Dephosphorylation of ZAP-70 and inhibition of T cell activation by activated SHP1

European Journal of Immunology

Volumn 29, Issue 8, 1999, Pages 2539-2550

  Brockdorff, Johannes ^a,d   Williams, Scott ^a,c   Couture, Clément ^b   Mustelin, Tomas ^a,c  

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

^b MCGILL UNIVERSITY   (Canada)

^c SIDNEY KIMMEL CANCER CENTER   (United States)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

SHP1; Signaling; Syk; T cell; ZAP 70

Indexed keywords

CELL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE C; PROTEIN TYROSINE PHOSPHATASE; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DEPHOSPHORYLATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION INITIATION;

ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; DNA-BINDING PROTEINS; ENZYME ACTIVATION; ENZYME PRECURSORS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; JURKAT CELLS; MICE; MUTATION; NFATC TRANSCRIPTION FACTORS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PROTEIN-TYROSINE-PHOSPHATASE; RECEPTORS, ANTIGEN, T-CELL; SEQUENCE DELETION; SHP1 PROTEIN TYROSINE PHOSPHATASE; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; T-LYMPHOCYTES; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION FACTORS; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 0032767536     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1521-4141(199908)29:08<2539::AID-IMMU2539>3.0.CO;2-M     Document Type: Article

References (68)

1. Hsi, E. D., Siegel, J. N., Minami, Y., Luong, E. T., Klausner, R. D. and Samelson, L. E., T cell activation induces rapid tyrosine phosphorylation of a limited number of cellular substrates. J. Biol. Chem. 1989. 264: 10836-10842.
2. June, C. H., Fletcher, M. C., Ledbetter, J. A. and Samelson, L. E., Increases in tyrosine phosphorylation are detected before phospholipase C activation after T cell receptor stimulation. J. Immunol. 1990. 144: 1591-1598.
3. Mustelin, T., Coggeshall, K. M., Isakov, N. and Altman, A., Tyrosine phosphorylation is required for T cell antigen receptor-mediated activation of phospholipase. C. Science 1990. 247: 1584-1587.
4. June, C. H., Fletcher, M. C., Ledbetter, J. A., Schieven, G. L., Siegel, J. N., Phillips, A. F. and Samelson, L. E., Inhibition of tyrosine phosphorylation prevents T-cell receptor-mediated signal transduction. Proc. Natl. Acad. Sci. USA 1990. 87: 7722-7727.
5. Mustelin, T., T cell antigen receptor signaling: three families of tyrosine kinases and a phosphatase. Immunity 1994. 1: 351-356.
6. Zenner, G., Zurhausen, J., Burn, P. and Mustelin, T., Towards unravelling the complexity of T cell signal transduction. BioEssays 1995. 17: 967-975.
7. Weiss, A., T cell antigen receptor signal transduction: a tale of tails and cytoplasmic protein-tyrosine kinases. Cell 1993. 73: 209-212.
8. Klausner, R. D. and Samelson, L. E., T cell antigen receptor activation pathways: the tyrosine kinase connection. Cell 1991. 64: 875-878.
9. Charbonneau, H. and Tonks, N. K., 1002 protein phosphatases. Annu. Rev. Cell. Biol. 1992. 8: 463-493.
10. Walton, K. M. and Dixon, J. E., Protein tyrosine phosphatases. Annu. Rev. Biochem. 1993. 62: 101-120.
11. Mustelin, T., Brockdorff, J., Gjörloff-Wingren, A., Tailor, P., Han, S., Wang, X. and Saxena, M., Lymphocyte activation: the coming of the protein tyrosine phosphatases. Front Biosci 1998. 3: d1060-1096.
12. Plas, D. R., and Thomas, M. L., Negative regulation of antigen receptor signaling in lymphocytes. J. Mol. Med. 1998. 76: 589-598.
13. Trowbridge, I. S. and Thomas, M. L., CD45: an emerging role as a protein tyrosine phosphatase required for lymphocyte activation and development. Annu. Rev. Immunol. 1994. 12: 85-116.
14. Pingel, J. T. and Thomas, M. L., Evidence that the leukocyte-common antigen is required for antigen-induced T lymphocyte proliferation. Cell 1989. 58: 1055-1065.
15. Koretzky, G. A., Picus, J., Thomas, M. L. and Weiss, A., Tyrosine phosphatase CD45 is essential for coupling T-cell antigen receptor to the phosphatidyl inositol pathway. Nature 1990. 346: 66-68.
16. Koretzky, G. A., Kohmetscher, M. A., Kadleck, T. and Weiss, A., Restoration of T Cell receptor-mediated signal transduction by transfection of CD45 cDNA into a CD45-deficient variant of the Jurkat T cell line. J. Immunol. 1992. 149: 1138-1142.
17. 2+ oscillations. J. Exp. Med. 1992. 176: 835-844.
18. Volarevic, S., Niklinska, B. B., Burns, C. M., June, C. H., Weissman, A. M. and Ashwell, J. D., Regulation of TCR signaling by CD45 lacking transmembrane and extracellular domains. Science 1993. 260: 541-544.
19. Wallace, V. A., Penninger, J. M., Kishiharta, K., Timms, E., Shahinian, A., Pircher, H., Kundig, T. M., Ohashi, P. S. and Mak, T. W., Alterations in the level of CD45 surface expression affect the outcome of thymic selection. J. Immunol. 1997. 158: 3205-3214.
20. lck by the CD45 phosphotyrosine phosphatase. Proc. Natl. Acad. Sci. USA 1989. 86: 6302-6306.
21. lck by the leukocyte common antigen (CD45). Oncogene 1990. 5: 809-813.
22. fyn tyrosine protein kinase by the CD45 phosphotyrosine phosphatase. Eur. J. Immunol. 1992. 22: 1173-1178.
23. Ostergaard, H. L., Shackelford, D. A., Hurley, T. R., Johnson, P., Hyman, R., Sefton, B. M. and Trowbridge, I. S., Expression of CD45 alters phosphorylation of the lck-encoded tyrosine protein kinase in murine lymphoma T cell lines. Proc. Natl. Acad. Sci. USA 1989. 86: 8959-8963.
24. Hurley, T. R., Hyman, R. and Sefton, B. M., Differential effects of expression of the CD45 tyrosine protein phosphatase on the tyrosine phosphorylation of the lck, fyn and c-src tyrosine protein kinases. Mol. Cell. Biol. 1993. 13: 1651-1656.
25. Cahir McFarland, E. D., Hurley, T. R., Pingel, J. T., Sefton, B. M., Shaw, A. and Thomas, M. L., Correlation between Src family member regulation by the protein-tyrosine-phosphatase CD45 and transmembrane signaling through the T-cell receptor. Proc. Natl. Acad. Sci. USA 1993. 90: 1402-1406.
26. Matthews, R. J., Bowne, D. B., Flores, E. and Thomas, M. L., Characterization of hematopoietic intracellular protein tyrosine phosphatases: Description of a phosphatase containing an SH2 domain and another enriched in proline-, glutamic acid-, serine-, and threonine-rich sequences. Mol. Cell. Biol. 1992. 12: 2396-2405.
27. Shen, S.-H., Bastien, L., Posner, B. I. and Chrétien, P., A protein-tyrosine phosphatase with sequence similarlity to the SH2 domain of the protein-tyrosine kinases. Nature 1991. 352: 736-739.
28. Yi, T., Cleveland, J. L. and Ihle, J. N., Protein tyrosine phosphatase containing SH2 domains: Characterization, preferential expression in hematopoietic cells, and localization to human chromosome 12p12-p13. Mol. Cell. Biol. 1992. 12: 836-846.
29. Plutzky, J., Neel, B. G. and Rosenberg, R. D., Isolation of a src homology 2-containing tyrosine phosphatase. Proc. Natl. Acad. Sci. USA 1992. 89: 1123-1127.
30. Ottinger, E. A., Botfield, M. C. and Shoelson, S. E., Tandem SH2 domains confer high specificity in tyrosine kinase signaling. J. Biol. Chem. 1998. 273: 729-735.
31. Shultz, L. D. and Green, M. C., Motheaten, an immunodeficient mutant of the mouse. J. Immunol. 1976. 116: 936-943.
32. Kozlowski, M., Mlinaric-Rascan, I., Feng, G.-S., Shen, R., Pawson, T. and Siminovitch, K. A., Expression and catalytic activity of the tyrosine phosphatase PTP1C is severely impaired in motheaten and viable motheaten mice. J. Exp. Med. 1993. 178: 2157-2163.
33. Tsui, H. W., Siminovitch, K. A., de Souza, L. and Tsui, F. W. L., Motheaten and viable motheaten mice have mutations in the haematopoietic cell phosphatase gene. Nat. Genet. 1993. 4: 124-129.
34. Pani, G., Fischer, K.-D., Mlinaric-Rascan, I. and Siminovitch, K. A., Signaling capacity of the T cell antigen receptor is negatively regulated by the PTP1C tyrosine phosphatase. J. Exp. Med. 1996. 184: 839-852.
35. Lorenz, U., Ravichandran, K. S., Burakoff, S. J. and Neel, B. G., Lack of SHPTP1 results in src-family kinase hyperactivation and thymocyte hyperresponsiveness. Proc. Natl. Acad. Sci. USA 1996. 93: 9624-9629.
36. Plas, D. R., Johnson, R., Pingel, T. J., Matthews, R. J., Dalton, M., Roy, G., Chan, A. C. and Thomas, M. L., Direct regulation of ZAP-70 by SHP-1 in T cell antigen receptor signaling. Science 1996. 272: 1173-1176.
37. LCK phosphorylation and ZAP-70 binding to T cell receptor ζ, chain. Biochem. Biophys. Res. Commun. 1996. 222: 50-57.
38. Muta, T., Kurosaki, T., Misulovin, Z., Sanchez, M., Nussenzweig, M. C. and Ravetch, J. V., A 13-amino-acid motif in the cytoplasmic domain of FcγRIIB modulates B-cell receptor signaling. Nature 1994. 368: 70-73.
39. Vivier, E. and Daëron, M., Immunoreceptor tyrosine-based inhibition motifs. Immunol. Today 1997. 18: 286-291.
40. Unkeless, J. C. and Jin, J., Inhibitory receptors, ITIM sequences and phosphatases. Curr. Opin. Immunol. 1997. 9: 338-343.
41. Hof, P., Pluskey, S., Dhe-Paganon, S., Eck, M. J. and Shoelson, S. E., Crystal structure of the tyrosine phosphatase SHP-2. Cell 1998. 92: 441-450.
42. Pluskey, S., Wandless, T. J., Walsh, C. T. and Shoelson, S. E., Potent stimulation of SH-PTP2 phosphatase activity by simultaneous occupancy of both SH2 domains. J. Biol. Chem. 1995. 270: 2897-2900.
43. D'Ambrosio, D., Hippen, K. L., Minskoff, S. A., Mellman, I., Pani, G., Siminovitch, K. A. and Cambier, J. C., Recruitment and activation of PTP1C in negative regulation of antigen receptor signaling by PcγRIIB1. Science 1995. 268: 293-297.
44. Dechert, U., Adam, M., Harder, K. W., Clark-Lewis, I., and Jirik, F., Characterization of protein tyrosine phosphatase SH-PTP2. J. Biol. Chem. 1994. 269: 5602-5611.
45. Pei, D., Lorenz, U., Klingmüller, U., Neel, B. G. and Walsh, C. T., Intramolecular regulation of protein tyrosine phosphatase SH-PTP1: A new function for Src homology 2 domains. Biochemistry 1994. 33: 15483-15493.
46. Burshtyn, D. N., Scharenberg, A. M., Wagtmann, N., Rajagopalan, S., Berrada, K., Yi, T., Kinet, J.-P. and Long, E. O., Recruitment of tyrosine phosphatase HCP by the killer cell inhibitory receptor. Immunity 1996. 4: 77-85.
47. Gupta, N., Scharenberg, A. M., Burshtyn, D. N., Wagtmann, N., Lioubin, M. N., Rohrschneider, L. R., Kinet, J.-P. and Long, E. O., Negative signaling pathways of the killer cell inhibitory receptor and FcγRIIβ1 require distinct phosphatases. J. Exp. Med. 1997. 186: 473-478.
48. Raulet, D. H. and Held, W., Natural killer cell receptors: The offs and ons of NK cell recognition. Cell 1995. 82: 697-700.
49. Cyster, J. G. and Goodnow, C. C., Protein tyrosine phosphatase 1C negatively regulates antigen receptor signaling in B lymphocytes and determines thresholds for negative selection. Immunity 1995. 2: 13-24.
50. 2+ mobilization is integrated by CD19 dephosphorylation. Immunity 1997. 7: 49-58.
51. Doody, G. M., Justement, L. B., Delibrias, C. C., Matthews, R. J., Lin, J., Thomas, M. L. and Fearon, D. T., A role in B cell activation for CD22 and the protein tyrosine phosphatase SHP. Science 1995. 269: 242-244.
52. Chan, A. C., Iwashima, M., Turck, C. W. and Weiss, A., ZAP-70: A 70 kd protein-tyrosine kinase that associates with the TcR ζ chain. Cell 1992. 71: 649-662.
53. Neumeister Kersh, E., Shaw, A. S. and Allen, P. M., Fidelity of T cell activation through multistep T cell receptor z phosphorylation. Science 1998. 281: 572-575.
54. Williams, S., Couture, C., Gilman, J., Jascur, T., Dekkert, M., Altman, A. and Mustelin, T., Reconstitution of TCP-induced Erk2 kinase activation in Lck-negative JCaM1 cells by Syk, but not Zap. Eur. J. Biochem. 1997. 245: 84-90.
55. Meyaard, L., Adema, G. J., Chang, C., Woollatt, E., Sutherland, G. R., Lanier, L. L and Phillips, J. H., LAIR-1, a novel inhibitory receptor expressed on human mononuclear leukocytes. Immunity 1997. 7: 283-290.
56. Couture, C., Songyang, Z., Jascur, T., Williams, S., Tailor, P., Cantley, L. C. and Mustelin, T., Regulation of the Lck SH2 domain by tyrosine phosphorylation. J. Biol. Chem. 1996. 271: 24880-24884.
57. Jin, Y.-J., Friedman, J. and Burakoff, S. J., Regulation of tyrosine phosphorylation in isolated T cell membrane by inhibition of protein tyrosine phosphatases. J. Immunol. 1998. 161: 1743-1750.
58. Frearson, J. A. and Alexander, D. R., The phosphotyrosine phosphatase SHP-2 participates in a multimeric signaling complex and regulates T cell receptor (TCR) coupling to the Ras/mitogen-activated protein kinase (MARK) pathway in Jurkat T cells. J. Exp. Med. 1998. 187: 1417-1426.
59. Kharitonenkov, A., Schnekenburger, J., Chen, Z., Knyazev, P., Ali, S., Zwick, E., White, M. and Ullrich, A., Adapter function of protein-tyrosine phosphatase 1D in insulin receptor/insulin receptor substrate-1 interaction. J. Biol. Chem. 1995. 270: 29189-29193.
60. Noguchi, T., Matozaki, T., Horita, K., Fujioka, Y. and Kasuga, M., Role of SH-PTP2, a protein-tyrosine phosphatase with Src homology 2 domains, in insulin-stimulated Ras activation. Mol. Cell. Biol. 1994. 14: 6674-6682.
61. Rocchi, S., Tartare-Deckert, S., Sawka-Verhelle, D., Gamha, A. and Obberghen, E. V., Interaction of SH2-containing protein tyrosine phosphatase 2 with the insulin receptor and the insulin-like growth factor-1 receptor: Studies of the domains involved using the yeast two-hybrid system. Endocrinology 1996. 137: 4944-4952.
62. syk by TCR/CD3 stimulation. Proc. Natl. Acad. Sci. USA 1994. 91: 5301-5305.
63. von Willebrand, M., Jascur, T., Bonnefoy-Bérard, N., Yano, H., Altman, A., Matsuda, Y. and Mustelin, T., Inhibition of phosphatidylinositol 3-kinase blocks TCR/ CD3-induced activation of the mitogen-activated kinase Erk2. Eur. J. Biochem. 1996. 235: 828-835.
64. Straus, D. B., and Weiss, A., Genetic evidence for the involvement of the lck tyrosine kinase in signal transduction through the T cell antigen receptor. Cell 1992. 70: 585-593.
65. Jascur, T., Gilman, J. and Mustelin, T., Involvement of phosphatidylinositol 3-kinase in NFAT activation in T cells. J. Biol. Chem. 1997. 272: 14483-14488.
66. von Willebrand, M., Williams, S., Tailor, P. and Mustelin, T., Phosphorylation of the Grb2- and phosphatidyl-inositol 3-kinase p85-binding p36/38 by Syk in Lck-negative T cells. Cell. Signal. 1998. 10: 407-413.
67. Saxena, M., Williams, S., Gilman, J. and Mustelin, T., Negative regulation of T cell antigen receptor signaling by hematopoietic tyrosine phosphatase (HePTP). J. Biol. Chem. 1998. 273: 15340-15344.
68. Tailor, P., Williams, S., Gilman, J., Couture, C. and Mustelin, T., Regulation of the low molecular weight phosphotyrosine phosphatase (LMPTP) by phosphorylation at tyrosines 131 and 132. J. Biol. Chem. 1997. 272: 5371-5376.