p27^kip1 Controls Cell Morphology and Motility by Regulating Microtubule-Dependent Lipid Raft Recycling

REFERENCES

• Balasubramanian, N., D. W. Scott, J. D. Castle, J. E. Casanova, and M. A. Schwartz. 2007. Arf6 and microtubules in adhesion-dependent trafficking of lipid rafts. Nat. Cell Biol. 12:1381–1391.
   Google Scholar
• Baldassarre, G., B. Belletti, M. S. Nicoloso, M. Schiappacassi, A. Vecchione, P. Spessotto, A. Morrione, V. Canzonieri, and A. Colombatti. 2005. p27(Kip1)-stathmin interaction influences sarcoma cell migration and invasion. Cancer Cell 7:51–63.
   PubMed Web of Science ®Google Scholar
• Belletti, B., M. S. Nicoloso, M. Schiappacassi, S. Berton, F. Lovat, K. Wolf, V. Canzonieri, S. D'Andrea, A. Zucchetto, P. Friedl, A. Colombatti, and G. Baldassarre. 2008. Stathmin activity influences sarcoma cell shape, motility, and metastatic potential. Mol. Biol. Cell 19:2003–2013.
   PubMedGoogle Scholar
• Belletti, B., M. S. Nicoloso, M. Schiappacassi, E. Chimienti, S. Berton, F. Lovat, A. Colombatti, and G. Baldassarre. 2005. p27(kip1) functional regulation in human cancer: a potential target for therapeutic designs. Curr. Med. Chem. 12:1589–1605.
   PubMedGoogle Scholar
• Berton, S., B. Belletti, K. Wolf, V. Canzonieri, F. Lovat, A. Vecchione, A. Colombatti, P. Friedl, and G. Baldassarre. 2009. The tumor suppressor functions of p27(kip1) include control of the mesenchymal/amoeboid transition. Mol. Cell. Biol. 29:5031–5045.
   PubMed Web of Science ®Google Scholar
• Besson, A., M. Gurian-West, A. Schmidt, A. Hall, and J. M. Roberts. 2004. p27Kip1 modulates cell migration through the regulation of RhoA activation. Genes Dev. 18:862–876.
   PubMed Web of Science ®Google Scholar
• Besson, A., H. C. Hwang,S. Cicero, S. L. Donovan, M. Gurian-West, D. Johnson, B. E. Clurman, M. A. Dyer, and J. M. Roberts. 2007. Discovery of an oncogenic activity in p27Kip1 that causes stem cell expansion and a multiple tumor phenotype. Genes Dev. 21:1731–1746.
   PubMed Web of Science ®Google Scholar
• Boehm, M., M. Olive, A. L. True, M. F. Crook, H. San, X. Qu, and E. G. Nabel. 2004. Bone marrow-derived immune cells regulate vascular disease through a p27(Kip1)-dependent mechanism. J. Clin. Invest. 114:419–426.
   PubMedGoogle Scholar
• Borghese, L., G. Fletcher, J. Mathieu, A. Atzberger, W. C. Eades, R. L. Cagan, and P. Rorth. 2006. Systematic analysis of the transcriptional switch inducing migration of border cells. Dev. Cell 10:497–508.
   PubMedGoogle Scholar
• Burridge, K., and K. Wennerberg. 2004. Rho and Rac take center stage. Cell 116:167–179.
   PubMed Web of Science ®Google Scholar
• Chang, Y. C., P. Nalbant, J. Birkenfeld, Z. F. Chang, and G. M. Bokoch. 2008. GEF-H1 couples nocodazole-induced microtubule disassembly to cell contractility via RhoA. Mol. Biol. Cell 19:2147–2153.
   PubMed Web of Science ®Google Scholar
• Degani, S., F. Balzac, M. Brancaccio, S. Guazzone, S. F. Retta, L. Silengo, A. Eva, and G. Tarone. 2002. The integrin cytoplasmic domain-associated protein ICAP-1 binds and regulates Rho family GTPases during cell spreading. J. Cell Biol. 156:277–287.
   Google Scholar
• del Pozo, M. A., N. Balasubramanian, N. B. Alderson, W. B. Kiosses, A. Grande-García, R. G. Anderson, and M. A. Schwartz. 2005. Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nat. Cell Biol. 7:901–908.
   PubMed Web of Science ®Google Scholar
• Etienne-Manneville, S. 2004. Actin and microtubules in cell motility: which one is in control? Traffic 5:470–477.
   PubMed Web of Science ®Google Scholar
• Fero, M. L., E. Randel, K. E. Gurley, J. M. Roberts, and C. J. Kemp. 1998. The murine gene p27Kip1 is haplo-insufficient for tumour suppression. Nature 396:177–180.
   PubMed Web of Science ®Google Scholar
• Fero, M. L., M. Rivkin, M. Tasch, P. Porter, C. E. Carow, E. Firpo, K. Polyak, L. H. Tsai, V. Broudy, R. M. Perlmutter, K. Kaushansky, and J. M. Roberts. 1996. A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27(Kip1)-deficient mice. Cell 85:733–744.
   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
• Goukassian, D., A. Diez-Juan, T. Asahara, P. Schratzberger, M. Silver, T. Murayama, J. M. Isner, and V. Andrés. 2001. Overexpression of p27(Kip1) by doxycycline-regulated adenoviral vectors inhibits endothelial cell proliferation and migration and impairs angiogenesis. FASEB J. 15:1877–1885.
   PubMed Web of Science ®Google Scholar
• Jin, K., X. O. Mao, B. Cottrell, B. Schilling, L. Xie, R. H. Row, Y. Sun, A. Peel, J. Childs, G. Gendeh, B. W. Gibson, and D. A. Greenberg. 2004. Proteomic and immunochemical characterization of a role for Stathmin in adult neurogenesis. FASEB J. 18:287–299.
   PubMed Web of Science ®Google Scholar
• Kawauchi, T., K. Chihama, Y. Nabeshima, and M. Hoshino. 2006. Cdk5 phosphorylates and stabilizes p27kip1 contributing to actin organization and cortical neuronal migration. Nat. Cell Biol. 8:17–26.
   PubMed Web of Science ®Google Scholar
• Krendel, M., F. T. Zenke, and G. M. Bokoch. 2002. Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat. Cell Biol. 4:294–301.
   PubMed Web of Science ®Google Scholar
• Langenickel, T. H., M. Olive, M. Boehm, H. San, M. F. Crook, and E. G. Nabel. 2008. KIS protects against adverse vascular remodeling by opposing Stathmin-mediated VSMC migration in mice. J. Clin. Invest. 118:3848–3859.
   PubMedGoogle Scholar
• Li, Z., X. Jiao, C. Wang, X. Ju, Y. Lu, L. Yuan, M. P. Lisanti, S. Katiyar, and R. G. Pestell. 2006. Cyclin D1 induction of cellular migration requires p27(KIP1). Cancer Res. 66:9986–9994.
   PubMed Web of Science ®Google Scholar
• Li, Z., C. Wang, X. Jiao, S. Katiyar, M. C. Casimiro, G. C. Prendergast, M. J. Powell, and R. G. Pestell. 2008. Alternate cyclin D1 mRNA splicing modulates p27KIP1 binding and cell migration. J. Biol. Chem. 283:7007–7015.
   PubMed Web of Science ®Google Scholar
• Liakopoulos, D., J. Kusch, S. Grava, J. Vogel, and Y. Barral. 2003. Asymmetric loading of Kar9 onto spindle poles and microtubules ensures proper spindle alignment. Cell 112:561–574.
   PubMedGoogle Scholar
• Maaser, K., K. Wolf, C. E. Klein, B. Niggemann, K. S. Zänker, E. B. Brocker, and P. Friedl. 1999. Functional hierarchy of simultaneously expressed adhesion receptors: integrin α2β1 but not CD44 mediates MV3 melanoma cell migration and matrix reorganization within three-dimensional hyaluronan-containing collagen matrices. Mol. Biol. Cell 10:3067–3079.
   PubMedGoogle Scholar
• Macia, E., M. Ehrlich, R. Massol, E. Boucrot, C. Brunner, and T. Kirchhausen. 2006. Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 10:839–850.
   PubMed Web of Science ®Google Scholar
• Maekawa, H., T. Usui, M. Knop, and E. Schiebel. 2003. Yeast Cdk1 translocates to the plus end of cytoplasmic microtubules to regulate bud cortex interactions. EMBO J. 22:438–449.
   PubMed Web of Science ®Google Scholar
• Manes, T., D. Q. Zheng, S. Tognin, A. S. Woodard, P. C. Marchisio, and L. R. Languino. 2003. αvβ3 integrin expression up-regulates cdc2, which modulates cell migration. J. Cell Biol. 161:817–826.
   PubMed Web of Science ®Google Scholar
• Marklund, U., O. Osterman, H. Melander, A. Bergh, and M. Gullberg. 1994. The phenotype of a “Cdc2 kinase target site-deficient” mutant of oncoprotein 18 reveals a role of this protein in cell cycle control. J. Biol. Chem. 269:30626–30635.
   PubMedGoogle Scholar
• McAllister, S. S., M. Becker-Hapak, G. Pintucci, M. Pagano, and S. F. Dowdy. 2003. Novel p27(kip1) C-terminal scatter domain mediates Rac-dependent cell migration independent of cell cycle arrest functions. Mol. Cell. Biol. 23:216–228.
   PubMed Web of Science ®Google Scholar
• Moffat, J., D. A. Grueneberg, X. Yang, S. Y. Kim, A. M. Kloepfer, G. Hinkle, B. Piqani, T. M. Eisenhaure, B. Luo, J. K. Grenier, A. E. Carpenter, S. Y. Foo, S. A. Stewart, B. R. Stockwell, N. Hacohen, W. C. Hahn, E. S. Lander, D. M. Sabatini, and D. E. Root. 2006. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124:1283–1298.
   PubMed Web of Science ®Google Scholar
• Muraoka, R. S., A. E. Lenferink, B. Law, E. Hamilton, D. M. Brantley, L. R. Roebuck, and C. L. Arteaga. 2002. ErbB2/Neu-induced, cyclin D1-dependent transformation is accelerated in p27-haploinsufficient mammary epithelial cells but impaired in p27-null cells. Mol. Cell. Biol. 22:2204–2219.
   PubMed Web of Science ®Google Scholar
• Nickeleit, I., S. Zender, F. Sasse, R. Geffers, G. Brandes, I. Sorensen, H. Steinmetz, S. Kubicka, T. Carlomagno, D. Menche, I. Gutgemann, J. Buer, A. Gossler, M. P. Manns, M. Kalesse, R. Frank, and N. P. Malek. 2008. Argyrin A reveals a critical role for the tumor suppressor protein p27(kip1) in mediating antitumor activities in response to proteasome inhibition. Cancer Cell 8:23–35.
   Google Scholar
• Ozon, S., A. Guichet, O. Gavet, S. Roth, and A. Sobel. 2002. Drosophila Stathmin: a microtubule-destabilizing factor involved in nervous system formation. Mol. Biol. Cell 13:698–710.
   PubMedGoogle Scholar
• Palazzo, A. F., C. H. Eng, D. D. Schlaepfer, E. E. Marcantonio, and G. G. Gundersen. 2004. Localized stabilization of microtubules by integrin- and FAK-facilitated Rho signaling. Science 303:836–839.
   PubMedGoogle Scholar
• Sahai, E., R. Garcia-Medina, J. Pouysségur, and E. Vial. 2007. Smurf1 regulates tumor cell plasticity and motility through degradation of RhoA leading to localized inhibition of contractility. J. Cell Biol. 176:35–42.
   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
• Sahai, E. 2007. Illuminating the metastatic process. Nat. Rev. Cancer 7:737–749.
   PubMed Web of Science ®Google Scholar
• Schiappacassi, M., F. Lovat, V. Canzonieri, B. Belletti, S. Berton, D. Di Stefano, A. Vecchione, A. Colombatti, and G. Baldassarre. 2008. p27Kip1 expression inhibits glioblastoma growth, invasion, and tumor-induced neoangiogenesis. Mol. Cancer Ther. 7:1164–1175.
   PubMed Web of Science ®Google Scholar
• Schubart, U. K., J. Yu, J. A. Amat, Z. Wang, M. K. Hoffmann, and W. Edelmann. 1996. Normal development of mice lacking metablastin (P19), a phosphoprotein implicated in cell cycle regulation. J. Biol. Chem. 271:14062–14066.
   PubMedGoogle Scholar
• Shima, T., S. Nada, and M. Okada. 2003. Transmembrane phosphoprotein Cbp senses cell adhesion signaling mediated by Src family kinase in lipid rafts. Proc. Natl. Acad. Sci. U. S. A. 100:14897–14902.
   PubMed Web of Science ®Google Scholar
• Siegrist, S. E., and C. Q. Doe. 2007. Microtubule-induced cortical cell polarity. Genes Dev. 21:483–496.
   PubMed Web of Science ®Google Scholar
• Tanaka, Y., S. Hamano, K. Gotoh, Y. Murata, Y. Kunisaki, A. Nishikimi, R. Takii, M. Kawaguchi, A. Inayoshi, S. Masuko, K. Himeno, T. Sasazuki, and Y. Fukui. 2007. T helper type 2 differentiation and intracellular trafficking of the interleukin 4 receptor-alpha subunit controlled by the Rac activator Dock2. Nat. Immunol. 8:1067–1075.
   PubMedGoogle Scholar
• Vial, E., E. Sahai, and C. J. Marshall. 2003. ERK-MAPK signaling coordinately regulates Rac1 and RhoA for tumor cell motility. Cancer Cell 4:67–79.
   PubMed Web of Science ®Google Scholar
• Watabe-Uchida, M., K. A. John, J. A. Janas, S. E. Newey, and L. Van Aelst. 2006. The Rac activator DOCK7 regulates neuronal polarity through local phosphorylation of Stathmin/Op18. Neuron 51:727–739.
   PubMedGoogle Scholar
• Watanabe, T., J. Noritake, and K. Kaibuchi. 2005. Regulation of microtubules in cell migration. Trends Cell Biol. 15:76–83.
   PubMed Web of Science ®Google Scholar
• Wittmann, T., G. M. Bokoch, and C. M. Waterman-Storer. 2004. Regulation of microtubule destabilizing activity of Op18/Stathmin downstream of Rac1. J. Biol. Chem. 279:6196–6203.
   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
• Yamada, K. M., and E. Cukierman. 2007. Modeling tissue morphogenesis and cancer in 3D. Cell 130:601–610.
   PubMed Web of Science ®Google Scholar