The stimulation of low-affinity, nontolerized clones by heteroclitic antigen analogues causes the breaking of tolerance established to an immunodominant T cell epitope

Journal of Experimental Medicine

Volumn 190, Issue 7, 1999, Pages 983-993

  Wang, Rongfang ^a   Wang Zhu, Yiran ^a   Gabaglia, Claudia Raja ^a   Kimachi, Kazuhiko ^a,b   Grey, Howard M ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b Chemo Sero Therapeutic Research Institute   (Japan)

Author keywords

Cytochrome c; Molecular mimicry; T cell repertoire; Tolerance

Indexed keywords

ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; EPITOPE; FREUND ADJUVANT; GAMMA INTERFERON; T LYMPHOCYTE ANTIGEN; T LYMPHOCYTE RECEPTOR;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ARTICLE; CLONAL ANERGY; CLONOGENESIS; COMPLEMENTARITY DETERMINING REGION; CONCENTRATION RESPONSE; CONTROLLED STUDY; FEMALE; HYBRIDOMA; IMMUNOSTIMULATION; LYMPHOCYTE CLONE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR AFFINITY; SEQUENCE ANALYSIS; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

EID: 0033523640     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.190.7.983     Document Type: Article

References (48)

1. Oldstone, M.B.A. 1990. Molecular mimicry and autoimmune disease. Cell. 50:819-820.
2. Luo, A.-M., K.M. Garza, D. Hunt, and K.S.K. Tung. 1993. Antigen mimicry in autoimmune disease. Sharing of amino acid residues critical for pathogenic T cell activation. J. Clin. Invest. 92:2117-2123.
3. 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. 80:695-705.
4. (27-35). J. Exp. Med. 184:647-657.
5. 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. 185:1651-1659.
6. Barnaba, V., and F. Sinigaglia. 1997. Molecular mimicry and T cell-mediated autoimmune disease. J. Exp. Med. 185: 1529-1531.
7. Zhao, Z.-S., F. Granucci, L. Yeh, P.A. Schaffer, and H. Cantor. 1998. Molecular mimicry by herpes simplex virus-type 1: autoimmune disease after viral infection. Science. 279: 1344-1347.
8. Kappler, J.W., N. Roehm, and P. Marrack. 1987. T cell tolerance by clonal elimination in the thymus. Cell. 49:273-280.
9. + thymocytes. Nature. 333:742-746.
10. Sha, W.C., C.A. Nelson, R.D. Newberry, D.M. Kranz, J.H. Russell, and D.Y. Loh. 1988. Positive and negative selection of an antigen receptor on T cells in transgenic mice. Nature. 336:73-76.
11. Bloom, B.R., R.L. Modlin, and P. Salgame. 1992. Stigma variations: observations on suppressor T cells and leprosy. Annu. Rev. Immunol. 10:453-488.
12. + Th1 but not Th2 cytokine responses. Int. Immunol. 6:721-730.
13. Nicholson, L.B., J.M. Greer, R.A. Sobel, M.B. Lees, and V.J. Kuchroo. 1995. An altered peptide ligand mediates immune deviation and prevents autoimmune encephalomyelitis. Immunity. 3:397-405.
14. Saoudi, A., S. Simmond, I. Huitinga, and D. Mason. 1995. Prevention of experimental allergic encephalomyelitis in rats by targeting autoantigen to B cells: evidence that the protective mechanism depends on changes in the cytokine response and migratory properties of the autoantigen-specific T cells. J. Exp. Med. 182:335-344.
15. Forsthuber, T., H.C. Yip, and P.V. Lehmann. 1996. Induction of TH1 and TH2 immunity in neonatal mice. Science. 271:1728-1730.
16. Gammon, G., and E. Sercarz. 1989. How some T cells escape tolerance induction. Nature. 342:183-185.
17. Benichou, G., P.A. Takizawa, P.T. Ho, C.C. Killion, C.A. Olson, M. McMillan, and E.E. Sercarz. 1990. Immunogenicity and tolerogenicity of self-major histocompatibility complex peptides. J. Exp. Med. 172:1341-1346.
18. Agrawal, B., M. Manickasundari, E. Fraga, and B. Singh. 1991. T cells that recognize peptide sequences of self MHC class II molecules exist in syngeneic mice. J. Immunol. 147: 383-390.
19. Cibotti, R., J.M. Kanellopoulos, J.P. Cabaniols, O. Halle-Panenko, K. Kosmatopoulos, E. Sercarz, and P. Kourilsky. 1992. Tolerance to a self-protein involves its immunodominant but does not involve its subdominant determinants. Proc. Natl. Acad. Sci. USA. 89:416-420.
20. Mamula, J. 1993. The inability to process a self-peptide allows autoreactive T cells to escape tolerance. J. Exp. Med. 177:567-571.
21. Kearney, E.R., K.A. Pape, D.Y. Loh, and M.K. Jenkins. 1994. Visualization of peptide-specific T cell immunity and peripheral tolerance induction in vivo. Immunity. 1:327-339.
22. Van Houten, N., and S.F. Blake. 1996. Direct measurement of anergy of antigen-specific T cells following oral tolerance induction. J. Immunol. 157:1337-1341.
23. Falb, D., T.J. Briner, G.H. Sunshine, C.R. Bourque, M. Luqman, M.L. Gefter, and T. Kamradt. 1996. Peripheral tolerance in T cell receptor-transgenic mice: evidence for T cell anergy. Eur. J. Immunol. 26:130-135.
24. + T cells. J. Exp. Med. 185:405-414.
25. + T cells persist in vivo following induction of peripheral tolerance. J. Immunol. 160:4719-4729.
26. Zügel, U., R. Wang, G. Shih, A. Sette, J. Alexander, and H.M. Grey. 1998. Termination of peripheral tolerance to a T cell epitope by heteroclitic antigen analogues. J. Immunol. 161:1705-1709.
27. La Face, D.M., C. Couture, K. Anderson, G. Shih, J. Alexander, A. Sette, T. Mustelin, A. Altman, and H.M. Grey. 1997. Differential T cell signaling induced by antagonist peptide-MHC complexes and the associated phenotypic responses. J. Immunol. 158:2057-2064.
28. Sette, A., S. Southwood, D. O'Sullivan, F.C.A. Gaeta J. Sidney, and H.M. Grey. 1992. Effect of pH on class II-peptide interactions. J. Immunol. 148:844-851.
29. Ignatowicz, L., J. Kappler, and P. Marrack. 1996. The repertoire of T cells shaped by a single MHC/peptide ligand. Cell. 84:521-529.
30. Candélas, S., J. Katz, C. Benoist, D. Mathis, and K. Haskins. 1991. Islet-specific T-cell clones from nonobese diabetic mice express heterogeneous T-cell receptors. Proc. Natl. Acad. Sci. USA. 88:6167-6170.
31. Pannetier, C., M. Cochet, S. Darche, A. Casrouge, M. Zöller, and P. Kourilsky. 1993. The sizes of the CDR3 hypervariable regions of the murine T-cell receptor β chains vary as a function of the recombined germ-line segments. Proc. Natl. Acad. Sci. USA. 90:4319-4323.
32. Sorger, S.B., Y. Paterson, P.J. Fink, and S.M. Hedrick. 1990. TCR junctional regions and the MHC molecule affect the recognition of antigenic peptides by T cell clones. J. Immunol. 144:1127-1135.
33. Jorgensen, J.L., P.A. Reay, E.W. Ehrich, and M.M. Davis. 1992. Molecular components of T-cell recognition. Annu. Rev. Immunol. 10:835-873.
34. Nakano, N., R. Rooke, C. Benoist, and D. Mathis. 1997. Positive selection of T cells induced by viral delivery of neopeptides to the thymus. Science. 275:678-683.
35. Kaye, J., G. Kersh, I. Engel, and S.M. Hedrick. 1991. Structure and specificity of the T cell antigen receptor. Semin. Immunol. 3:269-281.
36. Hedrick, S.M., I. Engel, D.L. McElligott, P.J. Fink, M.L. Hsu, D. Hansburg, and L.A. Matis. 1988. Selection of amino acid sequences in the beta chain of the T cell antigen receptor. Science. 239:1541-1544.
37. Cochet, M., C. Pannetier, A. Regnault, S. Darche, C. Leclerc, and P. Kourilsky. 1992. Molecular detection and in vivo analysis of the specific T cell response to a protein antigen. Eur. J. Immunol. 22:2639-2647.
38. McHeyzer-Williams, M.G., and M.M. Davis. 1995. Antigen-specific development of primary and memory T cells in vivo. Science. 268:106-111.
39. Jorgensen, J.L., U. Esser, B. Fazekas de St. Groth, P.A. Reay, and M.M. Davis. 1992. Mapping T-cell receptor-peptide contacts by variant peptide immunization of single-chain transgenics. Nature. 355:224-230.
40. Viville, S., J. Neefjes, V. Lotteau, A. Dierich, M. Lemeur, H. Ploegh, C. Benoist, and D. Mathis. 1993. Mice lacking the MHC class-II associated invariant chain. Cell. 72:635-648.
41. Tourne, S., N. Nakano, S. Viville, C. Benoist, and D. Mathis. 1995. The influence of invariant chain on the positive selection of single T cell receptor specificities. Eur. J. Immunol. 25:1851-1856.
42. Poplonski, L., B. Vukusic, J. Pawling, S. Clapoff, J. Roder, N. Hozumi, and J. Wither. 1996. Tolerance is overcome in beef insulin-transgenic mice by activation of low-affinity autoreactive T cells. Eur. J. Immunol. 26:601-609.
43. Theobald, M., J. Biggs, J. Hernández, J. Lustgarten, C. Labadie, and L.A. Sherman. 1997. Tolerance to p53 by A2.1-restricted cytotoxic T lymphocytes. J. Exp. Med. 185:833-841.
44. Targoni, O.S., and P.V. Lehmann. 1998. Endogenous myelin basic protein inactivates the high avidity T cell repertoire. J. Exp. Med. 187:2055-2063.
45. Marrack, P., R. Endres, R. Shimonkevitz, A. Zlotnik, D. Dialynas, F.W. Fitch, and J. Kappler. 1983. The major histocompatibility complex-restricted antigen receptor on T cells. II. Role of the L3T4 product. J. Exp. Med. 158:1077-1091.
46. Mannie, M.D., J.M. Rosser, and G.A. White. 1995. Autologous rate myelin basic protein is a partial agonist that is converted into a full antagonist upon blockade of CD4. J. Immunol. 154:2642-2654.
47. Hampl, J., Y. Chien, and M.M. Davis. 1997. CD4 augments the response of a T cell to agonist but not to antagonist ligands. Immunity. 7:379-385.
48. Vidal, K., B.L. Hsu, C.B. Williams, and P.M. Allen. 1996. Endogenous altered peptide ligands can affect peripheral T cell responses J. Exp. Med. 183:1311-1321.