Inhibition of focal adhesion kinase (FAK) signaling in focal adhesions decreases cell motility and proliferation

Molecular Biology of the Cell

Volumn 7, Issue 8, 1996, Pages 1209-1224

  Gilmore, Andrew P ^a   Romer, Lewis H ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MOTILITY; CELL PROLIFERATION; CELL STRAIN 3T3; ENDOTHELIUM CELL; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; MICROINJECTION; NONHUMAN; PRIORITY JOURNAL;

ANIMALIA;

EID: 0029741102     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.7.8.1209     Document Type: Article

References (79)

1. FAK and protein kinase C-δ to focal adhesions. J. Cell Sci. 107, 2033-2045.
2. Bellis, S.L., Miller, J.T., and Turner, C.E. (1995). Characterization of tyrosine phosphorylation of paxillin in vitro by focal adhesion kinase. J. Biol. Chem. 270, 17437-17441.
3. Birge, R.B., Fajardo, J.E., Reichman, C., Shoelson, S.E., Songyang, Z., Cantley, L.C., and Hanafusa, H. (1993). Identification and characterization of a high-affinity interaction between v-crk and tyrosine-phosphorylated paxillin in CT10-transformed fibroblasts. Mol. Cell. Biol. 13, 4648-4656.
4. Bockholt, S.B., and Burridge, K. (1993). Cell spreading on extracellular matrix proteins induces tyrosine phosphorylation of tensin. J. Biol. Chem. 268, 14565-14567.
5. Böhmer, R.-M., Scharf, E., and Assoian, R.K. (1996). Cytoskeletal integrity is required throughout the mitogen stimulation phase of the cell cycle and mediates the anchorage-dependent expression of cyclin D1. Mol. Biol. Cell 7, 101-111.
6. Burridge, K., Fath, K., Kelly, T., Nuckolls, G., and Turner, C. (1988). Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu. Rev. Cell Biol. 4, 487-525.
7. Burridge, K., Petch, L., and Romer, L. (1992a). Signals from focal adhesions. Curr. Biol. 2, 537-539.
8. FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly. J. Cell Biol. 119, 893-903.
9. Chen, H.-C., Appeddu, P.A., Parsons, J.T., Hildebrand, J.D., Schaller, M.D., and Guan, J.-L. (1995). Interaction of focal adhesion kinase with cytoskeletal protein talin. J. Biol. Chem. 270, 16995-16999.
10. Chen, H.-C., and Guan, J.-L. (1994). Association of focal adhesion kinase with phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA 91, 10148-10152.
11. Chen, Q., Kinch, M.S., Lin, T.H., Burridge, K., and Juliano, R.L. (1994). Integrin-mediated cell adhesion activates mitogen-activated protein kinases. J. Biol. Chem. 269, 26602-26605.
12. Chrzanowska-Wodnicka, M., and Burridge, K. (1994). Tyrosine phosphorylation is involved in the reorganization of the actin cytoskeleton in response to serum or LPA stimulation. J. Cell Sci. 107, 3643-3654.
13. Clark, E.A., and Brugge, J.S. (1995). Integrins and signal transduction pathways: the road taken. Science 268, 233-239.
14. Clarke, M.S.F., and McNeil, P.L. (1992). Syringe loading introduces macromolecules into living mammalian cell cytosol. J. Cell Sci. 102, 533-541.
15. Coomber, B.L., and Gotlieb, A.I. (1990). In vitro endothelial wound repair: interaction of cell migration and proliferation. Arteriosclerosis 10, 215-222.
16. DePasquale, J.A., and Izzard, C.S. (1987). Evidence for an actin-containing cytoplasmic precursor of the focal contact and incorporation of vinculin. J. Cell Biol. 105, 2803-2809.
17. DePasquale, J.A., and Izzard, C.S. (1991). Accumulation of talin in nodes at the edges of the lamellipodium and incorporation into adhesion plaques. J. Cell Biol. 113, 1351-1359.
18. Drenckhahn, D., Beckerle, M., Burridge, K., and Otto, J. (1988). Identification and subcellular location of talin in various cell types. Eur. J. Cell Biol. 46, 513-522.
19. Folkman, J., and Moscona, A. (1978). Role of cell shape in growth control. Nature 273, 345-349.
20. Guadagno, T.M., Ohtsubo, M., Roberts, J.M., and Assoian, R.K. (1993). A link between cyclin A expression and adhesion-dependent cell cycle progression. Science 262, 1572-1575.
21. Guan, J.-L., and Shalloway, D. (1992). Regulation of focal adhesion-associated protein tyrosine kinase by cellular adhesion and transformation. Nature 358, 690-692.
22. Guan, J.-L., Trevithick, J.E., and Hynes, R.O. (1991). Fibronectin/integrin interaction induces tyrosine phosphorylation of a 120-kDa protein. Cell Regul. 2, 951-964.
23. Guinebault, C., Payrastre, B., Racaud-Sultan, C., Mazarguil, H., Breton, M., Mauco, G., Plantavid, M., and Chap, H. (1995). Integrin-dependent translocation of phosphoinositide 3-kinase to the cytoskeleton of thrombin-activated platelets involves specific interactions of p85a with actin filaments and focal adhesion kinase. J. Cell Biol. 129, 831-842.
24. Haimovich, B., Lipfert, L., Brugge, J.S., and Shattil, S.J. (1993). Tyrosine phosphorylation and cytoskeletal reorganization in platelets are triggered by interaction of integrin receptors with their immobilized ligands. J. Biol. Chem. 268, 15868-15877.
25. Hanks, S.K., Calalb, M.B., and Patel, S.K. (1992). Focal adhesion protein-tyrosine kinase phosphorylated in response to cell attachment. Proc. Natl. Acad. Sci. USA 89, 8487-8491.
26. Herman, I.M. (1993). Molecular mechanisms regulating the vascular endothelial cell motile response to injury. J. Cardiovasc. Pharmacol. 22, S25-S36.
27. Hildebrand, J.D., Schaller, M.D., and Parsons, J.T. (1993). Identification of sequences required for localization of focal adhesion kinase to focal adhesion. J. Cell Biol. 123, 993-1005.
28. Hildebrand, J.D., Schaller, M.D., and Parsons, J.T. (1995). Paxillin, a tyrosine-phosphorylated focal adhesion-associated protein binds to the carboxy-terminal domains of focal adhesion kinase. Mol. Biol. Cell 6, 637-647.
29. Horwitz, A., Duggan, K., Buck, C., Beckerle, M.C., and Burridge, K. (1986). Interaction of the plasma-membrane fibronectin receptor with talin - a transmembrane linkage. Nature 320, 531-533.
30. Hynes, R.O. (1992). Integrins: versatility, modulation, and signalling in cell adhesion. Cell 69, 11-25.
31. Ilic, D., Furuta, Y., Kanazawa, S., Takeda, N., Sobue, K., Nakatsuji, N., Nomura, S., Fujimoto, J., Okada, M., Yamamoto, T., and Aizawa, S. (1995). Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377, 539-544.
32. Ingber, D.E., Prusty, D., Frangioni, J.V., Cragoe, E.J., Jr., Lechene, C., and Schwartz, M.A. (1990). Control of intracellular pH and growth by fibronectin in capillary endothelial cells. J. Cell Biol. 110, 1803-1811.
33. Izzard, C.S., and Lochner, L.R. (1980). Formation of cell-to-substrate contacts in fibroblast motility. J. Cell Sci. 42, 81-116.
34. Juliano, R.L., and Haskill, S. (1993). Signal transduction from ECM. J. Cell Biol. 120, 577-585.
35. Kapron-Bras, C., Fitz-Gibbon, L., Jeevaratnam, P., Wilkins, J., and Dedhar, S. (1993). Stimulation of tyrosine phosphorylation and accumulation of GTP-bound p21ras upon antibody-mediated alpha2beta1 integrin activation in T-lymphoblastic cells. J. Biol. Chem. 268, 20701-20704.
36. Kornberg, L., Earp, H.S., Parsons, J.T., Schaller, M., and Juliano, R.L. (1992). Cell adhesion or integrin clustering increases phosphorylation of a focal adhesion-associated tyrosine kinase. J. Biol. Chem. 267, 23439-23442.
37. Kornberg, L.J., Earp, H.S., Turner, C.E., Prockop, C., and Juliano, R.L. (1991). Signal transduction by integrins: increased tyrosine phosphorylation caused by clustering of beta1 integrins. Proc. Natl. Acad. Sci. USA 88, 8392-8396.
38. Kumagai, N., Morii, N., Fujisawa, K., Nemoto, Y., and Narumiya, S. (1993). ADP-ribosylation of Rho p21 inhibits lysophosphatidic acid-induced protein tyrosine phosphorylation and phosphatidylinositol 3-kinase activation in cultured Swiss 3T3 cells. J. Biol. Chem. 268, 24535-24538.
39. Laemmli, U.K. (1970). Cleavage of the structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
40. 2+-induced regulation of ion channel and MAP kinase functions. Nature 376, 737-744.
41. Lewis, J.M., and Schwartz, M.A. (1995). Mapping in vivo associations of cytoplasmic proteins with integrin β1 cytoplasmic domain mutants. Mol. Biol. Cell 6, 151-160.
42. FAK in platelets. J. Cell Biol. 119, 905-912.
43. Marcantonio, E.E., Guan, J.-L., Trevithick, J.E., and Hynes, R.O. (1990). Mapping the functional determinants of the integrin beta1 cytoplasmic domain by site-directed mutagenesis. Cell Regul. 1, 597-604.
44. McNeil, P.L., and Warder, E. (1987). Glass beads load macromolecules into living cells. J. Cell Sci. 88, 669-678.
45. Miyamoto, S., Teramoto, H., Coso, O.A., Gutkind, J.S., Burbelo, P.D., Akiyama, S.K., and Yamada, K.M. (1995). Integrin function: molec-ular hierarchies of cytoskeletal and signalling molecules. J. Cell Biol. 131, 791-805.
46. Morino, N., Mimura, T., Hamasaki, K., Tobe, K., Ueki, K., Kikuchi, K., Takehara, K., Kadowski, T., Yazaki, Y., and Nojima, Y. (1995). Matrix-integrin interaction activates the mitogen-activated protein kinase, p44erk-1 and p42erk-2. J. Biol. Chem. 270, 269-273.
47. Nobes, C.D., and Hall, A. (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.
48. Nojima, Y., Morino, N., Mimura, T., Hamasaki, K., Furuya, H., Sakai, R., Sato, T., Tachibana, K., Morimoto, C., Yazaki, Y., and Hirai, H. (1995). Integrin-mediated cell adhesion promotes tyrosine phosphorylation of p130cas, an src homology 3-containing molecule having multiple src homology 2-binding motifs. J. Biol. Chem. 270, 15398-15402.
49. Nuckolls, G.H., Romer, L.H., and Burridge, K. (1992). Microinjection of antibodies against talin inhibits the spreading and migration of fibroblasts. J. Cell Sci. 102, 753-762.
50. Olson, M.F., Ashworth, A., and Hall, A. (1995). An essential role for rho, rac, and cdc42 GTPases in cell cycle progression through G1. Science 269, 1270-1272.
51. Otey, C.A., Pavalko, F.M., and Burridge, K. (1990). An interaction between alpha-actinin and the β1 integrin subunit in vitro. J. Cell Biol. 111, 721-729.
52. 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.
53. 3: induction of calcium oscillations required for protein-tyrosine phosphorylation and ligand-induced spreading of stably transfected cells. Mol. Biol. Cell 3, 989-998.
54. Richardson, A., and Parsons, J.T. (1995). Signal transduction through integrins: a central role for focal adhesion kinase? BioEssays 17, 229-236.
55. FAK. Nature 380, 538-540.
56. Ridley, A.J., and Hall, A. (1992). The small GTP-binding Rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399.
57. Ridley, A.J., and Hall, A. (1994). Signal transduction pathways regulating Rho-mediated stress fiber formation: requirement for a tyrosine kinase. EMBO J. 13, 2600-2610.
58. Romer, L.H., Burridge, K., and Turner, C.E. (1992). Signaling between the extracellular matrix and the cytoskeleton: tyrosine phosphorylation, focal adhesion assembly; the cell surface. Cold Spring Harbor Symp. Quant. Biol. 57, 193-202.
59. Romer, L.H., McLean, N.V., Turner, C.E., and Burridge, K. (1994). Tyrphostins inhibit focal adhesion kinase activation, cytoskeletal organization, and motility in human vascular endothelial cells. Mol. Biol. Cell 5, 349-361.
60. Sabe, H., Hata, A., Okada, M., Nakagawa, H., and Hanafusa, H. (1994). Analysis of the binding of the src homology 2 domain csk to tyrosine-phosphorylated proteins in the suppression and mitotic activation of c-src. Proc. Natl. Acad. Sci. USA 91, 3984-3988.
61. Sasaki, H., Nagura, K., Ishino, M., Tobioka, H., Kotani, K., and Sasaki, T. (1995). Cloning and characterization of cell adhesion kinase β, a novel protein tyrosine kinase of the focal adhesion kinase subfamily. J. Biol. Chem. 270, 21206-21219.
62. FAK, a structurally unique protein tyrosine kinase associated with focal adhesions. Proc. Natl. Acad. Sci. USA 89, 5192-5196.
63. FAK. Mol. Cell. Biol. 13, 785-791.
64. src. Mol. Cell. Biol. 14, 1680-1688.
65. Schaller, M.D., Otey, C.A., Hildebrand, J.D., and Parsons, J.T. (1995). Focal adhesion kinase and paxillin bind to peptides mimicking β integrin cytoplasmic domains. J. Cell Biol. 130, 1181-1187.
66. FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for crk. Mol. Cell. Biol. 15, 2635-2645.
67. Schlaepfer, D.D., Hanks, S.K., Hunter, T., and van der Geer, P. (1994). Integrin-mediated signalling linked to ras by GRB2 binding to focal adhesion kinase. Nature 372, 786-791.
68. Schwartz, M.A., Rupp, J.V., and Lechene, C.P. (1990). Cytoplasmic pH and anchorage-independent growth induced by V-Ki-ras, V-src, and polyoma middle T. Oncogene 5, 55-88.
69. Schwartz, M.A., Schaller, M.D., and Ginsberg, M.H. (1995). Integrins: emerging paradigms of signal transduction. Annu. Rev. Cell Biol. 11, 549-599.
70. FAK and paxillin tyrosine phosphorylation, actin stress fiber formation, and focal contact assembly in Swiss 3T3 cells. J. Biol. Chem. 269, 27610-27617.
71. Tanaka, S., Morishita, T., Hashimoto, Y., Hattori, S., Nakamura, S., Shibuya, M., Matuoka, K., Takenawa, T., Kurata, T., Nagashima, K., and Matsuda, M. (1994). C3G, a guanine nucleotide-releasing protein expressed ubiquitously, binds to the src homology 3 domains of CRK and GRB2/ASH proteins. Proc. Natl. Acad. Sci. USA 91, 3443-3447.
72. Tsukada, T., Tomooka, Y., Takai, S., Ueda, Y., Nishikawa, S., Yagi, T., Tokunaga, T., Takeda, N., Suda, Y., and Abe, S. (1993). Enhanced proliferative potential in culture of cells from p53-deficient mice. Oncogene 8, 3312-3322.
73. FAK-binding region. J. Cell Sci. 107, 1583-1591.
74. Cas and cortactin accompanies integrin-mediated cell adhesion to extracellular matrix. J. Biol. Chem. 270, 22259-22262.
75. FAK tyrosine kinase activity is not required for the assembly of F-actin stress fibers and focal adhesions in cultured mouse aortic smooth muscle cells. J. Cell Sci. 108, 2381-2391.
76. Xing, Z., Chen, H.-C., Nowlen, J.K., Taylor, S.J., Shalloway, D., and Guan, J.-L. (1994). Direct interaction of v-src with the focal adhesion kinase. Mol. Biol. Cell 5, 413-421.
77. Xu, L.H., Owens, L.V., Sturge, G.C., Yang, X., Liu, E.T., Craven, R.J., and Cance, W.G. (1996). Attenuation of the expression of the focal adhesion kinase induces apoptosis in tumor cells. Cell Growth Differ. 7, 413-418.
78. Zachary, I., Sinnett-Smith, J., and Rozengurt, E. (1992). Bombesin, vasopressin, and endothelin stimulation of tyrosine phosphorylation in Swiss 3T3 cells: identification of a novel tyrosine kinase as a major substrate. J. Biol. Chem. 267, 19031-19034.
79. Zhu, X., and Assoian, R. (1995). Integrin-dependent activation of MAP kinase: a link to shape-dependent cell proliferation. Mol. Biol. Cell 6, 273-282.