TGF-β-induced differentiation into myofibroblasts involves specific regulation of two MKL1 isoforms

Journal of Cell Science

Volumn 127, Issue 5, 2014, Pages 1079-1091

  Scharenberg, Matthias A ^a,b   Pippenger, Benjamin E ^c   Sack, Ragna ^a   Zingg, Dominik ^a   Ferralli, Jacqueline ^a   Schenk, Susanne ^a,d   Martin, Ivan ^b   Chiquet Ehrismann, Ruth ^a,b  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY HOSPITAL BASEL   (Switzerland)

^d Pharmazentrum   (Switzerland)

Author keywords

Gene regulation; MKL1; Mrtf a; Myofibroblast differentiation

Indexed keywords

ISOPROTEIN; MATRIX METALLOPROTEINASE 16; SPOCK 3 PROTEIN; TESTICAN 3 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MKL1 L; TRANSCRIPTION FACTOR MKL1 S; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; EXTRACELLULAR MATRIX; FEMALE; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MYOFIBROBLAST; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN MOTIF; TRANSLATION INITIATION; UPREGULATION;

GENE REGULATION; MKL1; MRTF-A; MYOFIBROBLAST DIFFERENTIATION;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; BASE SEQUENCE; CELL DIFFERENTIATION; CELL NUCLEUS; CODON, INITIATOR; DNA-BINDING PROTEINS; HEK293 CELLS; HELA CELLS; HUMANS; MATRIX METALLOPROTEINASE 16; MOLECULAR SEQUENCE DATA; MYOFIBROBLASTS; ONCOGENE PROTEINS, FUSION; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA1; UP-REGULATION;

EID: 84896820736     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.142075     Document Type: Article

References (37)

1. Asparuhova, M. B., Ferralli, J., Chiquet, M. and Chiquet-Ehrismann, R. (2011). The transcriptional regulator megakaryoblastic leukemia-1 mediates serum response factor-independent activation of tenascin-C transcription by mechanical stress. FASEB J. 25, 3477-3488.
2. Charbonney, E., Speight, P., Masszi, A., Nakano, H. and Kapus, A. (2011). βcatenin and Smad3 regulate the activity and stability of myocardin-related transcription factor during epithelial-myofibroblast transition. Mol. Biol. Cell 22, 4472-4485.
3. Chiquet, M., Sarasa-Renedo, A. and Tunç-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.
4. Crider, B. J., Risinger, G. M., Jr, Haaksma, C. J., Howard, E. W. and Tomasek, J. J. (2011). Myocardin-related transcription factors A and B are key regulators of TGF-b1-induced fibroblast to myofibroblast differentiation. J. Invest. Dermatol. 131, 2378-2385.
5. Fan, L., Sebe, A., Péterfi, Z., Masszi, A., Thirone, A. C., Rotstein, O. D., Nakano, H., McCulloch, C. A., Szászi, K., Mucsi, I. et al. (2007). Cell contactdependent regulation of epithelial-myofibroblast transition via the rho-rho kinase-phospho-myosin pathway. Mol. Biol. Cell 18, 1083-1097.
6. Gupta, M., Korol, A. and West-Mays, J. A. (2013). Nuclear translocation of myocardin-related transcription factor-A during transforming growth factor betainduced epithelial to mesenchymal transition of lens epithelial cells. Mol. Vis. 19, 1017-1028.
7. Hinz, B., Phan, S. H., Thannickal, V. J., Prunotto, M., Desmoulière, A., Varga, J., De Wever, O., Mareel, M. and Gabbiani, G. (2012). Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am. J. Pathol. 180, 1340-1355.
8. Howard, E. W., Crider, B. J., Updike, D. L., Bullen, E. C., Parks, E. E., Haaksma, C. J., Sherry, D. M. and Tomasek, J. J. (2012). MMP-2 expression by fibroblasts is suppressed by the myofibroblast phenotype. Exp. Cell Res. 318, 1542-1553.
9. Jeon, E. S., Moon, H. J., Lee, M. J., Song, H. Y., Kim, Y. M., Cho, M., Suh, D.-S., Yoon, M.-S., Chang, C. L., Jung, J. S. et al. (2008a). Cancer-derived lysophosphatidic acid stimulates differentiation of human mesenchymal stem cells to myofibroblast-like cells. Stem Cells 26, 789-797.
10. Jeon, E. S., Park, W. S., Lee, M. J., Kim, Y. M., Han, J. and Kim, J. H. (2008b). A Rho kinase/myocardin-related transcription factor-A-dependent mechanism underlies the sphingosylphosphorylcholine-induced differentiation of mesenchymal stem cells into contractile smooth muscle cells. Circ. Res. 103, 635-642.
11. Jeon, E. S., Heo, S. C., Lee, I. H., Choi, Y. J., Park, J. H., Choi, K. U., Park, Y., Suh, D. S., Yoon, M. S. and Kim, J. H. (2010). Ovarian cancer-derived lysophosphatidic acid stimulates secretion of VEGF and stromal cell-derived factor-1 alpha from human mesenchymal stem cells. Exp. Mol. Med. 42, 280-293.
12. Jotzu, C., Alt, E., Welte, G., Li, J., Hennessy, B. T., Devarajan, E., Krishnappa, S., Pinilla, S., Droll, L. and Song, Y.-H. (2011). Adipose tissue derived stem cells differentiate into carcinoma-associated fibroblast-like cells under the influence of tumor derived factors. Cell. Oncol. (Dordr.) 34, 55-67.
13. Kakudo, N., Kushida, S., Suzuki, K., Ogura, T., Notodihardjo, P. V., Hara, T. and Kusumoto, K. (2012). Effects of transforming growth factor-beta1 on cell motility, collagen gel contraction, myofibroblastic differentiation, and extracellular matrix expression of human adipose-derived stem cell. Hum. Cell 25, 87-95.
14. Kozak, M. (1989). Context effects and inefficient initiation at non-AUG codons in eucaryotic cell-free translation systems. Mol. Cell. Biol. 9, 5073-5080.
15. Kurpinski, K., Chu, J., Wang, D. and Li, S. (2009). Proteomic profiling of mesenchymal stem cell responses to mechanical strain and TGF-beta1. Cell. Mol. Bioeng. 2, 606-614.
16. Maier, S., Lutz, R., Gelman, L., Sarasa-Renedo, A., Schenk, S., Grashoff, C. and Chiquet, M. (2008). Tenascin-C induction by cyclic strain requires integrinlinked kinase. Biochim. Biophys. Acta 1783, 1150-1162.
17. Martin, P. (2009). Common transactivation motif 9aaTAD recruits multiple general co-activators TAF9, MED15, CBP and p300. Nature Precedings 12, 30.
18. Masszi, A., Fan, L., Rosivall, L., McCulloch, C. A., Rotstein, O. D., Mucsi, I. and Kapus, A. (2004). Integrity of cell-cell contacts is a critical regulator of TGFbeta 1-induced epithelial-to-myofibroblast transition: role for beta-catenin. Am J. Pathol. 165, 1955-1967.
19. Masszi, A., Speight, P., Charbonney, E., Lodyga, M., Nakano, H., Szá szi, K. and Kapus, A. (2010). Fate-determining mechanisms in epithelial-myofibroblast transition: major inhibitory role for Smad3. J. Cell Biol. 188, 383-399.
20. Mihira, H., Suzuki, H. I., Akatsu, Y., Yoshimatsu, Y., Igarashi, T., Miyazono, K. and Watabe, T. (2012). TGF-b-induced mesenchymal transition of MS-1 endothelial cells requires Smad-dependent cooperative activation of Rho signals and MRTF-A. J. Biochem. 151, 145-156.
21. Minami, T., Kuwahara, K., Nakagawa, Y., Takaoka, M., Kinoshita, H., Nakao, K., Kuwabara, Y., Yamada, Y., Yamada, C., Shibata, J. et al. (2012). Reciprocal expression of MRTF-A and myocardin is crucial for pathological vascular remodelling in mice. EMBO J. 31, 4428-4440.
22. 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.
23. Morita, T., Mayanagi, T. and Sobue, K. (2007). Dual roles of myocardin-related transcription factors in epithelial mesenchymal transition via slug induction and actin remodeling. J. Cell Biol. 179, 1027-1042.
24. Nakada, M., Yamada, A., Takino, T., Miyamori, H., Takahashi, T., Yamashita, J. and Sato, H. (2001). Suppression of membrane-type 1 matrix metalloproteinase (MMP)-mediated MMP-2 activation and tumor invasion by testican 3 and its splicing variant gene product, N-Tes. Cancer Res. 61, 8896-8902.
25. Piskacek, S., Gregor, M., Nemethova, M., Grabner, M., Kovarik, P. and Piskacek, M. (2007). Nine-amino-acid transactivation domain: establishment and prediction utilities. Genomics 89, 756-768.
26. Sandbo, N., Lau, A., Kach, J., Ngam, C., Yau, D. and Dulin, N. O. (2011). Delayed stress fiber formation mediates pulmonary myofibroblast differentiation in response to TGF-β. Am. J. Physiol. 301, L656-L666.
27. Sarrazy, V., Billet, F., Micallef, L., Coulomb, B. and Desmoulière, A. (2011). Mechanisms of pathological scarring: role of myofibroblasts and current developments. Wound Repair Regen. 19 Suppl. 1, s10-s15.
28. Sasazuki, T., Sawada, T., Sakon, S., Kitamura, T., Kishi, T., Okazaki, T., Katano, M., Tanaka, M., Watanabe, M., Yagita, H. et al. (2002). Identification of a novel transcriptional activator, BSAC, by a functional cloning to inhibit tumor necrosis factor-induced cell death. J. Biol. Chem. 277, 28853-28860.
29. Selvaraj, A. and Prywes, R. (2004). Expression profiling of serum inducible genes identifies a subset of SRF target genes that are MKL dependent. BMC Mol. Biol. 5, 13.
30. Small, E. M. (2012). The actin-MRTF-SRF gene regulatory axis and myofibroblast differentiation. J. Cardiovasc. Transl. Res. 5, 794-804.
31. Tomasek, J. J., Gabbiani, G., Hinz, B., Chaponnier, C. and Brown, R. A. (2002). Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 3, 349-363.
32. Wang, D., Chang, P. S., Wang, Z., Sutherland, L., Richardson, J. A., Small, E., Krieg, P. A. and Olson, E. N. (2001). Activation of cardiac gene expression by myocardin, a transcriptional cofactor for serum response factor. Cell 105, 851-862.
33. Wang, D.-Z., Li, S., Hockemeyer, D., Sutherland, L., Wang, Z., Schratt, G., Richardson, J. A., Nordheim, A. and Olson, E. N. (2002). Potentiation of serum response factor activity by a family of myocardin-related transcription factors. Proc. Natl. Acad. Sci. USA 99, 14855-14860.
34. Yu, Q. and Stamenkovic, I. (2000). Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev. 14, 163-176.
35. Zheng, L., Baumann, U. and Reymond, J.-L. (2004). An efficient one-step sitedirected and site-saturation mutagenesis protocol. Nucleic Acids Res. 32, e115.
36. Zhou, Y., Huang, X., Hecker, L., Kurundkar, D., Kurundkar, A., Liu, H., Jin, T.-H., Desai, L., Bernard, K. and Thannickal, V. J. (2013). Inhibition ofmechanosensitive signaling in myofibroblasts ameliorates experimental pulmonary fibrosis. J. Clin. Invest. 123, 1096-1108.
37. Zuk, P. A. (2010). The adipose-derived stem cell: looking back and looking ahead. Mol. Biol. Cell 21, 1783-1787.