Evidence for In Vivo Phosphorylation of the Grb2 SH2-Domain Binding Site on Focal Adhesion Kinase by Src-Family Protein-Tyrosine Kinases

REFERENCES

• Abedi, H., K. E. Dawes, and I. Zachary. 1995. Differential effects of PDGF BB on p125FAK and paxillin tyrosine phosphorylation and cell migration in rabbit aortic vascular smooth muscle cells and Swiss 3T3 fibroblasts. J. Biol. Chem. 270: 11367–11376.
   PubMedGoogle Scholar
• Akiyama, S. K., S. E. Yamada, K. M. Yamada, and S. E. LaFlamme. 1994. Transmembrane signal transduction by integrin cytoplasmic domains expressed in single-subunit chimeras. J. Biol. Chem. 269: 15961–15964.
   PubMed Web of Science ®Google Scholar
• Avraham, S., R. London, Y. Fu, S. Ota, D. Hiregowdara, J. Li, S. Jiang, L. M. Pasztor, R. A. White, J. E. Groopman, and H. Avraham. 1995. Identification and characterization of a novel related adhesion focal tyrosine kinase (RAFTK) from megakaryocytes and brain. J. Biol. Chem. 270: 27742–27751.
   PubMed Web of Science ®Google Scholar
• Benjamin, C. W., D. A. Linseman, and D. A. Jones. 1994. Platelet-derived growth factor stimulates phosphorylation of growth factor receptor-binding protein-2 in vascular smooth muscle cells. J. Biol. Chem. 269: 31346–31349.
   PubMedGoogle Scholar
• Bockholt, S. M., and K. Burridge. 1993. Cell spreading on extracellular matrix protein induces tyrosine phosphorylation of tensin. J. Biol. Chem. 268: 14565–14567.
   PubMed Web of Science ®Google Scholar
• Bohmer, R. M., E. Scharf, and R. K. Assoian. 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.
   PubMedGoogle Scholar
• Boudreau, N., C. J. Sympson, Z. Werb, and M. J. Bissell. 1995. Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science 267: 891–893.
   PubMed Web of Science ®Google Scholar
• Boyle, W. J., P. van der Geer, and T. Hunter. 1991. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 201: 110–149.
   PubMed Web of Science ®Google Scholar
• Burridge, K., C. E. Turner, and L. H. Romer. 1992. Tyrosine phosphorylation of paxillin and pp125FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly. J. Cell Biol. 119: 893–903.
   PubMed Web of Science ®Google Scholar
• Calalb, M. B., T. R. Polte, and S. K. Hanks. 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.
   PubMed Web of Science ®Google Scholar
• Chan, P. Y., S. B. Kanner, G. Whitney, and A. Aruffo. 1994. A transmembrane-anchored chimeric focal adhesion kinase is constitutively activated and phosphorylated at tyrosine residues identicle to pp125FAK. J. Biol. Chem. 269: 20567–20574.
   PubMed Web of Science ®Google Scholar
• Chen, H. C., P. A. Appeddu, J. T. Parsons, J. D. Hildebrand, M. D. Schaller, and J. L. Guan. 1995. Interaction of focal adhesion kinase with cytoskeletal protein talin. J. Biol. Chem. 270: 16995–16999.
   PubMed Web of Science ®Google Scholar
• Chen, H. C., and J. L. Guan. 1994. Association of focal adhesion kinase with its potential substrate phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA 91: 10148–10152.
   PubMed Web of Science ®Google Scholar
• Chen, Q., M. S. Kinch, T. H. Lin, K. Burridge, and R. L. Juliano. 1994. Integrin-mediated cell adhesion activates mitogen-activated protein kinases. J. Biol. Chem. 269: 1–4.
   PubMedGoogle Scholar
• Chong, L. D., A. Trynor-Kaplan, G. M. Bokoch, and M. A. Schwartz. 1994. The small GTP-binding protein Rho regulates a phosphatidylinositol 4-phosphate 5-kinase in mammalian cells. Cell 79: 507–513.
   PubMed Web of Science ®Google Scholar
• Clark, E. A., and J. S. Brugge. 1995. Integrins and signal transduction pathways: the road taken. Science 268: 233–239.
   PubMed Web of Science ®Google Scholar
• Cobb, B. S., M. D. Schaller, T.-H. Leu, and J. T. Parsons. 1994. Stable association of pp60src and pp59fyn with the focal adhesion-associated protein tyrosine kinase, pp125FAK. Mol. Cell. Biol. 14: 147–155.
   PubMed Web of Science ®Google Scholar
• Cooper, J. A., and B. Howell. 1993. The when and how of Src regulation. Cell 73: 1051–1054.
   PubMed Web of Science ®Google Scholar
• Egan, S. E., B. W. Giddings, M. W. Brooks, L. Buday, A. W. Sizeland, and R. A. Weinberg. 1993. Association of Sos Ras exchange protein with Grb2 is implicated in tyrosine kinase signal transduction and transformation. Nature (London) 363: 45–51.
   PubMed Web of Science ®Google Scholar
• Eide, B. L., C. W. Turck, and J. A. Escobedo. 1995. Identification of Tyr-397 as the primary site of tyrosine phosphorylation and pp60src association in the focal adhesion kinase, pp125FAK. Mol. Cell. Biol. 15: 2819–2827.
   PubMed Web of Science ®Google Scholar
• Fang, F., G. Orend, N. Watanabe, T. Hunter, and E. Ruoslahti. 1996. Dependence of cyclin E-CDK2 kinase activity on cell anchorage. Science 271: 499–502.
   PubMed Web of Science ®Google Scholar
• Frisch, S. M., and H. Francis. 1994. Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 124: 619–626.
   PubMed Web of Science ®Google Scholar
• George, E. L., E. N. Georges-Labouesse, R. S. Patel-King, H. Rayburn, and R. O. Hynes. 1993. Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119: 1079–1091.
   PubMed Web of Science ®Google Scholar
• Grant, S. G. N., K. A. Karl, M. A. Kiebler, and E. R. Kandel. 1995. Focal adhesion kinase in the brain: novel subcellular localization and specific regulation by Fyn tyrosine kinase in mutant mice. Genes Dev. 9: 1909–1921.
   PubMed Web of Science ®Google Scholar
• Guan, J. L., and D. Shalloway. 1992. Regulation of focal adhesion-associated protein tyrosine kinase by both cellular adhesion and oncogenic transformation. Nature (London) 358: 690–692.
   PubMed Web of Science ®Google Scholar
• Guinebault, C., B. Payrastre, C. Racaud-Sultan, H. Mazarguil, M. Breton, G. Mauco, M. Plantavid, and H. Chap. 1995. Integrin-dependent translocation of phosphoinositide 3-kinase to the cytoskeleton of thrombin-activated platelets involves specific interactions of p85α with actin filaments and focal adhesion kinase. J. Cell Biol. 129: 831–842.
   PubMed Web of Science ®Google Scholar
• Hanks, S. K., M. B. Calalb, M. C. Harper, and S. K. Patel. 1992. Focal adhesion protein-tyrosine kinase phosphorylated in response to cell attachment to fibronectin. Proc. Natl. Acad. Sci. USA 89: 8487–8491.
   PubMed Web of Science ®Google Scholar
• Hildebrand, J. D., M. D. Schaller, and J. T. Parsons. 1993. Identification of sequences required for the efficient localization of the focal adhesion kinase, pp125FAK, to cellular focal adhesions. J. Cell Biol. 123: 993–1005.
   PubMed Web of Science ®Google Scholar
• Hildebrand, J. D., M. D. Schaller, and J. T. Parsons. 1995. Paxillin, a tyrosine phosphorylated focal adhesion-associated protein, binds to the carboxy terminal domain of focal adhesion kinase. Mol. Biol. Cell. 6: 637–647.
   PubMed Web of Science ®Google Scholar
• Howell, B. W., and J. A. Cooper. 1994. Csk suppression of Src involves movement of Csk to sites of Src activity. Mol. Cell. Biol. 14: 5402–5411.
   PubMed Web of Science ®Google Scholar
• Hughes, P. E., F. Diaz-Gonzalez, L. Leong, C. Wu, J. A. McDonald, S. J. Shattil, and M. H. Ginsberg. 1996. Breaking the integrin hinge. J. Biol. Chem. 271: 6571–6574.
   PubMed Web of Science ®Google Scholar
• Ilic, D., Y. Furuta, S. Kanazawa, N. Takeda, K. Sobue, N. Nakatsuji, S. Nomura, J. Fujimoto, M. Okada, T. Yamamoto, and S. Aizawa. 1995. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature (London) 377: 539–544.
   PubMed Web of Science ®Google Scholar
• Jockusch, B. M., P. Bubeck, K. Giehl, M. Kroemker, J. Moschner, M. Rothkegel, M. Rudiger, K. Schluter, G. Stanke, and J. Winkler. 1995. The molecular architecture of focal adhesions. Annu. Rev. Dev. Biol. 11: 379–416.
   PubMed Web of Science ®Google Scholar
• Kaplan, K. B., K. B. Bibbins, J. R. Swedlow, M. Arnaud, D. O. Morgan, and H. E. Varmus. 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.
   PubMed Web of Science ®Google Scholar
• Kapron-Bras, C., L. Fitz-Gibbon, P. Jeevaratnam, J. Wilkins, and S. Dedhar. 1993. Stimulation of tyrosine phosphorylation and accumulation of GTP-bound p21ras upon antibody-mediated α2β1 integrin activation in T-lymphoblastic cells. J. Biol. Chem. 268: 20701–20704.
   PubMed Web of Science ®Google Scholar
• Kharbanda, S., A. Saleem, Z. Yuan, Y. Emoto, K. S. V. Prasad, and D. Kufe. 1995. Stimulation of human monocytes with macrophage colony-stimulating factor induces a GRB2-mediated association of the focal adhesion kinase pp125FAK and dynamin. Proc. Natl. Acad. Sci. USA 92: 6132–6136.
   PubMed Web of Science ®Google Scholar
• Kornberg, L., H. S. Earp, J. T. Parsons, M. Schaller, and R. L. Juliano. 1992. Cell adhesion or integrin clustering increases phosphorylation of a focal adhesion-associated tyrosine kinase. J. Biol. Chem. 267: 23439–23442.
   PubMed Web of Science ®Google Scholar
• Lev, S., H. Moreno, R. Martinez, P. Canoll, E. Peles, J. M. Musacchio, G. D. Plowman, B. Rudy, and J. Schlessinger. 1995. Protein tyrosine kinase PYK2 involved in calcium-induced regulation of ion channel and MAP kinase functions. Nature (London) 376: 737–745.
   PubMed Web of Science ®Google Scholar
• Lin, T. H., C. Rosales, K. Mondal, J. B. Bolen, S. Haskill, and R. L. Juliano. 1995. Integrin-mediated tyrosine phosphorylation and cytokine message induction in monocytic cells. J. Biol. Chem. 270: 16189–16197.
   PubMed Web of Science ®Google Scholar
• Lowenstein, E. J., R. J. Daly, A. G. Batzer, W. Li, B. Margolis, R. Lammers, A. Ullrich, E. Y. Skolnik, S. D. Bar, and J. Schlessinger. 1992. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 70: 431–442.
   PubMed Web of Science ®Google Scholar
• Lukashev, M. E., D. Sheppard, and R. Pytela. 1994. Disruption of integrin function and induction of tyrosine phosphorylation by the autonomously expressed βl integrin cytoplasmic domain. J. Biol. Chem. 269: 18311–18314.
   PubMed Web of Science ®Google Scholar
• Matsumoto, K., K. Matsumoto, T. Nakamura, and R. H. Kramer. 1994. Hepatocyte growth factor/scatter factor induces tyrosine phosphorylation of focal adhesion kinase (p125FAK) and promotes migration and invasion by oral squamous cell carcinoma cells. J. Biol. Chem. 269: 31807–31813.
   PubMed Web of Science ®Google Scholar
• McNamee, H. P., D. E. Ingber, and M. A. Schwartz. 1993. Adhesion to fibronectin stimulates inositol lipid synthesis and enhances PDGF-induced inositol lipid breakdown. J. Cell Biol. 121: 673–678.
   PubMed Web of Science ®Google Scholar
• Miyamoto, S., H. Teramoto, O. A. Coso, J. S. Gutkind, P. D. Burbelo, S. K. Akiyama, and K. M. Yamada. 1995. Integrin function: molecular hierarchies of cytoskeletal and signaling molecules. J. Cell Biol. 131: 791–805.
   PubMed Web of Science ®Google Scholar
• Moodie, S. A., B. M. Willumsen, M. J. Weber, and A. Wolfman. 1993. Complexes of Ras-GTP with Raf-1 and mitogen-activated protein kinase kinase. Science 260: 1658–1661.
   PubMed Web of Science ®Google Scholar
• Nojima, Y., N. Morino, T. Mimura, K. Hamasaki, H. Furuya, R. Sakai, T. Sato, K. Tachibana, C. Morimoto, Y. Yazaki, and H. Hirai. 1995. Integrin-mediated cell adhesion promotes tyrosine phosphorylation of p130cas, a Src homology 3-containing molecule having multiple Src homology 2-binding motifs. J. Biol. Chem. 270: 15398–15402.
   PubMed Web of Science ®Google Scholar
• Pawson, T. 1995. Protein modules and signaling networks. Nature (London) 373: 573–579.
   PubMed Web of Science ®Google Scholar
• Rankin, S., R. Hooshmand-Rad, L. Claesson-Welsh, and E. Rozengurt. 1996. Requirement of phosphatidylinositol 3′-kinase activity in platelet-derived growth factor-stimulated tyrosine phosphorylation of p125 focal adhesion kinase and paxillin. J. Biol. Chem. 271: 7829–7834.
   PubMedGoogle Scholar
• Rodier, J. M., A. M. Valles, M. Denoyelle, J. P. Thiery, and B. Boyer. 1995. pp60c Src is a positive regulator of growth factor-induced cell scatter in a rat bladder carcinoma cell line. J. Cell Biol. 131: 761–773.
   PubMed Web of Science ®Google Scholar
• Rusanescu, G., H. Qi, S. M. Thomas, J. S. Brugge, and S. Halegoua. 1995. Calcium influx induces neurite growth through a Src-Ras signaling cassette. Neuron. 15: 1415–1425.
   PubMed Web of Science ®Google Scholar
• Sasaki, H., K. Nagura, M. Ishino, H. Tobioka, K. Kotani, and T. Sasaki. 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.
   PubMed Web of Science ®Google Scholar
• Schaller, M. D., C. A. Borgman, B. S. Cobb, R. R. Vines, A. B. Reynolds, and J. T. Parsons. 1992. pp125FAK, a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc. Natl. Acad. Sci. USA 89: 5192–5196.
   PubMed Web of Science ®Google Scholar
• Schaller, M. D., J. D. Hildebrand, J. D. Shannon, J. W. Fox, R. R. Vines, and J. T. Parsons. 1994. Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src. Mol. Cell. Biol. 14: 1680–1688.
   PubMed Web of Science ®Google Scholar
• Schaller, M. D., C. A. Otey, J. D. Hildebrand, and J. T. Parsons. 1995. Focal adhesion kinase and paxillin bind peptides mimicking β integrin cytoplasmic domains. J. Cell Biol. 130: 1181–1187.
   PubMed Web of Science ®Google Scholar
• Schlaepfer, D. D., M. A. Broome, and T. Hunter. Ras-dependent integrin activation of ERK2/MAP kinase: signaling from a FAK and c-Src complex. Submitted for publication.
   Google Scholar
• Schlaepfer, D. D., S. K. Hanks, T. Hunter, and P. van der Geer. 1994. Integrin-mediated signal transduction linked to RAS pathway by GRB2 binding to focal adhesion kinase. Nature (London) 372: 786–791.
   PubMed Web of Science ®Google Scholar
• Schlaepfer, D. D., and T. Hunter. Unpublished results.
   Google Scholar
• Schwartz, M. A., E. J. Brown, and B. Fazeli. 1993. A 50 kDa integrin-associated protein is required for integrin-regulated calcium entry in endothelial cells. J. Biol. Chem. 268: 19931–19934.
   PubMed Web of Science ®Google Scholar
• Schwartz, M. A., M. D. Schaller, and M. H. Ginsberg. 1995. Integrins: emerging paradigms of signal transduction. Annu. Rev. Cell Dev. Biol. 11: 549–599.
   PubMed Web of Science ®Google Scholar
• Seufferlein, T., and E. Rozengurt. 1994. Lysophosphatidic acid stimulates tyrosine phosphorylation of focal adhesion kinase, paxillin, and p130. J. Biol. Chem. 269: 9345–9351.
   PubMed Web of Science ®Google Scholar
• Shattil, S. J., B. Haimovich, M. Cunningham, L. Lipfert, J. T. Parsons, M. H. Ginsberg, and J. S. Brugge. 1994. Tyrosine phosphorylation of p125FAK in platelets requires coordinated signaling through integrin and agonist receptors. J. Biol. Chem. 269: 14738–14745.
   PubMed Web of Science ®Google Scholar
• Sinnett-Smith, J., I. Zachary, A. M. Valverde, and E. Rozengurt. 1993. Bombesin stimulation of p125 focal adhesion kinase tyrosine phosphorylation. Role of protein kinase C, Ca2+ mobilization, and the actin cytoskeleton. J. Biol. Chem. 268: 14261–14268.
   PubMedGoogle Scholar
• Tachibana, K., T. Sato, N. D’Avirro, and C. Morimoto. 1995. Direct association of pp125FAK with paxillin, the focal adhesion-targeting mechanism of pp125FAK. J. Exp. Med. 182: 1089–1100.
   PubMed Web of Science ®Google Scholar
• Thomas, S. M., P. Soriano, and A. Imamaoto. 1995. Specific and redundant roles of Src and Fyn in organizing the cytoskeleton. Nature (London) 376: 267–271.
   PubMed Web of Science ®Google Scholar
• Tremble, P., C. H. Damsky, and Z. Werb. 1995. Components of the nuclear signaling cascade that regulate collagenase gene expression in response to integrin-derived signals. J. Cell Biol. 129: 1707–1720.
   PubMed Web of Science ®Google Scholar
• Vuori, K., and E. Ruoslahti. 1994. Association of insulin receptor substrate-1 with integrins. Science 266: 1576–1578.
   PubMed Web of Science ®Google Scholar
• Xing, Z., H. C. Chen, J. K. Nowlen, S. Taylor, D. Shalloway, and J. L. Guan. 1994. Direct interaction of v-Src with the focal adhesion kinase mediated by the src SH2 domain. Mol. Biol. Cell. 5: 413–421.
   PubMed Web of Science ®Google Scholar
• Yamada, K. M., and S. Miyamoto. 1995. Integrin transmembrane signaling and cytoskeletal control. Curr. Biol. 7: 681–689.
   Google Scholar
• Zhang, C., M. P. Lambert, C. Bunch, K. Barber, W. S. Wade, G. A. Krafft, and W. L. Klein. 1994. Focal adhesion kinase expressed by nerve cell lines shows increased tyrosine phosphorylation in response to Alzheimer’s Aβ peptide. J. Biol. Chem. 269: 25247–25250.
   PubMedGoogle Scholar
• Zhang, Z., K. Vuori, J. C. Reed, and E. Ruoslahti. 1995. The α5βt integrin supports survival of cells on fibronectin and up-regulates Bcl-2 expression. Proc. Natl. Acad. Sci. USA 92: 6161–6165.
   PubMed Web of Science ®Google Scholar
• Zhu, X., and R. K. Assoian. 1995. Integrin-dependent activation of MAP kinase: a link to shape-dependent cell proliferation. Mol. Biol. Cell. 6: 273–282.
   PubMed Web of Science ®Google Scholar