Dendritic cell-dependent in vivo generation of autoregulatory T cells by antidiabetogenic MHC class II

Journal of Immunology

Volumn 191, Issue 1, 2013, Pages 70-82

  Tsai, Sue ^a   Serra, Pau ^b   Clemente Casares, Xavier ^a   Slattery, Robyn M ^c   Santamaria, Pere ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b HOSPITAL CLÍNIC   (Spain)

^c MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; B LYMPHOCYTE; CD4+ FOXP3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; GENE; GENE EXPRESSION; I E GENE; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; LYMPH NODE; MOUSE; NONHUMAN; PANCREAS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; TRANSGENIC MOUSE;

ANIMALS; CELL DIFFERENTIATION; DENDRITIC CELLS; DIABETES MELLITUS, EXPERIMENTAL; GENES, MHC CLASS II; INTEGRASES; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; MICE, TRANSGENIC; T-LYMPHOCYTES, REGULATORY;

EID: 84879674278     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300168     Document Type: Article

References (65)

1. Wang, W. Y., B. J. Barratt, D. G. Clayton, and J. A. Todd. 2005. Genome-wide association studies: theoretical and practical concerns. Nat. Rev. Genet. 6: 109-118. (Pubitemid 40179533)
2. Barton, N. H., and P. D. Keightley. 2002. Understanding quantitative genetic variation. Nat. Rev. Genet. 3: 11-21. (Pubitemid 34506600)
3. MacKay, K., S. Eyre, A. Myerscough, A. Milicic, A. Barton, S. Laval, J. Barrett, D. Lee, S. White, S. John, et al. 2002. Whole-genome linkage analysis of rheumatoid arthritis susceptibility loci in 252 affected sibling pairs in the United Kingdom. Arthritis Rheum. 46: 632-639. (Pubitemid 34214245)
4. Hafler, D. A., A. Compston, S. Sawcer, E. S. Lander, M. J. Daly, P. L. De Jager, P. I. de Bakker, S. B. Gabriel, D. B. Mirel, A. J. Ivinson, et al. 2007. Risk alleles for multiple sclerosis identified by a genomewide study. N. Engl. J. Med. 357:851-862. (Pubitemid 47347319)
5. Nejentsev, S., J. M. Howson, N. M. Walker, J. Szeszko, S. F. Field, H. E. Stevens, P. Reynolds, M. Hardy, E. King, J. Masters, et al. 2007. Localization of type 1 diabetes susceptibility to the MHC class I genes HLA-B and HLA-A. Nature 450: 887-892.
6. Erlich, H., A. M. Valdes, J. Noble, J. A. Carlson, M. Varney, P. Concannon, J. C. Mychaleckyj, J. A. Todd, P. Bonella, A. L. Fear, et al. 2008. HLA DR-DQ haplotypes and genotypes and type 1 diabetes risk: analysis of the type 1 diabetes genetics consortium families. Diabetes 57: 1084-1092.
7. Todd, J. A., J. I. Bell, and H. O. McDevitt. 1987. HLA-DQ β gene contributes to susceptibility and resistance to insulin-dependent diabetes mellitus. Nature 329: 599-604. (Pubitemid 17140111)
8. Howson, J. M., N. M. Walker, D. Clayton, and J. A. Todd, and; Type 1 Diabetes Genetics Consortium. 2009. Confirmation of HLA class II independent type 1 diabetes associations in the major histocompatibility complex including HLA-B and HLA-A. Diabetes Obes. Metab. 11(Suppl. 1): 31-45.
9. Tisch, R., and H. McDevitt. 1996. Insulin-dependent diabetes mellitus. Cell 85: 291-297. (Pubitemid 26160699)
10. Vyse, T. J., and J. A. Todd. 1996. Genetic analysis of autoimmune disease. Cell 85: 311-318. (Pubitemid 26160703)
11. Acha-Orbea, H., and H. O. McDevitt. 1987. The first external domain of the nonobese diabetic mouse class II I-A β chain is unique. Proc. Natl. Acad. Sci. USA 84: 2435-2439. (Pubitemid 17075881)
12. Uehira, M., M. Uno, T. Kürner, H. Kikutani, K. Mori, T. Inomoto, T. Uede, J. Miyazaki, H. Nishimoto, T. Kishimoto, et al. 1989. Development of autoimmune insulitis is prevented in Ea d but not in Abk NOD transgenic mice. Int. Immunol. 1: 209-213. (Pubitemid 19260473)
13. 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.
14. Reich, E. P., R. S. Sherwin, O. Kanagawa, and C. A. Janeway, Jr. 1989. An explanation for the protective effect of the MHC class II I-E molecule in murine diabetes. Nature 341: 326-328. (Pubitemid 20102100)
15. Miyazaki, T., M. Uno, M. Uehira, H. Kikutani, T. Kishimoto, M. Kimoto, H. Nishimoto, J. Miyazaki, and K. Yamamura. 1990. Direct evidence for the contribution of the unique I-ANOD to the development of insulitis in non-obese diabetic mice. Nature 345: 722-724.
16. Katz, J. D., B. Wang, K. Haskins, C. Benoist, and D. Mathis. 1993. Following a diabetogenic T cell from genesis through pathogenesis. Cell 74: 1089-1100. (Pubitemid 23289465)
17. Böhme, J., B. Schuhbaur, O. Kanagawa, C. Benoist, and D. Mathis. 1990. MHC-linked protection from diabetes dissociated from clonal deletion of T cells. Science 249: 293-295.
18. Slattery, R. M., L. Kjer-Nielsen, J. Allison, B. Charlton, T. E. Mandel, and J. F. Miller. 1990. Prevention of diabetes in non-obese diabetic I-Ak transgenic mice. Nature 345: 724-726.
19. 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: 67-77.
20. Singer, S. M., R. Tisch, X. D. Yang, and H. O. McDevitt. 1993. An Abd transgene prevents diabetes in nonobese diabetic mice by inducing regulatory T cells. Proc. Natl. Acad. Sci. USA 90: 9566-9570. (Pubitemid 23315826)
21. Parish, N. M., P. Chandler, R. Quartey-Papafio, E. Simpson, and A. Cooke. 1993. The effect of bone marrow and thymus chimerism between non-obese diabetic (NOD) and NOD-E transgenic mice, on the expression and prevention of diabetes. Eur. J. Immunol. 23: 2667-2675. (Pubitemid 23295154)
22. Verdaguer, J., D. Schmidt, A. Amrani, B. Anderson, N. Averill, and P. Santamaria. 1997. Spontaneous autoimmune diabetes in monoclonal T cell nonobese diabetic mice. J. Exp. Med. 186: 1663-1676. (Pubitemid 27506280)
23. 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. (Pubitemid 27441150)
24. Schmidt, D., A. Amrani, J. Verdaguer, S. Bou, and P. Santamaria. 1999. Autoantigen-independent deletion of diabetogenic CD4+ thymocytes by protective MHC class II molecules. J. Immunol. 162: 4627-4636. (Pubitemid 29314862)
25. Thiessen, S., P. Serra, A. Amrani, J. Verdaguer, and P. Santamaria. 2002. T-cell tolerance by dendritic cells and macrophages as a mechanism for the major histocompatibility complex-linked resistance to autoimmune diabetes. Diabetes 51: 325-338. (Pubitemid 34764787)
26. Kanagawa, O., B. A. Vaupel, G. Xu, E. R. Unanue, and J. D. Katz. 1998. Thymic positive selection and peripheral activation of islet antigen-specific T cells: separation of two diabetogenic steps by an I-A(g7) class II MHC beta-chain mutant. J. Immunol. 161: 4489-4492. (Pubitemid 28492017)
27. Lühder, F., J. Katz, C. Benoist, and D. Mathis. 1998. Major histocompatibility complex class II molecules can protect from diabetes by positively selecting T cells with additional specificities. J. Exp. Med. 187: 379-387.
28. Rickert, R. C., J. Roes, and K. Rajewsky. 1997. B lymphocyte-specific, Cremediated mutagenesis in mice. Nucleic Acids Res. 25: 1317-1318.
29. Caton, M. L., M. R. Smith-Raska, and B. Reizis. 2007. Notch-RBP-J signaling controls the homeostasis of CD8- dendritic cells in the spleen. J. Exp. Med. 204: 1653-1664. (Pubitemid 47048031)
30. Anderson, B., B. J. Park, J. Verdaguer, A. Amrani, and P. Santamaria. 1999. Prevalent CD8+ T cell response against one peptide/MHC complex in autoimmune diabetes. Proc. Natl. Acad. Sci. USA 96: 9311-9316. (Pubitemid 29374751)
31. Stratmann, T., N. Martin-Orozco, V. Malet-Designe, L. Poirot, D. McGavern, G. Losyev, C. M. Dobbs, M. B. Oldstone, K. Yoshida, H. Kikutani, et al. 2003. Susceptible MHC alleles, not background genes, select an autoimmune T cell reactivity. J. Clin. Invest. 112: 902-914. (Pubitemid 38063748)
32. Dash, P., J. L. McClaren, T. H. Oguin, III, W. Rothwell, B. Todd, M. Y. Morris, J. Becksfort, C. Reynolds, S. A. Brown, P. C. Doherty, and P. G. Thomas. 2011. Paired analysis of TCRα and TCRβ chains at the single-cell level in mice. J. Clin. Invest. 121: 288-295.
33. Verdaguer, J., J. W. Yoon, B. Anderson, N. Averill, T. Utsugi, B. J. Park, and P. Santamaria. 1996. Acceleration of spontaneous diabetes in TCR-β-transgenic nonobese diabetic mice by β-cell cytotoxic CD8+ T cells expressing identical endogenous TCR-a chains. J. Immunol. 157: 4726-4735. (Pubitemid 126449398)
34. Deng, H., R. Apple, M. Clare-Salzler, S. Trembleau, D. Mathis, L. Adorini, and E. Sercarz. 1993. Determinant capture as a possible mechanism of protection afforded by major histocompatibility complex class II molecules in autoimmune disease. J. Exp. Med. 178: 1675-1680. (Pubitemid 23318446)
35. Roberts, S. A., G. Barbour, M. R. Matarrese, D. L. Mason, E. H. Leiter, K. Haskins, and M. S. Hanson. 2003. Adoptive transfer of islet antigen-autoreactive T cell clones to transgenic NOD.Ea(d)mice induces diabetes indicating a lack of I-E mediated protection against activated effector T cells. J. Autoimmun. 21: 139-147. (Pubitemid 36993726)
36. Trembleau, S., S. Gregori, G. Penna, I. Gorny, and L. Adorini. 2001. IL-12 administration reveals diabetogenic T cells in genetically resistant I-Eα-transgenic nonobese diabetic mice: resistance to autoimmune diabetes is associated with binding of Eα-derived peptides to the I-A(g7) molecule. J. Immunol. 167: 4104-4114. (Pubitemid 32910859)
37. Amrani, A., J. Verdaguer, P. Serra, S. Tafuro, R. Tan, and P. Santamaria. 2000. Progression of autoimmune diabetes driven by avidity maturation of a T-cell population. Nature 406: 739-742.
38. Lieberman, S. M., A. M. Evans, B. Han, T. Takaki, Y. Vinnitskaya, J. A. Caldwell, D. V. Serreze, J. Shabanowitz, D. F. Hunt, S. G. Nathenson, et al. 2003. Identification of the β cell antigen targeted by a prevalent population of pathogenic CD8+ T cells in autoimmune diabetes. Proc. Natl. Acad. Sci. USA 100: 8384-8388. (Pubitemid 36842554)
39. 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 nonobese diabetic mice. J. Immunol. 172: 871-879. (Pubitemid 38113744)
40. Hanabuchi, S., T. Ito, W. R. Park, N. Watanabe, J. L. Shaw, E. Roman, K. Arima, Y. H. Wang, K. S. Voo, W. Cao, and Y. J. Liu. 2010. Thymic stromal lymphopoietin-activated plasmacytoid dendritic cells induce the generation of FOXP3+ regulatory T cells in human thymus. J. Immunol. 184: 2999-3007.
41. Serra, P., A. Amrani, J. Yamanouchi, B. Han, S. Thiessen, T. Utsugi, J. Verdaguer, and P. Santamaria. 2003. CD40 ligation releases immature dendritic cells from the control of regulatory CD4+CD25+ T cells. Immunity 19: 877-889. (Pubitemid 37542307)
42. Tang, Q., J. Y. Adams, A. J. Tooley, M. Bi, B. T. Fife, P. Serra, P. Santamaria, R. M. Locksley, M. F. Krummel, and J. A. Bluestone. 2006. Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat. Immunol. 7: 83-92. (Pubitemid 41823872)
43. Yamanouchi, J., M. C. Puertas, J. Verdaguer, P. A. Lyons, D. B. Rainbow, G. Chamberlain, K. M. Hunter, L. B. Peterson, L. S. Wicker, and P. Santamaria. 2010. Idd9.1 locus controls the suppressive activity of FoxP3+CD4+CD25+regulatory T-cells. Diabetes 59: 272-281.
44. Yamanouchi, J., D. Rainbow, P. Serra, S. Howlett, K. Hunter, V. E. Garner, A. Gonzalez-Munoz, J. Clark, R. Veijola, R. Cubbon, et al. 2007. Interleukin-2 gene variation impairs regulatory T cell function and causes autoimmunity. Nat. Genet. 39: 329-337. (Pubitemid 46328484)
45. 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 hemopoietically derived antigen-presenting cells in transgenic NOD/Lt mice determine level of diabetes resistance and indicate mechanism of protection. J. Immunol. 157: 1279-1287. (Pubitemid 126449645)
46. Pilström, B., and J. Böhme. 1997. Alleviation of insulitis in NOD mice is associated with expression of transgenic MHC E molecules on primary antigen-presenting cells. Immunology 90: 483-488.
47. Tsai, S., P. Serra, X. Clemente-Casares, J. Yamanouchi, S. Thiessen, R. M. Slattery, J. F. Elliott, and P. Santamaria. 2013. Antidiabetogenic MHC class II promotes the differentiation of MHC-promiscuous autoreactive T cells into FOXP3+ regulatory T cells. Proc. Natl. Acad. Sci. USA 110: 3471-3476.
48. Bill, J., V. B. Appel, and E. Palmer. 1988. An analysis of T-cell receptor variable region gene expression in major histocompatibility complex disparate mice. Proc. Natl. Acad. Sci. USA 85: 9184-9188. (Pubitemid 19001862)
49. Tomonari, K., and E. Lovering. 1988. T-cell receptor-specific monoclonal antibodies against a Vβ11-positive mouse T-cell clone. Immunogenetics 28: 445-451. (Pubitemid 18262878)
50. Nakano, N., H. Kikutani, H. Nishimoto, and T. Kishimoto. 1991. T cell receptor V gene usage of islet β cell-reactive T cells is not restricted in non-obese diabetic mice. J. Exp. Med. 173: 1091-1097.
51. Kappler, J. W., N. Roehm, and P. Marrack. 1987. T cell tolerance by clonal elimination in the thymus. Cell 49: 273-280.
52. Brenden, N., and J. Böhme. 1998. Disease-protected major histocompatibility complex Ea-transgenic non-obese diabetic (NOD) mice show interleukin-4 production not seen in susceptible Ea-transgenic and non-transgenic NOD mice. Immunology 95: 1-7.
53. 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. (Pubitemid 32747556)
54. Mellanby, R. J., J. M. Phillips, N. M. Parish, and A. Cooke. 2008. Both central and peripheral tolerance mechanisms play roles in diabetes prevention in NOD-E transgenic mice. Autoimmunity 41: 383-394. (Pubitemid 351891200)
55. Singer, S. M., R. Tisch, X. D. Yang, H. K. Sytwu, R. Liblau, and H. O. McDevitt. 1998. Prevention of diabetes in NOD mice by a mutated I-Ab transgene. Diabetes 47: 1570-1577. (Pubitemid 28445344)
56. O'Shea, H., N. Yousaf, D. Altmann, Z. Fehervari, P. Tonks, C. Hetherington, S. Harach, C. Bland, A. Cooke, and T. Lund. 2006. Effect of X- and Y-box deletions on the development of diabetes in H-2Eα-chain transgenic nonobese diabetic mice. Scand. J. Immunol. 63: 17-25.
57. Chen, Y. G., P. A. Silveira, M. A. Osborne, H. D. Chapman, and D. V. Serreze. 2007. Cellular expression requirements for inhibition of type 1 diabetes by a dominantly protective major histocompatibility complex haplotype. Diabetes 56: 424-430.
58. Samy, E. T., L. A. Parker, C. P. Sharp, and K. S. Tung. 2005. Continuous control of autoimmune disease by antigen-dependent polyclonal CD4+CD25+ regulatory T cells in the regional lymph node. J. Exp. Med. 202: 771-781. (Pubitemid 41345966)
59. Tarbell, K. V., S. Yamazaki, K. Olson, P. Toy, and R. M. Steinman. 2004. CD25+CD4+ T cells, expanded with dendritic cells presenting a single autoantigenic peptide, suppress autoimmune diabetes. J. Exp. Med. 199: 1467-1477. (Pubitemid 38780402)
60. Friese, M. A., K. B. Jakobsen, L. Friis, R. Etzensperger, M. J. Craner, R. M. McMahon, L. T. Jensen, V. Huygelen, E. Y. Jones, J. I. Bell, and L. Fugger. 2008. Opposing effects of HLA class I molecules in tuning autoreactive CD8+T cells in multiple sclerosis. Nat. Med. 14: 1227-1235.
61. Wucherpfennig, K. W., M. J. Call, L. Deng, and R. Mariuzza. 2009. Structural alterations in peptide-MHC recognition by self-reactive T cell receptors. Curr. Opin. Immunol. 21: 590-595.
62. Schubert, D. A., S. Gordo, J. J. Sabatino, Jr., S. Vardhana, E. Gagnon, D. K. Sethi, N. P. Seth, K. Choudhuri, H. Reijonen, G. T. Nepom, et al. 2012. Self-reactive human CD4 T cell clones form unusual immunological synapses. J. Exp. Med. 209: 335-352.
63. Han, B., P. Serra, J. Yamanouchi, A. Amrani, J. F. Elliott, P. Dickie, T. P. Dilorenzo, and P. Santamaria. 2005. Developmental control of CD8 T cell-avidity maturation in autoimmune diabetes. J. Clin. Invest. 115: 1879-1887. (Pubitemid 40979727)
64. Stadinski, B. D., T. Delong, N. Reisdorph, R. Reisdorph, R. L. Powell, M. Armstrong, J. D. Piganelli, G. Barbour, B. Bradley, F. Crawford, et al. 2010. Chromogranin A is an autoantigen in type 1 diabetes. Nat. Immunol. 11: 225-231.
65. Nikoopour, E., C. Sandrock, K. Huszarik, O. Krougly, E. Lee-Chan, E. L. Masteller, J. A. Bluestone, and B. Singh. 2011. Cutting edge: vasostatin-1-derived peptide ChgA29-42 is an antigenic epitope of diabetogenic BDC2.5 T cells in nonobese diabetic mice. J. Immunol. 186: 3831-3835.