Pericellular fibronectin is required for RhoA-dependent responses to cyclic strain in fibroblasts

Journal of Cell Science

Volumn 123, Issue 9, 2010, Pages 1511-1521

  Lutz, Roman ^a   Sakai, Takao ^b,d   Chiquet, Matthias ^c  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c UNIVERSITY OF BERN   (Switzerland)

^d LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Actin; Cyclic strain; Fibronectin; MAL MKL1 MRTF A; Mechanotransduction; RhoA; Tenascin C

Indexed keywords

ACTIN; ALPHA5 INTEGRIN; FIBRONECTIN; HEPARIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TENASCIN; TENSIN; VITRONECTIN;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL ADHESION; CELL NUCLEUS; CONTROLLED STUDY; ENZYME ACTIVATION; FIBROBLAST; KNOCKOUT GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ASSEMBLY; SIGNAL TRANSDUCTION;

ACTINS; ANIMALS; BINDING SITES; CELL ADHESION; CELL NUCLEUS; EMBRYO, MAMMALIAN; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLASTS; FIBRONECTINS; HEPARIN; INTEGRIN ALPHA5; MICE; MICROFILAMENT PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RHOA GTP-BINDING PROTEIN; RNA, MESSENGER; STRESS, MECHANICAL; TENASCIN; TRANS-ACTIVATORS; VITRONECTIN;

EID: 77951728146     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.060905     Document Type: Article

References (54)

1. Asparuhova, M. B., Gelman, L. and Chiquet, M. (2009). Role of the actin cytoskeleton in tuning cellular responses to external mechanical stress. Scand. J. Med. Sci. Sports. 19, 490-499.
2. Aufderheide, E. and Ekblom, P. (1988). Tenascin during gut development: appearance in the mesenchyme, shift in molecular forms, and dependence on epithelial-mesenchymal interactions. J. Cell Biol. 107, 2341-2349. (Pubitemid 19015112)
3. Bloom, L., Ingham, K. C. and Hynes, R. O. (1999). Fibronectin regulates assembly of actin filaments and focal contacts in cultured cells via the heparin-binding site in repeat III13. Mol. Biol. Cell 10, 1521-1536. (Pubitemid 29230906)
4. Butcher, D. T., Alliston, T. and Weaver, V. M. (2009). A tense situation: forcing tumour progression. Nat. Rev. Cancer 9, 108-122.
5. Chaqour, B. and Goppelt-Struebe, M. (2006). Mechanical regulation of the Cyr61/CCN1 and CTGF/CCN2 proteins. FEBS J. 273, 3639-3649.
6. Chaqour, B., Yang, R. and Sha, Q. (2006). Mechanical stretch modulates the promoter activity of the profibrotic factor CCN2 through increased actin polymerization and NF-kappaB activation. J. Biol. Chem. 281, 20608-20622. (Pubitemid 44065832)
7. Chen, C. S. (2008). Mechanotransduction-a field pulling together? J. Cell Sci. 121, 3285-3292.
8. Chiquet, M., Sarasa-Renedo, A. and Tunc-Civelek, V. (2004). Induction of tenascin-C by cyclic tensile strain versus growth factors: distinct contributions by Rho/ROCK and MAPK signaling pathways. Biochim. Biophys. Acta 1693, 193-204. (Pubitemid 39195237)
9. Chiquet, M., Tunc-Civelek, V. and Sarasa-Renedo, A. (2007). Gene regulation by mechanotransduction in fibroblasts. Appl. Physiol. Nutr. Metab. 32, 967-973.
10. Chiquet, M., Gelman, L., Lutz, R. and Maier, S. (2009). From mechanotransduction to extracellular matrix gene expression in fibroblasts. Biochim. Biophys. Acta 1793, 911-920. (Pubitemid 41032386)
11. Chiquet-Ehrismann, R., Kalla, P., Pearson, C. A., Beck, K. and Chiquet, M. (1988). Tenascin interferes with fibronectin action. Cell 53, 383-390.
12. Danen, E. H., Sonneveld, P., Sonnenberg, A. and Yamada, K. M. (2000). Dual stimulation of Ras/mitogen-activated protein kinase and RhoA by cell adhesion to fibronectin supports growth factor-stimulated cell cycle progression. J. Cell Biol. 151, 1413-1422. (Pubitemid 32047591)
13. Danen, E. H., Sonneveld, P., Brakebusch, C., Fassler, R. and Sonnenberg, A. (2002). The fibronectin-binding integrins alpha5beta1 and alphavbeta3 differentially modulate RhoA-GTP loading, organization of cell matrix adhesions, and fibronectin fibrillogenesis. J. Cell Biol. 159, 1071-1086. (Pubitemid 36055761)
14. Ehrismann, R., Roth, D. E., Eppenberger, H. M. and Turner, D. C. (1982). Arrangement of attachment-promoting, self-association, and heparin-binding sites in horse serum fibronectin. J. Biol. Chem. 257, 7381-7387. (Pubitemid 12002764)
15. Fluck, M., Tunc-Civelek, V. and Chiquet, M. (2000). Rapid and reciprocal regulation of tenascin-C and tenascin-Y expression by loading of skeletal muscle. J. Cell Sci. 113, 3583-3591.
16. Fontana, L., Chen, Y., Prijatelj, P., Sakai, T., Fassler, R., Sakai, L. Y. and Rifkin, D. B. (2005). Fibronectin is required for integrin alphavbeta6-mediated activation of latent TGF-beta complexes containing LTBP-1. FASEB J. 19, 1798-1808. (Pubitemid 41598764)
17. Friedland, J. C., Lee, M. H. and Boettiger, D. (2009). Mechanically activated integrin switch controls alpha5beta1 function. Science 323, 642-644.
18. Geiger, B., Spatz, J. P. and Bershadsky, A. D. (2009). Environmental sensing through focal adhesions. Nat. Rev. Mol. Cell Biol. 10, 21-33.
19. Graness, A., Giehl, K. and Goppelt-Struebe, M. (2006). Differential involvement of the integrin-linked kinase (ILK) in RhoA-dependent rearrangement of F-actin fibers and induction of connective tissue growth factor (CTGF). Cell. Signal. 18, 433-440. (Pubitemid 41794049)
20. Grinnell, F. and Feld, M. K. (1979). Initial adhesion of human fibroblasts in serum-free medium: possible role of secreted fibronectin. Cell 17, 117-129. (Pubitemid 9188216)
21. Hahn, C. and Schwartz, M. A. (2009). Mechanotransduction in vascular physiology and atherogenesis. Nat. Rev. Mol. Cell Biol. 10, 53-62.
22. Horton, M. A. (1997). The alpha v beta 3 integrin "vitronectin receptor". Int. J. Biochem. Cell Biol. 29, 721-725.
23. Hsieh, A. H., Tsai, C. M., Ma, Q. J., Lin, T., Banes, A. J., Villarreal, F. J., Akeson, W. H. and Sung, K. L. (2000). Time-dependent increases in type-III collagen gene expression in medical collateral ligament fibroblasts under cyclic strains. J. Orthop. Res. 18, 220-227. (Pubitemid 30304750)
24. Huang, W., Chiquet-Ehrismann, R., Moyano, J. V., Garcia-Pardo, A. and Orend, G. (2001). Interference of tenascin-C with syndecan-4 binding to fibronectin blocks cell adhesion and stimulates tumor cell proliferation. Cancer Res. 61, 8586-8594. (Pubitemid 33131143)
25. Huveneers, S., Truong, H., Fassler, R., Sonnenberg, A. and Danen, E. H. (2008). Binding of soluble fibronectin to integrin alpha5 beta1-link to focal adhesion redistribution and contractile shape. J. Cell Sci. 121, 2452-2462.
26. Inoh, H., Ishiguro, N., Sawazaki, S., Amma, H., Miyazu, M., Iwata, H., Sokabe, M. and Naruse, K. (2002). Uni-axial cyclic stretch induces the activation of transcription factor nuclear factor kappaB in human fibroblast cells. FASEB J. 16, 405-407.
27. Jones, P. F., Jakubowicz, T., Pitossi, F. J., Maurer, F. and Hemmings, B. A. (1991). Molecular cloning and identification of a serine/threonine protein kinase of the second-messenger subfamily. Proc. Natl. Acad. Sci. USA 88, 4171-4175. (Pubitemid 21914501)
28. Katz, B. Z., Zamir, E., Bershadsky, A., Kam, Z., Yamada, K. M. and Geiger, B. (2000). Physical state of the extracellular matrix regulates the structure and molecular composition of cell-matrix adhesions. Mol. Biol. Cell 11, 1047-1060. (Pubitemid 30159321)
29. Kong, F., Garcia, A. J., Mould, A. P., Humphries, M. J. and Zhu, C. (2009). Demonstration of catch bonds between an integrin and its ligand. J. Cell Biol. 185, 1275-1284.
30. Legate, K. R., Montanez, E., Kudlacek, O. and Fassler, R. (2006). ILK, PINCH and parvin: the tIPP of integrin signalling. Nat. Rev. Mol. Cell Biol. 7, 20-31. (Pubitemid 43361569)
31. Lehoux, S., Castier, Y. and Tedgui, A. (2006). Molecular mechanisms of the vascular responses to haemodynamic forces. J. Intern. Med. 259, 381-392. (Pubitemid 43384229)
32. Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408. (Pubitemid 34164012)
33. Magnusson, S. P., Narici, M. V., Maganaris, C. N. and Kjaer, M. (2008). Human tendon behaviour and adaptation, in vivo. J. Physiol. 586, 71-81.
34. Maier, S., Lutz, R., Gelman, L., Sarasa-Renedo, A., Schenk, S., Grashoff, C. and Chiquet, M. (2008). Tenascin-C induction by cyclic strain requires integrin-linked kinase. Biochim. Biophys. Acta. 1783, 1150-1162
35. Mao, Y. and Schwarzbauer, J. E. (2005). Fibronectin fibrillogenesis, a cell-mediated matrix assembly process. Matrix Biol. 24, 389-399. (Pubitemid 41765018)
36. Midwood, K. S. and Schwarzbauer, J. E. (2002). Tenascin-C modulates matrix contraction via focal adhesion kinase- and Rho-mediated signaling pathways. Mol. Biol. Cell 13, 3601-3613.
37. Midwood, K. S., Valenick, L. V., Hsia, H. C. and Schwarzbauer, J. E. (2004). Coregulation of fibronectin signaling and matrix contraction by tenascin-C and syndecan-4. Mol. Biol. Cell 15, 5670-5677.
38. Miralles, F., Posern, G., Zaromytidou, A. I. and Treisman, R. (2003). Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 113, 329-342. (Pubitemid 36556115)
39. Orr, A. W., Helmke, B. P., Blackman, B. R. and Schwartz, M. A. (2006). Mechanisms of mechanotransduction. Dev. Cell 10, 11-20.
40. Ren, X. D. and Schwartz, M. A. (2000). Determination of GTP loading on Rho. Methods Enzymol. 325, 264-272.
41. Sakai, T., Johnson, K. J., Murozono, M., Sakai, K., Magnuson, M. A., Wieloch, T., Cronberg, T., Isshiki, A., Erickson, H. P. and Fassler, R. (2001). Plasma fibronectin supports neuronal survival and reduces brain injury following transient focal cerebral ischemia but is not essential for skin-wound healing and hemostasis. Nat. Med. 7, 324-330. (Pubitemid 32224348)
42. Sarasa-Renedo, A., Tunc-Civelek, V. and Chiquet, M. (2006). Role of RhoA/ROCK-dependent actin contractility in the induction of tenascin-C by cyclic tensile strain. Exp. Cell Res. 312, 1361-1370.
43. Schild, C. and Trueb, B. (2004). Three members of the connective tissue growth factor family CCN are differentially regulated by mechanical stress. Biochim. Biophys. Acta 1691, 33-40. (Pubitemid 38410948)
44. Smith, P. G., Roy, C., Zhang, Y. N. and Chauduri, S. (2003). Mechanical stress increases RhoA activation in airway smooth muscle cells. Am. J. Respir. Cell Mol. Biol. 28, 436-442. (Pubitemid 36399365)
45. Stupack, D. G. and Cheresh, D. A. (2002). Get a ligand, get a life: integrins, signaling and cell survival. J. Cell Sci. 115, 3729-3738.
46. Vouret-Craviari, V., Boulter, E., Grall, D., Matthews, C. and Van Obberghen-Schilling, E. (2004). ILK is required for the assembly of matrix-forming adhesions and capillary morphogenesis in endothelial cells. J. Cell Sci. 117, 4559-4569. (Pubitemid 39360081)
47. Wehrle, B. and Chiquet, M. (1990). Tenascin is accumulated along developing peripheral nerves and allows neurite outgrowth in vitro. Development 110, 401-415. (Pubitemid 20330516)
48. Wenk, M. B., Midwood, K. S. and Schwarzbauer, J. E. (2000). Tenascin-C suppresses Rho activation. J. Cell Biol. 150, 913-920.
49. Wipff, P. J., Rifkin, D. B., Meister, J. J. and Hinz, B. (2007). Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix. J. Cell Biol. 179, 1311-1323.
50. Woods, A. and Couchman, J. R. (1994). Syndecan 4 heparan sulfate proteoglycan is a selectively enriched and widespread focal adhesion component. Mol. Biol. Cell 5, 183-192. (Pubitemid 24108464)
51. Zaidel-Bar, R., Cohen, M., Addadi, L. and Geiger, B. (2004). Hierarchical assembly of cell-matrix adhesion complexes. Biochem. Soc. Trans. 32, 416-420. (Pubitemid 38813527)
52. Zamir, E., Katz, M., Posen, Y., Erez, N., Yamada, K. M., Katz, B. Z., Lin, S., Lin, D. C., Bershadsky, A., Kam, Z. et al. (2000). Dynamics and segregation of cell-matrix adhesions in cultured fibroblasts. Nat. Cell Biol. 2, 191-196.
53. Zhao, X. H., Laschinger, C., Arora, P., Szaszi, K., Kapus, A. and McCulloch, C. A. (2007). Force activates smooth muscle alpha-actin promoter activity through the Rho signaling pathway. J. Cell Sci. 120, 1801-1809. (Pubitemid 46930418)
54. Ziegler, W. H., Liddington, R. C. and Critchley, D. R. (2006). The structure and regulation of vinculin. Trends Cell Biol. 16, 453-460.