Removal of C-terminal Src kinase from the immune synapse by a new binding protein

Molecular and Cellular Biology

Volumn 25, Issue 6, 2005, Pages 2227-2241

  Rahmouni, Souad ^a,d   Vang, Torkel ^a   Alonso, Andres ^a,e   Williams, Scott ^a   Van Stipdonk, Marianne ^b   Soncini, Chiara ^c   Moutschen, Michel ^d   Schoenberger, Stephen P ^b   Mustelin, Tomas ^a  

^a BURNHAM INSTITUTE   (United States)

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

^c PFIZER INC   (United States)

^d UNIVERSITY OF LIÈGE   (Belgium)

^e UNIVERSITY OF VALLADOLID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; INTERLEUKIN 2; PHOSPHOPROTEIN; PROTEIN CSK; PROTEIN G3BP; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ANTIGEN RECOGNITION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FRACTIONATION; CONFOCAL MICROSCOPY; GENE ACTIVATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LEUKEMIA CELL LINE; LIPID RAFT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; WESTERN BLOTTING;

EID: 14844339013     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.6.2227-2241.2005     Document Type: Article

References (66)

1. Alonso, A., S. Rahmouni, S. Williams, M. van Stipdonk, L. Jaroszewski, A. Godzik, R. T. Abraham, S. P. Schoenberger, and T. Mustelin. 2003. Tyrosine phosphorylation of VHR by ZAP-70. Nat. Immunol. 4:44-48.
2. lck, reveals its oncogenic potential in fibroblasts. Proc. Natl. Acad. Sci. USA 85:4247-4251.
3. Barnes, C. J., F. Li, M. Mandal, Z. Yang, A. A. Sahin, and R. Kumar. 2002. Heregulin induces expression, ATPase activity, and nuclear localization of G3BP, a Ras signaling component, in human breast tumors. Cancer Res. 62:1251-1255.
4. csk tyrosine kinase phosphorylates Lck at Tyr-505 and downregulates its catalytic activity. EMBO J. 11:2919-2924.
5. Brdicka, T., D. Pavlistova, A. Leo, E. Bruyns, V. Korinek, P. Angelisova, J. Scherer, A. Shevchenko, I. Hilgert, J. Cerny, K. Drbal, Y. Kuramitsu, B. Kornacker, V. Horejsi, and B. Schraven, 2000. Phosphoprotein associated with glycosphingolipid-enriched microdomains (PAG), a novel ubiquitously expressed transmembrane adapter protein, binds the protein tyrosine kinase csk and is involved in regulation of T-cell activation. J. Exp. Med. 191:1591-1604.
6. Cahir McFarland, E. D., T. R. Hurley, J. T. Pingel, B. M. Sefton, A. Shaw, and M. L. Thomas. 1993. 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 90:1402-1406.
7. 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.
8. 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.
9. csk. Nature 365:156-160.
10. csk with protein tyrosine phosphatase PEP in T cells and other hemopoietic cells. EMBO J. 15:4909-4918.
11. Cloutier, J. F., and A. Veillette. 1999. Cooperative inhibition of T-cell antigen receptor signaling by a complex between a kinase and a phosphatase. J. Exp. Med. 189:111-121.
12. syk through physical association and N-terminal tyrosine phosphorylation. Mol. Cell. Biol. 14:5249-5258.
13. lck. Eur. J. Immunol. 22:2915-2921.
14. Elbashir, S. M., J. Harborth, W. Lendeckel, A. Yalcin, K. Weber, and T. Tuschl. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494-498.
15. Gallouzi, I. E., F. Parker, K. Chebli, F. Maurier, E. Labourier, I. Barlat, J. P. Capony, B. Tocque, and T. Tazi. 1998. A novel phosphorylation- dependent RNase activity of GAP-SH3 binding protein: a potential link between signal transduction and RNA stability. Mol. Cell. Biol. 18:3956-3965.
16. Gibson, S., A. August, D. Branch, B. Dupont, and G. M. Mills. 1996. Functional LCK Is required for optimal CD28-mediated activation of the TEC family tyrosine kinase EMT/ITK. J. Biol. Chem. 271:7079-7083.
17. Gjörloff-Wingren, A., M. Saxena, S. Williams, D. Hammi, and T. Mustelin. 1999. Characterization of TCR-induced receptor-proximal signaling events negatively regulated by the protein tyrosine phosphatase PEP. Eur. J. Immunol. 29:3845-3854.
18. Guitard, E., F. Parker, F., R. Millon, J. Abecassis, and B. Tocque. 2001. G3BP is overexpressed in human tumors and promotes S phase entry. Cancer Lett. 162:213-221.
19. Heyeck, S. D., H. M. Wilcox, S. C. Bunnell, and L. J. Berg. 1997. Lck phosphorylates the activation loop tyrosine of the Itk kinase domain and activates Itk kinase activity. J. Biol. Chem. 272:25401-25408.
20. + T cells induced by major histocompatibility complex binding peptides in fetal thymic organ culture. J. Exp. Med. 177:1469-1473.
21. Hsi, E. D., J. N. Siegel, Y. Minami, E. T. Luong, R. D. Klausner, and L. E. Samelson. 1989. T-cell activation induces rapid tyrosine phosphorylation of a limited number of cellular substrates. J. Biol. Chem. 264:10836-10842.
22. Iivanainen, A. V., C. Lindqvist, T. Mustelin, and L. C. Andersson. 1990. Phosphotyrosine phosphatases are involved in reversion of T lymphoblastic proliferation. Eur. J. Immunol. 20:2509-2512.
23. 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.
24. Jascur, T., J. Gilman, and T. Mustelin. 1997. Involvement of phosphatidyl-inositol 3-kinase in NFAT activation in T cells. J. Biol. Chem. 272:14483-14488.
25. June, C. H., M. C. Hetcher, J. A. Ledbetter, and L. E. Samelson. 1990. Increases in tyrosine phosphorylation are detected before phospholipase C activation after T-cell receptor stimulation. J. Immunol. 144:1591-1598.
26. June, C. H., M. C. Fletcher, J. A. Ledbetter, G. L. Schieven, J. N. Siegel, A. F. Phillips, and L. E. Samelson. 1990. Inhibition of tyrosine phosphorylation prevents T-cell receptor-mediated signal transduction. Proc. Natl. Acad. Sci. USA 87:7722-7727.
27. Kawabuchi, M., Y. Satomi, T. Takao, Y. Shimonishi, S. Nada, K. Nagai, A. Tarakhovsky, and M. Okada. 2000. Transmembrane phosphoprotein Cbp regulates the activities of Src-family tyrosine kinases. Nature 404:999-1003.
28. Koretzky, G. A., J. Picus, M. L. Thomas, and A. Weiss, A. 1990. Tyrosine phosphatase CD45 is essential for coupling T-cell antigen receptor to the phosphatidyl inositol pathway. Nature 346:66-68.
29. Liu, K. Q., S. C. Bunnell, C. B. Gurniak, and L. J. Berg. 1998. T-cell receptor-initiated calcium release is uncoupled from capacitative calcium entry in Itk-deficient T cells. J. Exp. Med. 187:1721-1727.
30. lck) Mol. Cell. Biol. 8:540-550.
31. lck. Nature 357:161-164.
32. Mustelin, T. 1994. Src family tyrosine kinases in leukocytes. R. G. Landes Co., Austin, Tex.
33. Mustelin, T., R. T. Abraham, C. E. Rudd, A. Alonso, and J. J. Merlo. 2002. Protein tyrosine phosphorylation in T-cell signaling. Front. Biosci. 7:918-969.
34. lck by the leukocyte common antigen (CD45) Oncogene 5:809-813.
35. Mustelin, T., and P. Burn. 1993. Regulation of src-family tyrosine kinases in lymphocytes. Trends Biochem. Sci. 18:215-220.
36. lck by the CD45 phosphotyrosine phospnatase. Proc. Natl. Acad. Sci. USA 86:6302-6306.
37. Mustelin, T., K. M. Coggeshall, N. Isakov, and A. Altman. 1990. Tyrosine phosphorylation is required for T-cell antigen receptor-mediated activation of phospholipase C. Science 247:1584-1587.
38. Mustelin, T., G.-S. Feng, N. Bottini, A. Alonso, N. Kholod, D. Birle, J. J. Merlo, and H. Huynh. 2002. Protein tyrosine phosphatases. Front. Biosci. 7:85-142.
39. c-src. Nature 351:69-72.
40. Nada, S., T. Yagi, H. Takeda, T. Tokunaga, H. Nakagawa, Y. Ikawa, M. Okada, and S. Aizawa. 1993. Constitutive activation of Src family kinases in mouse embryos that lack Csk. Cell 73:1125-1135.
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 zeta and eta enhances its autophosphorylation and generates specific binding sites for SH2 domain-containing proteins. Mol. Cell. Biol. 15:3171-3178.
42. csk tyrosine kinase and engagement of its SH2 domain. Oncogene 9:1625-1631.
43. lck protein tyrosine kinase by phenylarsine oxide, a phosphotyrosine phosphatase inhibitor. Mol. Immunol. 31:1295-1302.
44. O'Shea, J. J., D. W. McVivar, T. L. Bailey, C. Burns, and M. J. Smyth. 1992. Activation of human peripheral blood T lymphocytes by pharmacological induction of protein-tyrosine phosphorylation. Proc. Natl. Acad. Sci. USA 89:10306-10310.
45. Ostergaard, H. L., D. A. Shackelford, T. R. Hurley, P. Johnson, R. Hyman, B. M. Sefton, and I. S. Trowbridge. 1989. Expression of CD45 alters phosphorylation of the Lck-encoded tyrosine protein kinase in murine lymphoma T-cell lines. Proc. Natl. Acad. Sci. USA 86:8959-8963.
46. Parker, F., F. Maurier, I. Delumeau, M. Duchesne, D. Faucher, L. Detrassche, A. Dugue, F. Schweighoffer, and B. Tocque. 1996. A Ras-GTPase-activating protein SH3-domain-binding protein. Mol. Cell. Biol. 16:2561-2569.
47. Partanen, J., E. Armstrong, M. Bergman, T. P. Mäkelä, H. Hirvonen, K. Huebner, and K. Alitalo. 1991. Cyl encodes a putative cytoplasmic tyrosine kinase lacking the conserved tyrosine autophosphorylation site (Y416src). Oncogene 6:2013-2018.
48. Perez-Villar, J. J., and S. B. Kanner. 1999. Regulated association between the tyrosine kinase Emt/Itk/Tsk and phospholipase-C γ1 in human T lymphocytes. J. Immunol. 163:6435-6441.
49. Pingel, J. T., and M. L. Thomas. 1989. Evidence that the leukocyte-common antigen is required for antigen-induced T lymphocyte proliferation. Cell 58:1055-1065.
50. Sanders, M. E., M. W. Makgoba, and S. Shaw. 1988. Human naive and memory T cells: reinterpretation of helper-inducer and suppressor-inducer subsets. Immunol. Today 9:195-199.
51. Saxena, M., S. Williams, K. Taskén, and T. Mustelin. 1999. Crosstalk between cAMP-dependent kinase and MAP kinase through hematopoietic protein tyrosine phosphatase (HePTP). Nat. Cell Biol. 1:305-311.
52. 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.
53. Sefton, B. M. 1990. The Lck tyrosine protein kinase. Oncogene 6:683-686.
54. Soncini, C., I. Berdo, and G. Draetta. 2001. Ras-GAP SH3 binding protein (G3BP) is a modulator of USP10, a novel human ubiquitin specific ligase. Oncogene 20:3869-3879.
55. 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.
56. Torgersen, K. M., T. Vang, H. Abrahamsen, S. Yaqub, V. Horejsi, B. Schraven, B. Rolstad, T. Mustelin, and K. Taskén. 2001. Release from tonic inhibition of T-cell activation through transient displacement of C-terminal Src kinase (Csk) from lipid rafts. J. Biol. Chem. 276:29313-29318.
57. fyn following T-cell antigen receptor cross-linking. J. Biol. Chem. 267:18259-18262.
58. Vang, T., K. M. Torgersen, V. Sundvold, S. Saxena, F. O. Levy, B. S. Skälhegg, V. Hansson, T. Mustelin, and K. Taskén. 2001. Activation of the COOH-terminal Src kinase (Csk) by cAMP-dependent protein kinase inhibits signaling through the T-cell receptor. J. Exp. Med. 193:497-507.
59. van Stipdonk, M. J., E. E. Lemmens, and S. P. Schoenberger. 2001. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat. Immunol. 2:423-429.
60. von Willebrand, M., T. Jascur, N. Bonnefoy-Bérard, H. Yano, A. Altman, Y. Matsuda, and T. Mustelin. 1996. Inhibition of phosphatidylinositol 3-kinase blocks TCR/CD3-induced activation of the mitogen-activated kinase Erk2. Eur. J. Biochem. 235:828-835.
61. von Willebrand, M., S. Williams, M. Saxena, J. Gilman, P. Tailor, T. Jascur, G. P. Amarante-Mendes, D. R. Green, and T. Mustelin. 1998. Modification of phosphatidylinositol 3-kinase SH2 domain binding properties by Abl- or Lck-mediated tyrosine phosphorylation at Tyr-688. J. Biol. Chem. 273:3994-4000.
62. Virolle, T., E. D. Adamson, V. Baron, D. Birle, D. Mercola, T. Mustelin, and I. de Belle. 2001. PTEN is directly transactivated in vivo by Egr-1 during irradiation-induced signalling. Nat. Cell Biol. 3:1124-1128.
63. Wang, X., A. Gjörloff-Wingren, M. Saxena, N. Pathan, J. C. Reed, and T. Mustelin. 2000. The tumor suppressor PTEN regulates T-cell survival and antigen receptor signaling by acting as a phosphatidylinositol 3-phosphatase. J. Immunol. 164:1934-1939.
64. Wang, X., H. Huynh, H., A. Gjörloff-Wingren, E. Monosov, M. Stridsberg, M. Fukuda, and T. Mustelin. 2002. Enlargement of secretory vesicles by protein tyrosine phosphatase PTP-MEG2 in RBL mast cells and Jurkat T cells. J. Immunol. 168:4612-4619.
65. Williams, S., C. Couture, J. Gilman, T. Jascur, M. Deckert, A. Altman, and T. Mustelin. 1997. Reconstitution of TCR-induced Erk2 kinase activation in Lck-negative JCaM1 cells by Syk, but not Zap. Eur. J. Biochem. 245:84-90.
66. Zbang, W. J., J. Sloan-Lancaster, J. Kitchen, R. P. Trible, and L. E. Samelson. 1998. LAT: the ZAP-70 tyrosine kinase substrate that links T-cell receptor to cellular activation. Cell 92:83-92.