Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor

Journal of Cell Biology

Volumn 147, Issue 2, 1999, Pages 447-461

  Janes, Peter W ^a   Ley, Steven C ^a   Magee, Anthony I ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Cholera toxin B; LCK; Lipid rafts; Signal transduction; T cell antigen receptor

Indexed keywords

CD45 ANTIGEN; CHOLERA TOXIN B SUBUNIT; DETERGENT; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; LIPID; OKT 3; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE; T LYMPHOCYTE RECEPTOR; TYROSINE;

ARTICLE; CHIMERA; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; LIPID MEMBRANE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; CELL MEMBRANE; HUMANS; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MEMBRANE LIPIDS; MICE; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 0032727709     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.147.2.447     Document Type: Article

References (75)

1. Anderson, R.G.W. 1998. The caveolae membrane system. Annu. Rev. Biochem. 67:199-225.
2. Boniface, J.J., J.D. Rabinowitz, C. Wulfing, J. Hampl, Z. Reich, J.D. Altman, R.M. Kantor, C. Beeson, H.M. McConnell, and M.M. Davis. 1998. Initiation of signal transduction through the T cell receptor requires the peptide multi-valent engagement of MHC ligands. Immunity. 9:459-466.
3. Brdicka, T., J. Cerny, and V. Horejsi. 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.
4. Brown, D. 1993. The tyrosine kinase connection: how GPI-anchored proteins activate T cells. Curr. Opin. Immunol. 5:349-354.
5. 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.
6. Brown, D.A., and E. London. 1998. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14:111-136.
7. Buday, L., S.E. Egan, P.R. Viciana, D.A. Cantrell, and J. Downward. 1994. A complex of GRB2 adaptor protein, Sos exchange factor, and 36 kDa membrane bound tyrosine phosphoprotein is implicated in Ras activation in T cells. J. Biol. Chem. 269:9019-9023.
8. Cantrell, D. 1996. T cell antigen receptor signal transduction pathways. Annu. Rev. Immunol. 14:259-274.
9. 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 zeta chain. Cell. 71: 649-662.
10. Chan, A.C., and A.S. Shaw. 1996. Regulation of antigen receptor signal transduction by protein tyrosine kinases. Curr. Opin. Immunol. 8:394-401.
11. Cubitt, A.B., R. Heim, S.R. Adams, A.E. Boyd, L.A. Gross, and R.Y. Tsien. 1995. Understanding, improving and using green fluorescent proteins. Trends Biochem. Sci. 20:448-455.
12. D'Ambrosio, D., D.A. Cantrell. L. Frati, A. Santoni, and R. Testi. 1994. Involvement of p21ras activation in T cell CD69 expression. Eur. J. Immunol. 24:616-620.
13. D'Oro, U., and J.D. Ashwell. 1999. The CD45 tyrosine phosphatase is an inhibitor of Lck activity in thymocytes. J. Immunol. 162:1879-1883.
14. Davis, S.J., and P.A. van der Merwe. 1996. The structure and ligand interactions of CD2: implications for T cell function. Immunol. Today. 17:177-187.
15. Deckert, M., M. Ticchioni, B. Mari, D. Mary, and A. Bernard. 1995. The glycosylphosphatidylinositol-anchored CD59 protein stimulates both T cell receptor ζ/ZAP-70-dependent and -independent signaling pathways in T cells. Eur. J. Immunol. 25:1815-1822.
16. Dustin, M., and A.S. Shaw. 1999. Costimulation: building an immunological synapse. Science. 283:649-650.
17. Field, K.A., D. Holowka, and B. Baird. 1997. Compartmentalized activation of the high affinity immunoglobulin E receptor within membrane domains. J. Biol. Chem. 272:4276-4280.
18. Finco, T.S., T. Kadlecek, W. Zhang, L.E. Samelson, and A. Weiss. 1998. LAT is required for TCR-mediated activation of PLC-γ1 and the Ras pathway. Immunity. 9:617-626.
19. Fra, A.M., E. Williamson, K. Simons, and R.G. Parton. 1994. Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J. Biol. Chem. 269:30745-30748.
20. Furukawa, T., M. Itoh, N.X. Krueger, M. Streuli, and H. Saito. 1994. Specific interaction of the CD45 protein tyrosine phosphatase with tyrosine phosphorylated CD3 ζ chain. Proc. Natl. Acad. Sci. USA. 91:10928-10932.
21. 2-terminal domain of Gi1α is sufficient to target a green fluorescent protein reporter to caveolin-enriched plasma membrane domains. J. Biol. Chem. 274:5843-5850.
22. lck in nonlymphoid cells. J. Biol. Chem 272:12754-12761.
23. Gouy, H., P. Deterre, P. Debre, and G. Bismuth. 1994. Cell calcium signaling via GM1 cell surface gangliosides in the human Jurkat T cell line. J. Immunol. 152:3271-3281.
24. Grakoui, A., S.K. Bromley, C. Sumen, M.M. Davis, A.S. Shaw, P.M. Allen, and M.L. Dustin. 1999. The immunological synapse: a molecular machine controlling T cell activation. Science. 285:221-227.
25. Hanada, K., M. Nishijima, Y. Akamatsu, and R.E. Pagano. 1995. Both sphingolipids and cholesterol participate in the detergent insolubility of alkaline phosphatase, a glycosylphosphatidylinositol-anchored protein, in mammalian membranes. J. Biol. Chem. 270:6254-6260.
26. Harder, T., and K. Simons. 1999. Clusters of glycolipid and glycosylphosphatidylinositol-anchored proteins in lymphoid cells: accumulation of actin regulated by local tyrosine phosphorylation. Eur. J. Immunol. 29:556-562.
27. Harder, T., P. Scheiffele, P. Verkade, and K. Simons. 1998. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141:929-942.
28. Huby, R.D.J., G.W. Carlile, and S.C. Ley. 1995. Interactions between the protein-tyrosine kinase. ZAP-70, the proto-oncoprotein Vav and tubulin in Jurkat T cells. J. Biol. Chem. 270:30241-30244.
29. Huby, R.D.J., A. Weiss, and S.C. Ley. 1998. Nocodazole inhibits signal transduction by the T cell antigen receptor. J. Biol. Chem. 273:12024-12031.
30. Ilangumaran, S., and D.C. Hoessli. 1998. Effects of cholesterol depletion by cyclodextrin on the sphingolipid microdomains of the plasma membrane. Biochem. J. 335:433-440.
31. Isakov, N. 1997. Immunoreceptor tyrosine-based activation motif (ITAM), a unique module linking antigen and Fc receptors to their signalling cascades. J. Leuk. Biol. 61:6-16.
32. Kabouridis, P.S., A.I. Magee, and S.C. Ley. 1997. S-acylation of LCK protein tyrosine kinase is essential for its signalling function in T lymphocytes. EMBO (Eur. Mol. Biol. Organ) J. 16:4983-4998.
33. lck deficiency on the growth and cytolytic effector function of an interleukin-2 dependent cytotoxic T cell line. Mol. Cell. Biol. 12:4521-4530.
34. Katagiri, T., M. Ogimoto, K. Hasegawa, Y. Arimura, K. Mitomo, M. Okada, M.R. Clark, K. Mizuno, and H. Yakura. 1999. CD45 negatively regulates Lyn activity by dephosphorylating both positive and negative regulatory tyrosine residues in immature B cells. J. Immunol. 163:1321-1326.
35. Klausner, R.D., and L.E. Samelson. 1991. T cell antigen receptor activation pathways: the tyrosine kinase connection. Cell. 64:875-878.
36. Koegl, M., P. Zlatkine, S.C. Ley, S.A. Courtneidge, and A.I. Magee. 1994. Palmitoylation of multiple Src-family kinases at a homologous N-terminal motif. Biochem. J. 303:749-753.
37. Kolanus, W., C. Romeo, and B. Seed. 1993. T cell activation by clustered tyrosine kinases. Cell. 74:171-183.
38. Koretzky, G.A., J. Picus, M.L. Thomas, and A. Weiss. 1990. Tyrosine phosphatase CD45 is essential for coupling T-cell antigen receptor to the phosphatidylinositol pathway. Nature. 346:66-68.
39. Koretzky, G.A., J. Picus, T. Schultz, and A. Weiss. 1991. Tyrosine phosphatase CD45 is required for T-cell antigen receptor and CD2-mediated activation of a protein tyrosine kinase and interleukin 2 production. Proc. Natl. Acad. Sci. USA. 88:2037-2041.
40. Korty, P.E., C. Brando, and E.M. Shevach. 1991. CD59 functions as a signal-transducing molecule for human T cell activation. J. Immunol. 146:4092-4098.
41. Ledbetter, J.A., N.K. Tonks, E.H. Fischer, and E.A. Clark. 1988. CD45 regulates signal transduction and lymphocyte activation by specific association with receptor molecules on T or B cells. Proc. Natl. Acad. Sci. USA. 85:8628-8632.
42. Ley, S.C., M. Marsh, C.R. Bebbington, K. Proudfoot, and P. Jordan. 1994. Distinct intracellular localization of Lck and Fyn protein tyrosine kinases in human T lymphocytes. J. Cell Biol. 125:639-649.
43. Monks, C.R.F., B.A. Freiberg, H. Kupfer, N. Sciaky, and A. Kupfer. 1998. Three-dimensional segregation of supramolecular activation clusters in T cells. Native. 395:82-86.
44. Montixi, C., C. Langtet, 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.
45. Okamoto, T., A. Schlegel, P.E. Scherer, and M.P. Lisanti. 1998. Caveolins, a family of scaffolding proteins for organising "preassembled signalling complexes" at the plasma membrane. J. Biol. Chem. 273:5419-5422.
46. Ostergaard, H.L., D.A. Shakelford, 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.
47. Parton, R.G. 1994. Ultrastruclural localization of gangliosides: GM1 is concentrated in caveolae. J. Histochem. Cytochem. 42:155-166.
48. Parton, R.G., and K. Simons. 1995. Digging into caveolae. Science. 269:1398-1399.
49. Pingel, J., and M.L. Thomas. 1989. Evidence that the leukocyte-common antigen is required for antigen-induced T lymphocyte proliferation. Cell. 58: 1055-1065.
50. lck associated with glycolipid-enriched membrane domains. J. Cell Biol. 135: 1515-1523.
51. 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.
52. Rothberg, K.G., Y.-S. Ying, B.A. Kamen, and R.G.W. Anderson. 1990. Cholesterol controls the clustering of the glycophospholipid-anchored membrane receptor for 5-methyltetrahydrofolate. J. Cell Biol. 111:2931-2938.
53. Scheiffele, P., M.G. Roth, and K. Simons. 1997. Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO (Eur. Mol. Biol. Organ.) J. 16:5501-5508.
54. Scherer, P.E., R.Y. Lewis, D. Volonte, J.A. Engelman, F. Galbiati, J. Couet, S. Kohtz, E. van Donselaar, P. Peters, and M.P. Lisanti. 1997. Cell-type and tissue-specific expression of caveolin-2. J. Biol. Chem. 272:29337-29346.
55. Schneider, C., R.A. Newman, D.R. Sutherland, U. Asser, and M.F. Greaves. 1982. A one-step purification of membrane proteins using a high efficiency immunomatrix. J. Biol. Chem. 257:10766-10769.
56. Shaw, A.S., and M.L. Dustin. 1997. Making the T cell receptor go the distance: a topological view of T cell activation. Immunity. 6:361-369.
57. Sheets, E.D., D. Holowka, and B. Baird. 1999. Critical role for cholesterol in Lyn-mediated tyrosine phosphorylation of FceRI and their association with detergent-resistant membranes. J. Cell Biol. 145:877-887.
58. Shenoy-Scaria, A.M., D.J. Dietzen, J. Kwong, D.C. Link, and D.M. Lublin. 1994. Cysteine3 of Src family protein tyrosine kinases determines palmitoylation and localization in caveolae. J. Cell Biol. 126:353-363.
59. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature. 387:569-572.
60. Sloan-Lancaster, J., J. Presley, J. Ellenberg, T. Yamazaki, J. Lippincott-Schwartz, and L.E. Samelson. 1998. ZAP-70 association with T cell receptor ζ (TCRζ): fluorescence imaging of dynamic changes upon cellular stimulation. J. Cell Biol. 143:613-624.
61. Stauffer, T.P., and T. Meyer. 1997. Compartmentalized IgE receptor-mediated signal transduction in living cells. J. Cell Biol. 139:1447-1454.
62. 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.
63. Sussman, J.J., T. Saito, E.M. Shevach, R.N. Germain, and J.D. Ashwell. 1988. Thy-1 and Ly-6-mediated lymphokine production and growth inhibition of a T cell hybridoma require co-expression of the T cell antigen receptor complex. J. Immunol. 140:2520-2526.
64. Turka, L.A., S.B. Kanner, G.L. Schieven, C.B. Thompson, and J.A. Ledbelter. 1992. CD45 modulates T cell receptor/CD3-induced activation of human thymocytes via regulation of tyrosine phosphorylation. Eur. J. Immunol. 22: 551-557.
65. Varma, R., and S. Mayor. 1998. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature. 394:798-801.
66. Verweij, C.L., C. Guidos, and G.R. Crabtree. 1990. Cell type specificity and activation requirements for NFAT1 (nuclear factor of activated T cells) transcriptional activity determined by a new method using transgenic mice to assay transcriptional activity of an activated nuclear factor. J. Biol. Chem. 265: 15788-15795.
67. Viola, A., S. Schroeder, Y. Sakakibara, and A. Lanzavecchia. 1999. T lymphocyte costimulation mediated by reorganisation of membrane microdomains. Science. 283:680-682.
68. Weiss, A. 1993. T cell antigen receptor signal transduction: a tale of tails and cytoplasmic protein-tyrosine kinases. Cell. 73:209-212.
69. 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.
70. Weiss, A., and D.R. Littman. 1994. Signal transduction by lymphocyte antigen receptors. Cell. 76:263-274.
71. 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 ZAP-70-deficient Jurkat T cell line. Mol. Cell. Biol. 18:1388-1399.
72. Wulfing, C., and M.M. Davis. 1998. A receptor/cytoskeletal movement triggered by costimulation during T cell activation. Science. 282:2266-2269.
73. Xavier, R., T. Brennan, Q. Li, C. McCormack, and B. Seed. 1998. Membrane compartmentation is required for efficient T cell activation. Immunity. 8:723-732.
74. Zhang, W., R.P. Trible, and L.E. Samelson. 1998a. LAT palmitoylation: its essential role in membrane microdomain targeting and tyrosine phosphorylation during T cell activation. Immunity. 9:239-246.
75. Zhang, W., J. Sloan-Lancaster, J. Kitchen, R.P. Trible, and L.E. Samelson. 1998b. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell. 92:83-92.