Histone deacetylase 3 is critical in endothelial survival and atherosclerosis development in response to disturbed flow

Circulation

Volumn 121, Issue 1, 2010, Pages 132-142

  Zampetaki, Anna ^a   Zeng, Lingfang ^a   Margariti, Andriana ^a   Xiao, Qingzhong ^a   Li, Hongling ^a   Zhang, Zhongyi ^a   Pepe, Anna Elena ^a   Wang, Gang ^a   Habi, Ouassila ^a   Defalco, Elena ^a   Cockerill, Gillian ^b   Mason, Justin C ^b   Hu, Yanhua ^a   Xu, Qingbo ^a,c  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^c HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

Atherosclerosis; Endothelial cells; Histone deacetylase 3; Proto oncogene proteins c akt

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; APOLIPOPROTEIN E; HISTONE DEACETYLASE 3; LENTIVIRUS VECTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SERINE; THREONINE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; AORTA GRAFT; APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; BLOOD FLOW; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; ENZYME STABILITY; GENE DELETION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; INTIMA; ISCHEMIA; ISOGRAFT; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; UMBILICAL VEIN; UPREGULATION; WESTERN BLOTTING;

ANIMALS; AORTA; APOLIPOPROTEINS E; APOPTOSIS; ATHEROSCLEROSIS; CELL SURVIVAL; CELLS, CULTURED; ENDOTHELIAL CELLS; HISTONE DEACETYLASES; HUMANS; LAC OPERON; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; PULSATILE FLOW; UMBILICAL VEINS;

EID: 74549187447     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.109.890491     Document Type: Article

References (40)

1. Gimbrone MA Jr, Nagel T, Topper JN. Biomechanical activation: an emerging paradigm in endothelial adhesion biology. J Clin Invest. 1997; 100:S61-S65. (Pubitemid 28009549)
2. Gimbrone MA Jr, Topper JN, Nagel T, Anderson KR, Garcia-Cardena G. Endothelial dysfunction, hemodynamic forces, and atherogenesis. Ann N Y Acad Sci. 2000;902:230-239.
3. Libby P. Inflammation in atherosclerosis. Nature. 2002;420:868-874.
4. Li YS, Haga JH, Chien S. Molecular basis of the effects of shear stress on vascular endothelial cells. J Biomech. 2005;38:1949-1971.
5. Foteinos G, Hu Y, Xiao Q, Metzler B, Xu Q. Rapid endothelial turnover in atherosclerosis-prone areas coincides with stem cell repair in apoli-poprotein E-deficient mice. Circulation. 2008;117:1856-1863.
6. Davies PF, Polacek DC, Handen JS, Helmke BP, DePaola N. A spatial approach to transcriptional profiling: mechanotransduction and the focal origin of atherosclerosis. Trends Biotechnol. 1999;17:347-351.
7. Hahn C, Schwartz MA. The role of cellular adaptation to mechanical forces in atherosclerosis. Arterioscler Thromb Vasc Biol. 2008;28: 2101-2107.
8. Rossig L, Urbich C, Bruhl T, Dernbach E, Heeschen C, Chavakis E, Sasaki K, Aicher D, Diehl F, Seeger F, Potente M, Aicher A, Zanetta L, Dejana E, Zeiher AM, Dimmeler S. Histone deacetylase activity is essential for the expression of HoxA9 and for endothelial commitment of progenitor cells. J Exp Med. 2005;201:1825-1835.
9. Guenther MG, Barak O, Lazar MA. The SMRT and N-CoR corepressors are activating cofactors for histone deacetylase 3. Mol Cell Biol. 2001; 21:6091-6101.
10. Longworth MS, Laimins LA. Histone deacetylase 3 localizes to the plasma membrane and is a substrate of Src. Oncogene. 2006;25: 4495-4500.
11. Bhaskara S, Chyla BJ, Amann JM, Knutson SK, Cortez D, Sun ZW, Hiebert SW. Deletion of histone deacetylase 3 reveals critical roles in S phase progression and DNA damage control. Mol Cell. 2008;30:61-72.
12. Xiao Q, Zeng L, Zhang Z, Margariti A, Ali ZA, Channon KM, Hu Y, Xu Q. 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.
13. 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.
14. Zeng L, Zhang Y, Chien S, Liu X, Shyy JY. The role of p53 deacetylation in p21Waf1 regulation by laminar flow. J Biol Chem. 2003;278: 24594-24599.
15. 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 U S A. 2009;106:8326-8331.
16. Hu Y, Davison F, Zhang ZG, Xu Q. Endothelial replacement and angio-genesis in arteriosclerotic lesions of allografts are contributed by circulating progenitor cells. Circulation. 2003;108:3122-3127.
17. Carracedo A, Pandolfi PP. The PTEN-PI3K pathway: of feedbacks and cross-talks. Oncogene. 2008;27:5527-5541.
18. Andrabi S, Gjoerup OV, Kean JA, Roberts TM, Schaffhausen B. Protein phosphatase 2A regulates life and death decisions via Akt in a context-dependent manner. Proc Natl Acad Sci U S A. 2007;104:19011-19016.
19. Hong K, Lou L, Gupta S, Ribeiro-Neto F, Altschuler DL. A novel Epac-Rap-PP2A signaling module controls cAMP-dependent Akt regulation. J Biol Chem. 2008;283:23129-23138.
20. Kennedy SG, Kandel ES, Cross TK, Hay N. Akt/Protein kinase B inhibits cell death by preventing the release of cytochrome c from mitochondria. Mol Cell Biol. 1999;19:5800-5810.
21. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell. 1997;91:231-241.
22. VanderLaan PA, Reardon CA, Getz GS. Site specificity of atherosclerosis: site-selective responses to atherosclerotic modulators. Arterioscler Thromb Vasc Biol. 2004;24:12-22.
23. Yang WM, Tsai SC, Wen YD, Fejer G, Seto E. Functional domains of histone deacetylase-3. J Biol Chem. 2002;277:9447-9454.
24. Yoon HG, Chan DW, Huang ZQ, Li J, Fondell JD, Qin J, Wong J. Purification and functional characterization of the human N-CoR complex: the roles of HDAC3, TBL1 and TBLR1. EMBO J. 2003;22: 1336-1346.
25. Weiss C, Schneider S, Wagner EF, Zhang X, Seto E, Bohmann D. JNK phosphorylation relieves HDAC3-dependent suppression of the transcrip-tional activity of c-Jun. EMBO J. 2003;22:3686-3695.
26. Zhang J, Kalkum M, Chait BT, Roeder RG. The N-CoR-HDAC3 nuclear receptor corepressor complex inhibits the JNK pathway through the integral subunit GPS2. Mol Cell. 2002;9:611-623.
27. Gloire G, Horion J, El Mjiyad N, Bex F, Chariot A, Dejardin E, Piette J. Promoter-dependent effect of IKKalpha on NF-kappaB/p65 DNA binding. J Biol Chem. 2007;282:21308-21318.
28. Ishii S, Kurasawa Y, Wong J, Yu-Lee LY. Histone deacetylase 3 localizes to the mitotic spindle and is required for kinetochore-microtubule attachment. Proc Natl Acad Sci U S A. 2008;105:4179-4184.
29. Escaffit F, Vaute O, Chevillard-Briet M, Segui B, Takami Y, Nakayama T, Trouche D. Cleavage and cytoplasmic relocalization of histone deacetylase 3 are important for apoptosis progression. Mol Cell Biol. 2007;27:554-567.
30. Takami Y, Nakayama T. N-terminal region, C-terminal region, nuclear export signal, and deacetylation activity of histone deacetylase-3 are essential for the viability of the DT40 chicken B cell line. J Biol Chem. 2000;275:16191-21201
31. Knutson SK, Chyla BJ, Amann JM, Bhaskara S, Huppert SS, Hiebert SW. Liver-specific deletion of histone deacetylase 3 disrupts metabolic tran-scriptional networks. EMBO J. 2008;27:1017-1028.
32. Montgomery RL, Potthoff MJ, Haberland M, Qi X, Matsuzaki S, Humphries KM, Richardson JA, Bassel-Duby R, Olson EN. Maintenance of cardiac energy metabolism by histone deacetylase 3 in mice. J Clin Invest. 2008;118:3588-3597.
33. Colussi C, Mozzetta C, Gurtner A, Illi B, Rosati J, Straino S, Ragone G, Pescatori M, Zaccagnini G, Antonini A, Minetti G, Martelli F, Piaggio G, Gallinari P, Steinkuhler C, Clementi E, Dell'Aversana C, Altucci L, Mai A, Capogrossi MC, Puri PL, Gaetano C. HDAC2 blockade by nitric oxide and histone deacetylase inhibitors reveals a common target in Duchenne muscular dystrophy treatment. Proc Natl Acad Sci U S A. 2008;105: 19183-19187.
34. Shiojima I, Walsh K. Regulation of cardiac growth and coronary angio-genesis by the Akt/PKB signaling pathway. Genes Dev. 2006;20: 3347-3365.
35. Plas DR, Talapatra S, Edinger AL, Rathmell JC, Thompson CB. Akt and Bcl-xL promote growth factor-independent survival through distinct effects on mitochondrial physiology. J Biol Chem. 2001;276: 12041-12048.
36. Plas DR, Thompson CB. Akt-dependent transformation: there is more to growth than just surviving. Oncogene. 2005;24:7435-7442.
37. Dje N'Guessan P, Riediger F, Vardarova K, Scharf S, Eitel J, Opitz B, Slevogt H, Weichert W, Hocke AC, Schmeck B, Suttorp N, Hippenstiel S. Statins control oxidized LDL-mediated histone modifications and gene expression in cultured human endothelial cells. Arterioscler Thromb Vasc Biol. 2009;29:380-386.
38. Xu X, Ha CH, Wong C, Wang W, Hausser A, Pfizenmaier K, Olson EN, McKinsey TA, Jin ZG. Angiotensin II stimulates protein kinase D-dependent histone deacetylase 5 phosphorylation and nuclear export leading to vascular smooth muscle cell hypertrophy. Arterioscler Thromb Vasc Biol. 2007;27:2355-2362.
39. Choi JH, Nam KH, Kim J, Baek MW, Park JE, Park HY, Kwon HJ, Kwon OS, Kim DY, Oh GT. Trichostatin A exacerbates atherosclerosis in low density lipoprotein receptor-deficient mice. Arterioscler Thromb Vasc Biol. 2005;25:2404-2409.
40. Passerini AG, Polacek DC, Shi C, Francesco NM, Manduchi E, Grant GR, Pritchard WF, Powell S, Chang GY, Stoeckert CJ Jr, Davies PF. Coexisting proinflammatory and antioxidative endothelial transcription profiles in a disturbed flow region of the adult porcine aorta. Proc Natl Acad Sci U S A. 2004;101:2482-2487.