Initiation of signal transduction through the T cell receptor requires the peptide multivalent engagement of MHC ligands

Immunity

Volumn 9, Issue 4, 1998, Pages 459-466

  Boniface, J Jay ^a,b   Rabinowitz, Joshua D ^a   Wülfing, Christoph ^a   Hampl, Johannes ^a,c   Reich, Ziv ^a   Altman, John D ^a,d   Kantor, Ronald M ^a   Beeson, Craig ^a,e   McConnell, Harden M ^a   Davis, Mark M ^a  

^a STANFORD UNIVERSITY   (United States)

^b Eos Biotechnology   (United States)

^c SRI INTERNATIONAL   (United States)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; SYNTHETIC PEPTIDE; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ARTICLE; LIGAND BINDING; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; SIGNAL TRANSDUCTION; SPLEEN CELL; T LYMPHOCYTE ACTIVATION; TRANSGENIC MOUSE;

EID: 0032192469     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-7613(00)80629-9     Document Type: Article

References (59)

1. Abastado, J-P., Lone, Y-C., Casrouge, A., Boulot, G., and Kourilsky, P. (1995). Dimerization of soluble major histocompatibility complex-peptide complexes is sufficient for activation of T cell hybridoma and induction of unresponsiveness. J. Exp. Med. 182, 439-447.
2. Alberola-lla, J., Satoshi, T., Kemer, J.D., and Perlmutter, R.M. (1997). Differential signaling by lymphocyte antigen receptors. Annu. Rev. Immunol. 15, 125-154.
3. Altman, J.D., Reay, P.A., and Davis, M.M. (1993). Formation of functional peptide complexes of class II major histocompatibility complex proteins from subunits produced in Escherichia coli. Proc. Natl. Acad. Sci. USA 90, 10330-10334.
4. Altman, J.D., Moss, P.A.H., Goulder, P.J.R., Barouch, D.H., McHeyzer-Williams, M.G., Bell, J.I., McMichael, A.J., and Davis, M.M. (1996). Phenotypic analysis of antigen-specific T lymphocytes. Science 274, 94-96.
5. Banner, D.W., D'Arcy, A., Janes, W., Gentz, R., Schoenfeld, H-J., Broger, C., Loetscher, H., and Lesslauer, W. (1993). Crystal structure of the soluble human 55 kd TNF receptor-human TNFβ complex: implications for TNF receptor activation. Cell 73, 431-445.
6. Beeson, C., Rabinowitz, J.D., Tate, K., Gütgemann, I., Chien, Y.H., Jones, P.P., Davis, M.M., and McConnell, H.M. (1996). Early biochemical signals arise from low affinity TCR-ligand reactions at the cell-cell surface. J. Exp. Med. 184, 777-782.
7. Becker, D.M., Patten, P., Chien, Y., Yokota, T., Eshhar, Z., Giedlin, M., Gascoigne, N.R., Goodnow, C., Wolf, R., Arai, K., et al. (1985). Variability and repertoire size of T-cell receptor V alpha gene segments. Nature 317, 430-434.
8. Brown, J.H., Jardetzky, T.S., Gorga, J.C., Stern, L.J., Urban, R.G., Strominger, J.L., and Wiley, D.C. (1993). Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1, Nature 364, 33-39.
9. Chien, Y.H., Gascoigne, N.R., Kavaler, J., Lee, N.E., and Davis, M.M. (1984). Somatic recombination in a murine T-cell receptor gene. Nature 309, 322-326.
10. Crawford, F., Kozono, H., White, J., Marrack, P., and Kappler, J. (1998). Detection of antigen-specific T cells with multivalent soluble class II MHC covalent peptide complexes. Immunity 8, 675-682.
11. Daeron, M. (1997). Fc receptor biology. Annu. Rev. Immunol. 15, 203-234.
12. Davis, M.M., Boniface, J.J., Reich, Z., Lyons, D.S., Hampl, J., Arden, B., and Chien, Y.-h. (1998). Ligand recognition by αβ T cell receptors. Annu. Rev. Immunol. 16, 523-544.
13. Dessen, A., Lawrence, C.M., Cupo, S., Zaller, D.M., and Wiley, D.C. (1997). X-ray crystal structure of HLA-DR4 (DRA*0101, DRB1*0401) complexed with a peptide from human collagen II. Immunity 7, 473-481.
14. Dintzis, R.Z., Okajima, M., Middleton, M.H., Green, G., and Dintzis, H.M. (1989). The immunogenicity of soluble haptenated polymers is determined by molecular mass and hapten valence. J. Immunol. 143, 1239-1244.
15. Evavold, B.D., Williams, S.G., Hsu, B.L., Buus, S., and Allen, P.M. (1992). Complete dissection of the Hb(64-76) determinant using T helper 1, T helper 2 clones, and T cell hybridomas. J. Immunol. 148, 347-353.
16. Fink, P.J., Matis, L.A., McElligott, D.L, Bookman, M., and Hedrick, S.M. (1986). Correlations between T-cell specificity and the structure of the antigen receptor. Nature 321, 219-226.
17. Fremont, D.H., Hendrickson, W.A., Marrack, P., and Kappler, J.W. (1996). Structures of an MHC class II molecule with covalently bound single peptides. Science 272, 1001-1004.
18. k in complex with a dominant epitope of lysozyme. Immunity 8, 305-317.
19. Garboczi, D.N., Ghosh, P., Utz, U., Fan, Q.R., Biddison, W.E., and Wiley, D.C. (1996). Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature 384, 134-141.
20. Garcia, K.C., Scott, C.A., Brunmark, A., Carbone, F.R., Peterson, P.A., Wilson, I.A., and Teyton, L. (1996). CD8 enhances formation of stable T-cell receptor/MHC class I molecule complexes. Nature 384, 577-581.
21. Garcia, K.C., Degano, M., Pease, L.R., Huang, M., Peterson, P.A., Teyton, L, and Wilson, I.A. (1998). Structural basis of plasticity in T cell receptor recognition of a self peptide-MHC antigen. Science 279, 1166-1172.
22. Ghosh, P., Amaya, M., Mellins, E., and Wiley, D.C. (1995). The structure of an intermediate in class II MHC maturation: clip bound to HLA-DR3. Nature 378, 457-462.
23. Gütgemann, I., Fahrer, A.M., Altman, J.D., Davis, M.M., and Chien, Y-h. (1998). Induction of rapid T cell activation and tolerance by systemic presentation of an orally administered antigen. Immunity 8, 667-673.
24. Hampl, J., Chien, Y-h., and Davis, M.M. (1997). CD4 augments the response of a T cell to agonist but not to antagonist ligands. Immunity 7, 379-385.
25. Hedrick, S.M., Matis, L.A., Hecht, T.T., Samelson, L.E., Longo, D.L., Heber-Katz, E., and Schwartz, R.H. (1982). The fine specificity of antigen and la determinant recognition by T cell hybridoma clones specific for pigeon cytochrome c. Cell 30, 141-152.
26. Kappler, J., Kubo, R., Haskins, K., White, J., and Marrack, P. (1983). The mouse T cell receptor: comparison of MHC-restricted receptors in two T cell hybridomas. Cell 34, 727-737.
27. Karjalainen, K. (1994). High sensitivity, low affinity-paradox of T-cell receptor recognition. Curr. Opin. Immunol. 6, 9-12.
28. Kaye, J., Porcelli, S., Tite, J., Jones, B., and Janeway, C.A., Jr. (1983). Both a monoclonal antibody and antisera specific for determinants unique to individual cloned helper T cell lines can substitute for antigen and antigen presenting cells in activation of T cells. J. Exp. Med. 158, 836-856.
29. Kolanus, W., Romeo, C., and Seed, B. (1993). T cell activation by clustered tyrosine kinases. Cell 74, 171-183.
30. Lyons, D.S., Lieberman, S.A., Hampl, J., Boniface, J.J., Reay, P.A., Chien, Y., Berg, L.J., and Davis, M.M. (1996). T cell receptor binding to antagonist peptide/MHC complexes exhibits lower affinities and faster dissociation rates than to agonist ligands. Immunity 5, 53-61.
31. Mason, D.W., and Williams, A.F. (1986). Kinetics of antibody reactions and the analysis of cell surface antigens. In Handbook of Experimental Immunology, D.M. Weir et al., eds. (Oxford: Blackwell Scientific Publications), Volume 1, Chapter 38.
32. k complexes: correlation of the dissociation rate with T-cell responsiveness. Proc. Natl. Acad. Sci. USA 91, 12862-12866.
33. McConnell, H.M., Owicki, J.C., Parce, J.W., Miller, D.L., Baxter, G.T., Wada, H.G., and Pitchford, S. (1992). The cytosensor microphysiometer: biological applications of silicon technology. Science 257, 1906-1912.
34. McKeithan, T.W. (1995). Kinetic proofreading in T-cell receptor signal transduction. Proc. Natl. Acad. Sci. USA 92, 5042-5046.
35. McMichael, A.J., and O'Callaghan, C.A. (1998). A new look at T cells. J. Exp. Med 187, 1367-1371.
36. Meuer, S.C., Hodgdon, J.C., Hussey, R.E., Protentis, J.P., Schlossman, S.F., and Reinherz, E.L. (1983). Antigen-like effects of monoclonal antibodies directed at receptors on human T cell clones. J. Exp. Med. 158, 988-995.
37. Molina, T.J., Kishihara, K., Siderovski, D.P., van Ewijk, W., Narendran, A., Timms, E., Wakeham, A., Paige, C.J., Hartmann, K.U., Veillette, A., et al. (1992). Profound block in thymocyte development in mice lacking p56lck. Nature 357, 161-164.
38. Ortega, E. (1995). How do multichain immune recognition receptors signal? A structural hypothesis. Mol. Immunol. 32, 941-945.
39. Pahler, A., Hendrickson, W.A., Kolks, M.A., Argarana, C.E., and Cantor, C.R. (1987). Characterization and crystallization of core streptavidin. J. Biol. Chem. 226, 13933-13937.
40. Punt, J.A., Roberts, J.L., Kearse, K.P., and Singer, A. (1994). Stoichiometry of the T cell antigen receptor (TCR) complex: each TCR/ CD3 complex contains one TCRα, one TCRβ, and two CD3∈ chains. J. Exp. Med. 180, 587-593.
41. Rabinowitz, J.D., Beeson, C., Lyons, D.S., Davis, M.M., and McConnell, H.M. (1996a). Kinetic discrimination in T-cell activation, Proc. Natl. Acad. Sci. USA 93, 1401-1405.
42. Rabinowitz, J.D., Beeson, C., Wülfing, C., Tate, K., Allen, P.M., Davis, M.M., and McConnell, H.M. (1996b). Altered T cell receptor ligands trigger a subset of early T cell signals. Immunity 5, 125-135.
43. Reay, P.A., Kantor, R.M., and Davis, M.M. (1994). Use of global amino acid replacement to define the requirements for MHC binding and T cell recognition of moth cytochrome c (93-103). J. Immunol. 752, 3946-3957.
44. Reich, Z., Boniface, J.J., Lyons, D.S., Borochov, N., Wachtel, E.J., and Davis, M.M. (1997). Ligand-specific oligomerization of T-cell receptor molecules. Nature 387, 617-620.
45. Reth, M., and Wienands, J. (1997). Initiation and processing of signals from the B cell antigen receptor. Annu. Rev. Immunol. 15, 453-479.
46. Rotzschke, O., Falk, K., and Strominger, J.L. (1997). Superactivation of an immune response triggered by oligomerized T cell epitopes. Proc. Natl. Acad. Sci. USA 94, 14642-14647.
47. Samelson, L.E., Germain, R.N., and Schwartz, R.H. (1983). Monoclonal antibodies against the antigen receptor on a cloned T-cell hybrid. Proc. Natl. Acad. Sci. USA 22, 6972-6976.
48. d-peptide complexes reveal that high affinity can be achieved without large anchor residues. Immunity 8, 319-329.
49. lck tyrosine kinase. Mol. Cell. Biol. 10, 1853-1862.
50. Spencer, D.M., Wandless, T.J., Schreiber, S.L., and Crabtree, G.R. (1993). Controlling signal transduction with synthetic ligands. Science 262, 1019-1024.
51. Straus, D.B., and Weiss, A. (1992). Genetic evidence for the involvement of the lck tyrosine kinase in signal transduction through the T cell antigen receptor. Cell 70, 585-593.
52. Symer, D.E., Dintzis, R.Z., Diamond, D.J., and Dintzis, H.M. (1992). Inhibition or activation of human T cell receptor transfectants is controlled by defined, soluble antigen arrays. J. Exp. Med. 176, 1421-1430.
53. + T cells by TCR ligation without aggregation even in the absence of MHC. Nature 371, 67-70.
54. Torigoe, C., Goldstein, B., Wofsy, C., and Metzger, H. (1997). Shuttling of initiating kinase between discrete aggregates of the high affinity receptor for IgE regulates the cellular response. Proc. Natl. Acad. Sci. USA 94, 1372-1377.
55. Turner, J.M., Brodsky, M.H., Irving, B.A., Levin, S.D., Perlmutter, R.M., and Littman, D.R. (1990). Interaction of the unique N-terminal region of the tyrosine kinase p56lck with the cytoplasmic domains of CD4 and CD8 is mediated by cysteine motifs. Cell 60, 755-765.
56. Valitutti, S., and Lanzavecchia, A. (1997). Serial triggering of TCRs: a basis for the sensitivity and specificity of antigen recognition, Immunol. Today 18, 299-304.
57. Watts, T.H. (1988). T cell activation by preformed, long-lived la-peptide complexes: quantitative aspects. J. Immunol. 141, 3708-3714.
58. Wülfing, C., Rabinowitz, J.D., Beeson, C., Sjaastad, M.D., McConnell, H.M., and Davis, M.M. (1997). Kinetics and extent of T cell activation as measured with the calcium signal. J. Exp. Med. 185, 1815-1825.
59. Wülfing, C., Sjaastad, M.D., and Davis, M.M. (1998). Visualizing the dynamics of T cell activation: intracellular adhesion molecule 1 migrates rapidly to the T cell/B cell interface and acts to sustain calcium levels. Proc. Natl. Acad. Sci. USA 95, 6302-6307.