GrpL, a Grb2-related adaptor protein, interacts with SLP-76 to regulate nuclear factor of activated T cell activation

Journal of Experimental Medicine

Volumn 189, Issue 8, 1999, Pages 1243-1253

  Law, Che Leung ^a,b   Ewings, Maria K ^a   Chaudhary, Preet M ^a   Solow, Sasha A ^a   Yun, Theodore J ^a   Marshall, Aaron J ^a   Hood, Leroy ^a   Clark, Edward A ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b CYCLACEL LTD   (United Kingdom)

Author keywords

Cell activation; Grb2; GrpL; Nuclear factor of activated cells; SLP 76

Indexed keywords

ADAPTOR PROTEIN; NUCLEAR FACTOR; T LYMPHOCYTE RECEPTOR;

ARTICLE; ENZYME ACTIVATION; HEMATOPOIESIS; HUMAN; HUMAN CELL; MOLECULAR CLONING; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD3; CARRIER PROTEINS; CLONING, MOLECULAR; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HUMANS; JURKAT CELLS; MICE; MOLECULAR SEQUENCE DATA; NFATC TRANSCRIPTION FACTORS; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PROLINE; RECEPTORS, ANTIGEN, T-CELL; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; T-LYMPHOCYTES; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS;

EID: 0033583420     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.189.8.1243     Document Type: Article

References (57)

1. Park, D.J., H.W. Rho, and S.G. Rhee. 1991. CD3 stimulation causes phosphorylation of phospholipase C-gamma 1 on serine and tyrosine residues in a human T-cell line. Proc. Natl. Acad. Sci. USA. 88:5453-5456.
2. Secrist, J.P., L. Karnitz, and R.T. Abraham. 1991. T-cell antigen receptor ligation induces tyrosine phosphorylation of phospholipase C-gamma 1. J. Biol. Chem. 266:12135-12139.
3. Weiss, A., G. Koretzky, R.C. Schatzman, and T. Kadlecek. 1991. Functional activation of the T-cell antigen receptor induces tyrosine phosphorylation of phospholipase C-gamma 1. Proc. Natl. Acad. Sci. USA. 88:5484-5488.
4. Fukazawa, T., K.A. Reedquist, G. Panchamoorthy, S. Soltoff, T. Trub, B. Druker, L. Cantley, S.E. Shoelson, and H. Band. 1995. T cell activation-dependent association between the p85 subunit of the phosphatidylinositol 3-kinase and Grb2/phospholipase C-gamma 1-binding phosphotyrosyl protein pp36/38. J. Biol. Chem. 270:20177-20182.
5. Motto, D.G., S.E. Ross, J.K. Jackman, Q. Sun, A.L. Olson, P.R. Findell, and G.A. Koretzky. 1994. In vivo association of Grb2 with pp116, a substrate of the T cell antigen receptor-activated protein tyrosine kinase. J. Biol. Chem. 269:21608-21613.
6. Jackman, J.K., D.G. Motto, Q. Sun, M. Tanemoto, C.W. Turck, G.A. Peltz, G.A. Koretzky, and P.R. Findell. 1995. Molecular cloning of SLP-76, a 76-kDa tyrosine phosphoprotein associated with Grb2 in T cells. J. Biol. Chem. 270: 7029-7032.
7. Fukazawa, T., K.A. Reedquist, T. Trub, S. Soltoff, G. Panchamoorthy, B. Druker, L. Cantley, S.E. Shoelson, and H. Band. 1995. The SH3 domain-binding T cell tyrosyl phosphoprotein p120. Demonstration of its identity with the c-cbl protooncogene product and in vivo complexes with Fyn, Grb2, and phosphatidylinositol 3-kinase. J. Biol. Chem. 270:19141-19150.
8. Margolis, B., P. Hu, S. Katzav, W. Li, J.M. Oliver, A. Ullrich, A. Weiss, and J. Schlessinger. 1992. Tyrosine phosphorylation of vav proto-oncogene product containing SH2 domain and transcription factor motifs. Nature. 356:71-74.
9. Tuosto, L., F. Michel, and O. Acuto. 1996. p95vav associates with tyrosine-phosphorylated SLP-76 in antigen-stimulated T cells. J. Exp. Med. 184:1161-1166.
10. Gilliland, L.K., G.L. Schieven, N.A. Norris, S.B. Kanner, A. Aruffo, and J.A. Ledbetter. 1992. Lymphocyte lineage-restricted tyrosine-phosphorylated proteins that bind PLC gamma 1 SH2 domains. J. Biol. Chem. 267:13610-13616.
11. Buday, L., S.E. Egan, V.-P. Rodriguez, D.A. Cantrell, and J. Downward. 1994. A complex of Grb2 adaptor protein, Sos exchange factor, and a 36-kDa membrane-bound tyrosine phosphoprotein is implicated in ras activation in T cells. J. Biol. Chem. 269:9019-9023.
12. Sieh, M., A. Batzer, J. Schlessinger, and A. Weiss. 1994. GRB2 and phospholipase C-gamma 1 associate with a 36-to 38-kilodalton phosphotyrosine protein after T-cell receptor stimulation. Mol. Cell. Biol. 14:4435-4442.
13. Zhang, W., L.-J. Sloan, J. Kitchen, R.P. Trible, and L.E. Samelson. 1998. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell. 92:83-92.
14. Weber, J.R., S. Ørstavik, K.M. Torgersen, N.C. Danbolt, S.F. Berg, J.C. Ryan, K. Taskén, J.B. Imboden, and J.T. Vaage. 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.
15. Weiss, A., and D.R. Littman. 1994. Signal transduction by lymphocyte antigen receptors. Cell. 76:263-274.
16. Chan, A.C., and A.S. Shaw. 1996. Regulation of antigen receptor signal transduction by protein tyrosine kinases. Curr. Opin. Immunol. 8:394-401.
17. Wange, R.L., and L.E. Samelson. 1996. Complex complexes: signaling at the TCR. Immunity. 5:197-205.
18. Wu, J., D.G. Motto, G.A. Koretzky, and A. Weiss. 1996. Vav and SLP-76 interact and functionally cooperate in IL-2 gene activation. Immunity. 4:593-602.
19. Raab, M., A.J. da Silva, P.R. Findell, and C.E. Rudd. 1997. Regulation of Vav-SLP-76 binding by ZAP-70 and its relevance to TCR zeta/CD3 induction of interleukin-2. Immunity. 6:155-164.
20. Fang, N., D.G. Motto, S.E. Ross, and G.A. Koretzky. 1996. Tyrosines 113, 128, and 145 of SLP-76 are required for optimal augmentation of NFAT promoter activity. J. Immunol. 157:3769-3773.
21. Motto, D.G., S.E. Ross, J. Wu, T.-L.R. Hendricks, 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.
22. Clements, J.L., B. Yang, S.E. Ross-Barta, S.L. Eliason, R.F. Hrstka, R.A. Williamson, and G.A. Koretzky. 1998. Requirement for the leukocyte-specific adapter SLP-76 for normal T cell development. Science. 281:416-419.
23. Pivniouk, V., E. Tsitsikov, P. Swinton, G. Rathbun, F.W. Alt, and R.S. Geha. 1998. Impaired viability and profound block in thymocyte development in mice lacking the adaptor protein SLP-76. Cell. 94:229-238.
24. Koretzky, G.A. 1997. The role of Grb2-associated proteins in T-cell activation. Immunol. Today. 18:401-406.
25. Osman, N., S.C. Lucas, H. Turner, and D. Cantrell. 1995. A comparison of the interaction of She and the tyrosine kinase ZAP-70 with the T cell antigen receptor zeta chain tyrosine-based activation motif. J. Biol. Chem. 270:13981-13986.
26. Vojtek, A.B., and J.C. Der. 1998. Increasing complexity of the Ras signaling pathway. J. Biol. Chem. 273:19925-19928.
27. Reif, K., L. Buday, J. Downward, and D.A. Cantrell. 1994. SH3 domains of the adapter molecule Grb2 complex with two proteins in T cells: the guanine nucleotide exchange protein Sos and a 75-kDa protein that is a substrate for T cell antigen receptor-activated tyrosine kinases. J. Biol. Chem. 269:14081-14087.
28. Meisner, H., B.R. Conway, D. Hartley, and M.P. Czech. 1995. Interactions of Cb1 with Grb2 and phosphatidylinositol 3′-kinase in activated Jurkat cells. Mol. Cell. Biol. 15:3571-3578.
29. Donovan, J.A., Y. Ota, W.Y. Langdon, and L.E. Samelson. 1996. Regulation of the association of p120cbl with Grb2 in Jurkat T cells. J. Biol. Cliem. 271:26369-26374.
30. Wardenburg, J.B., C. Fu, J.K. Jackman, H. Flotow, S.E. Wilkinson, D.H. Williams, R. Johnson, G. Kong, A.C. Chan, and P.R. Findell. 1996. Phosphorylation of SLP-76 by the ZAP-70 protein-tyrosine kinase is required for T-cell receptor function. J. Biol. Chem. 271:19641-19644.
31. Buday, L., A. Khwaja, S. Sipeki, A. Farago, and J. Downward. 1996. Interactions of Cb1 with two adapter proteins, Grb2 and Crk, upon T cell activation. J. Biol. Chem. 271:6159-6163.
32. Reedquist, K.A., T. Fukazawa, G. Panchamoorthy, W.Y. Langdon, S.E. Shoelson, B.J. Druker, and H. Band. 1996. Stimulation through the T cell receptor induces Cb1 association with Crk proteins and the guanine nucleotide exchange protein C3G. J. Biol. Chem. 271:8435-8442.
33. Feng, G.S., Y.B. Ouyang, D.P. Hu, Z.Q. Shi, R. Gentz, and J. Ni. 1996. Grap is a novel SH3-SH2-SH3 adaptor protein that couples tyrosine kinases to the Ras pathway. J. Biol. Chem. 271:12129-12132.
34. Trub, T., J.D. Frantz, M. Miyazaki, H. Band, and S.E. Shoelson. 1997. The role of a lymphoid-restricted, Grb2-like SH3-SH2-SH3 protein in T cell receptor signaling. J. Biol. Chem. 272:894-902.
35. Leprince, C., K.E. Draves, J.A. Ledbetter, R.M. Torres, and E.A. Clark. 1992. Characterization of molecular components associated with surface immunoglobulin M in human B lymphocytes: presence of tyrosine and serine/threonine protein kinases. Eur. J. Immunol. 22:2093-2099.
36. Mayer, B.J., and M.J. Eck. 1995. SH3 domains. Minding your p's and q's. Curr. Biol. 5:364-367.
37. Kuriyan, J., and D. Cowburn. 1997. Modular peptide recognition domains in eukaryotic signaling. Annu. Rev. Biophys. Biomiol. Struct. 26:259-298.
38. Lowenstein, E.J., R.J. Daly, A.G. Batzer, W. Li, B. Margolis, R. Lammers, A. Ullrich, E.Y. Skolnik, S.-D. Bar, and J. Schlessinger. 1992. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell. 70:431-442.
39. Musci, M.A., D.G. Motto, S.E. Ross, N. Fang, and G.A. Koretzky. 1997. Three domains of SLP-76 are required for its optimal function in a T cell line. J. Immunol. 159:1639-1647.
40. da Silva, A.J., Z. Li, C. de Vera, E. Canto, P. Findell, and C.E. Rudd. 1997. Cloning of a novel T-cell protein FYB that binds FYN and SH2-domain-containing leukocyte protein 76 and modulates interleukin 2 production. Proc. Natl. Acad. Sci. USA. 94:7493-7498.
41. Musci, M.A., T.-L.R. Hendricks, D.G. Motto, M. Paskind, J. Kamens, C.W. Turck, and G.A. Koretzky. 1997. Molecular cloning of SLAP-130, an SLP-76-associated substrate of the T cell antigen receptor-stimulated protein tyrosine kinases. J. Biol. Chem. 272:11674-11677.
42. Fra, A.M., E. Williamson, K. Simons, and R.G. Parton. 1995. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc. Natl. Acad. Sci. USA. 92: 8655-8659.
43. Brown, D.A., and E. London. 1997. Structure of detergent-resistant membrane domains: does phase separation occur in biological membranes? Biochem. Biophys. Res. Commun. 240:1-7.
44. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature. 387:569-572.
45. 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.
46. Xavier, R., T. Brennan, Q. Li, C. McConnack, and B. Seed. 1998. Membrane compartmentation is required for efficient T cell activation. Immunity. 8:723-732.
47. Xiao, S., D.W. Rose, T. Sasaoka, H. Maegawa, T.R. Burke, Jr., P.P. Roller, S.E. Shoelson, and J.M. Oleftky. 1994. Syp (SH-PTP2) is a positive mediator of growth factor-stimulated mitogenic signal transduction. J. Biol. Chem. 269:21244-21248.
48. Zhao, Z., Z. Tan, J.H. Wright, C.D. Diltz, S.H. Shen, E.G. Krebs, and E.H. Fischer. 1995. Altered expression of protein-tyrosine phosphatase 2C in 293 cells affects protein tyrosine phosphorylation and mitogen-activated protein kinase activation. J. Biol. Chem. 270:11765-11769.
49. Marengere, L.E., P. Waterhouse, G.S. Duncan, H.W. Mittrucker, G.S. Feng, and T.W. Mak. 1996. Regulation of T cell receptor signaling by tyrosine phosphatase SYP association with CTLA-4. Science. 272:1170-1173.
50. Frearson, J.A., and D.R. Alexander. 1998. The phosphotyrosine phosphatase SHP-2 participates in a multimeric signaling complex and regulates T cell receptor (TCR) coupling to the Ras/mitogen-activated protein kinase (MAPK) pathway in Jurkat T cells. J. Exp. Med. 187:1417-1426.
51. Crespo, P., K.E. Schuebel, A.A. Ostrom, J.S. Gutkind, and X.R. Bustelo. 1997. Phosphotyrosine-dependent activation of Rac-1 GDP/GTP exchange by the vav proto-oncogene product. Nature. 385:169-172.
52. Reif, K., and D.A. Cantrell. 1998. Networking Rho family GTPases in lymphocytes. Immunity. 8:395-401.
53. Wardenburg, J.B., R. Pappu, J.-Y. Bu, B. Mayer, J. Chernoff, D. Straus, and A.C. Chan. 1998. Regulation of PAK activation and the T cell cytoskeleton by the linker protein SLP-76. Immunity. 9:607-616.
54. Bourette, R.P., S. Arnaud, G.M. Myles, J.-P. Blanchet, L.R. Rohrschneider, and G. Mouchiroud. 1998. Mona, a novel hematopoietic-specific adaptor interacting with the macrophage colony-stimulating factor receptor, is implicated in monocyte/macrophage development. EMBO (Eur. Mol. Biol. Organ.) J. 17:7273-7281.
55. Liu, S.K., and C.J. McGlade. 1998. Gads is a novel SH2 and SH3 domain-containing adaptor protein that binds to tyrosine-phosphorylated Shc. Oncogene. 17:3073-3082.
56. Liu, S.K., N. Fang, G.A. Koretzky, and C.J. McGlade. 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.
57. Fu, C., C.W. Turck, T. Kurosaki, and A.C. Chan. 1998. BLNK: a central linker protein in B cell activation. Immunity. 9:93-103.