Erk/Src phosphorylation of cortactin acts as a switch on-switch off mechanism that controls its ability to activate N-WASP

Molecular and Cellular Biology

Volumn 24, Issue 12, 2004, Pages 5269-5280

  Martinez Quiles, Narcisa ^a   Ho, Hsin Yi Henry ^b   Kirschner, Marc W ^b   Ramesh, Narayanaswamy ^a   Geha, Raif S ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; CORTACTIN; F ACTIN; MITOGEN ACTIVATED PROTEIN KINASE; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PROLINE; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; TYROSINE; UNCLASSIFIED DRUG; WISKOTT ALDRICH SYNDROME PROTEIN;

ACTIN POLYMERIZATION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; MOLECULAR INTERACTION; MOLECULAR WEIGHT; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

ACTIN-RELATED PROTEIN 2; ACTIN-RELATED PROTEIN 3; ACTINS; ANIMALS; BINDING SITES; CELL LINE; CORTACTIN; CYTOSKELETAL PROTEINS; HUMANS; JURKAT CELLS; MICE; MICROFILAMENT PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASES; MUTAGENESIS, SITE-DIRECTED; NERVE TISSUE PROTEINS; PHOSPHORYLATION; PROTEINS; RECOMBINANT FUSION PROTEINS; SRC HOMOLOGY DOMAINS; SRC-FAMILY KINASES; SWISS 3T3 CELLS; WISKOTT-ALDRICH SYNDROME PROTEIN; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

ANIMALIA; VESPIDAE;

EID: 2942594602     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.12.5269-5280.2004     Document Type: Article

References (67)

1. Andreotti, A. H., S. C. Bunnell, S. Feng, L. J. Berg, and S. L. Schreiber. 1997. Regulatory intramolecular association in a tyrosine kinase of the Tec family. Nature 385:93-97.
2. Bear, J. E., J. F. Rawls, and C. L. Saxe III. 1998. SCAR, a WASP-related protein, isolated as a suppressor of receptor defects in late Dictyostelium development. J. Cell Biol. 142:1325-1335.
3. Bowden, E. T., M. Barth, D. Thomas, R. I. Glazer, and S. C. Mueller. 1999. An invasion-related complex of cortactin, paxillin and PKCmu associates with invadopodia at sites of extracellular matrix degradation. Oncogene 18:4440-4449.
4. Campbell, D. H., R. L. Sutherland, and R. J. Daly. 1999. Signaling pathways and structural domains required for phosphorylation of EMS1/cortactin. Cancer Res. 59:5376-5385.
5. Cannon, J. L., C. M. Labno, G. Bosco, A. Seth, M. H. McGavin, K. A. Siminovitch, M. K. Rosen, and J. K. Burkhardt. 2001. Wasp recruitment to the T cell: APC contact site occurs independently of Cdc42 activation. Immunity 15:249-259.
6. Cantarelli, V. V., A. Takahashi, Y. Akeda, K. Nagayama, and T. Honda. 2000. Interaction of enteropathogenic or enterohemorrhagic Escherichia coli with HeLa cells results in translocation of cortactin to the bacterial adherence site. Infect. Immun. 68:382-386.
7. Carlier, M. F., P. Nioche, I. Broutin-L'Hermite, R. Boujemaa, C. Le Clainche, C. Egile, C. Garbay, A. Ducruix, P. Sansonetti, and D. Pantaloni. 2000. GRB2 links signaling to actin assembly by enhancing interaction of neural Wiskott-Aldrich syndrome protein (N-WASp) with actin-related protein (ARP2/3) complex. J. Biol. Chem. 275:21946-21952.
8. Cinek, T., and V. Horejsi. 1992. The nature of large noncovalent complexes containing glycosyl-phosphatidylinositol-anchored membrane glycoproteins and protein tyrosine kinases. J. Immunol. 149:2262-2270.
9. Derry, J. M., H. D. Ochs, and U. Francke. 1994. Isolation of a novel gene mutated in Wiskott-Aldrich syndrome. Cell 79:922-644.
10. Du, Y., S. A. Weed, W. C. Xiong, T. D. Marshall, and J. T. Parsons. 1998. Identification of a novel cortactin SH3 domain-binding protein and its localization to growth cones of cultured neurons. Mol. Cell. Biol. 18:5838-5851.
11. Dudek, S. M., K. G. Birukov, X. Zhan, and J. G. Garcia. 2002. Novel interaction of cortactin with endothelial cell myosin light chain kinase. Biochem. Biophys. Res. Commun. 298:511-519.
12. Frischknecht, F., S. Cudmore, V. Moreau, I. Reckmann, S. Rottger, and M. Way. 1999. Tyrosine phosphorylation is required for actin-based motility of vaccinia but not Listeria or Shigella. Curr. Biol. 9:89-92.
13. Fukuoka, M., S. Suetsugu, H. Miki, K. Fukami, T. Endo, and T. Takenawa. 2001. A novel neural Wiskott-Aldrich syndrome protein (N-WASP) binding protein, WISH, induces Arp2/3 complex activation independent of Cdc42. J. Cell Biol. 152:471-482.
14. Gallet, C., J. P. Rosa, A. Habib, M. Lebret, S. Levy-Toledano, and J. Maclouf. 1999. Tyrosine phosphorylation of cortactin associated with Syk accompanies thromboxane analogue-induced platelet shape change. J. Biol. Chem. 274:23610-23616.
15. Grakoui, A., S. K. Bromley, C. Sumen, M. M. Davis, A. S. Shaw, P. M. Allen, and M. L. Dustin. 1999. The immunological synapse: a molecular machine controlling T cell activation. Science 285:221-227.
16. Gross, B. S., J. I. Wilde, L. Quek, H. Chapel, D. L. Nelson, and S. P. Watson. 1999. Regulation and function of WASp in platelets by the collagen receptor, glycoprotein VI. Blood 94:4166-4176.
17. Head, J. A., D. Jiang, M. Li, L. J. Zorn, E. M. Schaefer, J. T. Parsons, and S. A. Weed. 2003. Cortactin tyrosine phosphorylation requires rac1 activity and association with the cortical actin cytoskeleton. Mol. Biol. Cell 14:3216-3229.
18. 2 of Wiskott-Aldrich syndrome protein (WASp) stimulates actin nucleation by Arp2/3 complex. J. Cell Biol. 150:1311-1320.
19. Higgs, H. N., and T. D. Pollard. 2001. Regulation of actin filament network formation through ARP2/3 complex: activation by a diverse array of proteins. Annu. Rev. Biochem. 70:649-676.
20. Huang, C., J. Liu, C. C. Haudenschild, and X. Zhan. 1998. The role of tyrosine phosphorylation of cortactin in the locomotion of endothelial cells. J. Biol. Chem. 273:25770-25776.
21. Huang, C., Y. Ni, T. Wang, Y. Gao, C. C. Haudenschild, and X. Zhan. 1997. Down-regulation of the filamentous actin cross-linking activity of cortactin by Src-mediated tyrosine phosphorylation. J. Biol. Chem. 272:13911-13915.
22. Huang, C., N. N. Tandon, N. J. Greco, Y. Ni, T. Wang, and X. Zhan. 1997. Proteolysis of platelet cortactin by calpain. J. Biol. Chem. 272:19248-19252.
23. Kawai, S., M. Minegishi, Y. Ohashi, Y. Sasahara, S. Kumaki, T. Konno, H. Miki, J. Derry, S. Nonoyama, T. Miyawaki, K. Horibe, N. Tachibana, E. Kudoh, Y. Yoshimura, Y. Izumikawa, M. Sako, and S. Tsuchiya. 2002. Flow cytometric determination of intracytoplasmic Wiskott-Aldrich syndrome protein in peripheral blood lymphocyte subpopulations. J. Immunol. Methods 260:195-205.
24. Kim, A. S., L. T. Kakalis, N. Abdul-Manan, G. A. Liu, and M. K. Rosen. 2000. Autoinhibition and activation mechanisms of the Wiskott-Aldrich syndrome protein. Nature 404:151-158.
25. Kim, L., and T. W. Wong. 1998. Growth factor-dependent phosphorylation of the actin-binding protein cortactin is mediated by the cytoplasmic tyrosine kinase FER. J. Biol. Chem. 273:23542-23548.
26. Kinley, A. W., S. A. Weed, A. M. Weaver, A. V. Karginov, E. Bissonette, J. A. Cooper, and J. T. Parsons. 2003. Cortactin interacts with WIP in regulating Arp2/3 activation and membrane protrusion. Curr. Biol. 13:384-393.
27. Kinnunen, T., M. Kaksonen, J. Saarinen, N. Kalkkinen, H. B. Peng, and H. Rauvala. 1998. Cortactin-Src kinase signaling pathway is involved in N-syndecan-dependent neurite outgrowth. J. Biol. Chem. 273:10702-10708.
28. Kitamura, D., H. Kaneko, Y. Miyagoe, T. Ariyasu, and T. Watanabe. 1989. Isolation and characterization of a novel human gene expressed specifically in the cells of hematopoietic lineage. Nucleic Acids Res. 17:9367-9379.
29. Kozma, R., S. Ahmed, A. Best, and L. Lim. 1995. The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol. Cell. Biol. 15:1942-1952.
30. Kreishman-Deltrick, M., and M. K. Rosen. 2002. Ignition of a cellular machine. Nat. Cell Biol. 4:E31-E33.
31. Lagarkova, M. A., V. E. Boitchenko, A. A. Mescheryakov, U. A. Kashkarova, and S. A. Nedospasov. 2000. Human cortactin as putative cancer antigen. Oncogene 19:5204-5207.
32. Li, Y., M. Tondravi, J. Liu, E. Smith, C. C. Haudenschild, M. Kaczmarek, and X. Zhan. 2001. Cortactin potentiates bone metastasis of breast cancer cells. Cancer Res. 61:6906-6911.
33. Machesky, L. M., S. J. Atkinson, C. Ampe, J. Vandekerckhove, and T. D. Pollard. 1994. Purification of a cortical complex containing two unconventional actins from Acanthamoeba by affinity chromatography on profilin-agarose. J. Cell Biol. 127:107-115.
34. Machesky, L. M., and R. H. Insall. 1998. Scar1 and the related Wiskott-Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex. Curr. Biol. 8:1347-1356.
35. Marchand, J. B., D. A. Kaiser, T. D. Pollard, and H. N. Higgs. 2001. Interaction of WASP/Scar proteins with actin and vertebrate Arp2/3 complex. Nat. Cell Biol. 3:76-82.
36. Martinez-Quiles, N., R. Rohatgi, I. M. Anton, M. Medina, S. P. Saville, H. Miki, H. Yamaguchi, T. Takenawa, J. H. Hartwig, R. S. Geha, and N. Ramesh. 2001. WIP regulates N-WASP-mediated actin polymerization and filopodium formation. Nat. Cell Biol. 3:484-491.
37. Miki, H., K. Miura, and T. Takenawa. 1996. N-WASP, a novel actin-depolymerizing protein, regulates the cortical cytoskeletal rearrangement in a PIP2-dependent manner downstream of tyrosine kinases. EMBO J. 15:5326-5335.
38. Miki, H., S. Suetsugu, and T. Takenawa. 1998. WAVE, a novel WASP-family protein involved in actin reorganization induced by Rac. EMBO J. 17:6932-6941.
39. Mizutani, K., H. Miki, H. He, H. Maruta, and T. Takenawa. 2002. Essential role of neural Wiskott-Aldrich syndrome protein in podosome formation and degradation of extracellular matrix in src-transformed fibroblasts. Cancer Res. 62:669-674.
40. Mullins, R. D., and L. M. Machesky. 2000. Actin assembly mediated by Arp2/3 complex and WASP family proteins. Methods Enzymol. 325:214-237.
41. Nakagawa, H., H. Miki, M. Ito, K. Ohashi, T. Takenawa, and S. Miyamoto. 2001. N-WASP, WAVE and Mena play different roles in the organization of actin cytoskeleton in lamellipodia. J. Cell Sci. 114:1555-1565.
42. Nobes, C. D., and A. Hall. 1995. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81:53-62.
43. Ramesh, N., I. M. Anton, J. H. Hartwig, and R. S. Geha. 1997. WIP, a protein associated with Wiskott-Aldrich syndrome protein, induces actin polymerization and redistribution in lymphoid cells. Proc. Natl. Acad. Sci. USA 94:14671-14676.
44. Ren, R., B. J. Mayer, P. Cicchetti, and D. Baltimore. 1993. Identification of a ten-amino acid proline-rich SH3 binding site. Science 259:1157-1161.
45. Rivero-Lezcano, O. M., A. Marcilla, J. H. Sameshima, and K. C. Robbins. 1995. Wiskott-Aldrich syndrome protein physically associates with Nck through Src homology 3 domains. Mol. Cell. Biol. 15:5725-5731.
46. Robinson, R. C., K. Turbedsky, D. A. Kaiser, J. B. Marchand, H. N. Higgs, S. Choe, and T. D. Pollard. 2001. Crystal structure of Arp2/3 complex. Science 294:1679-1684.
47. Rohatgi, R., H. Y. Ho, and M. W. Kirschner. 2000. Mechanism of N-WASP activation by CDC42 and phosphatidylinositol 4,5-bisphosphate. J. Cell Biol. 150:1299-1310.
48. Rohatgi, R., L. Ma, H. Miki, M. Lopez, T. Kirchhausen, T. Takenawa, and M. W. Kirschner. 1999. The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97:221-231.
49. Rohatgi, R., P. Nollau, H. Y. Ho, M. W. Kirschner, and B. J. Mayer. 2001. Nck and phosphatidylinositol 4,5-bisphosphate synergistically activate actin polymerization through the N-WASP-Arp2/3 pathway. J. Biol. Chem. 276:26448-26452.
50. Schafer, D. A., S. A. Weed, D. Binns, A. V. Karginov, J. T. Parsons, and J. A. Cooper. 2002. Dynamin2 and cortactin regulate actin assembly and filament organization. Curr. Biol. 12:1852-1857.
51. Selbach, M., S. Moese, R. Hurwitz, C. R. Hauck, T. F. Meyer, and S. Backert. 2003. The Helicobacter pylori CagA protein induces cortactin dephosphorylation and actin rearrangement by c-Src inactivation. EMBO J. 22:515-528.
52. She, H. Y., S. Rockow, J. Tang, R. Nishimura, E. Y. Skolnik, M. Chen, B. Margolis, and W. Li. 1997. Wiskott-Aldrich syndrome protein is associated with the adapter protein Grb2 and the epidermal growth factor receptor in living cells. Mol. Biol. Cell 8:1709-1721.
53. Snapper, S. B., F. S. Rosen, E. Mizoguchi, P. Cohen, W. Khan, C. H. Liu, T. L. Hagemann, S. P. Kwan, R. Ferrini, L. Davidson, A. K. Bhan, and F. W. Alt. 1998. Wiskott-Aldrich syndrome protein-deficient mice reveal a role for WASP in T but not B cell activation. Immunity 9:81-91.
54. Snapper, S. B., F. Takeshima, I. Anton, C. H. Liu, S. M. Thomas, D. Nguyen, D. Dudley, H. Fraser, D. Purich, M. Lopez-Ilasaca, C. Klein, L. Davidson, R. Bronson, R. C. Mulligan, F. Southwick, R. Geha, M. B. Goldberg, F. S. Rosen, J. H. Hartwig, and F. W. Alt. 2001. N-WASP deficiency reveals distinct pathways for cell surface projections and microbial actin-based motility. Nat. Cell Biol. 3:897-904.
55. Tilghman, R. W., and R. L. Hoover. 2002. The Src-cortactin pathway is required for clustering of E-selectin and ICAM-1 in endothelial cells. FASEB J. 16:1257-1259.
56. Timpson, P., G. E. Jones, M. C. Frame, and V. G. Brunton. 2001. Coordination of cell polarization and migration by the Rho family GTPases requires Src tyrosine kinase activity. Curr. Biol. 11:1836-1846.
57. Uruno, T., J. Liu, P. Zhang, Y. Fan, C. Egile, R. Li, S. C. Mueller, and X. Zhan. 2001. Activation of Arp2/3 complex-mediated actin polymerization by cortactin. Nat. Cell Biol. 3:259-266.
58. Vidal, C., B. Geny, J. Melle, M. Jandrot-Perrus, and M. Fontenay-Roupie. 2002. Cdc42/Rac1-dependent activation of the p21-activated kinase (PAK) regulates human platelet lamellipodia spreading: implication of the cortical-actin binding protein cortactin. Blood 100:4462-4469.
59. Volkman, B. F., K. E. Prehoda, J. A. Scott, F. C. Peterson, and W. A. Lim. 2002. Structure of the N-WASP EVH1 domain-WIP complex: insight into the molecular basis of Wiskott-Aldrich syndrome. Cell 111:565-576.
60. Weaver, A., J. Heuser, A. Karginov, W. Lee, J. Parsons, and J. Cooper. 2002. Interaction of cortactin and N-wasp with arp2/3 complex. Curr. Biol. 12:1270.
61. Weaver, A. M., A. V. Karginov, A. W. Kinley, S. A. Weed, Y. Li, J. T. Parsons, and J. A. Cooper. 2001. Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr. Biol. 11:370-374.
62. Weed, S. A., Y. Du, and J. T. Parsons. 1998. Translocation of cortactin to the cell periphery is mediated by the small GTPase Rac1. J. Cell Sci. 111:2433-2443.
63. Weed, S. A., A. V. Karginov, D. A. Schafer, A. M. Weaver, A. W. Kinley, J. A. Cooper, and J. T. Parsons. 2000. Cortactin localization to sites of actin assembly in lamellipodia requires interactions with F-actin and the Arp2/3 complex. J. Cell Biol. 151:29-40.
64. Weed, S. A., and J. T. Parsons. 2001. Cortactin: coupling membrane dynamics to cortical actin assembly. Oncogene 20:6418-6434.
65. Wu, H., and J. T. Parsons. 1993. Cortactin, an 80/85-kilodalton pp60src substrate, is a filamentous actin-binding protein enriched in the cell cortex. J. Cell Biol. 120:1417-1426.
66. Wu, H., A. B. Reynolds, S. B. Kanner, R. R. Vines, and J. T. Parsons. 1991. Identification and characterization of a novel cytoskeleton-associated pp60src substrate. Mol. Cell. Biol. 11:5113-5124.
67. Yaffe, M. B., G. G. Leparc, J. Lai, T. Obata, S. Volinia, and L. C. Cantley. 2001. A motif-based profile scanning approach for genome-wide prediction of signaling pathways. Nat. Biotechnol. 19:348-353.