MACROPHAGE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PANCREAS ISLET TRANSPLANTATION; PHENOTYPE; PRIORITY JOURNAL; SKIN ALLOGRAFT; TRANSPLANTATION TOLERANCE;

EID: 0037530649     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.171.1.185     Document Type: Article

References (83)

1. Atkinson, M., and E. H. Leiter. 1999. The NOD mouse model of insulin dependent diabetes: as good as it gets? Nat. Med. 5:601.
2. Greiner, D. L., A. A. Rossini, and J. P. Mordes. 2001. Translating data from animal models into methods for preventing human autoimmune diabetes mellitus: caveat emptor and primum non nocere. Clin. Immunol. 100:134.
3. Morales, J. P., D. L. Greiner, and A. A. Rossini. 2000. Animal models of autoimmune diabetes mellitus. In Diabetes Mellitus: A Fundamental and Clinical Text, 2nd Ed. D. LeRoith, S. I. Taylor, and J. M. Olefsky, eds. Lippincott Williams and Wilkins, Philadelphia, p. 430.
4. Leiter, E. 1998. Genetics and immunogenetics of NOD mice and related strains. In NOD Mice and Related Strains: Research Applications in Diabetes, AIDS, Cancer, and Other Diseases. E. Leiter and M. Atkinson, eds. R. G. Landes, Austin, p. 37.
5. + T cells, interferon-γ, and CTLA4. J. Clin. Invest. 101:2446.
6. Rossini, A. A., J. P. Mordes, D. L. Greiner, and J. S. Stoff. 2001. Islet cell transplantation tolerance. Transplantation 72:S43.
7. Rossini, A. A., D. L. Greiner, and J. P. Mordes. 1999. Induction of immunological tolerance for transplantation. Physiol. Rev. 79:99.
8. Markees, T. G., D. V. Serreze, N. E. Phillips, C. H. Sorli, R. J. Noelle, B. A. Woda, D. L. Greiner, J. P. Mordes, and A. A. Rossini. 1999. NOD mice have a generalized defect in their response to transplantation tolerance induction. Diabetes 48:967.
9. Molano, R. D., T. Berney, H. Li, P. Cattan, A. Pileggi, C. Vizzardelli, N. S. Kenyon, C. Ricordi, L. C. Burkly, and L. Inverardi. 2001. Prolonged islet graft survival in NOD mice by blockade of the CD40-CD154 pathway of T-cell costimulation. Diabetes 50:270.
10. Sutherland, D. E., R. Sibley, X. Z. Xu, A. Michael, A. M. Srikanta, F. Taub, J. Najarian, and F. C. Goetz. 1984. Twin-to-twin pancreas transplantation: reversal and reenactment of the pathogenesis of type I diabetes. Trans. Assoc. Am. Physicians 97:80.
11. Molano, R. D., T. Berney, A. Pileggi, C. Ricordi, L. Burkly, D. Rothstein, G. Basadonna, and L. Inverardi. 2001. Prolonged survival of allogeneic islet grafts in NOD mice treated with a combination of anti-CD45 RB and anti-CD154 antibodies. Transplant. Proc. 33:248.
12. Dahlén, E., G. Hedlund, and K. Dawe. 2000. Low CD86 expression in the nonobese diabetic mouse results in the impairment of both T cell activation and CTLA-4 up-regulation. J. Immunol. 164:2444.
13. Serreze, D. V., J. W. Gaedeke, and E. H. Leiter. 1993. Hematopoietic stem-cell defects underlying abnormal macrophage development and maturation in NOD/Lt mice: defective regulation of cytokine receptors and protein kinase C. Proe. Natl. Acad. Sci. USA 90:9625.
14. Radons, J., V. Burkart, and H. Kolb. 1997. MHC class II-dependent abnormal reactivity toward bacterial superantigens in immune cells of NOD mice. Diabetes 46:379.
15. Noorchashm, H., D. J. Moore, L. E. Noto, N. Noorchashm, A. J. Reed, A. L. Reed, H. K. Song, R. Mozaffari, A. M. Jevnikar, C. F. Barker, and A. Naji. 2000. Impaired CD4 T cell activation due to reliance upon B cell-mediated costimulation in nonobese diabetic (NOD) mice. J. Immunol. 165:4685.
16. Kataoka, S., J. Satoh, H. Fujiya, T. Toyota, R. Suzuki, K. Itoh, and K. Kumagai. 1983. Immunologic aspects of the nonobese diabetic (NOD) mouse. Diabetes 32:247.
17. Naumov, Y. N., K. S. Bahjat, R. Gausling, R. Abraham, M. A. Exley, Y. Koezuka, S. B. Balk, J. L. Strominger, M. Clare-Salzier, and S. B. Wilson. 2001. Activation of CD1d-restricted T cells protects NOD mice from developing diabetes by regulating dendritic cell subsets. Proc. Natl. Acad. Sci. USA 98:13838.
18. Serreze, D. V., and E. H. Leiter. 1988. Defective activation of T suppressor cell function in nonobese diabetic mice: potential relation to cytokine deficiencies. J. Immunol. 140:3801.
19. Shultz, L. D., P. A. Schweitzer, S. W. Christianson, B. Gott, I. B. Schweitzer, B. Tennent, S. McKenna, L. Mobraaten, T. V. Rajan, D. L. Greiner, and E. H. Leiter. 1995. Multiple defects in innate and adaptive immunologic function in NOD/LtSz-scid mice. J. Immunol. 154:180.
20. + immunoregulatory T cells that control autoimmune diabetes. Immunity 12:431.
21. Pearson, T., T. G. Markees, L. S. Wicker, D. V. Serreze, L. B. Peterson, J. P. Mordes, A. A. Rossini, and D. L. Greiner. 2002. NOD congenic mice genetically protected from autoimmune diabetes remain resistant to transplantation tolerance induction. Diabetes 52:321.
22. null mice. J. Exp. Med. 184:2049.
23. Chiu, P. P. L., D. V. Serreze, and J. S. Danska. 2001. Development and function of diabetogenic T-cells in B-cell-deficient nonobese diabetic mice. Diabetes 50:763.
24. + T cells and prolonged graft survival in a CTLA4-dependent manner. J. Immunol. 164:512.
25. Foy, T. M., D. M. Shepherd, F. H. Durie, A. Aruffo, J. A. Ledbetter, and R. J. Noelle. 1993. In vivo CD40-gp39 interactions are essential for thymus-dependent humoral immunity. II. Prolonged suppression of the humoral immune response by an antibody to the ligand for CD40, gp39. J. Exp. Med. 178:1567.
26. Noelle, R. J., M. Roy, D. M. Shepherd, I. Stamenkovic, J. A. Ledbetter, and A. Aruffo. 1992. A 39-kDa protein on activated helper T cells binds CD40 and transduces the signal for cognate activation of B cells. Proc. Natl. Acad. Sci. USA 89:6550.
27. Iwakoshi, N. N., T. G. Markees, N. A. Turgeon, T. Thornley, A. Cuthbert, J. H. Leif, N. E. Phillips, J. P. Mordes, D. L. Greiner, and A. A. Rossini. 2001. Skin allograft maintenance in a new synchimeric model system of tolerance. J. Immunol. 167:6623.
28. Markees, T. G., N. E. Phillips, R. J. Noelle, L. D. Shultz, J. P. Mordes, D. L. Greiner, and A. A. Rossini. 1997. Prolonged survival of mouse skin allografts in recipients treated with donor splenocytes and antibody to CD40 ligand. Transplantation 64:329.
29. Woda, B. A., M. L. McFadden, R. M. Welsh, and K. M. Bain. 1984. Separation and isolation of rat natural killer (NK) cells from T cells with monoclonal antibodies. J. Immunol. 132:2183.
30. Ortaldo, J. R., R. Winkler-Pickett, A. C. Morgan, C. Woodhouse, R. Kantor, and C. W. Reynolds. 1987. Analysis of rat natural killer cytotoxic factor (NKCF) produced by rat NK cell lines and the production of a murine monoclonal antibody that neutralizes NKCF. J. Immunol. 139:3159.
31. null mice: an immunodeficient and radioresistant model for engraftment of human hematolymphoid cells, HIV infection, and adoptive transfer of NOD mouse diabetogenic T cells. J. Immunol. 164:2496.
32. Kaplan, E. L., and P. Meier. 1958. Nonparametric estimation from incomplete observations. J. Am. Stat. Assoc. 53:457.
33. Nie, N. H., C. H. Hull, J. G. Jenkins, K. Steinbrenner, and D. H. Bent. 1975. Statistical package for the social sciences. McGraw-Hill, New York, p. 1.
34. Pearson, T., T. G. Markees, L. S. Wicker, D. V. Serreze, L. B. Peterson, J. P. Mordes, A. A. Rossini, and D. L. Greiner. 2003. NOD congenic mice genetically protected from autoimmune diabetes remain resistant to transplantation tolerance induction. Diabetes 52:321.
35. Graser, R. T., C. E. Mathews, E. H. Leiter, and D. V. Serreze. 1999. MHC characterization of ALR and ALS mice: respective similarities to the NOD and NON strains. Immunogenetics 49:722.
36. Mathews, C. E., R. T. Graser, A. Savinov, D. V. Serreze, and E. H. Leiter. 2001. Unusual resistance of ALR/Lt mouse β destruction: role for β cell-expressed resistance determinants. Proc. Natl. Acad. Sci. USA 98:235.
37. Steinman, R. M., S. Turley, I. Mellman, and K. Inaba. 2000. The induction of tolerance by dendritic cells that have captured apoptotic cells. J. Exp. Med. 191:411.
38. Langenkamp, A., M. Messi, A. Lanzavecchia, and F. Sallusto. 2000. Kinetics of dendritic cell activation: impact on priming of TH1, TH2 and nonpolarized T cells. Nat. Immunol. 1:311.
39. Starzl, T. E., N. Murase, A. W. Thomson, M. Trucco, and A. Rao. 1999. Regulation of immune reactivity and tolerance by antigen migration and localization: with particular reference to allo- and xenotransplantation. Transplant. Proc. 31:763.
40. Thomson, A. W., and L. Lu. 1999. Are dendritic cells the key to liver transplant tolerance? Immunol. Today 20:27.
41. Min, W. P., R. Gorczynski, X. Y. Huang, M. Kushida, P. Kim, M. Obataki, J. Lei, R. M. Suri, and M. S. Cattral. 2000. Dendritic cells genetically engineered to express Fas ligand induce donor-specific hyporesponsiveness and prolong allograft survival. J. Immunol. 164:161.
42. Miga, A. J., S. R. Masters, B. G. Durell, M. Gonzalez, M. K. Jenkins, C. Maliszewski, H. Kikutani, W. F. Wade, and R. J. Noelle. 2001. Dendritic cell longevity and T cell persistence is controlled by CD154-CD40 interactions. Eur. J. Immunol. 31:959.
43. Feili-Hariri, M., and P. A. Morel. 2001. Phenotypic and functional characteristics of BM-derived DC from NOD and non-diabetes-prone strains. Clin. Immunol. 98:133.
44. Strid, J., L. Lopes, J. Marcinkiewicz, L. Petrovska, B. Nowak, B. M. Chain, and T. Lund. 2001. A defect in bone marrow derived dendritic cell maturation in the nonobese diabetic mouse. Clin. Exp. Immunol. 123:375.
45. Prasad, S. J., and C. C. Goodnow. 2002. Cell-intrinsic effects of non-MHC NOD genes on dendritic cell generation in vivo. Int. Immunol. 14:677.
46. Prasad, S. J., and C. C. Goodnow. 2002. Intrinsic in vitro abnormalities in dendrific cell generation caused by non-MHC non-obese diabetic genes. Immunol. Cell Biol. 80:198.
47. Poligone, B., D. J. Weaver Jr., P. Sen, A. S. Baldwin Jr., and R. Tisch. 2002. Elevated NF-κB activation in nonobese diabetic mouse dendritic cells results in enhanced APC function. J. Immunol. 168:188.
48. Steptoe, R. J., J. M. Ritchie, and L. C. Harrison. 2002. Increased generation of dendritic cells from myeloid progenitors in autoimmune-prone nonobese diabetic mice. J. Immunol. 168:5032.
49. George, T. C., J. R. Ortaldo, S. Lemieux, V. Kumar, and M. Bennett. 1999. Tolerance and alloreactivity of the Ly49D subset of murine NK cells. J. Immunol. 163:1859.
50. Poulton, L. D., M. J. Smyth, C. G. Hawke, P. Silveira, D. Shepherd, O. V. Naidenko, D. I. Godfrey, and A. G. Baxter. 2001. Cytometric and functional analyses of NK and NKT cell deficiencies in NOD mice. Int. Immunol. 13:887.
51. + immune regulatory cells are required for induction of tolerance to alloantigen latory blockade. J. Exp. Med 193:1311.
52. Hara, M., C. I. Kingsley, M. Niimi, S. Read, S. E. Turvey, A. R. Bushell, P. J. Morris, F. Powrie, and K. J. Wood. 2001. IL-10 is required for regulatory T cells to mediate tolerance to alloantigens in vivo. J. Immunol. 166:3789.
53. + regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol. Rev. 182:18.
54. - regulatory cells mediate dominant transplantation tolerance. J. Immunol. 168:5558.
55. + T cell-mediated graft rejection: implications for anti-CD154 immunotherapy. J. Immunol. 169:5401.
56. Todd, J. A., and L. S. Wicker. 2001. Genetic protection from the inflammatory disease type 1 diabetes in humans and animal models. Immunity 15:387.
57. Moore, K. J., and D. L. Nagle. 2000. Complex trait analysis in the mouse: the strengths, the limitations and the promise yet to come. Annu. Rev. Genet. 34:653.
58. Morel, P. A., A. C. Vasquez, and M. Feili-Hariri. 1999. Immunobiology of DC in NOD mice. J. Leukocyte Biol. 66:276.
59. Mackey, M. F., R. J. Barth Jr., and R. J. Noelle. 1998. The role of CD40/CD154 interactions in the priming, differentiation, and effector funcfion of helper and cytotoxic T cells. J. Leukocyte Biol. 63:418.
60. Clark, L. B., T. M. Foy, and R. J. Noelle. 1996. CD40 and its ligand. Adv. Immunol. 63:43.
61. Li, Y., X. C. Li, X. X. Zheng, A. D. Wells, L. A. Turka, and T. B. Strom. 1999. Blocking both signal 1 and signal 2 of T-cell activation prevents apoptosis of alloreactive T cells and induction of peripheral allograft tolerance. Nat. Med. 5:1298.
62. Wells, A. D., X. C. Li, Y. Li, M. C. Walsh, X. X. Zheng, Z. Wu, G. Nunez, A. Tang, M. Sayegh, W. W. Hancock, et al. 1999. Requirement for T-cell apoptosis in the induction of peripheral transplantation tolerance. Nat. Med. 5:1303.
63. + T cells play a critical role in costimulation blockade-resistant allograft rejection. J. Clin. Invest. 104:1715.
64. Fazekas de St. Groth, B. 1998. The evolution of self-tolerance: a new cell arises to meet the challenge of self-reactivity. Immunol. Today 19:448.
65. Menges, M., S. Rossner, C. Voigtlander, H. Schindler, N. A. Kukutsch, C. Bogdan, K. Erb, G. Schuler, and M. B. Lutz. 2002. Repetitive injections of dendritic cells matured with tumor necrosis factor a induce antigen-specific protection of mice from autoimmunity. J. Exp. Med. 195:15.
66. McGuirk, P., C. McCann, and K. H. Mills. 2002. Pathogen-specific T regulatory 1 cells induced in the respiratory tract by a bacterial molecule that stimulates interleukin 10 production by dendritic cells: a novel strategy for evasion of protective T helper type 1 responses by Bordetella pertussis. J. Exp. Med. 195:221.
67. Akbari, O., G. J. Freeman, E. H. Meyer, E. A. Greenfield, T. T. Chang, A. H. Sharpe, G. Berry, R. H. DeKruyff, and D. T. Umetsu. 2002. Antigen-specific regulatory T cells develop via the ICOS 150:ICOS-ligand pathway and inhibit allergen-induced airway hyperreactivity. Nat. Med 8:1024.
68. Akbari, O., R. H. DeKruyff, and D. T. Umetsu. 2001. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat. Immunol. 2:725.
69. Lutz, M., and G. Schuler. 2002. Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol. 23:445.
70. Zheng, X. X., T. G. Markees, W. W. Hancock, Y. Li, D. L. Greiner, X. C. Li, J. P. Mordes, M. H. Sayegh, A. A. Rossini, and T. B. Strom. 1999. CTLA4 signals are required to optimally induce allograft tolerance with combined DST and anti-CD154 mAb treatment. J. Immunol. 162:4983.
71. Serreze, D. V., H. R. Gaskins, and E. H. Leiter. 1993. Defects in the differentiation and function of antigen presenting cells in NOD/Lt mice. J. Immunol. 150:2534.
72. Serreze, D. V. 1993. Autoimmune diabetes results from genetic defects manifest by antigen presenting cells. FASEB J. 7:1092.
73. + T cell peripheral tolerance in nonobese diabetic mice. J. Immunol. 167:1112.
74. Harada, M., and S. Makino. 1984. Promotion of spontaneous diabetes in nonobese diabetes-prone mice by cyclophosphamide. Diabetologia 27:604.
75. Charlton, B., A. Bacelj, R. M. Slattery, and T. E. Mandel. 1989. Cyclophosphamide-induced diabetes in NOD/WEHI mice: evidence for suppression in spontaneous autoimmune diabetes mellitus. Diabetes 38:441.
76. Prochazka, M., D. V. Serreze, W. N. Frankel, and E. H. Leiter. 1992. NOR/Lt mice: MHC-matched diabetes-resistant control strain for NOD mice. Diabetes 41:98.
77. Wicker, L. S., M. C. Appel, F. Dotta, A. Pressey, B. J. Miller, N. H. DeLarato, P. A. Fischer, R. C. Boltz Jr., and L. B. Peterson. 1992. Autoimmune syndromes in major histocompatibility complex (MHC) congenic strains of nonobese diabetic (NOD) mice: the NOD MHC is dominant for insulitis and cyclophosphamide-induced diabetes. J. Exp. Med. 176:67.
78. Wicker, L. S., J. A. Todd, and L. B. Peterson. 1995. Genetic control of autoimmune diabetes in the NOD mouse. Annu. Rev. Immunol. 13:179.
79. McAleer, M. A., P. Reifsnyder, S. M. Palmer, M. Prochazka, J. M. Love, J. B. Copeman, E. E. Powell, N. R. Rodrigues, J. B. Prins, D. V. Serreze, et al. 1995. Crosses of NOD mice with the related NON strain: a polygenic model for IDDM. Diabetes 44:1186.
80. 2-microglobulin as a diabetes susceptibility gene in nonobese diabetic (NOD) mice. Proc. Natl. Acad. Sci. USA 98:11533.
81. Fox, C. J., A. D. Paterson, S. M. Mortin-Toth, and J. S. Danska. 2000. Two genetic loci regulate T cell-dependent islet inflammation and drive autoimmune diabetes pathogenesis. Am. J. Hum. Genet. 67:67.
82. 2-microglobulin. J. Immunol. 160:1472.
83. Yasunami, Y., and J.-F. Bach. 1988. Anti-suppressor effect of cyclophosphamide on the development of spontaneous diabetes in NOD mice. Eur. J. Immunol. 18:484.