Systematic analysis of the combinatorial nature of epitopes recognized by TCR leads to identification of mimicry epitopes for glutamic acid decarboxylase 65-specific TCRs

Journal of Immunology

Volumn 170, Issue 2, 2003, Pages 947-960

  Uemura, Yasushi ^a   Senju, Satoru ^a   Maenaka, Katsumi ^c,d   Iwai, Leo Kei ^a,e   Fujii, Shinji ^a,b   Tabata, Hiroki ^a,b   Tsukamoto, Hirotake ^a   Hirata, Shinya ^a   Chen, Yu Zhen ^a   Nishimura, Yasuharu ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b KUMAMOTO UNIV SCHOOL OF MEDICINE   (Japan)

^c NATIONAL INSTITUTE OF GENETICS   (Japan)

^d GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^e UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CYTOKINE; EPITOPE; GAMMA INTERFERON; GENOMIC DNA; GLUTAMATE DECARBOXYLASE; HLA DR ANTIGEN; SYNTHETIC PEPTIDE; T LYMPHOCYTE RECEPTOR;

ANTIGEN RECOGNITION; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INSULIN DEPENDENT DIABETES MELLITUS; LYMPHOCYTE CLONE; LYMPHOCYTE PROLIFERATION; NORTHERN BLOTTING; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION;

EID: 0037438470     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.170.2.947     Document Type: Article

References (53)

1. Oldstone, M. B. 1998. Molecular mimicry and immune-mediated diseases. FASEB J. 12:1255.
2. Wucherpfennig, K. W., and J. L. Strominger. 1995. Molecular mimicry in T cell-mediated autoimmunity: viral peptides activate human T cell clones specific for myelin basic protein. Cell 80:695.
3. Panoutsakopoulou, V., M. E. Sanchirico, K. M. Huster, M. Jansson, F. Granucci, D. J. Shim, K. W. Wucherpfennig, and H. Cantor. 2001. Analysis of the relationship between viral infection and autoimmune disease. Immunity 15:137.
4. Loftus, C., E. Huseby, P. Gopaul, C. Beeson, and J. Goverman. 1999. Highly cross-reactive T cell responses to myelin basic protein epitopes reveal a nonpredictable form of TCR degeneracy. J. Immunol. 162:6451.
5. Nanda, N. K., K. K. Arzoo, H. M. Geysen, A. Sette, and E. E. Sercarz. 1995. Recognition of multiple peptide cores by a single T cell receptor. J. Exp. Med. 182:531.
6. Quaratino, S., C. J. Thorpe, P. J. Travers, and M. Londei. 1995. Similar antigenic surfaces, rather than sequence homology, dictate T-cell epitope molecular mimicry. Proc. Natl. Acad. Sci. USA 92:10398.
7. Hemmer, B., B. T. Fleckenstein, M. Vergelli, G. Jung, H. McFarland, R. Martin, and K. H. Wiesmuller. 1997. Identification of high potency microbial and self ligands for a human autoreactive class II-restricted T cell clone. J. Exp. Med. 185:1651.
8. Hausmann, S., M. Martin, L. Gauthier, and K. W. Wucherpfennig. 1999. Structural features of autoreactive TCR that determine the degree of degeneracy in peptide recognition. J. Immunol. 162:338.
9. De Magistris, M. T., J. Alexander, M. Coggeshall, A. Altman, F. C. Gaeta, H. M. Grey, and A. Sette. 1992. Antigen analog-major histocompatibility complexes act as antagonists of the T cell receptor. Cell 68:625.
10. Combadiere, B., M. Freedman, L. Chen, E. W. Shores, P. Love, and M. J. Lenardo. 1996. Qualitative and quantitative contributions of the T cell receptor ψ chain to mature T cell apoptosis. J. Exp. Med. 183:2109.
11. Sloan-Lancaster, J., B. D. Evavold, and P. M. Allen. 1993. Induction of T-cell anergy by altered T-cell-receptor ligand on live antigen-presenting cells. Nature 363:156.
12. Kersh, G. J., and P. M. Allen. 1996. Structural basis for T cell recognition of altered peptide ligands: a single T cell receptor can productively recognize a large continuum of related ligands. J. Exp. Med. 184:1259.
13. Kersh, G. J., M. J. Miley, C. A. Nelson, A. Grakoui, S. Horvath, D. L. Donermeyer, J. Kappler, P. M. Allen, and D. H. Fremont. 2001. Structural and functional consequences of altering a peptide MHC anchor residue. J. Immunol. 166:3345.
14. Ausubel, L. J., C. K. Kwan, A. Sette, V. Kuchroo, and D. A. Hafler. 1996. Complementary mutations in an antigenic peptide allow for crossreactivity of autoreactive T-cell clones. Proc. Natl. Acad. Sci. USA 93:15317.
15. Leggatt, G. R., A. Hosmalin, C. D. Pendleton, A. Kumar, S. Hoffman, and J. A. Berzofsky. 1998. The importance of pairwise interactions between peptide residues in the delineation of TCR specificity. J. Immunol. 161:4728.
16. Hemmer, B., C. Pinilla, B. Gran, M. Vergelli, N. Ling, P. Conlon, H. F. McFarland, R. Houghten, and R. Martin. 2000. Contribution of individual amino acids within MHC molecule or antigenic peptide to TCR ligand potency. J. Immunol. 164:861.
17. + T cells and induce T cell responses to native peptide ligands. J. Immunol. 163:6424.
18. Hemmer, B., B. Gran, Y. Zhao, A. Marques, J. Pascal, A. Tzou, T. Kondo, I. Cortese, B. Bielekova, S. E. Straus, et al. 1999. Identification of candidate T-cell epitopes and molecular mimics in chronic Lyme disease. Nat. Med. 5:1375.
19. Zhao, Y., B. Gran, C. Pinilla, S. Markovic-Plese, B. Hemmer, A. Tzou, L. W. Whitney, W. E. Biddison, R. Martin, and R. Simon. 2001. Combinatorial peptide libraries and biometric score matrices permit the quantitative analysis of specific and degenerate interactions between clonotypic TCR and MHC peptide ligands. J. Immunol. 167:2130.
20. van Bergen, J., S. P. Schoenberger, F. Verreck, R. Amons, R. Offringa, and F. Koning. 1997. Efficient loading of HLA-DR with a T helper epitope by genetic exchange of CLIP. Proc. Natl. Acad. Sci. USA 94:7499.
21. Malcherek, G., C. Wirblich, N. Willcox, H. G. Rammensee, J. Trowsdale, and A. Melms. 1998. MHC class II-associated invariant chain peptide replacement by T cell epitopes: engineered invariant chain as a vehicle for directed and enhanced MHC class II antigen processing and presentation. Eur. J. Immunol. 28:1524.
22. Fujii, S., S. Senju, Y. Z. Chen, M. Ando, S. Matsushita, and Y. Nishimura. 1998. The CLIP-substituted invariant chain efficiently targets an antigenic peptide to HLA class II pathway in L cells. Hum. Immunol. 59:607.
23. Senju, S., S. Hirata, H. Matsuyosi, M. Masuda, Y. Uemura, K. Araki, K. Yamamura, and Y. Nishimura. Generation and genetic modification of dendritic cells derived from mouse embryonic stem cells. Blood. In press.
24. + T cell epitopes. Biochem. Biophys. Res. Commun. 284:1140.
25. + T-cell clones established from Japanese patients with insulin-dependent diabetes mellitus. Hum. Immunol. 59:549.
26. Wicker, L. S., S. L. Chen, G. T. Nepom, J. F. Elliott, D. C. Freed, A. Bansal, S. Zheng, A. Herman, A. Lernmark, D. M. Zaller, et al. 1996. Naturally processed T cell epitopes from human glutamic acid decarboxylase identified using mice transgenic for the type 1 diabetes-associated human MHC class II allele, DRB1*0401. J. Clin. Invest. 98:2597.
27. Patel, S. D., A. P. Cope, M. Congia, T. T. Chen, E. Kim, L. Fugger, D. Wherrett, and G. Sonderstrup-McDevitt. 1997. Identification of immunodominant T cell epitopes of human glutamic acid decarboxylase 65 by using HLA-DR(α*0101,β1*0401) transgenic mice. Proc. Natl. Acad. Sci. USA 94:8082.
28. Chen, Y. Z., S. Matsushita, and Y. Nishimura. 1996. Response of a human T cell clone to a large panel of altered peptide ligands carrying single residue substitutions in an antigenic peptide: characterization and frequencies of TCR agonism and TCR antagonism with or without partial activation. J. Immunol. 157:3783.
29. Misko, I. S., S. M. Cross, R. Khanna, S. L. Elliott, C. Schmidt, S. J. Pye, and S. L. Silins. 1999. Crossreactive recognition of viral, self, and bacterial peptide ligands by human class I-restricted cytotoxic T lymphocyte clonotypes: implications for molecular mimicry in autoimmune disease. Proc. Natl. Acad. Sci. USA 96:2279.
30. Masuda, M., S. Senju, S. Fujii Si, Y. Terasaki, M. Takeya, S. Hashimoto Si, K. Matsushima, E. Yumoto, and Y. Nishimura. 2002. Identification and immunocytochemical analysis of DCNP1, a dendritic cell-associated nuclear protein. Biochem. Biophys. Res. Commun. 290:1022.
31. + T cells specific to p53 self peptides respond to p53 proteins of both wild and mutant forms. Eur. J. Immunol. 28:305.
32. Padovan, E., G. Casoratí, P. Dellabona, S. Meyer, M. Brockhaus, and A. Lanzavecchia. 1993. Expression of two T cell receptor α chains: dual receptor T cells. Science 262:422.
33. Busch, R., C. M. Hill, J. D. Hayball, J. R. Lamb, and J. B. Rothbard. 1991. Effect of natural polymorphism at residue 86 of the HLA-DR β chain on peptide binding. J. Immunol. 147:1292.
34. Rammensee, H. G., T. Friede, and S. Stevanoviic. 1995. MHC ligands and peptide motifs: first listing. Immunogenetics 41:178.
35. Vergelli, M., B. Hemmer, M. Kalbus, A. B. Vogt, N. Ling, P. Conlon, J. E. Coligan, H. McFarland, and R. Martin, 1997. Modifications of peptide ligands enhancing T cell responsiveness imply large numbers of stimulatory ligands for autoreactive T cells. J. Immunol. 158:3746.
36. Grogan, J. L., A. Kramer, A. Nogai, L. Dong, M. Ohde, J. Schneider-Mergener, and T. Kamradt. 1999. Cross-reactivity of myelin basic protein-specific T cells with multiple microbial peptides: experimental autoimmune encephalomyelitis induction in TCR transgenic mice. J. Immunol. 163:3764.
37. Maier, B., M. Molinger, A. P. Cope, L. Fugger, J. Schneider-Mergener, G. Sonderstrup, T. Kamradt, and A. Kramer. 2000. Multiple cross-reactive self-ligands for Borrelia burgdorferi-specific HLA-DR4-restricted T cells. Eur. J. Immunol. 30:448.
38. Hiemstra, H. S., P. A. van Veelen, N. C. Schloot, A. Geluk, K. E. van Meijgaarden, S. J. Willemen, J. A. Leunissen, W. E. Benckhuijsen, R. Amons, R. R. de Vries, et al. 1998. Definition of natural T cell antigens with mimicry epitopes obtained from dedicated synthetic peptide libraries. J. Immunol. 161:4078.
39. + T cell clone using combinatorial peptide libraries and mass spectrometry. J. Immunol. 162:7155.
40. Judkowski, V., C. Pinilla, K. Schroder, L. Tucker, N. Sarvetnick, and D. B. Wilson. 2001. Identification of MHC class II-restricted peptide ligands, including a glutamic acid decarboxylase 65 sequence, that stimulate diabetogenic T cells from transgenic BDC2.5 nonobese diabetic mice. J. Immunol. 166:908.
41. Hemmer, B., M. Vergelli, B. Gran, N. Ling, P. Conlon, C. Pinilla, R. Houghten, H. F. McFarland, and R. Martin. 1998. Predictable TCR antigen recognition based on peptide scans leads to the identification of agonist ligands with no sequence homology. J. Immunol. 160:3631.
42. Hennecke, J., A. Carfi, and D. C. Wiley. 2000. Structure of a covalently stabilized complex of a human αβ T-cell receptor, influenza HA peptide and MHC class II molecule, HLA-DR1. EMBO J. 19:5611.
43. Esnouf, R. M. 1997. An extensively modified version of MolScript that includes greatly enhanced coloring capabilities. J. Mol. Graph. Model 15:132.
44. Merritt, E. A., and M. E. P. Murphy. 1994. Raster3D version-2.0: a program for photorealistic molecular graphics. Acta Cryst. D50:869.
45. Texier, C., S. Pouvelle-Moratille, M. Busson, D. Charron, A. Menez, and B. Maillere. 2001. Complementarity and redundancy of the binding specificity of HLA-DRB1, -DRB3, -DRB4 and -DRB5 molecules. Eur. J. Immunol. 31:1837.
46. Clot, F., C. Gianfrani, M. C. Babron, F. Bouguerra, S. Southwood, M. F. Kagnoff, R. Troncone, S. Percopo, J. F. Eliaou, F. Clerget-Darpoux, A. Sette, and L. Greco. 1999. HLA-DR53 molecules are associated with susceptibility to celiac disease and selectively bind gliadin-derived peptides. Immunogenetics 49:800.
47. Geluk, A., K. E. van Meijgaarden, S. Southwood, C. Oseroff, J. W. Drijfhout, R. R. de Vries, T. H. Ottenhoff, and A. Sette. 1994. HLA-DR3 molecules can bind peptides carrying two alternative specific submotifs. J. Immunol. 152:5742.
48. Baum, H., V. Brusic, K. Choudhuri, P. Cunningham, D. Vergani, and M. Peakman. 1995. MHC molecular mimicry in diabetes. Nat. Med. 1:388.
49. Akerblom, H. K., and M. Knip. 1998. Putative environmental factors in Type 1 diabetes. Diabetes Metab. Rev. 14:31.
50. Taha, M. K., A. E. Deghmane, A. Antignac, M. L. Zarantonelli, M. Larribe, and J. M. Alonso. 2002. The duality of virulence and transmissibility in Neisseria meningitidis. Trends Microbiol. 10:376.
51. Giebink, G. S. 2001. The prevention of pneumococcal disease in children. N. Engl. J. Med. 345:1177.
52. Steidler, L., W. Hans, L. Schotte, S. Neirynck, F. Obermeier, W. Falk, W. Fiers, and E. Remaut. 2000. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science 289:1352.
53. Kimpimaki, T., M. Erkkola, S. Korhonen, A. Kupila, S. M. Virtanen, J. Ilonen, O. Simell, and M. Knip. 2001. Short-term exclusive breastfeeding predisposes young children with increased genetic risk of type I diabetes to progressive β-cell autoimmunity. Diabetologia 44:63.