Epigenetic regulation of vascular smooth muscle cell proliferation and neointima formation by histone deacetylase inhibition

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 4, 2011, Pages 851-860

  Findeisen, Hannes M ^a   Gizard, Florence ^a   Zhao, Yue ^a   Qing, Hua ^a   Heywood, Elizabeth B ^a   Jones, Karrie L ^a   Cohn, Dianne ^a   Bruemmer, Dennis ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b Wethington Bldg   (United States)

Author keywords

gene expression; growth factors; HDAC inhibitors; proliferation; restenosis; vascular biology; vascular muscle

Indexed keywords

6 (1,3 DIOXO 1H,3H BENZO[DE]ISOQUINOLIN 2 YL) N HYDROXYHEXANAMIDE; CYCLIN D1; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; MESSENGER RNA; MITOGENIC AGENT; RETINOBLASTOMA PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR E2F;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTERY INJURY; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENE INDUCTION; GENE REPRESSION; GENE TARGETING; MOUSE; NEOINTIMA; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; RNA INTERFERENCE; SMOOTH MUSCLE FIBER; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ACETYLATION; ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; CELL PROLIFERATION; CELLS, CULTURED; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYCLIN D1; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; DISEASE MODELS, ANIMAL; E2F TRANSCRIPTION FACTORS; EPIGENESIS, GENETIC; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HISTONES; HYDROXYLAMINES; HYPERPLASIA; MICE; MICE, INBRED C57BL; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PHOSPHORYLATION; QUINOLINES; RATS; RETINOBLASTOMA PROTEIN; RNA INTERFERENCE; TIME FACTORS; TRANSCRIPTION, GENETIC; TUNICA MEDIA; VASCULAR SYSTEM INJURIES;

EID: 79953749086     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.110.221952     Document Type: Article

References (40)

1. Dzau VJ, Braun-Dullaeus RC, Sedding DG. Vascular proliferation and atherosclerosis: new perspectives and therapeutic strategies. Nat Med. 2002;8:1249-1256. (Pubitemid 35373556)
2. Doran AC, Meller N, McNamara CA. Role of smooth muscle cells in the initiation and early progression of atherosclerosis. Arterioscler Thromb Vasc Biol. 2008;28:812-819. (Pubitemid 351544093)
3. Moses JW, Leon MB, Popma JJ, Fitzgerald PJ, Holmes DR, O'Shaughnessy C, Caputo RP, Kereiakes DJ, Williams DO, Teirstein PS, Jaeger JL, Kuntz RE, the SIRIUS Investigators. Sirolimus-eluting stents versus standard stents in patients with stenosis in a native coronary artery. N Engl J Med. 2003;349:1315-1323. (Pubitemid 37186209)
4. 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)
5. Li B, Carey M, Workman JL. The role of chromatin during transcription. Cell. 2007;128:707-719. (Pubitemid 46273570)
6. Bernstein BE, Meissner A, Lander ES. The mammalian epigenome. Cell. 2007;128:669-681. (Pubitemid 46273573)
7. Jenuwein T, Allis CD. Translating the histone code. Science. 2001;293: 1074-1080. (Pubitemid 32758077)
8. Sambucetti LC, Fischer DD, Zabludoff S, Kwon PO, Chamberlin H, Trogani N, Xu H, Cohen D. Histone deacetylase inhibition selectively alters the activity and expression of cell cycle proteins leading to specific chromatin acetylation and antiproliferative effects. J Biol Chem. 1999; 274:34940-34947. (Pubitemid 129509542)
9. 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)
10. Margariti A, Zampetaki A, Xiao Q, Zhou B, Karamariti E, Martin D, Yin X, Mayr M, Li H, Zhang Z, De Falco E, Hu Y, Cockerill G, Xu Q, Zeng L. Histone deacetylase 7 controls endothelial cell growth through modulation ofβ-catenin. Circ Res. 106:1202-1211.
11. Miao F, Gonzalo IG, Lanting L, Natarajan R. In vivo chromatin remodeling events leading to inflammatory gene transcription under diabetic conditions. J Biol Chem. 2004;279:18091-18097. (Pubitemid 38560579)
12. Nomiyama T, Zhao Y, Gizard F, Findeisen HM, Heywood EB, Jones KL, Conneely OM, Bruemmer D. Deficiency of the NR4A neuron-derived orphan receptor-1 attenuates neointima formation after vascular injury. Circulation. 2009;119:577-586.
13. Su GH, Sohn TA, Ryu B, Kern SE. A novel histone deacetylase inhibitor identified by high-throughput transcriptional screening of a compound library. Cancer Res. 2000;60:3137-3142. (Pubitemid 30407906)
14. Keen JC, Yan L, Mack KM, Pettit C, Smith D, Sharma D, Davidson NE. A novel histone deacetylase inhibitor, Scriptaid, enhances expression of functional estrogen receptor (ER) in ER negative human breast cancer cells in combination with 5-aza 2β-deoxycytidine. Breast Cancer Res Treat. 2003;81:177-186. (Pubitemid 37352455)
15. Kong Y, Tannous P, Lu G, Berenji K, Rothermel BA, Olson EN, Hill JA. Suppression of class I and II histone deacetylases blunts pressureoverload cardiac hypertrophy. Circulation. 2006;113:2579-2588. (Pubitemid 43948006)
16. Weinberg RA. E2f and cell proliferation: a world turned upside down. Cell. 1996;85:457-459. (Pubitemid 26157183)
17. Tanner FC, Boehm M, Akyurek LM, San H, Yang Z-Y, Tashiro J, Nabel GJ, Nabel EG. Differential effects of the cyclin-dependent kinase inhibitors p27(Kip1), p21(Cip1), and p16(Ink4) on vascular smooth muscle cell proliferation. Circulation. 2000;101:2022-2025. (Pubitemid 30233162)
18. Bartl S, Taplick J, Lagger G, Khier H, Kuchler K, Seiser C. Identification of mouse histone deacetylase 1 as a growth factor-inducible gene. Mol Cell Biol. 1997;17:5033-5043. (Pubitemid 27357602)
19. Senese S, Zaragoza K, Minardi S, Muradore I, Ronzoni S, Passafaro A, Bernard L, Draetta GF, Alcalay M, Seiser C, Chiocca S. A role for histone deacetylase 1 in human tumor cell proliferation. Mol Cell Biol. 2007;MCB. 00494-00407.
20. Lagger G, O'Carroll D, Rembold M, Khier H, Tischler J, Weitzer G, Schuettengruber B, Hauser C, Brunmeir R, Jenuwein T, Seiser C. Essential function of histone deacetylase 1 in proliferation control and cdk inhibitor repression. EMBO J. 2002;21:2672-2681. (Pubitemid 34619383)
21. Glaser KB, Li J, Staver MJ, Wei RQ, Albert DH, Davidsen SK. Role of class I and class II histone deacetylases in carcinoma cells using siRNA. Biochem Biophys Res Commun. 2003;310:529-536. (Pubitemid 37163696)
22. Ma X, Ezzeldin HH, Diasio RB. Histone deacetylase inhibitors: current status and overview of recent clinical trials. Drugs. 2009;69:1911-1934.
23. Qiu L, Burgess A, Fairlie DP, Leonard H, Parsons PG, Gabrielli BG. Histone deacetylase inhibitors trigger a G2 checkpoint in normal cells that is defective in tumor cells. Mol Biol Cell. 2000;11:2069-2083. (Pubitemid 30408065)
24. Richon VM, Sandhoff TW, Rifkind RA, Marks PA. Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation. Proc Natl Acad Sci USA. 2000;97:10014-10019.
25. Yang ZY, Simari RD, Perkins ND, San H, Gordon D, Nabel GJ, Nabel EG. Role of the p21 cyclin-dependent kinase inhibitor in limiting intimal cell proliferation in response to arterial injury. Proc Natl Acad Sci USA. 1996;93:7905-7910. (Pubitemid 26277137)
26. Okamoto H, Fujioka Y, Takahashi A, Takahashi T, Taniguchi T, Ishikawa Y, Yokoyama M. Trichostatin A, an inhibitor of histone deacetylase, inhibits smooth muscle cell proliferation via induction of p21(WAF1). J Atheroscler Thromb. 2006;13:183-191.
27. Wilting RH, Yanover E, Heideman MR, Jacobs H, Horner J, van der Torre J, Depinho RA, Dannenberg JH. Overlapping functions of Hdac1 and Hdac2 in cell cycle regulation and haematopoiesis. EMBO J. 2010; 29:2586-2597.
28. Chen JS, Faller DV. Histone deacetylase inhibition-mediated posttranslational elevation of p27KIP1 protein levels is required for G1 arrest in fibroblasts. J Cell Physiol. 2005;202:87-99. (Pubitemid 39603365)
29. Baldin V, Lukas J, Marcote M, Pagano M, Draetta G. Cyclin D1 is a nuclear protein required for cell cycle progression in G1. Genes Dev. 1993;7:812-821. (Pubitemid 23163585)
30. Yamaguchi K, Lantowski A, Dannenberg AJ, Subbaramaiah K. Histone deacetylase inhibitors suppress the induction of c-Jun and its target genes including COX-2. J Biol Chem. 2005;280:32569-32577. (Pubitemid 41368298)
31. Hu J, Colburn NH. Histone deacetylase inhibition down-regulates cyclin D1 transcription by inhibiting nuclear factor-βB/p65 DNA binding. Mol Cancer Res. 2005;3:100-109. (Pubitemid 40271140)
32. Sharma P, Kumar S, Kundu GC. Transcriptional regulation of human osteopontin promoter by histone deacetylase inhibitor, trichostatin A in cervical cancer cells. Mol Cancer. 2010;9:178.
33. Hu Y, Cheng L, Hochleitner B-W, Xu Q. Activation of mitogen-activated protein kinases (ERK/JNK) and AP-1 transcription factor in rat carotid arteries after balloon injury. Arterioscler Thromb Vasc Biol. 1997;17: 2808-2816. (Pubitemid 28016025)
34. Bellas RE, Lee JS, Sonenshein GE. Expression of a constitutive NF-βB-like activity is essential for proliferation of cultured bovine vascular smooth muscle cells. J Clin Invest. 1995;96:2521-2527.
35. Santiago FS, Ishii H, Shafi S, Khurana R, Kanellakis P, Bhindi R, Ramirez MJ, Bobik A, Martin JF, Chesterman CN, Zachary IC, Khachigian LM. Yin Yang-1 inhibits vascular smooth muscle cell growth and intimal thickening by repressing p21WAF1/Cip1 transcription and p21WAF1/Cip1-Cdk4-cyclin D1 assembly. Circ Res. 2007;101:146-155. (Pubitemid 47196582)
36. Karpurapu M, Wang D, Van Quyen D, Kim T-K, Kundumani-Sridharan V, Pulusani S, Rao GN. Cyclin D1 is a bona fide target gene of NFATc1 and is sufficient in the mediation of injury-induced vascular wall remodeling. J Biol Chem. 2010;285:3510-3523.
37. Roque M, Fallon JT, Badimon JJ, Zhang WX, Taubman MB, Reis ED. Mouse model of femoral artery denudation injury associated with the rapid accumulation of adhesion molecules on the luminal surface and recruitment of neutrophils. Arterioscler Thromb Vasc Biol. 2000;20: 335-342. (Pubitemid 30086088)
38. Liu T, Tee AE, Porro A, Smith SA, Dwarte T, Liu PY, Iraci N, Sekyere E, Haber M, Norris MD, Diolaiti D, Della Valle G, Perini G, Marshall GM. Activation of tissue transglutaminase transcription by histone deacetylase inhibition as a therapeutic approach for Myc oncogenesis. Proc Natl Acad Sci USA. 2007;104:18682-18687. (Pubitemid 350210757)
39. Imre G, Gekeler V, Leja A, Beckers T, Boehm M. Histone deacetylase inhibitors suppress the inducibility of nuclear factor-βB by tumor necrosis factor-β receptor-1 down-regulation. Cancer Res. 2006;66:5409-5418. (Pubitemid 43844968)
40. Yan Z-Q, Yao Q-P, Zhang M-L, Qi Y-X, Guo Z-Y, Shen B-R, Jiang Z-L. Histone deacetylases modulate vascular smooth muscle cell migration induced by cyclic mechanical strain. J Biomech. 2009;42:945-948.