Partial versus full allogeneic hemopoietic chimerization is a preferential means to inhibit type 1 diabetes as the latter induces generalized immunosuppression

Journal of Immunology

Volumn 177, Issue 10, 2006, Pages 6675-6684

  Serreze, David V ^a   Osborne, Melissa A ^a   Chen, Yi Guang ^a   Chapman, Harold D ^a   Pearson, Todd ^b   Brehm, Michael A ^b   Greiner, Dale L ^b  

^a JACKSON LABORATORY   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; CHIMERA; CONTROLLED STUDY; DENDRITIC CELL; EFFECTOR CELL; FEMALE; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; INSULIN DEPENDENT DIABETES MELLITUS; LYMPHOCYTE FUNCTION; MACROPHAGE; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; THYMUS;

EID: 33750818891     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.10.6675     Document Type: Article

References (51)

1. Serreze, D. V., and E. H. Leiter. 2001. Genes and pathways underlying autoimmune diabetes in NOD mice. In Molecular Pathology of Insulin Dependent Diabetes Mellitus. M. G. von Herrath, ed. Karger Press, New York, pp. 31-67.
2. Choisy-Rossi, C.-M., T. M. Holl, M. A. Pierce, H. D. Chapman, and D. V. Serreze. 2004. Enhanced pathogenicity of diabetogenic T-cells escaping a non-MHC gene controlled near death experience. J. Immunol. 173: 3791-3800.
3. Acha-Orbea, H., and H. O. McDevitt. 1987. The first external domain of the nonobese diabetic mouse class II I-Aβ chain is unique. Proc. Natl. Acad. Sci. USA 84; 2435-2439.
4. Hattori, M., J. B. Buse, R. A. Jackson, L. Glimcher, M. E. Dorf, M. Minami, S. Makino, K. Moriwaki, H. Kuzuya, H. Imura, et al. 1986. The NOD mouse; recessive diabetogenic gene in the major histocompatability complex. Science 23I: 733-735.
5. Hanson, M. S., M. Cetkovic-Cvrlje, V. K. Ramiya, M. A. Atkinson, N. K. MacLaren, B. Singh, J. F. Elliott, D. V. Serreze, and E. H. Leiter. 1996. Quantitative thresholds of MHC class II I-E expressed on hematopoietically derived APC in transgenic NOD/Lt mice determine level of diabetes resistance and indicate mechanism of protection. J. Immunol. 157: 1279-1287.
6. Lund, T., L. O'Reilly, P. Hutchings, O. Kanagawa, E. Simpson, R. Gravely, P. Chandler, J. Dyson, J. K. Picard, A. Edwards, et al. 1990. Prevention of insulin-dependent diabetes mellitus in non-obese diabetic mice by transgenes encoding modified I-A β-chain or normal I-E α-chain. Nature 345: 727-729.
7. nod to the development of insulins in non-obese diabetic mice. Nature 345: 722-724.
8. d transgene prevents diabetes in nonobese diabetic mice by inducing regulatory T cells. Proc. Natl. Acad. Sci. USA 90: 9566-9570.
9. k transgenic mice. Nature 345: 724-726.
10. Prochazka, M., D. V. Serreze, S. M. Worthen, and E. H. Leiter. 1989. Genetic control of diabetogenesis in NOD/Lt mice; development and analysis of congenic stocks. Diabetes 38: 1446-1455.
11. Serreze, D. V., and E. H. Leiter. 1991. Development of diabetogenic T cells from NOD/Lt marrow is blocked when an allo-H-2 haplotype is expressed on cells of hematopoietic origin, but not on thymic epithelium. J. Immunol. 147: 1222-1229.
12. nod/b heterozygote. J. Immunol. 142: 781-784.
13. Johnson, E. A., P. Silveira, H. D. Chapman, E. H. Leiter, and D. V. Serreze. 2001. Inhibition of autoimmune diabetes in nonobese diabetic mice by transgenic restoration of H2-E MHC class II expression: additive, but unequal, involvement of multiple APC subtypes. J. Immunol. 167: 2404-2410.
14. Schmidt, D., J. Verdaguer, N. Averill, and P. Santamaria. 1997. A mechanism for the major histocompatibility complex-linked resistance to autoimmunity. J. Exp. Med. 186: 1059-1075.
15. + thymocytes by protective MHC class II molecules. J. Immunol. 162: 4627-4636.
16. 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: 3801-3807.
17. Serreze, D. V., T. M. Holl, M. P. Marron, R. T. Graser, E. A. Johnson, C. Choisy-Rossi, R. M. Slattery, S. M. Lieberman, and T. P. DiLorenzo. 2004. MHC class II molecules play a role in the selection of autoreactive class I restricted CD8 T cells that are essential contributors to type 1 diabetes development in NOD mice. J. Immunol. 172: 871-879.
18. Nepom, G. T., and W. W. Kwok. 1998. Molecular basis for HLA-DQ associations with IDDM. Diabetes 47: 1177-1184.
19. Nikolic, B., Y. Takeuchi, I. Leykin, Y. Fudaba, R. N. Smith, and M. Sykes. 2004. Mixed hematopoietic chimerism allows cure of autoimmune diabetes through allogeneic tolerance and reversal of autoimmunity. Diabetes 53: 376-383.
20. Seung, E., N. Iwakoshi, B. A. Woda, T. G. Markees, J. P. Mordes, A. A. Rossini, and D. L. Greiner. 2000. Allogeneic hematopoietic chimerism in mice treated with sublethal myeloablation and anti-CD154 antibody: absence of graft-versus-host disease, induction of skin allograft tolerance, and prevention of recurrent autoimmunity in islet-allografted NOD/Lt mice. Blood 95: 2175-2182.
21. Hogquist, K. A., T. A. Baldwin, and S. C. Jameson. 2005. Central tolerance: learning self control in the thymus. Nat. Rev. Immunol. 5: 772-782.
22. Zinkernagel, R. M., and A. Althage. 1999. On the role of thymic epithelium vs. bone marrow-derived cells in repertoire selection of T cells. Proc. Natl. Acad. Sci. USA 96: 8092-8097.
23. + cytotoxic T lymphocyte responses in autoimmune diabetes prone NOD mice. Diabetes 45: 902-908.
24. null mice. J. Exp. Med. 184: 2049-2053.
25. Prochazka, M., H. R. Gaskins, L. D. Shultz, and E. H. Leiter. 1992. The nonobese diabetic seid mouse: model for spontaneous thymomagenesis associated with immunodeficiency. Proc. Natl. Acad. Sci. USA 89: 3290-3294.
26. Graser, R. T., T. P. DiLorenzo, F. Wang, G. J. Christianson, H. D. Chapman, D. C. Roopenian, S. G. Nathenson, and D. V. Serreze. 2000. Identification of a CD8 T cell that can independently mediate autoimmune diabetes development in the complete absence of CD4 T cell helper functions. J. Immunol. 164: 3913-3918.
27. Serreze, D. V., E. A. Johnson, H. D. Chapman, R. T. Graser, M. P. Marron, Y. Yoshimura, T. P. DiLorenzo, S. G. Nathenson, and S. Joyce. 2001. Autoreactive T cells in NOD mice can efficiently expand from a greatly reduced precursor pool. Diabetes 50: 1992-2000.
28. Silveira, P. A., J. Dombrowsky, E. Johnson, H. D. Chapman, D. Nemazee, and D. V. Serreze. 2004. B-cell selection defects underlie the development of diabetogenic antigen presenting cells in NOD mice. J. Immunol. 172: 5086-5094.
29. Selin, L. K., S. R. Nahill, and R. M. Welsh. 1994. Cross-reactivities in memory cytotoxic T lymphocyte recognition of heterologous viruses. J. Exp. Med. 179: 1933-1943.
30. Brehm, M. A., A. K. Pinto, K. A. Daniels, J. P. Schneck, R. M. Welsh, and L. K. Selin. 2002. T cell immunodominance and maintenance of memory regulated by unexpectedly cross-reactive pathogens. Nat. Immunol. 3: 627-634.
31. Markees, T. G., N. E. Phillips, E. J. Gordon, R. J. Noelle, L. D. Shultz, J. P. Mordes, D. L. Greiner, and A. A. Rossini. 1998. Long-term survival of skin allografts induced by donor splenocytes and anti-CD154 antibody in thymectomized mice requires CD4 T cells, interferon-γ and CTLA-4. J. Clin. Invest. 101: 2446-2455.
32. 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: 329-335.
33. Beilhack, G. F., Y. C. Scheffold, I. L. Weismann, C. Taylor, L. Jerabeck, M. J. Burge, M. A. Masek, and J. A. Shizuru. 2003. Purified allogeneic hematopoietic stem cell transplantation blocks diabetes pathogenesis in NOD mice. Diabetes 52: 59-68.
34. Li, H., C. L. Kaufman, S. S. Boggs, P. C. Johnson, K. D. Patrene, and S. T. Ildstad. 1996. Mixed allogeneic chimerism induced by a sublethal approach prevents autoimmune diabetes and reverses insulitis in nonobese diabetic (NOD) mice. J. Immunol. 156: 380-388.
35. Chilton, P. M., F. Rezzoug, I. Fugier-Vivier, L. A. Weeter, H. Xu, Y. Huang, M. B. Ray, and S. T. Ildstad. 2004. Flt3-ligand treatment prevents diabetes in NOD mice. Diabetes 53: 1995-2002.
36. Mathieu, C., K. Castells, R. Bouillon, and M. Waer. 1997. Protection against autoimmune diabetes in mixed bone marrow chimeras. J. Immunol. 158: 1453-1457.
37. 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. Proc. Natl. Acad. Sci. USA 90: 9625-9629.
38. Liang, Y., T. Huang, C. Zhang, I. Todorov, M. Atkinson, F. Kadeel, S. Forman, and D. Zeng. 2005. Donor CD8 T cells facilitate induction of chimerism and tolerance without GHVD in autoimmune NOD mice conditioned with anti-CD3 mAb Blood 105: 2180-2188.
39. Pearson, T., T. G. Markees, D. V. Serreze, M. A. Pierce, M. P. Marron, L. S. Wicker, L. B. Peterson, L. D. Shultz, J. P. Mordes, A. A. Rossini, and D. L. Greiner. 2003. Genetic dissociation of autoimmunity and resistance to costimulation blockade-induced transplantation tolerance in nonobese diabetic mice. J. Immunol. 171: 185-195.
40. Kreuwel, H. T., J. A. Biggs, I. M. Pilip, E. G. Pamer, D. Lo, and L. A. Sherman. 2001. Defective CD8 T cell peripheral tolerance in nonobese diabetic mice. J. Immunol. 167: 1112-1117.
41. Martinez, X., H. T. C. Kreuwel, W. L. Redmond, R. Trenney, K. Hunter, H. Rosen, N. Sarvetnick, L. S. Wicker, and L. A. Sherman. 2005. CD8 T cell tolerance in nonobese diabetic mice is restored by insulin-dependent diabetes resistance alleles. J. Immunol. 175: 1677-1685.
42. Seung, E., J. P. Mordes, A. A. Rossini, and D. L. Greiner. 2003. Hematopoietic chimerism and central tolerance created by peripheral-tolerance induction without myeloablative conditioning. J. Clin. Invest. 112: 795-808.
43. Butz, E. A., and M. J. Bevan. 1998. Massive expansion of antigen specific CD8 T cells during an acute virus infection. Immunity 8: 167-175.
44. Murali-Krishna, K., J. D. Altman, M. Suresh, D. J. Sourdive, A. J. Zajac, J. D. Miller, J. Slansky, and R. Ahmed. 1998. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation after viral infection. Immunity 8: 177-187.
45. Lieberman, S. M., T. Takaki, B. Han, P. Santamaria, D. V. Serreze, and T. P. DiLorenzo. 2004. Individual nonobese diabetic mice exhibit unique patterns of CD8 T cell reactivity to three islet antigens including the newly identified widely expressed dystrophia myotonica kinase. J. Immunol. 173: 6727-6734.
46. Sebzda, E., S. Mariathasan, T. Ohteki, R. Jones, M. F. Bachmann, and P. S. Ohashi. 1999. Selection of the T cell repertoire. Annu. Rev. Immunol. 17: 829-874.
47. + and CD4 T cells negates the effect. Blood 105: 2577-2584.
48. Williams, M. A., A. B. Adams, M. B. Walsh, N. Shirasugi, T. M. Onami, T. C. Pearson, R. Ahmed, and C. P. Larsen. 2003. Primary and secondary immunocompetence in mixed allogeneic chimeras. J. Immunol. 170: 2382-2389.
49. Wekerle, T., M. H. Sayegh, J. Hill, Y. Zhao, A. Chandraker, K. G. Swenson, G. Zhao, and M. Sykes. 1998. Extrathymic T cell deletion and allogeneic stem cell engraftment induced with co-stimulatory blockade is followed by central T cell tolerance. J. Exp. Med. 187: 2037-2044.
50. Wekerle, T., M. H. Sayegh, H. Ito, J. Hill, A. Chandraker, D. A. Pearson, K. G. Swenson, G. Zhao, and M. Sykes. 1999. Anti-CD154 or CTLA4Ig obviates the need for thymic irradiation in a non-myeloablative conditioning regimen for the induction of mixed hematopoietic chimerism and tolerance. Transplantation 68: 1348-1355.
51. Markees, T. G., D. V. Serreze, N. E. Phillips, C. H. Sorli, E. J. Gordon, L. D. Shultz, 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: 967-974.