Variant TCR ligands: New insights into the molecular basis of antigen-dependent signal transduction and T-cell activation

Seminars in Immunology

Volumn 8, Issue 2, 1996, Pages 83-101

  Madrenas, Joaquín ^a,b   Germain, Ronald N ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b ROBARTS RESEARCH INSTITUTE   (Canada)

Author keywords

Antagonist; MHC molecule; Partial agonist; Peptide; T cell receptor; Variant TCR ligand

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN;

MAJOR HISTOCOMPATIBILITY COMPLEX; MODEL; RECEPTOR OCCUPANCY; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

EID: 0030008145     PISSN: 10445323     EISSN: None     Source Type: Journal    
DOI: 10.1006/smim.1996.0011     Document Type: Review

References (99)

1. Germain RN (1994) MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell 76:287-299
2. Davis MM, Bjorkman PJ (1988) T-cell antigen receptor genes and T-cell recognition. Nature 334:395-402
3. Ashwell JD, Klausner RD (1990) Genetic and mutational analysis of the T-cell antigen receptor. Annu Rev Immunol 8:139-167
4. Taga T, Kishimoto T (1995) Signaling mechanisms through cytokine receptors that share signal transducing receptor components. Curr Opin Immunol 7:17-23
5. Keegan AD, Paul WE (1992) Multichain immune recognition receptors similarities in structure and signaling pathways. Immunol Today 13:63-68
6. Matis LA, Glimcher LH, Paul WE, Schwartz RH (1983) Magnitude of response of histocompatibility-restricted T-cell clones is a function of the product of the concentrations of antigen and Ia molecules. Proc Natl Acad Sci USA 80:6019-6023
7. Ashwell JD, Fox BS, Schwartz RH (1986) Functional analysis of the interaction of the antigen-specific T cell receptor with its ligands. J Immunol 136:757-768
8. Evavold BD, Sloan-Lancaster J, Allen PM (1993) Tickling the TCR: selective T-cell functions stimulated by altered peptide ligands. Immunol Today 14:602-609
9. Sette A, Alexander J, Ruppert J, Snoke K, Franco A, Ishioka G, Grey HM (1994) Antigen analogs/ MHC complexes as specific T cell receptor antagonists. Annu Rev Immunol 12:413-431
10. Jameson SC, Bevan MJ (1995) T cell receptor antagonists and partial agonists. Immunity 2:1-12
11. Racioppi L, Germain RN (1995) Modified T cell receptor ligands moving beyond a strict occupancy model for T cell activation by ligand, in Selective Immunosuppresaon: Basic Concepts and Clinical Applications (L. Adorini, ed) (Karger, Basel). Chem Immuno 60:79-99
12. Germain RN, Levine EH, Madrenas J (1995) The T-cell receptor as a diverse signal transduction machine. The Immunologist 3:113-121
13. Janeway Jr, CA (1995) Ligands for the T-cell receptor: hard times for avidity models. Immunol Today 16:223-225
14. Klinman NR (1972) The mechanism of antigenic stimulation of primary and secondary clonal precursor cells. J Exp Med 136:241-260
15. Solinger AM, Ultee ME, Margoliash E, Schwartz RH (1979) T-lymphocyte response to cytochrome c. I. Demonstration of a T-cell heteroclitic proliferative response and identification of a topographic antigenic determinant on pigeon cytochrome c whose immune recognition requires two complementing major histocompatibility complex-linked immune response genes. J Exp Med 150:830-843
16. Fox BS, Chen C, Fraga E, French CA, Singh B, Schwartz RH (1987) Functionally distinct agretopic and epitopic sites. Analysis of the dominant T cell determinant of moth and pigeon cytochromes c with the use of synthetic peptide antigens. J Immunol 139:1578-1588
17. Rao A, Faas SJ, Cantor H (1984) Analogs that compete for antigen binding to an arsonate-reactive T-cell clone inhibit the functional response to arsonate. Cell 36:889-895
18. Janeway Jr CA, Dianzani U, Portoles P, Rath S, Reich EP, Rojo J, Yagi J, Murphy DB (1989) Cross-linking and conformational change in T-cell receptors: role in activation and in repertoire selection. Cold Spring Harb Symp Quant Biol 2:657-666
19. Mannie MD (1991) A unified model for T cell antigen recognition and thymic sslection of the T cell repertoire. J Theor Biol 151:169-192
20. Evavold BD, Allen PM (1991) Separation of IL-4 production from Th cell proliferation by an altered T cell receptor ligand. Science 252:1308-1310
21. De Magistris MT, Alexander J, Coggeshall M, Altman A, Gaeta FC, Grey HM, Sette A (1992) Antigen analog-major histocompatibility complexes act as antagonists of the T cell receptor. Cell 68:625-634
22. Racioppi L, Ronchese F, Matis LA, Germain RN (1993) Peptide-major histocompatibility complex class II complexes with mixed agonist/ antagonist properties provide evidence for ligand-related differences in T cell receptor-dependent intracellular signaling. J Exp Med 177:1047-1060
23. Jameson SC, Carbone FR, Bevan MJ (1993) Clone-specific T cell receptor antagonists of major histocompatibility complex class I-restricted cytotoxic T cells. J Exp Med 177:1541-1550
24. Sloan-Lancaster J, Evavold BD, Allen PM (1993) Induction of T-cell anergy by altered T-cell-receptor ligand on live antigen-presenting cells. Nature 363:156-159
25. Weiss A, Littman DR (1994) Signal transduction by lymphocyte antigen receptors. Cell 76:263-274
26. June CH, Fletcher MC, Ledbetter JA, Samelson LE (1990) Increases in tyrosine phosphorylation are detectable before phospholipase C activation after T cell receptor stimulation. J Immunol 144:1591-1599
27. Chan AC, Desai DM, Weiss A (1994) The role of protein tyrosine kinases and protein tyrosine phosphatases in T cell antigen receptor signal transduction. Annu Rev Immunol 12:555-592
28. Qian D, Griswold-Prenner I, Rosner MR, Fitch FW (1993) Multiple components of the T cell antigen receptor complex become tyrosine-phosphorylated upon activation. J Biol Chem 268:4488-4493
29. Irving BA, Chan AC, Weiss A (1993) Functional characterization of a signal transducing motif present in the T cell antigen receptor zeta chain. J Exp Med 177:1093-1103
30. Wange RL, Malek SN, Desiderio S, Samelson LE (1993) Tandem SH2 domains of ZAP-70 bind to T cell antigen receptor zeta and CD3 epsilon from activated Jurkat T cells. J Biol Chem 268:19797-19801
31. Bu JY, Shaw AS, Chan AC (1995) Analysis of the interaction of ZAP-70 and syk protein-tyrosine kinases with the T-cell antigen receptor by plasmon resonance. Proc Natl Acad Sci USA 92:5106-5110
32. Osman N, Lucas SC, Turner H, Cantrell D (1995) A comparison of the interaction of Shc and the tyrosine kinase ZAP-70 with the T cell antigen receptor zeta chain tyrosine-based activation motif. J Biol Chem 270:13981-13986
33. Neumeister EN, Zhu Y, Richard S, Terhorst C, Chan AC, Shaw AS (1995) Binding of ZAP-70 to phosphorylated T-cell receptor zeta and eta enhances its autophosphorylation and generates specific binding sites for SH2 domain-containing proteins. Mol Cell Biol 15:3171-3178
34. Isakov N, Wange RL, Burgess WH, Watts JD, Aebersold R, Samelson LE (1995) ZAP-70 binding specificity to T cell receptor tyrosine-based activation motifs: the tandem SH2 domains of ZAP-70 bind distinct tyrosine-based activation motifs with varying affinity. J Exp Med 181:375-380
35. Exley M, Varticovski L, Peter M, Sancho J, Terhorst C (1994) Association of phosphatidylinositol 3-kinase with a specific sequence of the T cell receptor zeta chain isdependent on T cell activation. J Biol Chem 269:15140-15146
36. Chan AC, Iwashima M, Turck CW, Weiss A (1992) ZAP-70: a 70 kd protein-tyrosine kinase that associates with the TCR zeta chain. Cell 71:649-662
37. Chan AC, Dalton M, Johnson R, Kong GH, Wang T, Thoma R, Kurosaki T (1995) Activation of ZAP-70 kinase activity by phosphorylation of tyrosine 493 is required for lymphocyte antigen receptor function. EMBO J 14:2499-2508
38. Weil R, Cloutier JF, Fournel M, Veillette A (1995) Regulation of Zap-70 by Src family tyrosine protein kinases in an antigen-specific T-cell line. J Biol Chem 270:2791-2799
39. Elder ME, Lin D, Clever J, Chan AC, Hope TJ, Weiss A, Parslow TG (1994) Human severe combined immunodeficiency due to a defect in ZAP-70, a T cell tyrosine kinase. Science 264:1596-1599
40. Chan AC, Kadlecek TA, Elder ME, Filipovich AH, Kuo WL, Iwashima M, Parslow TG, Weiss A (1994) ZAP-70 deficiency in an autosomal recessive form of severe combined immunodeficiency. Science 264:1599-1601
41. Arpaia E, Shahar M, Dadi H, Cohen A, Roifman CM (1994) Defective T cell receptor signaling and CD8 + thymic selection in humans lacking ZAP-70 kinase. Cell 76:947-958
42. Roifman CM (1995) Selection transduction defect (STD) due to ZAP-70 kinase deficiency. Immunodeficiency 5:193-211
43. Madrenas J, Wange RL, Wang JL, Isakov N, Samelson LE, Germain RN (1995) ζ phosphorylation without ZAP-70 activation induced by TCR antagonists or partial agonists. Science 267:515-518
44. Sloan-Lancaster J, Shaw AS, Rothbard JB, Allen PM (1994) Partial T cell signaling: altered phospho-ζ and lack of ZAP-70 recruitment in APL-induced T cell anergy. Cell 79:913-922
45. Windhagen A, Scholz C, Hollsberg P, Fukaura H, Sette A, Hafler DA (1995) Modulation of cytokine patterns of human autoreactive T cell clones by a single amino acid substitution of their peptide ligand. Immunity 2:373-380
46. Collins TL, Kassner PD, Bierer BE, Burakoff SJ (1994) Adhesion receptors in lymphocyte activation. Curr Opin Immunol 6:385-393
47. Dustin ML, Springer TA (1989) T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature 341:619-624
48. Valitutti S, Muller S, Cella M, Padovan E, Lanzavecchia A (1995) Serial triggering of many T-cell receptors by a few peptide-MHC complexes. Nature 375:148-151
49. Kupfer A, Singer SJ, Janeway Jr CA, Swain SL (1987) Coclustering of CD4 (L3T4) molecule with the T-cell receptor is induced by specific direct interaction of helper T cells and antigen-presenting cells. Proc Natl Acad Sci USA 84:5888-5892
50. Kupfer A, Singer SJ (1989) The specific interaction of helper T cells and antigen-presenting B cells IV. Membrane and cytoskeletal reorganizations in the bound T cell as a function of antigen dose. J Exp Med 170:1697-1713
51. Pawson T (1995) Protein modules and signalling networks. Nature 373:573-580
52. Matsui K, Boniface JJ, Steffner P, Reay PA, Davis MM (1994) Kinetics of T-cell receptor binding to peptide/ I-Ek complexes: correlation of the dissociation rate with T-cell responsiveness. Proc Natl Acad Sci USA 91:12862-12866
53. Rojo JM, Saizawa K, Janeway Jr CA (1989) Physical association of CD4 and the T-cell receptor can be induced by anti-T-cell receptor antibodies. Proc Natl Acad Sci (USA) 86:3311-3315
54. König R, Shen X, Germain RN (1995) Involvement of both MHC class II α and β chains in CD4 function indicates a role for ordered oligomerization in T cell activation. J Exp Med 182:779-787
55. Desai DM, Sap J, Schlessinger J, Weiss A (1993) Ligand-mediated negative regulation of a chimeric transmembrane receptor tyrosine phosphatase. Cell 73:541-554
56. Samelson LE, Phillips AF, Luong ET, Klausner RD (1990) Association of the fyn protein-tyrosine kinase with the T-cell antigen receptor. Proc Natl Acad Sci USA 87:4358-4362
57. Straus DB, 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
58. Hall CG, Sancho J, Terhorst C (1993) Reconstitution of T cell receptor zeta-mediated calcium mobilization in nonlymphoid cells. Science 261:915-918
59. Iwashima M, Irving BA, van Oers NS, Chan AC, Weiss A (1994) Sequential interactions of the TCR with two distinct cytoplasmic tyrosine kinases. Science 263:1136-1139
60. Gauen LK, Zhu Y, Letourneur F, Hu Q, Bolen JB, Matis LA, Klausner RD, Shaw AS (1994) Interactions of p59fyn and ZAP-70 with T-cell receptor activation motifs: defining the nature of a signaling motif. Mol Cell Biol 14:3729-3741
61. Haughn L, Gratton S, Caron L, Sekaly RP, Veillette A, Julius M (1992) Association of tyrosine kinase p56lck with CD4 inhibits the induction of growth through the αβ T-cell receptor. Nature 358:328-331
62. Ravichandran KS, Lee KK, Songyang Z, Cantley LC, Burn P, Burakoff SJ (1993) Interaction of Shc with the ζ chain of the T cell receptor upon T cell activation. Science 262:902-905
63. Straus DB, Weiss A (1993) The CD3 chains of the T cell antigen receptor associate with the ZAP-70 tyrosine kinase and are tyrosine phosphorylated after receptor stimulation. J Exp Med 178:1523-1530
64. Duplay P, Thome M, Herve F, Acuto O (1994) p56lck interacts via its src homology 2 domain with the ZAP-70 kinase. J Exp Med 179:1163-1170
65. Thome M, Duplay P, Guttinger M, Acuto O (1995) Syk and ZAP-70 mediate recruitment of p56lck/ CD4 to the activated T cell receptor/ CD3/ ζ complex. J Exp Med 181:1997-2006
66. Xu H, Littman DR (1993) A kinase-independent function of Lck in potentiating antigen-specific T cell activation. Cell 74:633-643
67. Collins TL, Burakoff SJ (1993) Tyrosine kinase activity of CD4-associated p56lck may not be required for CD4-dependent T-cell activation. Proc Natl Acad Sci USA 90:11885-11889
68. Portoles P, Rojo JM, Janeway Jr CA (1989) The co-receptor function of murine CD4. Immunol Rev 109:77-92
69. Chow LM, Fournel M, Davidson D, Veillette A (1993) Negative regulation of T-cell receptor signalling by tyrosine protein kinase p50csk. Nature 365:156-160
70. Takeuchi M, Kuramochi S, Fusaki N, Nada S, Kawamura-Tsuzuku J, Matsuda S, Semba K, Toyoshima K, Okada M, Yamamoto T (1993) Functional and physical interaction of protein-tyrosine kinases Fyn and Csk in the T-cell signaling system. J Biol Chem 268:27413-27419
71. Baldari CT, Di Somma MM, Milia E, Bergman M, Telford JL (1995) Interactions between the tyrosine kinasesp 56lck, p59fyn and p50csk in CD4 signaling in T cells. Eur J Immunol 25:919-925
72. Pani G, Kozlowski M, Cambier JC, Mills GB, Siminovitch KA (1995) Identification of the tyrosine phosphatase PTP1C as a B cell antigen receptor-associated protein involved in the regulation of B cell signaling. J Exp Med 181:2077-2084
73. Lorenz U, Ravichandran KS, Pei D, Walsh CT, Burakoff SJ, Neel BG (1994) Lck-dependent tyrosyl phosphorylation of the phosphotyrosine phosphatase SH-PTP1 in murine T cells. Mol Cell Biol 14:1824-1834
74. Negishi I, Motoyama N, Nakayama K-i, Nakayama N, Senju S, Hatakeyama S, Zhang Q, Chann AC, Loh DY (1995) Essential role for ZAP-70 in both positive and negative selection of thymocytes Nature 376:435-438
75. Jameson SC, Hogquist KA, Bevan MJ (1994) Specificity and flexibility in thymic selection. Nature 369:750-752
76. Mannie MD, Rosser JM, White GA (1995) Autologous rat myelin basic protein isa partial agonist that is converted into a full antagonist upon blockade of CD4. Evidence for the integration of efficacious and nonefficacious signals during T cell antigen recognition. J Immunol 154:2642-2654
77. Vignali DA, Strominger JL (1994) Amino acid residues that flank core peptide epitopes and the extracellular domains of CD4 modulate differential signaling through the T cell receptor. J Exp Med 179:1945-1956
78. Locksley RM, Reiner SL, Hatam F, Littman DR, Killeen N (1993) Helper T cells without CD4: control of leishmaniasis in CD4-deficient mice. Science 261:1448-1451
79. König R, Huang L-Y, Germain RN (1992) MHC class II interaction with CD4 mediated by a region analogous to the MHC class I binding site for CD8. Nature 356:796-798
80. Maroun CR, Julius M (1994) Distinct roles for CD4 and CD8 as co-receptors in T cell receptor signalling. Eur J Immunol 24:959-966
81. Garrity PA, Chen D, Rothenberg EV, Wold BJ (1994) Interleukin-2 transcription is regulated in vivo at the level of coordinated binding of both constitutive and regulated factors. Mol Cell Biol 14:2159-2169
82. Adams CC, Workman JL (1995) Binding of disparate transcriptional activators to nucleosomal DNA is inherently cooperative. Mol Cell Biol 15:1405-1421
83. Hogquist KA, Jameson SC, Heath WR, Howard JL, Bevan MJ, Carbone FR (1994) T cell receptor antagonist peptides induce positive selection. Cell 76:17-27
84. Robey E, Fowlkes BJ (1994) Selective events in T cell development. Annu Rev Immunol 12:675-705
85. van Oers NSC, Killeen N, Weiss A (1994) ZAP-70 is constitutively associated with tyrosine-phosphorylated TCR ζ in murine thymocytes and lymph node T cells. Immunity 1:675-685
86. Van Oers NS, Tao W, Watts JD, Johnson P, Aebersold R, Teh HS (1993) Constitutive tyrosine phosphorylation of the T-cell receptor (TCR) ζ subunit: regulation of TCR-associated protein tyrosine kinase activity by TCR ζ. Mol Cell Biol 13:5771-5780
87. + T cells. Annu Rev Immunol 12:635-673
88. Gautam AM, Pearson CI, Sinha AA, Smilek DE, Steinman L, Mcdevitt HO (1992) Inhibition of experimental autoimmune encephalomyelitis by a nonimmunogenic non-self peptide that binds to I-A(UI). J Immunol 148:3049-3054
89. Kuchroo VK, Greer JM, Kaul D, Ishioka G, Franco A, Sette A, Sobel RA, Lees MB (1994) A single TCR antagonist peptide inhibits experimental allergic encephalomyelitis mediated by a diverse T cell repertoire. J Immunol 153:3326-3336
90. Harding FA, McArthur JG, Gross JA, Raulet DH, Allison JP (1992) CD28-mediated signalling co-stimulates murine T cells and prevents induction of anergy in T-cell clones. Nature 356:607-660
91. DeSilva DR, Urdahl KB, Jenkins MK (1991) Clonal anergy is induced in vitro by T cell receptor occupancy in the absence of proliferation. J Immunol 147:3261-3267
92. Beverly B, Kang SM, Lenardo MJ, Schwartz RH (1992) Reversal of in vitro T cell clonal anergy by IL-2 stimulation. Int Immunol 4:661-671
93. Jenkins MK (1992) The role of cell division in the induction of clonal anergy. Immunol Today 13:69-73
94. Wucherpfennig KW, Strominger JL (1995) Molecular mimicry in T cell-mediated autoimmunity: viral peptides activate human T cell clones specific for myelin basic protein. Cell 80:695-705
95. Klenerman P, Rowlands JS, McAdam S, Edwards J, Daenke S, Lalloo D, Koppe B, Rosenberg W, Boyd D, Edwards A, Giangrande P, Phillips RE, McMichael AJ (1994) Cytotoxic T-cell activity antagonized by naturally occurring HIV-1 Gag variants. Nature 369:403-407
96. Bertoletti A, Sette A, Chisari FV, Penna A, Levrero M, De Carli M, Fiaccadori F, Ferrari C (1994) Natural variants of cytotoxic epitopesare T-cell receptor antagonists for antiviral cytotoxic T cells. Nature 369:407-410
97. Janeway Jr C, Haque S, Smith LA, Saizawa K (1987) The role of the murine L3T4 molecule in T cell activation: differential effects of anti-L3T4 on activation by monoclonal anti-receptor antibodies. J Mol Cell Immunol 3:121-131
98. Tite JP, Sloan A, Janeway Jr CA (1986) The role of L3T4 in T cell activation: L3T4 may be both an Ia-binding protein and a receptor that transduces a negative signal. J Mol Cell Immunol 2:179-190
99. Emmrich F, Strittmatter U, Eichmann K (1986) Synergism in the activation of human CD8 T cells by cross-linking the T-cell receptor complex with the CD8 differentiation antigen. Proc Natl Acad Sci USA 83:8298-8302