Multiple Grb2-Mediated Integrin-Stimulated Signaling Pathways to ERK2/Mitogen-Activated Protein Kinase: Summation of Both c-Src- and Focal Adhesion Kinase-Initiated Tyrosine Phosphorylation Events

REFERENCES

• Bellis, S. L., J. A. Perrotta, M. S. Curtis, and C. E. Turner 1997. Adhesion of fibroblasts to fibronectin stimulates both serine and tyrosine phosphorylation of paxillin. Biochem. J. 325: 375–381.
   PubMed Web of Science ®Google Scholar
• Blaikie, P. A., E. Fournier, S. M. Dilworth, D. Birnbaum, J. P. Borg, and B. Margolis 1997. The role of the Shc phosphotyrosine interaction/phosphotyrosine binding domain and tyrosine phosphorylation sites in polyoma middle T antigen-mediated cell transformation. J. Biol. Chem. 272: 20671–20677.
   PubMedGoogle 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
• Brown, M. C., J. A. Perrotta, and C. E. Turner 1996. Identification of LIM3 as the principal determinant of paxillin focal adhesion localization and characterization of a novel motif on paxillin directing vinculin and focal adhesion kinase binding. J. Cell Biol. 135: 1109–1123.
   PubMed Web of Science ®Google Scholar
• Calalb, M., T. Polte, and S. K. Hanks 1995. Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for the Src family kinases. Mol. Cell. Biol. 15: 954–963.
   PubMed Web of Science ®Google Scholar
• Calalb, M. B., X. Zhang, T. R. Polte, and S. K. Hanks 1996. Focal adhesion kinase tyrosine-861 is a major site of phosphorylation by Src. Biochem. Biophys. Res. Commun. 228: 662–668.
   PubMedGoogle Scholar
• Chen, H. C., P. A. Appeddu, H. Isoda, and J. L. Guan 1996. Phosphorylation of tyrosine 397 in focal adhesion kinase is required for binding phosphatidylinositol 3-kinase. J. Biol. Chem. 271: 26329–26334.
   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, 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: 26602–26605.
   PubMed Web of Science ®Google Scholar
• Chrzanowska-Wodnicka, M., and K. Burridge 1996. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133: 1403–1415.
   PubMed Web of Science ®Google Scholar
• Clark, E. A., and J. S. Brugge 1993. Redistribution of activated pp60c-src to integrin-dependent cytoskeletal complexes in thrombin-stimulated platelets. Mol. Cell. Biol. 13: 1863–1871.
   PubMed Web of Science ®Google Scholar
• Clark, E. A., and R. O. Hynes 1996. Ras activation is necessary for integrin-mediated activation of extracellular signal regulated kinase 2 and cytosolic phospholipase A2 but not for cytoskeletal organization. J. Biol. Chem. 271: 14814–14818.
   PubMedGoogle Scholar
• Clark, E. A., S. J. Shattil, and J. S. Brugge 1994. Regulation of protein tyrosine kinases in platelets. Trends Biochem. Sci. 19: 464–469.
   PubMed Web of Science ®Google Scholar
• den Hertog, J., and T. Hunter 1996. Tight association of GRB2 with receptor protein-tyrosine phosphatase α is mediated by the SH2 and C-terminal SH3 domains. EMBO J. 15: 3016–3027.
   PubMedGoogle 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
• Gould, K. L., J. R. Woodgett, J. A. Cooper, J. E. Buss, D. Shalloway, and T. Hunter 1985. Protein kinase C phosphorylates pp60src at a novel site. Cell 42: 849–857.
   PubMedGoogle Scholar
• Guan, J.-L., J. E. Trevithick, and R. O. Hynes 1991. Fibronectin/integrin interaction induces tyrosine phosphorylation of a 120-kDa protein. Cell Regul. 2: 951–964.
   PubMedGoogle Scholar
• Hamasaki, K., T. Mimura, H. Furuya, N. Morino, T. Yamazaki, I. Komuro, Y. Yazaki, and Y. Nojima 1995. Stretching mesangial cells stimulates tyrosine phosphorylation of focal adhesion kinase pp125FAK. Biochem. Biophys. Res. Commun. 212: 544–549.
   PubMedGoogle Scholar
• Hanke, J. H., J. P. Gardner, R. L. Dow, P. S. Changelian, W. H. Brissette, E. J. Weringer, B. A. Pollok, and P. A. Connelly 1996. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J. Biol. Chem. 271: 695–701.
   PubMed Web of Science ®Google Scholar
• Hanks, S. K., and T. R. Polte 1997. Signaling through focal adhesion kinase. Bioessays 19: 137–145.
   PubMed Web of Science ®Google Scholar
• Harmer, S. L., and A. L. DeFranco 1997. Shc contains two Grb2 binding sites needed for efficient formation of complexes with SOS in B lymphocytes. Mol. Cell. Biol. 17: 4087–4095.
   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 carboxyl terminal domain of focal adhesion kinase. Mol. Biol. Cell 6: 637–647.
   PubMed Web of Science ®Google Scholar
• Huang, M. M., L. Lipfert, M. Cunningham, J. S. Brugge, M. H. Ginsberg, and S. J. Shattil 1993. Adhesive ligand binding to integrin αIIbβ3 stimulates tyrosine phosphorylation of novel protein substrates before phosphorylation of pp125FAK. J. Cell Biol. 122: 473–83.
   PubMed Web of Science ®Google Scholar
• Ilic, D., C. H. Damsky, and T. Yamamoto 1997. Focal adhesion kinase: at the crossroads of signal transduction. J. Cell Sci. 110: 401–407.
   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 377: 539–544.
   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 alter their properties and is regulated by phosphorylation of tyrosine 527. EMBO J. 13: 4745–4756.
   PubMed Web of Science ®Google Scholar
• Kaplan, K. B., J. R. Swedlow, D. O. Morgan, and H. E. Varmus 1995. c-Src enhances the spreading of src−/− fibroblasts on fibronectin by a kinase-independent mechanism. Genes Dev. 9: 1505–1517.
   PubMed Web of Science ®Google Scholar
• King, W. G., M. D. Mattaliano, T. O. Chan, P. N. Tsichlis, and J. S. Brugge 1997. Phosphatidylinositol 3-kinase is required for integrin-stimulated AKT and Raf-1/mitogen-activated protein kinase pathway activation. Mol. Cell. Biol. 17: 4406–4418.
   PubMed Web of Science ®Google Scholar
• Klemke, R. L., S. Cai, A. L. Giannini, P. J. Gallagher, P. de Lanerolle, and D. A. Cheresh 1997. Regulation of cell motility by mitogen-activated protein kinase. J. Cell Biol. 137: 481–492.
   PubMed Web of Science ®Google Scholar
• Leong, L., P. E. Hughes, M. A. Schwartz, M. H. Ginsberg, and S. J. Shattil 1995. Integrin signaling: roles for the cytoplasmic tails of αIIbβ3 in the tyrosine phosphorylation of pp125FAK. J. Cell Sci. 108: 3817–3825.
   PubMed Web of Science ®Google Scholar
• Lewis, J. M., R. Baskaran, S. Taagepera, M. A. Schwartz, and J. Y. J. Wang 1996. Integrin regulation of c-Abl tyrosine kinase activity and cytoplasmic nuclear transport. Proc. Natl. Acad. Sci. USA 93: 15174–15179.
   PubMed Web of Science ®Google Scholar
• Lewis, J. M., D. A. Cheresh, and M. A. Schwartz 1996. Protein kinase C regulates αvβ5-dependent cytoskeletal associations and focal adhesion kinase phosphorylation. J. Cell Biol. 134: 1323–1332.
   PubMed Web of Science ®Google Scholar
• Li, S., J. Couet, and M. P. Lisanti 1996. Src tyrosine kinase, Gα subunits, and H-Ras share a common membrane-anchored scaffolding protein caveolin. J. Biol. Chem. 271: 29182–29190.
   PubMed Web of Science ®Google Scholar
• Li, S., M. Kim, Y.-L. Hu, S. Jalali, D. D. Schlaepfer, T. Hunter, S. Chien, and J. Y. Shyy 1997. Fluid shear stress activation of focal adhesion kinase. Linking to mitogen-activated protein kinases. J. Biol. Chem. 272: 30455–30462.
   PubMed Web of Science ®Google Scholar
• Lin, T. H., A. E. Aplin, Y. Shen, Q. Chen, M. Schaller, L. Romer, I. Aukhil, and R. L. Juliano 1997. Integrin-mediated activation of MAP kinase is independent of FAK: evidence for dual integrin signaling pathways in fibroblasts. J. Cell Biol. 136: 1385–1395.
   PubMed Web of Science ®Google Scholar
• Lipfert, L., B. Haimovich, M. D. Schaller, B. S. Cobb, J. T. Parsons, and J. S. Brugge 1992. Integrin-dependent phosphorylation and activation of the protein tyrosine kinase pp125FAK in platelets. J. Cell Biol. 119: 905–912.
   PubMed Web of Science ®Google Scholar
• Mainiero, F., C. Murgia, K. K. Wary, A. M. Curatola, A. Pepe, M. Blumemberg, J. K. Westwick, C. J. Der, and F. G. Giancotti 1997. The coupling of α6β4 integrin to Ras-MAP kinase pathways mediated by Shc controls keratinocyte proliferation. EMBO J. 16: 2365–2375.
   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
• Morino, N., T. Mimura, K. Hamasaki, K. Tobe, K. Ueki, K. Kikuchi, T. Kadowaki, Y. Yazaki, and Y. Nojima 1995. Matrix/integrin interaction activates the mitogen-activated protein kinase, p44Erk-1 and p42Erk-2. J. Biol. Chem. 270: 269–273.
   PubMed Web of Science ®Google Scholar
• Renshaw, M. W., D. Toksoz, and M. A. Schwartz 1996. Involvement of the small GTPase Rho in integrin-mediated activation of mitogen-activated protein kinase. J. Biol. Chem. 271: 21691–21694.
   PubMed Web of Science ®Google Scholar
• Roach, T., S. Slater, M. Koval, M. White, E. Cahir-McFarland, M. Okumura, M. Thomas, and E. Brown 1997. CD45 regulates Src family member kinase activity associated with macrophage integrin-mediated adhesion. Curr. Biol. 7: 407–417.
   Google Scholar
• Rodriguez-Fernandez, J. L., and E. Rozengurt 1996. Bombesin, bradykinin, vasopressin, and phorbol esters rapidly and transiently activate Src family tyrosine kinases in Swiss 3T3 cells. J. Biol. Chem. 271: 27895–27901.
   PubMedGoogle 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
• Schaller, M. D., and J. T. Parsons 1995. pp125FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for Crk. Mol. Cell. Biol. 15: 2635–2645.
   PubMed Web of Science ®Google Scholar
• Schlaepfer, D. D. Unpublished data.
   Google Scholar
• Schlaepfer, D. D., et al. Submitted for publication.
   Google Scholar
• Schlaepfer, D. D., M. A. Broome, and T. Hunter 1997. Fibronectin-stimulated signaling from a focal adhesion kinase–c-Src complex: involvement of the Grb2, p130cas, and Nck adaptor [sic] proteins. Mol. Cell. Biol. 17: 1702–1713.
   PubMed Web of Science ®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 372: 786–791.
   PubMed Web of Science ®Google Scholar
• Schlaepfer, D. D., and T. Hunter 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.
   PubMed Web of Science ®Google Scholar
• Schlaepfer, D. D., and T. Hunter 1997. FAK overexpression enhances Ras-dependent integrin signaling to ERK2/mitogen-activated protein kinase through interactions with and activation of c-Src. J. Biol. Chem. 272: 13189–13195.
   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
• Sjaastad, M. D., B. Angres, R. S. Lewis, and W. J. Nelson 1994. Feedback regulation of cell-substratum adhesion by integrin-mediated intracellular Ca2+ signaling. Proc. Natl. Acad. Sci. USA 91: 8214–8218.
   PubMedGoogle Scholar
• Tahiliani, P. D., L. Singh, K. L. Auer, and S. E. LaFlamme 1997. The role of conserved amino acid motifs within the integrin β3 cytoplasmic domain in triggering focal adhesion kinase phosphorylation. J. Biol. Chem. 272: 7892–7898.
   PubMed Web of Science ®Google Scholar
• Tanaka, M., R. Gupta, and B. J. Mayer 1995. Differential inhibition of signaling pathways by dominant-negative SH2/SH3 adapter proteins. Mol. Cell. Biol. 15: 6829–6837.
   PubMed Web of Science ®Google Scholar
• van der Geer, P., S. Wiley, G. D. Gish, and T. Pawson 1996. The Shc adaptor protein is highly phosphorylated at conserved, twin tyrosine residues (Y239/240) that mediate protein-protein interactions. Curr. Biol. 6: 1435–1444.
   PubMed Web of Science ®Google Scholar
• Vuori, K., H. Hirai, S. Aizawa, and E. Ruoslahti 1996. Induction of p130cas signaling complex formation upon integrin-mediated cell adhesion: a role for the Src family kinases. Mol. Cell. Biol. 16: 2606–2613.
   PubMed Web of Science ®Google Scholar
• Vuori, K., and E. Ruoslahti 1993. Activation of protein kinase C precedes α5β1 integrin-mediated cell spreading on fibronectin. J. Biol. Chem. 268: 21459–21462.
   PubMed Web of Science ®Google Scholar
• Wary, K. K., F. Mainiero, S. J. Isakoff, E. E. Marcantonio, and F. G. Giancotti 1996. The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell 87: 733–743.
   PubMed Web of Science ®Google Scholar
• Xu, W., S. C. Harrison, and M. J. Eck 1997. Three-dimensional structure of the tyrosine kinase c-Src. Nature 385: 595–602.
   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