Activation of Rho-Dependent Cell Spreading and Focal Adhesion Biogenesis by the v-Crk Adaptor Protein

REFERENCES

• Adra, C. N., D. Manor, J. L. Ko, S. Zhu, T. Horiuchi, L. Van Aelst, R. A. Cerione, and B. Lim 1997. RhoGDIgamma: a GDI-dissociation inhibitor for Rho proteins with preferential expression in brain and pancreas. Proc. Natl. Acad. Sci. USA 94: 4279–4284.
   PubMed Web of Science ®Google Scholar
• Altun-Gultekin, Z. F., and J. A. Wagner 1996. Src, ras, and rac mediate the migratory response elicited by NGF and PMA in PC12 cells. J. Neurosci. Res. 44: 308–327.
   PubMed Web of Science ®Google Scholar
• Arraro, M., K. Chihara, K. Kimura, Y. Fukata, N. Nahamura, Y. Matsura, and K. Kaibuchi 1996. Formation of actin stress fibers and focal adhesions enhanced by rho-kinase. Science 275: 1308–1311.
   Google Scholar
• Barry, S. T., H. M. Flinn, M. J. Humphries, D. R. Critchley, and A. J. Ridley 1997. Requirement for rho in integrin signaling. Cell Adhes. Commun. 4: 387–398.
   PubMed Web of Science ®Google Scholar
• Bershadsky, A. D., I. S. Tint, Neyfakh A. A., Jr., and J. M. Vasiliev 1985. Focal contacts of normal and RSV-transformed quail cells. Hypothesis of the transformation-induced deficient maturation of focal contacts. Exp. Cell Res. 158: 433–444.
   PubMedGoogle Scholar
• Birge, R. B., B. S. Knudsen, D. Besser, and H. Hanafusa 1996. SH2- and SH3-containing adaptor proteins: redundant or independent mediators of intracellular signal transduction. Gene Cell 1: 595–613.
   PubMedGoogle Scholar
• Bokoch, G. M., B. P. Bohl, and T.-H. Chuang 1994. Guanine nucleotide exchange regulates membrane translocation of rac/rho GTP-binding proteins. J. Biol. Chem. 269: 31674–31679.
   PubMed Web of Science ®Google Scholar
• Burridge, K., and M. Chrzanowska-Wodnicka 1996. Focal adhesions, contractility, and signaling. Annu. Rev. Cell Biol. 12: 463–519.
   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
• Cerione, R. A., and Y. Zheng 1996. The dbl family of oncogenes. Curr. Opin. Cell Biol. 8: 216–222.
   PubMed Web of Science ®Google Scholar
• Chong, L. D., A. Traynor-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
• Chou, M. M., and J. Blenis 1996. The 70 kDa S6 kinase complexes with and is activated by the Rho family G proteins Cdc42 and Rac1. Cell 85: 573–583.
   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
• Crespo, P., K. E. Schuebel, A. A. Ostrom, J. S. Gutkind, and X. R. Bustelo 1997. Phosphotyrosine-dependent activation of rac-1 GDP/GTP exchange by the vav proto-oncogene product. Nature (London) 385: 169–172.
   PubMed Web of Science ®Google Scholar
• Delannet, M., F. Martin, B. Bossy, D. A. Cheresh, L. F. Reichardt, and J. L. Duband 1994. Specific roles of the alpha V beta 1, alpha V beta 3, and alpha V beta 5 integrins in avian neural crest cell adhesion and migration on vitronectin. Development 120: 2687–2702.
   PubMed Web of Science ®Google Scholar
• Fath, K. R., C.-J. S. Edgell, and K. Burridge 1989. The distribution of distinct integrins in focal contacts is determined by the substratum composition. J. Cell Sci. 92: 67–75.
   PubMed Web of Science ®Google Scholar
• Feller, S. M., B. Knudsen, T. W. Wong, and H. Hanafusa 1995. Detection of SH3 binding proteins in total cell lysates with GST-SH3 fusion proteins. Methods Enzymol. 255: 369–378.
   PubMedGoogle Scholar
• Flinn, H. M., and A. J. Ridley 1996. Rho stimulates tyrosine phosphorylation of focal adhesion kinase, p130, and paxillin. J. Cell Sci. 109: 1133–1141.
   PubMed Web of Science ®Google Scholar
• Frisch, S. M., K. Vuori, E. Ruoslahti, and P. Chan-Hui 1996. Control of adhesion-dependent cell survival by focal adhesion kinase. J. Cell Biol. 134: 793–799.
   PubMed Web of Science ®Google Scholar
• Gebbink, M. F. B. G., O. Kranenburg, M. Poland, F. P. G. van Horck, B. Houssa, and W. H. Moolenaar 1997. Identification of a novel, putative Rho-specific GDP/GTP exchange factor and a RhoA-binding protein: control of neuronal morphology. J. Cell Biol. 137: 1603–1613.
   PubMedGoogle Scholar
• Gilmore, A. P., and K. Burridge 1996. Regulation of vinculin binding to talin and actin by phosphatidyl inositol 4,5-bisphosphate. Nature (London) 381: 531–535.
   PubMed Web of Science ®Google Scholar
• Glassman, R. H., B. L. Hempstead, L. Stainco-Coico, M. G. Steiner, H. Hanafusa, and R. B. Birge 1997. v-Crk, an effector of the NGF signaling pathway, delays apoptotic cell death in neurotrophin-deprived PC12 cells. Cell Death Differ. 4: 82–93.
   PubMedGoogle Scholar
• Gotoh, T., S. Hattori, S. Nakamura, H. Kitayama, M. Noda, Y. Takai, K. Kaibuchi, H. Matsui, O. Hatase, H. Takahashi, T. Kurata, and M. Matsuda 1995. Identification of Rap1 as a target for the Crk SH3 domain-binding guanine nucleotide-releasing protein C3G. Mol. Cell. Biol. 15: 6746–6753.
   PubMed Web of Science ®Google Scholar
• Gulbins, E., K. M. Coggeshell, G. Baier, S. Katzav, P. Burn, and A. Altman 1993. Tyrosine kinase stimulated guanine nucleotide exchange activity of vav in T cell activation. Science 260: 822–825.
   PubMedGoogle Scholar
• Hall, A. 1994. Small GTP-binding proteins and the regulation of the actin cytoskeleton. Annu. Rev. Cell Biol. 10: 31–54.
   PubMedGoogle Scholar
• Hanks, S. K., and T. R. Polte 1997. Signaling through focal adhesion kinase. Bioessays 19: 137–145.
   PubMed Web of Science ®Google Scholar
• Hartwig, J. H., G. M. Bokoch, C. L. Carpenter, P. A. Janmey, L. A. Taylor, A. Toker, and T. P. Stossel 1995. Thrombin receptor ligation and activated rac uncap actin filament barbed ends through phosphoinositide synthesis in permeabilized human platelets. Cell 82: 643–653.
   PubMed Web of Science ®Google Scholar
• Hempstead, B. L., R. B. Birge, J. E. Fajardo, R. Glassman, D. Mahadeo, R. Kraemer, and H. Hanafusa 1994. Expression of the v-Crk oncogene product in PC12 cells results in rapid differentiation by both nerve growth factor-dependent and epidermal growth factor-dependent pathways. Mol. Cell Biol. 14: 1964–1971.
   PubMedGoogle Scholar
• Hotchin, N. A., and A. Hall 1995. The assembly of integrin adhesion complexes requires both extracellular matrix and intracellular rho/rac GTPases. J. Cell Biol. 131: 1857–1865.
   PubMed Web of Science ®Google Scholar
• Hungerford, J. E., M. T. Compton, M. L. Matter, B. G. Hoffstom, and C. A. Otey 1996. Inhibition of pp125FAK in cultured fibroblasts results in apoptosis. J. Cell Biol. 135: 1383–1390.
   PubMed Web of Science ®Google Scholar
• Ishizaki, T., M. Maekawa, K. Fujisawa, K. Okawa, A. Iwamatsu, A. Fujita, N. Watanabe, Y. Saito, A. Kakizuka, N. Morii, and S. Narumiya 1996. The small GTP-binding protein rho binds to and activates a 160 kDa Ser/Thr protein kinase homologous to myotonic dystrophy kinase. EMBO J. 15: 1885–1893.
   PubMed Web of Science ®Google Scholar
• Ishizaki, T., M. Naito, K. Fuzisawa, M. Maekawa, N. Watarabe, Y. Saito, and S. Narumiya 1997. p160 rock, a rho-associated coiled-coil forming protein kinase, works downstream of rho and induces focal adhesions. FEBS Lett. 404: 118–124.
   PubMedGoogle Scholar
• Jalink, K., and W. H. Moolenaar 1992. Thrombin receptor activation causes rapid cell rounding and neurite retraction independent of classic second messengers. J. Cell Biol. 118: 411–419.
   PubMed Web of Science ®Google Scholar
• Jalink, K., E. J. VanCorven, T. Hengeveld, N. Morii, S. Narumiya, and W. H. Moolenaar 1994. Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein rho. J. Cell Biol. 126: 801–810.
   PubMed Web of Science ®Google Scholar
• Janmey, P. A., and T. P. Stossel 1987. Modulation of gelsolin function by phosphatidylinositol-4,5-bisphosphate. Nature (London) 325: 362–365.
   PubMed Web of Science ®Google Scholar
• Kimura, K., M. Ito, M. Amano, K. Chihara, Y. Fukata, M. Nakafuku, B. Yamamori, J. Feng, T. Nakano, K. Okawa, A. Iwamatsu, and K. Kaibuchi 1996. Regulation of myosin phosphatase by rho and rho-associated kinase (rho-kinase). Science 273: 245–248.
   PubMed Web of Science ®Google Scholar
• Knudsen, B. S., S. M. Feller, and H. Hanafusa 1994. Four proline-rich sequences of the guanine-nucleotide exchange factor C3G bind with unique specificity to the first src homology 3 domain of Crk. J. Biol. Chem. 269: 32781–32787.
   PubMed Web of Science ®Google Scholar
• Kozma, R., S. Sarner, S. Ahmed, and L. Lim 1997. Rho family GTPases and neuronal growth cone remodelling: relationship between increased complexity induced by Cdc42Hs, Rac1, and acetylcholine and collapse induced by RhoA and lysophosphatidic acid. Mol. Cell. Biol. 17: 1201–1211.
   PubMed Web of Science ®Google Scholar
• Kumagai, N., N. Morii, K. Fujisawa, Y. Nemoto, and S. Narumiya 1993. ADP-ribosylation of Rho p21 inhibits lysophosphatidic acid-induced protein tyrosine phosphorylation and phosphatidylinositol 3-kinase activation in Swiss 3T3 cells. J. Biol. Chem. 268: 24535–24538.
   PubMed Web of Science ®Google Scholar
• Lamoureux, P., Z. F. Altun-Gultekin, C. Lin, J. A. Wagner, and S. R. Heideman 1997. Rac is required for growth cone function but not neurite assembly. J. Cell Sci. 110: 635–641.
   PubMedGoogle Scholar
• Leberer, E., D. Y. Thomas, and M. Whiteway 1997. Pheromone signalling and polarized morphogenesis in yeast. Curr. Opin. Genet. Dev. 7: 59–66.
   PubMedGoogle Scholar
• Leung, T., X.-Q. Chen, E. Manser, and L. Lim 1996. The p160 RhoA-binding kinase ROKα is a member of a kinase family and is involved in the reorganization of the cytoskeleton. Mol. Cell. Biol. 16: 5313–5327.
   PubMed Web of Science ®Google Scholar
• Leung, T., E. Manser, L. Tan, and L. Lim 1995. A novel serine/threonine kinase binding the ras-related rhoA GTPase which translocates the kinase to peripheral membranes. J. Biol. Chem. 270: 29051–29054.
   PubMed Web of Science ®Google Scholar
• Luo, L., T. K. Hensch, L. Ackerman, S. Barbel, L. Y. Jan, and Y. N. Jan 1996. Differential effects of the rac GTPase on Purkinje cell axons and dendritic trunks and spines. Nature (London) 379: 837–840.
   PubMed Web of Science ®Google Scholar
• Luo, L., L. Y. Jan, and Y.-N. Jan 1997. Rho family small GTP-binding proteins in growth cone signalling. Curr. Opin. Neurobiol. 7: 81–86.
   PubMed Web of Science ®Google Scholar
• Luo, L., Y. J. Liao, J. Y. Jan, and Y. N. Jan 1994. Distinct morphogenetic functions of similar small GTPases: Drosophilia Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 8: 1787–1802.
   PubMed Web of Science ®Google Scholar
• Mackay, D. J. G., C. D. Nobes, and A. Hall 1995. The Rho’s progress: a potential role during neuritogenesis for the Rho family of GTPases. Trends Neurosci. 18: 496–501.
   PubMedGoogle Scholar
• Madaule, P., T. Furuyashiki, T. Reid, T. Ishizaki, G. Watanabe, N. Morii, and S. Narumiya 1995. A novel partner for the GTP-bound forms of rho and rac. FEBS Lett. 377: 243–248.
   PubMedGoogle Scholar
• Manser, E., T. Leung, H. Salihuddin, Z. Zhao, and L. Lim 1994. A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature (London) 367: 40–46.
   PubMed Web of Science ®Google Scholar
• Matsui, T., M. Amano, T. Yamamoto, K. Chiara, M. Nakafulu, M. Ito, T. Nakano, K. Okawa, A. Iwamatsu, and K. Kaibuchi 1996. Rho-associated kinase, a novel serine/threonine kinase, as a putative target for the small GTP-binding protein rho. EMBO J. 15: 2208–2216.
   PubMed Web of Science ®Google Scholar
• Mayer, B. J., and H. Hanafusa 1990. Mutagenic analysis of the v-crk oncogene: requirement for SH2 and SH3 domains and correlation between increased cellular phosphotyrosine and transformation. J. Virol. 64: 3581–3589.
   PubMedGoogle Scholar
• Meier, T., and H. Leying 1996. A laboratory guide to biotin-labeling in biomolecule analysis. Birkhauser, Basel, Switzerland.
   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
• Nievers, M., R. B. Birge, H. Greulich, A. J. Verkleif, H. Hanafusa, and P. M. P. van Bergen en Henegouwen 1996. v-Crk induced cell transformation: changes in focal adhesion composition and signaling. J. Cell Sci. 110: 389–399.
   Google Scholar
• Nishiki, T., S. Narumiya, N. Morii, M. Yamamoto, M. Fujiwara, Y. Kamata, G. Sakaguchi, and S. Kozaki 1990. ADP-ribosylation of the rho/rac proteins induces growth inhibition, neurite outgrowth and acetylcholine esterase in cultured PC12 cells. Biochem. Biophys. Res. Commun. 167: 265–272.
   PubMed Web of Science ®Google Scholar
• Nobes, C. D., and A. Hall 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.
   PubMed Web of Science ®Google Scholar
• Nobes, C. D., P. Hawkins, L. Stephens, and A. Hall 1995. Activation of the small GTP-binding proteins rho and rac by growth factor receptors. J. Cell Sci. 108: 225–233.
   PubMed Web of Science ®Google Scholar
• Plopper, G. E., H. P. McNamee, L. E. Dike, K. Bojanowski, and D. E. Ingber 1995. Convergence of integrin and growth factor receptor signaling pathways within the focal adhesion complex. Mol. Biol. Cell 6: 1349–1365.
   PubMed Web of Science ®Google Scholar
• Reid, T., T. Furuyashiki, T. Ishizaki, G. Watanabe, N. Watanabe, K. Fujisawa, N. Morii, P. Madaule, and S. Narumiya 1996. Rhotekin, a new putative target for Rho bearing homology to a serine/threonine kinase, PKN, and rhophilin in the rho-binding domain. J. Biol. Chem. 271: 13556–13560.
   PubMed Web of Science ®Google Scholar
• Ren, X.-D., G. M. Bokoch, A. Traynor-Kaplan, G. H. Jenkins, R. A. Anderson, and M. A. Schwartz 1996. Physical association of the small GTPase rho with a 68-kDa phosphatidylinositol 4-phosphate 5-kinase in Swiss 3T3 cells. Mol. Biol. Cell 7: 435–442.
   PubMedGoogle Scholar
• Ridley, A. J., and A. Hall 1994. Signal transduction pathways regulating rho-mediated stress fibre formation: requirement for a tyrosine kinase. EMBO J. 13: 2600–2610.
   PubMed Web of Science ®Google Scholar
• Ridley, A. J., and A. Hall 1992. The small GTP binding protein rho regulates the assembly of focal adhesions and stress fibers in response to growth factors. Cell 70: 389–399.
   PubMed Web of Science ®Google Scholar
• Rossino, P., I. Gavazzi, R. Timpl, M. Aumailley, M. Abbadini, F. Giancotti, L. Silengo, P. C. Marchisio, and G. Tarone 1990. Nerve growth factor induces increased expression of a laminin-binding integrin in rat pheochromocytoma PC12 cells. Exp. Cell Res. 189: 100–108.
   PubMed Web of Science ®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 proteins. Mol. Cell. Biol. 17: 1702–1713.
   PubMed Web of Science ®Google Scholar
• Seckl, M. J., N. Morii, S. Narumiya, and E. Rozengurt 1995. Guanosine 5′-3′-O-(thio)triphosphate stimulates tyrosine phosphorylation of p125FAK and paxillin in permeabilized Swiss 3T3 cells. J. Biol. Chem. 270: 6984–6990.
   PubMedGoogle Scholar
• Suidan, H. S., S. R. Stone, B. A. Hemmings, and D. Monard 1992. Thrombin causes neurite retraction in neural cells through activation of cell surface receptors. Neuron 8: 363–375.
   PubMed Web of Science ®Google Scholar
• Tahagi, J., T. Kamata, J. Meredith, W. Puzon-McLaughlin, and Y. Takada 1997. Changing ligand specificities of αVβ1 and αVβ3 integrins by swapping a short diverse sequence of the β subunit. J. Biol. Chem. 272: 19796–19800.
   Google Scholar
• Tanaka, S., T. Morishita, Y. Hashimoto, S. Hattori, S. Nakamura, M. Shibuya, K. Matuoka, T. Takenawa, T. Kurata, K. Nagashima, and M. Matsuda 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.
   PubMed Web of Science ®Google Scholar
• Tanaka, S., T. Ouchi, and H. Hanafusa 1997. Downstream of Crk adaptor signaling pathway: activation of Jun kinase by v-Crk through the guanine nucleotide exchange protein C3G. Proc. Natl. Acad. Sci. USA 94: 2356–2361.
   PubMedGoogle Scholar
• Teng, K. K., H. Lander, J. E. Fajardo, H. Hanafusa, B. L. Hempstead, and R. B. Birge 1995. v-crk modulation of growth factor-induced PC12 cell differentiation involves the src homology 2 domain of v-crk and sustained activation of the Ras/mitogen-activated protein kinase pathway. J. Biol. Chem. 270: 20677–20685.
   PubMed Web of Science ®Google Scholar
• Tigyi, G., D. J. Fischer, A. Sebok, C. Yang, D. L. Dyer, and R. Miledi 1996. Lysophosphatidic acid-induced neurite retraction in PC12 cells: control by phosphoinositide-Ca2+ signaling and rho. J. Neurochem. 66: 537–548.
   PubMed Web of Science ®Google Scholar
• Tigyi, G., and R. Miledi 1992. Lysophosphatidates bound to serum albumin activate membrane currents in Xenopus oocytes and neurite retraction in PC12 pheochromocytoma cells. J. Biol. Chem. 267: 21360–21367.
   PubMed Web of Science ®Google Scholar
• Tomaselli, K. J., D. E. Hall, L. A. Flier, K. R. Gehlsen, D. C. Turner, S. Carbonetto, and L. F. Reichardt 1990. A neuronal cell line (PC12) express two β1-class integrins—α1β1 and α3β1—that recognize different neurite outgrowth-promoting domains in laminin. Neuron 5: 651–662.
   PubMed Web of Science ®Google Scholar
• Vincent, S., and J. Settleman 1997. The PRK2 kinase is a potential effector target of both Rho and Rac GTPases and regulates actin cytoskeletal organization. Mol. Cell. Biol. 17: 2247–2256.
   PubMedGoogle Scholar
• Watanabe, G., Y. Saito, P. Madaule, T. Ishizaki, K. Fujisawa, N. Morii, H. Mukai, Y. Ono, and A. Kakizuka 1996. Protein kinase N (PKN) and PKN-related protein rhophilin as targets of small GTPase rho. Science 271: 645–648.
   PubMed Web of Science ®Google Scholar
• Watanabe, N., P. Madaule, T. Reid, T. Ishizaki, G. Watanabe, A. Kakizuka, Y. Saito, K. Nakao, B. M. Jockusch, and S. Narumiya 1997. p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for rho small GTPase and is a ligand for profilin. EMBO J. 16: 3044–3056.
   PubMed Web of Science ®Google Scholar
• Zachary, I., J. Sinnett-Smith, C. E. Turner, and E. Rozengurt 1993. Bombesin, vasopressin, and endothelin rapidly stimulate tyrosine phopshorylation of the focal adhesion-associated protein paxillin in Swiss 3T3 cells. J. Biol. Chem. 268: 22060–22065.
   PubMed Web of Science ®Google Scholar
• Zhang, Z., G. Tarone, and D. C. Turner 1993. Expression of integrin α1 β1 is regulated by nerve growth factor and dexamethasone in PC12 cells. Functional consequences for adhesion and neurite outhgrowth. J. Biol. Chem. 268: 5557–5565.
   PubMed Web of Science ®Google Scholar
• Zheng, Y., D. Zangrilli, R. A. Cerione, and A. Eva 1996. The pleckstrin homology domain mediates transformation by oncogenic dbl through specific intracellular targeting. J. Biol. Chem. 271: 19017–19020.
   PubMed Web of Science ®Google Scholar