NADPH Oxidase 1 Controls the Persistence of Directed Cell Migration by a Rho-Dependent Switch of α2/α3 Integrins

REFERENCES

• Abo, A., E. Pick, A. Hall, N. Totty, C. G. Teahan, and A. W. Segal. 1991. Activation of the NADPH oxidase involves the small GTP-binding protein p21rac1. Nature 353:668–670.
   PubMed Web of Science ®Google Scholar
• Amano, M., Y. Fukata, and K. Kaibuchi. 2000. Regulation and functions of Rho-associated kinase. Exp. Cell Res. 261:44–51.
   PubMed Web of Science ®Google Scholar
• Bradley, W. D., S. E. Hernandez, J. Settleman, and A. J. Koleske. 2006. Integrin signaling through Arg activates p190RhoGAP by promoting its binding to p120RasGAP and recruitment to the membrane. Mol. Biol. Cell 17:4827–4836.
   PubMed Web of Science ®Google Scholar
• Chiarugi, P., G. Pani, E. Giannoni, L. Taddei, R. Colavitti, G. Raugei, M. Symons, S. Borrello, T. Galeotti, and G. Ramponi. 2003. Reactive oxygen species as essential mediators of cell adhesion: the oxidative inhibition of a FAK tyrosine phosphatase is required for cell adhesion. J. Cell Biol. 161:933–944.
   PubMed Web of Science ®Google Scholar
• Danen, E. H., J. van Rheenen, W. Franken, S. Huveneers, P. Sonneveld, K. Jalink, and A. Sonnenberg. 2005. Integrins control motile strategy through a Rho-cofilin pathway. J. Cell Biol. 169:515–526.
   PubMed Web of Science ®Google Scholar
• de Carvalho, D. D., A. Sadok, V. Bourgarel-Rey, F. Gattacceca, C. Penel, M. Lehmann, and H. Kovacic. 2008. Nox1 downstream of 12-lipoxygenase controls cell proliferation but not cell spreading of colon cancer cells. Int. J. Cancer 122:1757–1764.
   PubMed Web of Science ®Google Scholar
• del Pozo, M. A., L. S. Price, N. B. Alderson, X. D. Ren, and M. A. Schwartz. 2000. Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK. EMBO J. 19:2008–2014.
   PubMed Web of Science ®Google Scholar
• Dunn, G. A., and G. E. Jones. 2004. Cell motility under the microscope: Vorsprung durch Technik. Nat. Rev. Mol. Cell Biol. 5:667–672.
   PubMedGoogle Scholar
• Fantini, J., B. Abadie, A. Tirard, L. Remy, J. P. Ripert, A. el Battari, and J. Marvaldi. 1986. Spontaneous and induced dome formation by two clonal cell populations derived from a human adenocarcinoma cell line, HT29. J. Cell Sci. 83:235–249.
   PubMed Web of Science ®Google Scholar
• Friedl, P., and K. Wolf. 2003. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat. Rev. Cancer 3:362–374.
   PubMed Web of Science ®Google Scholar
• Geiszt, M., and T. L. Leto. 2004. The Nox family of NAD(P)H oxidases: host defense and beyond. J. Biol. Chem. 279:51715–51718.
   PubMed Web of Science ®Google Scholar
• Gianni, D., B. Bohl, S. A. Courtneidge, and G. M. Bokoch. 2008. The involvement of the tyrosine kinase c-Src in the regulation of reactive oxygen species generation mediated by NADPH oxidase-1. Mol. Biol. Cell 19:2984–2994.
   PubMed Web of Science ®Google Scholar
• Hall, A. 2005. Rho GTPases and the control of cell behaviour. Biochem. Soc. Trans. 33:891–895.
   PubMed Web of Science ®Google Scholar
• Hanahan, D., and R. A. Weinberg. 2000. The hallmarks of cancer. Cell 100:57–70.
   PubMed Web of Science ®Google Scholar
• Haurani, M. J., M. E. Cifuentes, A. D. Shepard, and P. J. Pagano. 2008. Nox4 oxidase overexpression specifically decreases endogenous Nox4 mRNA and inhibits angiotensin II-induced adventitial myofibroblast migration. Hypertension 52:143–149.
   PubMed Web of Science ®Google Scholar
• Hilenski, L. L., R. E. Clempus, M. T. Quinn, J. D. Lambeth, and K. K. Griendling. 2004. Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 24:677–683.
   PubMed Web of Science ®Google Scholar
• Hordijk, P. L. 2006. Regulation of NADPH oxidases: the role of Rac proteins. Circ. Res. 98:453–462.
   PubMed Web of Science ®Google Scholar
• Huang, T. Y., C. DerMardirossian, and G. M. Bokoch. 2006. Cofilin phosphatases and regulation of actin dynamics. Curr. Opin. Cell Biol. 18:26–31.
   PubMed Web of Science ®Google Scholar
• Knaus, U. G., P. G. Heyworth, T. Evans, J. T. Curnutte, and G. M. Bokoch. 1991. Regulation of phagocyte oxygen radical production by the GTP-binding protein Rac 2. Science 254:1512–1515.
   PubMed Web of Science ®Google Scholar
• Kwon, J., S. R. Lee, K. S. Yang, Y. Ahn, Y. J. Kim, E. R. Stadtman, and S. G. Rhee. 2004. Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors. Proc. Natl. Acad. Sci. USA 101:16419–16424.
   PubMed Web of Science ®Google Scholar
• Lambeth, J. D. 2004. NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4:181–189.
   PubMed Web of Science ®Google Scholar
• Li, Q., Y. Zhang, J. J. Marden, B. Banfi, and J. F. Engelhardt. 2008. Endosomal NADPH oxidase regulates c-Src activation following hypoxia/reoxygenation injury. Biochem. J. 411:531–541.
   PubMed Web of Science ®Google Scholar
• Liu, R., B. Li, and M. Qiu. 2001. Elevated superoxide production by active H-ras enhances human lung WI-38VA-13 cell proliferation, migration and resistance to TNF-α. Oncogene 20:1486–1496.
   PubMed Web of Science ®Google Scholar
• Llobet, A., V. Beaumont, and L. Lagnado. 2003. Real-time measurement of exocytosis and endocytosis using interference of light. Neuron 40:1075–1086.
   PubMedGoogle Scholar
• Macé, G., M. Miaczynska, M. Zerial, and A. R. Nebreda. 2005. Phosphorylation of EEA1 by p38 MAP kinase regulates mu opioid receptor endocytosis. EMBO J. 24:3235–3246.
   PubMed Web of Science ®Google Scholar
• Margadant, C., K. Raymond, M. Kreft, N. Sachs, H. Janssen, and A. Sonnenberg. 2009. Integrin α3β1 inhibits directional migration and wound re-epithelialization in the skin. J. Cell Sci. 122:278–288.
   PubMedGoogle Scholar
• Matsumura, F. 2005. Regulation of myosin II during cytokinesis in higher eukaryotes. Trends Cell Biol. 15:371–377.
   PubMed Web of Science ®Google Scholar
• Meng, D., D.-D. Lv, and J. Fang. 2008. Insulin-like growth factor-I induces reactive oxygen species production and cell migration through Nox4 and Rac1 in vascular smooth muscle cells. Cardiovasc. Res. 80:299–308.
   PubMed Web of Science ®Google Scholar
• Moissoglu, K., and M. A. Schwartz. 2006. Integrin signalling in directed cell migration. Biol. Cell 98:547–555.
   PubMed Web of Science ®Google Scholar
• Moldovan, L., N. I. Moldovan, R. H. Sohn, S. A. Parikh, and P. J. Goldschmidt-Clermont. 2000. Redox changes of cultured endothelial cells and actin dynamics. Circ. Res. 86:549–557.
   PubMed Web of Science ®Google Scholar
• Nimnual, A. S., L. J. Taylor, and D. Bar-Sagi. 2003. Redox-dependent downregulation of Rho by Rac. Nat. Cell Biol. 5:236–241.
   PubMed Web of Science ®Google Scholar
• Palecek, S. P., J. C. Loftus, M. H. Ginsberg, D. A. Lauffenburger, and A. F. Horwitz. 1997. Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 385:537–540.
   PubMed Web of Science ®Google Scholar
• Pankov, R., Y. Endo, S. Even-Ram, M. Araki, K. Clark, E. Cukierman, K. Matsumoto, and K. M. Yamada. 2005. A Rac switch regulates random versus directionally persistent cell migration. J. Cell Biol. 170:793–802.
   PubMedGoogle Scholar
• Pegtel, D. M., S. I. Ellenbroek, A. E. Mertens, R. A. van der Kammen, J. de Rooij, and J. G. Collard. 2007. The Par-Tiam1 complex controls persistent migration by stabilizing microtubule-dependent front-rear polarity. Curr. Biol. 17:1623–1634.
   PubMed Web of Science ®Google Scholar
• Pellinen, T., A. Arjonen, K. Vuoriluoto, K. Kallio, J. A. Fransen, and J. Ivaska. 2006. Small GTPase Rab21 regulates cell adhesion and controls endosomal traffic of β1-integrins. J. Cell Biol. 173:767–780.
   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 actin stress fibers in response to growth factors. Cell 70:389–399.
   PubMed Web of Science ®Google Scholar
• Ridley, A. J., M. A. Schwartz, K. Burridge, R. A. Firtel, M. H. Ginsberg, G. Borisy, J. T. Parsons, and A. R. Horwitz. 2003. Cell migration: integrating signals from front to back. Science 302:1704–1709.
   PubMed Web of Science ®Google Scholar
• Sadok, A., V. Bourgarel-Rey, F. Gattacceca, C. Penel, M. Lehmann, and H. Kovacic. 2008. Nox1-dependent superoxide production controls colon adenocarcinoma cell migration. Biochim. Biophys. Acta 1783:23–33.
   PubMed Web of Science ®Google Scholar
• Sahai, E., and C. J. Marshall. 2003. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat. Cell Biol. 5:711–719.
   PubMed Web of Science ®Google Scholar
• Schröder, K., I. Helmcke, K. Palfi, K. H. Krause, R. Busse, and R. P. Brandes. 2007. Nox1 mediates basic fibroblast growth factor-induced migration of vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 27:1736–1743.
   PubMedGoogle Scholar
• Shinohara, M., W. H. Shang, M. Kubodera, S. Harada, J. Mitsushita, M. Kato, H. Miyazaki, H. Sumimoto, and T. Kamata. 2007. Nox1 redox signaling mediates oncogenic Ras-induced disruption of stress fibers and focal adhesions by down-regulating Rho. J. Biol. Chem. 282:17640–17648.
   PubMed Web of Science ®Google Scholar
• Suh, Y. A., R. S. Arnold, B. Lassegue, J. Shi, X. Xu, D. Sorescu, A. B. Chung, K. K. Griendling, and J. D. Lambeth. 1999. Cell transformation by the superoxide-generating oxidase Mox1. Nature 401:79–82.
   PubMed Web of Science ®Google Scholar
• Terada, L. S. 2006. Specificity in reactive oxidant signaling: think globally, act locally. J. Cell Biol. 174:615–623.
   PubMed Web of Science ®Google Scholar
• Ushio-Fukai, M. 2006. Localizing NADPH oxidase-derived ROS. Sci. STKE 2006:re8.
   PubMedGoogle Scholar
• Ushio-Fukai, M., and R. W. Alexander. 2004. Reactive oxygen species as mediators of angiogenesis signaling: role of NAD(P)H oxidase. Mol. Cell. Biochem. 264:85–97.
   PubMed Web of Science ®Google Scholar
• van der Bij, G. J., S. J. Oosterling, M. Bogels, F. Bhoelan, D. M. Fluitsma, R. H. Beelen, S. Meijer, and M. van Egmond. 2008. Blocking α2 integrins on rat CC531s colon carcinoma cells prevents operation-induced augmentation of liver metastases outgrowth. Hepatology 47:532–543.
   PubMedGoogle Scholar
• van der Flier, A., and A. Sonnenberg. 2001. Function and interactions of integrins. Cell Tissue Res. 305:285–298.
   PubMed Web of Science ®Google Scholar
• Verschueren, H. 1985. Interference reflection microscopy in cell biology: methodology and applications. J. Cell Sci. 75:279–301.
   PubMedGoogle Scholar
• Wesley, U. V., P. F. Bove, M. Hristova, S. McCarthy, and A. van der Vliet. 2007. Airway epithelial cell migration and wound repair by ATP-mediated activation of dual oxidase 1. J. Biol. Chem. 282:3213–3220.
   PubMedGoogle Scholar
• White, D. P., P. T. Caswell, and J. C. Norman. 2007. αvβ3 and α5β1 integrin recycling pathways dictate downstream Rho kinase signaling to regulate persistent cell migration. J. Cell Biol. 177:515–525.
   PubMed Web of Science ®Google Scholar
• Wolf, K., I. Mazo, H. Leung, K. Engelke, U. H. von Andrian, E. I. Deryugina, A. Y. Strongin, E. B. Brocker, and P. Friedl. 2003. Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 160:267–277.
   PubMed Web of Science ®Google Scholar
• Woods Ignatoski, K. M., N. K. Grewal, S. Markwart, D. L. Livant, and S. P. Ethier. 2003. p38MAPK induces cell surface α4 integrin downregulation to facilitate erbB-2-mediated invasion. Neoplasia 5:128–134.
   PubMedGoogle Scholar
• Worthylake, R. A., and K. Burridge. 2003. RhoA and ROCK promote migration by limiting membrane protrusions. J. Biol. Chem. 278:13578–13584.
   PubMedGoogle Scholar
• Wu, R. F., Y. C. Xu, Z. Ma, F. E. Nwariaku, G. A. Sarosi, Jr., and L. S. Terada. 2005. Subcellular targeting of oxidants during endothelial cell migration. J. Cell Biol. 171:893–904.
   PubMed Web of Science ®Google Scholar
• Yamaguchi, H., J. Wyckoff, and J. Condeelis. 2005. Cell migration in tumors. Curr. Opin. Cell Biol. 17:559–564.
   PubMed Web of Science ®Google Scholar
• Zwang, Y., and Y. Yarden. 2006. p38 MAP kinase mediates stress-induced internalization of EGFR: implications for cancer chemotherapy. EMBO J. 25:4195–4206.
   PubMed Web of Science ®Google Scholar