N-WASP-directed actin polymerization activates Cas phosphorylation and lamellipodium spreading

Journal of Cell Science

Volumn 127, Issue 7, 2014, Pages 1394-1405

  Zhang, Xian ^a   Moore, Simon W ^a   Iskratsch, Thomas ^a   Sheetz, Michael P ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Actin dynamics; BCAR1; Cas; Crk associatied substrate; FAK; Focal adhesion kinase; p130Cas; SFK; Src family kinase

Indexed keywords

CELLULAR APOPTOSIS SUSCEPTIBILITY PROTEIN; FOCAL ADHESION KINASE; INTEGRIN; MYOSIN; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PROTEIN TYROSINE KINASE; ACTIN; CRK ASSOCIATED SUBSTRATE PROTEIN; WASL PROTEIN, MOUSE;

ACTIN POLYMERIZATION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ANCHORAGE; CELL MIGRATION; CELL SPREADING; COMPLEX FORMATION; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVATION; LAMELLIPODIUM; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; ACTIN FILAMENT; ANIMAL; CELL ADHESION; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; POLYMERIZATION; PROTEIN TERTIARY STRUCTURE; PSEUDOPODIUM; SIGNAL TRANSDUCTION;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; CELL ADHESION; CRK-ASSOCIATED SUBSTRATE PROTEIN; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; MICE; PHOSPHORYLATION; POLYMERIZATION; PROTEIN STRUCTURE, TERTIARY; PSEUDOPODIA; SIGNAL TRANSDUCTION; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

EID: 84897386482     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.134692     Document Type: Article

References (55)

1. Albiges-Rizo, C., Destaing, O., Fourcade, B., Planus, E. and Block, M. R. (2009). Actin machinery and mechanosensitivity in invadopodia, podosomes and focal adhesions. J. Cell Sci. 122, 3037-3049.
2. Alexander, N. R., Branch, K. M., Parekh, A., Clark, E. S., Iwueke, I. C., Guelcher, S. A. and Weaver, A. M. (2008). Extracellular matrix rigidity promotes invadopodia activity. Curr. Biol. 18, 1295-1299.
3. Arias-Salgado, E. G., Lizano, S., Sarkar, S., Brugge, J. S., Ginsberg, M. H. and Shattil, S. J. (2003). Src kinase activation by direct interaction with the integrin beta cytoplasmic domain. Proc. Natl. Acad. Sci. USA 100, 13298-13302.
4. Auvinen, M., Paasinen-Sohns, A., Hirai, H., Andersson, L. C. and Hölttä , E. (1995). Ornithine decarboxylase- and ras-induced cell transformations: reversal by protein tyrosine kinase inhibitors and role of pp130CAS. Mol. Cell. Biol. 15, 6513-6525.
5. Boettner, B. and Van Aelst, L. (2009). Control of cell adhesion dynamics by Rap1 signaling. Curr. Opin. Cell Biol. 21, 684-693.
6. Burridge, K. and Wennerberg, K. (2004). Rho and Rac take center stage. Cell 116, 167-179.
7. de Oliveira, C. A. and Mantovani, B. (1988). Latrunculin A is a potent inhibitor of phagocytosis by macrophages. Life Sci. 43, 1825-1830.
8. Defilippi, P., Di Stefano, P. and Cabodi, S. (2006). p130Cas: a versatile scaffold in signaling networks. Trends Cell Biol. 16, 257-263.
9. Felsenfeld, D. P., Schwartzberg, P. L., Venegas, A., Tse, R. and Sheetz, M. P.(1999). Selective regulation of integrin-cytoskeleton interactions by the tyrosine kinase Src. Nat. Cell Biol. 1, 200-206.
10. Fonseca, P. M., Shin, N. Y., Brábek, J., Ryzhova, L., Wu, J. and Hanks, S. K. (2004). Regulation and localization of CAS substrate domain tyrosine phosphorylation. Cell. Signal. 16, 621-629.
11. Geiger, B. (2006). A role for p130Cas in mechanotransduction. Cell 127, 879-881.
12. Giannone, G., Dubin-Thaler, B. J., Döbereiner, H. G., Kieffer, N., Bresnick, A.R. and Sheetz, M. P. (2004). Periodic lamellipodial contractions correlate with rearward actin waves. Cell 116, 431-443.
13. Hamamura, K., Tsuji, M., Ohkawa, Y., Nakashima, H., Miyazaki, S., Urano, T., Yamamoto, N., Ueda, M., Furukawa, K. and Furukawa, K. (2008). Focal adhesion kinase as well as p130Cas and paxillin is crucially involved in the enhanced malignant properties under expression of ganglioside GD3 in melanoma cells. Biochim. Biophys. Acta 1780, 513-519.
14. Han, J., Lim, C. J., Watanabe, N., Soriani, A., Ratnikov, B., Calderwood, D. A., Puzon-McLaughlin, W., Lafuente, E. M., Boussiotis, V. A., Shattil, S. J. et al. (2006). Reconstructing and deconstructing agonist-induced activation of integrin alphaIIbbeta3. Curr. Biol. 16, 1796-1806.
15. Harte, M. T., Hildebrand, J. D., Burnham, M. R., Bouton, A. H. and Parsons, J. T. (1996). p130Cas, a substrate associated with v-Src and v-Crk, localizes to focal adhesions and binds to focal adhesion kinase. J. Biol. Chem. 271, 13649- 13655.
16. Honda, H., Nakamoto, T., Sakai, R. and Hirai, H. (1999). p130(Cas), an assembling molecule of actin filaments, promotes cell movement, cell migration, and cell spreading in fibroblasts. Biochem. Biophys. Res. Commun. 262, 25-30.
17. Huveneers, S., van den Bout, I., Sonneveld, P., Sancho, A., Sonnenberg, A.and Danen, E. H. (2007). Integrin alpha v beta 3 controls activity and oncogenic potential of primed c-Src. Cancer Res. 67, 2693-2700.
18. Jiang, G., Huang, A. H., Cai, Y., Tanase, M. and Sheetz, M. P. (2006). Rigidity sensing at the leading edge through alphavbeta3 integrins and RPTPalpha.Biophys. J. 90, 1804-1809.
19. Klemke, R. L., Leng, J., Molander, R., Brooks, P. C., Vuori, K. and Cheresh, D. A. (1998). CAS/Crk coupling serves as a ''molecular switch'' for induction of cell migration. J. Cell Biol. 140, 961-972.
20. Kostic, A. and Sheetz, M. P. (2006). Fibronectin rigidity response through Fyn and p130Cas recruitment to the leading edge. Mol. Biol. Cell 17, 2684- 2695.
21. Liu, G., Li, W., Gao, X., Li, X., Jürgensen, C., Park, H. T., Shin, N. Y., Yu, J., He, M. L., Hanks, S. K. et al. (2007). p130CAS is required for netrin signaling and commissural axon guidance. J. Neurosci. 27, 957-968.
22. Merrifield, C. J., Qualmann, B., Kessels, M. M. and Almers, W. (2004). Neural Wiskott Aldrich Syndrome Protein (N-WASP) and the Arp2/3 complex are recruited to sites of clathrin-mediated endocytosis in cultured fibroblasts. Eur. J. Cell Biol. 83, 13-18.
23. Michael, K. E., Dumbauld, D. W., Burns, K. L., Hanks, S. K. and García, A. J. (2009). Focal adhesion kinase modulates cell adhesion strengthening via integrin activation. Mol. Biol. Cell 20, 2508-2519.
24. Nakamoto, T., Sakai, R., Ozawa, K., Yazaki, Y. and Hirai, H. (1996). Direct binding of C-terminal region of p130Cas to SH2 and SH3 domains of Src kinase. J. Biol. Chem. 271, 8959-8965.
25. Nakamoto, T., Sakai, R., Honda, H., Ogawa, S., Ueno, H., Suzuki, T., Aizawa, S., Yazaki, Y. and Hirai, H. (1997). Requirements for localization of p130cas to focal adhesions. Mol. Cell. Biol. 17, 3884-3897.
26. O'Neill, G. M., Fashena, S. J. and Golemis, E. A. (2000). Integrin signalling: a new Cas(t) of characters enters the stage. Trends Cell Biol. 10, 111-119.
27. Peterson, J. R., Bickford, L. C., Morgan, D., Kim, A. S., Ouerfelli, O., Kirschner, M. W. and Rosen, M. K. (2004). Chemical inhibition of N-WASP by stabilization of a native autoinhibited conformation. Nat. Struct. Mol. Biol. 11, 747-755.
28. Polte, T. R. and Hanks, S. K. (1995). Interaction between focal adhesion kinase and Crk-associated tyrosine kinase substrate p130Cas. Proc. Natl. Acad. Sci.USA 92, 10678-10682.
29. Poullet, P., Gautreau, A., Kadaré , G., Girault, J. A., Louvard, D. and Arpin, M.(2001). Ezrin interacts with focal adhesion kinase and induces its activation independently of cell-matrix adhesion. J. Biol. Chem. 276, 37686-37691.
30. Priddle, H., Hemmings, L., Monkley, S., Woods, A., Patel, B., Sutton, D., Dunn, G. A., Zicha, D. and Critchley, D. R. (1998). Disruption of the talin gene compromises focal adhesion assembly in undifferentiated but not differentiated embryonic stem cells. J. Cell Biol. 142, 1121-1133.
31. Reiske, H. R., Kao, S. C., Cary, L. A., Guan, J. L., Lai, J. F. and Chen, H. C.(1999). Requirement of phosphatidylinositol 3-kinase in focal adhesion kinasepromoted cell migration. J. Biol. Chem. 274, 12361-12366.
32. Richardson, A. and Parsons, T. (1996). A mechanism for regulation of the adhesion-associated proteintyrosine kinase pp125FAK. Nature 380, 538- 540.
33. Roca-Cusachs, P., Iskratsch, T. and Sheetz, M. P. (2012). Finding the weakest link: exploring integrin-mediated mechanical molecular pathways. J. Cell Sci.125, 3025-3038.
34. Ruest, P. J., Shin, N. Y., Polte, T. R., Zhang, X. and Hanks, S. K. (2001).Mechanisms of CAS substrate domain tyrosine phosphorylation by FAK and Src. Mol. Cell. Biol. 21, 7641-7652.
35. Sakai, R., Nakamoto, T., Ozawa, K., Aizawa, S. and Hirai, H. (1997).Characterization of the kinase activity essential for tyrosine phosphorylation of p130Cas in fibroblasts. Oncogene 14, 1419-1426.
36. Sanders, M. A. and Basson, M. D. (2005). p130cas but not paxillin is essential for Caco-2 intestinal epithelial cell spreading and migration on collagen IV. J. Biol.Chem. 280, 23516-23522.
37. Sanders, M. A. and Basson, M. D. (2008). Collagen IV regulates Caco-2 cell spreading and p130Cas phosphorylation by FAK-dependent and FAKindependent pathways. Biol. Chem. 389, 47-55.
38. Sawada, Y., Tamada, M., Dubin-Thaler, B. J., Cherniavskaya, O., Sakai, R., Tanaka, S. and Sheetz, M. P. (2006). Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell 127, 1015-1026.
39. Serrels, B., Serrels, A., Brunton, V. G., Holt, M., McLean, G. W., Gray, C. H., Jones, G. E. and Frame, M. C. (2007). Focal adhesion kinase controls actin assembly via a FERM-mediated interaction with the Arp2/3 complex. Nat. Cell Biol. 9, 1046-1056.
40. Sharma, A. and Mayer, B. J. (2008). Phosphorylation of p130Cas initiates Rac activation and membrane ruffling. BMC Cell Biol. 9, 50.
41. Shattil, S. J. (2005). Integrins and Src: dynamic duo of adhesion signaling. Trends Cell Biol. 15, 399-403.
42. Shin, N. Y., Dise, R. S., Schneider-Mergener, J., Ritchie, M. D., Kilkenny, D. M.and Hanks, S. K. (2004). Subsets of the major tyrosine phosphorylation sites in Crk-associated substrate (CAS) are sufficient to promote cell migration. J. Biol.Chem. 279, 38331-38337.
43. Slack-Davis, J. K., Martin, K. H., Tilghman, R. W., Iwanicki, M., Ung, E. J., Autry, C., Luzzio, M. J., Cooper, B., Kath, J. C., Roberts, W. G. et al. (2007).Cellular characterization of a novel focal adhesion kinase inhibitor. J. Biol.Chem. 282, 14845-14852.
44. Sturge, J., Hamelin, J. and Jones, G. E. (2002). N-WASP activation by a beta1-integrin-dependent mechanism supports PI3K-independent chemotaxis stimulated by urokinase-type plasminogen activator. J. Cell Sci. 115, 699- 711.
45. Suetsugu, S., Hattori, M., Miki, H., Tezuka, T., Yamamoto, T., Mikoshiba, K. and Takenawa, T. (2002). Sustained activation of N-WASP through phosphorylation is essential for neurite extension. Dev. Cell 3, 645-658.
46. Takenawa, T. and Suetsugu, S. (2007). The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat. Rev. Mol. Cell Biol. 8, 37-48.
47. Tamada, M., Sheetz, M. P. and Sawada, Y. (2004). Activation of a signaling cascade by cytoskeleton stretch. Dev. Cell 7, 709-718.
48. Tanjoni, I., Walsh, C., Uryu, S., Tomar, A., Nam, J. O., Mielgo, A., Lim, S. T., Liang, C., Koenig, M., Sun, C. et al. (2010). PND-1186 FAK inhibitor selectively promotes tumor cell apoptosis in three-dimensional environments. Cancer Biol.Ther. 9, 764-777.
49. Urbanik, E. and Ware, B. R. (1989). Actin filament capping and cleaving activity of cytochalasins B, D, E, and H. Arch. Biochem. Biophys. 269, 181-187.
50. von Wichert, G., Jiang, G., Kostic, A., De Vos, K., Sap, J. and Sheetz, M. P.(2003). RPTP-alpha acts as a transducer of mechanical force on alphav/beta3- integrin-cytoskeleton linkages. J. Cell Biol. 161, 143-153.
51. Vuori, K., Hirai, H., Aizawa, S. and Ruoslahti, E. (1996). Introduction of p130cas signaling complex formation upon integrin-mediated cell adhesion: a role for Src family kinases. Mol. Cell. Biol. 16, 2606-2613.
52. Wei, L., Yang, Y., Zhang, X. and Yu, Q. (2002). Anchorage-independent phosphorylation of p130(Cas) protects lung adenocarcinoma cells from anoikis.J. Cell. Biochem. 87, 439-449.
53. Wu, X., Suetsugu, S., Cooper, L. A., Takenawa, T. and Guan, J. L. (2004). Focal adhesion kinase regulation of N-WASP subcellular localization and function.J. Biol. Chem. 279, 9565-9576.
54. Yu, C. H., Law, J. B., Suryana, M., Low, H. Y. and Sheetz, M. P. (2011). Early integrin binding to Arg-Gly-Asp peptide activates actin polymerization and contractile movement that stimulates outward translocation. Proc. Natl. Acad.Sci. USA 108, 20585-20590.
55. Zhang, X., Jiang, G., Cai, Y., Monkley, S. J., Critchley, D. R. and Sheetz, M. P.(2008). Talin depletion reveals independence of initial cell spreading from integrin activation and traction. Nat. Cell Biol. 10, 1062-1068.