The role of membrane rafts in Lck transport, regulation and signalling in T-cells

Biochemical Journal

Volumn 454, Issue 2, 2013, Pages 169-179

  Ventimiglia, Leandro N ^a   Alonso, Miguel A ^a  

^a CSIC   (Spain)

Author keywords

Lck; Membrane raft; T cells; Tyrosine kinase; Tyrosine phosphatase

Indexed keywords

PROTEIN KINASE LCK; PROTEIN SH2; PROTEIN SH3; T LYMPHOCYTE RECEPTOR;

CELL MEMBRANE; DEPHOSPHORYLATION; ENZYME ACTIVE SITE; HUMAN; LIPID RAFT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGEN PRESENTATION; CELL MEMBRANE; HUMANS; LYMPHOCYTE ACTIVATION; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MEMBRANE MICRODOMAINS; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84881529180     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20130468     Document Type: Review

References (147)

1. Hunter, T. (2009) Tyrosine phosphorylation: thirty years and counting. Curr. Opin. Cell Biol. 21, 140-146
2. Martin, G. S. (2001) The hunting of the Src. Nat. Rev. Mol. Cell Biol. 2, 467-475
3. Casnellie, J. E., Harrison, M. L., Hellstrom, K. E. and Krebs, E. G. (1982) A lymphoma protein with an in vitro site of tyrosine phosphorylation homologous to that in pp60src. J. Biol. Chem. 257, 13877-13879
4. Casnellie, J. E., Harrison, M. L., Hellstrom, K. E. and Krebs, E. G. (1983) A lymphoma cell line expressing elevated levels of tyrosine protein kinase activity. J. Biol. Chem. 258, 10738-10742
5. Marth, J. D., Peet, R., Krebs, E. G. and Perlmutter, R. M. (1985) A lymphocyte-specific protein-tyrosine kinase gene is rearranged and overexpressed in the murine T cell lymphoma LSTRA. Cell 43, 393-404
6. Samelson, L. E., Harford, J., Schwartz, R. H. and Klausner, R. D. (1985) A 20-kDa protein associated with the murine T-cell antigen receptor is phosphorylated in response to activation by antigen or concanavalin A. Proc. Natl. Acad. Sci. U.S.A. 82, 1969-1973
7. Rudd, C. E., Anderson, P., Morimoto, C., Streuli, M. and Schlossman, S. F. (1989) Molecular interactions, T-cell subsets and a role of the CD4/CD8:p56lck complex in human T-cell activation. Immunol. Rev. 111, 225-266
8. Abraham, N., Miceli, M. C., Parnes, J. R. and Veillette, A. (1991) Enhancement of T-cell responsiveness by the lymphocyte-specific tyrosine protein kinase p56lck. Nature 350, 62-66
9. Abraham, R. T. and Weiss, A. (2004) Jurkat T cells and development of the T-cell receptor signaling paradigm. Nat. Rev. Immunol. 4, 301-308
10. Goldsmith, M. A. and Weiss, A. (1987) Isolation and characterization of a T-lymphocyte somatic mutant with altered signal transduction by the antigen receptor. Proc. Natl. Acad. Sci. U.S.A. 84, 6879-6883
11. Straus, D. B. and Weiss, A. (1992) Genetic evidence for the involvement of the lck tyrosine kinase in signal transduction through the T cell antigen receptor. Cell 70, 585-593
12. Molina, T. J., Kishihara, K., Siderovskid, D. P., van Ewijk, W., Narendran, A., Timms, E., Wakeham, A., Paige, C. J., Hartmann, K. U., Veillette, A. et al. (1992) Profound block in thymocyte development in mice lacking p56lck. Nature 357, 161-164
13. Goldman, F. D., Ballas, Z. K., Schutte, B. C., Kemp, J., Hollenback, C., Noraz, N. and Taylor, N. (1998) Defective expression of p56lck in an infant with severe combined immunodeficiency. J. Clin. Invest. 102, 421-429
14. Sicheri, F. and Kuriyan, J. (1997) Structures of Src-family tyrosine kinases. Curr. Opin. Struct. Biol. 7, 777-785
15. Bolen, J. B. (1993) Nonreceptor tyrosine kinases. Oncogene 8, 2025-2031
16. Resh, M. D. (1994) Myristylation and palmitylation of Src family members: the fats of the matter. Cell 76, 411-413
17. Paige, L. A., Nadler, M. J., Harrison, M. L., Cassady, J. M. and Geahlen, R. L. (1993) Reversible palmitoylation of the protein-tyrosine kinase p56lck. J. Biol. Chem. 268, 8669-8674
18. Kwong, J. and Lublin, D. M. (1995) Amino-terminal palmitate or polybasic domain can provide required second signal to myristate for membrane binding of p56lck. Biochem. Biophys. Res. Commun. 207, 868-876
19. Yasuda, K., Kosugi, A., Hayashi, F., Saitoh, S.-i., Nagafuku, M., Mori, Y., Ogata, M. and Hamaoka, T. (2000) Serine 6 of Lck tyrosine kinase: a critical site for Lck myristoylation, membrane localization, and function in T lymphocytes. J. Immunol. 165, 3226-3231
20. Veillette, A., Bookman, M. A., Horak, E. M. and Bolen, J. B. (1988) The CD4 and CD8 T cell surface antigens are associated with the internal membrane tyrosine-protein kinase p56lck. Cell 55, 301-308
21. Shaw, A. S., Amrein, K. E., Hammond, C., Stern, D. F., Sefton, B. M. and Rose, J. K. (1989) The Lck tyrosine protein kinase interacts with the cytoplasmic tail of the CD4 glycoprotein through its unique amino-terminal domain. Cell 59, 627-636
22. Rudd, C. E., Trevillyan, J. M., Dasgupta, J. D., Wong, L. L. and Schlossman, S. F. (1988) The CD4 receptor is complexed in detergent lysates to a protein-tyrosine kinase (pp58) from human T lymphocytes. Proc. Natl. Acad. Sci. U.S.A. 85, 5190-5194
23. Kim, P. W., Sun, Z.-Y. J., Blacklow, S. C., Wagner, G. and Eck, M. (2003) A zinc clasp structure tethers Lck to T cell coreceptors CD4 and CD8. Science 301, 1725-1728
24. Sicheri, F., Moarefi, I. and Kuriyan, J. (1997) Crystal structure of the Src family tyrosine kinase Hck. Nature 385, 602-609
25. Xu, W., Harrison, S. C. and Eck, M. J. (1997) Three-dimensional structure of the tyrosine kinase c-Src. Nature 385, 595-602
26. Moarefi, I., LaFevre-Bernt, M., Sicheri, F., Huse, M., Lee, C.-H., Kuriyan, J. and Miller, W. T. (1997) Activation of the Src-family tyrosine kinase Hck by SH3 domain displacement. Nature 385, 650-653
27. Hubbard, S. R. and Till, J. H. (2000) Protein tyrosine kinase structure and function. Annu. Rev. Biochem. 69, 373-398
28. Simons, K. and Ikonen, E. (1997) Functional rafts in cell membranes. Nature 387, 569-572
29. Brown, D. A. and London, E. (1998) Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14, 111-136
30. Lingwood, D. and Simons, K. (2010) Lipid rafts as a membrane-organizing principle. Science 327, 46-50
31. Gaus, K., Gratton, E., Kable, E. P. W., Jones, A. S., Gelissen, I., Kritharides, L. and Jessup, W. (2003) Visualizing lipid structure and raft domains in living cells with two-photon microscopy. Proc. Natl. Acad. Sci. U.S.A. 100, 15554-15559
32. Brown, D. A. and Rose, J. K. (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533-544
33. Simons, K. and Gerl, M. J. (2010) Revitalizing membrane rafts: new tools and insights. Nat. Rev. Mol. Cell Biol. 11, 688-699
34. Simons, K. and Toomre, D. (2000) Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-39
35. Cao, X., Surma, M. A. and Simons, K. (2012) Polarized sorting and trafficking in epithelial cells. Cell Res. 22, 793-805
36. Shaw, A. S. (2006) Lipid rafts: now you see them, now you don't. Nat. Immunol. 7, 1139-1142
37. Munro, S. (2003) Lipid rafts: elusive or illusive? Cell 115, 377-388
38. Pike, L. J. (2006) Rafts defined: a report on the Keystone symposium on lipid rafts and cell function. J. Lipid Res. 47, 1597-1598
39. Hoessli, D. C. and Rungger-Brändle, E. (1983) Isolation of plasma membrane domains from murine T lymphocytes. Proc. Natl. Acad. Sci. U.S.A. 80, 439-443
40. Stefanová, I., Horejsí, V., Ansotegui, I. J., Knapp, W. and Stockinger, H. (1991) GPI-anchored cell surface molecules complexed to tyrosine kinases. Science 254, 1016-1019
41. Montixi, C., Langlet, C., Bernard, A.-M., Thimonier, J., Dubois, C., Wurbel, M.-A., Chauvin, J.-P., Pierres, M. and He, H.-T. (1998) Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J. 17, 5334-5348
42. Xavier, R., Brennan, T., Li, Q., McCormack, C. and Seed, B. (1998) Membrane compartmentation is required for efficient T cell activation. Immunity 8, 723-732
43. Zhang, W., Trible, R. P. and Samelson, L. E. (1998) LAT palmitoylation: its essential role in membrane microdomain targeting and tyrosine phosphorylation during T cell activation. Immunity 9, 239-246
44. Huppa, J. B. and Davis, M. M. (2003) T-cell-antigen recognition and the immunological synapse. Nat. Rev. Immunol. 3, 973-983
45. Fooksman, D. R., Vardhana, S., Vasiliver-Shamis, G., Liese, J., Blair, D. A., Waite, J., Sacristan, C., Victora, G. D., Zanin-Zhorov, A. and Dustin, M. L. (2010) Functional anatomy of T cell activation and synapse formation. Annu. Rev. Immunol. 28, 79-105
46. Burack, W. R., Lee, K.-H., Holdorf, A. D., Dustin, M. L. and Shaw, A. S. (2002) Quantitative imaging of raft accumulation in the immunological synapse. J. Immunol. 169, 2837-2841
47. Gaus, K., Chklovskaia, E., Fazekas de St. Groth, B., Jessup, W. and Harder, T. (2005) Condensation of the plasma membrane at the site of T lymphocyte activation. J. Cell Biol. 171, 121-131
48. Zech, T., Ejsing, C. S., Gaus, K., de Wet, B., Shevchenko, A., Simons, K. and Harder, T. (2009) Accumulation of raft lipids in T-cell plasma membrane domains engaged in TCR signaling. EMBO J. 28, 466-476
49. Douglass, A. D. and Vale, R. D. (2005) Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell 121, 937-950
50. Millán, J. and Alonso, M. A. (1998) MAL, a novel integral membrane protein of human T lymphocytes, associates with glycosylphosphatidylinositol- anchored proteins and Src-like tyrosine kinases. Eur. J. Immunol. 28, 3675-3684
51. Zlatkine, P., Mehul, B. and Magee, A. I. (1997) Retargeting of cytosolic proteins to the plasma membrane by the Lck protein tyrosine kinase dual acylation motif. J. Cell Sci. 110, 673-679
52. Chichili, G. R. and Rodgers, W. (2007) Clustering of membrane raft proteins by the actin cytoskeleton. J. Biol. Chem. 282, 36682-36691
53. Rodgers, W., Crise, B. and Rose, J. K. (1994) Signals determining protein tyrosine kinase and glycosyl-phosphatidylinositol-anchored protein targeting to a glycolipid-enriched membrane fraction. Mol. Cell. Biol. 14, 5384-5391
54. Shenoy-Scaria, A. M., Gauen, L. K., Kwong, J., Shaw, A. S. and Lublin, D. M. (1993) Palmitylation of an amino-terminal cysteine motif of protein tyrosine kinases p56lck and p59fyn mediates interaction with glycosyl- phosphatidylinositol-anchored proteins. Mol. Cell. Biol. 13, 6385-6392
55. Kabouridis, P. S., Magee, A. I. and Ley, S. C. (1997) S-acylation of LCK protein tyrosine kinase is essential for its signaling function in T lymphocytes. EMBO J. 16, 4983-4998
56. Kosugi, A., Hayashi, F., Liddicoat, D. R., Yasuda, K., Saitoh, S.-i. and Hamaoka, T. (2001) A pivotal role of cysteine 3 of Lck tyrosine kinase for localization to glycolipid-enriched microdomains and T cell activation. Immunol. Lett. 76, 133-138
57. Yurchak, L. K. and Sefton, B. M. (1995) Palmitoylation of either Cys-3 or Cys-5 is required for the biological activity of the Lck tyrosine protein kinase. Mol. Cell. Biol. 15, 6914-6922
58. Hawash, I. Y., Kesavan, K. P., Magee, A. I., Geahlen, R. L. and Harrison, M. L. (2002) The Lck SH3 domain negatively regulates localization to lipid rafts through an interaction with c-Cbl. J. Biol. Chem. 277, 5683-5691
59. Nadler, M. J., Harrison, M. L., Ashendel, C. L., Cassady, J. M. and Geahlen, R. L. (1993) Treatment of T cells with 2-hydroxymyristic acid inhibits the myristoylation and alters the stability of p56lck. Biochemistry 33, 9250-9255
60. Hawash, I. Y., Hu, X. E., Adal, A., Cassady, J. M., Geahlen, R. L. and Harrison, M. L. (2002) The oxygen-substituted palmitic acid analogue, 13-oxypalmitic acid, inhibits Lck localization to lipid rafts and T cell signaling. Biochim. Biophys. Acta 1589, 140-150
61. Janes, P. W., Ley, S. C. and Magee, A. I. (1999) Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J. Cell Biol. 147, 447-461
62. Rossy, J., Owen, D. M., Williamson, D. J., Yang, Z. and Gaus, K. (2013) Conformational states of the kinase Lck regulate clustering in early T cell signaling. Nat. Immunol. 14, 82-89
63. Ley, S. C., Marsh, M., Bebbington, C. R., Proudfoot, K. and Jordan, P. (1994) Distinct intracellular localization of Lck and Fyn protein tyrosine kinases in human T lymphocytes. J. Cell Biol. 125, 639-649
64. Bijlmakers, M.-J. J. E., Isobe-Nakamura, M., Ruddock, L. J. and Marsh, M. (1997) Intrinsic signals in the unique domain target p56lck to the plasma membrane independently of CD4. J. Cell Biol. 137, 1029-1040
65. Bijlmakers, M.-J. J. E. and Marsh, M. (1999) Trafficking of an acylated cytosolic protein: newly synthesized p56lck travels to the plasma membrane via the exocytic pathway. J. Cell Biol. 145, 457-468
66. Alonso, M. A. and Weissman, S. M. (1987) cDNA cloning and sequence of MAL, a hydrophobic protein associated with human T-cell differentiation. Proc. Natl. Acad. Sci. U.S.A. 84, 1997-2001
67. Puertollano, R., Martin-Belmonte, F., Millan, J., de Marco, M. C., Albar, J. P., Kremer, L. and Alonso, M. A. (1999) The MAL proteolipid is necessary for normal apical transport and accurate sorting of the influenza virus hemagglutinin in Madin-Darby canine kidney cells. J. Cell Biol. 145, 141-151
68. Schaeren-Wiemers, N., Schaefer, C., Valenzuela, D. M., Yancopoulos, G. D. and Schwab, M. E. (1995) Identification of new oligodendrocyte- and melin-specific genes by a differential screening approach. J. Neurochem. 65, 10-22
69. Kim, T., Fiedler, K., Madison, D. L., Krueger, W. H. and Pfeiffer, S. E. (1995) Cloning and characterization of MVP17: a developmentally regulated myelin protein in oligodendrocytes. J. Neurosci. Res. 42, 413-422
70. Cheong, K. H., Zacchetti, D., Schneeberger, E. E. and Simons, K. (1999) VIP17/MAL, a lipid raft-associated protein, is involved in apical transport in MDCK cells. Proc. Natl. Acad. Sci. U.S.A. 96, 6241-6248
71. Martin-Belmonte, F., Arvan, P. and Alonso, M. A. (2001) MAL mediates apical transport of secretory proteins in polarized epithelial Madin-Darby canine kidney cells. J. Biol. Chem. 276, 49337-49342
72. Anton, O., Batista, A., Millan, J., Andres-Delgado, L., Puertollano, R., Correas, I. and Alonso, M. A. (2008) An essential role for the MAL protein in targeting Lck to the plasma membrane of human T lymphocytes. J. Exp. Med. 205, 3201-3213
73. Anton, O. M., Andres-Delgado, L., Reglero-Real, N., Batista, A. and Alonso, M. A. (2011) MAL protein controls protein sorting at the supramolecular activation cluster of human T lymphocytes. J. Immunol. 186, 6345-6356
74. Andres-Delgado, L., Anton, O. M., Madrid, R., Byrne, J. A. and Alonso, M. A. (2010) Formin INF2 regulates MAL-mediated transport of Lck to the plasma membrane of human T lymphocytes. Blood 116, 5919-5929
75. Gaillard, J., Ramabhadran, V., Neumanne, E., Gurel, P., Blanchoin, L., Vantard, M. and Higgs, H. N. (2011) Differential interactions of the formins INF2, mDia1, and mDia2 with microtubules. Mol. Biol. Cell 22, 4575-4587
76. Andrés-Delgado, L., Antón, O. M., Bartolini, F., Ruiz-Sáenz, A., Correas, I., Gundersen, G. G. and Alonso, M. A. (2012) INF2 promotes the formation of detyrosinated microtubules necessary for centrosome reorientation in T cells. J. Cell Biol. 198, 1025-1037
77. Magal, L. G., Yaffe, Y., Shepshelovich, J., Aranda, J. F., de Marco, M. d. C., Gaus, K., Alonso, M. A. and Hirschberg, K. (2009) Clustering and lateral concentration of raft lipids by the MAL protein. Mol. Biol. Cell 20, 3751-3762
78. Cen, O., Gorska, M. M., Stafford, S. J., Sur, S. and Alam, R. (2003) Identification of UNC119 as a novel activator of SRC-type tyrosine kinases. J. Biol. Chem. 278, 8837-8845
79. Gorska, M. M., Liang, Q., Karim, Z. and Alam, R. (2009) Uncoordinated 119 protein controls trafficking of Lck via the Rab11 endosome and is critical for immunological synapse formation. J. Immunol. 183, 1675-1684
80. Zhang, H., Constantine, R., Vorobiev, S., Chen, Y., Seetharaman, J., Huang, Y. J., Xiao, R., Montelione, G. T., Gerstner, C. D., Davis, M. W. et al. (2011) UNC119 is required for G protein trafficking in sensory neurons. Nat. Neurosci. 14, 874-880
81. Wright, K. J., Baye, L. M., Olivier-Mason, A., Mukhopadhyay, S., Sang, L., Kwong, M., Wang, W., Pretorius, P. R., Sheffield, V. C., Sengupta, P. et al. (2011) An ARL3-UNC119-RP2 GTPase cycle targets myristoylated NPHP3 to the primary cilium. Genes Dev. 25, 2347-2360
82. Monks, C. R. F., Freiberg, B. A., Kupfer, H., Sciaky, N. and Kupfer, A. (1998) Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395, 82-86
83. Ehrlich, L. I. R., Ebert, P. J. R., Krummel, M. F., Weiss, A. and Davis, M. M. (2002) Dynamics of p56lck translocation to the T cell immunological synapse following agonist and antagonist stimulation. Immunity 17, 809-822
84. Okada, M., Nada, S., Yamanashi, Y., Yamamoto, T. and Nakagawa, H. (1991) CSK: a protein-tyrosine kinase involved in regulation of src family kinases. J. Biol. Chem. 266, 24249-24252
85. Bergman, M., Mustelin, T., Oetken, C., Partanen, J., Flint, N. A., Amrein, K. E., Autero, M., Burn, P. and Alitalo, K. (1992) The human p50csk tyrosine kinase phosphorylates p56lck at Tyr-505 and down regulates its catalytic activity. EMBO J. 11, 2919-2924
86. Partanen, J., Amsgrong, E., Bergman, M., Mäkelä, T. P., Hirvonen, H., Huebner, K. and Alitalo, K. (1991) Cyl encodes a putative cytoplasmic tyrosine kinase lacking the conserved tyrosine authophosphorylation site (Y416src). Oncogene 6, 2013-2018
87. Chow, L. M. L. and Veillette, A. (1995) The Src and Csk families of tyrosine protein kinases in hemopoietic cells. Semin. Immunol. 7, 207-226
88. Horejsi, V., Zhang, W. and Schraven, B. (2004) Transmembrane adaptor proteins: organizers of immunoreceptor signalling. Nat. Rev. Immunol. 4, 603-616
89. Brdicka, T., Pavlistová, D., Leo, A., Bruyns, E., Korínek, V., Angelisová, P., Scherer, J., Shevchenko, A., Shevchenko, A., Hilgert, I. et al. (2000) 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. J. Exp. Med. 191, 1591-1604
90. Yasuda, K., Nagafuku, M., Shima, T., Okada, M., Yagi, T., Yamada, T., Minaki, Y., Kato, A., Tani-ichi, S., Hamaoka, T. and Kosugi, A. (2002) Fyn is essential for tyrosine phosphorylation of Csk-binding protein/phosphoprotein associated with glycolipid-enriched microdomains in lipid rafts in resting T cells. J. Immunol. 169, 2813-2817
91. Davidson, D., Bakinowski, M., Thomas, M. L., Horejsi, V. and Veillette, A. (2003) Phosphorylation-dependent regulation of T-cell activation by PAG/Cbp, a lipid raft-associated transmembrane adaptor. Mol. Cell. Biol. 23, 2017-2028
92. Torgersen, K. M., Vang, T., Abrahamsen, H., Yaqub, S., Horejsi, V., Schraven, B., Rolstad, B., Mustelin, T. and Taskén, K. (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
93. Posevitz-Fejfár, A., Smída, M., Kliche, S., Hartig, R., Schraven, B. and Lindquist, J. A. (2008) A displaced PAG enhances proximal signaling and SDF-1-induced T cell migration. Eur. J. Immunol. 38, 250-259
94. Zhang, S. Q., Yang, W., Kontaridis, M. I., Bivona, T. G., Wen, G., Araki, T., Luo, J., Thompson, J. A., Schraven, B. L., Philips, M. R. and Neel, B. G. (2004) SHP2 regulates Src family kinase activity and Ras/Erk activation by controlling Csk recruitment. Mol. Cell 13, 341-355
95. Brdickova, N., Brdicka, T., Angelisová, P., Horváth, O., Spicka, J., Hilgert, I., Paces, J., Simeoni, L., Kliche, S., Merten, C. et al. (2003) LIME: a new membrane raft-associated adaptor protein involved in CD4 and CD8 coreceptor signaling. J. Exp. Med. 198, 1453-1462
96. Hur, E. M., Son, M., Lee, O.-H., Choi, Y. B., Park, C., Lee, H. and Yun, Y. (2003) LIME, a novel transmembrane adaptor protein, associates with p56lck and mediates T cell activation. J. Exp. Med. 198, 1463-1473
97. Otáhal, P., Pata, S., Angelisová, P., Horejsí, V. and Brdicka, T. (2011) The effects of membrane compartmentalization of csk on TCR signaling. Biochim. Biophys. Acta 1813, 367-376
98. Dobenecker, M.-W., Schmedt, C., Okada, M. and Tarakhovsky, A. (2005) The ubiquitously expressed Csk adaptor protein Cbp is dispensable for embryogenesis and T-cell development and function. Mol. Cell. Biol. 25, 10533-10542
99. Xu, S., Huo, J., Tan, J. E.-L. and Lam, K.-P. (2005) Cbp deficiency alters Csk localization in lipid rafts but does not affect T-cell development. Mol. Cell. Biol. 25, 8486-8495
100. Saito, K., Enya, K., Oneyama, C., Hikita, T. and Okada, M. (2008) Proteomic identification of ZO-1/2 as a novel scaffold for Src/Csk regulatory circuit. Biochem. Biophys. Res. Commun. 366, 969-975
101. Wang, B., Lemay, S., Tsai, S. and Veillette, A. (2001) SH2 domain-mediated interaction of inhibitory protein tyrosine kinase Csk with protein tyrosine phosphatase-HSCF. Mol. Cell. Biol. 21, 1077-1088
102. Vang, T., Torgersen, K. M., Sundvold, V., Saxena, M., Levy, F. O., Skalhegg, B. S., Hansson, V., Mustelin, T. and Taskén, K. (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, 497-508
103. Tasken, K. and Ruppelt, A. (2006) Negative regulation of T-cell receptor activation by the cAMP-PKA-Csk signaling pathway in T-cell lipid rafts. Front. Biosci. 11, 2929-2939
104. Hermiston, M. L., Xu, Z. and Weiss, A. (2003) CD45: a critical regulator of signaling thresholds in immune cells. Annu. Rev. Immunol. 21, 107-137
105. Ng, D. H. W., Watts, J. D., Aebersold, R. and Johnson, P. (1996) Demonstration of a direct interaction between p56 and the cytoplasmic domain of CD45 in vitro. J. Biol. Chem. 271, 1295-1300
106. Veillette, A., Caron, L., Fournel, M. and Pawson, T. (1992) Regulation of the enzymatic function of the lymphocyte-specific tyrosine protein kinase p56lck by the non-catalytic SH2 and SH3 domains. J. Immunol. 7, 971-980
107. Seavitt, J. R., White, L. S., Murphy, K. M., Loh, D. Y., Perlmutter, R. M. and Thomas, M. L. (1999) Expression of the p56 lck Y505F mutation in CD45-deficient mice rescues thymocyte development. Mol. Cell. Biol. 19, 4200-4208
108. Pingel, S., Baker, M., Turner, M., Holmes, N. and Alexander, D. R. (1999) The CD45 tyrosine phosphatase regulates CD3-induced signal transduction and T cell development in recombinase-deficient mice: restoration of pre-TCR function by active p56lck. Eur. J. Immunol. 29, 2376-2384
109. Burns, C. M., Sakaguchi, K., Appella, E. and Ashwell, J. D. (1994) CD45 regulation of tyrosine phosphorylation and enzyme activity of src family kinases. J. Biol. Chem. 269, 13594-13600
110. D'Oro, U. and Ashwell, J. D. (1999) The CD45 tyrosine phosphatase is an inhibitor of Lck activity in thymocytes. J. Immunol. 162, 1879-1883
111. McNeill, L., Salmond, R. J., Cooper, J. C., Carret, C. l. K., Cassady-Cain, R. L., Roche-Molina, M., Tandon, P., Holmes, N. and Alexander, D. R. (2007) The differential regulation of Lck kinase phosphorylation sites by CD45 is critical for T cell receptor signaling responses. Immunity 27, 425-437
112. Rodgers, W. and Rose, J. K. (1996) Exclusion of CD45 inhibits activity of p56lck associated with glycolipid-enriched membrane domains. J. Cell Biol. 135, 1515-1523
113. Edmonds, S. D. and Ostergaard, H. L. (2002) Dynamic association of CD45 with detergent-insoluble microdomains in T lymphocytes. J. Immunol. 169, 5036-5042
114. Irles, C., Symons, A., Michel, M., Bakker, T. R., van der Merwe, P. A. and Acuto, O. (2003) CD45 ectodomain controls interaction with GEMs and Lck activity for optimal TCR signaling. Nat. Immunol. 4, 189-197
115. Davis, S. J. and van der Merwe, P. A. (2006) The kinetic-segregation model: TCR triggering and beyond. Nat. Immunol. 7, 803-809
116. Davis, S. J. and van der Merwe, P. A. (2011) Lck and the nature of the T cell receptor trigger. Trends Immunol. 32, 1-5
117. Zhang, M., Moran, M., Round, J., Low, T. A., Patel, V. P., Tomassian, T., Hernandez, J. D. and Miceli, M. C. (2005) CD45 signals outside of lipid rafts to promote ERK activation, synaptic raft clustering, and IL-2 production. J. Immunol. 174, 1479-1490
118. Jury, E. C., Kabouridis, P. S., Flores-Borja, F., Mageed, R. A. and Isenberg, D. A. (2004) Altered lipid raft-associated signaling and ganglioside expression in T lymphocytes from patients with systemic lupus erythematosus. J. Clin. Invest. 113, 1176-1187
119. Jury, E. C., Kabouridis, P. S., Abba, A., Mageed, R. A. and Isenberg, D. A. (2003) Increased ubiquitination and reduced expression of LCK in T lymphocytes from patients with systemic lupus erythematosus. Arthritis Rheum. 48, 1343-1354
120. Matache, C., Stefanescu, M., Onu, A., Tanaseanu, S., Matei, I., Frade, R. and Szegli, G. (1999) p56lck activity and expression in peripheral blood lymphocytes from patients with systemic lupus eryhtematosus. Autoimmunity 29, 111-120
121. Blasini, A. M., Brundula, V., Paris, M., Rivas, L., Salazar, S., Stekman, I. L. and Rodriguez, M. A. (1998) Protein tyrosine kinase activity in T lymphocytes from patients with systemic lupus erythematosus. J. Autoimmun. 11, 387-393
122. Vratsanos, G. S., Jung, S., Park, Y.-M. and Craft, J. (2001) Cd4+ T cells from lupus-prone mice are hyperresponsive to T cell receptor engagement with low and high affinity peptide antigens. J. Exp. Med. 193, 329-338
123. Jury, E. C., Isenberg, D. A., Mauri, C. and Ehrenstein, M. R. (2006) Atorvastatin restores Lck expression and lipid raft-associated signaling in T cells from patients with systemic lupus erythematosus. J. Immunol. 177, 7416-7422
124. Jury, E. C., Flores-Borja, F. and Kabouridis, P. S. (2007) Lipid rafts in T cell signaling and disease. Semin. Cell Dev. Biol. 18, 608-615
125. Gjörloff-Wingren, A., Saxena, M., Williams, S., Hammi, D. and Mustelin, T. (1999) Characterization of TCR-induced receptor-proximal signaling events negatively regulated by the protein tyrosine phosphatase PEP. Eur. J. Immunol. 29, 3845-3854
126. Kosugi, A., Sakakura, J., Yasuda, K., Ogata, M. and Hamaoka, T. (2001) Involvement of SHP-1 tyrosine phosphatase in TCR-mediated signaling pathways in lipid rafts. Immunity 14, 669-680
127. Chiang, G. G. and Sefton, B. M. (2001) Specific dephosphorylation of the Lck tyrosine protein kinase at Tyr-394 by the SHP-1 protein-tyrosine phosphatase. J. Biol. Chem. 276, 23173-23178
128. Tiganis, T. and Bennett, A. M. (2007) Protein tyrosine phosphatase function: the substrate perspective. Biochem. J. 402, 1-15
129. Rhee, I. and Veillette, A. (2012) Protein tyrosine phosphatases in lymphocyte activation and autoimmunity. Nat. Immunol. 13, 439-447
130. Su, M. W.-C., Yu, C.-L., Burakoff, S. J. and Jin, Y.-J. (2001) Targeting Src homology 2 domain-containing tyrosine phosphatase (SHP-1) into lipid rafts inhibits CD3-induced T cell activation. J. Immunol. 166, 3975-3982
131. Cloutier, J.-F. and Veillette, A. (1999) Cooperative inhibition of T-cell antigen receptor signaling by a complex between a kinase and a phosphatase. J. Exp. Med. 189, 111-121
132. Hasegawa, K., Martin, F., Huang, G., Tumas, D., Diehl, L. and Chan, A. C. (2004) PEST domain-enriched tyrosine phosphatase (PEP) regulation of effector/memory T cells. Science 303, 685-689
133. Lorenz, U. (2009) SHP-1 and SHP-2 in T cells: two phosphatases functioning at many levels. Immunol. Rev. 228, 342-359
134. Fawcett, V. C. J. and Lorenz, U. (2005) Localization of Src homology 2 domain-containing phosphatase 1 (SHP-1) to lipid rafts in T lymphocytes: functional implications and a role for the SHP-1 carboxyl terminus. J. Immunol. 174, 2849-2859
135. Sankarshanan, M., Ma, Z., Iype, T. and Lorenz, U. (2007) Identification of a novel lipid raft-targeting motif in Src homology 2-containing phosphatase 1. J. Immunol. 179, 483-490
136. Methi, T., Ngai, J., Mahic, M., Amarzguioui, M., Vang, T. and Tasken, K. (2005) Short-interfering RNA-mediated Lck knockdown results in augmented downstream T cell responses. J. Immunol. 175, 7398-7406
137. Stefanova, I., Hemmer, B., Vergelli, M., Martin, R., Biddison, W. E. and Germain, R. N. (2003) TCR ligand discrimination is enforced by competing ERK positive and SHP-1 negative feedback pathways. Nat. Immunol. 4, 248-254
138. Nika, K., Soldani, C., Salek, M., Paster, W., Gray, A., Etzensperger, R., Fugger, L., Polzella, P., Cerundolo, V., Dushek, O. et al. (2010) Constitutively active Lck kinase in T cells drives antigen receptor signal transduction. Immunity 32, 766-777
139. Irles, C., Arias-Martinez, J., Guzmán-Bárcenas, J. and Ortega, A. (2010) Plasma membrane subdomain partitioning of Lck in primary human T lymphocytes. Can. J. Physiol. Pharmacol. 88, 487-496
140. Kabouridis, P. S. (2003) Selective interaction of LAT (linker of activated T cells) with the open-active form of Lck in lipid rafts reveals a new mechnanism for the regulation of Lck in T-cells. Biochem. J. 371, 907-915
141. Ballek, O., Brouckova, A., Manning, J. and Filipp, D. (2012) A specific type of membrane microdomains is involved in the maintenance and translocation of kinase active Lck to lipid rafts. Immunol. Lett. 142, 64-74
142. Rossy, J., Williamson, D. J. and Gaus, K. (2012) How does the kinase Lck phosphorylates the T cell receptor? Spatial organization as a regulatory mechanism. Front. Immunol. 3, 167
143. Gil, D., Schamel, W. W. A., Montoya, M., Sánchez-Madrid, F. and Alarcón, B. (2002) Recruitment of Nck by CD3ε reveals a ligand-induced conformational change essential for T cell receptor signaling and synapse formation. Cell 109, 901-912
144. Stirnweiss, A., Hartig, R., Gieseler, S., Lindquist, J. A., Reichardt, P., Philipsen, L., Simeoni, L., Poltorak, M., Merten, C., Zuschratter, W. et al. (2013) T cell activation results in conformational changes in the Src family kinase Lck to induce its activation. Sci. Signaling 6, ra13
145. Filipp, D., Ballek, O. and Manning, J. (2012) Lck, membrane microdomains and TCR triggering machinery: defining the new rules of engagement. Front. Immunol. 3, 155
146. Chichili, G. R., Westmuckett, A. D. and Rodgers, W. (2010) T cell signal regulation by the actin cytoskeleton. J. Biol. Chem. 285, 14737-14746
147. Chichili, G. R., Cail, R. C. and Rodgers, W. (2012) Cytoskeletal modulation of lipid interactions regulates Lck kinase activity. J. Biol. Chem. 287, 24186-24194