Serine residues in the LAT adaptor are essential for TCR-dependent signal transduction

Journal of Leukocyte Biology

Volumn 89, Issue 1, 2011, Pages 63-73

  Martínez Florensa, Mario ^a   García Blesa, Antonio ^b   Yélamos, José ^d   Muñoz Suano, Alba ^b   Domínguez Villar, Margarita ^b   Valdor, Rut ^e   Alonso, Antonio ^f   García Cózar, Francisco ^b   Aparicio, Pedro ^a   Malissen, Bernard ^g   Aguado, Enrique ^b,c  

^a UNIVERSITY OF MURCIA   (Spain)

^b UNIVERSITY OF CÁDIZ   (Spain)

^c HOSPITAL UNIVERSITARIO DE PUERTO REAL   (Spain)

^d HOSPITAL DEL MAR   (Spain)

^e HOSPITAL UNIVERSITARIO VIRGEN DE LA ARRIXACA   (Spain)

^f UNIVERSITY OF MÁLAGA   (Spain)

^g CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

Author keywords

CD3; MAPK kinases; PLC 1; Signaling

Indexed keywords

CALCIUM; FURA 2; INTERLEUKIN 2; LAT PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE C GAMMA1; SERINE;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LEUKEMIA CELL LINE; MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; WESTERN BLOTTING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CALCIUM; CELL MEMBRANE; CONSERVED SEQUENCE; ENZYME ACTIVATION; HEK293 CELLS; HUMANS; INTERLEUKIN-2; JURKAT CELLS; MEMBRANE PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; PHOSPHOLIPASE C GAMMA; PHOSPHOPROTEINS; PHOSPHOTYROSINE; PROTEIN BINDING; RECEPTORS, ANTIGEN, T-CELL; SERINE; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSFECTION; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 79251585263     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0509342     Document Type: Article

References (48)

1. Lin, J., Weiss, A. (2001) T cell receptor signaling. J. Cell Sci. 114, 243-244.
2. Koretzky, G. A., Abtahian, F., Derimanov, G. S., Dmowski, S. A., Guerriero, A., Jordan, M. S., Maltzman, J. S., Olenchock, B. A., Singer, A. L., Wu, J. N., Zhong, X. P. (2003) Regulation of hematopoietic cell development and activation by adapter proteins. Immunol. Res. 27, 357-366. (Pubitemid 36995018)
3. Zhang, W., Sloan-Lancaster, J., Kitchen, J., Trible, R. P., Samelson, L. E. (1998) LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 92, 83-92. (Pubitemid 28053300)
4. Weber, J. R., Orstavik, S., Torgersen, K. M., Danbolt, N. C., Berg, S. F., Ryan, J. C., Tasken, K., Imboden, J. B., Vaage, J. T. (1998) Molecular cloning of the cDNA encoding pp36, a tyrosine-phosphorylated adaptor protein selectively expressed by T cells and natural killer cells. J. Exp. Med. 187, 1157-1161.
5. Oya, K., Wang, J., Watanabe, Y., Koga, R., Watanabe, T. (2003) Appearance of the LAT protein at an early stage of B-cell development and its possible role. Immunology 109, 351-359.
6. Asada, H., Ishii, N., Sasaki, Y., Endo, K., Kasai, H., Tanaka, N., Takeshita, T., Tsuchiya, S., Konno, T., Sugamura, K. (1999) Grf40, a novel Grb2 family member, is involved in T cell signaling through interaction with SLP-76 and LAT. J. Exp. Med. 189, 1383-1390.
7. Liu, S. K., Fang, N., Koretzky, G. A., McGlade, C. J. (1999) The hematopoietic-specific adaptor protein Gads functions in T-cell signaling via interactions with the SLP-76 and LAT adaptors. Curr. Biol. 9, 67-75.
8. Nuñez-Cruz, S., Aguado, E., Richelme, S., Chetaille, B., Mura, A. M., Richelme, M., Pouyet, L., Jouvin-Marche, E., Xerri, L., Malissen, B., Malissen, M. (2003) LAT regulates γδ T cell homeostasis and differentiation. Nat. Immunol. 4, 999-1008. (Pubitemid 37265921)
9. Zhang, W., Sommers, C. L., Burshtyn, D. N., Stebbins, C. C., DeJarnette, J. B., Trible, R. P., Grinberg, A., Tsay, H. C., Jacobs, H. M., Kessler, C. M., Long, E. O., Love, P. E., Samelson, L. E. (1999) Essential role of LAT in T cell development. Immunity 10, 323-332.
10. Lin, J., Weiss, A. (2001) Identification of the minimal tyrosine residues required for linker for activation of T cell function. J. Biol. Chem. 276, 29588-29595. (Pubitemid 37452058)
11. Paz, P. E., Wang, S., Clarke, H., Lu, X., Stokoe, D., Abo, A. (2001) Mapping the Zap-70 phosphorylation sites on LAT (linker for activation of T cells) required for recruitment and activation of signaling proteins in T cells. Biochem. J. 356, 461-471.
12. Zhang, W., Trible, R. P., Zhu, M., Liu, S. K., McGlade, C. J., Samelson, L. E. (2000) Association of Grb2, Gads, and phospholipase C-γ 1 with phosphorylated LAT tyrosine residues. Effect of LAT tyrosine mutations on T cell antigen receptor-mediated signaling. J. Biol. Chem. 275, 23355-23361.
13. Aguado, E., Richelme, S., Nunez-Cruz, S., Miazek, A., Mura, A. M., Richelme, M., Guo, X. J., Sainty, D., He, H. T., Malissen, B., Malissen, M. (2002) Induction of T helper type 2 immunity by a point mutation in the LAT adaptor. Science 296, 2036-2040.
14. Sommers, C. L., Park, C. S., Lee, J., Feng, C., Fuller, C. L., Grinberg, A., Hildebrand, J. A., Lacana, E., Menon, R. K., Shores, E. W., Samelson, L. E., Love, P. E. (2002) A LAT mutation that inhibits T cell development yet induces lymphoproliferation. Science 296, 2040-2043.
15. Matsuda, S., Miwa, Y., Hirata, Y., Minowa, A., Tanaka, J., Nishida, E., Koyasu, S. (2004) Negative feedback loop in T-cell activation through MAPK-catalyzed threonine phosphorylation of LAT. EMBO J. 23, 2577-2585. (Pubitemid 38988229)
16. Blom, N., Gammeltoft, S., Brunak, S. (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 294, 1351-1362.
17. Gross, S. D., Anderson, R. A. (1998) Casein kinase I: spatial organization and positioning of a multifunctional protein kinase family. Cell. Signal. 10, 699-711.
18. Vielhaber, E., Virshup, D. M. (2001) Casein kinase I: from obscurity to center stage. IUBMB Life 51, 73-78.
19. Zhu, J., Shibasaki, F., Price, R., Guillemot, J. C., Yano, T., Dotsch, V., Wagner, G., Ferrara, P., McKeon, F. (1998) Intramolecular masking of nuclear import signal on NF-AT4 by casein kinase I and MEKK1. Cell 93, 851-861. (Pubitemid 28257590)
20. Obenauer, J. C., Cantley, L. C., Yaffe, M. B. (2003) Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31, 3635-3641.
21. Goldsmith, M. A., Dazin, P. F., Weiss, A. (1988) At least two non-antigen-binding molecules are required for signal transduction by the T-cell antigen receptor. Proc. Natl. Acad. Sci. USA 85, 8613-8617.
22. Finco, T. S., Kadlecek, T., Zhang, W., Samelson, L. E., Weiss, A. (1998) LAT is required for TCR-mediated activation of PLCγ1 and the Ras pathway. Immunity 9, 617-626.
23. Atucha, N., Iyu, D., De Rycker, M., Soler, A., Garcia-Estan, J. (2003) Altered calcium regulation in freshly isolated aortic smooth muscle cells from bile duct-ligated rats: role of nitric oxide. Cell Calcium 33, 129-135.
24. Prinz, I., Gregoire, C., Mollenkopf, H., Aguado, E., Wang, Y., Malissen, M., Kaufmann, S. H., Malissen, B. (2005) The type 1 cysteinyl leukotriene receptor triggers calcium influx and chemotaxis in mouse α β- and γ δ effector T cells. J. Immunol. 175, 713-719.
25. Desagher, S., Osen-Sand, A., Montessuit, S., Magnenat, E., Vilbois, F., Hochmann, A., Journot, L., Antonsson, B., Martinou, J. C. (2001) Phosphorylation of bid by casein kinases I and II regulates its cleavage by caspase 8. Mol. Cell 8, 601-611.
26. Saeki, K., Yuo, A., Takaku, F. (1999) Cell-cycle-regulated phosphorylation of cAMP response element-binding protein: identification of novel phosphorylation sites. Biochem. J. 338, 49-54.
27. Marin, O., Bustos, V. H., Cesaro, L., Meggio, F., Pagano, M. A., Antonelli, M., Allende, C. C., Pinna, L. A., Allende, J. E. (2003) A noncanonical sequence phosphorylated by casein kinase 1 in β-catenin may play a role in casein kinase 1 targeting of important signaling proteins. Proc. Natl. Acad. Sci. USA 100, 10193-10200.
28. Lickert, H., Bauer, A., Kemler, R., Stappert, J. (2000) Casein kinase II phosphorylation of E-cadherin increases E-cadherin/β-catenin interaction and strengthens cell- cell adhesion. J. Biol. Chem. 275, 5090-5095.
29. Zhu, M., Shen, S., Liu, Y., Granillo, O., Zhang, W. (2005) Cutting edge: localization of linker for activation of T cells to lipid rafts is not essential in T cell activation and development. J. Immunol. 174, 31-35.
30. Payne, D. M., Rossomando, A. J., Martino, P., Erickson, A. K., Her, J. H., Shabanowitz, J., Hunt, D. F., Weber, M. J., Sturgill, T. W. (1991) Identification of the regulatory phosphorylation sites in pp42/mitogen-activated protein kinase (MAP kinase). EMBO J. 10, 885-892.
31. Sturgill, T. W., Ray, L. B., Erikson, E., Maller, J. L. (1988) Insulin-stimulated MAP-2 kinase phosphorylates and activates ribosomal protein S6 kinase II. Nature 334, 715-718.
32. Wang, Z., Gluck, S., Zhang, L., Moran, M. F. (1998) Requirement for phospholipase C-γ1 enzymatic activity in growth factor-induced mitogenesis. Mol. Cell. Biol. 18, 590-597.
33. Reynolds, L. F., de Bettignies, C., Norton, T., Beeser, A., Chernoff, J., Tybulewicz, V. L. J. (2004) Vav1 transduces T cell receptor signals to the activation of the Ras/ERK pathway via LAT, Sos, and RasGRP1. J. Biol. Chem. 279, 18239-18246.
34. Houtman, J. C. D., Houghtling, R. A., Barda-Saad, M., Toda, Y., Samelson, L. E. (2005) Early phosphorylation kinetics of proteins involved in proximal TCR-mediated signaling pathways. J. Immunol. 175, 2449-2458.
35. Watts, J. D., Affolter, M., Krebs, D. L., Wange, R. L., Samelson, L. E., Aebersold, R. (1994) Identification by electrospray ionization mass spectrometry of the sites of tyrosine phosphorylation induced in activated Jurkat T cells on the protein tyrosine kinase ZAP-70. J. Biol. Chem. 269, 29520-29529.
36. Rellahan, B. L., Graham, L. J., Tysgankov, A. Y., DeBell, K. E., Veri, M. C., Noviello, C., Bonvini, E. (2003) A dynamic constitutive and inducible binding of c-Cbl by PLCγ1 SH3 and SH2 domains (negatively) regulates antigen receptor-induced PLCγ1 activation in lymphocytes. Exp. Cell Res. 289, 184-194.
37. Chiang, Y. J., Sommers, C. L., Jordan, M. S., Gu, H., Samelson, L. E., Koretzky, G. A., Hodes, R. J. (2004) Inactivation of c-Cbl reverses neonatal lethality and T cell developmental arrest of SLP-76-deficient mice. J. Exp. Med. 200, 25-34. (Pubitemid 38924725)
38. Braiman, A., Barda-Saad, M., Sommers, C. L., Samelson, L. E. (2006) Recruitment and activation of PLCγ1 in T cells: a new insight into old domains. EMBO J. 25, 774-784. (Pubitemid 43292439)
39. Balagopalan, L., Barr, V. A., Sommers, C. L., Barda-Saad, M., Goyal, A., Isakowitz, M. S., Samelson, L. E. (2007) c-Cbl-mediated regulation of LAT-nucleated signaling complexes. Mol. Cell. Biol. 27, 8622-8636.
40. Jhun, B. S., Oh, Y. T., Lee, J. Y., Kong, Y., Yoon, K. S., Kim, S. S., Baik, H. H., Ha, J., Kang, I. (2005) AICAR suppresses IL-2 expression through inhibition of GSK-3 phosphorylation and NF-AT activation in Jurkat T cells. Biochem. Biophys. Res. Commun. 332, 339-346. (Pubitemid 40724983)
41. Yablonski, D., Kuhne, M. R., Kadlecek, T., Weiss, A. (1998) Uncoupling of nonreceptor tyrosine kinases from PLC-γ1 in an SLP-76-deficient T cell. Science 281, 413-416. (Pubitemid 28340785)
42. Wang, Y., Johnson, P. (2005) Expression of CD45 lacking the catalytic protein tyrosine phosphatase domain modulates Lck phosphorylation and T cell activation. J. Biol. Chem. 280, 14318-14324. (Pubitemid 40517335)
43. Ardouin, L., Rolink, A. G., Mura, A. M., Gommeaux, J., Melchers, F., Busslinger, M., Malissen, M., Malissen, B. (2005) Rapid in vivo analysis of mutant forms of the LAT adaptor using Pax5-Lat double-deficient pro-B cells. Eur. J. Immunol. 35, 977-986. (Pubitemid 40425554)
44. Ande, S. R., Moulik, S., Mishra, S. (2009) Interaction between O-GlcNAc modification and tyrosine phosphorylation of prohibitin: implication for a novel binary switch. PLoS ONE 4, e4586.
45. Golks, A., Guerini, D. (2008) The O-linked N-acetylglucosamine modification in cellular signaling and the immune system. "Protein modifications: beyond the usual suspects" review series. EMBO Rep. 9, 748-753.
46. Malissen, B., Aguado, E., Malissen, M. (2005) Role of the LAT adaptor in T cell development and Th2 differentiation. Adv. Immunol., 87, 1-25. (Pubitemid 41133491)
47. Zhang, W., Irvin, B. J., Trible, R. P., Abraham, R. T., Samelson, L. E. (1999) Functional analysis of LAT in TCR-mediated signaling pathways using a LAT-deficient Jurkat cell line. Int. Immunol. 11, 943-950. (Pubitemid 29276606)
48. Sommers, C. L., Menon, R. K., Grinberg, A., Zhang, W., Samelson, L. E., Love, P. E. (2001) Knock-in mutation of the distal four tyrosines of linker for activation of T cells blocks murine T cell development. J. Exp. Med. 194, 135-142. (Pubitemid 32673346)