The actin/MKL1 signalling pathway influences cell growth and gene expression through large-scale chromatin reorganization and histone post-translational modifications

Biochemical Journal

Volumn 461, Issue 2, 2014, Pages 257-268

  Flouriot, Gilles ^a   Huet, Guillaume ^a   Demay, Florence ^a   Pakdel, Farzad ^a   Boujrad, Noureddine ^a   Michel, Denis ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

Author keywords

Actin dynamics; Epithelial cell growth; Euchromatinization; Myocardin related transcription factor; Steroid receptor

Indexed keywords

G ACTIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MKL1; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CELL GROWTH; CELL PROLIFERATION; CHROMATIN; CHROMATIN STRUCTURE; CONTROLLED STUDY; EPIGENETICS; EUCHROMATIN; GENE EXPRESSION; HETEROCHROMATIN; HISTONE MODIFICATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN MODIFICATION; SIGNAL TRANSDUCTION;

ACETYLATION; ACTINS; CELL LINE, TUMOR; CELL PROLIFERATION; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA-BINDING PROTEINS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION; HISTONES; HUMANS; METHYLATION; ONCOGENE PROTEINS, FUSION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION;

EID: 84903291616     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20131240     Document Type: Article

References (44)

1. Thiery, J. P., Acloque, H., Huang, R. Y. J. and Nieto, M. A. (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139, 871-890 CrossRef PubMed
2. Chen, C. S., Mrksich, M., Huang, S., Whitesides, G. M. and Ingber, D. E. (1997) Geometric control of cell life and death. Science 276, 1425-1428 CrossRef PubMed (Pubitemid 27235413)
3. Nelson, C. M., Jean, R. P., Tan, J. L., Liu, W. F., Sniadecki, N. J., Spector, A. A. and Chen, C. S. (2005) Emergent patterns of growth controlled by multicellular form and mechanics. Proc. Natl. Acad. Sci. U.S.A. 102, 11594-11599 CrossRef PubMed (Pubitemid 41170771)
4. Solanas, G., Porta-de-la-Riva, M., Agustí, C., Casagolda, D., Sánchez-Aguilera, F., Larriba, M. J., Pons, F., Peiró, S., Escrivà, M., Muñoz, A. et al. (2008) E-cadherin controls beta-catenin and NF-κB transcriptional activity in mesenchymal gene expression. J. Cell Sci. 121, 2224-2234 CrossRef PubMed
5. Liu, C., Huang, W. and Lei, Q. (2011) Regulation and function of the TAZ transcription co-activator. Int. J. Biochem. Mol. Biol. 2, 247-256 PubMed
6. Dupont, S., Morsut, L., Aragona, M., Enzo, E., Giulitti, S., Cordenonsi, M., Zanconato, F., Le Digabel, J., Forcato, M., Bicciato, S. et al. (2011) Role of YAP/TAZ in mechanotransduction. Nature 474, 179-183 CrossRef PubMed
7. Wu, J. I., Crabtree, G. R. and Crabtee, G. R. (2007) Cell signaling. Nuclear actin as choreographer of cell morphology and transcription. Science 316, 1710-1711 (Pubitemid 46988537)
8. Zheng, B., Han, M., Bernier, M. and Wen, J. (2009) Nuclear actin and actin-binding proteins in the regulation of transcription and gene expression. FEBS J. 276, 2669-2685 CrossRef PubMed
9. Olson, E. N. and Nordheim, A. (2010) Linking actin dynamics and gene transcription to drive cellular motile functions. Nat. Rev. Mol. Cell Biol. 11, 353-365 CrossRef PubMed
10. Han, Z., Li, X., Wu, J. and Olson, E. N. (2004) A myocardin-related transcription factor regulates activity of serum response factor in Drosophila . Proc. Natl. Acad. Sci. U.S.A. 101, 12567-12572 CrossRef PubMed (Pubitemid 39122064)
11. 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. U.S.A. 99, 14855-14860 CrossRef PubMed (Pubitemid 35334573)
12. 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 CrossRef PubMed (Pubitemid 36556115)
13. Cen, B., Selvaraj, A., Burgess, R. C., Hitzler, J. K., Ma, Z., Morris, S. W. and Prywes, R. (2003) Megakaryoblastic leukemia 1, a potent transcriptional coactivator for serum response factor (SRF), is required for serum induction of SRF target genes. Mol. Cell. Biol. 23, 6597-6608 CrossRef PubMed (Pubitemid 37075770)
14. Vartiainen, M. K., Guettler, S., Larijani, B. and Treisman, R. (2007) Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 316, 1749-1752 CrossRef PubMed (Pubitemid 46988550)
15. Posern, G., Miralles, F., Guettler, S. and Treisman, R. (2004) Mutant actins that stabilise F-actin use distinct mechanisms to activate the SRF coactivator MAL. EMBO J. 23, 3973-3983 CrossRef PubMed (Pubitemid 39472419)
16. Huet, G., Mérot, Y., Percevault, F., Tiffoche, C., Arnal, J.-F., Boujrad, N., Pakdel, F., Métivier, R. and Flouriot, G. (2009) Repression of the estrogen receptor-α transcriptional activity by the Rho/megakaryoblastic leukemia 1 signaling pathway. J. Biol. Chem. 284, 33729-33739 CrossRef PubMed
17. Mérot, Y., Métivier, R., Penot, G., Manu, D., Saligaut, C., Gannon, F., Pakdel, F., Kah, O. and Flouriot, G. (2004) The relative contribution exerted by AF-1 and AF-2 transactivation functions in estrogen receptor α transcriptional activity depends upon the differentiation stage of the cell. J. Biol. Chem. 279, 26184-26191 CrossRef PubMed (Pubitemid 38798764)
18. Penot, G., Le Péron, C., Mérot, Y., Grimaud- Fanouillère, E., Ferrière, F., Boujrad, N., Kah, O., Saligaut, C., Ducouret, B., Métivier, R. et al. (2005) The human estrogen receptor-alpha isoform hERα46 antagonizes the proliferative influence of hERα66 in MCF7 breast cancer cells. Endocrinology 146, 5474-5484 CrossRef PubMed (Pubitemid 41653062)
19. Mérot, Y., Ferrière, F., Gailhouste, L., Huet, G., Percevault, F., Saligaut, C. and Flouriot, G. (2009) Different outcomes of unliganded and liganded estrogen receptor-α on neurite outgrowth in PC12 cells. Endocrinology 150, 200-211 CrossRef PubMed
20. Haukenes, G., Szilvay, A. M., Brokstad, K. A., Kanestrøm, A. and Kalland, K. H. (1997) Labeling of RNA transcripts of eukaryotic cells in culture with BrUTP using a liposome transfection reagent (DOTAP). BioTechniques 22, 308-312 PubMed (Pubitemid 27084275)
21. Shogren-Knaak, M., Ishii, H., Sun, J.-M., Pazin, M. J., Davie, J. R. and Peterson, C. L. (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311, 844-847 CrossRef PubMed (Pubitemid 43228847)
22. Latham, J. A. and Dent, S. Y. R. (2007) Cross-regulation of histone modifications. Nat. Struct. Mol. Biol. 14, 1017-1024 CrossRef PubMed (Pubitemid 350060331)
23. Canzio, D., Chang, E. Y., Shankar, S., Kuchenbecker, K. M., Simon, M. D., Madhani, H. D., Narlikar, G. J. and Al-Sady, B. (2011) Chromodomain-mediated oligomerization of HP1 suggests a nucleosome-bridging mechanism for heterochromatin assembly. Mol. Cell 41, 67-81 CrossRef PubMed
24. Herz, H.-M., Nakanishi, S. and Shilatifard, A. (2009) The curious case of bivalent marks. Dev. Cell 17, 301-303 CrossRef PubMed
25. Posern, G., Sotiropoulos, A. and Treisman, R. (2002) Mutant actins demonstrate a role for unpolymerized actin in control of transcription by serum response factor. Mol. Biol. Cell 13, 4167-4178 CrossRef PubMed (Pubitemid 35471176)
26. Mammoto, A. and Ingber, D. E. (2009) Cytoskeletal control of growth and cell fate switching. Curr. Opin. Cell Biol. 21, 864-870 CrossRef PubMed
27. Miano, J. M., Long, X. and Fujiwara, K. (2007) Serum response factor: master regulator of the actin cytoskeleton and contractile apparatus. Am. J. Physiol. Cell. Physiol. 292, C70-C81 CrossRef PubMed (Pubitemid 46115122)
28. Mokalled, M. H., Johnson, A., Kim, Y., Oh, J. and Olson, E. N. (2010) Myocardin-related transcription factors regulate the Cdk5/Pctaire1 kinase cascade to control neurite outgrowth, neuronal migration and brain development. Development 137, 2365-2374 CrossRef PubMed
29. Medjkane, S., Perez-Sanchez, C., Gaggioli, C., Sahai, E. and Treisman, R. (2009) Myocardin-related transcription factors and SRF are required for cytoskeletal dynamics and experimental metastasis. Nat. Cell Biol. 11, 257-268 CrossRef PubMed
30. Grandori, C. and Eisenman, R. N. (1997) Myc target genes. Trends Biochem. Sci. 22, 177-181 CrossRef PubMed (Pubitemid 27199319)
31. Kenneth, N. S. and White, R. J. (2009) Regulation by c-Myc of ncRNA expression. Curr. Opin. Genet. Dev. 19, 38-43 CrossRef PubMed
32. Knoepfler, P. S., Zhang, X., Cheng, P. F., Gafken, P. R., McMahon, S. B. and Eisenman, R. N. (2006) Myc influences global chromatin structure. EMBO J. 25, 2723-2734 CrossRef PubMed (Pubitemid 43980380)
33. Laurenti, E., Wilson, A. and Trumpp, A. (2009) Myc's other life: stem cells and beyond. Curr. Opin. Cell Biol. 21, 844-854 CrossRef PubMed
34. McDonald, O. G., Wu, H., Timp, W., Doi, A. and Feinberg, A. P. (2011) Genome-scale epigenetic reprogramming during epithelial-to-mesenchymal transition. Nat. Struct. Mol. Biol. 18, 867-874 CrossRef PubMed
35. Kalluri, R. and Weinberg, R. A. (2009) The basics of epithelial- mesenchymal transition. J. Clin. Invest. 119, 1420-1428 CrossRef PubMed
36. Mathias, R. A. and Simpson, R. J. (2009) Towards understanding epithelial-mesenchymal transition: a proteomics perspective. Biochim. Biophys. Acta 1794, 1325-1331 CrossRef PubMed
37. Cano, A., Pérez-Moreno, M. A., Rodrigo, I., Locascio, A., Blanco, M. J., del Barrio, M. G., Portillo, F. and Nieto, M. A. (2000) The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2, 76-83 CrossRef PubMed
38. Vesuna, F., Lisok, A., Kimble, B., Domek, J., Kato, Y., van der Groep, P., Artemov, D., Kowalski, J., Carraway, H., van Diest, P. et al. (2011) Twist contributes to hormone resistance in breast cancer by downregulating estrogen receptor-α. Oncogene 31, 3223-3334 CrossRef PubMed
39. Muehlich, S., Wang, R., Lee, S.-M., Lewis, T. C., Dai, C. and Prywes, R. (2008) Serum-induced phosphorylation of the serum response factor coactivator MKL1 by the extracellular signal-regulated kinase 1/2 pathway inhibits its nuclear localization. Mol. Cell. Biol. 28, 6302-6313 CrossRef PubMed
40. McLean, C. Y., Bristor, D., Hiller, M., Clarke, S. L., Schaar, B. T., Lowe, C. B., Wenger, A. M. and Bejerano, G. (2010) GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28, 495-501 CrossRef PubMed
41. Razin, S. V., Gavrilov, A. A., Pichugin, A., Lipinski, M., Iarovaia, O. V. and Vassetzky, Y. S. (2011) Transcription factories in the context of the nuclear and genome organization. Nucleic Acids Res. 39, 9085-9092 CrossRef PubMed
42. Aravind, L. and Koonin, E. V. (2000) SAP: a putative DNA-binding motif involved in chromosomal organization. Trends Biochem. Sci. 25, 112-114 CrossRef PubMed (Pubitemid 30122420)
43. 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 CrossRef PubMed
44. Descot, A., Hoffmann, R., Shaposhnikov, D., Reschke, M., Ullrich, A. and Posern, G. (2009) Negative regulation of the EGFR-MAPK cascade by actin-MAL-mediated Mig6/Errfi-1 induction. Mol. Cell 35, 291-304