Vascular smooth muscle cell phenotypic plasticity: Focus on chromatin remodelling

Cardiovascular Research

Volumn 95, Issue 2, 2012, Pages 147-155

  Spin, Joshua M ^a   Maegdefessel, Lars ^a   Tsao, Philip S ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Histone modification; Phenotypic switching; Vascular development; Vascular disease

Indexed keywords

BUTYRIC ACID; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; KRUPPEL LIKE FACTOR 4; METHYLTRANSFERASE; MYOCARDIN; PHOSPHOLIPID; PLATELET DERIVED GROWTH FACTOR; RETINOIC ACID; TRANSFORMING GROWTH FACTOR BETA;

CELL FUNCTION; CHROMATIN; CHROMATIN STRUCTURE; DIABETES MELLITUS; HISTONE MODIFICATION; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SMOOTH MUSCLE FIBER; THORACIC AORTA ANEURYSM; TRANSCRIPTION REGULATION; VASCULAR SMOOTH MUSCLE;

ANIMALS; CELL DIFFERENTIATION; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; HISTONES; HUMANS; MYOCYTES, SMOOTH MUSCLE; PHENOTYPE;

EID: 84862874415     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvs098     Document Type: Review

References (95)

1. Owens GK. Regulation of differentiation of vascular smooth muscle cells. Physiol Rev 1995;75:487-517.
2. Owens GK, Kumar MS,Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 2004;84:767-801. (Pubitemid 38823766)
3. Ross R. Atherosclerosis: an inflammatory disease. N Engl J Med 1999;340:115-126.
4. Ailawadi G, Moehle CW, Pei H, Walton SP, Yang Z, Kron IL et al. Smooth muscle phenotypic modulation is an early event in aortic aneurysms. J Thorac Cardiovasc Surg 2009;138:1392-1399.
5. 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. (Pubitemid 34132512)
6. 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. (Pubitemid 43121789)
7. McDonald OG, Owens GK. Programming smooth muscle plasticity with chromatin dynamics. Circ Res 2007;100:1428-1441. (Pubitemid 46834755)
8. Backs J, Olson EN. Control of cardiac growth by histone acetylation/deacetylation. Circ Res 2006;98:15-24. (Pubitemid 43977219)
9. McKinsey TA, Zhang CL, Olson EN. Signaling chromatin to make muscle. Curr Opin Cell Biol 2002;14:763-772. (Pubitemid 35449391)
10. Fischle W, Wang Y, Allis CD. Histone and chromatin cross-talk. Curr Opin Cell Biol 2003;15:172-183. (Pubitemid 36332192)
11. Marmorstein R. Protein modules that manipulate histone tails for chromatin regulation. Nat Rev Mol Cell Biol 2001;2:422-432. (Pubitemid 33680581)
12. Khorasanizadeh S. The nucleosome: from genomic organization to genomic regulation. Cell 2004;116:259-272. (Pubitemid 38167316)
13. Allfrey VG, Faulkner R, Mirsky AE. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc Natl Acad Sci USA 1964;51: 786-794.
14. Bradbury EM. Reversible histone modifications and the chromosome cell cycle. Bioessays 1992;14:9-16.
15. Wolffe AP, Hayes JJ. Chromatin disruption and modification. Nucleic Acids Res 1999; 27:711-720. (Pubitemid 29209356)
16. Cheung P, Allis CD, Sassone-Corsi P. Signaling to chromatin through histone modifications. Cell 2000;103:263-271.
17. Strahl BD, Allis CD. The language of covalent histone modifications. Nature 2000;403: 41-45. (Pubitemid 30038513)
18. Spin JM, Nallamshetty S, Tabibiazar R, Ashley EA, King JY, Chen M et al. Transcriptional profiling of in vitro smooth muscle cell differentiation identifies specific patterns of gene and pathway activation. Physiol Genomics 2004;19:292-302. (Pubitemid 40039935)
19. Spin JM, Quertermous T, Tsao PS. Chromatin remodeling pathways in smooth muscle cell differentiation, and evidence for an integral role for p300. PLoS One 2010;5: e14301.
20. Peserico A, Simone C. Physical and functional HAT/HDAC interplay regulates protein acetylation balance. J Biomed Biotechnol 2011;2011:371832.
21. Goodman RH, Smolik S. CBP/p300 in cell growth, transformation, and development. Genes Dev 2000;14:1553-1577. (Pubitemid 30460905)
22. Polesskaya A, Naguibneva I, Fritsch L, Duquet A, Ait-Si-Ali S, Robin P et al. CBP/p300 and muscle differentiation: no HAT, no muscle. Embo J 2001;20:6816-6825. (Pubitemid 33134211)
23. Eckner R, Yao TP, Oldread E, Livingston DM. Interaction and functional collaboration of p300/CBP and bHLH proteins in muscle and B-cell differentiation. Genes Dev 1996; 10:2478-2490. (Pubitemid 26341882)
24. Dai YS, Cserjesi P, Markham BE, Molkentin JD. The transcription factors GATA4 and dHAND physically interact to synergistically activate cardiac gene expression through a p300-dependent mechanism. J Biol Chem 2002;277:24390-24398. (Pubitemid 34951961)
25. Poizat C, Sartorelli V, Chung G, Kloner RA, Kedes L. Proteasome-mediated degradation of the coactivator p300 impairs cardiac transcription. Mol Cell Biol 2000;20: 8643-8654. (Pubitemid 32245898)
26. 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. (Pubitemid 34633877)
27. Aravind L, Koonin EV. SAP: a putative DNA-binding motif involved in chromosomal organization. Trends Biochem Sci 2000;25:112-114. (Pubitemid 30122420)
28. Cao D, Wang Z, Zhang CL, Oh J, Xing W, Li S et al. Modulation of smooth muscle gene expression by association of histone acetyltransferases and deacetylases with myocardin. Mol Cell Biol 2005;25:364-376. (Pubitemid 40039826)
29. Wada H, Hasegawa K, Morimoto T, Kakita T, Yanazume T, Sasayama S. A p300 protein as a coactivator of GATA-6 in the transcription of the smooth muscle-myosin heavy chain gene. J Biol Chem 2000;275:25330-25335.
30. Wang SX, Elder PK, Zheng Y, Strauch AR, Kelm RJ Jr. Cell cycle-mediated regulation of smooth muscle alpha-actin gene transcription in fibroblasts and vascular smooth muscle cells involves multiple adenovirus E1A-interacting cofactors. J Biol Chem 2005;280:6204-6214. (Pubitemid 40280105)
31. Chakravarti D, LaMorte VJ, Nelson MC, Nakajima T, Schulman IG, Juguilon H et al. Role of CBP/P300 in nuclear receptor signalling. Nature 1996;383:99-103. (Pubitemid 26296470)
32. Partanen A, Motoyama J, Hui CC. Developmentally regulated expression of the transcriptional cofactors/histone acetyltransferases CBP and p300 during mouse embryogenesis. Int J Dev Biol 1999;43:487-494.
33. Yao TP, Oh SP, Fuchs M, Zhou ND, Ch'ng LE, Newsome D et al. Gene dosagedependent embryonic development and proliferation defects in mice lacking the transcriptional integrator p300. Cell 1998;93:361-372. (Pubitemid 28232081)
34. Vo N, Goodman RH. CREB-binding protein and p300 in transcriptional regulation. J Biol Chem 2001;276:13505-13508.
35. Wang D, Chang PS, Wang Z, Sutherland L, Richardson JA, Small E et al. Activation of cardiac gene expression by myocardin, a transcriptional cofactor for serum response factor. Cell 2001;105:851-862. (Pubitemid 32635087)
36. 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. (Pubitemid 35244412)
37. Du KL, Ip HS, Li J, Chen M, Dandre F, Yu W et al. Myocardin is a critical serum response factor cofactor in the transcriptional program regulating smooth muscle cell differentiation. Mol Cell Biol 2003;23:2425-2437. (Pubitemid 36351024)
38. Wang Z, Wang DZ, Pipes GC, Olson EN. Myocardin is a master regulator of smooth muscle gene expression. Proc Natl Acad Sci USA 2003;100:7129-7134. (Pubitemid 36706404)
39. Yoshida T, Sinha S, Dandre F, Wamhoff BR, Hoofnagle MH, Kremer BE et al. Myocardin is a key regulator of CArG-dependent transcription of multiple smooth muscle marker genes. Circ Res 2003;92:856-864. (Pubitemid 36542526)
40. 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. (Pubitemid 39180881)
41. Ramirez S, Ait-Si-Ali S, Robin P, Trouche D, Harel-Bellan A, Ait Si Ali S. The CREBbinding protein (CBP) cooperates with the serum response factor for transactivation of the c-fos serum response element. J Biol Chem 1997;272:31016-31021. (Pubitemid 27527547)
42. Kalkhoven E. CBP and p300: HATs for different occasions. Biochem Pharmacol 2004; 68:1145-1155. (Pubitemid 39094280)
43. Dietze EC, Troch MM, Bowie ML, Yee L, Bean GR, Seewaldt VL. CBP/p300 induction is required for retinoic acid sensitivity in human mammary cells. Biochem Biophys Res Commun 2003;302:841-848. (Pubitemid 36294051)
44. Ait-Si-Ali S, Ramirez S, Barre FX, Dkhissi F, Magnaghi-Jaulin L, Girault JA et al. Histone acetyltransferase activity of CBP is controlled by cycle-dependent kinases and oncoprotein E1A. Nature 1998;396:184-186. (Pubitemid 28523622)
45. Kawasaki H, Eckner R, Yao TP, Taira K, Chiu R, Livingston DM et al. Distinct roles of the co-activators p300 and CBP in retinoic-acid-induced F9-cell differentiation. Nature 1998;393:284-289. (Pubitemid 28261730)
46. Brouillard F, Cremisi CE. Concomitant increase of histone acetyltransferase activity and degradation of p300 during retinoic acid-induced differentiation of F9 cells. J Biol Chem 2003;278:39509-39516. (Pubitemid 37258322)
47. Katsumoto T, Aikawa Y, Iwama A, Ueda S, Ichikawa H, Ochiya T et al. MOZ is essential for maintenance of hematopoietic stem cells. Genes Dev 2006;20:1321-1330. (Pubitemid 43727592)
48. Scott HS, Antonarakis SE, Lalioti MD, Rossier C, Silver PA, Henry MF. Identification and characterization of two putative human arginine methyltransferases (HRMT1L1 and HRMT1L2). Genomics 1998;48:330-340. (Pubitemid 28180733)
49. Qi C, Chang J, Zhu Y, Yeldandi AV, Rao SM, Zhu YJ. Identification of protein arginine methyltransferase 2 as a coactivator for estrogen receptor alpha. J Biol Chem 2002; 277:28624-28630. (Pubitemid 41079291)
50. Thiagalingam S, Cheng KH, Lee HJ, Mineva N, Thiagalingam A, Ponte JF. Histone deacetylases: unique players in shaping the epigenetic histone code. Ann N Y Acad Sci 2003;983:84-100. (Pubitemid 36399322)
51. Gao L, Cueto MA, Asselbergs F, Atadja P. Cloning and functional characterization of HDAC11, a novel member of the human histone deacetylase family. J Biol Chem 2002; 277:25748-25755. (Pubitemid 34951896)
52. McKinsey TA, Zhang CL, Olson EN. Control of muscle development by dueling HATs and HDACs. Curr Opin Genet Dev 2001;11:497-504. (Pubitemid 32800722)
53. Minucci S, Horn V, Bhattacharyya N, Russanova V, Ogryzko VV, Gabriele L et al. A histone deacetylase inhibitor potentiates retinoid receptor action in embryonal carcinoma cells. Proc Natl Acad Sci USA 1997;94:11295-11300. (Pubitemid 27450992)
54. Okamoto H, Fujioka Y, Takahashi A, Takahashi T, Taniguchi T, Ishikawa Y et al. Trichostatin A, an inhibitor of histone deacetylase, inhibits smooth muscle cell proliferation via induction of p21(WAF1). J Atheroscler Thromb 2006;13:183-191.
55. 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. (Pubitemid 44188580)
56. Findeisen HM, Gizard F, Zhao Y, Qing H, Heywood EB, Jones KL et al. Epigenetic regulation of vascular smooth muscle cell proliferation and neointima formation by histone deacetylase inhibition. Arterioscler Thromb Vasc Biol 2011;31:851-860.
57. Yoshida T, Kaestner KH, Owens GK. Conditional deletion of Kruppel-like factor 4 delays downregulation of smooth muscle cell differentiation markers but accelerates neointimal formation following vascular injury. Circ Res 2008;102:1548-1557.
58. Singh N, Trivedi CM, Lu M, Mullican SE, Lazar MA, Epstein JA. Histone deacetylase 3 regulates smooth muscle differentiation in neural crest cells and development of the cardiac outflow tract. Circ Res 2011;109:1240-1249.
59. Margariti A, Xiao Q, Zampetaki A, Zhang Z, Li H, Martin D et al. Splicing of HDAC7 modulates the SRF-myocardin complex during stem-cell differentiation towards smooth muscle cells. J Cell Sci 2009;122:460-470.
60. Zhang L, Jin M, Margariti A, Wang G, Luo Z, Zampetaki A et al. Sp1-dependent activation of HDAC7 is required for platelet-derived growth factor-BB-induced smooth muscle cell differentiation from stem cells. J Biol Chem 2010;285:38463-38472.
61. Waltregny D, De Leval L, Glenisson W, Ly Tran S, North BJ, Bellahcene A et al. Expression of histone deacetylase 8, a class I histone deacetylase, is restricted to cells showing smooth muscle differentiation in normal human tissues. Am J Pathol 2004; 165:553-564. (Pubitemid 38971385)
62. Waltregny D, Glenisson W, Tran SL, North BJ, Verdin E, Colige A et al. Histone deacetylase HDAC8 associates with smooth muscle alpha-actin and is essential for smooth muscle cell contractility. Faseb J 2005;19:966-968. (Pubitemid 40827719)
63. Bouras T, Fu M, Sauve AA,Wang F, Quong AA, Perkins ND et al. SIRT1 deacetylation and repression of p300 involves lysine residues 1020/1024 within the cell cycle regulatory domain 1. J Biol Chem 2005;280:10264-10276. (Pubitemid 40395882)
64. Fulco M, Schiltz RL, Iezzi S, King MT, Zhao P, Kashiwaya Y et al. Sir2 regulates skeletal muscle differentiation as a potential sensor of the redox state. Mol Cell 2003;12: 51-62. (Pubitemid 36945036)
65. Li L, Zhang HN, Chen HZ, Gao P, Zhu LH, Li HL et al. SIRT1 acts as a modulator of neointima formation following vascular injury in mice. Circ Res 2011;108: 1180-1189.
66. Zou J, Huang Y, Cao K, Yang G, Yin H, Len J et al. Effect of resveratrol on intimal hyperplasia after endothelial denudation in an experimental rabbit model. Life Sci 2000;68:153-163.
67. Stunkel W, Campbell RM. Sirtuin 1 (SIRT1): the misunderstood HDAC. J Biomol Screen 2011;16:1153-1169.
68. Yoshida T, Gan Q, Shang Y, Owens GK. Platelet-derived growth factor-BB represses smooth muscle cell marker genes via changes in binding of MKL factors and histone deacetylases to their promoters. Am J Physiol Cell Physiol 2007;292: C886-C895.
69. Yoshida T, Gan Q, Owens GK. Kruppel-like factor 4, Elk-1, and histone deacetylases cooperatively suppress smooth muscle cell differentiation markers in response to oxidized phospholipids. Am J Physiol Cell Physiol 2008;295:C1175-C1182. (Pubitemid 352790337)
70. Wang DZ, Li S, Hockemeyer D, Sutherland L,Wang Z, Schratt G et al. Potentiation of serum response factor activity by a family of myocardin-related transcription factors. Proc Natl Acad Sci USA 2002;99:14855-14860. (Pubitemid 35334573)
71. Li J, Zhu X, Chen M, Cheng L, Zhou D, Lu MM et al. Myocardin-related transcription factor B is required in cardiac neural crest for smooth muscle differentiation and cardiovascular development. Proc Natl Acad Sci USA 2005;102:8916-8921. (Pubitemid 40881053)
72. Hinson JS, Medlin MD, Lockman K, Taylor JM, Mack CP. Smooth muscle cell-specific transcription is regulated by nuclear localization of the myocardin-related transcription factors. Am J Physiol Heart Circ Physiol 2007;292:H1170-H1180.
73. Lockman K, Taylor JM, Mack CP. The histone demethylase, Jmjd1a, interacts with the myocardin factors to regulate SMC differentiation marker gene expression. Circ Res 2007;101:e115-e123. (Pubitemid 350294652)
74. Tachibana M, Sugimoto K, Nozaki M, Ueda J, Ohta T, Ohki M et al. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev 2002;16:1779-1791. (Pubitemid 34803894)
75. Dodge JE, Kang YK, Beppu H, Lei H, Li E. Histone H3-K9 methyltransferase ESET is essential for early development. Mol Cell Biol 2004;24:2478-2486. (Pubitemid 38326002)
76. Stewart MD, Li J,Wong J. Relationship between histone H3 lysine 9 methylation, transcription repression, and heterochromatin protein 1 recruitment. Mol Cell Biol 2005; 25:2525-2538. (Pubitemid 40381619)
77. de la Cruz CC, Kirmizis A, Simon MD, Isono K, Koseki H, Panning B. The polycomb group protein SUZ12 regulates histone H3 lysine 9 methylation and HP1 alpha distribution. Chromosome Res 2007;15:299-314. (Pubitemid 46709798)
78. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 2001;410:116-120. (Pubitemid 32225847)
79. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 2001;410:120-124. (Pubitemid 32225848)
80. Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 2006;439:871-874. (Pubitemid 43255707)
81. Pidkovka NA, Cherepanova OA, Yoshida T, Alexander MR, Deaton RA, Thomas JA et al. Oxidized phospholipids induce phenotypic switching of vascular smooth muscle cells in vivo and in vitro. Circ Res 2007;101:792-801. (Pubitemid 350287194)
82. Thomas JA, Deaton RA, Hastings NE, Shang Y, Moehle CW, Eriksson U et al. PDGF-DD, a novel mediator of smooth muscle cell phenotypic modulation, is upregulated in endothelial cells exposed to atherosclerosis-prone flow patterns. Am J Physiol Heart Circ Physiol 2009;296:H442-H452.
83. Yu K, Zheng B, Han M, Wen JK. ATRA activates and PDGF-BB represses the SM22alpha promoter through KLF4 binding to, or dissociating from, its cis-DNA elements. Cardiovasc Res 2011;90:464-474.
84. Xie C, Huang H, Sun X, Guo Y, Hamblin M, Ritchie RP et al. MicroRNA-1 regulates smooth muscle cell differentiation by repressing Kruppel-like factor 4. Stem Cells Dev 2011;20:205-210.
85. Davis-Dusenbery BN, Chan MC, Reno KE, Weisman AS, Layne MD, Lagna G et al. down-regulation of Kruppel-like factor-4 (KLF4) by microRNA-143/145 is critical for modulation of vascular smooth muscle cell phenotype by transforming growth factor-beta and bone morphogenetic protein 4. J Biol Chem 2011;286:28097-28110.
86. Huang H, Xie C, Sun X, Ritchie RP, Zhang J, Chen YE. miR-10a contributes to retinoid acid-induced smooth muscle cell differentiation. J Biol Chem 2010;285:9383-9389.
87. Zhang QJ, Goddard M, Shanahan C, Shapiro L, Bennett M. Differential gene expression in vascular smooth muscle cells in primary atherosclerosis and in stent stenosis in humans. Arterioscler Thromb Vasc Biol 2002;22:2030-2036. (Pubitemid 36025210)
88. Chang DF, Belaguli NS, Chang J, Schwartz RJ. LIM-only protein, CRP2, switched on smooth muscle gene activity in adult cardiac myocytes. Proc Natl Acad Sci USA 2007;104:157-162. (Pubitemid 46068001)
89. Zhang M, Fang H, Zhou J, Herring BP. A novel role of Brg1 in the regulation of SRF/MRTFA-dependent smooth muscle-specific gene expression. J Biol Chem 2007;282: 25708-25716. (Pubitemid 47372829)
90. Davis CA, Haberland M, Arnold MA, Sutherland LB, McDonald OG, Richardson JA et al. PRISM/PRDM6, a transcriptional repressor that promotes the proliferative gene program in smooth muscle cells. Mol Cell Biol 2006;26: 2626-2636.
91. Mathew OP, Ranganna K, Yatsu FM. Butyrate, an HDAC inhibitor, stimulates interplay between different posttranslational modifications of histone H3 and differently alters G1-specific cell cycle proteins in vascular smooth muscle cells. Biomed Pharmacother 2010;64:733-740.
92. Villeneuve LM, Kato M, Reddy MA, Wang M, Lanting L, Natarajan R. Enhanced levels of microRNA-125b in vascular smooth muscle cells of diabetic db/db mice lead to increased inflammatory gene expression by targeting the histone methyltransferase Suv39h1. Diabetes 2010;59:2904-2915.
93. Villeneuve LM, Reddy MA, Lanting LL, Wang M, Meng L, Natarajan R. Epigenetic histone H3 lysine 9 methylation in metabolic memory and inflammatory phenotype of vascular smooth muscle cells in diabetes. Proc Natl Acad Sci USA 2008;105: 9047-9052.
94. Reddy MA, Villeneuve LM,Wang M, Lanting L, Natarajan R. Role of the lysine-specific demethylase 1 in the proinflammatory phenotype of vascular smooth muscle cells of diabetic mice. Circ Res 2008;103:615-623.
95. Gomez D, Coyet A, Ollivier V, Jeunemaitre X, Jondeau G, Michel JB et al. Epigenetic control of vascular smooth muscle cells in Marfan and non-Marfan thoracic aortic aneurysms. Cardiovasc Res 2011;89:446-456.