Complex formation with focal adhesion kinase: A mechanism to regulate activity and subcellular localization of Src kinases

Molecular Biology of the Cell

Volumn 10, Issue 10, 1999, Pages 3489-3505

  Schaller, Michael D ^a   Hildebrand, Jeffrey D ^b,c   Parsons, J Thomas ^b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FOCAL ADHESION KINASE; PAXILLIN; PROTEIN KINASE P60; PROTEIN TYROSINE KINASE;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME LOCALIZATION; ENZYME REGULATION; GENE TRANSLOCATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REGULATORY MECHANISM; SEQUENCE HOMOLOGY;

EID: 0032859988     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.10.10.3489     Document Type: Article

References (87)

1. Abedi, H., Dawes, K.E., and Zachary, I. (1995). Differential effects of platelet-derived growth factor BB on p125 focal adhesion kinase and paxillin tyrosine phosphorylation and on cell migration in rabbit aortic vascular smooth muscle cells and Swiss 3T3 fibroblasts. J. Biol. Chem. 270, 11367-11376.
2. cas-related protein, Sin. Genes Dev. 10, 1341-1355.
3. Alonso, G., Koegl, M., Mazurenko, N., and Courtneidge, S.A. (1995). Sequence requirements for binding of Src family tyrosine kinases to activated growth factor receptors. J. Biol. Chem. 270, 9840-9848.
4. FAK and protein kinase C-delta to focal adhesions. J. Cell Sci. 107, 2033-2045.
5. 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.
6. Bockholt, S.M., and Burridge, K. (1995). An examination of focal adhesion formation and tyrosine phosphorylation in fibroblasts isolated from src, fyn and yes mice. Cell Adhes. Commun. 3, 91-100.
7. FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly. J. Cell Biol. 119, 893-903.
8. Calalb, M.B., Polte, T.R., and Hanks, S.K. (1995). Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for src family kinases. Mol. Cell. Biol. 15, 954-963.
9. Calalb, M.B., Zhang, X.E., Polte, T.R., and Hanks, S.K. (1996). Focal adhesion kinase tyrosine-861 is a major site of phosphorylation by Src. Biochem. Biophys. Res. Commun. 228, 662-668.
10. Cary, L.A., Chang, J.F., and Guan, J.L. (1996). Stimulation of cell migration by overexpression of focal adhesion kinase and its association with src and fyn. J. Cell Sci. 109, 1787-1794.
11. FAK. J. Biol. Chem. 269, 20567-20574.
12. Chrzanowska-Wodnicka, M., and Burridge, K. (1994). Tyrosine phosphorylation is involved in reorganization of the actin cytoskeleton in response to serum or LPA stimulation. J. Cell Sci. 107, 3643-3654.
13. c-src to integrin-dependent cytoskeletal complexes in thrombin-stimulated platelets. Mol. Cell. Biol. 13, 1863-1871.
14. FAK. Mol. Cell. Biol. 14, 147-155.
15. fyn. J. Exp. Med. 175, 1483-1492.
16. FAK. Mol. Cell. Biol. 15, 2819-2827.
17. Frisch, S.M., Vuori, K., Ruoslahti, E., and Chan-Hui, P.-Y. (1996). Control of adhesion-dependent cell survival by focal adhesion kinase. J. Cell Biol. 134, 793-799.
18. Gilmore, A., and Romer, L.H. (1996). Inhibition of FAK signaling in focal adhesions decreases cell motility and proliferation. Mol. Biol. Cell 7, 1209-1224.
19. Glenney, J.R., and Zokas, L. (1989). Novel tyrosine kinase substrates from Rous sarcoma virus-transformed cells are present in the membrane skeleton. J. Cell Biol. 108, 2401-2408.
20. c-src and increases its protein-tyrosine kinase activity. Mol. Cell. Biol. 8, 3345-3356.
21. FAK both by cellular adhesion and by oncogenic transformation. Nature 358, 690-692.
22. Hanks, S.K., Calalb, M.B., Harper, M.C., and Patel, S.K. (1992). Focal adhesion protein tyrosine kinase phosphorylated in response to cell spreading on fibronectin. Proc. Natl. Acad. Sci. USA 89, 8487-8489.
23. Hanks, S.K., Quinn, A.M., and Hunter, T. (1988). The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241, 42-52.
24. FAK, to cellular focal adhesions. J. Cell Biol. 123, 993-1005.
25. Howell, B.W., and Cooper, J.A. (1994). Csk suppression of src involves movement of csk to sites of src activity. Mol. Cell. Biol. 14, 5402-5411.
26. Hughes, H.S., Greenhouse, J.J., Petropoulos, C.J., and Sutrave, P. (1987). Adaptor plasmids simplify the insertion of foreign DNA into helper-independent retroviral vectors. J. Virol. 61, 3004-3012.
27. FAK in cultured fibroblasts results in apoptosis. J. Cell Biol. 135, 1383-1390.
28. Hynes, R.O. (1992). Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69, 11-25.
29. 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.
30. Kanner, S.B., Reynolds, A.B., and Parsons, J.T. (1989). Immunoaffinity purification of tyrosine-phosphorylated cellular proteins. J. Immunol. Methods 120, 115-124.
31. Kanner, S.B., Reynolds, A.B., Vines, R.R., and Parsons, J.T. (1990). Monoclonal antibodies to individual tyrosine-phosphorylated protein substrates of oncogene-encoded tyrosine kinases. Proc. Natl. Acad. Sci. USA 87, 3328-3332.
32. Kaplan, K.B., Bibbins, K.B., Swedlow, J.R., Arnaud, M., Morgan, D.O., and Varmus, H.E. (1994). Association of the amino-terminal half of c-src with focal adhesions alters their properties and is regulated by phosphorylation of tyrosine 527. EMBO J. 13, 4745-4756.
33. Kaplan, K.B., Swedlow, J.R., Morgan, D.O., and Varmus, H.E. (1995). c-Src enhances the spreading of src-/-fibroblasts on fibronectin by a kinase-independent mechanism. Genes Dev. 9, 1505-1517.
34. Kaplan, K.B., Swedlow, J.R., Varmus, H.E., and Morgan, D.O. (1992). Association of p60c-src with endosomal membranes in mammalian fibroblasts. J. Cell Biol. 118, 321-333.
35. Klinghoffer, R.A, Sachsenmaier, C., Cooper, J.A., and Soriano, P. (1999). Src family kinases are required for integrin but not PDGFR signal transduction. EMBO J. 18, 2459-2471.
36. c-src transforming ability by mutation of its primary sites of tyrosine phosphorylation. Cell 49, 65-73.
37. Kornberg, L., Earp, H.S., Parsons, J.T., Schaller, M.D., 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.
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. Kypta, R.M., Goldberg, Y., Ulug, E.T., and Courtneidge, S.A. (1990). Association between the PDGF receptor and members of the src family of tyrosine kinases. Cell 62, 481-492.
40. Laemmli, U.K. (1970). Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227, 680-685.
41. FAK in platelets. J. Cell Biol. 119, 905-912.
42. Liu, X., Brodeur, S.R., Gish, G., Zhou, S., Cantley, L.C., Laudano, A.P., and Pawson, T. (1993). Regulation of c-Src tyrosine kinase activity by the Src SH2 domain. Oncogene 8, 1119-1126.
43. Luo, K., Hurley, T.R., and Sefton, B.M. (1991). Cyanogen bromide cleavage and proteolytic peptide mapping of proteins immobilized to membranes. Methods Enzymol. 201, 149-152.
44. FAK) and promotes migration and invasion by oral squamous cell carcinoma cells. J. Biol. Chem. 269, 31807-31813.
45. Moarefi, I., LaFevre-Bernt, M., Sicheri, F., Huse, M., Lee, C-H., Kuriyan, J., and Miller, W.T. (1997). Activation of the Src-family tyrosine kinase Hck by SH3 domain displacement. Nature 385, 650-653.
46. Mori, S., Ronnstrand, L., Yokote, K., Engstrom, A., Courtneidge, S.A., Claesson-Welsh, L., and Heldin, C.H. (1993). Identification of two juxtamembrane autophosphorylation sites in the PDGF beta-receptor; involvement in the interaction with src family tyrosine kinases. EMBO J. 12, 2257-2264.
47. src. Nature 351, 69-72.
48. cas to SH2 and SH3 domains of src kinase. J. Biol. Chem. 271, 8959-8965.
49. src of avian and mammalian origin. J. Virol. 51, 272-282.
50. c-src. Cell 49, 75-82.
51. Polte, T.R., Naftilan, A.J., and Hanks, S.K. (1994). Focal adhesion kinase is abundant in developing blood vessels and elevation of its phosphotyrosine content in vascular smooth muscle cells is a rapid response to angiotensin II. J. Cell. Biochem. 55, 106-119.
52. Ralston, R., and Bishop, J.M. (1985). The product of the protooncogene c-src is modified during the cellular response to platelet-derived growth factor. Proc. Natl. Acad. Sci. USA 82, 7845-7849.
53. FAK) and paxillin tyrosine phosphorylation in Swiss 3T3 cells. J. Biol. Chem. 269, 704-710.
54. Reynolds, A.B., Roesel, D.J., Kanner, S.B., and Parsons, J.T. (1989). Transformation-specific tyrosine phosphorylation of a novel cellular protein in chicken cells expressing oncogenic variants of the avian cellular src gene. Mol. Cell. Biol. 9, 629-638.
55. Richardson, A., Malik, R.K., Hildebrand, J.D., and Parsons, J.T. (1997). Inhibition of cell spreading by expression of the C-terminal domain of focal adhesion kinase (FAK) is rescued by coexpression of Src or catalytically inactive FAK: a role for paxillin tyrosine phosphorylarion. Mol. Cell. Biol. 17, 6906-6914.
56. FAK. Nature 380, 538-540.
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. Rodriguez-Fernandez, J.L., and Rozengurt, E. (1996). Bombesin, bradykinin, vasopressin and phorbol esters rapidly and transiently activate Src family tyrosine kinase in Swiss 3T3 cells: dissociation from tyrosine phosphorylation of p125 focal adhesion kinase. J. Biol. Chem. 271, 27895-27901.
59. Rohrschneider, L.R. (1980). Adhesion plaques of Rous sarcoma virus-transformed cells contain the src gene product. Proc. Natl. Acad. Sci. USA 77, 3514-3518.
60. Sakai, R., Iwamatsu, A., Hirano, N., Ogawa, S., Tanaka, T., Mano, H., Yazaki, Y., and Hirai, H. (1994). A novel signaling molecule, p130, forms stable complexes in vivo with v-Crk and v-Src in a tyrosine phosphorylation-dependent manner. EMBO J. 13, 3748-3756.
61. Schagger, H., and von Jagow, G. (1987). Tricine-SDS-PAGE for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166, 368-379.
62. FAK, a structurally distinctive protein tyrosine kinase associated with focal adhesions. Proc. Natl. Acad. Sci. USA 89, 5192-5196.
63. FAK. Mol. Cell. Biol. 13, 785-791.
64. Schaller, M.D., Bouton, A.H., Flynn, D.C., and Parsons, J.T. (1993b). Identification and characterization of novel substrates for protein tyrosine kinases. Prog. Nucleic Acid Res. Mol. Biol. 44, 205-227.
65. src. Mol. Cell. Biol. 14, 1680-1688.
66. Schaller, M.D., and Parsons, J.T. (1994). Focal adhesion kinase and associated proteins. Curr. Opin. Cell Biol. 6, 705-710.
67. FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for Crk. Mol. Cell. Biol. 15, 2635-2645.
68. cas, and Nck adaptor proteins. Mol. Cell. Biol. 17, 1702-1713.
69. Schlaepfer, D.D., Hanks, S.K., Hunter, T., and van der Geer, P. (1994). Integrin-mediated signal transduction linked to ras pathway by GRB2 binding to focal adhesion kinase. Nature 372, 786-791.
70. Schlaepfer, D.D., and Hunter, T. (1996). Evidence for in vivo phosphorylation of the grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein-tyrosine kinases. Mol. Cell. Biol. 16, 5623-5633.
71. c-src on tyrosine 527. Mol. Cell. Biol. 8, 2465-2471.
72. Schwartz, M.A., Schaller, M.D., and Ginsberg, M.H. (1995). Integrins: emerging paradigms of signal transduction. Annu. Rev. Cell Dev. Biol. 11, 549-599.
73. Seufferlein, T., and Rozengurt, E. (1994). Lysophosphatidic acid stimulates tyrosine phosphorylation of focal adhesion kinase, paxillin and p130. J. Biol. Chem. 269, 9345-9351.
74. Sicheri, F., Moarefi, I., and Kuriyan, J. (1997). Crystal structure of the Src family tyrosine kinase Hck. Nature 385, 602-609.
75. Sinnett-Smith, J., Zachary, I., Valverde, A.M., and Rozengurt, E. (1993). Bombesin stimulation of pp125 focal adhesion kinase tyrosine phosphorylation. J. Biol. Chem. 268, 14261-14268.
76. Songyang, Z., Shoelson, S.E., Chaudhuri, M., Gish, G., Pawson, T., Haser, W.G., King, F., Roberts, T., Ratnofsky, S., Lechleider, R.J., Neel, B.G., Birge, R.B., Fajardo, J.E., Chou, M.M., Hanafusa, H., Schaffhausen, B., and Cantley, L.C. (1993). SH2 domains recognize specific phosphopeptide sequences. Cell 72, 767-778.
77. Sparks, A.B., Rider, J.E., Hoffman, N.G., Fowlkes, D.M., Quilliam, L.A., and Kay, B.K. (1996). Distinct ligand preferences of Src homology 3 domains from Src, Yes, Abl, cortactin, p53bp2, PLC-gamma, Crk and Grb2. Proc. Natl. Acad. Sci. USA 93, 1540-1544.
78. Thomas, J.W., Ellis, B., Boerner, R.J., Knight, W.B., White, G.C., and Schaller, M.D. (1998). SH2-and SH3-mediated interactions between focal adhesion kinase and Src. J. Biol. Chem. 273, 577-583.
79. Thomas, S.M., Soriano, P., and Imamoto, A. (1995). Specific and redundant roles of src and fyn in organizing the cytoskeleton. Nature 376, 267-271.
80. cas signaling complex formation upon integrin-mediated cell adhesion: a role for src family kinases. Mol. Cell. Biol. 16, 2606-2613.
81. Weng, Z., Taylor, J.A., Turner, C.E., Brugge, J.S., and Seidel-Dugan, C. (1993). Detection of Src homology 3-binding proteins, including paxillin, in normal and v-src transformed BALB/c 3T3 cells. J. Biol. Chem. 268, 14956-14963.
82. c-src tyrosine kinase, myristylation, and modulatory domains are required for enhanced mitogenic responsiveness to epidermal growth factor seen in cells overexpressing c-src. Mol. Cell. Biol. 9, 1536-1544.
83. src substrate. Mol. Cell. Biol. 11, 5113-5124.
84. 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 mediated by the src SH2 domain. Mol. Biol. Cell 5, 413-421.
85. Xu, W., Harrison, S.C., and Eck, M.J. (1997). Three-dimensional structure of the tyrosine kinase c-Src. Nature 385, 595-602.
86. Yu, H., Chen, J.K., Feng, S., Dalgarno, D.C., Brauer, A.W., and Schreiber, S.L. (1994). Structural basis for the binding of proline-rich peptides to SH3 domains. Cell 76, 933-945.
87. 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.