Bone morphogenetic protein signaling modulates myocardin transactivation of cardiac genes

Circulation Research

Volumn 97, Issue 10, 2005, Pages 992-1000

  Callis, Thomas E ^a   Cao, Dongsun ^a   Wang, Da Zhi ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Bone morphogenetic protein; Cardiac gene expression; Myocardin; Serum response factor; Smad

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; MYOCARDIN; SERUM RESPONSE FACTOR; SMAD1 PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HEART MUSCLE; HEART MUSCLE CELL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RAT; SERUM RESPONSIVE ELEMENT; SIGNAL TRANSDUCTION; SMOOTH MUSCLE; TRANSACTIVATION;

ANIMALS; ATRIAL NATRIURETIC FACTOR; BINDING SITES; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEINS; CERCOPITHECUS AETHIOPS; COS CELLS; GENE EXPRESSION REGULATION; MYOCARDIUM; MYOCYTES, CARDIAC; NUCLEAR PROTEINS; PROMOTER REGIONS (GENETICS); RESPONSE ELEMENTS; SERUM RESPONSE FACTOR; SIGNAL TRANSDUCTION; SMAD1 PROTEIN; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 27944454815     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000190670.92879.7d     Document Type: Article

References (44)

1. 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.
2. 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.
3. Wang DZ, Olson EN. Control of smooth muscle development by the myocardin family of transcriptional coactivators. Curr Opin Genet Dev. 2004;14:558-566.
4. 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.
5. Ueyama T, Kasahara H, Ishiwata T, Nie Q, Izumo S. Myocardin expression is regulated by Nkx2.5, and its function is required for car diomyogenesis. Mol Cell Biol. 2003;23:9222-9232.
6. 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.
7. 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.
8. 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.
9. Majesky MW. Decisions, decisions. SRF coactivators and smooth muscle myogenesis. Circ Res. 2003;92:824-826.
10. 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.
11. 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.
12. 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.
13. 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.
14. Massague J. TGF-beta signal transduction. Annu Rev Biochem. 1998;67:753-791.
15. Attisano L, Wrana JL. Signal transduction by the TGF-beta superfamily. Science. 2002;296:1646-1647.
16. Monzen K, Nagai R, Komuro I. A role for bone morphogenetic protein signaling in cardiomyocyte differentiation. Trends Cardiovasc Med. 2002;12:263-269.
17. Shi Y, Katsev S, Cai C, Evans S. BMP signaling is required for heart formation in vertebrates. Dev Biol. 2000;224:226-237.
18. Schultheiss TM, Burch JB, Lassar AB. A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev. 1997;11:451-462.
19. Monzen K, Shiojima I, Hiroi Y, Kudoh S, Oka T, Takimoto E, Hayashi D, Hosoda T, Habara-Ohkubo A, Nakaoka T, Fujita T, Yazaki Y, Komuro I. Bone morphogenetic proteins induce cardiomyocyte differentiation through the mitogen-activated protein kinase kinase kinase TAK1 and cardiac transcription factors Csx/Nkx-2.5 and GATA-4. Mol Cell Biol. 1999;19:7096-7105.
20. Monzen K, Hiroi Y, Kudoh S, Akazawa H, Oka T, Takimoto E, Hayashi D, Hosoda T, Kawabata M, Miyazono K, Ishii S, Yazaki Y, Nagai R, Komuro I. Smads, TAK1, and their common target ATF-2 play a critical role in cardiomyocyte differentiation. J Cell Biol. 2001;153:687-698.
21. Ghosh-Choudhury N, Abboud SL, Mahimainathan L, Chandrasekar B, Choudhury GG. Phosphatidylinositol 3-kinase regulates bone morphogenetic protein-2 (BMP-2)-induced myocyte enhancer factor 2A-dependent transcription of BMP-2 gene in cardiomyocyte precursor cells. J Biol Chem. 2003;278:21998-22005.
22. 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.
23. Macias-Silva M, Hoodless PA, Tang SJ, Buchwald M, Wrana JL. Specific activation of Smadl signaling pathways by the BMP7 type I receptor, ALK2. J Biol Chem. 1998;273:25628-25636.
24. Zhu HJ, Iaria J, Sizeland AM. Smad7 differentially regulates transforming growth factor beta-mediated signaling pathways. J Biol Chem. 1999;274:32258-32264.
25. Pouponnot C, Jayaraman L, Massague J. Physical and functional interaction of SMADs and p300/CBP. J Biol Chem. 1998;273:22865-22868.
26. Janknecht R, Wells NJ, Hunter T. TGF-beta-stimulated cooperation of smad proteins with the coactivators CBP/p300. Genes Dev. 1998;12:2114-2119.
27. Chen CY, Croissant J, Majesky M, Topouzis S, McQuinn T, Frankovsky MJ, Schwartz RJ. Activation of the cardiac alpha-actin promoter depends upon serum response factor, Tinman homologue, Nkx-2.5, and intact serum response elements. Dev Genet. 1996;19:119-130.
28. Zhu H, Garcia AV, Ross RS, Evans SM, Chien KR. A conserved 28-base-pair element (HF-1) in the rat cardiac myosin light-chain-2 gene confers cardiac-specific and alpha-adrenergic-inducible expression in cultured neonatal rat myocardial cells. Mol Cell Biol. 1991;11:2273-2281.
29. Lien CL, McAnally J, Richardson JA, Olson EN. Cardiac-specific activity of an Nkx2-5 enhancer requires an evolutionarily conserved Smad binding site. Dev Biol. 2002;244:257-266.
30. Nicol RL, Frey N, Pearson G, Cobb M, Richardson J, Olson EN. Activated MEK5 induces serial assembly of sarcomeres and eccentric cardiac hypertrophy. EMBO J. 2001;20:2757-2767.
31. Chang PS, Li L, McAnally J, Olson EN. Muscle specificity encoded by specific serum response factor-binding sites. J Biol Chem. 2001;276:17206-17212.
32. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell. 2003;113:685-700.
33. Shi Y, Wang YF, Jayaraman L, Yang H, Massague J, Pavletich NP. Crystal structure of a Smad MH1 domain bound to DNA: insights on DNA binding in TGF-beta signaling. Cell. 1998;94:585-594.
34. Zawel L, Dai JL, Buckhaults P, Zhou S, Kinzler KW, Vogelstein B, Kern SE. Human Smad3 and Smad4 are sequence-specific transcription activators. Mol Cell. 1998;1:611-617.
35. 1 signaling in a CArG box-independent manner. Smad-binding element is a critical cis element for SM22α transcription in vivo. Circ Res. 2005;97:983-991.
36. Oh J, Wang Z, Wang DZ, Lien CL, Xing W, Olson EN. Target gene-specific modulation of myocardin activity by GATA transcription factors. Mol Cell Biol. 2004;24:8519-8528.
37. Wang DZ, Valdez MR, McAnally J, Richardson J, Olson EN. The Mef2c gene is a direct transcriptional target of myogenic bHLH and MEF2 proteins during skeletal muscle development. Development. 2001;128:4623-4633.
38. Spiegelman BM, Heinrich R. Biological control through regulated transcriptional coactivators. Cell. 2004;119:157-167.
39. Brown CO 3rd, Chi X, Garcia-Gras E, Shirai M, Feng XH, Schwartz RJ. The cardiac determination factor, Nkx2-5, is activated by mutual cofactors GATA-4 and Smad1/4 via a novel upstream enhancer. J Biol Chem. 2004;279:10659-10669.
40. Lee KH, Evans S, Ruan TY, Lassar AB. SMAD-mediated modulation of YY1 activity regulates the BMP response and cardiac-specific expression of a GATA4/5/6-dependent chick Nkx2.5 enhancer. Development. 2004;131:4709-4723.
41. Blokzijl A, ten Dijke P, Ibanez CF. Physical and functional interaction between GATA-3 and Smad3 allows TGF-beta regulation of GATA target genes. Curr Biol. 2002;12:35-45.
42. Chang DF, Belaguli NS, Iyer D, Roberts WB, Wu SP, Dong XR, Marx IG, Moore MS, Beckerle MC, Majesky MW, Schwartz RJ. Cysteine-rich LIM-only proteins CRP1 and CRP2 are potent smooth muscle differentiation cofactors. Dev Cell. 2003;4:107-118.
43. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev. 2004;84:767-801.
44. Qiu P, Feng XH, Li L. Interaction of Smad3 and SRF-associated complex mediates TGF-beta1 signals to regulate SM22 transcription during myofibroblast differentiation. J Mol Cell Cardiol. 2003;35:1407-1420.