Myocardin-related transcription factors: Critical coactivators regulating cardiovascular development and adaptation

Circulation Research

Volumn 100, Issue 5, 2007, Pages 633-644

  Parmacek, Michael S ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b 9123 Founders Pavilion ^*  (United States)

Author keywords

Cardiovascular development; Congenital heart disease; Myocardin; Myocardin related transcription factor; Serum response factor; Smooth muscle cell; Transcription

Indexed keywords

ACTIN; LEUCINE ZIPPER PROTEIN; MADS DOMAIN PROTEIN; MYOCARDIN; MYOCARDIN RELATED TRANSCRIPTION FACTOR A; MYOCARDIN RELATED TRANSCRIPTION FACTOR B; RHO FACTOR; SERUM RESPONSE FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; MKL1 PROTEIN, MOUSE; MYOCARDIN RELATED TRANSCRIPTION FACTOR B, MOUSE; MYOCARDIN-RELATED TRANSCRIPTION FACTOR B, MOUSE; NUCLEAR PROTEIN; TRANSACTIVATOR PROTEIN;

ADAPTATION; AMINO ACID SEQUENCE; CARDIOVASCULAR ADAPTATION; CELL DIFFERENTIATION; CELL FUNCTION; CELL NUCLEUS; CHROMATIN; CONGENITAL HEART DISEASE; CYTOSKELETON; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; GENE STRUCTURE; HEART DEVELOPMENT; HUMAN; HYPERTROPHIC CARDIOMYOPATHY; MOLECULAR BIOLOGY; MUSCLE DEVELOPMENT; MYOEPITHELIUM CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; TISSUE DIFFERENTIATION; TRANSCRIPTION INITIATION; VASCULAR DISEASE; VASCULAR SMOOTH MUSCLE; ANIMAL; CARDIOVASCULAR SYSTEM; CONGENITAL HEART MALFORMATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CARDIOVASCULAR SYSTEM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART DEFECTS, CONGENITAL; HUMANS; MICE; NUCLEAR PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

EID: 33947727502     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000259563.61091.e8     Document Type: Review

References (100)

1. Spiegelman BM, Heinrich R. Biological control through regulated transcriptional coactivators. Cell. 2004;119:157-167.
2. Olson EN. A genetic blueprint for growth and development of the heart. Harvey Lect. 2002;98:41-64.
3. Wang D, Chang PS, Wang Z, Sutherland L, Richardson JA, Small E, Krieg PA, Olson EN. Activation of cardiac gene expression by myocardin, a transcriptional cofactor for serum response factor. Cell. 2001;105:851-862.
4. Wang DZ, Li S, Hockemeyer D, Sutherland L, Wang Z, Schratt G, Richardson JA, Nordheim A, Olson EN. Potentiation of serum response factor activity by a family of myocardin-related transcription factors. Proc Natl Acad Sci U S A. 2002;99:14855-14860.
5. Pipes GC, Creemers EE, Olson EN. The myocardin family of transcriptional coactivators: versatile regulators of cell growth, migration, and myogenesis. Genes Dev. 2006;20:1545-1556.
6. Mack CP, Hinson JS. Regulation of smooth muscle differentiation by the myocardin family of serum response factor cofactors. J Thromb Haemost. 2005;3:1976-1984.
7. Wang DZ, Olson EN. Control of smooth muscle development by the myocardin family of transcriptional coactivators. Curr Opin Genet Dev. 2004;14:558-566.
8. Miano JM. Serum response factor: toggling between disparate programs of gene expression. J Mol Cell Cardiol. 2003;35:577-593.
9. Posern G, Treisman R. Actin' together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol. 2006;16:588-596.
10. Minty A, Kedes L. Upstream regions of the human cardiac actin gene that modulate its transcription in muscle cells: presence of an evolutionarily conserved repeated motif. Mol Cell Biol. 1986;6:2125-2136.
11. Miwa T, Boxer LM, Kedes L. CArG boxes in the human cardiac alpha-actin gene are core binding sites for positive trans-acting regulatory factors. Proc Natl Acad Sci U S A. 1987;84:6702-6706.
12. Miwa T, Kedes L. Duplicated CArG box domains have positive and mutually dependent regulatory roles in expression of the human alpha-cardiac actin gene. Mol Cell Biol. 1987;7:2803-2813.
13. Norman C, Runswick M, Pollock R, Treisman R. Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element. Cell. 1988;55:989-1003.
14. Treisman R. DNA-binding proteins. Inside the MADS box. Nature. 1995;376:468-469.
15. Solway J, Seltzer J, Samaha FF, Kim S, Alger LE, Niu Q, Morrisey EE, Ip HS, Parmacek MS. Structure and expression of a smooth muscle cell-specific gene, SM22 alpha. J Biol Chem. 1995;270:13460-13469.
16. Li L, Liu Z, Mercer B, Overbeek P, Olson EN. Evidence for serum response factor-mediated regulatory networks governing SM22alpha transcription in smooth, skeletal, and cardiac muscle cells. Dev Biol. 1997;187:311-321.
17. Kim S, Ip HS, Lu MM, Clendenin C, Parmacek MS. A serum response factor-dependent transcriptional regulatory program identifies distinct smooth muscle cell sublineages. Mol Cell Biol. 1997;17:2266-2278.
18. Blank RS, McQuinn TC, Yin KC, Thompson MM, Takeyasu K, Schwartz RJ, Owens GK. Elements of the smooth muscle alpha-actin promoter required in cis for transcriptional activation in smooth muscle. Evidence for cell type-specific regulation. J Biol Chem. 1992;267:984-989.
19. Chow KL, Schwartz RJ. A combination of closely associated positive and negative cis-acting promoter elements regulates transcription of the skeletal alpha-actin gene. Mol Cell Biol. 1990;10:528-538.
20. Sun Q, Chen G, Streb JW, Long X, Yang Y, Stoeckert CJ Jr, Miano JM. Defining the mammalian CArGome. Genome Res. 2006;16:197-207.
21. Selvaraj A, Prywes R. Expression profiling of serum inducible genes identifies a subset of SRF target genes that are MKL dependent. BMC Mol Biol. 2004;5:13.
22. Philippar U, Schratt G, Dieterich C, Muller JM, Galgoczy P, Engel FB, Keating MT, Gertler F, Schule R, Vingron M, Nordheim A. The SRF target gene Fhl2 antagonizes RhoA/MAL-dependent activation of SRF. Mol Cell. 2004;16:867-880.
23. Tullai JW, Schaffer ME, Mullenbrock S, Kasif S, Cooper GM. Identification of transcription factor binding sites upstream of human genes regulated by the phosphatidylinositol 3-kinase and MEK/ERK signaling pathways. J Biol Chem. 2004;279:20167-20177.
24. Zhang SX, Garcia-Gras E, Wycuff DR, Marriot SJ, Kadeer N, Yu W, Olson EN, Garry DJ, Parmacek MS, Schwartz RJ. Identification of direct serum-response factor gene targets during Me2SO-induced P19 cardiac cell differentiation. J Biol Chem. 2005;280:19115-19126.
25. Parmacek MS. Transcriptional programs regulating vascular smooth muscle cell development and differentiation. Curr Top Dev Biol. 2001;51:69-89.
26. Olson EN, Schneider MD. Sizing up the heart: development redux in disease. Genes Dev. 2003;17:1937-1956.
27. Schratt G, Philippar U, Berger J, Schwarz H, Heidenreich O, Nordheim A. Serum response factor is crucial for actin cytoskeletal organization and focal adhesion assembly in embryonic stem cells. J Cell Biol. 2002;156:737-750.
28. Weinhold B, Schratt G, Arsenian S, Berger J, Kamino K, Schwarz H, Ruther U, Nordheim A. Srf(-/-) ES cells display non-cell-autonomous impairment in mesodermal differentiation. EMBO J. 2000;19:5835-5844.
29. Niu Z, Yu W, Zhang SX, Barron M, Belaguli NS, Schneider MD, Parmacek M, Nordheim A, Schwartz RJ. Conditional mutagenesis of the murine serum response factor gene blocks cardiogenesis and the transcription of downstream gene targets. J Biol Chem. 2005;280:32531-32538.
30. Arsenian S, Weinhold B, Oelgeschlager M, Ruther U, Nordheim A. Serum response factor is essential for mesoderm formation during mouse embryogenesis. EMBO J. 1998;17:6289-6299.
31. Parlakian A, Tuil D, Hamard G, Tavernier G, Hentzen D, Concordet JP, Paulin D, Li Z, Daegelen D. Targeted inactivation of serum response factor in the developing heart results in myocardial defects and embryonic lethality. Mol Cell Biol. 2004;24:5281-5289.
32. Miano JM, Ramanan N, Georger MA, de Mesy Bentley KL, Emerson RL, Balza RO Jr, Xiao Q, Weiler H, Ginty DD, Misra RP. Restricted inactivation of serum response factor to the cardiovascular system. Proc Natl Acad Sci U S A. 2004;101:17132-17137.
33. Balza RO Jr, Misra RP. Role of the serum response factor in regulating contractile apparatus gene expression and sarcomeric integrity in cardiomyocytes. J Biol Chem. 2006;281:6498-6510.
34. Parlakian A, Charvet C, Escoubet B, Mericskay M, Molkentin JD, Gary-Bobo G, De Windt LJ, Ludosky MA, Paulin D, Daegelen D, Tuil D, Li Z. Temporally controlled onset of dilated cardiomyopathy through disruption of the SRF gene in adult heart. Circ. 2005;112:2930-2939.
35. Lepore JJ, Cheng L, Min Lu M, Mericko PA, Morrisey EE, Parmacek MS. High-efficiency somatic mutagenesis in smooth muscle cells and cardiac myocytes in SM22alpha-Cre transgenic mice. Genesis. 2005;41:179-184.
36. Parmacek MS. Myocardin-not quite MyoD. Arterioscler Thromb Vasc Biol. 2004;24:1535-1537.
37. Du KL, Ip HS, Li J, Chen M, Dandre F, Yu W, Lu MM, Owens GK, Parmacek MS. Myocardin is a critical serum response factor cofactor in the transcriptional program regulating smooth muscle cell differentiation. Mol Cell Biol. 2003;23:2425-2437.
38. Creemers EE, Sutherland LB, Oh J, Barbosa AC, Olson EN. Coactivation of MEF2 by the SAP domain proteins myocardin and MASTR. Mol Cell. 2006;23:83-96.
39. Miralles F, Posern G, Zaromytidou AI, Treisman R. Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell. 2003;113:329-342.
40. Du KL, Chen M, Li J, Lepore JJ, Mericko P, Parmacek MS. Megakaryoblastic leukemia factor-1 transduces cytoskeletal signals and induces smooth muscle cell differentiation from undifferentiated embryonic stem cells. J Biol Chem. 2004;279:17578-17586.
41. Zaromytidou AI, Miralles F, Treisman R. MAL and ternary complex factor use different mechanisms to contact a common surface on the serum response factor DNA-binding domain. Mol Cell Biol. 2006;26:4134-4148.
42. Aravind L, Koonin EV. SAP-a putative DNA-binding motif involved in chromosomal organization. Trends Biochem Sci. 2000;25:112-114.
43. Han Z, Li X, Wu J, Olson EN. A myocardin-related transcription factor regulates activity of serum response factor in Drosophila. Proc Natl Acad Sci U S A. 2004;101:12567-12572.
44. Somogyi K, Rorth P. Evidence for tension-based regulation of Drosophila MAL and SRF during invasive cell migration. Dev Cell. 2004;7:85-93.
45. Ma Z, Morris SW, Valentine V, Li M, Herbrick JA, Cui X, Bouman D, Li Y, Mehta PK, Nizetic D, Kaneko Y, Chan GC, Chan LC, Squire J, Scherer SW, Hitzler JK. Fusion of two novel genes, RBM15 and MKL1, in the t(1;22)(p13;q13) of acute megakaryoblastic leukemia. Nat Genet. 2001;28:220-221.
46. Mercher T, Coniat MB, Monni R, Mauchauffe M, Khac FN, Gressin L, Mugneret F, Leblanc T, Dastugue N, Berger R, Bernard OA. Involvement of a human gene related to the Drosophila spen gene in the recurrent t(1;22) translocation of acute megakaryocytic leukemia. Proc Natl Acad Sci U S A. 2001;98:5776-5779.
47. Sasazuki T, Sawada T, Sakon S, Kitamura T, Kishi T, Okazaki T, Katano M, Tanaka M, Watanabe M, Yagita H, Okumura K, Nakano H. Identification of a novel transcriptional activator, BSAC, by a functional cloning to inhibit tumor necrosis factor-induced cell death. J Biol Chem. 2002;277:28853-28860.
48. Li J, Zhu X, Chen M, Cheng L, Zhou D, Lu MM, Du K, Epstein JA, Parmacek MS. Myocardin-related transcription factor B is required in cardiac neural crest for smooth muscle differentiation and cardiovascular development. Proc Natl Acad Sci U S A. 2005;102:8916-8921.
49. Sotiropoulos A, Gineitis D, Copeland J, Treisman R. Signal-regulated activation of serum response factor is mediated by changes in actin dynamics. Cell. 1999;98:159-169.
50. Cen B, Selvaraj A, Burgess RC, Hitzler JK, Ma Z, Morris SW, Prywes R. Megakaryoblastic leukemia 1, a potent transcriptional coactivator for serum response factor (SRF), is required for serum induction of SRF target genes. Mol Cell Biol. 2003;23:6597-6608.
51. Hill CS, Treisman R. Transcriptional regulation by extracellular signals: mechanisms and specificity. Cell. 1995;80:199-211.
52. Copeland JW, Treisman R. The diaphanous-related formin mDia1 controls serum response factor activity through its effects on actin polymerization. Mol Biol Cell. 2002;13:4088-4099.
53. Posern G, Miralles F, Guettler S, Treisman R. Mutant actins that stabilise F-actin use distinct mechanisms to activate the SRF coactivator MAL. EMBO J. 2004;23:3973-3983.
54. Kuwahara K, Barrientos T, Pipes GC, Li S, Olson EN. Muscle-specific signaling mechanism that links actin dynamics to serum response factor. Mol Cell Biol. 2005;25:3173-3181.
55. Zhou J, Herring BP. Mechanisms responsible for the promoter-specific effects of myocardin. J Biol Chem. 2005;280:10861-10869.
56. Lilly B, Olson EN, Beckerle MC. Identification of a CArG box-dependent enhancer within the cysteine-rich protein 1 gene that directs expression in arterial but not venous or visceral smooth muscle cells. Dev Biol. 2001;240:531-547.
57. Wang Z, Wang DZ, Hockemeyer D, McAnally J, Nordheim A, Olson EN. Myocardin and ternary complex factors compete for SRF to control smooth muscle gene expression. Nature. 2004;428:185-189.
58. Small EM, Warkman AS, Wang DZ, Sutherland LB, Olson EN, Krieg PA. Myocardin is sufficient and necessary for cardiac gene expression in Xenopus. Development. 2005;132:987-997.
59. Wang Z, Wang DZ, Pipes GC, Olson EN. Myocardin is a master regulator of smooth muscle gene expression. Proc Natl Acad Sci U S A. 2003;100:7129-7134.
60. Pipes GC, Sinha S, Qi X, Zhu CH, Gallardo TD, Shelton J, Creemers EE, Sutherland L, Richardson JA, Garry DJ, Wright WE, Owens GK, Olson EN. Stem cells and their derivatives can bypass the requirement of myocardin for smooth muscle gene expression. Dev Biol. 2005;288:502-513.
61. Li S, Wang DZ, Wang Z, Richardson JA, Olson EN. The serum response factor coactivator myocardin is required for vascular smooth muscle development. Proc Natl Acad Sci U S A. 2003;100:9366-9370.
62. Xing W, Zhang TC, Cao D, Wang Z, Antos CL, Li S, Wang Y, Olson EN, Wang DZ. Myocardin induces cardiomyocyte hypertrophy. Circ Res. 2006;98:1089-1097.
63. Badorff C, Seeger FH, Zeiher AM, Dimmeler S. Glycogen synthase kinase 3beta inhibits myocardin-dependent transcription and hypertrophy induction through site-specific phosphorylation. Circ Res. 2005;97:645-654.
64. Antos CL, McKinsey TA, Frey N, Kutschke W, McAnally J, Shelton JM, Richardson JA, Hill JA, Olson EN. Activated glycogen synthase-3 beta suppresses cardiac hypertrophy in vivo. Proc Natl Acad Sci U S A. 2002;99:907-912.
65. Haq S, Choukroun G, Kang ZB, Ranu H, Matsui T, Rosenzweig A, Molkentin JD, Alessandrini A, Woodgett J, Hajjar R, Michael A, Force T. Glycogen synthase kinase-3beta is a negative regulator of cardiomyocyte hypertrophy. J Cell Biol. 2000;151:117-130.
66. Torrado M, Lopez E, Centeno A, Medrano C, Castro-Beiras A, Mikhailov AT. Myocardin mRNA is augmented in the failing myocardium: expression profiling in the porcine model and human dilated cardiomyopathy. J Mol Med. 2003;81:566-577.
67. Yoshida T, Sinha S, Dandre F, Wamhoff BR, Hoofnagle MH, Kremer BE, Wang DZ, Olson EN, Owens GK. Myocardin is a key regulator of CArG-dependent transcription of multiple smooth muscle marker genes. Circ Res. 2003;92:856-864.
68. Chen J, Kitchen CM, Streb JW, Miano JM. Myocardin: a component of a molecular switch for smooth muscle differentiation. J Mol Cell Cardiol. 2002;34:1345-1356.
69. Yin F, Hoggatt AM, Zhou J, Herring BP. 130-kDa smooth muscle myosin light chain kinase is transcribed from a CArG-dependent, internal promoter within the mouse mylk gene. Am J Physiol. 2006;290:C1599-C1609.
70. Rensen SS, Niessen PM, Long X, Doevendans PA, Miano JM, van Eys GJ. Contribution of serum response factor and myocardin to transcriptional regulation of smoothelins. Cardiovasc Res. 2006;70:136-145.
71. Yoshida T, Kawai-Kowase K, Owens GK. Forced expression of myocardin is not sufficient for induction of smooth muscle differentiation in multipotential embryonic cells. Arterioscler Thromb Vasc Biol. 2004;24:1596-1601.
72. Mack CP, Somlyo AV, Hautmann M, Somlyo AP, Owens GK. Smooth muscle differentiation marker gene expression is regulated by RhoA-mediated actin polymerization. J Biol Chem. 2001;276:341-347.
73. Hayashi K, Saga H, Chimori Y, Kimura K, Yamanaka Y, Sobue K. Differentiated phenotype of smooth muscle cells depends on signaling pathways through insulin-like growth factors and phosphatidylinositol 3-kinase. J Biol Chem. 1998;273:28860-28867.
74. Liu ZP, Wang Z, Yanagisawa H, Olson EN. Phenotypic modulation of smooth muscle cells through interaction of Foxo4 and myocardin. Dev Cell. 2005;9:261-270.
75. Manabe I, Owens GK. Recruitment of serum response factor and hyperacetylation of histones at smooth muscle-specific regulatory regions during differentiation of a novel P19-derived in vitro smooth muscle differentiation system. Circ Res. 2001;88:1127-1134.
76. Qiu P, Li L. Histone acetylation and recruitment of serum responsive factor and CREB-binding protein onto SM22 promoter during SM22 gene expression. Circ Res. 2002;90:858-865.
77. Qiu P, Ritchie RP, Gong XQ, Hamamori Y, Li L. Dynamic changes in chromatin acetylation and the expression of histone acetyltransferases and histone deacetylases regulate the SM22alpha transcription in response to Smad3-mediated TGFbeta1 signaling. Biochem Biophys Res Commun. 2006;348:351-358.
78. Cao D, Wang Z, Zhang CL, Oh J, Xing W, Li S, Richardson JA, Wang DZ, Olson EN. Modulation of smooth muscle gene expression by association of histone acetyltransferases and deacetylases with myocardin. Mol Cell Biol. 2005;25:364-376.
79. McDonald OG, Wamhoff BR, Hoofnagle MH, Owens GK. Control of SRF binding to CArG box chromatin regulates smooth muscle gene expression in vivo. J Clin Invest. 2006;116:36-48.
80. Davis CA, Haberland M, Arnold MA, Sutherland LB, McDonald OG, Richardson JA, Childs G, Harris S, Owens GK, Olson EN. PRISM/PRDM6, a transcriptional repressor that promotes the proliferative gene program in smooth muscle cells. Mol Cell Biol. 2006;26:2626-2636.
81. Owens GK. Molecular control of vascular smooth muscle cell differentiation. Acta Physiol Scand. 1998;164:623-635.
82. Campbell GR, Campbell JH. Smooth muscle phenotypic changes in arterial wall hemostasis: implications for the pathogenesis of atherosclerosis. Exp Mol Pathol. 1985;42:139-162.
83. Campbell GR, Campbell JH, Manderson JA, Horrigan S, Rennick RE. Arterial smooth muscle: a mutifunctional mesenchymal cell. Arch Pathol Lab Med. 1988;112:977-986.
84. Gineitis D, Treisman R. Differential usage of signal transduction pathways defines two types of serum response factor target gene. J Biol Chem. 2001;276:24531-24539.
85. Zhou J, Hu G, Herring BP. Smooth muscle-specific genes are differentially sensitive to inhibition by Elk-1. Mol Cell Biol. 2005;25:9874-9885.
86. Treisman R. Ternary complex factors: growth factor regulated transcriptional activators. Curr Opin Genet Dev. 1994;4:96-101.
87. Shore P, Whitmarsh AJ, Bhaskaran R, Davis RJ, Waltho JP, Sharrocks AD. Determinants of DNA-binding specificity of ETS-domain transcription factors. Mol Cell Biol. 1996;16:3338-3349.
88. Shawber CJ, Kitajewski J. Notch function in the vasculature: insights from zebrafish, mouse and man. Bioessays. 2004;26:225-234.
89. Proweller A, Pear WS, Parmacek MS. Notch signaling represses myocardin-induced smooth muscle cell differentiation. J Biol Chem. 2005;280:8994-9004.
90. Doi H, Iso T, Yamazaki M, Akiyama H, Kanai H, Sato H, Kawai-Kowase K, Tanaka T, Maeno T, Okamoto E, Arai M, Kedes L, Kurabayashi M. HERP1 inhibits myocardin-induced vascular smooth muscle cell differentiation by interfering with SRF binding to CArG box. Arterioscler Thromb Vasc Biol. 2005;25:2328-2334.
91. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev. 2004;84:767-801.
92. Liu Y, Sinha S, McDonald OG, Shang Y, Hoofnagle MH, Owens GK. Kruppel-like factor 4 abrogates myocardin-induced activation of smooth muscle gene expression. J Biol Chem. 2005;280:9719-9727.
93. Wamhoff BR, Hoofnagle MH, Burns A, Sinha S, McDonald OG, Owens GK. A G/C element mediates repression of the SM22alpha promoter within phenotypically modulated smooth muscle cells in experimental atherosclerosis. Circ Res. 2004;95:981-988.
94. Sun Y, Boyd K, Xu W, Ma J, Jackson CW, Fu A, Shillingford JM, Robinson GW, Hennighausen L, Hitzler JK, Ma Z, Morris SW. Acute myeloid leukemia-associated Mkl1 (Mrtf-a) is a key regulator of mammary gland function. Mol Cell Biol. 2006;26:5809-5826.
95. Li S, Chang S, Qi X, Richardson JA, Olson EN. Requirement of a myocardin-related transcription factor for development of mammary myoepithelial cells. Mol Cell Biol. 2006;26:5797-5808.
96. Oh J, Richardson JA, Olson EN. Requirement of myocardin-related transcription factor-B for remodeling of branchial arch arteries and smooth muscle differentiation. Proc Natl Acad Sci U S A. 2005;102:15122-15127.
97. Cen B, Selvaraj A, Prywes R. Myocardin/MKL family of SRF coactivators: key regulators of immediate early and muscle specific gene expression. J Cell Biochem. 2004;93:74-82.
98. Kirby ML, Gale TF, Stewart DE. Neural crest cells contribute to normal aorticopulmonary septation. Science. 1983;220:1059-1061.
99. Creazzo TL, Godt RE, Leatherbury L, Conway SJ, Kirby ML. Role of cardiac neural crest cells in cardiovascular development. Annu Rev Physiol. 1998;60:267-286.
100. Olson EN, Klein WH. bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out. Genes Dev. 1994;8:1-8.