Cadherins and Pak1 Control Contact Inhibition of Proliferation by Pak1-βPIX-GIT Complex-Dependent Regulation of Cell-Matrix Signaling

REFERENCES

• Audebert, S., C. Navarro, C. Nourry, S. Chasserot-Golaz, P. Lecine, Y. Bellaiche, J. L. Dupont, R. T. Premont, C. Sempere, J. M. Strub, A. Van Dorsselaer, N. Vitale, and J. P. Borg. 2004. Mammalian Scribble forms a tight complex with the betaPIX exchange factor. Curr. Biol. 14:987–995.
   PubMed Web of Science ®Google Scholar
• Avizienyte, E., and M. C. Frame. 2005. Src and FAK signalling controls adhesion fate and the epithelial-to-mesenchymal transition. Curr. Opin. Cell Biol. 17:542–547.
   PubMed Web of Science ®Google Scholar
• Beeser, A., Z. M. Jaffer, C. Hofmann, and J. Chernoff. 2005. Role of group A p21-activated kinases in activation of extracellular-regulated kinase by growth factors. J. Biol. Chem. 280:36609–36615.
   PubMed Web of Science ®Google Scholar
• Birukova, A. A., I. Malyukova, A. Mikaelyan, P. Fu, and K. G. Birukov. 2007. Tiam1 and betaPIX mediate Rac-dependent endothelial barrier protective response to oxidized phospholipids. J. Cell. Physiol. 211:608–617.
   PubMedGoogle Scholar
• Bokoch, G. M. 2003. Biology of the p21-activated kinases. Annu. Rev. Biochem. 72:743–781.
   PubMed Web of Science ®Google Scholar
• Capaldo, C. T., and I. G. Macara. 2007. Depletion of E-cadherin disrupts establishment but not maintenance of cell junctions in Madin-Darby canine kidney epithelial cells. Mol. Biol. Cell 18:189–200.
   PubMed Web of Science ®Google Scholar
• Chen, X., and B. M. Gumbiner. 2006. Crosstalk between different adhesion molecules. Curr. Opin. Cell Biol. 18:572–578.
   PubMed Web of Science ®Google Scholar
• Coles, L. C., and P. E. Shaw. 2002. PAK1 primes MEK1 for phosphorylation by Raf-1 kinase during cross-cascade activation of the ERK pathway. Oncogene 21:2236–2244.
   PubMed Web of Science ®Google Scholar
• Coniglio, S. J., S. Zavarella, and M. H. Symons. 2008. Pak1 and Pak2 mediate tumor cell invasion through distinct signaling mechanisms. Mol. Cell. Biol. 28:4162–4172.
   PubMed Web of Science ®Google Scholar
• den Elzen, N., C. V. Buttery, M. P. Maddugoda, G. Ren, and A. S. Yap. 2009. Cadherin adhesion receptors orient the mitotic spindle during symmetric cell division in mammalian epithelia. Mol. Biol. Cell 20:3740–3750.
   PubMed Web of Science ®Google Scholar
• Gavard, J., and J. S. Gutkind. 2006. VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat. Cell Biol. 8:1223–1234.
   PubMed Web of Science ®Google Scholar
• Greenwood, J. A., A. B. Theibert, G. D. Prestwich, and J. E. Murphy-Ullrich. 2000. Restructuring of focal adhesion plaques by PI 3-kinase. Regulation by PtdIns (3,4,5)-p(3) binding to alpha-actinin. J. Cell Biol. 150:627–642.
   PubMedGoogle Scholar
• Hansen, S., M. Zegers, M. Woodrow, P. Rodriguez-Viciana, P. Chardin, K. Mostov, and M. McMahon. 2001. Induced expression of Rnd3 is associated with transformation of polarized epithelial cells by the Raf-MEK-extracellular signal-regulated kinase pathway. Mol. Cell. Biol. 20:9364–9375.
   Google Scholar
• Harden, N. 2002. Signaling pathways directing the movement and fusion of epithelial sheets: lessons from dorsal closure in Drosophila. Differentiation 70:181–203.
   PubMed Web of Science ®Google Scholar
• Herzig, M., F. Savarese, M. Novatchkova, H. Semb, and G. Christofori. 2007. Tumor progression induced by the loss of E-cadherin independent of beta-catenin/Tcf-mediated Wnt signaling. Oncogene 26:2290–2298.
   PubMed Web of Science ®Google Scholar
• Jacinto, A., A. Martinez-Arias, and P. Martin. 2001. Mechanisms of epithelial fusion and repair. Nat. Cell Biol. 3:E117–E123.
   PubMed Web of Science ®Google Scholar
• Jeanes, A., C. J. Gottardi, and A. S. Yap. 2008. Cadherins and cancer: how does cadherin dysfunction promote tumor progression? Oncogene 27:6920–6929.
   PubMed Web of Science ®Google Scholar
• Katso, R., K. Okkenhaug, K. Ahmadi, S. White, J. Timms, and M. D. Waterfield. 2001. Cellular function of phosphoinositide 3-kinases: implications for development, homeostasis, and cancer. Annu. Rev. Cell Dev. Biol. 17:615–675.
   PubMed Web of Science ®Google Scholar
• Korinek, V., N. Barker, P. J. Morin, D. van Wichen, R. de Weger, K. W. Kinzler, B. Vogelstein, and H. Clevers. 1997. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC−/− colon carcinoma. Science 275:1784–1787.
   PubMed Web of Science ®Google Scholar
• Kreis, P., and J. V. Barnier. 2009. PAK signalling in neuronal physiology. Cell Signal. 21:384–393.
   PubMed Web of Science ®Google Scholar
• Kumar, R., A. E. Gururaj, and C. J. Barnes. 2006. p21-activated kinases in cancer. Nat. Rev. Cancer 6:459–471.
   PubMed Web of Science ®Google Scholar
• Lozano, E., M. A. Frasa, K. Smolarczyk, U. G. Knaus, and V. M. Braga. 2008. PAK is required for the disruption of E-cadherin adhesion by the small GTPase Rac. J. Cell Sci. 121:933–938.
   PubMed Web of Science ®Google Scholar
• Manser, E., T. H. Loo, C. G. Koh, Z. S. Zhao, X. Q. Chen, L. Tan, I. Tan, T. Leung, and L. Lim. 1998. PAK kinases are directly coupled to the PIX family of nucleotide exchange factors. Mol. Cell 1:183–192.
   PubMed Web of Science ®Google Scholar
• Miura, K., J. M. Nam, C. Kojima, N. Mochizuki, and H. Sabe. 2009. EphA2 engages Git1 to suppress Arf6 activity modulating epithelial cell-cell contacts. Mol. Biol. Cell 20:1949–1959.
   PubMedGoogle Scholar
• Motti, M. L., D. Califano, G. Baldassarre, A. Celetti, F. Merolla, F. Forzati, M. Napolitano, B. Tavernise, A. Fusco, and G. Viglietto. 2005. Reduced E-cadherin expression contributes to the loss of p27kip1-mediated mechanism of contact inhibition in thyroid anaplastic carcinomas. Carcinogenesis 26:1021–1034.
   PubMedGoogle Scholar
• Papakonstanti, E. A., and C. Stournaras. 2002. Association of PI-3 kinase with PAK1 leads to actin phosphorylation and cytoskeletal reorganization. Mol. Biol. Cell 13:2946–2962.
   PubMed Web of Science ®Google Scholar
• Park, H. S., S. H. Lee, D. Park, J. S. Lee, S. H. Ryu, W. J. Lee, S. G. Rhee, and Y. S. Bae. 2004. Sequential activation of phosphatidylinositol 3-kinase, beta Pix, Rac1, and Nox1 in growth factor-induced production of H2O2. Mol. Cell. Biol. 24:4384–4394.
   PubMed Web of Science ®Google Scholar
• Pece, S., M. Chiariello, C. Murga, and J. S. Gutkind. 1999. Activation of the protein kinase Akt/PKB by the formation of E-cadherin-mediated cell-cell junctions. Evidence for the association of phosphatidylinositol 3-kinase with the E-cadherin adhesion complex. J. Biol. Chem. 274:19347–19351.
   PubMed Web of Science ®Google Scholar
• Pece, S., and J. S. Gutkind. 2000. Signaling from E-cadherins to the MAPK pathway by the recruitment and activation of epidermal growth factor receptors upon cell-cell contact formation. J. Biol. Chem. 275:41227–41233.
   PubMedGoogle Scholar
• Perrais, M., X. Chen, M. Perez-Moreno, and B. M. Gumbiner. 2007. E-cadherin homophilic ligation inhibits cell growth and epidermal growth factor receptor signaling independently of other cell interactions. Mol. Biol. Cell 18:2013–2025.
   PubMed Web of Science ®Google Scholar
• Popoff, M. R., and B. Geny. 2009. Multifaceted role of Rho, Rac, Cdc42 and Ras in intercellular junctions, lessons from toxins. Biochim. Biophys. Acta 1788:797–812.
   PubMed Web of Science ®Google Scholar
• Qian, X., T. Karpova, A. M. Sheppard, J. McNally, and D. R. Lowy. 2004. E-cadherin-mediated adhesion inhibits ligand-dependent activation of diverse receptor tyrosine kinases. EMBO J. 23:1739–1748.
   PubMed Web of Science ®Google Scholar
• Rennefahrt, U. E., S. W. Deacon, S. A. Parker, K. Devarajan, A. Beeser, J. Chernoff, S. Knapp, B. E. Turk, and J. R. Peterson. 2007. Specificity profiling of Pak kinases allows identification of novel phosphorylation sites. J. Biol. Chem. 282:15667–15678.
   PubMed Web of Science ®Google Scholar
• Sasaki, C. Y., H. Lin, P. J. Morin, and D. L. Longo. 2000. Truncation of the extracellular region abrogates cell contact but retains the growth-suppressive activity of E-cadherin. Cancer Res. 60:7057–7065.
   PubMedGoogle Scholar
• Sells, M. A., J. T. Boyd, and J. Chernoff. 1999. p21-activated kinase 1 (Pak1) regulates cell motility in mammalian fibroblasts. J. Cell Biol. 145:837–849.
   PubMed Web of Science ®Google Scholar
• Shin, E. Y., K. S. Shin, C. S. Lee, K. N. Woo, S. H. Quan, N. K. Soung, Y. G. Kim, C. I. Cha, S. R. Kim, D. Park, G. M. Bokoch, and E. G. Kim. 2002. Phosphorylation of p85 beta PIX, a Rac/Cdc42-specific guanine nucleotide exchange factor, via the Ras/ERK/PAK2 pathway is required for basic fibroblast growth factor-induced neurite outgrowth. J. Biol. Chem. 277:44417–44430.
   PubMed Web of Science ®Google Scholar
• Slack-Davis, J. K., S. T. Eblen, M. Zecevic, S. A. Boerner, A. Tarcsafalvi, H. B. Diaz, M. S. Marshall, M. J. Weber, J. T. Parsons, and A. D. Catling. 2003. PAK1 phosphorylation of MEK1 regulates fibronectin-stimulated MAPK activation. J. Cell Biol. 162:281–291.
   PubMedGoogle Scholar
• St. Croix, B., C. Sheehan, J. W. Rak, V. A. Flørenes, J. M. Slingerland, and R. S. Kerbel. 1998. E-cadherin-dependent growth suppression is mediated by the cyclin-dependent kinase inhibitor p27(KIP1). J. Cell Biol. 142:557–571.
   PubMed Web of Science ®Google Scholar
• Stewart, D. B., A. I. Barth, and W. J. Nelson. 2000. Differential regulation of endogenous cadherin expression in Madin-Darby canine kidney cells by cell-cell adhesion and activation of beta-catenin signaling. J. Biol. Chem. 275:20707–20716.
   PubMedGoogle Scholar
• Stockinger, A., A. Eger, J. Wolf, H. Beug, and R. Foisner. 2001. E-cadherin regulates cell growth by modulating proliferation-dependent beta-catenin transcriptional activity. J. Cell Biol. 154:1185–1196.
   PubMed Web of Science ®Google Scholar
• Stockton, R., J. Reutershan, D. Scott, J. Sanders, K. Ley, and M. A. Schwartz. 2007. Induction of vascular permeability: betaPIX and GIT1 scaffold the activation of extracellular signal-regulated kinase by PAK. Mol. Biol. Cell 18:2346–2355.
   PubMedGoogle Scholar
• Takahashi, K., and K. Suzuki. 1996. Density-dependent inhibition of growth involves prevention of EGF receptor activation by E-cadherin-mediated cell-cell adhesion. Exp. Cell Res. 226:214–222.
   PubMed Web of Science ®Google Scholar
• Troxell, M. L., Y. T. Chen, N. Cobb, W. J. Nelson, and J. A. Marrs. 1999. Cadherin function in junctional complex rearrangement and posttranslational control of cadherin expression. Am. J. Physiol. 276:C404–C418.
   PubMedGoogle Scholar
• Troxell, M. L., S. Gopalakrishnan, J. McCormack, B. A. Poteat, J. Pennington, S. M. Garringer, E. E. Schneeberger, W. J. Nelson, and J. A. Marrs. 2000. Inhibiting cadherin function by dominant mutant E-cadherin expression increases the extent of tight junction assembly. J. Cell Sci. 113:985–996.
   PubMed Web of Science ®Google Scholar
• Van Aelst, L., and M. Symons. 2002. Role of Rho family GTPases in epithelial morphogenesis. Genes Dev. 16:1032–1054.
   PubMed Web of Science ®Google Scholar
• Vizirianakis, I. S., Y. Q. Chen, S. S. Kantak, A. S. Tsiftsoglou, and R. H. Kramer. 2002. Dominant-negative E-cadherin alters adhesion and reverses contact inhibition of growth in breast carcinoma cells. Int. J. Oncol. 21:135–144.
   PubMedGoogle Scholar
• Weiner, O. D., P. O. Neilsen, G. D. Prestwich, M. W. Kirschner, L. C. Cantley, and H. R. Bourne. 2002. A PtdInsP(3)- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity. Nat. Cell Biol. 4:509–513.
   PubMed Web of Science ®Google Scholar
• Wheelock, M. J., and K. R. Johnson. 2003. Cadherins as modulators of cellular phenotype. Annu. Rev. Cell Dev. Biol. 19:207–235.
   PubMed Web of Science ®Google Scholar
• Yeaman, C. 2003. Ultracentrifugation-based approaches to study regulation of Sec6/8 (exocyst) complex function during development of epithelial cell polarity. Methods 30:198–206.
   PubMed Web of Science ®Google Scholar
• Yin, G., Q. Zheng, C. Yan, and B. C. Berk. 2005. GIT1 is a scaffold for ERK1/2 activation in focal adhesions. J. Biol. Chem. 280:27705–27712.
   PubMed Web of Science ®Google Scholar
• Yoshii, S., M. Tanaka, Y. Otsuki, D. Y. Wang, R. J. Guo, Y. Zhu, R. Takeda, H. Hanai, E. Kaneko, and H. Sugimura. 1999. alphaPIX nucleotide exchange factor is activated by interaction with phosphatidylinositol 3-kinase. Oncogene 18:5680–5690.
   PubMed Web of Science ®Google Scholar
• Zegers, M. 2008. Roles of p21-activated kinases and associated proteins in epithelial wound healing. Int. Rev. Cell Mol. Biol. 267:253–298.
   PubMedGoogle Scholar
• Zegers, M. M., M. A. Forget, J. Chernoff, K. E. Mostov, M. B. ter Beest, and S. H. Hansen. 2003. Pak1 and PIX regulate contact inhibition during epithelial wound healing. EMBO J. 22:4155–4165.
   PubMedGoogle Scholar