Villin Enhances Hepatocyte Growth Factor-induced Actin Cytoskeleton Remodeling in Epithelial Cells

Molecular Biology of the Cell

Volumn 14, Issue 11, 2003, Pages 4641-4653

  Louvard, Rafika Athman Daniel ^a   Robine, Sylvie ^a  

^a INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; PHOSPHOLIPASE C; SCATTER FACTOR; VILLIN;

ANIMAL CELL; ARTICLE; CELL MOTILITY; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CYTOSKELETON; DOG; ENZYME ACTIVITY; EPITHELIUM CELL; KIDNEY CELL; KNOCKOUT MOUSE; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; WILD TYPE;

ACTINS; ANIMALS; CARRIER PROTEINS; CELL FRACTIONATION; CELL MOVEMENT; CELLS, CULTURED; CLONING, MOLECULAR; CYTOSKELETON; DOGS; ENTEROCYTES; GENE EXPRESSION REGULATION; HEPATOCYTE GROWTH FACTOR; MICE; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; MICROSCOPY, FLUORESCENCE; MORPHOGENESIS; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA; SIGNAL TRANSDUCTION; WOUND HEALING;

ANIMALIA; CANIS FAMILIARIS;

EID: 0345255702     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E03-02-0091     Document Type: Article

References (50)

1. Arpin, M., Pringault, E., Finidori, J., Garcia, A., Jeltsch, J.M., Vandekerckhove, J., and Louvard, D. (1988). Sequence of human villin: a large duplicated domain homologous with other actin-severing proteins and a unique small carboxyterminal domain related to villin specificity. J. Cell Biol. 107, 1759-1766.
2. Athman, R., Louvard, D., and Robine, S. (2002a). The epithelial cell cytoskeleton and intracellular trafficking. III. How is villin involved in the actin cytoskeleton dynamics in intestinal cells? Am. J. Physiol. 283, G496-G502.
3. Athman, R., Niewohner, J., Louvard, D., and Robine, S. (2002b). Epithelial cells: establishment of primary cultures and immortalization. In: Molecular Cellular Microbiology, vol. 31, ed. P.S.a.A. Zychlinsky, New York: Academic Press, 93-113.
4. Bhargava, M.M., Li, Y., Joseph, A., Jin, L., Rosen, E.M., and Goldberg, I.D. (1993). HGF-SF: effects on motility and morphology of normal and tumor cells. EXS 65, 341-349.
5. Boyer, B., Valles, A.M., and Thiery, J.P. (1996). Model systems of epithelium-mesenchyme transitions. Acta Anat. 156, 227-239.
6. Bretscher, A., and Weber, K. (1980). Villin is a major protein of the microvillus cytoskeleton which binds both G and F actin in a calcium-dependent manner. Cell 20, 839-847.
7. Chan, A.Y., Bailly, M., Zebda, N., Segall, J.E., and Condeelis, J.S. (2000). Role of cofilin in epidermal growth factor-stimulated actin polymerization and lamellipod protrusion. J. Cell Biol. 148, 531-542.
8. Chan, A.Y., Raft, S., Bailly, M., Wyckoff, J.B., Segall, J.E., and Condeelis, J.S. (1998). EGF stimulates an increase in actin nucleation and filament number at the leading edge of the lamellipod in mammary adenocarcinoma cells. J. Cell Sci. 111, 199-211.
9. Costa de Beauregard, M.A., Pringault, E., Robine, S., and Louvard, D. (1995). Suppression of villin expression by antisense RNA impairs brush border assembly in polarized epithelial intestinal cells. EMBO J. 14, 409-421.
10. Cramer, L.P., Briggs, L.J., and Dawe, H.R. (2002). Use of fluorescently labelled deoxyribonuclease I to spatially measure G-actin levels in migrating and non-migrating cells. Cell Motil. Cytoskeleton. 51, 27-38.
11. Dudouet, B., Robine, S., Huet, C., Sahuquillo-Merino, C., Blair, L., Coudrier, E., and Louvard, D. (1987). Changes in villin synthesis and subcellular distribution during intestinal differentiation of HT29-18 clones. J. Cell Biol. 105, 359-369.
12. Eddy, R.J., Han, J., and Condeelis, J.S. (1997). Capping protein terminates but does not initiate chemoattractant-induced actin assembly in Dictyostelium. J. Cell Biol. 139, 1243-1253.
13. Evans, G.S., Flint, N., Somers, A.S., Eyden, B., and Potten, C.S. (1992). The development of a method for the preparation of rat intestinal epithelial cell primary cultures. J. Cell Sci. 101, 219-231.
14. 2+ dependent F-actin disruption in intestinal brush-borders. J. Cell Biol. 146, 819-829.
15. Friederich, E., Gouin, E., Hellio, R., Kocks, C., Cossart, P., and Louvard, D. (1995). Targeting of Listeria monocytogenes ActA protein to the plasma membrane as a tool to dissect both actin-based cell morphogenesis and ActA function. EMBO J. 14, 2731-2744.
16. Friederich, E., Huet, C., Arpin, M., and Louvard, D. (1989). Villin induces microvilli growth and actin redistribution in transfected fibroblasts. Cell 59, 461-475.
17. Friederich, E., Vancompernolle, K., Huet, C., Goethals, M., Finidori, J., Vandekerckhove, J., and Louvard, D. (1992). An actin-binding site containing a conserved motif of charged amino acid residues is essential for the morphogenic effect of villin. Cell 70, 81-92.
18. Friederich, E., Vancompernolle, K., Louvard, D., and Vandekerckhove, J. (1999). Villin function in the organization of the actin cytoskeleton. Correlation of in vivo effects to its biochemical activities in vitro. J. Biol. Chem. 274, 26751-26760.
19. Gautreau, A., Poullet, P., Louvard, D., and Arpin, M. (1999). Ezrin, a plasma membrane-microfilament linker, signals cell survival through the phosphatidylinositol 3-kinase/Akt pathway. Proc. Natl. Acad. Sci. USA 96, 7300-7305.
20. Goldschmidt-Clermont, P.J., Kim, J.W., Machesky, L.M., Rhee, S.G., and Pollard, T.D. (1991). Regulation of phospholipase C-gamma 1 by profilin and tyrosine phosphorylation. Science 251, 1231-1233.
21. Gossen, M., and Bujard, H. (1992). Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. USA 89, 5547-5551.
22. Grant, D.S., Kleinman, H.K., Goldberg, I.D., Bhargava, M.M., Nickoloff, B.J., Kinsella, J.L., Polverini, P., and Rosen, E.M. (1993). Scatter factor induces blood vessel formation in vivo. Proc. Natl. Acad. Sci. USA 90, 1937-1941.
23. Graziani, A., Gramaglia, D., Cantley, L.C., and Comoglio, P.M. (1991). The tyrosine-phosphorylated hepatocyte growth factor/scatter factor receptor associates with phosphatidylinositol 3-kinase. J. Biol. Chem. 266, 22087-22090.
24. Gual, P., Giordano, S., Williams, T.A., Rocchi, S., Van Obberghen, E., and Comoglio, P.M. (2000). Sustained recruitment of phospholipase C-gamma to Gab1 is required for HGF-induced branching tubulogenesis. Oncogene 19, 1509-1518.
25. Handel, S.E., Hendry, K.A., and Sheterline, P. (1990). Microinjection of covalently cross-linked actin oligomers causes disruption of existing actin filament architecture in PtK2 cells. J. Cell Sci. 97, 325-333.
26. Janmey, P.A., Iida, K., Yin, H.L., and Stossel, T.P. (1987). Polyphosphoinositide micelles and polyphosphoinositide-containing vesicles dissociate endogenous gelsolin-actin complexes and promote actin assembly from the fast-growing end of actin filaments blocked by gelsolin. J. Biol. Chem. 262, 12228-12236.
27. Janmey, P.A., Lamb, J., Allen, P.G., and Matsudaira, P.T. (1992). Phosphoinositide-binding peptides derived from the sequences of gelsolin and villin. J. Biol. Chem. 267, 11818-11823.
28. 2+, KCl, and polyphosphoinositides. J. Biol. Chem. 263, 16738-16743.
29. Khurana, S., M. Arpin, R. Patterson, and M. Donowitz. (1997). Ileal microvillar protein villin is tyrosine-phosphorylated and associates with PLC-gamma1. Role of cytoskeletal rearrangement in the carbachol-induced inhibition of ileal NaCl absorption. J. Biol. Chem. 272, 30115-30121.
30. Kwiatkowski, D.J. (1999). Functions of gelsolin: motility, signaling, apoptosis, cancer. Curr. Opin. Cell Biol. 11, 103-108.
31. Kwiatkowski, D.J., and Yin, H.L. (1987). Molecular biology of gelsolin, a calcium-regulated actin filament severing protein. Biorheology 24, 643-647.
32. Lueck, A., Brown, D., and Kwiatkowski, D.J. (1998). The actin-binding proteins adseverin and gelsolin are both highly expressed but differentially localized in kidney and intestine. J. Cell Sci. 111, 3633-3643.
33. Marks, P.W., Arai, M., Bandura, J.L., and Kwiatkowski, D.J. (1998). Advillin (p92): a new member of the gelsolin/villin family of actin regulatory proteins. J. Cell Sci. 111, 2129-2136.
34. Mine, T., Kojima, I., Ogata, E., and Nakamura, T. (1991). Comparison of effects of HGF and EGF on cellular calcium in rat hepatocytes. Biochem. Biophys. Res. Commun. 181, 1173-1180.
35. Moon, A., and Drubin, D.G. (1995). The ADF/cofilin proteins: stimulus-responsive modulators of actin dynamics. Mol. Biol. Cell. 6, 1423-1431.
36. Northrop, J., Weber, A., Mooseker, M.S., Franzini-Armstrong, C., Bishop, M.F., Dubyak, G.R., Tucker, M., and Walsh, T.P. (1986). Different calcium dependence of the capping and cutting activities of villin. J. Biol. Chem. 261, 9274-9281.
37. Panebra, A., Ma, S.X., Zhai, L.W., Wang, X.T., Rhee, S.G., and Khurana, S. (2001). Regulation of phospholipase C-gamma(1) by the actin-regulatory protein villin. Am. J. Physiol. 281, C1046-C1058.
38. Papakonstanti, E.A., Emmanouel, D.S., Gravanis, A., and Stournaras, C. (2000). PLC-gamma1 signaling pathway and villin activation are involved in actin cytoskeleton reorganization induced by Na+/Pi cotransport up-regulation. Mol. Med. 6, 303-318.
39. Pinson, K.I., Dunbar, L., Samuelson, L., and Gumucio, D.L. (1998). Targeted disruption of the mouse villin gene does not impair the morphogenesis of microvilli. Dev. Dyn. 211, 109-121.
40. Ponzetto, C., Bardelli, A., Zhen, Z., Maina, F., dalla Zonca, P., Giordano, S., Graziani, A., Panayotou, G., and Comoglio, P.M. (1994). A multifunctional docking site mediates signaling and transformation by the hepatocyte growth factor/ scatter factor receptor family. Cell 77, 261-271.
41. Potempa, S., and Ridley, A.J. (1998). Activation of both MAP kinase and phosphatidylinositide 3-kinase by Ras is required for hepatocyte growth factor/ scatter factor-induced adherens junction disassembly. Mol. Biol. Cell. 9, 2185-2200.
42. Ridley, A.J., Comoglio, P.M., and Hall, A. (1995). Regulation of scatter factor/ hepatocyte growth factor responses by Ras, Rac, and Rho in MDCK cells. Mol. Cell. Biol. 15, 1110-1122.
43. Royal, I., Lamarche-Vane, N., Lamorte, L., Kaibuchi, K., and Park, M. (2000). Activation of cdc42, rac, PAK, and rho-kinase in response to hepatocyte growth factor differentially regulates epithelial cell colony spreading and dissociation. Mol. Biol. Cell. 11, 1709-1725.
44. Saelman, E.U., Keely, P.J., and Santoro, S.A. (1995). Loss of MDCK cell alpha-2 beta 1 integrin expression results in reduced cyst formation, failure of hepatocyte growth factor/scatter factor-induced branching morphogenesis, and increased apoptosis. J. Cell Sci. 108, 3531-3540.
45. Sonnenberg, E., Meyer, D., Weidner, K.M., and Birchmeier, C. (1993). Scatter factor/hepatocyte growth factor and its receptor, the c-met tyrosine kinase, can mediate a signal exchange between mesenchyme and epithelia during mouse development. J. Cell Biol. 123, 223-235.
46. 2+-sensitive, 41, 000-dalton protein which reversibly blocks the "barbed" ends of actin filaments but does not sever them. J. Biol. Chem. 261, 14191-14195.
47. Stoker, M., and Gherardi, E. (1991). Regulation of cell movement: the motogenic cytokines. Biochim. Biophys. Acta 1072, 81-102.
48. Weiser, M.M. (1973). Intestinal epithelial cell surface membrane glycoprotein synthesis. I. An indicator of cellular differentiation. J. Biol. Chem. 248, 2536-2541.
49. Wulfkuhle, J.D., Donina, I.E., Stark, N.H., Pope, R.K., Pestonjamasp, K.N., Niswonger, M.L., and Luna, E.J. (1999). Domain analysis of supervillin, an F-actin bundling plasma membrane protein with functional nuclear localization signals. J. Cell Sci. 112, 2125-2136.
50. Zhai, L., Zhao, P., Panebra, A., Guerrerio, A.L., and Khurana, S. (2001). Tyrosine phosphorylation of villin regulates the organization of the actin cytoskeleton. J. Biol. Chem. 276, 36163-36167.