Cdc42 downregulates MMP-1 expression by inhibiting the ERK1/2 pathway

Journal of Cell Science

Volumn 118, Issue 6, 2005, Pages 1173-1183

  Deroanne, Christophe F ^a   Hamelryckx, Delphine ^a   Ho, T T Giang ^a   Lambert, Charles A ^a   Catroux, Philippe ^b   Lapière, Charles M ^a   Nusgens, Betty V ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b L ORÉAL RECHERCHE   (France)

Author keywords

Cdc42; ERK1 2; MMP 1; Rac1; RhoA; siRNA

Indexed keywords

COLLAGEN TYPE 1; GELATINASE A; INTEGRIN; INTERLEUKIN 8; INTERSTITIAL COLLAGENASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN CDC42; RAC1 PROTEIN; RHO KINASE; SMALL INTERFERING RNA;

ARTICLE; CELL INTERACTION; CONTROLLED STUDY; CYTOSKELETON; DOWN REGULATION; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; ENZYME RELEASE; ENZYME REPRESSION; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HOMEOSTASIS; HUMAN; HUMAN CELL; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MICROARRAY; PROTEIN TARGETING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SKIN FIBROBLAST; UPREGULATION; WILD TYPE;

BLOTTING, WESTERN; CDC42 GTP-BINDING PROTEIN; CELL ADHESION; CELL LINE, TUMOR; CULTURE MEDIA, SERUM-FREE; DNA PRIMERS; DOWN-REGULATION; ENZYME INHIBITORS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FIBROBLASTS; GENE SILENCING; GTP PHOSPHOHYDROLASES; HUMANS; IMMUNOBLOTTING; INTERLEUKIN-8; MATRIX METALLOPROTEINASE 1; MICROSCOPY, PHASE-CONTRAST; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RAC1 GTP-BINDING PROTEIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHOA GTP-BINDING PROTEIN; RNA INTERFERENCE; RNA, SMALL INTERFERING; SKIN; TIME FACTORS; TRANSFECTION; UP-REGULATION;

EID: 17244367860     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01707     Document Type: Article

References (47)

1. Aguirre-Ghiso, J. A., Estrada, Y., Liu, D. and Ossowski, L. (2003). ERK(MAPK) activity as a determinant of tumor growth and dormancy; regulation by p38(SAPK). Cancer Res. 63, 1684-1695.
2. Brauchle, M., Gluck, D., di Padova, F., Han, J. and Gram, H. (2000). Independent role of p38 and ERK1/2 mitogen-activated kinases in the upregulation of matrix metalloproteinase-1. Exp. Cell Res. 258, 135-144.
3. Danen, E. H., Lafrenie, R. M., Miyamoto, S. and Yamada, K. M. (1998). Integrin signaling: cytoskeletal complexes, MAP kinase activation, and regulation of gene expression. Cell Adhes. Commun. 6, 217-224.
4. del Pozo, M. A., Price, L. S., Alderson, N. B., Ren, X. D. and Schwartz, M. A. (2000). Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK. EMBO J. 19, 2008-2014.
5. Deroanne, C. F., Lapiere, C. M. and Nusgens, B. V. (2001). In vitro tubulogenesis of endothelial cells by relaxation of the coupling extracellular matrix-cytoskeleton. Cardiovasc. Res. 49 647-658.
6. Deroanne, C., Vouret-Craviari, V., Wang, B. and Pouyssegur, J. (2003). EphrinA1 inactivates integrin-mediated vascular smooth muscle cell spreading via the Rac/PAK pathway. J. Cell Sci. 116, 1367-1376.
7. Elbashir, S. M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K. and Tuschl, T. (2001). Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411 494-498.
8. Feig, L. A. (1999). Tools of the trade: use of dominant-inhibitory mutants of Ras-family GTPases. Nat. Cell Biol. 1, E25-E27.
9. Haas, T. L., Davis, S. J. and Madri, J. A. (1998). 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, 3604-3610.
10. Hall, A. (1998). Rho GTPases and the actin cytoskeleton. Science 279, 509-514.
11. Hotchin, N. A. and Hall, A. (1995). The assembly of integrin adhesion complexes requires both extracellular matrix and intracellular Rho/Rac GTPases. J. Cell Biol. 131, 1857-1865.
12. Huntington, J. T., Shields, J. M., Der, C. J., Wyatt, C. A., Benbow, U., Slingluff, C. L., Jr and Brinckerhoff, C. E. (2004). Overexpression of collagenase 1 (MMP-1) is mediated by the ERK pathway in invasive melanoma cells: role of BRAF mutation and FGF signaling. J. Biol. Chem. 279, 33168-33176.
13. Hynes, R. O. (1992). Integrins: versatility, modulation, and signaling in cell adhesion, Cell 69, 11-25.
14. Ingber, D. E. (2002). Mechanical signaling and the cellular response to extracellular matrix in angiogenesis and cardiovascular physiology. Circ. Res. 91, 877-887.
15. Juliano, R. L. (2002). Signal transduction by cell adhesion receptors and the cytoskeleton: functions of integrins, cadherins, selectins, and immunoglobulin-superfamily members. Annu. Rev. Pharmacol. Toxicol. 42, 283-323.
16. Kheradmand, F., Werner, E., Tremble, P., Symons, M. and Werb, Z. (1998). Role of Rac1 and oxygen radicals in collagenase-1 expression induced by cell shape change. Science 280, 898-902.
17. Lambert, C. A., Soudant, E. P., Nusgens, B. V. and Lapiere, C. M. (1992). Pretranslational regulation of extracellular matrix macromolecules and collagenase expression in fibroblasts by mechanical forces. Lab. Invest. 66, 444-451.
18. Lambert, C. A., Lapiere, C. M. and Nusgens, B. V. (1998). An interleukin-1 loop is induced in human skin fibroblasts upon stress relaxation in a three-dimensional collagen gel but is not involved in the up-regulation of matrix metalloproteinase 1. J. Biol. Chem. 273, 23143-23149.
19. Lambert, C. A., Colige, A. C., Lapiere, C. M. and Nusgens, B. V. (2001a). Coordinated regulation of procollagens I and III and their post-translational enzymes by dissipation of mechanical tension in human dermal fibroblasts. Eur. J. Cell Biol. 80, 479-485.
20. Lambert, C. A., Colige, A. C., Munaut, C., Lapiere, C. M. and Nusgens, B. V. (2001b). Distinct pathways in the over-expression of matrix metalloproteinases in human fibroblasts by relaxation of mechanical tension. Matrix Biol. 20, 397-408.
21. Langholz, O., Rockel, D., Mauch, C., Kozlowska, E., Bank, I., Krieg, T. and Eckes, B. (1995). Collagen and collagenase gene expression in three-dimensional collagen lattices are differentially regulated by alpha 1 beta 1 and alpha 2 beta 1 integrins. J. Cell Biol. 131, 1903-1915.
22. Lerm, M., Schmidt, G. and Aktories, K. (2000). Bacterial protein toxins targeting Rho GTPases. FEMS Microbiol. Lett. 188, 1-6.
23. Liao, J., Wolfman, J. C. and Wolfman, A. (2003). K-Ras regulates the steady-state expression of matrix metalloprotemase 2 in fibroblasts. J. Biol. Chem. 278, 31871-31878.
24. Mauch, C., Hatamochi, A., Scharffetter, K. and Krieg, T. (1988). Regulation of collagen synthesis in fibroblasts within a three-dimensional collagen gel. Exp. Cell Res. 178, 493-503.
25. Mauch, C., Adelmann-Grill, B., Hatamochi, A. and Krieg, T. (1989). Collagenase gene expression in fibroblasts is regulated by a three-dimensional contact with collagen. FEBS Lett. 250, 301-305.
26. Minden, A., Lin, A., Claret, F. X., Abo, A. and Karin, M. (1995). Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 81, 1147-1157.
27. Nur-E-Kamal, M. S., Kamal, J. M., Qureshi, M. M. and Maruta, H. (1999). The CDC42-specific inhibitor derived from ACK-1 blocks v-Ha-Ras-induced transformation. Oncogene 18, 7787-7793.
28. Ren, X. D., Mosses, 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.
29. Reunanen, N., Li, S. P., Ahonen, M., Foschi, M., Han, J. and Kahari, V. M. (2002). Activation of p38 alpha MAPK enhances collagenase-1 (matrix metalloproteinase (MMP)-1) and stromelysin-1 (MMP-3) expression by mRNA stabilization. J. Biol. Chem. 277, 32360-32368.
30. Ridley, A. J. (2001). Rho GTPases and cell migration. J. Cell Sci. 114, 2713-2722.
31. Ridley, S. H., Sarsfield, S. J., Lee, J. C., Bigg, H. F., Cawston, T. E., Taylor, D. J., DeWitt, D. L. and Saklatvala, J. (1997). Actions of IL-1 are selectively controlled by p38 mitogen-activated protein kinase: regulation of prostaglandin H synthase-2, metalloproteinases, and IL-6 at different levels. J. Immunol. 158, 3165-3173.
32. Sander, E. E., ten Klooster, J. P., van Delft, S., van der Kammen, R. A. and Collard, J. G. (1999). Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J. Cell Biol. 147, 1009-1022.
33. Singh, R. P., Dhawan, P., Golden, C., Kapoor, G. S. and Mehta, K. D. (1999). One-way cross-talk between p38(MAPK) and p42/44(MAPK). Inhibition of p38(MAPK) induces low density lipoprotein receptor expression through activation of the p42/44(MAPK) cascade. J. Biol. Chem. 274, 19593-19600.
34. Sledz, C. A., Holko, M., de Veer, M. J., Silverman, R. H. and Williams, B. R. (2003). Activation of the interferon system by short-interfering RNAs. Nat. Cell Biol. 5, 834-839.
35. Takenawa, T. and Miki, H. (2001). WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J. Cell Sci. 114, 1801-1809.
36. Unemori, E. N. and Werb, Z. (1986). Reorganization of polymerized actin: a possible trigger for induction of procollagenase in fibroblasts cultured in and on collagen gels. J. Cell Biol. 103 1021-1031.
37. Utani, A., Momota, Y., Endo, H., Kasuya, Y., Beek, K., Suzuki, N., Nomizu, M. and Shinkai, H. (2003). Laminin alpha 3 LG4 module induces matrix metalloproteinase-1 through mitogen-activated protein kinase signaling. J. Biol. Chem. 278, 34483-34490.
38. Vincenti, M. P., Coon, C. I., White, L. A., Barchowsky, A. and Brinckerhoff, C. E. (1996). Src-related tyrosine kinases regulate transcriptional activation of the interstitial collagenase gene, MMP-1, in interleukin-1-stimulated synovial fibroblasts. Arthritis Rheum. 39, 574-582.
39. Wells, C. M., Walmsley, M., Ooi, S., Tybulewicz, V. and Ridley, A. J. (2004). Rac1-deficient macrophages exhibit defects in cell spreading and membrane ruffling but not migration. J. Cell Sci. 117, 1259-1268.
40. Werner, E. and Werb, Z. (2002). Integrins engage mitochondrial function for signal transduction by a mechanism dependent on Rho GTPases. J. Cell Biol. 158, 357-368.
41. Werner, E., Kheradmand, F., Isberg, R. R. and Werb, Z. (2001). Phagocytosis mediated by Yersinia invasin induces collagenase-1 expression in rabbit synovial fibroblasts through a proinflammatory cascade. J. Cell Sci. 114, 3333-3343.
42. West-Mays, J. A., Strissel, K. J., Sadow, P. M. and Fini, M. E. (1995). Competence for collagenase gene expression by tissue fibroblasts requires activation of an interleukin 1 alpha autocrine loop. Proc. Natl. Acad. Sci. USA 92, 6768-6772.
43. Westermarck, J., Li, S. P., Kallunki, T., Han, J. and Kahari, V. M. (2001). p38 mitogen-activated protein kinase-dependent activation of protein phosphatases 1 and 2A inhibits MEK1 and MEK2 activity and collagenase I (MMP-1) gene expression. Mol. Cell. Biol. 21, 2373-2383.
44. Xu, J., Clark, R. A. and Parks, W. C. (2001). p38 mitogen-activated kinase is a bidirectional regulator of human fibroblast collagenase-1 induction by three-dimensional collagen lattices. Biochem. J. 355, 437-447.
45. Yamamoto, T., Eckes, B., Mauch, C., Hartmann, K. and Krieg, T. (2000). Monocyte chemoattractant protein-1 enhances gene expression and synthesis of matrix metalloproteinase-1 in human fibroblasts by an autocrine IL-1 alpha loop. J. Immunol. 164, 6174-6179.
46. Zugasti, O., Rul, W., Roux, P., Peyssonnaux, C., Eychene, A., Franke, T. F., Fort, P. and Hibner, U. (2001). Raf-MEK-Erk cascade in anoikis is controlled by Rac1 and Cdc42 via Akt. Mol. Cell. Biol. 21, 6706-6717.
47. Zhuge, Y. and Xu, J. (2001). Rac1 mediates type I collagen-dependent MMP-2 activation. role in cell invasion across collagen barrier. J. Biol. Chem. 276, 16248-16256.