Phosphoprotein associated with glycosphingolipid-enriched microdomains (PAG), a novel ubiquitously expressed transmembrane adaptor protein, binds the protein tyrosine kinase Csk and is involved in regulation of T cell activation

Journal of Experimental Medicine

Volumn 191, Issue 9, 2000, Pages 1591-1604

  Brdička, Tomáš ^a   Pavlištová, Dagmar ^a   Leo, Albrecht ^b   Bruyns, Eddy ^b   Kořínek, Vladimír ^a   Angelisová, Pavla ^a   Scherer, Jeanette ^b   Shevchenko, Andrej ^c   Shevchenko, Anna ^c   Hilgert, Ivan ^a   Černý, Jan ^a,d   Drbal, Karel ^a   Kuramitsu, Yasuhiro ^b   Kornacker, Birgit ^b   Hořejší, Václav ^a,d   Schraven, Burkhart ^b  

^a INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d CHARLES UNIVERSITY   (Czech Republic)

Author keywords

Csk; Lymphocytes; Phosphorylation; Signal transduction; Src family kinases

Indexed keywords

ADAPTOR PROTEIN; GLYCOSPHINGOLIPID; MEMBRANE PROTEIN; NUCLEAR FACTOR; PHOSPHOPROTEIN; PROTEIN TYROSINE KINASE; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CELL STRAIN COS1; CONTROLLED STUDY; DEPHOSPHORYLATION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION;

AMINO ACID SEQUENCE; ANTIGENS, CD3; CLONING, MOLECULAR; DNA, COMPLEMENTARY; GLYCOSPHINGOLIPIDS; HUMANS; LYMPHOCYTE ACTIVATION; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN-TYROSINE KINASES; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 0342313755     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.191.9.1591     Document Type: Article

References (63)

1. Tamir, I., and J.C. Cambier. 1998. Antigen receptor signaling: integration of protein tyrosine kinase functions. Oncogene. 17:1353-1364.
2. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature. 387:569-572.
3. Xavier, R., and B. Seed. 1999. Membrane compartmentation and the response to antigen. Curr. Opin. Immunol. 11: 265-269.
4. Brown, D.A., and E. London. 1998. Structure and origin of ordered lipid domains in biological membranes. J. Membr. Biol. 164:103-114.
5. Harder, T., and K. Simons. 1997. Caveolae, DIGs, and the dynamics of sphingolipid-cholesterol microdomains. Curr. Opin. Cell Biol. 9:534-542.
6. Schroeder, R., E. London, and D. Brown. 1994. Interactions between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behavior. Proc. Natl. Acad. Sci. USA. 91:12130-12134.
7. Schroeder, R.J., S.N. Ahmed, Y. Zhu, E. London, and D.A. Brown. 1998. Cholesterol and sphingolipid enhance the Triton X-100 insolubility of glycosylphosphatidylinositol-anchored proteins by promoting the formation of detergent-insoluble ordered membrane domains. J. Biol. Chem. 273:1150-1157.
8. Brown, D.A., and J.K. Rose. 1992. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 68:533-544.
9. Cinek, T., and V. Hořejší. 1992. The nature of large noncovalent complexes containing glycosyl-phosphatidylinositol-anchored membrane glycoproteins and protein tyrosine kinases. J. Immunol. 149:2262-2270.
10. lyn are associated in large detergent-resistant complexes in rat basophilic leukemia cells. Proc. Natl. Acad. Sci. USA. 90:3611-3615.
11. Hořejší, V., K. Drbal, M. Cebecauer, J. Černý, T. Brdička, P. Angelisová, and H. Stockinger. 1999. GPI-microdomains: a role in signalling via immunoreceptors. Immunol. Today. 20: 356-361.
12. Ilangumaran, S., H.-T. He, and D. Hoessli. 2000. Microdomains in lymphocyte signalling: beyond GPI-anchored proteins. Immunol. Today. 21:2-7.
13. Zhang, W., J. Sloan-Lancaster, J. Kitchen, R.P. Trible, and L.E. Samelson. 1998. LAT: the ZAP70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell. 92: 83-92.
14. Brdička, T., J. Černý, and V. Hořejší. 1998. T cell receptor signalling results in rapid tyrosine phosphorylation of the linker protein LAT present in detergent-resistant membrane microdomains. Biochem. Biophys. Res. Commun. 248:356-360.
15. Zhang, W., R.P. Trible, and L.E. Samelson. 1998. LAT palmitoylation: its essential role in membrane microdomain targeting and tyrosine phosphorylation during T cell activation. Immunity. 9:239-246.
16. Rodgers, W., B. Crise, and J.K. Rose. 1994. Signals determining protein tyrosine kinase and glycosyl-phosphatidylinositol-anchored protein targeting to a glycolipid-enriched membrane fraction. Mol. Cell. Biol. 14:5384-5391.
17. Melkonian, K.A., A.G. Ostermeyer, J.Z. Chen, M.G. Roth, and D.A. Brown. 1999. Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated. J. Biol. Chem. 274:3910-3917.
18. Cinek, T., I. Hilgert, and V. Hořejší. 1995. An alternative way of CD4 and CD8 association with protein kinases of the Src family. Immunogenetics. 41:110-116.
19. lck. Cell. 55:301-308.
20. Bosselut, R., W. Zhang, J.M. Ashe, J.L. Kopacz, L.E. Samelson, and A. Singer. 1999. Association of the adaptor molecule LAT with CD4 and CD8 coreceptors identifies a new coreceptor function in T cell receptor signal transduction. J. Exp. Med. 190:1517-1526.
21. lyn to detergent-resistant membrane domains accompanies cellular signaling. Proc. Natl. Acad. Sci. USA. 92:9201-9205.
22. Xavier, R., T. Brennan, Q. Li, C. McCormack, and B. Seed. 1998. Membrane compartmentalization is required for efficient T cell activation. Immunity. 8:723-732.
23. Montixi, C., C. Langlet, A.M. Bernard, J. Thimonier, C. Dubois, M.A. Wurbel, J.P. Chauvin, M. Pierres, and H.T. He. 1998. Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO (Eur. Mol. Biol. Organ.) J. 17:5334-5348.
24. Viola, A., S. Schroeder, Y. Sakakibara, and A. Lanzavecchia. 1999. T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science. 283:680-682.
25. Cheng, P.C., M.L. Dykstra, R.N. Mitchell, and S.K. Pierce. 1999. A role for lipid rafts in B cell antigen receptor signaling and antigen targeting. J. Exp. Med. 190:1549-1560.
26. Janes, P.W., S.C. Ley, and A.I. Magee. 1999. Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J. Cell. Biol. 147:447-461.
27. Kosugi, A., S. Saitoh, S. Noda, K. Yasuda, F. Hayashi, M. Ogata, and T. Hamaoka. 1999. Translocation of tyrosine-phosphorylated TCRζ chain to glycolipid-enriched membrane domains upon T cell activation. Int. Immunol. 11: 1395-1401.
28. Sheets, E.D., D. Holowka, and B. Baird. 1999. Critical role for cholesterol in Lyn-mediated tyrosine phosphorylation of Fc∈RI and their association with detergent-resistant membranes. J. Cell Biol. 145:877-887.
29. Stulnig, T.M., M. Berger, T. Sigmund, D. Raederstorff, H. Stockinger, and W. Waldhausl. 1998. Polyunsaturated fatty acids inhibit T cell signal transduction by modification of detergent-insoluble membrane domains. J. Cell Biol. 143:637-644.
30. fyn with the glycosyl phosphatidylinositol-anchored proteins Thy-1 and CD48 in rat thymocytes is dependent on the state of cellular activation. Eur. J. Immunol. 23:2540-2544.
31. Ilangumaran, S., S. Arni, G. van Echten-Deckert, B. Borisch, and D.C. Hoessli. 1999. Microdomain-dependent regulation of Lck and Fyn protein-tyrosine kinases in T lymphocyte plasma membranes. Mol. Biol. Cell. 10:891-905.
32. fyn in human T-lymphocytes. J. Biol. Chem. 272:16077-16080.
33. Marie-Cardine, A., H. Kirchgessner, and B. Schraven. 1999. Molecular alterations of the Fyn-complex occur as late events of human T cell activation. Eur. J. Immunol. 29:1175-1187.
34. Schraven, B., E. Bruyns, H. Kirchgessner, S. Meuer, and A. Marie-Cardine. 1997. Identification and molecular characterisation of novel phosphoproteins associated with signaling receptor complexes in human T-lymphocytes. In Kinases and Phosphatases in Lymphocyte and Neuronal Signaling. H. Yakura, editor. Springer Verlag, Berlin. 100-111.
35. Williams, B.L., K.L. Schreiber, W. Zhang, R.L. Wange, L.E. Samelson, P.J. Leibson, and R.T. Abraham. 1998. Genetic evidence for differential coupling of Syk family kinases to the T cell receptor: reconstitution studies in a ZAP70-deficient Jurkat T-cell line. Mol. Cell. Biol. 18:1388-1399.
36. 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.
37. Schraven, B., S. Ratnofsky, Y. Gaumont, H. Lindegger, H. Kirchgessner, E. Bruyns, U. Moebius, and S.C. Meuer. 1994. Identification of a novel dimeric phosphoprotein (PP29/30) associated with signaling receptors in human T lymphocytes and natural killer cells. J. Exp. Med. 180:897-906.
38. Bruyns, E., A. Marie-Cardine, H. Kirchgessner, K. Sagolla, A. Shevchenko, M. Mann, F. Autschbach, A. Bensussan, S. Meuer, and B. Schraven. 1998. T cell receptor (TCR) interacting molecule (TRIM), a novel disulfide-linked duner associated with the TCR-CD3-ζ complex, recruits intracellular signaling proteins to the plasma membrane. J. Exp. Med. 188:561-575.
39. Shevchenko, A., M. Wilm, O. Vorm, and M. Mann. 1996. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68:850-858.
40. Wilm, M., and M. Mann. 1996. Analytical properties of the nanoelectrospray ion source. Anal. Chem. 68:1-8.
41. Wilm, M., A. Shevchenko, T. Houthaeve, S. Breit, L. Schweigerer, T. Fotsis, and M. Mann. 1996. Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature. 379:466-469.
42. Mizushima, S., and S. Nagata. 1990. pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res. 18:5322.
43. Černý, J., H. Stockinger, and V. Hořejší. 1996. Noncovalent associations of T lymphocyte surface proteins. Eur. J. Immunol. 26:2335-2343.
44. Marie-Cardine, A., H. Kirchgessner, E. Bruyns, A. Shevchenko, M. Mann, F. Autschbach, S. Ratnofsky, S. Meuer, and B. Schraven. 1999. SHP2-interacting transmembrane adaptor protein (SIT), a novel disulfide-linked dimer regulating human T cell activation. J. Exp. Med. 189:1181-1194.
45. Hanke, J.H., J.P. Gardner, R.L. Dow, P.S. Changelian, W.H. Brissette, E.J. Weringer, B.A. Pollok, and P.A. Connelly. 1996. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J. Biol. Chem. 271:695-701.
46. Mayer, B.J., and M.J. Eck. 1995. Minding your p's and q's. Curr. Biol. 5:364-367.
47. Schraven, B., A. Marie-Cardine, C. Hubener, E. Bruyns, and I. Ding. 1999. Integration of receptor-mediated signals in T cells by transmembrane adaptor proteins. Immunol. Today. 20:431-434.
48. Marie-Cardine, A., and B. Schraven. 1999. Coupling the TCR to downstream signalling pathways: the role of cytoplasmic and transmembrane adaptor proteins. Cell. Signal. 11: 705-712.
49. Motto, D.G., S.E. Ross, J. Wu, L.R. Hendricks-Taylor, and G.A. Koretzky. 1996. Implication of the GRB2-associated phosphoprotein SLP-76 in T cell receptor-mediated interleukin 2 production. J. Exp. Med. 183:1937-1943.
50. csk with protein tyrosine phosphatase PEP in T cells and other hemopoietic cells. EMBO (Eur. Mol. Biol. Organ.) J. 15:4909-4918.
51. csk is associated with protein-tyrosine phosphatase PTP-PEST in hemopoietic and non-hemopoietic cells. J. Biol. Chem. 272:23455-23462.
52. Okada, M., S. Nada, Y. Yamanashi, T. Yamamoto, and H. Nakagawa. 1991. CSK: a protein-tyrosine kinase involved in regulation of src family kinases. J. Biol. Chem. 266:24249-24252.
53. lck at Tyr-505 and down regulates its catalytic activity. EMBO (Eur. Mol. Biol. Organ.) J. 11:2919-2924.
54. csk. Nature. 365:156-159.
55. 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.
56. Imamoto, A., and P. Soriano. 1993. Disruption of the csk gene, encoding a negative regulator of Src family tyrosine kinases, leads to neural tube defects and embryonic lethality in mice. Cell. 73:1117-1124.
57. Schmedt, C., K. Saijo, T. Niidome, R. Kuhn, S. Aizawa, and A. Tarakhovsky. 1998. Csk controls antigen receptor-mediated development and selection of T-lineage cells. Nature. 394:901-904.
58. 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.
59. Gjorloff-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.
60. Timms, J.F., K.D. Swanson, A. Marie-Cardine, M. Raab, C.E. Rudd, B. Schraven, and B.G. Neel. 1999. SHPS-1 is a scaffold for assembling distinct adhesion-regulated multi-protein complexes in macrophages. Curr. Biol. 9:927-930.
61. Hunter, A.J., N. Ottoson, N. Boerth, G.A. Koretzky, and Y. Shimizu. 2000. A novel function for the SLAP-130/FYB adapter protein in β1 integrin signaling and T lymphocyte migration. J. Immunol. 164:1143-1147.
62. Biemann, K. 1988. Contributions of mass spectrometry to peptide and protein structure. Biomed. Environ. Mass Spectrom. 16:99-111.
63. Mann, M., and M. Wilm. 1994. Error-tolerant identification of peptides in sequence databases by peptide sequence tags. Anal. Chem. 66:4390-4399.