Genetic evidence for differential coupling of Syk family kinases to the T-cell receptor: Reconstitution studies in a ZAP-70-deficient Jurkat T-cell line

Molecular and Cellular Biology

Volumn 18, Issue 3, 1998, Pages 1388-1399

  Williams, Brandi L ^a   Schreiber, Kathy L ^b   Zhang, Weiguo ^c   Wange, Ronald L ^a,c   Samelson, Lawrence E ^c   Leibson, Paul J ^a   Abraham, Robert T ^a,d  

^a MAYO GRADUATE SCHOOL   (United States)

^b MONTREAL HEART INSTITUTE   (Canada)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN TYROSINE KINASE;

ARTICLE; CALCIUM MOBILIZATION; ENZYME ACTIVATION; ENZYME ACTIVITY; GENETIC ANALYSIS; GENETIC TRANSFECTION; LEUKEMIA CELL LINE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 0031912097     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.18.3.1388     Document Type: Article

References (63)

1. 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.
2. + thymic selection in humans lacking Zap-70 kinase. Cell 76:947-958.
3. Binstadt, B. A., K. M. Brumbaugh, C. J. Dick, A. M. Scharenberg, B. L. Williams, M. Colonna, L. L. Lanier, J.-P. Kinet, R. T. Abraham, and P. J. Leibson. 1996. Sequential involvement of Lck and SHP-1 with MHC-recognizing receptors on NK cells inhibits FcR-initiated tyrosine kinase activation. Immunity 5:629-638.
4. Bu, J.-Y., A. S. Shaw, and A. C. Chan. 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.
5. Buerstedde, J. M., L. R. Pease, M. P. Bell, and A. E. Nilson. 1988. Identification of an immunodominant region on the I-A beta chain using site-directed mutagenesis and DNA-mediated gene transfer. J. Exp. Med. 167:473-487.
6. Burkhardt, A. L., B. Stealey, R. B. Rowley, S. Mahajan, M. Prendergast, J. Fargnoli, and J. B. Bolen. 1994. Temporal regulation of non-transmembrane protein tyrosine kinase enzyme activity following T cell antigen receptor engagement. J. Biol. Chem. 269:23642-23647.
7. Cantrell, D. 1996. T cell antigen receptor signal transduction pathway. Annu. Rev. Immunol. 14:259-274.
8. Chan, A. C., D. M. Desai, and A. Weiss. 1994. The role of protein tyrosine kinases and protein tyrosine phosphatases in T cell antigen receptor signal transduction. Annu. Rev. Immunol. 12:555-592.
9. 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.
10. Chan, A. C., M. Iwashima, C. W. Turck, and A. Weiss. 1992. ZAP-70: a 70 kd protein-tyrosine kinase that associates with the TCR ζ chain. Cell 71:649-662.
11. Chan, A. C., N. S. C. van Oers, A. Tran, L. Turka, C.-L. Law, J. C. Ryan, E. A. Clark, and A. Weiss. 1994. Differential expression of ZAP-70 and Syk protein tyrosine kinases, and the role of this family of protein tyrosine kinases in TCR signaling. J. Immunol. 152:4758-4766.
12. 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.
13. Cheng, A. M., B. Rowley, W. Pao, A. Hayday, J. B. Bolen, and T. Pawson. 1995. Syk tyrosine kinase required for mouse viability and B-cell development. Nature 378:303-306.
14. Chu, D. H., H. Spits, J.-F. Peyron, R. B. Rowley, J. B. Bolen, and A. Weiss. 1996. The Syk protein kinase can function independently of CD45 or Lck in T cell antigen receptor signaling. EMBO J. 15:6251-6261.
15. Couture, C., G. Baier, A. Altman, and T. Mustelin. 1994. p561ck-independent activation and tyrosine phosphorylation of p72syk by T-cell antigen receptor/ CD3 stimulation. Proc. Natl. Acad. Sci. USA 91:5301-5305.
16. 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.
17. Durand, D. B., J.-P. Shaw, M. R. Bush, R. E. Replogle, R. Belagaje, and G. R. Crabtree. 1988. Characterization of antigen receptor response elements within the interleukin-2 enhancer. Mol. Cell. Biol. 8:1715-1724.
18. Eischen, C. M., B. L. Williams, W. Zhang, L. E. Samelson, D. H. Lynch, R. T. Abraham, and P. J. Leibson. 1997. ZAP-70 tyrosine kinase is required for the up-regulation of Fas ligand in activation-induced T cell apoptosis. J. Immunol. 159:1135-1139.
19. Elder, M. E., D. Lin, J. Clever, A. C. Chan, T. 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.
20. El-Hillal, O., T. Kurosaki, H. Yamamura, J.-P. Kinet, and A. M. Scharenberg. 1997. Syk kinase activation by a src kinase-initiated activation loop phosphorylation chain reaction. Proc. Natl. Acad. Sci. USA 94:1919-1924.
21. Evan, G. I., G. K. Lewis, G. Ramsay, and J. M. Bishop. 1985. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5:3610-3616.
22. syk expression. J. Biol. Chem. 270:26533-26537.
23. 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. 182:1057-1065.
24. Goldsmith, M. A., and A. Weiss. 1987. Isolation and characterization of a T-lymphocyte somatic mutant with altered signal transduclion by the antigen receptor. Proc. Natl. Acad. Sci. USA 84:6879-6883.
25. Groves, T., P. Smiley, M. P. Cooke, K. Forbush, R. M. Perlmutter, and C. J. Guidos. 1996. Fyn can partially substitute for Lck in T lymphocyte development. Immunity 5:417-428.
26. 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 377:32-38.
27. Hivroz-Burgaud, C., N. A. Clipstone, and D. A. Cantrell. 1991. Signaling requirements for the expression of the transactivating factor NF-AT in human T lymphocytes. J. Immunol. 21:2811-2819.
28. Irving, B. A., A. C. Chan, and A. Weiss. 1993. Functional characterization of a signal transducing motif present in the T cell antigen receptor ζ chain. J. Exp. Med. 177:1093-1103.
29. Isakov, N., R. L. Wange, J. D. Watts, R. Aebersold, and L. E. Samelson. 1996. Purification and characterization of human ZAP-70 protein-tyrosine kinase from a baculovirus expression system. J. Biol. Chem. 271:15753-15761.
30. 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 263:1136-1139.
31. lck deficiency on the growth and cytolylic effector function of an interleukin-2-dependent cytotoxic T-cell line. Mol. Cell. Biol. 12:4521-4530.
32. Karnitz, L. M., L. A. Burns, S. L. Sutor, J. Blenis, and R. T. Abraham. 1995. Interleukin-2 triggers a novel phosphatidylinositol 3-kinase-dependent MEK activation pathway. Mol. Cell. Biol. 15:3049-3057.
33. Keshvara, L. M., C. Isaacson, M. L. Harrison, and R. L. Geahlen. 1997. Syk activation and dissociation from the B-cell antigen receptor is mediated by phosphorylation of tyrosine 130. J. Biol. Chem. 272:10377-10381.
34. Kolanus, W., C. Romeo, and B. Seed. 1993. T cell activation by clustered tyrosine kinases. Cell 74:171-183.
35. Kong, G., M. Dalton, J. B. Wardenburg, D. Straus, T. Kurosaki, and A. C. Chan. 1996. Distinct tyrosine phosphorylation sites in ZAP-70 mediate activation and negative regulation of antigen receptor function. Mol. Cell. Biol. 16:5026-5035.
36. 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.
37. Latour, S., L. M. L. Chow, and A. Veillette. 1996. Differential intrinsic enzymatic activity of Syk and ZAP-70 protein-tyrosine kinases. J. Biol. Chem. 271:22782-22790.
38. Letourneur, F., and R. D. Klausner. 1992. Activation of T cells by a tyrosine kinase activation domain in the cytoplasmic tail of CD3 epsilon. Science 255:79-82.
39. lck. Nature 357:161-164.
40. Negishi, I., N. Motoyama, K.-I. Nakayama, K. Nakayama, S. Senju, S. Hatakeyama, Q. Zhang, A. C. Chan, and D. Y. Loh. 1995. Essential rule for ZAP-70 in both positive and negative selection of thymocytes. Nature 376:435-438.
41. 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.
42. Orloff, D. G., S. J. Frank, F. A. Robey, A. M. Weissman, and R. D. Klausner. 1989. Biochemical characterization of the eta chain of the T-cell receptor. A unique subunit related to zeta. J. Biol. Chem. 264:14812-14817.
43. Park, J., H. W. Rho, and S. G. Rhee. 1991. CD3 stimulation causes phosphorylation of phospholipase C-γ1 on serine and tyrosine residues in a human T-cell line. Proc. Natl. Acad. Sci. USA 88:5453-5456.
44. Reth, M. 1989. Antigen receptor tail clue. Nature 338:383-384.
45. 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 Ig alpha/Ig beta immunoreceptor tyrosine activation motif binding and autophosphorylation. J. Biol. Chem. 270:11590-11594.
46. Secrist, J. P., L. A. Burns, L. Karnitz, G. A. Koretzky, and R. T. Abraham. 1993. Stimulatory effects of the protein tyrosine phosphatase inhibitor, pervanadate, on T-cell activation events. J. Biol. Chem. 268:5886-5893.
47. Secrist, J. P., L. Karnitz, and R. T. Abraham. 1991. T-cell antigen receptor ligation induces tyrosine phosphorylation of phospholipase C-γ1. J. Biol. Chem. 255:12135-12139.
48. Shiue, L., J. 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.
49. Stein, P. L., H. M. Lee, S. Rich, and P. Soriano. 1992. p59fyn mutant mice display differential signaling in thymocytes and peripheral T cells. Cell 70:741-750.
50. Straus, D. B., 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.
51. Ting, A. T., L. M. Karnitz, R. A. Schoon, R. T. Abraham, and P. J. Leibson. 1992. Fcγ receptor activation induces the tyrosine phosphorylation of both phospholipase C (PLC)-γ1 and PLC-γ2 in natural killer cells. J. Exp. Med. 176:1751-1755.
52. Turner, M., P. J. Mee, P. S. Costello, O. Williams, A. A. Price, L. P. Duddy, M. T. Furlong, R. L. Geahlen, and V. L. J. Tybulewicz. 1995. Perinatal lethality and blocked B-cell development in mice lacking the tyrosine kinase Syk. Nature 378:298-302.
53. van Oers, N. S., N. Killeen, and A. Weiss. 1996. Lck regulates the tyrosine phosphorylation of the T cell receptor subunits and ZAP-70 in murine thymocytes. J. Exp. Med. 183:1053-1062.
54. van Oers, N. S. C., B. Lowin-Kropf, D. Finlay, K. Connolly, and A. Weiss. 1996. αβ T cell development is abolished in mice lacking both Lck and Fyn protein tyrosine kinases. Immunity 5:429-436.
55. Van Wauwe, J. P., R. R. De Mey, and J. G. Goossens. 1980. OKT3: a monoclonal anti-human T lymphocyte antibody with potent mitogenic properties. J. Immunol. 124:2708-2713.
56. Wang, C. C., J. A. Badylak, S. E. Lux, R. Moriyama, J. E. Dixon, and P. S. Low. 1992. Expression, purification, and characterization of the functional dimeric cytoplasmic domain of human erythrocyte band 3 in Escherichia coli. Protein Sci. 1:1206-1214.
57. 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.
58. 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.
59. Wardenburg, J. B., C. Fu, J. K. Jackman, H. Flotow, S. E. Wilkinson, D. H. Williams, R. Johnson, G. Kong, A. C. Chan, and P. R. Findell. 1996. Phosphorylation of SLP-76 by the ZAP-70 protein-tyrosine kinase is required for T-cell receptor function. J. Biol. Chem. 271:19641-19644.
60. Watts, J. D., M. Affolter, D. L. Krebs, R. L. Wange, L. E. Samelson, and R. Aebersold. 1494. 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.
61. Weiss, A., G. Koretzky, R. C. Schatzman, and T. Kadlecek. 1991. Functional activation of the T-cell antigen receptor induces tyrosine phosphorylation of phospholipase C-γ1. Proc. Natl. Acad. Sci. USA 88:5484-5488.
62. Williams, B. L., and R. T. Abraham. Unpublished observations.
63. ras and calcineurin synergize to regulate the nuclear factor of activated T cells. J. Exp. Med. 178:1517-1522.