Splicing of histone deacetylase 7 modulates smooth muscle cell proliferation and neointima formation through nuclear β-catenin translocation

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 11, 2011, Pages 2676-2684

  Zhou, Boda ^a,b   Margariti, Andriana ^b   Zeng, Lingfang ^b   Habi, Ouassila ^b   Xiao, Qingzhong ^c   Martin, Daniel ^b   Wang, Gang ^b   Hu, Yanhua ^b   Wang, Xian ^a   Xu, Qingbo ^b  

^a PEKING UNIVERSITY   (China)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

beta catenin; HDAC; mouse model; neointima; smooth muscle

Indexed keywords

BETA CATENIN; CYCLIN D1; HISTONE DEACETYLASE 7; HISTONE DEACETYLASE 7U; ISOENZYME; PLATELET DERIVED GROWTH FACTOR BB; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY INJURY; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE ARREST; CELL NUCLEUS; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; FEMORAL ARTERY; GENE DELETION; GENE OVEREXPRESSION; GENE SILENCING; MOUSE; NEOINTIMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOOTH MUSCLE FIBER;

ALTERNATIVE SPLICING; ANIMALS; AORTA; BETA CATENIN; CELL NUCLEUS; CELL PROLIFERATION; CELLS, CULTURED; CYTOPLASM; FEMORAL ARTERY; HISTONE DEACETYLASES; HUMANS; MICE; MODELS, ANIMAL; MUSCLE, SMOOTH, VASCULAR; NEOINTIMA; PLATELET-DERIVED GROWTH FACTOR; RNA, SMALL INTERFERING;

EID: 80054964464     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.230888     Document Type: Article

References (41)

1. World CJ, Garin G, Berk B. Vascular shear stress and activation of inflammatory genes. Curr Atheroscler Rep. 2006;8:240-244. (Pubitemid 43676328)
2. Ross R. Atherosclerosis: an inflammatory disease. N Engl J Med. 1999; 340:115-126.
3. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993;362:801-809. (Pubitemid 23132154)
4. Millette E, Rauch BH, Kenagy RD, Daum G, Clowes AW. Plateletderived growth factor-BB transactivates the fibroblast growth factor receptor to induce proliferation in human smooth muscle cells. Trends Cardiovasc Med. 2006;16:25-28. (Pubitemid 43012038)
5. Marks PA, Xu WS. Histone deacetylase inhibitors: potential in cancer therapy. J Cell Biochem. 2009;107:600-608.
6. Pons D, de Vries FR, Van den Elsen PJ, Heijmans BT, Quax PH, Jukema JW. Epigenetic histone acetylation modifiers in vascular remodelling: new targets for therapy in cardiovascular disease. Eur Heart J. 2009;30: 266-277.
7. Chang S, Young BD, Li S, Qi X, Richardson JA, Olson EN. Histone deacetylase 7 maintains vascular integrity by repressing matrix metalloproteinase. Cell. 2006;126:321-334. (Pubitemid 44092958)
8. Mottet D, Bellahcene A, Pirotte S, Waltregny D, Deroanne C, Lamour V, Lidereau R, Castronovo V. Histone deacetylase 7 silencing alters endothelial cell migration, a key step in angiogenesis. Circ Res. 2007;101: 1237-1246. (Pubitemid 350294640)
9. Ha CH, Jhun BS, Kao HY, Jin ZG. VEGF stimulates HDAC7 phosphorylation and cytoplasmic accumulation modulating matrix metalloproteinase expression and angiogenesis. Arterioscler Thromb Vasc Biol. 2008;28:1782-1788.
10. Wang S, Li X, Parra M, Verdin E, Bassel-Duby R, Olson EN. Control of endothelial cell proliferation and migration by VEGF signaling to histone deacetylase 7. Proc Natl Acad Sci USA. 2008;105:7738-7743. (Pubitemid 351872708)
11. Margariti A, Xiao Q, Zampetaki A, Zhang Z, Li H, Martin D, Hu Y, Zeng L, Xu Q. Splicing of HDAC7 modulates the SRF-myocardin complex during stem-cell differentiation towards smooth muscle cells. J Cell Sci. 2009;122:460-470.
12. 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 of α-catenin. Circ Res. 2010;106:1202-1211.
13. Spallotta F, Rosati J, Straino S, Nanni S, Grasselli A, Ambrosino V, Rotili D, Valente S, Farsetti A, Mai A, Capogrossi MC, Gaetano C, Illi B. Nitric oxide determines mesodermic differentiation of mouse embryonic stem cells by activating class IIa histone deacetylases: potential therapeutic implications in a mouse model of hindlimb ischemia. Stem Cells. 2010; 28:431-442.
14. Black DL. Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem. 2003;72:291-336. (Pubitemid 36930448)
15. Cooper TA. Alternative splicing regulation impacts heart development. Cell. 2005;120:1-2. (Pubitemid 40094593)
16. Indik Z, Yeh H, Ornstein-Goldstein N, Kucich U, Abrams W, Rosenbloom JC, Rosenbloom J. Structure of the elastin gene and alternative splicing of elastin mRNA: implications for human disease. Am J Med Genet. 1989;34:81-90. (Pubitemid 19228952)
17. Zeng L, Zampetaki A, Margariti A, Pepe AE, Alam S, Martin D, Xiao Q, Wang W, Jin ZG, Cockerill G, Mori K, Li YS, Hu Y, Chien S, Xu Q. Sustained activation of XBP1 splicing leads to endothelial apoptosis and atherosclerosis development in response to disturbed flow. Proc Natl Acad Sci USA. 2009;106:8326-8331.
18. Matlin AJ, Clark F, Smith CW. Understanding alternative splicing: towards a cellular code. Nat Rev Mol Cell Biol. 2005;6:386-398. (Pubitemid 40637856)
19. Gosens R, Meurs H, Schmidt M. The GSK-3/α-catenin-signalling axis in smooth muscle and its relationship with remodelling. Naunyn Schmiedebergs Arch Pharmacol. 2008;378:185-191. (Pubitemid 351977640)
20. Quasnichka H, Slater SC, Beeching CA, Boehm M, Sala-Newby GB, George SJ. Regulation of smooth muscle cell proliferation by α-catenin/T-cell factor signaling involves modulation of cyclin D1 and p21 expression. Circ Res. 2006;99:1329-1337. (Pubitemid 44949668)
21. Slater SC, Koutsouki E, Jackson CL, Bush RC, Angelini GD, Newby AC, George SJ. R-cadherin: α-catenin complex and its association with vascular smooth muscle cell proliferation. Arterioscler Thromb Vasc Biol. 2004;24:1204-1210. (Pubitemid 38880009)
22. Huang M, Wang Y, Sun D, Zhu H, Yin Y, Zhang W, Yang S, Quan L, Bai J, Wang S, Chen Q, Li S, Xu N. Identification of genes regulated by wnt/α-catenin pathway and involved in apoptosis via microarray analysis. BMC Cancer. 2006;6:221.
23. Wang X, Xiao Y, Mou Y, Zhao Y, Blankesteijn WM, Hall JL. A role for the α-catenin/T-cell factor signaling cascade in vascular remodeling. Circ Res. 2002;90:340-347. (Pubitemid 34633936)
24. Skurk C, Maatz H, Rocnik E, Bialik A, Force T, Walsh K. Glycogensynthase kinase3-/-catenin axis promotes angiogenesis through activation of vascular endothelial growth factor signaling in endothelial cells. Circ Res. 2005;96:308-318. (Pubitemid 40279905)
25. Hu Y, Zou Y, Dietrich H, Wick G, Xu Q. Inhibition of neointima hyperplasia of mouse vein grafts by locally applied suramin. Circulation. 1999;100:861-868. (Pubitemid 29398886)
26. Mayr M, Hu Y, Hainaut H, Xu Q. Mechanical stress-induced DNA damage and rac-p38MAPK signal pathways mediate p53-dependent apoptosis in vascular smooth muscle cells. FASEB J. 2002;16:1423-1425.
27. Mayr M, Siow R, Chung YL, Mayr U, Griffiths JR, Xu Q. Proteomic and metabolomic analysis of vascular smooth muscle cells: role of PKCδ . Circ Res. 2004;94:e87-e96.
28. Hu Y, Davison F, Ludewig B, Erdel M, Mayr M, Url M, Dietrich H, Xu Q. Smooth muscle cells in transplant atherosclerotic lesions are originated from recipients, but not bone marrow progenitor cells. Circulation. 2002; 106:1834-1839.
29. Pepe AE, Xiao Q, Zampetaki A, Zhang Z, Kobayashi A, Hu Y, Xu Q. Crucial role of nrf3 in smooth muscle cell differentiation from stem cells. Circ Res. 106:870-879.
30. Zeng L, Xiao Q, Margariti A, Zhang Z, Zampetaki A, Patel S, Capogrossi MC, Hu Y, Xu Q. HDAC3 is crucial in shear-and VEGF-induced stem cell differentiation toward endothelial cells. J Cell Biol. 2006;174: 1059-1069. (Pubitemid 44455193)
31. Xiao Q, Zeng L, Zhang Z, Margariti A, Ali ZA, Channon KM, Xu Q, Hu Y. Sca-1+ progenitors derived from embryonic stem cells differentiate into endothelial cells capable of vascular repair after arterial injury. Arterioscler Thromb Vasc Biol. 2006;26:2244-2251. (Pubitemid 44465718)
32. Valdivia HH. One gene, many proteins: alternative splicing of the ryanodine receptor gene adds novel functions to an already complex channel protein. Circ Res. 2007;100:761-763. (Pubitemid 46555679)
33. Zheng ZM. Regulation of alternative RNA splicing by exon definition and exon sequences in viral and mammalian gene expression. J Biomed Sci. 2004;11:278-294.
34. Vadiveloo PK, Filonzi EL, Stanton HR, Hamilton JA. G1 phase arrest of human smooth muscle cells by heparin, IL-4 and cAMP is linked to repression of cyclin D1 and cdk2. Atherosclerosis. 1997;133:61-69. (Pubitemid 27322118)
35. Staal FJ, Noort Mv M, Strous GJ, Clevers HC. Wnt signals are transmitted through n-terminally dephosphorylated α-catenin. EMBO Rep. 2002;3:63-68. (Pubitemid 34144817)
36. Bornfeldt KE, Raines EW, Graves LM, Skinner MP, Krebs EG, Ross R. Platelet-derived growth factor: distinct signal transduction pathways associated with migration versus proliferation. Ann N Y Acad Sci. 1995;766: 416-430. (Pubitemid 26169122)
37. Wang L, Zheng J, Bai X, Liu B, Liu CJ, Xu Q, Zhu Y, Wang N, Kong W, Wang X. ADAMTS-7 mediates vascular smooth muscle cell migration and neointima formation in balloon-injured rat arteries. Circ Res. 2009;104:688-698.
38. Modrek B, Lee C. A genomic view of alternative splicing. Nat Genet. 2002;30:13-19.
39. Song S, Kang SW, Choi C. Trichostatin A enhances proliferation and migration of vascular smooth muscle cells by downregulating thioredoxin 1. Cardiovasc Res. 2010;85:241-249.
40. Catania A, Iavarone C, Carlomagno SM, Chiariello M. Selective transcription and cellular proliferation induced by PDGF require histone deacetylase activity. Biochem Biophys Res Commun. 2006;343:544-554.
41. Hao H, Gabbiani G, Bochaton-Piallat ML. Arterial smooth muscle cell heterogeneity: implications for atherosclerosis and restenosis development. Arterioscler Thromb Vasc Biol. 2003;23:1510-1520. (Pubitemid 37108191)