Fibronectin matrix regulates activation of RHO and CDC42 GTPases and cell cycle progression

Journal of Cell Biology

Volumn 143, Issue 1, 1998, Pages 267-276

  Bourdoulous, Sandrine ^a,b   Orend, Gertraud ^a,c   MacKenna, Deidre A ^a,d   Pasqualini, Renata ^a   Ruoslahti, Erkki ^a  

^a BURNHAM INSTITUTE   (United States)

^b CNRS   (France)

^c FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^d Tanabe Research Laboratories   (United States)

Author keywords

Cyclin E cdk2; Extracellular matrix; F actin; Mitogen activated protein kinase (MAPK); Signal transduction

Indexed keywords

FIBRONECTIN; GUANOSINE TRIPHOSPHATASE;

ARTICLE; CELL ADHESION; CELL CYCLE; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; SIGNAL TRANSDUCTION;

ACTINS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CDC42 GTP-BINDING PROTEIN, SACCHAROMYCES CEREVISIAE; CELL CYCLE; CELL CYCLE PROTEINS; CYTOSKELETON; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; FIBROBLASTS; FIBRONECTINS; GTP PHOSPHOHYDROLASES; GTP-BINDING PROTEINS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LAMININ; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PEPTIDE FRAGMENTS; PROTEIN-TYROSINE KINASES; RECOMBINANT PROTEINS; UMBILICAL VEINS; VITRONECTIN;

EID: 0032487438     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.143.1.267     Document Type: Article

References (56)

1. Aguirre, K.M., R.J. McCormick, and J.E. Schwarzbauer. 1994. Fibronectin self-association is mediated by complementary sites within the amino-terminal one-third of the molecules. J. Biol. Chem. 269:27863-27868.
2. Assoian, R.K., and X. Zhu. 1997. Cell anchorage and the cytoskeleton as partners in growth factor dependent cell cycle progression. Curr. Opin. Cell Biol. 9:93-98.
3. Busk, M., R. Pytela, and D. Sheppard. 1992. Characterization of the integrin alphavbeta6 as a fibronectin-binding protein. J. Biol. Chem. 267:5790-5796.
4. Cavigelli, M., F. Dolfi, F.X. Claret, and M. Karin. 1995. Induction of c-fos expression through JNK mediated TCF/Elk-1 phosphorylation. EMBO (Eur. Mol. Biol. Organ.) J. 14:5957-5964.
5. Chen, Q., M.S. Kinch, T.H. Lin, K. Burridge, and R.L. Juliano. 1994. Integrin-mediated cell adhesion activates mitogen-activated protein kinases. J. Biol. Chem. 269:26602-26605.
6. Chen, W., and S. Singer. 1980. Fibronectin is not present in the focal adhesions formed between normal cultured fibroblasts and their substrata. Proc. Natl. Acad. Sci. USA. 77:7318.
7. Chen, W., and S. Singer. 1982. Immunoelectron microscopic studies of the sites of cell-substratum and cell-cell contacts in cultured fibroblasts. J. Cell Biol. 95:205-222.
8. Chen, W.T., E. Hasegawa, T. Hasegawa, C. Weinstock, and K. Yamada. 1985. Development of cell surface linkage complexes in cultured fibroblasts. J. Cell Biol. 100:1103-1114.
9. 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.
10. Coso, O.A., M. Chiariello, J.C. Yu, H. Teramoto, P. Crespo, N. Xu, T. Miki, and J.S. Gutkind. 1995. The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell. 81:1137-1146.
11. Fang, F., G. Orend, N. Watanabe, T. Hunter, and E. Ruoslahti. 1996. Dependence of cyclin E-CDK2 kinase activity on cell anchorage. Science. 271:499-502.
12. Frisch, S.M., and E. Ruoslahti. 1997. Integrins and anoikis. Curr. Opin. Cell Biol. 9:701-706.
13. Frisch, S.M., K. Vuori, D. Kelaita, and S. Sicks. 1996. A role for Jun-N-terminal kinase in anoikis; suppression by bcl-2 and crmA. J. Cell Biol. 135:1377-1382.
14. Hall, A. 1998. Rho GTPases and the actin cytoskeleton. Science. 279:509-514.
15. Hocking, D.C., J. Sottile, and J. McKeown-Longo. 1994. Fibronectin's III-1 module contain a conformation-dependent binding site for the amino-terminal region of fibronectin. J. Biol. Chem. 269:19183-19191.
16. 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.
17. Hynes, R.O. 1990. Fibronectins. Springer-Verlag, New York. 546 pp.
18. Joneson, T., M. McDonough, D. Bar-Sagi, and L. Van Aelst. 1996. RAC regulation of actin polymerization and proliferation by a pathway distinct from Jun kinase. Science. 274:1374-1376.
19. Khwaja, A., and J. Downward. 1997. Lack of correlation between activation of Jun-NH2-terminal kinase and induction of apoptosis after detachment of epithelial cells. J. Cell Biol. 139:1017-1023.
20. Kumagai, N., N. Morii, K. Fujisawa, Y. Nemoto, and S. Narumiya. 1993. ADP-rybosylation of rho p21 inhibits lysophosphatidic-acid induced protein tyrosine phosphorylation and phosphatidylinositol 3-kinase activation in cultured Swiss 3T3 cells. J. Biol. Chem. 268:24535-24538.
21. Lamarche, N., N. Tapon, L. Stowers, P.D. Burbelo, P. Aspenstrom, T. Bridges, J. Chant, and A. Hall. 1996. Rac and Cdc42 induce actin polymerization and G1 cell cycle progression independently of p65PAK and the JNK/SAPK MAP kinase cascade. Cell. 87:519-529.
22. Manser, E., C. Chong, Z.S. Zhao, T. Leung, G. Michael, C. Hall, and L. Lim. 1995. Molecular cloning of a new member of the p21-Cdc42/Rac-activated kinase (PAK) family. J. Biol. Chem. 270:25070-25078.
23. Manser, E., T. Leung, H. Salihuddin, L. Tan, and L. Lim. 1993. A non-receptor tyrosine kinase that inhibits the GTPase activity of p21cdc42. Nature. 363: 364-367.
24. Manser, E., T. Leung, H. Salihuddin, Z.S. Zhao, and L. Lim. 1994. A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature. 367: 40-46.
25. McDonald, J. 1988. Extracellular matrix assembly. Annu. Rev. Cell Biol. 4:183-207.
26. Mercurius, K.O., and A.O. Morla. 1998. Inhibition of vascular smooth muscle cell growth by inhibition of fibronectin matrix assembly. Circ. Res. 82:548-556.
27. Minden, A., A. Lin, F.X. Claret, A. Abo, and M. Karin. 1995. Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell. 81:1147-1157.
28. Molnar, A., A.M. Theodoras, L.I. Zon, and J.M. Kyriakis. 1997. Cdc42Hs, but not Rac1, inhibits serum-stimulated cell cycle progression at G1/S through a mechanism requiring p38/RK. J. Biol. Chem. 272:13229-13235.
29. Morla, A., and E. Ruoslahti. 1992. A fibronectin self-assembly site involved in fibronectin matrix assembly: reconstruction in a synthetic peptide. J. Cell Biol. 118:421-429.
30. Morla, A., Z. Zhang, and E. Ruoslahti. 1994. Superfibronectin is a functionally distinct form of fibronectin. Nature. 367:193-196.
31. Mosher, D.F. 1993. Assembly of fibronectin into extracellular matrix. Curr. Opin. Struct. Biol. 3:214-222.
32. Mosher, D.F., J. Sottile, C. Wu, and J.A. McDonald. 1992. Assembly of extracellular matrix. Curr. Opin. Cell. Biol. 4:810-818.
33. 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. 7:53-62.
34. Olson, M.F., A. Ashworth, and A. Hall. 1995. An essential role for Rho, Rac, and Cdc42 GTPases in cell cycle progression through G1. Science. 269-1270-1272.
35. Price, L.S., J. Leng, M.A. Schwartz, and G.M. Bockoch. 1998. Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol. Cell. Biol. In press.
36. Raingeaud, J., S. Gupta, J.S. Rogers, M. Dickens, J. Han, R.J. Ulevitch, and R.J. Davis. 1995. Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J. Biol. Chem. 270:7420-7426.
37. Rankin, S., N. Morii, S. Narumiya, and E. Rozengurt. 1994. Botulinum C3 exoenzyme blocks the tyrosine phosphorylation of p125FAK and paxillin induced by bombesin and endothelin. FEBS Lett. 354:315-319.
38. Renshaw, M.W., X.D. Ren, and M.A. Schwartz. 1997. Growth factor activation of MAP kinase requires cell adhesion. EMBO (Eur. Mol. Biol. Organ.) J. 16: 5592-5599.
39. Retta, S.F., F. Balzac, P. Ferraris, A.M. Belkin, R. Fassler, M.J. Humphries, G. De Leo, L. Silengo, and G. Tarone. 1998. Betal-integrin cytoplasmic subdomains involved in dominant negative function. Mol. Cell. Biol. 9:715-731.
40. Ruoslahti, E. 1991. Integrins. J. Clin. Invest. 87:1-5.
41. Satoh, T., J. Kato, K. Nishida, and Y. Kaziro. 1996. Tyrosine phosphorylation of ACK in response to temperature shift-down, hyperosmotic shock, and epidermal growth factor stimulation. FEBS Lett. 386:230-234.
42. Saulnier, R., B. Bhardwaj, J. Klassen, D. Leopold, N. Rahimi, E. Tremblay, D. Mosher, and B. Elliott. 1996. Fibronectin fibrils and growth factors stimulate anchorage independent growth of a murine mammary carcinoma. Exp. Cell Res. 222:360-369.
43. Schlaepfer, D.D., S.K. Hanks, T. Hunter, and P. van der Geer. 1994. Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature. 372:786-791.
44. Seufferlein, T., and E. Rozengurt. 1994. Lysophosphatidic acid stimulates tyrosine phosphorylation of focal adhesion kinase, paxillin, and p130. Signaling pathways and cross-talk with platelet-derived growth factor. J. Biol. Chem. 269:9345-9351.
45. Tang, Y., Z. Chen, D. Ambrose, J. Liu, J.B. Gibbs, J. Chernoff, and J. Field. 1997. Kinase-deficient Pak1 mutants inhibit Ras transformation of Rat-1 fibroblasts. Mol. Cell. Biol. 17:4454-4464.
46. Wennerberg, K., L. Lohikangas, D. Gullberg, M. Pfaff, S. Johansson, and R. Fässler. 1996. beta1 integrin-dependent and -independent polymerization of fibronectin. J. Cell Biol. 132:227-238.
47. Wu, C., J.S. Bauer, R.L. Juliano, and J.A. McDonald. 1993. The α5β1 integrin fibronectin receptor, but not the α5 cytoplasmic domain, functions in an early and essential step in fibronectin matrix assembly. J. Biol. Chem. 268: 21883-21888.
48. Wu, C., A.J. Fields, B.A.E. Kapteijn, and J.A. McDonald. 1995a. The role of alpha4beta1 integrin in cell motility and fibronectin matrix assembly. J. Cell Sci. 108:821-829.
49. Wu, C., V.M. Keivens, T.E. O'Toole, J.A. McDonald, and M.H. Ginsberg. 1995b. Integrin activation and cytoskeletal interaction are essential for the assembly of a fibronectin matrix. Cell. 83:715-724.
50. Wu, C., P.E. Hughes, M.H. Ginsberg, and J.A. McDonald. 1996. Identification of a new biological function for the integrin alpha v beta 3: initiation of fibronectin matrix assembly. Cell Adh. Com. 4:149-158.
51. Yang, J.T., H. Rayburn, and R.O. Hynes. 1993. Embryonic mesoderaml defects in alpha5 integrin-deficient mice. Development. 119:1093-1105.
52. Yang, W., and R.A. Cerione. 1997. Cloning and characterization of a novel Cdc42-associated tyrosine kinase, ACK-2, from bovine brain. J. Biol. Chem. 272:24819-24824.
53. Yatohgo, T., M. Izumi, H. Kashiwagi, and M. Hayashi. 1988. Novel purification of vitronectin from human plasma by heparin affinity chromatography. Cell Struct. Funct. 13:281-292.
54. Zhang, Q., W.J. Checovich, D.M. Peters, R.M. Albrecht, and D.F. Mosher. 1994. Modulation of cell surface fibronectin assembly sites by lysophosphatidic acid. J. Cell Biol. 127:1447-1459.
55. Zhang, Q., M.K. Magnusson, and D.F. Mosher. 1997. Lysophosphatidic acid and microtubule-destabilizing agents stimulate fibronectin matrix assembly through Rho-dependent actin stress fiber formation and cell contraction. Mol. Biol. Cell. 8:1415-1425.
56. Zhang, Z., A.O. Morla, K. Vuori, J.S. Bauer, R.L. Juliano, and E. Ruoslahti. 1993. The alphavbetal integrin functions as a fibronectin receptor but does not support fibronectin matrix assembly and cell migration on fibronectin. J. Cell Biol. 122:235-242.