Dynamic recruitment of PAK1 to the immunological synapse is mediated by PIX independently of SLP-76 and Vav1

Nature Immunology

Volumn 6, Issue 6, 2005, Pages 608-617

  Phee, Hyewon ^a   Abraham, Robert T ^b   Weiss, Arthur ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOLIPASE C GAMMA; PHOSPHOPROTEIN; PROTEIN CDC42; PROTEIN SERINE THREONINE KINASE; PROTEIN SLP 76; RAC PROTEIN; T LYMPHOCYTE ANTIGEN; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; VAV PROTEIN; CELL CYCLE PROTEIN; DNA; GUANINE NUCLEOTIDE EXCHANGE FACTOR; LYMPHOCYTE ANTIGEN RECEPTOR; MULTIPROTEIN COMPLEX; ONCOPROTEIN; PAK1 PROTEIN, HUMAN; PHOSPHOLIPASE C; RECOMBINANT PROTEIN; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR 6; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SLP 76 SIGNAL TRANSDUCING ADAPTOR PROTEINS; SLP-76 SIGNAL TRANSDUCING ADAPTOR PROTEINS; VAV1 PROTEIN, HUMAN;

ANTIGEN PRESENTING CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LEUKEMIA CELL LINE; PRIORITY JOURNAL; PROTEIN BINDING; SIGNAL TRANSDUCTION; T LYMPHOCYTE; CHEMISTRY; DRUG ANTAGONISM; GENETICS; IMMUNOLOGY; METABOLISM; NUCLEOTIDE SEQUENCE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANTIGEN-PRESENTING CELLS; BASE SEQUENCE; BINDING SITES; CDC42 GTP-BINDING PROTEIN; CELL CYCLE PROTEINS; DNA; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; JURKAT CELLS; MULTIPROTEIN COMPLEXES; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-VAV; RAC GTP-BINDING PROTEINS; RECEPTORS, ANTIGEN, T-CELL; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSCRIPTION, GENETIC;

EID: 20644447796     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni1199     Document Type: Article

References (53)

1. Samelson, L.E. Signal transduction mediated by the T cell antigen receptor: the role of adapter proteins. Annu. Rev. Immunol. 20, 371-394 (2002).
2. Tomlinson, M.G., Lin, J. & Weiss, A. Lymphocytes with a complex: adapter proteins in antigen receptor signaling, Immunol. Today 21, 584-591 (2000).
3. Bubeck Wardenburg, J. et al. Regulation of PAK activation and the T cell cytoskeleton by the linker protein SLP-76. Immunity 9, 607-616 (1998).
4. Yablonski, D., Kane, L.P., Qian, D. & Weiss, A.A. Nck-Pak1 signaling module is required for T-cell receptor-mediated activation of NFAT, but not of JNK. EMBO J. 17, 5647-5657 (1998).
5. Chu, P. et al. Systematic identification of regulatory proteins critical for T-cell activation. J. Biol. 2, 21 (2003).
6. Chu, P.C. et al. A novel role for p21-activated protein kinase 2 in T cell activation. J. Immunol. 172, 7324-7334 (2004).
7. Bokoch, G.M. Biology of the p21-activated kinases. Annu. Rev. Biochem. 72, 743-781 (2003).
8. Monks, C.R., Freiberg, B.A., Kupfer, H., Sciaky, N. & Kupfer, A. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395, 82-86 (1998).
9. Jacobelli, J., Andres, P.G., Boisvert, J. & Krummel, M.F. New views of the immunological synapse: variations in assembly and function. Curr. Opin. Immunol. 16, 345-352 (2004).
10. Lee, K.H. et al. T cell receptor signaling precedes immunological synapse formation. Science 295, 1539-1542 (2002).
11. Montoya, M.C. et al. Role of ICAM-3 in the initial interaction of T lymphocytes and APCs. Nat. Immunol. 3, 159-168 (2002).
12. Bonello, G. et al. Dynamic recruitment of the adaptor protein LAT: LAT exists in two distinct intracellular pools and controls its own recruitment. J. Cell Sci, 117, 1009-1016 (2004).
13. Ku, G.M., Yablonski, D., Manser, E., Lim, L. & Weiss, A.A. PAK1-PIX-PKL complex is activated by the T-cell receptor independent of Nck, Slp-76 and LAT. EMBO J. 20, 457-165 (2001).
14. Manser, E., Leung, T., Salihuddin, H., Zhao, Z.S. & Lim, L. A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature 367, 40-46 (1994).
15. DeFranco, A.L. Vav and the B cell signalosome. Nat. Immunol. 2, 482-484 (2001).
16. l6. Tybulewicz, V.L., Ardouin, L., Prisco, A. & Reynolds, L.F. Vav1: a key signal transducer downstream of the TCR. Immunol. Rev. 192, 42-52 (2003).
17. Crespo, P., Schuebel, K.E., Ostrom, A.A., Gutkind, J.S. & Bustelo, X.R. Phosphotyrosine-dependent activation of Rac-1 GDP/GTP exchange by the vav proto-oncogene product. Nature 385, 169-172 (1997).
18. Han, J. et al. Lck regulates Vav activation of members of the Rho family of GTPases. Mol. Cell. Biol. 17, 1346-1353 (1997).
19. Zeng, R. et al. SLP-76 coordinates Nck-dependent Wiskott-Aldrich syndrome protein recruitment with Vav-1/Cdc42-dependent Wiskott-Aldrich syndrome protein activation at the T cell-APC contact site. J. Immunol. 171, 1360-1368 (2003).
20. Liu, S.K., Fang, N., Koretzky, G.A. & McGlade, C.J. 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 (1999).
21. Bagrodia, S., Taylor, S.J., Jordon, K.A., Van Aelst, L. & Cerione, R.A. A novel regulator of p21-activated kinases. J. Biol. Chem. 273, 23633-23636 (1998).
22. Manser, E. et al. PAK kinases are directly coupled to the PIX family of nucleotide exchange factors. Mol. Cell 1, 183-192 (1998).
23. Zhao, Z.S., Manser, E. & Lim, L. Interaction between PAK and Nck: a template for Nck targets and role of PAK autophosphorylation. Mol. Cell. Biol. 20, 3906-3917 (2000).
24. 2-Adrenergic receptor regulation by GIT1, a G protein-coupled receptor kinase-associated ADP ribosylation factor GTPase-activating protein. Proc, Natl. Acad. Sci. USA 495, 14082-14087 (1998).
25. Bagrodia, S. et al. A tyrosine-phosphorylated protein that binds to an important regulatory region on the cool family of p21-activated kinase-binding proteins. J. Biol. Chem. 274, 22393-22400 (1999).
26. Premont, R.T., Claing, A., Vitale, N., Perry, S.J. & Lefkowitz, R.J. The GIT family of ADP-ribosylation factor GTPase-activating proteins. Functional diversity of GIT2 through alternative splicing. J. Biol. Chem. 275, 22373-22380 (2000).
27. Turner, C.E. et al. Paxillin LD4 motif binds PAK and PIX through a novel 95-kD ankyrin repeat, ARF-GAP protein: A role in cytoskeletal remodeling. J. Cell Biol. 145, 851-863 (1999).
28. Turner, C.E., West, K.A. & Brown, M.C. Paxillin-ARF GAP signaling and the cytoskeleton. Curr. Opin. Cell Biol. 13, 593-599 (2001).
29. Natarajan, K., Yin, G. & Berk, B.C. Scaffolds direct Src-specific signaling in response to angiotensin II: new roles for Cas and GIT1. Mol. Pharmacol. 65, 822-825 (2004).
30. Zakaria, S. et al. Differential regulation of TCR-mediated gene transcription by Vav family members. J. Exp. Med. 199, 429-434 (2004).
31. Wu, J., Motto, D.G., Koretzky, G.A. & Weiss, A. Vav and SLP-76 interact and functionally cooperate in IL-2 gene activation. Immunity 4, 593-602 (1996).
32. Benard, V., Bohl, B.P. & Bokoch, G.M. Characterization of Rac and Cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J. Biol. Chem. 274, 13198-13204 (1999).
33. Kraynov, V.S. et al. Localized Rac activation dynamics visualized in living cells. Science 290, 333-337 (2000).
34. Ardouin, L. et al. Vav1 transduces TCR signals required for LFA-1 function and cell polarization at the immunological synapse. Eur. J, Immunol. 33, 790-797 (2003).
35. King, C.C. et al. p21-activated kinase (PAK1) is phosphorylated and activated by 3-phosphoinositide-dependent kinase-1 (PDK1). J. Biol. Chem. 275, 41201-41209 (2000).
36. Chong, C., Tan, L., Lim, L. & Manser, E. The mechanism of PAK activation. Autophosphorylation events in both regulatory and kinase domains control activity. J. Biol. Chem. 276, 17347-17353 (2001).
37. Krummel, M.F., Sjaastad, M.D., Wulfing, C. & Davis, M.M. Differential clustering of CD4 and CD3ζ during T cell recognition. Science 289, 1349-1352 (2000).
38. Kim, H.K. et al. PDGF stimulation of inositol phospholipid hydrolysis requires PLC-γ1 phosphorylation on tyrosine residues 783 and 1254. Cell 65, 435-41 (1991).
39. Fraser, J.D., Newton, M.E. & Weiss, A. CD28 and T cell antigen receptor signal transduction coordinately regulate interleukin 2 gene expression in response to superantigen stimulation. J. Exp. Med. 175, 1131-1134 (1992).
40. Shapiro, V.S., Truitt, K.E., Imboden, J.B. & Weiss, A. CD28 mediates transcriptional upregulation of the interleukin-2 (IL-2) promoter through a composite element containing the CD28RE and NF-IL-2B AP-I sites. Mol. Cell. Biol. 17, 4051-4058 (1997).
41. Daniels, R.H., Hall, P.S. & Bokoch, G.M. Membrane targeting of p21-activated kinase 1 (PAK1) induces neurite outgrowth from PC12 cells. EMBO J. 17, 754-764 (1998).
42. Loo, T.H., Ng, Y.W., Lim, L. & Manser, E. GIT1 activates p21-activated kinase through a mechanism independent of p21 binding. Mol. Cell. Biol. 24, 3849-3859 (2004).
43. Dustin, M.L. & Cooper, J.A. The immunological synapse and the actin cytoskeleton: molecular hardware for T cell signaling. Nat. Immunol. 1, 23-29 (2000).
44. Bunnell, S.C., Kapoor, V., Trible, R.P., Zhang, W. & Samelson, L.E. Dynamic actin polymerization drives T cell receptor-induced spreading: a role for the signal transduction adaptor LAT. Immunity 14, 315-329 (2001).
45. Barda-Saad, M. et al. Dynamic molecular interactions linking the T cell antigen receptor to the actin cytoskeleton. Nat. Immunol. 6, 80-89 (2005).
46. Negulescu, P.A., Krasieva, T.B., Khan, A., Kerschbaum, H.H. & Cahalan, M.D. Polarity of T cell shape, motility, and sensitivity to antigen. Immunity 4, 421-430 (1996).
47. Weiss, A. & Stobo, J.D. 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 (1984).
48. Yablonski, D., Kuhne, M.R., Kadlecek, T. & Weiss, A. Uncoupling of nonreceptor tyrosine kinases from PLC-γ1 in an SLP-76-deficient T cell. Science 281, 413-416 (1998).
49. Cao, Y. et al. Pleiotropic defects in TCR signaling in a Vav-1-null Jurkat T-cell line. EMBO J. 21, 4809-4819 (2002).
50. Williams, B.L. et al. 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 (1998).
51. Kuhne, M.R., Ku, G. & Weiss, A. A guanine nucleotide exchange factor-independent function of Vav1 in transcriptional activation. J. Biol. Chem, 275, 2185-2190 (2000).
52. Takesono, A., Horai, R., Mandai, M., Dombroski, D. & Schwartzberg, P.L. Requirement for Tec kinases in chemokine-induced migration and activation of Cdc42 and Rac. Curr. Biol. 14, 917-922 (2004).
53. Shapiro, V.S., Mollenauer, M.N., Greene, W.C. & Weiss, A. c-rel regulation of IL-2 gene expression may be mediated through activation of AP-1. J. Exp. Med. 184, 1663-1669 (1996).