Myocardin-related transcription factors control the motility of epicardium-derived cells and the maturation of coronary vessels

Development (Cambridge)

Volumn 142, Issue 1, 2015, Pages 21-30

  Trembley, Michael A ^a   Velasquez, Lissette S ^a   de Mesy Bentley, Karen L ^a   Small, Eric M ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Epicardium; Heart; Migration; Pericyte; Progenitor; Transcription

Indexed keywords

MYOCARDIN; MYOCARDIN RELATED TRANSCRIPTION FACTOR A; MYOCARDIN RELATED TRANSCRIPTION FACTOR B; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; MKL1 PROTEIN, MOUSE; MYOCARDIN-RELATED TRANSCRIPTION FACTOR B, MOUSE; SERUM RESPONSE FACTOR; TRANSACTIVATOR PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CONTACT; CELL LINEAGE; CELL MATURATION; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; CORONARY BLOOD VESSEL; EMBRYO; EPICARDIUM; EPICARDIUM DERIVED PROGENITOR CELL; EPITHELIAL MESENCHYMAL TRANSITION; GENE; GENE ACTIVATION; GENE EXPRESSION; MOUSE; MRTFA GENE; MRTFB GENE; NONHUMAN; PERICYTE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STEM CELL; STEM CELL MOBILIZATION; TRANSCRIPTION REGULATION; ANGIOGENESIS; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CELL MOTION; CELL NUCLEUS; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; CYTOLOGY; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; MAMMALIAN EMBRYO; METABOLISM; PATHOLOGY; PERICARDIUM; ULTRASTRUCTURE;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; CORONARY VESSELS; COS CELLS; EMBRYO, MAMMALIAN; MICE, INBRED C57BL; NEOVASCULARIZATION, PHYSIOLOGIC; PERICARDIUM; PERICYTES; SERUM RESPONSE FACTOR; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84918515802     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.116418     Document Type: Article

References (59)

1. Aguilera, K. Y. and Brekken, R. A. (2014). Recruitment and retention: factors that affect pericyte migration. Cell. Mol. Life Sci. 71, 299-309.
2. Armulik, A., Genové, G. and Betsholtz, C. (2011). Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell 21, 193-215.
3. Austin, A. F., Compton, L. A., Love, J. D., Brown, C. B. and Barnett, J. V. (2008). Primary and immortalized mouse epicardial cells undergo differentiation in response to TGFbeta. Dev. Dyn. 237, 366-376.
4. Braitsch, C. M., Kanisicak, O., van Berlo, J. H., Molkentin, J. D. and Yutzey, K. E. (2013). Differential expression of embryonic epicardial progenitor markers and localization of cardiac fibrosis in adult ischemic injury and hypertensive heart disease. J. Mol. Cell. Cardiol. 65, 108-119.
5. Busche, S., Kremmer, E. and Posern, G. (2010). E-cadherin regulates MAL-SRFmediated transcription in epithelial cells. J. Cell Sci. 123, 2803-2809.
6. Cai, C.-L., Martin, J. C., Sun, Y., Cui, L., Wang, L., Ouyang, K., Yang, L., Bu, L., Liang, X., Zhang, X. et al. (2008). A myocardial lineage derives from Tbx18 epicardial cells. Nature 454, 104-108.
7. Casanova, J. C., Travisano, S. and de la Pompa, J. L. (2013). Epithelial-tomesenchymal transition in epicardium is independent of Snail1. Genesis 51, 32-40.
8. Chintalgattu, V., Rees, M. L., Culver, J. C., Goel, A., Jiffar, T., Zhang, J., Dunner, K., Jr, Pati, S., Bankson, J. A., Pasqualini, R. et al. (2013). Coronary microvascular pericytes are the cellular target of sunitinib malate-induced cardiotoxicity. Sci. Transl. Med. 5, 187ra169.
9. Dettman, R.W., Denetclaw, W. Jr, Ordahl, C. P. and Bristow, J. (1998). Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts, and intermyocardial fibroblasts in the avian heart. Dev. Biol. 193, 169-181.
10. Eralp, I., Lie-Venema, H., DeRuiter, M. C., van den Akker, N. M. S., Bogers, A. J. J. C., Mentink, M. M. T., Poelmann, R. E. and Gittenberger-de Groot, A. C. (2005). Coronary artery and orifice development is associated with proper timing of epicardial outgrowth and correlated Fas ligand associated apoptosis patterns. Circ. Res. 96, 526-534.
11. Evelyn, C. R., Wade, S. M., Wang, Q., Wu, M., Iniguez-Lluhi, J. A., Merajver, S. D. and Neubig, R. R. (2007). CCG-1423: a small-molecule inhibitor of RhoA transcriptional signaling. Mol. Cancer Ther. 6, 2249-2260.
12. Fan, L., Sebe, A., Peterfi, Z., Masszi, A., Thirone, A. C. P., Rotstein, O. D., Nakano, H., McCulloch, C. A., Szaszi, K., Mucsi, I. et al. (2007). Cell contactdependent regulation of epithelial-myofibroblast transition via the rho-rho kinasephospho-myosin pathway. Mol. Biol. Cell 18, 1083-1097.
13. Gittenberger-de Groot, A. C., Vrancken Peeters, M.-P. F. M., Bergwerff, M., Mentink, M. M. T. and Poelmann, R. E. (2000). Epicardial outgrowth inhibition leads to compensatory mesothelial outflow tract collar and abnormal cardiac septation and coronary formation. Circ. Res. 87, 969-971.
14. Guettler, S., Vartiainen, M. K., Miralles, F., Larijani, B. and Treisman, R. (2008). RPEL motifs link the serum response factor cofactor MAL but not myocardin to Rho signaling via actin binding. Mol. Cell. Biol. 28, 732-742.
15. Haak, A. J., Tsou, P.-S., Amin, M. A., Ruth, J. H., Campbell, P., Fox, D. A., Khanna, D., Larsen, S. D. and Neubig, R. R. (2014). Targeting the myofibroblast genetic switch: inhibitors of myocardin-related transcription factor/serum response factor-regulated gene transcription prevent fibrosis in a murine model of skin injury. J. Pharmacol. Exp. Ther. 349, 480-486.
16. Hinkel, R., Trenkwalder, T., Petersen, B., Husada, W., Gesenhues, F., Lee, S., Hannappel, E., Bock-Marquette, I., Theisen, D., Leitner, L. et al. (2014). MRTF-A controls vessel growth and maturation by increasing the expression of CCN1 and CCN2. Nat. Commun. 5, 3970.
17. Katz, T. C., Singh, M. K., Degenhardt, K., Rivera-Feliciano, J., Johnson, R. L., Epstein, J. A. and Tabin, C. J. (2012). Distinct compartments of the proepicardial organ give rise to coronary vascular endothelial cells. Dev. Cell 22, 639-650.
18. Kim, J., Wu, Q., Zhang, Y., Wiens, K. M., Huang, Y., Rubin, N., Shimada, H., Handin, R. I., Chao, M. Y., Tuan, T.-L. et al. (2010). PDGF signaling is required for epicardial function and blood vessel formation in regenerating zebrafish hearts. Proc. Natl. Acad. Sci. USA 107, 17206-17210.
19. Lamouille, S., Xu, J. and Derynck, R. (2014). Molecular mechanisms of epithelialmesenchymal transition. Nat. Rev. Mol. Cell Biol. 15, 178-196.
20. Lepilina, A., Coon, A. N., Kikuchi, K., Holdway, J. E., Roberts, R. W., Burns, C. G. and Poss, K. D. (2006). A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 127, 607-619.
21. Li, J., Zhu, X., Chen, M., Cheng, L., Zhou, D., Lu, M. M., Du, K., Epstein, J. A. and Parmacek, M. S. (2005). Myocardin-related transcription factor B is required in cardiac neural crest for smooth muscle differentiation and cardiovascular development. Proc. Natl. Acad. Sci. USA 102, 8916-8921.
22. Li, S., Chang, S., Qi, X., Richardson, J. A. and Olson, E. N. (2006). Requirement of a myocardin-related transcription factor for development of mammary myoepithelial cells. Mol. Cell. Biol. 26, 5797-5808.
23. Li, P., Cavallero, S., Gu, Y., Chen, T. H. P., Hughes, J., Hassan, A. B., Bruning, J. C., Pashmforoush, M. and Sucov, H. M. (2011). IGF signaling directs ventricular cardiomyocyte proliferation during embryonic heart development. Development 138, 1795-1805.
24. Limana, F., Zacheo, A., Mocini, D., Mangoni, A., Borsellino, G., Diamantini, A., De Mori, R., Battistini, L., Vigna, E., Santini, M. et al. (2007). Identification of myocardial and vascular precursor cells in human and mouse epicardium. Circ. Res. 101, 1255-1265.
25. Lu, J., Landerholm, T. E., Wei, J. S., Dong, X.-R., Wu, S.-P., Liu, X., Nagata, K.-i., Inagaki, M. and Majesky, M. W. (2001). Coronary smooth muscle differentiation from proepicardial cells requires rhoA-mediated actin reorganization and p160 rho-kinase activity. Dev. Biol. 240, 404-418.
26. Männer, J., Schlueter, J. and Brand, T. (2005). Experimental analyses of the function of the proepicardium using a new microsurgical procedure to induce lossof-proepicardial-function in chick embryos. Dev. Dyn. 233, 1454-1463.
27. Martínez-Estrada, O. M., Lettice, L. A., Essafi, A., Guadix, J. A., Slight, J., Velecela, V., Hall, E., Reichmann, J., Devenney, P. S., Hohenstein, P. et al. (2010). Wt1 is required for cardiovascular progenitor cell formation through transcriptional control of Snail and E-cadherin. Nat. Genet. 42, 89-93.
28. 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.
29. Mellgren, A. M., Smith, C. L., Olsen, G. S., Eskiocak, B., Zhou, B., Kazi, M. N., Ruiz, F. R., Pu, W. T. and Tallquist, M. D. (2008). Platelet-derived growth factor receptor beta signaling is required for efficient epicardial cell migration and development of two distinct coronary vascular smooth muscle cell populations. Circ. Res. 103, 1393-1401.
30. Merki, E., Zamora, M., Raya, A., Kawakami, Y., Wang, J., Zhang, X., Burch, J., Kubalak, S. W., Kaliman, P., Izpisua Belmonte, J. C. et al. (2005). Epicardial retinoid X receptor alpha is required for myocardial growth and coronary artery formation. Proc. Natl. Acad. Sci. USA 102, 18455-18460.
31. Miano, J. M. (2003). Serum response factor: toggling between disparate programs of gene expression. J. Mol. Cell. Cardiol. 35, 577-593.
32. Miano, J. M., Ramanan, N., Georger, M. A., de Mesy Bentley, K. L., Emerson, R. L., Balza, R. O., Jr, Xiao, Q., Weiler, H., Ginty, D. D. and Misra, R. P. (2004). Restricted inactivation of serum response factor to the cardiovascular system. Proc. Natl. Acad. Sci. USA 101, 17132-17137.
33. Mikawa, T. and Gourdie, R. G. (1996). Pericardial mesoderm generates a population of coronary smooth muscle cells migrating into the heart along with ingrowth of the epicardial organ. Dev. Biol. 174, 221-232.
34. 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.
35. Mokalled, M. H., Johnson, A., Kim, Y., Oh, J. and Olson, E. N. (2010). Myocardinrelated transcription factors regulate the Cdk5/Pctaire1 kinase cascade to control neurite outgrowth, neuronal migration and brain development. Development 137, 2365-2374.
36. Nelson, T. J., Duncan, S. A. and Misra, R. P. (2004). Conserved enhancer in the serum response factor promoter controls expression during early coronary vasculogenesis. Circ. Res. 94, 1059-1066.
37. Oh, J., Richardson, J. A. and Olson, E. N. (2005). Requirement of myocardinrelated transcription factor-B for remodeling of branchial arch arteries and smooth muscle differentiation. Proc. Natl. Acad. Sci. USA 102, 15122-15127.
38. 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.
39. Pennisi, D. J. and Mikawa, T. (2009). FGFR-1 is required by epicardium-derived cells for myocardial invasion and correct coronary vascular lineage differentiation. Dev. Biol. 328, 148-159.
40. Red-Horse, K, Ueno, H., Weissman, I. L. and Krasnow, M. A. (2010). Coronary arteries form by developmental reprogramming of venous cells. Nature 464, 549-553.
41. Rouget, C. (1873). Memoire sur le developpement, la structures et les proprietes des capillaires sanguins et lymphatiques. Archs. Physiol. Norm. Pathol. 5, 603-633.
42. Rudat, C. and Kispert, A. (2012). Wt1 and epicardial fate mapping. Circ. Res. 111, 165-169.
43. 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-beta. Am. J. Physiol. Lung Cell Mol. Physiol. 301, L656-L666.
44. Small, E. M., Thatcher, J. E., Sutherland, L. B., Kinoshita, H., Gerard, R. D., Richardson, J. A., DiMaio, J. M., Sadek, H., Kuwahara, K. and Olson, E. N. (2010). Myocardin-related transcription factor-a controls myofibroblast activation and fibrosis in response to myocardial infarction. Circ. Res. 107, 294-304.
45. Smart, N., Bollini, S., Dubé, K. N., Vieira, J. M., Zhou, B., Davidson, S., Yellon, D., Riegler, J., Price, A. N., Lythgoe, M. F. et al. (2011). De novo cardiomyocytes from within the activated adult heart after injury. Nature 474, 640-644.
46. Tian, X., Hu, T., Zhang, H., He, L., Huang, X., Liu, Q., Yu, W., He, L., Yang, Z., Zhang, Z. et al. (2013). Subepicardial endothelial cells invade the embryonic ventricle wall to form coronary arteries. Cell Res. 23, 1075-1090.
47. Velasquez, L. S., Sutherland, L. B., Liu, Z., Grinnell, F., Kamm, K. E., Schneider, J. W., Olson, E. N. and Small, E. M. (2013). Activation of MRTF-A-dependent gene expression with a small molecule promotes myofibroblast differentiation and wound healing. Proc. Natl. Acad. Sci. USA 110, 16850-16855.
48. von Gise, A., Zhou, B., Honor, L. B., Ma, Q., Petryk, A. and Pu,W. T. (2011). WT1 regulates epicardial epithelial to mesenchymal transition through beta-catenin and retinoic acid signaling pathways. Dev. Biol. 356, 421-431.
49. Wada, A. M., Smith, T. K., Osler, M. E., Reese, D. E. and Bader, D. M. (2003). Epicardial/Mesothelial cell line retains vasculogenic potential of embryonic epicardium. Circ. Res. 92, 525-531.
50. Wang, D.-Z., 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.
51. 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.
52. Wang, Z., Wang, D.-Z., Hockemeyer, D., McAnally, J., Nordheim, A. and Olson, E. N. (2004). Myocardin and ternary complex factors compete for SRF to control smooth muscle gene expression. Nature 428, 185-189.
53. Weinl, C., Riehle, H., Park, D., Stritt, C., Beck, S., Huber, G., Wolburg, H., Olson, E. N., Seeliger, M. W., Adams, R. H. et al. (2013). Endothelial SRF/MRTF ablation causes vascular disease phenotypes in murine retinae. J. Clin. Invest. 123, 2193-2206.
54. Wessels, A., van den Hoff, M. J. B., Adamo, R. F., Phelps, A. L., Lockhart, M. M., Sauls, K., Briggs, L. E., Norris, R. A., vanWijk, B., Perez-Pomares, J. M. et al. (2012). Epicardially derived fibroblasts preferentially contribute to the parietal leaflets of the atrioventricular valves in the murine heart. Dev. Biol. 366, 111-124.
55. Wilm, B., Ipenberg, A., Hastie, N. D., Burch, J. B. E. and Bader, D. M. (2005). The serosal mesothelium is a major source of smooth muscle cells of the gut vasculature. Development 132, 5317-5328.
56. Zhou, B. and Pu, W. T. (2012). Genetic Cre-loxP assessment of epicardial cell fate using Wt1-driven Cre alleles. Circ. Res. 111, e276-e280.
57. Zhou, B., Ma, Q., Rajagopal, S., Wu, S. M., Domian, I., Rivera-Feliciano, J., Jiang, D., von Gise, A., Ikeda, S., Chien, K. R. et al. (2008). Epicardial progenitors contributeto the cardiomyocytelineagein the developing heart.Nature 454, 109-113.
58. Zhou, B., Honor, L. B., He, H., Ma, Q., Oh, J.-H., Butterfield, C., Lin, R.-Z., Melero-Martin, J. M., Dolmatova, E., Duffy, H. S. et al. (2011). Adult mouse epicardium modulates myocardial injury by secreting paracrine factors. J. Clin. Invest. 121, 1894-1904.
59. 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.