MMP-2 expression by fibroblasts is suppressed by the myofibroblast phenotype

Experimental Cell Research

Volumn 318, Issue 13, 2012, Pages 1542-1553

  Howard, Eric W ^a   Crider, Beverly J ^a   Updike, Dawn L ^a   Bullen, Elizabeth C ^a   Parks, Eileen E ^a   Haaksma, Carol J ^a   Sherry, David M ^a,b   Tomasek, James J ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

Author keywords

Cell tension; Contractility; Fibroblast; MMP 2; Myofibroblast

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; GELATINASE A; MYOCARDIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FIBROBLAST; GENE EXPRESSION; MYOFIBROBLAST; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION;

EID: 84862000643     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2012.03.007     Document Type: Article

References (61)

1. Tomasek J.J., Gabbiani G., Hinz B., Chaponnier C., Brown R.A. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 2002, 3:349-363.
2. Schafer M., Werner S. Transcriptional control of wound repair. Annu. Rev. Cell Dev. Biol. 2007, 23:69-92.
3. Hinz B. Formation and function of the myofibroblast during tissue repair. J. Invest. Dermatol. 2007, 127:526-537.
4. Hinz B. Masters and servants of the force: the role of matrix adhesions in myofibroblast force perception and transmission. Eur. J. Cell Biol. 2006, 85:175-181.
5. Darby I.A., Hewitson T.D. Fibroblast differentiation in wound healing and fibrosis. Int. Rev. Cytol. 2007, 257:143-179.
6. Watsky M.A., Weber K.T., Sun Y., Postlethwaite A. New insights into the mechanism of fibroblast to myofibroblast transformation and associated pathologies. Int. Rev. Cell Mol. Biol. 2010, 282:165-192.
7. Hinz B. The myofibroblast: paradigm for a mechanically active cell. J. Biomech. 2010, 43:146-155.
8. Sun Q., Chen G., Streb J.W., Long X., Yang Y., Stoeckert C.J., Miano J.M. Defining the mammalian CArGome. Genome Res. 2006, 16:197-207.
9. Johansen F.E., Prywes R. Serum response factor: transcriptional regulation of genes induced by growth factors and differentiation. Biochim. Biophys. Acta 1995, 1242:1-10.
10. Posern G., Treisman R. Actin' together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol. 2006, 16:588-596.
11. Kumar M.S., Owens G.K. Combinatorial control of smooth muscle-specific gene expression. Arterioscler. Thromb. Vasc. Biol. 2003, 23:737-747.
12. Owens G.K., Kumar M.S., Wamhoff B.R. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 2004, 84:767-801.
13. Pipes G.C., Creemers E.E., Olson E.N. The myocardin family of transcriptional coactivators: versatile regulators of cell growth, migration, and myogenesis. Genes Dev. 2006, 20:1545-1556.
14. Parmacek M.S. Myocardin-related transcription factors: critical coactivators regulating cardiovascular development and adaptation. Circ. Res. 2007, 100:633-644.
15. Vartiainen M.K., Guettler S., Larijani B., Treisman R. Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 2007, 316:1749-1752.
16. Crider B.J., Risinger G.M., Haaksma C.J., Howard E.W., Tomasek J.J. Myocardin-Related Transcription Factors A and B Are Key Regulators of TGF-beta1-Induced Fibroblast to Myofibroblast Differentiation. J. Invest. Dermatol. 2011, 131:2378-2385.
17. Page-McCaw A., Ewald A.J., Werb Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 2007, 8:221-233.
18. Rodriguez D., Morrison C.J., Overall C.M. Matrix metalloproteinases: what do they not do? New substrates and biological roles identified by murine models and proteomics. Biochim. Biophys. Acta 2010, 1803:39-54.
19. Wu L., Derynck R. Essential role of TGF-beta signaling in glucose-induced cell hypertrophy. Dev. Cell 2009, 17:35-48.
20. Yu Q., Stamenkovic I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev. 2000, 14:163-176.
21. Hultgardh-Nilsson A., Lovdahl C., Blomgren K., Kallin B., Thyberg J. Expression of phenotype- and proliferation-related genes in rat aortic smooth muscle cells in primary culture. Cardiovasc. Res. 1997, 34:418-430.
22. Kenagy R.D., Clowes A.W. A possible role for MMP-2 and MMP-9 in the migration of primate arterial smooth muscle cells through native matrix. Ann. N. Y. Acad. Sci. 1994, 732:462-465.
23. Risinger G.M., Hunt T.S., Updike D.L., Bullen E.C., Howard E.W. Matrix metalloproteinase-2 expression by vascular smooth muscle cells is mediated by both stimulatory and inhibitory signals in response to growth factors. J. Biol. Chem. 2006, 281:25915-25925.
24. Uzui H., Lee J.D., Shimizu H., Tsutani H., Ueda T. The role of protein-tyrosine phosphorylation and gelatinase production in the migration and proliferation of smooth muscle cells. Atherosclerosis 2000, 149:51-59.
25. Risinger G.M., Updike D.L., Bullen E.C., Tomasek J.J., Howard E.W. TGF-beta suppresses the upregulation of MMP-2 by vascular smooth muscle cells in response to PDGF-BB. Am. J. Physiol. Cell Physiol. 2010, 298:C191-C201.
26. Tomasek J.J., Halliday N.L., Updike D.L., Ahern-Moore J.S., Vu T.K., Liu R.W., Howard E.W. Gelatinase A activation is regulated by the organization of the polymerized actin cytoskeleton. J. Biol. Chem. 1997, 272:7482-7487.
27. Xie T.X., Huang F.J., Aldape K.D., Kang S.H., Liu M., Gershenwald J.E., Xie K., Sawaya R., Huang S. Activation of stat3 in human melanoma promotes brain metastasis. Cancer Res. 2006, 66:3188-3196.
28. Freshney I.J. Culture of Animal Cells: A Manual of Basic Technique 1987, Alan R. Liss, Inc., New York.
29. Vaughan M.B., Howard E.W., Tomasek J.J. Transforming growth factor-beta1 promotes the morphological and functional differentiation of the myofibroblast. Exp. Cell Res. 2000, 257:180-189.
30. Parizi M., Howard E.W., Tomasek J.J. Regulation of LPA-promoted myofibroblast contraction: role of Rho, myosin light chain kinase, and myosin light chain phosphatase. Exp. Cell Res. 2000, 254:210-220.
31. Guilluy C., Swaminathan V., Garcia-Mata R., O'Brien E.T., Superfine R., Burridge K. The Rho GEFs LARG and GEF-H1 regulate the mechanical response to force on integrins. Nat. Cell Biol. 2011, 13:722-727.
32. Spector I., Shochet N.R., Blasberger D., Kashman Y. Latrunculins-novel marine macrolides that disrupt microfilament organization and affect cell growth: I. Comparison with cytochalasin D. Cell Motil. Cytoskeleton 1989, 13:127-144.
33. Follonier Castella L., Gabbiani G., McCulloch C.A., Hinz B. Regulation of myofibroblast activities: calcium pulls some strings behind the scene. Exp. Cell Res. 2010, 316:2390-2401.
34. Bogatkevich G.S., Tourkina E., Silver R.M., Ludwicka-Bradley A. Thrombin differentiates normal lung fibroblasts to a myofibroblast phenotype via the proteolytically activated receptor-1 and a protein kinase C-dependent pathway. J. Biol. Chem. 2001, 276:45184-45192.
35. Jiang H., Rhee S., Ho C.H., Grinnell F. Distinguishing fibroblast promigratory and procontractile growth factor environments in 3-D collagen matrices. FASEB J. 2008, 22:2151-2160.
36. Grinnell F., Petroll W.M. Cell motility and mechanics in three-dimensional collagen matrices. Annu. Rev. Cell Dev. Biol. 2010, 26:335-361.
37. LeRoith D., Roberts C.T. The insulin-like growth factor system and cancer. Cancer Lett. 2003, 195:127-137.
38. Pyne S., Lee S.C., Long J., Pyne N.J. Role of sphingosine kinases and lipid phosphate phosphatases in regulating spatial sphingosine 1-phosphate signalling in health and disease. Cell. Signal. 2009, 21:14-21.
39. Miralles F., Posern G., Zaromytidou A.I., Treisman R. Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 2003, 113:329-342.
40. Ispanovic E., Serio D., Haas T.L. Cdc42 and RhoA have opposing roles in regulating membrane type 1-matrix metalloproteinase localization and matrix metalloproteinase-2 activation. Am. J. Physiol. Cell Physiol. 2008, 295:C600-C610.
41. Wall I.B., Bhadal N., Broad S., Whawell S.A., Mudera V., Lewis M.P. Force generation and protease gene expression in organotypic co-cultures of fibroblasts and keratinocytes. J. Tissue Eng. Regen. Med. 2009, 3:647-650.
42. Lee J.W., Kwak H.J., Lee J.J., Kim Y.N., Park M.J., Jung S.E., Hong S.I., Lee J.H., Lee J.S. HSP27 regulates cell adhesion and invasion via modulation of focal adhesion kinase and MMP-2 expression. Eur. J. Cell Biol. 2008, 87:377-387.
43. Zhuge Y., Xu J. Rac1 mediates type I collagen-dependent MMP-2 activation. role in cell invasion across collagen barrier. J. Biol. Chem. 2001, 276:16248-16256.
44. Kim E.S., Lee K.M., Noh D.Y., Moon A. Regulation of matrix metalloproteinases and invasion by G(alpha12/13) proteins in NIH3T3 mouse fibroblast cells. Oncol. Res. 2011, 19:297-301.
45. Knowles J.P., Shi-Wen X., Haque S.U., Bhalla A., Dashwood M.R., Yang S., Taylor I., Winslet M.C., Abraham D.J., Loizidou M. Endothelin-1 stimulates colon cancer adjacent fibroblasts. Int. J. Cancer 2011, 130:1264-1272.
46. Hawwa R.L., Hokenson M.A., Wang Y., Huang Z., Sharma S., Sanchez-Esteban J. Differential Expression of MMP-2 and -9 and their Inhibitors in Fetal Lung Cells Exposed to Mechanical Stretch: Regulation by IL-10. Lung 2011, 189:341-349.
47. Shelton L., Rada J.S. Effects of cyclic mechanical stretch on extracellular matrix synthesis by human scleral fibroblasts. Exp. Eye Res. 2007, 84:314-322.
48. Dalla Costa A.P., Clemente C.F., Carvalho H.F., Carvalheira J.B., Nadruz W., Franchini K.G. FAK mediates the activation of cardiac fibroblasts induced by mechanical stress through regulation of the mTOR complex. Cardiovasc. Res. 2010, 86:421-431.
49. Saygili E., Rana O.R., Meyer C., Gemein C., Andrzejewski M.G., Ludwig A., Weber C., Schotten U., Kruttgen A., Weis J., Schwinger R.H., Mischke K., Rassaf T., Kelm M., Schauerte P. The angiotensin-calcineurin-NFAT pathway mediates stretch-induced up-regulation of matrix metalloproteinases-2/-9 in atrial myocytes. Basic Res. Cardiol. 2009, 104:435-448.
50. Choe M.M., Sporn P.H., Swartz M.A. Extracellular matrix remodeling by dynamic strain in a three-dimensional tissue-engineered human airway wall model. Am. J. Respir. Cell Mol. Biol. 2006, 35:306-313.
51. Chiquet M., Gelman L., Lutz R., Maier S. From mechanotransduction to extracellular matrix gene expression in fibroblasts. Biochim. Biophys. Acta 2009, 1793:911-920.
52. Karamichos D., Brown R.A., Mudera V. Collagen stiffness regulates cellular contraction and matrix remodeling gene expression. J. Biomed. Mater. Res. A 2007, 83:887-894.
53. Werner S., Grose R. Regulation of wound healing by growth factors and cytokines. Physiol. Rev. 2003, 83:835-870.
54. Ye H., Cai P.C., Zhou Q., Ma W.L. Transforming growth factor-beta1 suppresses the up-regulation of matrix metalloproteinase-2 by lung fibroblasts in response to tumor necrosis factor-alpha. Wound Repair Regen. 2011, 19:392-399.
55. Marquez-Aguirre A., Sandoval-Rodriguez A., Gonzalez-Cuevas J., Bueno-Topete M., Navarro-Partida J., Arellano-Olivera I., Lucano-Landeros S., Armendariz-Borunda J. Adenoviral delivery of dominant-negative transforming growth factor beta type II receptor up-regulates transcriptional repressor SKI-like oncogene, decreases matrix metalloproteinase 2 in hepatic stellate cell and prevents liver fibrosis in rats. J. Gene Med. 2009, 11:207-219.
56. Overall C.M., Wrana J.L., Sodek J. Independent regulation of collagenase, 72-kDa progelatinase, and metalloendoproteinase inhibitor expression in human fibroblasts by transforming growth factor-beta. J. Biol. Chem. 1989, 264:1860-1869.
57. Simionescu A., Simionescu D.T., Vyavahare N.R. Osteogenic responses in fibroblasts activated by elastin degradation products and transforming growth factor-beta1: role of myofibroblasts in vascular calcification. Am. J. Pathol. 2007, 171:116-123.
58. Meng X.M., Huang X.R., Chung A.C., Qin W., Shao X., Igarashi P., Ju W., Bottinger E.P., Lan H.Y. Smad2 protects against TGF-beta/Smad3-mediated renal fibrosis. J. Am. Soc. Nephrol. 2010, 21:1477-1487.
59. Piek E., Ju W.J., Heyer J., Escalante-Alcalde D., Stewart C.L., Weinstein M., Deng C., Kucherlapati R., Bottinger E.P., Roberts A.B. Functional characterization of transforming growth factor beta signaling in Smad2- and Smad3-deficient fibroblasts. J. Biol. Chem. 2001, 276:19945-19953.
60. Sandbo N., Lau A., Kach J., Ngam C., Yau D., Dulin N.O. Delayed stress fiber formation mediates pulmonary myofibroblast differentiation in response to TGF-beta. Am. J. Physiol. Lung Cell. Mol. Physiol. 2011, 301:L656-L666.
61. Zhao X.H., Laschinger C., Arora P., Szaszi K., Kapus A., McCulloch C.A. Force activates smooth muscle alpha-actin promoter activity through the Rho signaling pathway. J. Cell Sci. 2007, 120:1801-1809.