Intracellular MHC class II controls regulatory tolerance to allogeneic transplants

Journal of Immunology

Volumn 184, Issue 5, 2010, Pages 2394-2400

  LeGuern, Christian ^a   Akiyama, Yoshinobu ^a   Germana, Sharon ^a   Tanaka, Katsunori ^a   Fernandez, Luis ^a   Iwamoto, Yoshiko ^a   Houser, Stuart ^a   Benichou, Gilles ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUSULFAN; FLUOROURACIL; IA ANTIBODY; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; HLA ANTIGEN CLASS 2;

ANIMAL EXPERIMENT; ARTICLE; BONE MARROW; CARDIAC ALLOGRAFT VASCULOPATHY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DONOR; FEMALE; GENE TRANSFER; GRAFT RECIPIENT; HEART TRANSPLANTATION; IMMUNOSUPPRESSIVE TREATMENT; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SURVIVAL TIME; T LYMPHOCYTE; TH2 CELL; ALLOTRANSPLANTATION; ANIMAL; BAGG ALBINO MOUSE; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; C57BL MOUSE; CBA MOUSE; CYTOLOGY; DENDRITIC CELL; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; GRAFT SURVIVAL; IMMUNOLOGY; INTRACELLULAR SPACE; METABOLISM; METHODOLOGY; RETROVIRUS; TRANSPLANTATION TOLERANCE;

ANIMALS; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; DENDRITIC CELLS; FEMALE; GENETIC VECTORS; GRAFT SURVIVAL; HEART TRANSPLANTATION; HISTOCOMPATIBILITY ANTIGENS CLASS II; INTRACELLULAR SPACE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED CBA; RETROVIRIDAE; T-LYMPHOCYTES; TRANSDUCTION, GENETIC; TRANSPLANTATION TOLERANCE; TRANSPLANTATION, HOMOLOGOUS;

EID: 77951894259     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0803664     Document Type: Article

References (47)

1. Starr, T. K., S. C. Jameson, and K. A. Hogquist. 2003. Positive and negative selection of T cells. Annu. Rev. Immunol. 21: 139-176.
2. Sprent, J., and H. Kishimoto. 2002. The thymus and negative selection. Immunol. Rev. 185: 126-135.
3. Watanabe, N., Y. H. Wang, H. K. Lee, T. Ito, Y. H. Wang, W. Cao, and Y. J. Liu. 2005. Hassall's corpuscles instruct dendritic cells to induce CD4+CD25+ regulatory T cells in human thymus. Nature 436: 1181-1185. (Pubitemid 41232298)
4. Sakaguchi, S. 2005. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat. Immunol. 6: 345-352.
5. McDevitt, H. O., B. D. Deak, D. C. Shreffler, J. Klein, J. H. Stimpfling, and G. D. Snell. 1972. Genetic control of the immune response. Mapping of the Ir-1 locus. J. Exp. Med. 135: 1259-1278.
6. Shevach, E. M., and A. S. Rosenthal. 1973. Function of macrophages in antigen recognition by guinea pig T lymphocytes. II. Role of the macrophage in the regulation of genetic control of the immune response. J. Exp. Med. 138: 1213-1229.
7. Hunt, D. F., H. Michel, T. A. Dickinson, J. Shabanowitz, A. L. Cox, K. Sakaguchi, E. Appella, H. M. Grey, and A. Sette. 1992. Peptides presented to the immune system by the murine class II major histocompatibility complex molecule I-Ad. Science 256: 1817-1820.
8. Ashton-Rickardt, P. G., A. Bandeira, J. R. Delaney, L. Van Kaer, H. P. Pircher, R. M. Zinkernagel, and S. Tonegawa. 1994. Evidence for a differential avidity model of T cell selection in the thymus. Cell 76: 651-663.
9. Fukui, Y., T. Ishimoto, M. Utsuyama, T. Gyotoku, T. Koga, K. Nakao, K. Hirokawa, M. Katsuki, and T. Sasazuki. 1997. Positive and negative CD4+ thymocyte selection by a single MHC class II/peptide ligand affected by its expression level in the thymus. Immunity 6: 401-410. (Pubitemid 27208195)
10. Schaeffer, E. B., A. Sette, D. L. Johnson, M. C. Bekoff, J. A. Smith, H. M. Grey, and S. Buus. 1989. Relative contribution of "determinant selection" and "holes in the T-cell repertoire" to T-cell responses. Proc. Natl. Acad. Sci. USA 86: 4649-4653.
11. Gelder, C., M. Davenport, M. Barnardo, T. Bourne, J. Lamb, B. Askonas, A. Hill, and K. Welsh. 1998. Six unrelated HLA-DR-matched adults recognize identical CD4+ T cell epitopes from influenza A haemagglutinin that are not simply peptides with high HLA-DR binding affinities. Int. Immunol. 10: 211-222.
12. Erlich, H. A., G. Opelz, and J. Hansen. 2001. HLA DNA typing and transplantation. Immunity 14: 347-356.
13. Rosengard, B. R., C. A. Ojikutu, P. C. Guzzetta, C. V. Smith, T. M. Sundt, 3rd, K. Nakajima, S. M. Boorstein, G. S. Hill, J. M. Fishbein, and D. H. Sachs. 1992. Induction of specific tolerance to class I-disparate renal allografts in miniature swine with cyclosporine. Transplantation 54: 490-497.
14. LeGuern, C., H. Shimada, D. W. Emery, S. Germana, G. E. Shafer, and D. H. Sachs. 1995. Retrovirus-mediated transfer of MHC class II cDNA into swine bone marrow cells. J. Mol. Med. 73: 269-278.
15. Emery, D. W., T. Sablinski, H. Shimada, S. Germana, P. Gianello, A. Foley, S. Shulman, S. Arn, J. Fishman, T. Lorf, et al. 1997. Expression of an allogeneic MHC DRB transgene, through retroviral transduction of bone marrow, induces specific reduction of alloreactivity. Transplantation 64: 1414-1423.
16. Sonntag, K. C., D. W. Emery, A. Yasumoto, G. W. Haller, S. Germana, T. Sablinski, A. Shimizu, K. Yamada, H. Shimada, S. Arn, et al. 2001. Tolerance to solid organ transplants through transfer of MHC class II genes. J. Clin. Invest. 107: 65-71.
17. Orbaek Andersen, H. 1999. Heart allograft vascular disease: an obliterative vascular disease in transplanted hearts. Atherosclerosis 142: 243-263. (Pubitemid 29059482)
18. Miller, A. D., and G. J. Rosman. 1989. Improved retroviral vectors for gene transfer and expression. Biotechniques 7: 980-982, 984-986, 989-990.
19. Banerjee, P. T., G. C. Kanor, S. Muthukumar, M. Denaro, H. Shimada, S. Zhu, M. D. Rosa, D. H. Sachs, and C. LeGuern. 1997. A polycistronic retrovirus vector for expression of swine MHC class II DR α/β heterodimers. Xeno-transplantation 4: 161-173.
20. Andersson, G., M. Denaro, K. Johnson, P. Morgan, A. Sullivan, S. Houser, C. Patience, M. E. White-Scharf, and J. D. Down. 2003. Engraftment of retroviral EGFP-transduced bone marrow in mice prevents rejection of EGFP-transgenic skin grafts. Mol. Ther. 8: 385-391.
21. Andersson, G., B. M. Illigens, K. W. Johnson, D. Calderhead, C. LeGuern, G. Benichou, M. E. White-Scharf, and J. D. Down. 2003. Nonmyeloablative conditioning is sufficient to allow engraftment of EGFP-expressing bone marrow and subsequent acceptance of EGFP-transgenic skin grafts in mice. Blood 101: 4305-4312. (Pubitemid 36857794)
22. Corry, R. J., H. J. Winn, and P. S. Russell. 1973. Primarily vascularized allografts of hearts in mice. The role of H-2D, H-2K, and non-H-2 antigens in rejection. Transplantation 16: 343-350.
23. Houser, S. L., I. M. McMorrow, C. LeGuern, M. L. Schwarze, Y. Fuchimoto, D. H. Sachs, and J. C. Madsen. 2004. Histomorphometric comparison of cardiac allograft vasculopathy in miniature swine. J. Heart Lung Transplant. 23: 50-60.
24. Ozato, K., and D. H. Sachs. 1981. Monoclonal antibodies to mouse MHC antigens. III. Hybridoma antibodies reacting to antigens of the H-2b haplotype reveal genetic control of isotype expression. J. Immunol. 126: 317-321.
25. Benichou, G., A. Valujskikh, and P. S. Heeger. 1999. Contributions of direct and indirect T cell alloreactivity during allograft rejection in mice. J. Immunol. 162: 352-358. (Pubitemid 29018940)
26. Csencsits, K. L., and D. K. Bishop. 2003. Contrasting alloreactive CD4+ and CD8+ T cells: there's more to it than MHC restriction. Am. J. Transplant. 3: 107-115.
27. Strom, T. B., P. Roy-Chaudhury, R. Manfro, X. X. Zheng, P. W. Nickerson, K. Wood, and A. Bushell. 1996. The Th1/Th2 paradigm and the allograft response. Curr. Opin. Immunol. 8: 688-693.
28. Oldenhove, G., M. de Heusch, G. Urbain-Vansanten, J. Urbain, C. Maliszewski, O. Leo, and M. Moser. 2003. CD4+ CD25+ regulatory T cells control T helper cell type 1 responses to foreign antigens induced by mature dendritic cells in vivo. J. Exp. Med. 198: 259-266.
29. de Bont, E. S., C. R. Reilly, D. Lo, L. H. Glimcher, and T. M. Laufer. 1999. A minimal level of MHC class II expression is sufficient to abrogate autoreactivity. Int. Immunol. 11: 1295-1306.
30. Cobbold, S. P., and H. Waldmann. 1998. Infectious tolerance. Curr. Opin. Immunol. 10: 518-524.
31. Suri-Payer, E., A. Z. Amar, A. M. Thornton, and E. M. Shevach. 1998. CD4+CD25 + T cells inhibit both the induction and effector function of autoreactive T cells and represent a unique lineage of immunoregulatory cells. J. Immunol. 160: 1212-1218. (Pubitemid 28093417)
32. Roelen, D. L., J. J. van Rood, A. Brand, and F. H. Claas. 2000. Immunomodulation by blood transfusions. Vox Sang. 78(Suppl. 2): 273-275.
33. Qin, S., S. P. Cobbold, H. Pope, J. Elliott, D. Kioussis, J. Davies, and H. Waldmann. 1993. "Infectious" transplantation tolerance. Science 259: 974-977.
34. Madsen, J. C., R. A. Superina, K. J. Wood, and P. J. Morris. 1988. Immunological unresponsiveness induced by recipient cells transfected with donor MHC genes. Nature 332: 161-164.
35. Fraser, C. C., M. Sykes, R. S. Lee, D. H. Sachs, and C. LeGuern. 1995. Specific unresponsiveness to a retrovirally-transferred class I antigen is controlled through the helper pathway. J. Immunol. 154: 1587-1595.
36. McDevitt, H. O. 2000. Discovering the role of the major histocompatibility complex in the immune response. Annu. Rev. Immunol. 18: 1-17.
37. Libby, P., and J. S. Pober. 2001. Chronic rejection. Immunity 14: 387-397.
38. Shirasugi, N., A. B. Adams, M. M. Durham, A. E. Lukacher, H. Xu, P. Rees, S. R. Cowan, M. A. Williams, T. C. Pearson, and C. P. Larsen. 2002. Prevention of chronic rejection in murine cardiac allografts: a comparison of chimerism-and nonchimerism-inducing costimulation blockade-based tolerance induction regimens. J. Immunol. 169: 2677-2684. (Pubitemid 34921016)
39. Adler, A. J., D. W. Marsh, G. S. Yochum, J. L. Guzzo, A. Nigam, W. G. Nelson, and D. M. Pardoll. 1998. CD4+ T cell tolerance to parenchymal self-antigens requires presentation by bone marrow-derived antigen-presenting cells. J. Exp. Med. 187: 1555-1564.
40. Umemura, A., A. P. Monaco, and T. Maki. 2000. Donor MHC class II antigen is essential for induction of transplantation tolerance by bone marrow cells. J. Immunol. 164: 4452-4457. (Pubitemid 30238039)
41. Denaro, M., D. Kolber-Simonds, V. Schad, S. Muthukumar, S. Germana, M. E. White-Scharf, P. T. Banerjee, C. LeGuern, and G. Andersson. 2002. Expression of xenogeneic MHC class II molecules in HLA-DR+ and -DR(-) cells: influence of retrovirus vector design and cellular context. Xenotransplantation 9: 115-124. (Pubitemid 36358968)
42. Kingsley, C. I., M. Karim, A. R. Bushell, and K. J. Wood. 2002. CD25+CD4+ regulatory T cells prevent graft rejection: CTLA-4- and IL-10-dependent immunoregulation of alloresponses. J. Immunol. 168: 1080-1086.
43. van Rood, J. J., and F. H. Claas. 1990. The influence of allogeneic cells on the human T and B cell repertoire. Science 248: 1388-1393. (Pubitemid 20208191)
44. Thornton, A. M., and E. M. Shevach. 2000. Suppressor effector function of CD4+CD25+ immunoregulatory T cells is antigen nonspecific. J. Immunol. 164: 183-190.
45. Chaturvedi, P., B. Agrawal, M. Zechel, E. Lee-Chan, and B. Singh. 2000. A self MHC class II β-chain peptide prevents diabetes in nonobese diabetic mice. J. Immunol. 164: 6610-6620. (Pubitemid 30408848)
46. Gonzalez-Gay, M. A., G. H. Nabozny, M. J. Bull, E. Zanelli, J. Douhan, 3rd, M. M. Griffiths, L. H. Glimcher, H. S. Luthra, and C. S. David. 1994. Protective role of major histocompatibility complex class II Ebd transgene on collagen-induced arthritis. J. Exp. Med. 180: 1559-1564.
47. Murphy, D. B., S. Rath, E. Pizzo, A. Y. Rudensky, A. George, J. K. Larson, and C. A. Janeway, Jr. 1992. Monoclonal antibody detection of a major self peptide. MHC class II complex. J. Immunol. 148: 3483-3491.