RhoA induces MMP-9 expression at CD44 lamellipodial focal complexes and promotes HMEC-1 cell invasion

Experimental Cell Research

Volumn 291, Issue 2, 2003, Pages 363-376

  Abécassis, Irina ^a   Olofsson, Birgitta ^b   Schmid, Michel ^a   Zalcman, Gérard ^c   Karniguian, Aïda ^a  

^a SAINT LOUIS HOSPITAL   (France)

^b LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

^c CHU CÔTE DE NACRE   (France)

Author keywords

Adhesion receptor; CD44; Endothelial cells; Invasion; Lamellipodia; Metalloproteinases; Migration; MMP 9; Rho proteins; Small GTPases

Indexed keywords

ENZYME; GELATINASE B; HERMES ANTIGEN; MATRIX PROTEIN; MEMBRANE RECEPTOR; METALLOPROTEINASE; PROTEINASE; RHOA GUANOSINE TRIPHOSPHATASE; UNCLASSIFIED DRUG;

ARTICLE; CELL INVASION; CELL STRAIN; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; LAMELLIPODIUM; MICROVASCULATURE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; TUMOR CELL; TUMOR GROWTH; UPREGULATION;

EID: 0344010182     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2003.08.006     Document Type: Article

References (59)

1. Hanahan D., Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell. 86:1996;353-364.
2. Carmeliet P., Jain R.K. Angiogenesis in cancer and other diseases. Nature. 407:2000;249-257.
3. Risau W. Mechanisms of angiogenesis. Nature. 386:1997;671-674.
4. Veikkola T., Karkkainen M., Claesson-Welsh L., Alitalo K. Regulation of angiogenesis via vascular endothelial growth factor receptors. Cancer Res. 60:2000;203-212.
5. Eliceiri B.P., Cheresh D.A. Role of alpha v integrins during angiogenesis. Cancer J. 6:(Suppl. 3):2000;S245-S249.
6. Yancopoulos G.D., Davis S., Gale N.W., Rudge J.S., Wiegand S.J., Holash J. Vascular-specific growth factors and blood vessel formation. Nature. 407:2000;242-248.
7. Ferrara N. VEGF and the quest for tumour angiogenesis factors. Nat. Rev. Cancer. 2:2002;795-803.
8. Nobes C.D., Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell. 81:1995;53-62.
9. Van Aelst L., D'Souza-Schorey C. Rho GTPases and signaling networks. Genes Dev. 11:1997;2295-2322.
10. Hall A. Rho GTPases and the actin cytoskeleton. Science. 279:1998;509-514.
11. Ridley A.J. Rho family proteins and regulation of the actin cytoskeleton. Prog. Mol. Subcell. Biol. 22:1999;1-22.
12. Nobes C.D., Hall A. Rho GTPases control polarity, protrusion, and adhesion during cell movement. J. Cell Biol. 144:1999;1235-1244.
13. del Peso L., Hernandez-Alcoceba R., Embade N., Carnero A., Esteve P., Paje C., Lacal J.C. Rho proteins induce metastatic properties in vivo. Oncogene. 15:1997;3047-3057.
14. Schmitz A.A., Govek E.E., Bottner B., Van Aelst L. Rho GTPases signaling, migration, and invasion . Exp. Cell Res. 261:2000;1-12.
15. Sahai E., Marshall C.J. RHO-GTPases and cancer. Nat. Rev. Cancer. 2:2002;133-142.
16. O'Connor K.L., Nguyen B.K., Mercurio A.M. RhoA function in lamellae formation and migration is regulated by the alpha6beta4 integrin and cAMP metabolism. J. Cell Biol. 148:2000;253-258.
17. Genda T., Sakamoto M., Ichida T., Asakura H., Kojiro M., Narumiya S., Hirohashi S. Cell motility mediated by rho and Rho-associated protein kinase plays a critical role in intrahepatic metastasis of human hepatocellular carcinoma. Hepatology. 30:1999;1027-1036.
18. Itoh K., Yoshioka K., Akedo H., Uehata M., Ishizaki T., Narumiya S. An essential part for Rho-associated kinase in the transcellular invasion of tumor cells. Nat. Med. 5:1999;221-225.
19. Sander E.E., Collard J.G. Rho-like GTPases their role in epithelial cell-cell adhesion and invasion . Eur. J. Cancer. 35:1999;1302-1308.
20. Menager C., Vassy J., Doliger C., Legrand Y., Karniguian A. Subcellular localization of RhoA and ezrin at membrane ruffles of human endothelial cells differential role of collagen and fibronectin . Exp. Cell Res. 249:1999;221-230.
21. Mangeat P., Roy C., Martin M. ERM proteins in cell adhesion and membrane dynamics. Trends Cell Biol. 9:1999;187-192.
22. Gingras D., Lamy S., Beliveau R. Tyrosine phosphorylation of the vascular endothelial-growth-factor receptor-2 (VEGFR-2) is modulated by Rho proteins. Biochem. J. 348:(Pt 2):2000;273-280.
23. Zeng H., Zhao D., Mukhopadhyay D. KDR stimulates endothelial cell migration through heterotrimeric G protein Gq/11-mediated activation of a small GTPase RhoA. J. Biol. Chem. 277:2002;46791-46798.
24. Ades E.W., Candal F.J., Swerlick R.A., George V.G., Summers S., Bosse D.C., Lawley T.J. HMEC-1 establishment of an immortalized human microvascular endothelial cell line . J. Invest. Dermatol. 99:1992;683-690.
25. Bouis D.A., Popova T.G., Takashima A., Norgard M.V. Dendritic cells phagocytose and are activated by Treponema pallidum. Infect. Immun. 69:2001;518-528.
26. Bordier C. Phase separation of integral membrane proteins in Triton X-114 solution. J. Biol. Chem. 256:1981;1604-1607.
27. Nagase H., Woessner J.F. Jr. Matrix metalloproteinases. J. Biol. Chem. 274:1999;21491-21494.
28. McCawley L.J., Matrisian L.M. Matrix metalloproteinases multifunctional contributors to tumor progression . Mol. Med. Today. 6:2000;149-156.
29. Johansson N., Ahonen M., Kahari V.M. Matrix metalloproteinases in tumor invasion. Cell Mol. Life. Sci. 57:2000;5-15.
30. Bergers G., Brekken R., McMahon G., Vu T.H., Itoh T., Tamaki K., Tanzawa K., Thorpe P., Itohara S., Werb Z., Hanahan D. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat. Cell Biol. 2:2000;737-744.
31. Tsukita S., Yonemura S. ERM (ezrin/radixin/moesin) family from cytoskeleton to signal transduction . Curr. Opin. Cell Biol. 9:1997;70-75.
32. Takahashi K., Eto H., Tanabe K.K. Involvement of CD44 in matrix metalloproteinase-2 regulation in human melanoma cells. Int. J. Cancer. 80:1999;387-395.
33. Bourguignon L.Y. CD44-mediated oncogenic signaling and cytoskeleton activation during mammary tumor progression. J. Mammary Gland Biol. Neoplasia. 6:2001;287-297.
34. Qiu R.G., Chen J., McCormick F., Symons M. A role for Rho in Ras transformation. Proc. Natl. Acad. Sci. USA. 92:1995;11781-11785.
35. Sahai E., Ishizaki T., Narumiya S., Treisman R. Transformation mediated by RhoA requires activity of ROCK kinases. Curr. Biol. 9:1999;136-145.
36. Partridge C.A., Phillips P.G., Niedbala M.J., Jeffrey J.J. Localization and activation of type IV collagenase/gelatinase at endothelial focal contacts. Am. J. Physiol. 272:1997;L813-L822.
37. Legrand C., Gilles C., Zahm J.M., Polette M., Buisson A.C., Kaplan H., Birembaut P., Tournier J.M. Airway epithelial cell migration dynamics. MMP-9 role in cell-extracellular matrix remodeling. J. Cell Biol. 146:1999;517-529.
38. Werb Z., Vu T.H., Rinkenberger J.L., Coussens L.M. Matrix-degrading proteases and angiogenesis during development and tumor formation. Apmis. 107:1999;11-18.
39. Ilan N., Madri J.A. New paradigms of signaling in the vasculature ephrins and metalloproteases . Curr. Opin. Biotechnol. 10:1999;536-540.
40. Stetler-Stevenson W.G. Matrix metalloproteinases in angiogenesis a moving target for therapeutic intervention . J. Clin. Invest. 103:1999;1237-1241.
41. Haas T.L., Davis S.J., Madri J.A. Three-dimensional type I collagen lattices induce coordinate expression of matrix metalloproteinases MT1-MMP and MMP-2 in microvascular endothelial cells. J. Biol. Chem. 273:1998;3604-3610.
42. Vu T.H., Shipley J.M., Bergers G., Berger J.E., Helms J.A., Hanahan D., Shapiro S.D., Senior R.M., Werb Z. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell. 93:1998;411-422.
43. Benbow U., Brinckerhoff C.E. The AP-1 site and MMP gene regulation what is all the fuss about? Matrix Biol. 15:1997;519-526.
44. Borden P., Heller R.A. Transcriptional control of matrix metalloproteinases and the tissue inhibitors of matrix metalloproteinases. Crit. Rev. Eukaryot. Gene Expr. 7:1997;159-178.
45. Amano M., Chihara K., Kimura K., Fukata Y., Nakamura N., Matsuura Y., Kaibuchi K. Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science. 275:1997;1308-1311.
46. Bar-Sagi D., Hall A. Ras and Rho GTPases a family reunion . Cell. 103:2000;227-238.
47. Zhuge Y., Xu J. Rac1 mediates type I collagen-dependent MMP-2 activation. role in cell invasion across collagen barrier. J. Biol. Chem. 276:2001;16248-16256.
48. Takaishi K., Sasaki T., Kameyama T., Tsukita S., Takai Y. Translocation of activated Rho from the cytoplasm to membrane ruffling area, cell-cell adhesion sites and cleavage furrows. Oncogene. 11:1995;39-48.
49. Michaely P.A., Mineo C., Ying Y.S., Anderson R.G. Polarized distribution of endogenous Rac1 and RhoA at the cell surface. J. Biol. Chem. 274:1999;21430-21436.
50. Wojciak-Stothard B., Williams L., Ridley A.J. Monocyte adhesion and spreading on human endothelial cells is dependent on Rho-regulated receptor clustering. J. Cell Biol. 145:1999;1293-1307.
51. Hirao M., Sato N., Kondo T., Yonemura S., Monden M., Sasaki T., Takai Y., Tsukita S. Regulation mechanism of ERM (ezrin/radixin/moesin) protein/plasma membrane association possible involvement of phosphatidylinositol turnover and Rho-dependent signaling pathway . J. Cell Biol. 135:1996;37-51.
52. Matsui T., Maeda M., Doi Y., Yonemura S., Amano M., Kaibuchi K., Tsukita S. Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J. Cell Biol. 140:1998;647-657.
53. Bourguignon L.Y., Zhu H., Shao L., Zhu D., Chen Y.W. Rho-kinase (ROK) promotes CD44v(3,8-10)-ankyrin interaction and tumor cell migration in metastatic breast cancer cells. Cell Motil. Cytoskeleton. 43:1999;269-287.
54. Yu Q., Stamenkovic I. Localization of matrix metalloproteinase 9 to the cell surface provides a mechanism for CD44-mediated tumor invasion. Genes Dev. 13:1999;35-48.
55. Bourguignon L.Y., Gunja-Smith Z., Iida N., Zhu H.B., Young L.J., Muller W.J., Cardiff R.D. CD44v(3,8-10) is involved in cytoskeleton-mediated tumor cell migration and matrix metalloproteinase (MMP-9) association in metastatic breast cancer cells. J. Cell Physiol. 176:1998;206-215.
56. Okamoto I., Kawano Y., Tsuiki H., Sasaki J., Nakao M., Matsumoto M., Suga M., Ando M., Nakajima M., Saya H. CD44 cleavage induced by a membrane-associated metalloprotease plays a critical role in tumor cell migration. Oncogene. 18:1999;1435-1446.
57. Kajita M., Itoh Y., Chiba T., Mori H., Okada A., Kinoh H., Seiki M. Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration. J. Cell Biol. 153:2001;893-904.
58. Rottner K., Hall A., Small J.V. Interplay between Rac and Rho in the control of substrate contact dynamics. Curr. Biol. 9:1999;640-648.
59. Yu Q., Stamenkovic I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev. 14:2000;163-176.