Compensatory Mechanisms Allow Undersized Anchor-Deficient Class i MHC Ligands to Mediate Pathogenic Autoreactive T Cell Responses

Journal of Immunology

Volumn 193, Issue 5, 2014, Pages 2135-2146

  Lamont, Deanna ^a   Mukherjee, Gayatri ^b   Kumar, P Rajesh ^b   Samanta, Dibyendu ^b   McPhee, Caroline G ^a   Kay, Thomas W H ^c,d   Almo, Steven C ^b   DiLorenzo, Teresa P ^b   Serreze, David V ^a  

^a JACKSON LABORATORY   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GLUCOSE 6 PHOSPHATASE; ISLET SPECIFIC GLUCOSE 6 PHOSPHATASE CATALYTIC SUBUNIT RELATED PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROINSULIN; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; HLA ANTIGEN CLASS 1; PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; AUTOIMMUNE DISEASE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; CYTOTOXIC T LYMPHOCYTE; INSULIN DEPENDENT DIABETES MELLITUS; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; PURIFYING SELECTION; T LYMPHOCYTE; ANIMAL; CHEMISTRY; EXPERIMENTAL DIABETES MELLITUS; GENETICS; IMMUNOLOGY; PATHOLOGY; STRUCTURE ACTIVITY RELATION; TRANSGENIC MOUSE; X RAY CRYSTALLOGRAPHY;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CRYSTALLOGRAPHY, X-RAY; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; HISTOCOMPATIBILITY ANTIGENS CLASS I; MICE; MICE, INBRED NOD; MICE, TRANSGENIC; PEPTIDES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84907024857     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400997     Document Type: Article

References (40)

1. Serreze, D. V., E. H. Leiter, G. J. Christianson, D. Greiner, and D. C. Roopenian. 1994. Major histocompatibility complex class I-deficient NOD-B2mnull mice are diabetes and insulitis resistant. Diabetes 43: 505-509.
2. 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 disassociation of autoimmunity and resistance to costimulation blockade-induced transplantation tolerance in nonobese diabetic mice. J. Immunol. 171: 185-195.
3. In't Veld, P. 2011. Insulitis in human type 1 diabetes: The quest for an elusive lesion. Islets 3: 131-138.
4. 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.
5. 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.
6. Wong, F. S., J. Karttunen, C. Dumont, L. Wen, I. Visintin, I. M. Pilip, N. Shastri, E. G. Pamer, and C. A. Janeway, Jr. 1999. Identification of an MHC class Irestricted autoantigen in type 1 diabetes by screening an organ-specific cDNA library. Nat. Med. 5: 1026-1031.
7. Wong, F. S., L. K. Siew, G. Scott, I. J. Thomas, S. Chapman, C. Viret, and L. Wen. 2009. Activation of insulin-reactive CD8 T-cells for development of autoimmune diabetes. Diabetes 58: 1156-1164.
8. DiLorenzo, T. P., S. M. Lieberman, T. Takaki, S. Honda, H. D. Chapman, P. Santamaria, D. V. Serreze, and S. G. Nathenson. 2002. During the early prediabetic period in NOD mice, the pathogenic CD8+ T-cell population comprises multiple antigenic specificities. Clin. Immunol. 105: 332-341.
9. 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.
10. DiLorenzo, T. P., R. T. Graser, T. Ono, G. J. Christianson, H. D. Chapman, D. C. Roopenian, S. G. Nathenson, and D. V. Serreze. 1998. Major histocompatibility complex class I-restricted T cells are required for all but the end stages of diabetes development in nonobese diabetic mice and use a prevalent T cell receptor a chain gene rearrangement. Proc. Natl. Acad. Sci. USA 95: 12538-12543.
11. Takaki, T., S. M. Lieberman, T. M. Holl, B. Han, P. Santamaria, D. V. Serreze, and T. P. DiLorenzo. 2004. Requirement for both H-2Db and H-2Kd for the induction of diabetes by the promiscuous CD8+ T cell clonotype AI4. J. Immunol. 173: 2530-2541.
12. 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.
13. Krishnamurthy, B., N. L. Dudek, M. D. McKenzie, A. W. Purcell, A. G. Brooks, S. Gellert, P. G. Colman, L. C. Harrison, A. M. Lew, H. E. Thomas, and T. W. Kay. 2006. Responses against islet antigens in NOD mice are prevented by tolerance to proinsulin but not IGRP. J. Clin. Invest. 116: 3258-3265.
14. Krishnamurthy, B., L. Mariana, S. A. Gellert, P. G. Colman, L. C. Harrison, A. M. Lew, P. Santamaria, H. E. Thomas, and T. W. Kay. 2008. Autoimmunity to both proinsulin and IGRP is required for diabetes in nonobese diabetic 8.3 TCR transgenic mice. J. Immunol. 180: 4458-4464.
15. French, M. B., J. Allison, D. S. Cram, H. E. Thomas, M. Dempsey-Collier, A. Silva, H. M. Georgiou, T. W. Kay, L. C. Harrison, and A. M. Lew. 1997. Transgenic expression of mouse proinsulin II prevents diabetes in nonobese diabetic mice. Diabetes 46: 34-39.
16. Thébault-Baumont, K., D. Dubois-Laforgue, P. Krief, J. P. Briand, P. Halbout, K. Vallon-Geoffroy, J. Morin, V. Laloux, A. Lehuen, J. C. Carel, et al. 2003. Acceleration of type 1 diabetes mellitus in proinsulin 2-deficient NOD mice. J. Clin. Invest. 111: 851-857.
17. Garboczi, D. N., P. Ghosh, U. Utz, Q. R. Fan, W. E. Biddison, and D. C. Wiley. 1996. Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature 384: 134-141.
18. Zhang, X., J. C. Schwartz, S. C. Almo, and S. G. Nathenson. 2002. Expression, refolding, purification, molecular characterization, crystallization, and preliminary X-ray analysis of the receptor binding domain of human B7-2. Protein Expr. Purif. 25: 105-113.
19. Adams, P. D., P. V. Afonine, G. Bunkóczi, V. B. Chen, I. W. Davis, N. Echols, J. J. Headd, L. W. Hung, G. J. Kapral, R. W. Grosse-Kunstleve, et al. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66: 213-221.
20. Strong, M., M. R. Sawaya, S. Wang, M. Phillips, D. Cascio, and D. Eisenberg. 2006. Toward the structural genomics of complexes: crystal structure of a PE/ PPE protein complex from Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 103: 8060-8065.
21. Jarchum, I., T. Takaki, and T. P. DiLorenzo. 2008. Efficient culture of CD8+ T cells from the islets of NOD mice and their use for the study of autoreactive specificities. J. Immunol. Methods 339: 66-73.
22. Moodie, Z., L. Price, C. Gouttefangeas, A. Mander, S. Janetzki, M. Löwer, M. J. Welters, C. Ottensmeier, S. H. van der Burg, and C. M. Britten. 2010. Response definition criteria for ELISPOT assays revisited. Cancer Immunol. Immunother. 59: 1489-1501.
23. Aschenbrenner, K., L. M. D'Cruz, E. H. Vollmann, M. Hinterberger, J. Emmerich, L. K. Swee, A. Rolink, and L. Klein. 2007. Selection of Foxp3+ regulatory T cells specific for self antigen expressed and presented by Aire+ medullary thymic epithelial cells. Nat. Immunol. 8: 351-358.
24. Falk, K., O. Rötzschke, S. Stevanović, G. Jung, and H. G. Rammensee. 1991. Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 351: 290-296.
25. 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.
26. Amrani, A., P. Serra, J. Yamanouchi, J. D. Trudeau, R. Tan, J. F. Elliott, and P. Santamaria. 2001. Expansion of the antigenic repertoire of a single T cell receptor upon T cell activation. J. Immunol. 167: 655-666.
27. Derbinski, J., A. Schulte, B. Kyewski, and L. Klein. 2001. Promiscuous gene expression in medullary thymic epithelial cells mirrors the peripheral self. Nat. Immunol. 2: 1032-1039.
28. Anderson, M. S., and M. A. Su. 2011. Aire and T cell development. Curr. Opin. Immunol. 23: 198-206.
29. Glithero, A., J. Tormo, J. S. Haurum, G. Arsequell, G. Valencia, J. Edwards, S. Springer, A. Townsend, Y. L. Pao, M. Wormald, et al. 1999. Crystal structures of two H-2Db/glycopeptide complexes suggest a molecular basis for CTL crossreactivity. Immunity 10: 63-74.
30. Young, A. C., W. Zhang, J. C. Sacchettini, and S. G. Nathenson. 1994. The threedimensional structure of H-2Db at 2.4 A resolution: implications for antigendeterminant selection. Cell 76: 39-50.
31. 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.
32. Li, L., B. Wang, J. A. Frelinger, and R. Tisch. 2008. T-cell promiscuity in autoimmune diabetes. Diabetes 57: 2099-2106.
33. 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.
34. Wooldridge, L., J. Ekeruche-Makinde, H. A. van den Berg, A. Skowera, J. J. Miles, M. P. Tan, G. Dolton, M. Clement, S. Llewellyn-Lacey, D. A. Price, et al. 2012. A single autoimmune T cell receptor recognizes more than a million different peptides. J. Biol. Chem. 287: 1168-1177.
35. Chaparro, R. J., A. R. Burton, D. V. Serreze, D. A. Vignali, and T. P. DiLorenzo. 2008. Rapid identification of MHC class I-restricted antigens relevant to autoimmune diabetes using retrogenic T cells. J. Immunol. Methods 335: 106-115.
36. Fremont, D. H., M. Matsumura, E. A. Stura, P. A. Peterson, and I. A. Wilson. 1992. Crystal structures of two viral peptides in complex with murine MHC class I H-2Kb. Science 257: 919-927.
37. Glithero, A., J. Tormo, K. Doering, M. Kojima, E. Y. Jones, and T. Elliott. 2006. The crystal structure of H-2Db complexed with a partial peptide epitope suggests a major histocompatibility complex class I assembly intermediate. J. Biol. Chem. 281: 12699-12704.
38. Jarchum, I., and T. P. DiLorenzo. 2010. Ins2 deficiency augments spontaneous HLA-A∗0201-restricted T cell responses to insulin. J. Immunol. 184: 658-665.
39. Mallone, R., E. Martinuzzi, P. Blancou, G. Novelli, G. Afonso, M. Dolz, G. Bruno, L. Chaillous, L. Chatenoud, J.-M. Bach, and P. van Endert. 2007. CD8+ T-cell responses identify b-cell autoimmunity in human type 1 diabetes. Diabetes 56: 613-621.
40. Karges, W., T. Rajasalu, A. Spyrantis, A. Wieland, B. Boehm, and R. Schirmbeck. 2007. The diabetogenic, insulin-specific CD8 T cell response primed in the experimental autoimmune diabetes model in RIP-B7.1 mice. Eur. J. Immunol. 37: 2097-2103.