Plasma membrane subdomain partitioning of Lck in primary human T lymphocytes

Canadian Journal of Physiology and Pharmacology

Volumn 88, Issue 4, 2010, Pages 487-496

  Irles, Claudine ^a   Arias Martinez, Joel ^a   Guzmán Bárcenas, José ^a   Ortega, Alicia ^a,b  

^a INSTITUTO NACIONAL DE PERINATOLOGÍA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Coreceptor CD4; Human; Leukocyte specific protein tyrosine kinase; Lipid raft; Protein kinases; Protein phosphatases; T cell receptor

Indexed keywords

PROTEIN KINASE LCK; PROTEIN TYROSINE KINASE; T LYMPHOCYTE RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR;

ARTICLE; CD4+ T LYMPHOCYTE; CELL MEMBRANE; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; LIPID RAFT; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; T LYMPHOCYTE; ENZYMOLOGY; IMMUNOLOGY; IMMUNOPRECIPITATION; METABOLISM; PHOSPHORYLATION;

CELL MEMBRANE; HUMANS; IMMUNOPRECIPITATION; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MEMBRANE MICRODOMAINS; PHOSPHORYLATION; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES;

EID: 77952084426     PISSN: 00084212     EISSN: None     Source Type: Journal    
DOI: 10.1139/Y09-125     Document Type: Article

References (48)

1. Alexander, D.R. 2000. The CD45 tyrosine phosphatase: a positive and negative regulator of immune cell function. Semin. Immunol. 12(4): 349-359. doi:10.1006/smim.2000.0218. PMID: 10995582.
2. Bergman, M., Mustelin, T., Oetken, C., Partanen, J., Flint, N.A., Amrein, K.E., et al. 1992. The human p50csk tyrosine kinase phosphorylates p56lck at Tyr-505 and down regulates its catalytic activity. EMBO J. 11(8): 2919-2924. PMID:1639064.
3. Boggon, T.J., and Eck, M.J. 2004. Structure and regulation of Src family kinases. Oncogene, 23(48): 7918-7927. doi:10.1038/sj.onc.1208081. PMID:15489910.
4. 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(23): 13877-13879. PMID:6292212.
5. D'Oro, U., and Ashwell, J.D. 1999. Cutting edge: the CD45 tyrosine phosphatase is an inhibitor of Lck activity in thymocytes. J. Immunol. 162(4): 1879-1883. PMID:9973453. (Pubitemid 29288800)
6. Drevot, P.C., Langlet, C., Guo, X.J., Bernard, A.M., Colard, O., Chauvin, J.P., et al. 2002. TCR signal initiation machinery is pre-assembled and activated in a subset of membrane rafts. EMBO J. 21(8): 1899-1908. doi:10.1093/emboj/21.8.1899. PMID:11953309. (Pubitemid 34437187)
7. Edmonds, S.D., and Ostergaard, H.L. 2002. Dynamic association of CD45 with detergent-insoluble microdomains in T lymphocytes. J. Immunol. 169(9): 5036-5042. PMID:12391219.
8. Filby, A., Seddon, B., Kleczkowska, J., Salmond, R., Tomlinson, P., Smida, M., et al. 2007. Fyn regulates the duration of TCR engagement needed for commitment to effector function. J. Immunol. 179(7): 4635-4644. PMID:17878361.
9. Filipp, D., and Julius, M. 2004. Lipid rafts: resolution of the "fyn problem"? Mol. Immunol. 41(6-7): 645-656. doi:10.1016/j.molimm.2004.04. 011. PMID:15220001.
10. Filipp, D., Zhang, J., Leung, B.L., Shaw, A., Levin, S.D., Veillette, A., and Julius, M. 2003. Regulation of Fyn through translocation of activated Lck into lipid rafts. J. Exp. Med. 197(9): 1221-1227. doi:10.1084/jem.20022112. PMID:12732664.
11. Filipp, D., Leung, B.L., Zhang, J., Veillette, A., and Julius, M. 2004. Enrichment of lck in lipid rafts regulates colocalized fyn activation and the initiation of proximal signals through TCR alpha beta. J. Immunol. 172(7): 4266-4274. PMID:15034040. (Pubitemid 38375240)
12. Fragoso, R., Ren, D., Zhang, X., Su, M.W., Burakoff, S.J., and Jin, Y.J. 2003. Lipid raft distribution of CD4 depends on its palmitoylation and association with Lck, and evidence for CD4-induced lipid raft aggregation as an additional mechanism to enhance CD3 signaling. J. Immunol. 170(2): 913-921. PMID: 12517957. (Pubitemid 36070545)
13. Hardwick, J.S., and Sefton, B.M. 1997. The activated form of the Lck tyrosine protein kinase in cells exposed to hydrogen peroxide is phosphorylated at both Tyr-394 and Tyr-505. J. Biol. Chem. 272(41): 25429-25432. doi:10.1074/jbc.272.41.25429. PMID:9325251.
14. He, H.T., and Marguet, D. 2008. T-cell antigen receptor triggering and lipid rafts: a matter of space and time scales. Talking point on the involvement of lipid rafts in T-cell activation. EMBO Rep. 9(6): 525-530. doi:10.1038/embor.2008.78. PMID: 18516087.
15. Hermiston, M.L., Xu, Z., and Weiss, A. 2003. CD45: a critical regulator of signaling thresholds in immune cells. Annu. Rev. Immunol. 21(1): 107-137. doi:10.1146/annurev.immunol.21.120601.140946. PMID:12414720.
16. Holdorf, A.D., Lee, K.H., Burack, W.R., Allen, P.M., and Shaw, A.S. 2002. Regulation of Lck activity by CD4 and CD28 in the immunological synapse. Nat. Immunol. 3(3): 259-264. doi:10.1038/ni761. PMID:11828322.
17. Hurley, T.R., and Sefton, B.M. 1989. Analysis of the activity and phosphorylation of the lck protein in lymphoid cells. Oncogene, 4(3): 265-272. PMID:2468122.
18. Ilangumaran, S., Arni, S., van Echten-Deckert, G., Borisch, B., and Hoessli, D.C. 1999. Microdomain-dependent regulation of Lck and Fyn protein-tyrosine kinases in T lymphocyte plasma membranes. Mol. Biol. Cell, 10(4): 891-905. PMID:10198045.
19. Irles, C., Symons, A., Michel, F., 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(2): 189-197. doi:10.1038/ni877. PMID:12496963.
20. 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 mechanism for the regulation of Lck in T cells. Biochem. J. 371(Pt 3): 907-915. doi:10.1042/BJ20021578. PMID:12570875.
21. Kabouridis, P.S., Magee, A.I., and Ley, S.C. 1997. S-acylation of LCK protein tyrosine kinase is essential for its signalling function in T lymphocytes. EMBO J. 16(16): 4983-4998. doi:10.1093/emboj/16.16.4983. PMID:9305640.
22. Kawabuchi, M., Satomi, Y., Takao, T., Shimonishi, Y., Nada, S., Nagai, K., et al. 2000. Transmembrane phosphoprotein Cbp regulates the activities of Src-family tyrosine kinases. Nature, 404(6781): 999-1003. doi:10.1038/35010121. PMID:10801129. (Pubitemid 30243594)
23. Kenworthy, A.K. 2008. Have we become overly reliant on lipid rafts? Talking point on the involvement of lipid rafts in T-cell activation. EMBO Rep. 9(6): 531-535. doi:10.1038/embor.2008. 92. PMID:18516088. (Pubitemid 351772915)
24. Kosugi, A., Hayashi, F., Liddicoat, D.R., Yasuda, K., Saitoh, S., 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(2): 133-138. doi:10.1016/S0165-2478(01)00174-2. PMID:11274732.
25. + T cells do not require the polarization of lipid rafts for activation and proliferation. Proc. Natl. Acad. Sci. U.S.A. 99(23): 15006-.doi:10.1073/pnas.232058599. PMID:12419850.
26. Lovatt, M., Filby, A., Parravicini, V., Werlen, G., Palmer, E., and Zamoyska, R. 2006. Lck regulates the threshold of activation in primary T cells, while both Lck and Fyn contribute to the magnitude of the extracellular signal-related kinase response. Mol. Cell. Biol. 26(22): 8655-8665. doi:10.1128/MCB.00168-06. PMID:16966372.
27. Marth, J.D., Cooper, J.A., King, C.S., Ziegler, S.F., Tinker, D.A., Overell, R.W., et al. 1988. Neoplastic transformation induced by an activated lymphocyte-specific protein tyrosine kinase (pp56lck). Mol. Cell. Biol. 8(2): 540-550. PMID:3352600.
28. Montixi, C., Langlet, C., Bernard, A.M., Thimonier, J., Dubois, C., Wurbel, M.A., et al. 1998. Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J. 17(18): 5334-5348. doi:10.1093/emboj/17.18.5334. PMID:9736612. (Pubitemid 28427048)
29. Oetken, C., von Willebrand, M., Marie-Cardine, A., Pessa-Morikawa, T., Ståhls, A., Fisher, S., and Mustelin, T. 1994. Induction of hyperphosphorylation and activation of the p56lck protein tyrosine kinase by phenylarsine oxide, a phosphotyrosine phosphatase inhibitor. Mol. Immunol. 31(17): 1295-1302. doi:10.1016/0161-5890(94)90047-7. PMID:7997241.
30. Ostergaard, H.L., Shackelford, D.A., Hurley, T.R., Johnson, P.R., Hyman, R., Sefton, B.M., and Trowbridge, I.S. 1989. Expression of CD45 alters phosphorylation of the lck-encoded tyrosine protein kinase in murine lymphoma T-cell lines. Proc. Natl. Acad. Sci. U.S.A. 86(22): 8959-8963 . [abstract.] doi:10.1073/pnas.86.22.8959. PMID:2530588.
31. Parolini, I., Sargiacomo, M., Lisanti, M.P., and Peschle, C. 1996. Signal transduction and glycophosphatidylinositol-linked proteins (lyn, lck, CD4, CD45, G proteins, and CD55) selectively localize in Triton-insoluble plasma membrane domains of human leukemic cell lines and normal granulocytes. Blood, 87(9): 3783-3794. PMID:8611704. (Pubitemid 26129606)
32. 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 p56(lck). Eur. J. Immunol. 29(8): 2376-2384. doi:10.1002/(SICI)1521- 4141(199908)29:08〈2376::AID-IMMU2376〉3.0.CO;2-7. PMID: 10458749.
33. Pitcher, L.A., Young, J.A., Mathis, M.A., Wrage, P.C., Bartók, B., and van Oers, N.S. 2003. The formation and functions of the 21- and 23-kDa tyrosine-phosphorylated TCRz subunits. Immunol. Rev. 191(1): 47-61. doi:10.1034/j.1600-065X.2003.00003.x. PMID:12614351.
34. Rodgers, W., and Rose, J.K. 1996. Exclusion of CD45 inhibits activity of p56lck associated with glycolipid-enriched membrane domains. J. Cell Biol. 135(6 Pt 1): 1515-1523. doi:10.1083/jcb. 135.6.1515. PMID:8978819. (Pubitemid 26427648)
35. 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(1): 225-266. doi:10.1111/j.1600-065X.1989.tb00548.x. PMID:2534114.
36. Sharp, L.L., and Hedrick, S.M. 1999. Commitment to the CD4 lineage mediated by extracellular signal-related kinase mitogenactivated protein kinase and lck signaling. J. Immunol. 163(12): 6598-6605. PMID:10586054.
37. Tavano, R., Gri, G., Molon, B., Marinari, B., Rudd, C.E., Tuosto, L., and Viola, A. 2004. CD28 and lipid rafts coordinate recruitment of Lck to the immunological synapse of human T lymphocytes. J. Immunol. 173(9): 5392-5397. PMID: 15494485. (Pubitemid 39392122)
38. Terszowski, G., Jankowski, A., Hendriks, W.J., Rolink, A.G., and Kisielow, P. 2001. Within the hemopoietic system, LAR phosphatase is a T cell lineage-specific adhesion receptor-like protein whose phosphatase activity appears dispensable for T cell development, repertoire selection and function. Eur. J. Immunol. 31(3): 832-840. doi:10.1002/1521-4141(200103)31:3〈832:: AIDIMMU832〉3.0.CO;2-D. PMID:11241288.
39. Thomas, M.L., and Brown, E.J. 1999. Positive and negative regulation of Src-family membrane kinases by CD45. Immunol. Today, 20(9): 406-411. doi:10.1016/S0167-5699(99)01506-6. PMID:10462740.
40. Torgersen, K.M., Vang, T., Abrahamsen, H., Yaqub, S., Horejsí, V., Schraven, B., et al. 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(31): 29313-29318. doi:10.1074/jbc.C100014200. PMID:11390365.
41. Tsujikawa, K., Ichijo, T., Moriyama, K., Tadotsu, N., Sakamoto, K., Sakane, N., et al. 2002. Regulation of Lck and Fyn tyrosine kinase activities by transmembrane protein tyrosine phosphatase leukocyte common antigen-related molecule. Mol. Cancer Res. 1(2): 155-163. PMID:12496362.
42. van Oers, N.S., Tao, W., Watts, J.D., Johnson, P., Aebersold, R., and Teh, H.S. 1993. Constitutive tyrosine phosphorylation of the T-cell receptor (TCR) zeta subunit: regulation of TCR-associated protein tyrosine kinase activity by TCR zeta. Mol. Cell. Biol. 13(9): 5771-5780. PMID:7689151.
43. Vang, T., Abrahamsen, H., Myklebust, S., Enserink, J., Prydz, H., Mustelin, T., et al. 2004. Knockdown of C-terminal Src kinase by siRNA-mediated RNA interference augments T cell receptor signaling in mature T cells. Eur. J. Immunol. 34(8): 2191-2199. doi:10.1002/eji.200425036. PMID:15259016.
44. Viola, A., Schroeder, S., Sakakibara, Y., and Lanzavecchia, A. 1999. T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science, 283(5402): 680-682. doi:10.1126/science.283.5402.680. PMID:9924026.
45. Weiss, A., and Littman, D.R. 1994. Signal transduction by lymphocyte antigen receptors. Cell, 76(2): 263-274. doi:10.1016/0092-8674(94)90334-4. PMID:8293463.
46. Xavier, R., Brennan, T., Li, Q., McCormack, C., and Seed, B. 1998. Membrane compartmentation is required for efficient T cell activation. Immunity, 8(6): 723-732. doi:10.1016/S1074-7613(00)80577-4. PMID:9655486.
47. Yamashita, M., Hashimoto, K., Kimura, M., Kubo, M., Tada, T., and Nakayama, T. 1998. Requirement for p56(lck) tyrosine kinase activation in Th subset differentiation. Int. Immunol. 10(5): 577-591. doi:10.1093/intimm/10.5. 577. PMID:9645606.
48. Yasuda, K., Nagafuku, M., Shima, T., Okada, M., Yagi, T., Yamada, T., et al. 2002. Cutting edge: 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(6): 2813-2817. PMID: 12218089. (Pubitemid 35013117)