Focal adhesion kinase is required for the spatial organization of the leading edge in migrating cells

Journal of Cell Science

Volumn 118, Issue 12, 2005, Pages 2613-2623

  Tilghman, Robert W ^a   Slack Davis, Jill K ^a   Sergina, Natalia ^a   Martin, Karen H ^a   Iwanicki, Marcin ^a   Hershey, E Daniel ^a   Beggs, Hilary E ^b   Reichardt, Louis F ^b   Parsons, J Thomas ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell migration; Cell polarity; FAK; Lamellipodium

Indexed keywords

CORTACTIN; FOCAL ADHESION KINASE; RAC PROTEIN; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; CELL ACTIVATION; CELL ASSAY; CELL MEMBRANE; CELL MIGRATION; CELL SPREADING; CELL STRUCTURE; CELL TYPE; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYO; FIBROBLAST; INHIBITION KINETICS; LAMELLIPODIUM; MOUSE; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; WILD TYPE; WOUND HEALING;

ANIMALS; CELL LINE; CELL MOVEMENT; CELL POLARITY; CELL SHAPE; FIBROBLASTS; FIBRONECTINS; FOCAL ADHESION KINASE 1; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; GENE DELETION; GENE EXPRESSION REGULATION; GOLGI APPARATUS; MICE; PROTEIN-TYROSINE KINASES; PSEUDOPODIA; RATS; RNA, SMALL INTERFERING; TIME FACTORS;

ANIMALIA;

EID: 21644483424     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02380     Document Type: Article

References (39)

1. Abassi, Y. A. and Vuori, K. (2002). Tyrosine 221 in Crk regulates adhesion-dependent membrane localization of Crk and Rac and activation of Rac signaling. EMBO J. 21, 4571-4582.
2. Beggs, H. E., Schahin-Reed, D., Zang, K., Goebbels, S., Nave, K. A., Gorski, J., Jones, K. R., Sretavan, D. and Reichardt, L. F. (2003). FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron 40, 501-514.
3. Beningo, K. A., Dembo, M., Kaverina, I., Small, J. V. and Wang, Y. L. (2001). Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. J. Cell Biol. 153, 881-888.
4. Brennan, H., Smith, S. and Stoker, A. (1999). Phosphotyrosine signalling as a regulator of neural crest cell adhesion and motility. Cell Motil. Cytoskeleton 42, 101-113.
5. Cary, L. A., Han, D. C., Polte, T. R., Hanks, S. K. and Guan, J. L. (1998). Identification of p130Cas as a mediator of focal adhesion kinase-promoted cell migration. J. Cell Biol. 140, 211-221.
6. Chung, C. Y., Funamoto, S. and Firtel, R. A. (2001). Signaling pathways controlling cell polarity and chemotaxis. Trends Biochem. Sci. 26, 557-566.
7. Dormann, D. and Weijer, C. J. (2003). Chemotactic cell movement during development. Curr. Opin. Genet. Dev. 13, 358-364.
8. Fincham, V. J. and Frame, M. C. (1998). The catalytic activity of Src is dispensable for translocation to focal adhesions but controls the turnover of these structures during cell motility. EMBO J. 17, 81-92.
9. Hood, J. D. and Cheresh, D. A. (2002). Role of integrins in cell invasion and migration. Nat. Rev. Cancer 2, 91-100.
10. Huang, C., Jacobson, K. and Schaller, M. D. (2004). A role for JNK-paxillin signaling in cell migration. Cell Cycle 3, 4-6.
11. Ilic, D., Furuta, Y., Kanazawa, S., Takeda, N., Sobue, K., Nakatsuji, N., Nomura, S., Fujimoto, J., Okada, M. and Yamamoto, T. (1995a). Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377, 539-544.
12. Ilic, D., Furuta, Y., Suda, T., Atsumi, T., Fujimoto, J., Ikawa, Y., Yamamoto, T. and Aizawa, S. (1995b). Focal adhesion kinase is not essential for in vitro and in vivo differentiation of ES cells. Biochem. Biophys. Res. Commun.. 209, 300-309.
13. Kupfer, A., Louvard, D. and Singer, S. J. (1982). Polarization of the Golgi apparatus and the microtubule-organizing center in cultured fibroblasts at the edge of an experimental wound. Proc. Natl. Acad. Sci. USA 79, 2603-2607.
14. Lu, M., Kinchen, J. M., Rossman, K. L., Grimsley, C., deBakker, C., Brugnera, E., Tosello-Trampont, A. C., Haney, L. B., Klingele, D., Sondek, J. et al. (2004). PH domain of ELMO functions in trans to regulate Rac activation via Dock180. Nat. Struct. Mol. Biol. 11, 756-762.
15. Manes, S., Mira, E., Gomez-Mouton, C., Zhao, Z. J., Lacalle, R. A. and Martinez, A. C. (1999). Concerted activity of tyrosine phosphatase SHP-2 and focal adhesion kinase in regulation of cell motility. Mol. Cell Biol. 19, 3125-3135.
16. Nobes, C. D. and Hall, A. (1999). Rho GTPases control polarity, protrusion, and adhesion during cell movement. J. Cell Biol. 144, 1235-1244.
17. Owen, J. D., Ruest, P. J., Fry, D. W. and Hanks, S. K. (1999). Induced focal adhesion kinase (FAK) expression in FAK-null cells enhances cell spreading and migration requiring both auto- and activation loop phosphorylation sites and inhibits adhesion-dependent tyrosine phosphorylation of Pyk2. Mol. Cell. Biol. 19, 4806-4818.
18. Parsons, J. T. (2003). Focal adhesion kinase: the first ten years. J. Cell Sci. 116, 1409-1416.
19. Petch, L. A., Bockholt, S. M., Bouton, A., Parsons, J. T. and Burridge, K. (1995). Adhesion-induced tyrosine phosphorylation of the p130 src substrate. J. Cell Sci. 108, 1371-1379.
20. Ren, X. D., Kiosses, W. B., Sieg, D. J., Otey, C. A., Schlaepfer, D. D. and Schwartz, M. A. (2000). Focal adhesion kinase suppresses Rho activity to promote focal adhesion turnover. J. Cell Sci. 113, 3673-3678.
21. Ridley, A. J., Paterson, H. F., Johnston, C. L., Diekmann, D. and Hall, A. (1992). The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70, 401-410.
22. Ridley, A. J., Schwartz, M. A., Burridge, K., Firtel, R. A., Ginsberg, M. H., Borisy, G., Parsons, J. T. and Horwitz, A. R. (2003). Cell migration: integrating signals from front to back. Science 302, 1704-1709.
23. 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.
24. Sastry, S. K. and Burridge, K. (2000). Focal adhesions: a nexus for intracellular signaling and cytoskeletal dynamics. Exp. Cell Res. 261, 25-36.
25. Schaller, M. D., Hildebrand, J. D., Shannon, J. D., Fox, J. W., Vines, R. R. and Parsons, J. T. (1994). Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src. Mol. Cell. Biol. 14, 1680-1688.
26. Schaller, M. D., Hildebrand, J. D. and Parsons, J. T. (1999). Complex formation with focal adhesion kinase: A mechanism to regulate activity and subcellular localization of Src kinases. Mol. Cell. Biol. 10, 3489-3505.
27. Schmoranzer, J., Kreitzer, G. and Simon, S. M. (2003). Migrating fibroblasts perform polarized, microtubule-dependent exocytosis towards the leading edge. J. Cell Sci. 116, 4513-4519.
28. Sieg, D. J., Hauck, C. R. and Schlaepfer, D. D. (1999). Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J. Cell Sci. 112, 2677-2691.
29. Sieg, D. J., Hauck, C. R., Ilic, D., Klingbeil, C. K., Schaefer, E., Damsky, C. H. and Schlaepfer, D. D. (2000). FAK integrates growth-factor and integrin signals to promote cell migration. Nat. Cell. Biol. 2, 249-256.
30. Small, J. V., Stradal, T., Vignal, E. and Rottner, K. (2002). The lamellipodium: where motility begins. Trends Cell Biol. 12, 112-120.
31. Wakatsuki, T., Wysolmerski, R. B. and Elson, E. L. (2003). Mechanics of cell spreading: role of myosin II. J. Cell Sci. 116, 1617-1625.
32. Wang, H. B., Dembo, M., Hanks, S. K. and Wang, Y. (2001). Focal adhesion kinase is involved in mechanosensing during fibroblast migration. Proc. Natl. Acad. Sci. USA 98, 11295-11300.
33. Weaver, A. M., Karginov, A. V., Kinley, A. W., Weed, S. A., Li, Y., Parsons, J. T. and Cooper, J. A. (2001). Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr. Biol. 11, 370-374.
34. Webb, D. J., Parsons, J. T. and Horwitz, A. F. (2002). Adhesion assembly, disassembly and turnover in migrating cells - over and over and over again. Nat. Cell. Biol. 4, E97-E100.
35. Webb, D. J., Donais, K., Whitmore, L. A., Thomas, S. M., Turner, C. E., Parsons, J. T. and Horwitz, A. F. (2004). FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat. Cell. Biol. 6, 154-161.
36. Weed, S. A., Du, Y. and Parsons, J. T. (1998). Translocation of cortactin to the cell periphery is mediated by the small GTPase Rac1. J. Cell Sci. 111, 2433-2443.
37. Weed, S. A., Karginov, A. V., Schafer, D. A., Weaver, A. M., Kinley, A. W., Cooper, J. A. and Parsons, J. T. (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.
38. Wu, H., Reynolds, A. B., Kanner, S. B., Vines, R. R. and Parsons, J. T. (1991). Identification and characterization of a novel cytoskeleton-associated pp60src substrate. Mol. Cell. Biol. 11, 5113-5124.
39. Yano, H., Mazaki, Y., Kurokawa, K., Hanks, S. K., Matsuda, M. and Sabe, H. (2004). Roles played by a subset of integrin signaling molecules in cadherin-based cell-cell adhesion. J. Cell Biol. 166, 283-295.