Lysophosphatidic acid and microtubule-destabilizing agents stimulate fibronectin matrix assembly through Rho-dependent actin stress fiber formation and cell contraction

Molecular Biology of the Cell

Volumn 8, Issue 8, 1997, Pages 1415-1425

  Zhang, Qinghong ^a   Magnusson, Magnus K ^a   Mosher, Deane F ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; FIBRONECTIN; LYSOPHOSPHATIDIC ACID; NOCODAZOLE; PACLITAXEL; VINBLASTINE;

ACTIN FILAMENT; ACTIN MYOSIN INTERACTION; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; MICROTUBULE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN PHOSPHORYLATION;

EID: 0030928057     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.8.8.1415     Document Type: Article

References (72)

1. Aguirre, K.M., McCormick, R.J., and Schwarzbauer, J.E. (1994). Fibronectin self-association is mediated by complementary sites within the amino-terminal one-third of the molecule. J. Biol. Chem. 269, 27863-27868.
2. Akiyama, S.K., Yamada, S.S., Chen, W.-T., and Yamada, K.M. (1989). Analysis of fibronectin receptor function with monoclonal antibodies: roles in cell adhesion, migration, matrix assembly, and cytoskeletal organization. J. Cell Biol. 109, 863-875.
3. Aktories, K., and Just, I. (1995). In vitro ADP-ribosylation of Rho by bacterial ADP-ribosyltransferase. Methods Enzymol. 256, 184-195.
4. Allen-Hoffmann, B.L., and Mosher, D.F. (1987). Matrix assembly sites for exogenous fibronectin are decreased on human fibroblasts after treatment with agents which increase intracellular cAMP. J. Biol. Chem. 262, 14361-14365.
5. Allio, A.E., and McKeown-Longo, P.J. (1988). Extracellular matrix assembly of cell-derived and plasma-derived fibronectins by substrate-attached fibroblasts. J. Cell. Physiol. 135, 459-466.
6. Amano, M., Ito, M., Kimura, K., Fukata, Y., Chihara, K., Nakano, T., Matsuura, Y., and Kaibuchi, K. (1996). Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271, 20246-20249.
7. Barry, E.L., and Mosher, D.F. (1988). Factor XIII cross-linking of fibronectin at cellular matrix assembly sites. J. Biol. Chem. 263, 10464-10469.
8. Barry, E.L., and Mosher, D.F. (1989). Factor XIIIa-mediated cross-linking of fibronectin in fibroblast cell layers. Cross-linking of cellular and plasma fibronectin and of amino-terminal fibronectin fragments. J. Biol. Chem. 264, 4179-4185.
9. Bershadsky, A., Chausovsky, A., Becker, E., Lyubimova, A., and Geiger B. (1996). Involvement of microtubules in the control of adhesion-dependent signal transduction. Curr. Biol. 6, 1279-1289.
10. Billah, M.M., Lapetina, E.G., and Cuatrecasas, P. (1981). Phospholipase A2 activity specific for phosphatidic acid. A possible mechanism for the production of arachidonic acid in platelets. J. Biol. Chem. 256, 5399-5403.
11. Boucaut, J.C., Darribere, T., Poole, T.J., Aoyama, H., Yamada, K.M., and Thiery J.P. (1984). Biologically active synthetic peptides as probes of embryonic development: a competitive peptide inhibitor of fibronectin function inhibits gastrulation in amphibian embryos and neural crest cell migration in avian embryos. J. Cell Biol. 99, 1822-1830.
12. 13 stimulate Rho-dependent stress fiber formation and focal adhesion assembly. J. Biol. Chem. 270, 24631-24634.
13. Checovich, W.J., and Mosher, D.F. (1993). Lysophosphatidic acid enhances fibronectin binding to adherent cells. Arterioscler. Thromb. 13, 1662-1667.
14. 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.
15. Cramer, L.P., and Mitchison, T.J. (1995). Myosin is involved in postmitotic cell spreading. J. Cell Biol. 232, 179-189.
16. Crossin, K.L., and Carney, D.H. (1981). Evidence that microtubule depolymerization early in the cell cycle is sufficient to initiate DNA synthesis. Cell 23, 61-71.
17. Danowski, B.A. (1989). Fibroblast contractility and actin organization are stimulated by microtubule inhibitors. J. Cell Sci. 93, 255-266.
18. Exton, J.H. (1990). Signaling through phosphatidylcholine breakdown. J. Biol. Chem. 265, 1-4.
19. Fourcade, O., Simon, M.F., Viode, C., Rugani, N., Leballe, F., Ragab A, Fournie, B., Sarda, L., and Chap, H. (1995). Secretory phospholipase A2 generates the novel lipid mediator lysophosphatidic acid in membrane microvesicles shed from activated cells. Cell 80, 919-927.
20. Gailit, J., and Clark, R.A. (1994). Wound repair in the context of extracellular matrix. Curr. Opin. Cell Biol. 6, 717-725.
21. George, E.L., Georges-Labouesse, E.N., Patel-King, R.S., Rayburn, H., and Hynes, R.O. (1993). Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119, 1079-1091.
22. Gerrard, J.M., and Robinson, P. (1989). Identification of the molecular species of lysophosphatidic acid produced when platelets are stimulated by thrombin. Biochim. Biophys. Acta. 1001, 282-285.
23. Giancotti, F.G., and Ruoslahti, E. (1990). Elevated levels of the α5β1 fibronectin receptor suppresses the transformed phenotype of Chinese hamster ovary cells. Cell 60, 849-859.
24. Guo, Z., Lilliom, K., Fischer, D.J., Bathurst, I.C., Tomei, L.D., Kiefer, M.C., and Tigyi, G. (1996). Molecular cloning of a high-affinity receptor for the growth factor-like lipid mediator lysophosphatic acid from Xenopus oocytes. Proc. Natl. Acad. Sci. USA 93, 14367-14372.
25. Hecht, J.H., Weiner, J.A., Post, S.R., and Chun, J. (1996). Ventricular zone gene-1 (VZG-1) encodes a lysophosphatidic acid receptor expressed in neurogenic regions of the developing cerebral cortex. J. Cell Biol. 135, 1071-1083.
26. Higuchi, H., and Takemori, S. (1989). Butanedione monoxime suppresses contraction and ATPase activity of rabbit skeletal muscle. J. Biochem. 105, 638-643.
27. Hocking, D.C., Smith, R.K., and McKeown-Longo, P.J. (1996). A novel role for the integrin-binding III-10 module in fibronectin matrix assembly. J. Cell Biol. 133, 431-444.
28. Hocking, D.C., Sottile, J., and McKeown-Longo, P.J. (1994). Fibronectin's III-1 module contains a conformation-dependent binding site for the amino-terminal region of fibronectin. J. Biol. Chem. 269, 19183-19191.
29. Hynes, R.O. (1990). Fibronectins, New York: Springer-Verlag.
30. Hynes, R.O. (1992). Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69, 11-25.
31. Jalink, K., van Corven, E.J., Hengeveld, T., Morii, N., Narumiya, S. and Moolenaar, W.H. (1994). Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho. J. Cell Biol. 126, 801-810.
32. 2+-mobilizing stimulus for fibroblasts. J. Biol. Chem. 265, 12232-12239.
33. Kajstura, J., and Bereiter-Hahn, J. (1993). Disruption of microtubule: induces formation of actin fibrils in density-inhibited 3T3 cells. Cell Biol. Int. 17, 1023-1031.
34. Kapeller, R., Chakrabarti, R., Cantley, L., Fay, F., and Corvera, S. (1993). Internalization of activated platelet-derived growth factor receptor-phosphatidylinositol-3′ kinase complexes: potential interactions with the microtubule cytoskeleton. Mol. Cell. Biol. 13, 6052-6063.
35. Kimura, K., et al. (1996). Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248.
36. Kolodney, M.S., and Elson, E.L. (1995). Contraction due to microtubule disruption is associated with increased phosphorylation of myosin regulatory light chain. Proc. Natl. Acad. Sci. USA 92, 10252-10256.
37. Kumagai, N., Morii, N., Fujisawa, K., Nemoto, Y., and Narumiya, S. (1993). ADP-ribosylation of Rho p21 inhibits lysophosphatidic acid induced protein tyrosine phosphorylation and phosphatidylinosito 3-kinase activation in cultured Swiss 3T3 cells. J. Biol. Chem. 268, 24535-34538.
38. Lapetina, E.G., Billah, M.M., and Cuatrecasas, P. (1981). The phosphatidylinositol cycle and the regulation of arachidonic acid production. Nature 292, 367-369.
39. Lloyd, C.W., Smith, C.G., Woods, A., and Rees, D.A. (1977). Mech anisms of cellular adhesion. II. The interplay between adhesion, the cytoskeleton and morphology in substrate-attached cells. Exp. Cell. Res. 110, 427-437.
40. Matsui, T., Amano, M., Yamamoto, T., Chihara, K., Nakafuku, M. Ito, M., Nakano, T., Okawa, K., Iwamatsu, A., and Kaibuchi, K. (1996). Rho-associated kinase, a novel serine/threonine kinase, as putative target for small GTP binding protein Rho. EMBO J. 15 2208-2216.
41. Mautner, V.M., and Hynes, R.O. (1977). Surface distribution of LET protein in relation to the cytoskeleton of normal and transforme cells. J. Cell Biol. 75, 743-768.
42. McKeown-Longo, P.J., and Mosher, D.F. (1983). Binding of plasma fibronectin to cell layers of human skin fibroblasts. J. Cell Biol. 97 466-472.
43. McKeown-Longo, P.J., and Mosher, D.F. (1984). Mechanism of for mation of disulfide-bonded multimers of plasma fibronectin in cell layers of cultured human fibroblasts. J. Biol. Chem. 259, 12210-12215.
44. McKeown-Longo, P.J., and Mosher, D.F. (1985). Interaction of the 70,000-mol-wt amino-terminal fragment of fibronectin with the mattrix-assembly receptor of fibroblasts. J. Cell Biol. 100, 364-374.
45. McKeown-Longo, P.J., and Mosher, D.F. (1989). The assembly of the fibronectin matrix in cultured human fibroblast cells. In: Fibronectin, ed. D.F. Mosher, San Diego: Academic Press, 163-179.
46. McKillop, D.F., Fortune, N.S., Ranatunga, K.W., and Geeves, M.A. (1994). The influence of 2,3-butanedione 2-monoxime (BDM) on the interaction between actin and myosin in solution and in skinne muscle fibres. J. Muscle Res. Cell Motil. 15, 309-318.
47. Miura, Y., Kikuchi, A., Musha, T., Kuroda, S., Yaku, H., Sasaki, T., and Takai, V. (1993). Regulation of morphology by rho p21 and its inhibitory GDP/GTP exchange protein (rho GDI) in Swiss 3T3 cells. J. Biol. Chem. 268, 510-515.
48. Moolenaar, W.H., Kranenburg, O., Postma, F.R., and Zondag, G.C. (1997). Lysophosphatidic Acid: G-protein signalling and cellular responses. Curr. Opin. Cell Biol. 9, 168-173.
49. Moolenaar, W.H., Kruijer, W., Tilly, B.C., Verlaan, I., Bierman, A.J., and de Laat, S.W. (1986). Growth factor-like action of phosphatidic acid. Nature 323, 171-173.
50. Mosher, D.F. (1989). Fibronectin, San Diego: Academic Press.
51. Mosher, D.F., and Vaheri, A. (1978). Thrombin stimulates the production and release of a major surface-associated glycoprotein (fibronectin) in cultures of human fibroblasts. Exp. Cell Res. 112, 323-334.
52. Narumiya, S., Sekine, A., and Fujiwara, M. (1988). Substrate for botulinum ADP-ribosyltransferase, Gb, has an amino acid sequence homologous to a putative rho gene product. J. Biol. Chem. 263, 17255-17257.
53. Peters, D.M., and Mosher, D.F. (1987). Localization of cell surface sites involved in fibronectin fibrillogenesis. J. Cell Biol. 104, 121-130.
54. Rennard, S.I., Wind, M.L., Hewitt, A.T., and Kleinman, H.K. (1981). Effect of collagen and cell shape on binding of fibronectin to cells. Arch. Biochem. Biophys. 206, 205-212.
55. Reszka, A.A., Seger, R., Diltz, C.D., Krebs, E.G., and Fischer, E.H. (1995). Association of mitogen-activated protein kinase with the microtubule cytoskeleton. Proc. Natl. Acad. Sci. USA 92, 8881-8885.
56. 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.
57. Roman, J., LaChance, R.M., Broekelmann, T.J., Kennedy, C.J., Wayner, EA., Carter, W.G., and McDonald, J.A. (1989). The fibronectin receptor is organized by extracellular matrix fibronectin: implications for oncogenic transformation and for cell recognition of fibronectin matrices. J. Cell Biol. 108, 2529-2543.
58. Roychowdhury, S., and Rasenick, M.M. (1994). Tubulin-G protein association stabilizes GTP binding and activates GTPase: cytoskeletal participation in neuronal signal transduction. Biochemistry 33, 9800-9805.
59. Sechler, J.L., and Schwarzbauer, J.E. (1997). Coordinated regulation of fibronectin fibril assembly and actin stress fiber formation. Cell Adhesion Commun. (in press).
60. Shinohara, Y., Nishida, E., and Sakai, H. (1989). Initiation of DNA synthesis by microtubule disruption in quiescent rat 3Y1 cells. Eur. J. Biochem. 183, 275-280.
61. Somers, C.E., and Mosher, D.F. (1993). Protein kinase C modulation of fibronectin matrix assembly. J. Biol. Chem. 268, 22277-22280.
62. Sontag, E., Nunbhakdi-Craig, V., Bloom, G.S., and Mumby, M.C. (1995). A novel pool of protein phosphatase 2A is associated with microtubuies and is regulated during the cell cycle. J. Cell Biol. 128, 1131-1144.
63. Thiery, J.-P., Duband, J.-L., Dufour, S., Savagner, P., and Imhof, B.A. (1989). Roles of fibronectin in embryogenesis. In: Fibronectin, ed. D.F. Mosher, San Diego: Academic Press, 181-212.
64. van Corven, E.J., Groenink, A., Jalink, K., Eichholtz, T., and Moolenaar, W.H. (1989). Lysophosphatidate-induced cell proliferation: identification and dissection of signaling pathways mediated by G proteins. Cell 59, 45-54.
65. ras by G protein-coupled receptor agonists in fibroblasts. Proc. Natl. Acad. Sci. USA 90, 1257-1261.
66. Watson, S.P., McConnell, R.T., and Lapetina, E.G. (1985). Decanoyl lysophosphatidic acid induces platelet aggregation through an extracellular action. Evidence against a second messenger role for lysophosphatidic acid. Biochem. J. 232, 61-66.
67. Wilson, L., and Jordan, M.A. (1994). Pharmacological probes of microtubule function. In: Microtubules, ed. J.S. Hyams and C.W. Lloyd, New York: Wiley-Liss, 59-83.
68. 5 cytoplasmic domain, functions in an early and essential step in fibronectin matrix assembly. J. Biol. Chem. 268, 21883-21888.
69. Wu, C., Keivens, V.M., O'Toole, T.E., McDonald, J.A., and Ginsberg, M.H. (1995). Integrin activation and cytoskeletal interaction are essential for the assembly of a fibronectin matrix. Cell 83, 715-724,
70. Yan, K., Greene, E., Belga, F., and Rasenick, M.M. (1996). Synaptic membrane G proteins are complexed with tubulin in situ. J. Neurochem. 66, 1489-1495.
71. Zhang, Q., Checovich, W.J., Peters, D.M., Albrecht, R.M., and Mosher, D.F. (1994). Modulation of cell surface fibronectin assembly sites by lysophosphatidic acid. J. Cell Biol. 127, 1447-1459.
72. Zhang, Q., and Mosher, D.F. (1996). Crosslinking of the N-terminal region of fibronectin to molecules of large apparent molecular mass (LAMMs): characterization of fibronectin assembly sites induced by the treatment of fibroblasts with lysophosphatidic acid. J. Biol. Chem. 271, 33284-33292.