The kinase, SH3, and SH2 domains of Lck play critical roles in T-cell activation after ZAP-70 membrane localization

Molecular and Cellular Biology

Volumn 16, Issue 12, 1996, Pages 7151-7160

  Yamasaki, Sho ^a,b   Takamatsu, Masako ^a   Iwashima, Makio ^a,c  

^a JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^b MITSUBISHI CHEMICAL CORPORATION   (Japan)

^c MITSUBISHI KASEI INST OF LIFE SCI   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CHIMERIC PROTEIN; MEMBRANE PROTEIN; NUCLEAR FACTOR; PHOSPHOTRANSFERASE; PROTEIN TYROSINE KINASE; T LYMPHOCYTE RECEPTOR; TYROSINE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MONKEY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

ANIMALIA;

EID: 0029909498     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.16.12.7151     Document Type: Article

References (80)

1. lck through mutation of a regulatory carboxy-terminal tyrosine residue requires intact sites of autophosphorylation and myristylation. Mol. Cell. Biol. 10:5197-5206.
2. Amrein, K. E., N. Flint, B. Panholzer, and P. Burn. 1992. Ras GTPase-activating protein: a substrate and a potential binding protein of the protein-tyrosine kinase p56lck. Proc. Natl. Acad. Sci. USA 89:3343-3346.
3. Amrein, K. E., B. Panholzer, N. A. Flint, W. Bannwarth, and P. Burn. 1993. The Src homology 2 domain of the protein-tyrosine kinase p56lck mediates both intermolecular and intramolecular interactions. Proc. Natl. Acad. Sci. USA 90:10285-10289.
4. Anderson, P., M. Caligiuri, J. Ritz, and S. F. Schlossman. 1989. CD3-negative natural killer cells express ζ TCR as part of a novel molecular complex. Nature (London) 341:159-162.
5. Aoki, Y., K. J. Isselbacher, and S. Pillai. 1994. Bruton tyrosine kinase is tyrosine phosphorylated and activated in pre-B lymphocytes and receptor-ligated B cells. Proc. Natl. Acad. Sci. USA 91:10606-10609.
6. Appleby, M. W., J. A. Gross, M. P. Cooke, S. D. Levin, X. Qian, and R. M. Perlmutter. 1992. Defective T cell receptor signaling in mice lacking the thymic isoform of p59fyn. Cell 70:751-763.
7. + thymic selection in humans lacking Zap-70 kinase. Cell 76:947-958.
8. Ashwell, J. D., R. E. Cunningham, P. D. Noguchi, and D. Hernandez. 1987. Cell growth cycle block of T cell hybridomas upon activation with antigen. J. Exp. Med. 165:173-194.
9. Baumann, G., D. Maier, F. Freuler, C. Tschopp, K. Baudisch, and J. Wienands. 1994. In vitro characterization of major ligands for Src homology 2 domains derived from protein tyrosine kinases, from the adapter protein SHC and from GTPase-activating protein in Ramos B cells. Eur. J. Immunol. 24:1799-1807.
10. Bell, G. M., and J. B. Imboden. 1995. CD2 and the regulation of T cell anergy. J. Immunol. 155:2805-2807.
11. Briggs, S. D., S. S. Bryant, R. Jove, S. D. Sanderson, and T. E. Smithgall. 1995. The Ras GTPase-activating protein (GAP) is an SH3 domain-binding protein and substrate for the Src-related tyrosine kinase, Hck. J. Biol. Chem. 270:14718-14724.
12. Cambier, J. C. 1995. New nomenclature for the Reth motif (or ARH1/TAM/ ARAM/YXXL). Immunol. Today 16:110.
13. lck. Mol. Cell. Biol. 12:2720-2729.
14. Chan, A. C., M. Dalton, R. Johnson, G.-H. Kong, T. Wang, R. Thoma, and T. Kurosaki. 1995. Activation of ZAP-70 kinase activity by phosphorylation of tyrosine 493 is required for lymphocyte antigen receptor function. EMBO J. 14:2499-2508.
15. Chan, A. C., M. Iwashima, C. W. Turck, and A. Weiss. 1992. ZAP-70: a 70kd protein-tyrosine kinase that associates with the TCR ζ chain. Cell 71:649-662.
16. Chan, A. C., T. A. Kadlecek, M. E. Elder, A. H. Filipovich, W. L. Kuo, M. Iwashima, T. G. Parslow, and A. Weiss. 1994. ZAP-70 deficiency in an autosomal recessive form of severe combined immunodeficiency. Science 264:1599-1601.
17. Cheng, G., Z.-S. Ye, and D. Baltimore. 1994. Binding of Bruton's tyrosine kinase to Fyn, Lyn, or Hck through a Src homology 3 domain-mediated interaction. Proc. Natl. Acad. Sci. USA 91:8152-8155.
18. Clark, S. G., M. J. Stern, and H. R. Horvitz. 1992. C. elegans cell-signalling gene sem-5 encodes a protein with SH2 and SH3 domains. Nature (London) 356:340-344.
19. Couture, C., G. Baier, A. Altman, and T. Mustelin. 1994. p56lck-independent activation and tyrosine phosphorylation of p72syk by T-cell antigen receptor/ CD3 stimulation. Proc. Natl. Acad. Sci. USA 91:5301-5305.
20. syk through physical association and N-terminal tyrosine phosphorylation. Mol. Cell. Biol. 14:5249-5258.
21. Crabtree, G. R., and N. A. Clipstone. 1994. Signal transmission between the plasma membrane and nucleus of T lymphocytes. Annu. Rev. Biochem. 63:1045-1083.
22. deWeers, M., G. B. Brouns, S. Hinshelwood, C. Kinnon, R. K. B. Schuurman, R. W. Hendriks, and J. Borst. 1994. B-cell antigen receptor stimulation activates the human Bruton's tyrosine kinase, which is deficient in X-linked agammaglobulinemia. J. Biol. Chem. 269:23857-23860.
23. Donovan, J. A., R. L. Wange, W. Y. Langdon, and L. E. Samelson. 1994. The protein product of the c-cbl protooncogene is the 120-kDa tyrosine-phosphorylated protein in Jurkat cells activated via the T cell antigen receptor. J. Biol. Chem. 269:22921-22924.
24. Duplay, P., M. Thome, F. Herve, and O. Acuto. 1994. p56lck interacts via its src homology 2 domain with the ZAP-70 kinase. J. Exp. Med. 179:1163-1172.
25. Elder, M. E., D. Lin, J. Clever, A. C. Chan, Y. J. Hope, A. Weiss, and T. G. Parslow. 1994. Human severe combined immunodeficiency due to a defect in ZAP-70, a T cell tyrosine kinase. Science 264:1596-1599.
26. Erpel, T., G. Superti-Furga, and S. A. Courtneidge. 1995. Mutational analysis of the Src SH3 domain: the same residues of the ligand binding surface are important for intra- and intermolecular interactions. EMBO J. 14:963-975.
27. Feng, S., J. K. Chen, H. Yu, J. A. Simon, and S. L. Schreiber. 1994. Two binding orientations for peptides to the Src SH3 domain: development of a general model for SH3-ligand interactions. Science 266:1241-1247.
28. Flanagan, W. M., B. Corthesy, R. J. Bram, and G. R. Crabtree. 1991. Nuclear association of a T-cell transcription factor blocked by FK-506 and cyclosporin A. Nature (London) 352:803-807.
29. Fukazawa, T., K. A. Reedquist, T. Trub, S. Soltoff, G. Panchamoorthy, B. Druker, L. Cantley, S. E. Shoelson, and H. Band. 1995. The SH3 domain-binding T cell tyrosyl phosphoprotein p120. J. Biol. Chem. 270:19141-19150.
30. Fukuda, T., D. Kitamura, I. Taniuchi, Y. Maekawa, L. E. Benhamou, P. Sarthou, and T. Watanabe. 1995. Restoration of surface IgM-mediated apoptosis in an anti-IgM-resistant variant of WEHI-231 lymphoma cells by HS1, a protein-tyrosine kinase substrate. Proc. Natl. Acad. Sci. USA 92: 7302-7306.
31. fyn and ZAP-70, in T-cell signaling. J. Immunol. 156:1369-1377.
32. Gelfand, E. W., K. Weinberg, B. D. Mazer, T. A. Kadlecek, and A. Weiss. 1995. Absence of ZAP-70 prevents signaling through the antigen receptor on peripheral blood T cells but not on thymocytes. J. Exp. Med. 182:1057-1066.
33. Goldsmith, M. A., and A. Weiss. 1987. Isolation and characterization of a T-lymphocyte somatic mutant with altered signal transduction by the antigen receptor. Proc. Natl. Acad. Sci. USA 84:6879-6883.
34. Hatada, M. H., X. Lu, E. R. Laird, J. Green, J. P. Morgenstern, M. Lou, C. S. Marr, T. B. Phillips, M. K. Ram, K. Theriault, M. J. Zoller, and J. L. Karas. 1995. Molecular basis for interaction of the protein tyrosine kinase ZAP-70 with the T-cell receptor. Nature (London) 377:32-38.
35. Irving, B., and A. Weiss. 1991. The cytoplasmic domain of the T cell receptor ζ chain is sufficient to couple to receptor-associated signal transduction pathways. Cell 64:891-901.
36. Iwashima, M., B. A. Irving, N. S. C. van Oers, A. C. Chan, and A. Weiss. 1994. Sequential interactions of the TCR with two distinct cytoplasmic tyrosine kinases. Science 263:1136.
37. lck on the growth and cytolytic effector function of an interleukin-2-dependent cytotoxic T-cell line. Mol. Cell. Biol. 12:4521-4530.
38. Kitamura, D., H. Kaneko, Y. Miyagoe, T. Ariyasu, and T. Watanabe. 1989. Isolation and characterization of a novel human gene expressed specifically in the cells of hematopoietic lineage. Nucleic Acids Res. 17:9367-9379.
39. Kolanus, W., C. Romeo, and B. Seed. 1993. T cell activation by clustered tyrosine kinases. Cell 74:171-183.
40. Kong, G.-H., J.-Y. Bu, T. Kurosaki, A. S. Shaw, and A. C. Chan. 1995. Reconstitution of Syk function by the ZAP-70 protein tyrosine kinase. Immunity 2:485-492.
41. Lanier, L. L., G. Yu, and J. H. Phillips. 1989. Co-association of CD3ζ with a receptor (CD16) for IgG Fc on human natural killer cells. Nature (London) 342:803-805.
42. Liao, X. C., and D. R. Littman. 1995. Altered T cell receptor signaling and disrupted T cell development in mice lacking Itk. Immunity 3:757-769.
43. Liu, J., J. D. Farmer, W. S. Lane, J. Friedman, I. Weissman, and S. L. Schreiber. 1991. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66:807-815.
44. Madrenas, J., R. L. Wange, J. L. Wang, N. Isakov, L. E. Samelson, and R. N. Germain. 1995. ζ phosphorylation without ZAP-70 activation induced by TCR antagonists or partial agonists. Science 267:515-518.
45. Moingeon, P., H.-C. Chang, P. H. Sayre, L. K. Clayton, A. Alcover, P. Gardner, and E. L. Reinherz. 1989. The structural biology of CD2. Immunol. Rev. 111:111-144.
46. Molina, T. J., K. Kishihara, D. P. Siderovski, W. van Ewijk, A. Narendran, E. Timms, A. Wakeham, C. J. Paige, K.-U. Hartmann, A. Veillette, D. Davidson, and T. W. Mak. 1992. Profound block in thymocyte development in mice lacking p56lck. Nature (London) 357:161-164.
47. Moroi, Y., Y. Koga, K. Nakamura, M. Ohtsu, G. Kimura, and K. Nomoto. 1991. Accumulation of p60lck in HTLV-1-transformed T cell lines detected by an anti-Lck monoclonal antibody, MOL 171. Jpn. J. Cancer Res. 82:909-915.
48. Negishi, I., N. Motoyama, K.-I. Nakayama, K. Nakayama, S. Senju, S. Hatakeyama, Q. Zhang, A. C. Chan, and D. Y. Loh. 1995. Essential role for ZAP-70 in both positive and negative selection of thymocytes. Nature (London) 376:435-438.
49. Neumeister, E. N., Y. Zhu, S. Richard, C. Terhorst, A. C. Chan, and A. S. Shaw. 1995. Binding of ZAP-70 to phosphorylated T-cell receptor ζ and η enhances its autophosphorylation and generates specific binding sites for SH2-domain-containing proteins. Mol. Cell. Biol. 15:3171-3178.
50. Northrop, J. P., K. S. Ullman, and G. R. Crabtree. 1993. Characterization of the nuclear and cytoplasmic components of the lymphoid-specific nuclear factor of activated T cells (NF-AT) complex. J. Biol. Chem. 268:2917-2923.
51. Pawson, T. 1995. Protein modules and signalling networks. Nature (London) 373:573-580.
52. lck SH3 domain binds to PI 3-kinase but not PI 4-kinase. Mol. Cell. Biol. 13:7708-7717.
53. Rawlings, D. J., and O. N. Wittee. 1995. The Btk subfamily of cytoplasmic tyrosine kinases: structure, regulation and function. Semin. Immunol. 7:237-246.
54. Reedquist, K. A., T. Fukazawa, B. Druker, G. Panchamoorthy, S. E. Shoelson, and H. Bond. 1994. Rapid T-cell receptor-mediated tyrosine phosphorylation of p120, an Fyn/Lck Src homology 3 domain-binding protein. Proc. Natl. Acad. Sci. USA 91:4135-4139.
55. Resh, M. D. 1994. Myristylation and palmitylation of Src family members: the fats of the matter. Cell 76:411-413.
56. Reth, M. 1989. Antigen receptor tail clue. Nature (London) 338:383-384.
57. Rowley, R. B., A. L. Burkhardt, H.-G. Chao, G. R. Matsueda, and J. B. Bolen. 1995. Syk protein-tyrosine kinase is regulated by tyrosine-phosphorylated Igα/Igβ immunoreceptor tyrosine activation motif binding and autophosphorylation. J. Biol. Chem. 270:11590-11594.
58. Rudd, C. E., O. Janssen, Y.-C. Cai, A. J. da Silva, M. Raab, and K. V. S. Prasad. 1994. Two-step TCRζ/CD3-CD4 and CD28 signaling in T cells: SH2/SH3 domains, protein-tyrosine and lipid kinases. Immunol. Today 15: 225-234.
59. Saouaf, S. J., S. Mahajan, R. B. Rowley, S. A. Kut, J. Fargnoli, A. L. Burkhardt, S. Tsukada, O. N. Witte, and J. B. Bolen. 1994. Temporal differences in the activation of three classes of non-transmembrane protein tyrosine kinases following B-cell antigen receptor surface engagement. Proc. Natl. Acad. Sci. USA 91:9524-9528.
60. Sewell, W. A., M. H. Brown, J. Dunne, M. J. Owen, and M. J. Crumpton. 1986. Molecular cloning of the human T-lymphocyte surface CD2(T11) antigen. Proc. Natl. Acad. Sci. USA 83:8718-8722.
61. Shiue, L., M. J. Zoller, and J. S. Brugge. 1995. Syk is activated by phosphotyrosine-containing peptides representing the tyrosine-based activation motifs of the high affinity receptor for IgE. J. Biol. Chem. 270:10498-10502.
62. Sloan-Lancaster, J., A. S. Shaw, J. B. Rothbard, and P. M. Allen. 1994. Partial T cell signaling: altered phospho-ζ and lack of Zap70 recruitment in APL-induced T cell anergy. Cell 79:913-922.
63. Stein, P. L., H.-M. Lee, S. Rich, and P. Soriano. 1992. pp59fyn mutant mice display differential signaling in thymocytes and peripheral T cells. Cell 70: 741-750.
64. Straus, D., and A. Weiss. 1992. Genetic evidence for the involvement of the Lck tyrosine kinase in signal transduction through the T cell antigen receptor. Cell 70:585-593.
65. Straus, D., A. C. Chan, B. Patai, and A. Weiss. 1996. SH2 domain function is essential for the role of the Lck tyrosine kinase in T cell receptor signal transduction. J. Biol. Chem. 271:9976-9981.
66. Takemoto, Y., M. Furuta, X.-K. Li, W. J. Strong-Sparks, and Y. Hashimoto. 1995. LckBP1, a proline-rich protein expressed in hematopoietic lineage cells, directly associates with the SH3 domain of protein tyrosine kinase p56lck. EMBO J. 14:3403-3414.
67. Takeya, T., and H. Hanafusa. 1983. Structure and sequence of the cellular gene homologous to the RSV src gene and the mechanism for generating the transforming virus. Cell 32:881-890.
68. Taniuchi, I., D. Kitamura, Y. Maekawa, T. Fukuda, H. Kishi, and T. Watanabe. 1995. Antigen-receptor induced clonal expansion and deletion of lymphocytes are impaired in mice lacking HS1 protein, a substrate of the antigen-receptor-coupled tyrosine kinases. EMBO J. 14:3664-3678.
69. Thome, M., P. Duplay, M. Guttinger, and O. Acuto. 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.
70. van Oers, N. S. C., N. Killeen, and A. Weiss. 1994. ZAP-70 is constitutively associated with tyrosine-phosphorylated TCRζ in murine thymocytes and lymph node T cells. Immunity 1:675-685.
71. Vogel, L. B., and D. J. Fujita. 1993. The SH3 domain of p56lck is involved in binding to phosphatidylinositol 3′-kinase from T lymphocytes. Mol. Cell. Biol. 13:7408-7417.
72. Wange, R. L., R. Guitian, N. Isakov, J. D. Watts, R. Aebersold, and L. E. Samelson. 1995. Activating and inhibitory mutations in adjacent tyrosines in the kinase domain of ZAP-70. J. Biol. Chem. 270:18730-18733.
73. Wange, R. L., S. N. Malek, S. Desiderio, and L. E. Samelson. 1993. Tandem SH2 domains of ZAP-70 bind to T cell antigen receptor ζ and CD3ε from activated Jurkat T cells. J. Biol. Chem. 268:19797-19801.
74. Watts, J. D., M. Affolter, D. L. Krebs, R. L. Wange, L. E. Samelson, and R. Aebersold. 1994. Identification by electrospray ionization mass spectrometry of the sites of tyrosine phosphorylation induced in activated Jurkat T cells on the protein tyrosine kinase ZAP-70. J. Biol. Chem. 269:29520-29529.
75. Weiss, A., and D. R. Littman. 1994. Signal transduction by lymphocyte antigen receptors. Cell 76:263-274.
76. Weiss, A., and J. D. Stobo. 1984. Requirement for the coexpression of T3 and the T cell antigen receptor on a malignant human T cell line. J. Exp. Med. 160:1284-1299.
77. lck. Immunity 4:494-504.
78. Xu, H., and D. R. Littman. 1993. A kinase-independent function of lck in potentiating antigen-specific T cell activation. Cell 74:633-643.
79. Yamanashi, Y., M. Okada, T. Semba, T. Yamori, H. Umemori, S. Tsunasawa, K. Toyoshima, D. Kitamura, T. Watanabe, and T. Yamamoto. 1993. Identification of HS1 protein as a major substrate of protein-tyrosine kinase(s) upon B-cell antigen receptor-mediated signaling. Proc. Natl. Acad. Sci. USA 90:3631-3635.
80. Yang, W., S. N. Malek, and S. Desiderio. 1995. An SH3-binding site conserved in Bruton's tyrosine kinase and related tyrosine kinases mediates specific protein interactions in vitro and in vivo. J. Biol. Chem. 270:20832-20840.