p27Kip1 modulates cell migration through the regulation of RhoA activation

Genes and Development

Volumn 18, Issue 8, 2004, Pages 862-876

  Besson, Arnaud ^a   Gurian West, Mark ^a   Schmidt, Anja ^b   Hall, Alan ^b   Roberts, James M ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Actin stress fibers; Migration; p27Kip1; Ras; Rho; ROCK

Indexed keywords

ACTIN; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE INHIBITOR; CYCLINE; GROWTH FACTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN P27; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; CDKN1A PROTEIN, MOUSE; CDKN1B PROTEIN, MOUSE; CELL CYCLE PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 1B; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; FOCAL ADHESION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; STRESS FIBER; ANIMAL; CELL MOTION; METABOLISM; MOUSE; PHYSIOLOGY;

ACTINS; ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; CELL MOVEMENT; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYCLINS; MICE; RHOA GTP-BINDING PROTEIN; STRESS FIBERS; TUMOR SUPPRESSOR PROTEINS;

EID: 1942466518     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1185504     Document Type: Article

References (62)

1. Amano, A., Chihara, K., Kimura, K., Fukata, Y., Nakamura, N., Matsuura, Y., and Kaibuchi, K. 1997. Formation of actin stress fibers and focal adhesions enhanced by rho-kinase. Science 275: 1308-1311.
2. Kip1 expression and progression in human esophageal squamous cell carcinoma. Int. J. Cancer 79: 439-443.
3. Arthur, W.T. and Burridge, K. 2001. RhoA inactivation by p190RhoGAP regulates cell spreading and migration by promoting membrane protrusion and polarity. Mol. Biol. Cell 12: 2711-2720.
4. Arthur, W.T., Petch, L.A., and Burridge, K. 2000. Integrin engagement suppresses RhoA activity via a c-Src-dependent mechanism. Curr. Biol. 10: 719-722.
5. Bar-Sagi, D. and Hall, A. 2000. Ras and Rho GTPases: A family reunion. Cell 103: 227-238.
6. Besson, A., Wilson, T.L., and Yong, V.W. 2002. The anchoring protein RACK1 links protein kinase C ε to integrin β chains. J. Biol. Chem. 277: 22073-22084.
7. Bloom, J. and Pagano, M. 2003. Deregulated degradation of the CDK inhibitor p27 and malignant transformation. Semin. Cancer Biol. 13: 41-47.
8. Kip1 and regulates cell cycle progression. EMBO J. 21: 3390-3401.
9. Chrzanowska-Wodnicka, M. and Burridge, K. 1996. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell. Biol. 133: 1403-1415.
10. Coqueret, O. 2003. New roles for p21 and p27 cell cycle inhibitors: A function for each cell compartment. Trends Cell Biol. 13: 65-70.
11. Cox, E.A., Sastry, S.K., and Huttenlocher, A. 2001. Integrin-mediated adhesion regulates cell polarity and membrane protrusion through the Rho family of GTPases. Mol. Biol. Cell 12: 265-277.
12. Kip1, cyclin E and c-myc expression with progression and prognosis in HPV-positive cervical neoplasms. Anticancer Res. 18: 3991-3998.
13. Kip1/cyclin-dependent kinase/Retinoblastoma pathway in vascular smooth muscle cells and fibroblasts. Circ Res. 92: 402-410.
14. Etienne-Manneville, S. and Hall, A. 2002. Rho GTPases in cell biology. Nature 420: 629-635.
15. Frost, J.A., Khokhlatchev, A., Stippec, S., White, M.A., and Cobb, M.H. 1998. Differential effects of PAK1-activating mutations reveal activity-dependent and -independent effects on cytoskeletal regulation. J. Biol. Chem. 273: 28191-28198.
16. Kip1 by doxycycline-regulated adenoviral vectors inhibits endothelial cell proliferation and migration and impairs angiogenesis. FASEB J. 15: 1877-1885.
17. Kip1 degradation through its regulation of cyclin E/CDK2 activity. J. Biol. Chem. 274: 3396-3401.
18. Kip1 on serine 10 is required for its binding to CRM1 and nuclear export. J. Biol. Chem. 277: 14355-14358.
19. Kimura, K., Ito, M., Amano, M., Chihara, K., Fukata, Y., Nakafuku, M., Yamamori, B., Feng, J., Nakano, T., Okawa, K., et al. 1996. Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273: 245-248.
20. Kouvaraki, M., Gorgoulis, V.G., Rassidakis, G.Z., Liodis, P., Markopoulos, C., Gogas, J., and Kittas, C. 2002. High expression levels of p27 correlate with lymph node status in a subset of advanced invasive breast carcinomas. Cancer 94: 2454-2465.
21. Cip1 is involved in Ras-induced inhibition of the ROCK/LIMK/Cofilin pathway. J. Biol. Chem. 279: 1885-1891.
22. Leung, T., Chen, X.Q., Manser, E., and Lim, L. 1996. The p160 RhoA-binding kinase ROKa is a member of a kinase family and is involved in the reorganization of the cytoskeleton. Mol. Cell. Biol. 16: 5313-5327.
23. Malliri, A., ten Klooster, J.P., Olivio, C., and Collard, J.G. 2000. Determination of the activity of Rho-like GTPases in cells. Methods Mol. Biol. 189: 99-109.
24. Manser, E., Huang, H.Y., Loo, T.H., Chen, X.Q., Dong, J.M., Leung, T., and Lim, L. 1997. Expression of constitutively active α-PAK reveals effects of the kinase on actin and focal complexes. Mol. Cell. Biol. 17: 1129-1143.
25. kip1 C-terminal scatter domain mediates Rac-dependent cell migration independent of cell cycle arrest functions. Mol. Cell. Biol. 23: 216-228.
26. McFall, A., Ulku, A., Lambert, Q.T., Kusa, A., Rogers-Graham, K., and Der, C.J. 2001. Oncogenic ras blocks anoikis by activation of a novel effector pathway independent of phosphatidylinositol 3-kinase. Mol. Cell. Biol. 21: 5488-5499.
27. Kip1 inhibition of Grb2-Sos formation can regulate Ras activation. Mol. Cell. Biol. 23: 3735-3752.
28. Kip1 induces cell migration. Nat. Med. 4: 1449-1452.
29. Nobes, C. and Hall, A. 1999. Rho GTPases control polarity, protrusion, and adhesion during cell movement. J. Cell. Biol. 144: 1235-1244.
30. Waf1/Cip1. Nature 394: 295-299.
31. Kip1: Regulation and function of a haploinsufficient tumor suppressor and its misregulation in cancer. Exp. Cell Res. 264: 148-168.
32. Ren, X.D., Kiosses, W.B., and Schwartz, M.A. 1999. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 18: 578-585.
33. Ren, X.D., Kiosses, W.B., Sieg, D.J., Otey, C.A., Schlaepfer, D.D., and Schwartz, M.A. 2000. Focal adhesion kinase suppresses Rho activity to promote focal adhesion turnover. J. Cell Sci. 113: 3637-3678.
34. Ridley, A.J. and Hall, A. 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.
35. Ridley, A.J., Paterson, H.F., Johnston, C.L., Diekmann, D., and Hall, A. 1992. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70: 401-410.
36. Ridley, A.J., Schwartz, M.A., Burridge, K., Firtel, R., Ginsberg, M., Borisy, G., Parsons, J.T., and Horwitz, A.F. 2003. Cell migration: Integrating signals from front to back. Science 302: 1704-1709.
37. Rodier, G., Montaglioni, A., Di Marcotullio, L., Coulombe, P., Draetta, G., Pagano, M., and Meloche, S. 2001. p27 cytoplasmic localization is regulated by phosphorylation on Ser 10 and is not a prerequisite for its proteolysis. EMBO J. 20: 6672-6682.
38. Kip1 is abnormally expressed in diffuse large B-cell lymphomas and is associated with an adverse clinical outcome. Br. J. Cancer 80: 1427-1434.
39. Sahai, E., Olson, M.F., and Marshall, C.J. 2001. Cross-talk between Ras and Rho signalling pathways in transformation favours proliferation and increased motility. EMBO J. 20: 755-766.
40. Kip1-cyclin D3 colocalization in tumor cells. Blood 94: 765-772.
41. Sander, E.E., van Delft, S., ten Klooster, J.P., Reid, T., van Der Kammen, R.A., Michiels, F., and Collard, J.G. 1998. Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase. J. Cell. Biol. 143: 1385-1398.
42. Schmidt, A. and Hall, A. 2002. Guanine nucleotide exchange factors for Rho GTPases: Turning on the switch. Genes & Dev. 16: 1587-1609.
43. Seasholtz, T.M., Majumdar, M., and Brown, J.H. 1999. Rho as a mediator of G protein-coupled receptor signaling. Mol. Pharmacol. 55: 949-956.
44. Sherr, C.J. and Roberts, J.M. 2001. CDK inhibitors: Positive and negative regulators of G1-phase progression. Genes & Dev. 13: 1501-1512.
45. Shimada, Y., Gulli, M., and Peter, M. 2000. Nuclear sequestration of the exchange factor Cdc24 by Far1 regulates cell polarity during yeast mating. Nat. Cell Biol. 2: 117-124.
46. Kip1 in normal squamous epithelium, cervical intraepithelial neoplasia, and invasive squamous cell carcinoma of the uterine cervix. Cancer 92: 3005-3011.
47. Slingerland, J. and Pagano, M. 2000. Regulation of the CDK inhibitor p27 and its deregulation in cancer. J. Cell Physiol. 183: 10-17.
48. Spector, D.L. 1997. Isolation of fibroblasts. In Cells: A laboratory manual (eds. D. Spector et al.), pp. 4.3-4.7. Cold Spring Harbor Laboratory Press, New York.
49. Kip1. J. Biol. Chem. 276: 12084-12090.
50. Kip1 in vascular smooth muscle cell migration. Circulation 103: 2967-2972.
51. Kip1 on the ability of invasion and metastasis of an oral cancer cell line. Oncol. Rep. 10: 527-532.
52. Cip1/Waf1 regulates neurite remodeling by inhibiting Rho-kinase activity. J. Cell. Biol. 158: 321-329.
53. Todaro, G.J. and Green, H. 1963. Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell. Biol. 17: 299-313.
54. Vial, E., Sahai, E., and Marshall, C.J. 2003. ERK-MAPK signaling coordinately regulates activity of Rac1 and RhoA for tumor cell motility. Cancer Cell 4: 67-79.
55. V12-induced transformation in a manner dependent on p27 status. J. Biol. Chem. 277: 16433-16440.
56. Kip1. EMBO J. 16: 5334-5344.
57. Kip1 in chronic B-cell lymphocytic leukemia. Blood 91: 4694-4700.
58. Watanabe, J., Sato, H., Kanai, T., Kamata, Y., Jobo, T., Hata, H., Fujisawa, T., Ohno, E., Kameya, T., and Kuramoto, H. 2002. Paradoxical expression of cell cycle inhibitor p27 in endometrioid adenocarcinomas of the uterine corpus with proliferation and clinicopathological parameters. Br. J. Cancer 87: 81-85.
59. Webb, D.J., Parsons, J.T., and Horwitz, A.F. 2002. Adhesion assembly, disassembly and turnover in migrating cells - Over and over and over again. Nat. Cell Biol. 4: E97-E100.
60. Kip1. J. Biol. Chem. 272: 32966-32971.
61. Worthylake, R., Lemoine, S., Watson, J., and Burridge, K. 2001. RhoA is required for monocyte tail retraction during transendothelial migration. J. Cell. Biol. 154: 147-160.
62. Kip2 regulates actin dynamics by binding and translocating LIM-kinase 1 to the nucleus. J. Biol. Chem. 278: 52919-52923.