An autoantigenic T cell epitope forms unstable complexes with class II MHC: A novel route for escape from tolerance induction

International Immunology

Volumn 5, Issue 9, 1993, Pages 1151-1158

  Fairchild, Paul J ^a   Wildgoose, Richard ^a,b   Atherton, Eric ^a,b   Webb, Sandra ^c   Wraith, David C ^c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b Cambridge Research Biochemicals Limited ^*  (United Kingdom)

^c NONE

Author keywords

Affinity; Autoimmunity; I Au molecule; Myelin basic protein; T cell tolerance

Indexed keywords

AUTOANTIGEN; EPITOPE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MYELIN BASIC PROTEIN; SYNTHETIC PEPTIDE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANTIGEN PRESENTATION; ARTICLE; BINDING AFFINITY; HAPLOTYPE; IMMUNOLOGICAL TOLERANCE; INTERNALIZATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; T LYMPHOCYTE ACTIVATION;

AMINO ACID SEQUENCE; ANIMAL; ANTIGEN-PRESENTING CELLS; AUTOANTIGENS; AUTOIMMUNITY; CELLS, CULTURED; EPITOPES; HISTOCOMPATIBILITY ANTIGENS CLASS II; HYBRIDOMAS; IMMUNE TOLERANCE; MAJOR HISTOCOMPATIBILITY COMPLEX; MICE; MOLECULAR SEQUENCE DATA; MYELIN BASIC PROTEINS; RATS; SUPPORT, NON-U.S. GOV'T; T-LYMPHOCYTES;

EID: 0027439013     PISSN: 09538178     EISSN: None     Source Type: Journal    
DOI: 10.1093/intimm/5.9.1151     Document Type: Article

References (45)

1. Sprent, J., Lo, D., Gao, E.-K., and Ron, Y. 1988. T cell selection in the thymus. Immunol. Rev. 101:173.
2. Fowlkes, B. J. and Pardoll, D. M. 1989. Molecular and cellular events of T cell development. Adv. Immunol. 44:207.
3. Schluesener, H. J. and Wekerle, H. 1985. Autoaggressive T lymphocyte lines recognizing the encephalitogenic region of myelin basic protein: in vitro selection from unprimed rat T lymphocyte populations. J. Immunol. 135:3128.
4. Burns, J., Rosenzweig, A., Zweiman, B., and Lisak, R. P. 1983. Isolation of myelin basic protein-reactive T-cell lines from normal human blood. Cell. Immunol. 81:435.
5. Gammon, G., Sercarz, E. E., and Benichou, G. 1991. The dominant self and the cryptic self: shaping the autoreactive T-cell repertoire. Immunol. Today 12:193.
6. Adorini, L, Appella, E., Doria, G., and Nagy, Z. A. 1988. Mechanisms influencing the immunodominance of T cell determinants. J. Exp. Med. 168:2091.
7. Gammon, G. and Sercarz, E. 1989. How some T cells escape tolerance induction. Nature 342:183.
8. Zamvil, S. S. and Steinman, L. 1990. The T lymphocyte in experimental allergic encephalomyelitis. Annu. Rev. Immunol. 8:579.
9. Wraith, D. C., Smilek, D. E., Mitchell, D. J., Steinman, L, and McDevitt, H. O.1989. Antigen recognition in autoimmune encephalomyelitis and the potential for peptide-mediated immunotherapy. Cell 59:247.
10. Wraith, D. C., Smilek, D. E., and Webb, S. 1991. MHC-binding peptides for immunotherapy of experimental autoimmune disease. J. Autoimmun. 5:103.
11. Atherton, E. and Sheppard, R. C. 1985. Solid-phase peptide synthesis using Na-fluorenylmethoxycarbonylamino acid pentafluorophenyl esters. J. Chem. Soc. Chem. Commun. 165.
12. Salisbury, S. A., Tremeer, E. J., Davies, J. W., and Owen, D. E. I. A. 1990. Acylation monitoring in solid phase peptide synthesis by the equilibrium distribution of coloured ions. J. Chem. Soc. Chem. Commun. 538.
13. Kappler, J. W., Skidmore, B., White, J., and Marrack, P. 1981. Antigeninducible, H-2-restricted, interleukin-2-producing T cell hybridomas. Lack of independent antigen and H-2 recognition. J. Exp. Med. 153:1198.
14. Harding, C. V., Roof, R. W., and Unanue, E. R. 1989. Turnover of lapeptide complexes is facilitated in viable antigen-presenting cells: Biosynthetic turnover of la vs. peptide exchange. Proc. Natl Acad. Sci. USA 86:4230.
15. Watson, J. 1979. Continuous proliferation of murine antigen specific helper T lymphocytes in culture. J. Exp. Med. 150:1510.
16. Zamvil, S. S., Mitchell, D. J., Moore, A. C., Kitamura, K., Steinman, L., and Rothbard, J. B. 1986. T-cell epitope of the autoantigen myelin basic protein that induces encephalomyelitis. Nature 324:258.
17. Acha-Orbea, H., Mitchell, D. J., Timmermann, L, Wraith, D. C., Tausch, G. S., Waldor, M. K., Zamvil, S. S., McDevitt, H. O., and Steinman, L. 1988. Limited heterogeneity of T cell receptors from lymphocytes mediating autoimmune encephalomyelitis allows specific immune intervention. Cell 54:263.
18. Emerson, S. G. and Cone, R. E. 1979. Turnover and shedding of la antigens by murine spleen cells in culture. J. Immunol. 122:892.
19. Emerson, S. G. and Cone, R. E. 1981. I-Ak and H-2Kk antigens are shed as supramolecular particles in association with membrane lipids. J. Immunol. 127:482.
20. Sachs, D. H., Kiszkiss, P., and Kim, K. J. 1980. Release of la antigens by a cultured B cell line. J. Immunol. 124:2130.
21. Golding, H. and Singer, A. 1984. Role of accessory cell processing and presentation of shed H-2 alloantigens in allospecific cytotoxic T lymphocyte responses. J. Immunol. 133:597.
22. Reid, P. A. and Watts, C. 1990. Cycling of cell-surface MHC glycoproteins through primaquine-sensitive intracellular compartments. Nature 346:655.
23. Seglen, P. O., Grinde, B., and Solheim, A. E. 1979. Inhibition of the lysosomal pathway of protein degradation in isolated rat hepatocytes by ammonia, methylamine, chloroquine and leupeptin. Eur. J. Biochem. 95:215.
24. Lee, J. M., Kay, C. M., and Watts, T. H. 1992. Conformational changes in mouse MHC class II proteins at acidic pH. Int. Immunol. 4:889.
25. Jensen, P. E. 1991. Enhanced binding of peptide antigen to purified class II major histocompatibility glycoproteins at acidic pH. J. Exp. Med. 174:1111.
26. Jensen, P. E. 1990. Regulation of antigen presentation by acidic pH. J. Exp. Med. 171:1779.
27. Martenson, R. E. 1984. Myelin basic protein speciation. In Alvord Jr., E. C., Keis, M. W., and Suckling, A. J. (eds), Experimental Autoimmune Encephalomyelitis: A Useful Model for Multiple Sclerosis, p. 511. Alan R. Liss, New York.
28. Wraith, D. C., Smilek, D. E., Mitchell, D. J., Steinman, L., and McDevitt, H. O. 1990. T cell recognition in experimental autoimmune encephalomyelitis: prospects for immune intervention with synthetic peptides. Intern. Rev. Immunol. 6:37.
29. Garrett, T. P. J., Saper, M. A., Bjorkman, P. J., Strominger, J. L., and Wiley, D. C. 1989. Specificity pockets for the side chains of peptide antigens in HLA-Aw68. Nature 342:692.
30. Latron, F., Pazmany, L., Morrison, J., Moots, R., Saper, M. A., McMichael, A., and Strominger, J. L. 1992. A critical role for conserved residues in the cleft of HLA-A2 in presentation of a nonapeptide to T cells. Science 257:964.
31. Matsumura, M., Fremont, D. H., Peterson, P. A., and Wilson, I. A. 1992. Emerging principles for the recognition of peptide antigens by MHC class I molecules. Science 257:927.
32. Kropshofer, H., Bohlinger, I., Max, H., and Kalbacher, H. 1991. Self and foreign peptides interact with intact and disassembled MHC class II antigen HLA-DR via tryptophan pockets. Biochemistry 30:9177.
33. Marsh, E. W., Dalke, D. P., and Pierce, S. K. 1992. Biochemical evidence for the rapid assembly and disassembly of processed antigenmajor histocompatibility complex class II complexes in acidic vesicles of B cells. J. Exp. Med. 175:425.
34. Busch, R., Strang, G., Howland, K., and Rothbard, J. B. 1990. Degenerate binding of immunogenic peptides to HLA-DR proteins on B cell surfaces. Int. Immunol. 2:443.
35. Li, W.-F., Fan, M.-D., Pan, C.-B., and Lai, M.-Z. 1992. T cell epitope selection: dominance may be determined by both affinity for Major Histocompatibility Complex and stoichiometry of epitope. Eur. J. Immunol. 22:943.
36. Davidson, H. W., Reid, P. A., Lanzavecchia, A., and Watts, C. 1991. Processed antigen binds to newly synthesized MHC class II molecules in antigen-specific B lymphocytes. Cell 67:105.
37. Lanzavecchia, A., Reid, P. A., and Watts, C. 1992. Irreversible association of peptides with class II MHC molecules in living cells. Nature 357:249.
38. Reay, P. A., Wettstein, D. A., and Davis, M. M. 1992. pH dependence and exchange of high and low responder peptides binding to a class II MHC molecule. EMBO J. 11:2829.
39. Wall, M., Southwood, S., Sidney, J., Oseroff, C., del Guericio, M.-F., Lamont, A. G., Colon, S. M., Arrhenius, T., Gaeta, F. C. A., and Sette, A. 1992. High affinity for class II molecules as a necessary but not sufficient characteristic of encephalitogenic determinants. Int. Immunol. 4:773.
40. Cibotti, R., Kanellopoulos, J. M., Cabaniols, J-P, Halle-Panenko, O., Kosmatopoulos, K., Sercarz, E., and Kourilsky, P. 1992. Tolerance to a self-protein involves its immunodominant but does not involve its subdominant determinants. Proc. Natl Acad. Sci. USA 89:416.
41. Lipham, W. J., Redmond, T. M., Takahashi, H., Berzofsky, J. A., Wiggert, B., Chader, G. J., and Gery, I.1991. Recognition of peptides that are immunopathogenic but cryptic. Mechanisms that allow lymphocytes sensitized against cryptic peptides to initiate pathogenic autoimmune processes. J. Immunol. 146:3757.
42. Redmond, T. M., Sanui, H., Hu, L.-H., Wiggert, B., Margalit, H., Berzofsky, J. A., Chader, G. J., and Gery, I. 1989. Immune responses to peptides derived from the retinal protein IRBP: immunopathogenic determinants are not necessarily immunodominant. Clin. Immunol. Immunopathol. 53:212.
43. Kono, D. H., Urban, J. L., Horvath, S. J., Ando, D. G., Saavedra, R. A., and Hood, L. 1988. Two minor determinants of myelin basic protein induce experimental allergic encephalomyelitis in SJL/J mice. J. Exp. Med. 168:213.
44. Lehmann, P. V., Forsthuber, T., Miller, A., and Sercarz, E. E. 1992. Spreading of T cell autoimmunity to cryptic determinants of an autoantigen. Nature 358:155.
45. Chothia, C. 1984. Principles that determine the structure of proteins. Annu. Rev. Biochem. 53:537.