Readers, writers, and erasers: Chromatin as the whiteboard of heart disease

Circulation Research

Volumn 116, Issue 7, 2015, Pages 1245-1253

  Gillette, Thomas G ^a,b   Hill, Joseph A ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Chromatin; Chromatin assembly and disassembly; Epigenomics

Indexed keywords

HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; HISTONE DEMETHYLASE; HISTONE METHYLTRANSFERASE; CARDIOTONIC AGENT; CHROMATIN; HISTONE; HISTONE DEACETYLASE INHIBITOR; HISTONE LYSINE METHYLTRANSFERASE; MULTIPROTEIN COMPLEX; NUCLEOSOME;

CELL DEATH; CELL STRESS; CELL SURVIVAL; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; DNA TRANSCRIPTION; GENE EXPRESSION; HEART DEVELOPMENT; HEART DISEASE; HEART MUSCLE ISCHEMIA; HEART VENTRICLE HYPERTROPHY; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HISTONE PHOSPHORYLATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; SUMOYLATION; TRANSCRIPTION ELONGATION; ACETYLATION; ANIMAL; CARDIOMEGALY; EMBRYOLOGY; FETUS HEART; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEART; HEART MUSCLE; METABOLISM; METHYLATION; NUCLEOSOME; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; RAT; ULTRASTRUCTURE;

ACETYLATION; ANIMALS; CARDIOMEGALY; CARDIOTONIC AGENTS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; EPIGENESIS, GENETIC; FETAL HEART; GENE EXPRESSION REGULATION; HEART; HEART DISEASES; HISTONE ACETYLTRANSFERASES; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HISTONE DEMETHYLASES; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; METHYLATION; MULTIPROTEIN COMPLEXES; MYOCARDIAL ISCHEMIA; MYOCARDIUM; NUCLEOSOMES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; RATS; TRANSCRIPTION, GENETIC;

EID: 84940079857     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.116.303630     Document Type: Review

References (96)

1. Rothbart SB, Strahl BD, Interpreting the language of histone and DNA modifications. Biochim Biophys Acta 2014; 1839: 627-643. doi: 10.1016/j.bbagrm.2014.03.001.
2. 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 U S A 1964 51 786 794
3. Brownell JE, Zhou J, Ranalli T, Kobayashi R, Edmondson DG, Roth SY, Allis CD, Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell 1996 84 843 851
4. Parthun MR, Widom J, Gottschling DE, The major cytoplasmic histone acetyltransferase in yeast: links to chromatin replication and histone metabolism. Cell 1996 87 85 94
5. Mizzen CA, Yang XJ, Kokubo T, Brownell JE, Bannister AJ, Owen-Hughes T, Workman J, Wang L, Berger SL, Kouzarides T, Nakatani Y, Allis CD, The TAF(II)250 subunit of TFIID has histone acetyltransferase activity. Cell 1996 87 1261 1270
6. Bannister AJ, Kouzarides T, The CBP co-activator is a histone acetyltransferase. Nature 1996; 384: 641-643. doi: 10.1038/384641a0.
7. Lee KK, Workman JL, Histone acetyltransferase complexes: one size doesn't fit all. Nat Rev Mol Cell Biol 2007; 8: 284-295. doi: 10.1038/nrm2145.
8. Yuan H, Marmorstein R, Histone acetyltransferases: rising ancient counterparts to protein kinases. Biopolymers 2013; 99: 98-111. doi: 10.1002/bip.22128.
9. Strahl BD, Ohba R, Cook RG, Allis CD, Methylation of histone H3 at lysine 4 is highly conserved and correlates with transcriptionally active nuclei in Tetrahymena. Proc Natl Acad Sci U S A 1999 96 14967 14972
10. Rea S, Eisenhaber F, O'Carroll D, Strahl BD, Sun ZW, Schmid M, Opravil S, Mechtler K, Ponting CP, Allis CD, Jenuwein T, Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 2000; 406: 593-599. doi: 10.1038/35020506.
11. Del Rizzo PA, Trievel RC, Molecular basis for substrate recognition by lysine methyltransferases and demethylases. Biochim Biophys Acta 2014 1404 1415. doi: 10.1016/j.bbagrm.2014.06.008.
12. Lyons DB, Lomvardas S, Repressive histone methylation: a case study in deterministic versus stochastic gene regulation. Biochim Biophys Acta 2014; 1839: 1373-1384. doi: 10.1016/j.bbagrm.2014.05.010.
13. Taunton J, Hassig CA, Schreiber SL, A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p. Science 1996 272 408 411
14. Gregoretti IV, Lee YM, Goodson HV, Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J Mol Biol 2004; 338: 17-31. doi: 10.1016/j.jmb.2004.02.006.
15. Xie M, Hill JA, HDAC-dependent ventricular remodeling. Trends Cardiovasc Med 2013; 23: 229-235. doi: 10.1016/j.tcm.2012.12.006.
16. Falkenberg KJ, Johnstone RW, Histone deacetylases and their inhibitors in cancer, neurological diseases and immune disorders. Nat Rev Drug Discov 2014; 13: 673-691. doi: 10.1038/nrd4360.
17. Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA, Shi Y, Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004; 119: 941-953. doi: 10.1016/j.cell.2004.12.012.
18. Thinnes CC, England KS, Kawamura A, Chowdhury R, Schofield CJ, Hopkinson RJ, Targeting histone lysine demethylases-progress, challenges, and the future. Biochim Biophys Acta 2014; 1839: 1416-1432. doi: 10.1016/j.bbagrm.2014.05.009.
19. Yun M, Wu J, Workman JL, Li B, Readers of histone modifications. Cell Res 2011; 21: 564-578. doi: 10.1038/cr.2011.42.
20. Awad S, Hassan AH, The Swi2/Snf2 bromodomain is important for the full binding and remodeling activity of the SWI/SNF complex on H3- and H4-acetylated nucleosomes. Ann N Y Acad Sci 2008; 1138: 366-375. doi: 10.1196/annals.1414.038.
21. Filippakopoulos P, Knapp S, Targeting bromodomains: epigenetic readers of lysine acetylation. Nat Rev Drug Discov 2014; 13: 337-356. doi: 10.1038/nrd4286.
22. Shi J, Vakoc CR, The mechanisms behind the therapeutic activity of BET bromodomain inhibition. Mol Cell 2014; 54: 728-736. doi: 10.1016/j.molcel.2014.05.016.
23. Han P, Hang CT, Yang J, Chang CP, Chromatin remodeling in cardiovascular development and physiology. Circ Res 2011; 108: 378-396. doi: 10.1161/CIRCRESAHA.110.224287.
24. Lickert H, Takeuchi JK, Von Both I, Walls JR, McAuliffe F, Adamson SL, Henkelman RM, Wrana JL, Rossant J, Bruneau BG, Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature 2004; 432: 107-112. doi: 10.1038/nature03071.
25. Wang Z, Zhai W, Richardson JA, Olson EN, Meneses JJ, Firpo MT, Kang C, Skarnes WC, Tjian R, Polybromo protein BAF180 functions in mammalian cardiac chamber maturation. Genes Dev 2004; 18: 3106-3116. doi: 10.1101/gad.1238104.
26. Hang CT, Yang J, Han P, Cheng HL, Shang C, Ashley E, Zhou B, Chang CP, Chromatin regulation by Brg1 underlies heart muscle development and disease. Nature 2010; 466: 62-67. doi: 10.1038/nature09130.
27. Singh AP, Archer TK, Analysis of the SWI/SNF chromatin-remodeling complex during early heart development and BAF250a repression cardiac gene transcription during P19 cell differentiation. Nucleic Acids Res 2014; 42: 2958-2975. doi: 10.1093/nar/gkt1232.
28. Yao TP, Oh SP, Fuchs M, Zhou ND, Ch'ng LE, Newsome D, Bronson RT, Li E, Livingston DM, Eckner R, Gene dosage-dependent embryonic development and proliferation defects in mice lacking the transcriptional integrator p300. Cell 1998 93 361 372
29. Shikama N, Lutz W, Kretzschmar R, Sauter N, Roth JF, Marino S, Wittwer J, Scheidweiler A, Eckner R, Essential function of p300 acetyltransferase activity in heart, lung and small intestine formation. Embo J 2003; 22: 5175-5185. doi: 10.1093/emboj/cdg502.
30. 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. doi: 10.1172/JCI35847.
31. Montgomery RL, Davis CA, Potthoff MJ, Haberland M, Fielitz J, Qi X, Hill JA, Richardson JA, Olson EN, Histone deacetylases 1 and 2 redundantly regulate cardiac morphogenesis, growth, and contractility. Genes Dev 2007; 21: 1790-1802. doi: 10.1101/gad.1563807.
32. Chang S, McKinsey TA, Zhang CL, Richardson JA, Hill JA, Olson EN, Histone deacetylases 5 and 9 govern responsiveness of the heart to a subset of stress signals and play redundant roles in heart development. Mol Cell Biol 2004; 24: 8467-8476. doi: 10.1128/MCB.24.19.8467-8476.2004.
33. Cheng HL, Mostoslavsky R, Saito S, Manis JP, Gu Y, Patel P, Bronson R, Appella E, Alt FW, Chua KF, Developmental defects and p53 hyperacetylation in Sir2 homolog (SIRT1)-deficient mice. Proc Natl Acad Sci U S A 2003; 100: 10794-10799. doi: 10.1073/pnas.1934713100.
34. Gottlieb PD, Pierce SA, Sims RJ, Yamagishi H, Weihe EK, Harriss JV, Maika SD, Kuziel WA, King HL, Olson EN, Nakagawa O, Srivastava D, Bop encodes a muscle-restricted protein containing MYND and SET domains and is essential for cardiac differentiation and morphogenesis. Nat Genet 2002; 31: 25-32. doi: 10.1038/ng866.
35. Nimura K, Ura K, Shiratori H, Ikawa M, Okabe M, Schwartz RJ, Kaneda Y, A histone H3 lysine 36 trimethyltransferase links Nkx2-5 to Wolf-Hirschhorn syndrome. Nature 2009; 460: 287-291. doi: 10.1038/nature08086.
36. Takeuchi T, Kojima M, Nakajima K, Kondo S, jumonji gene is essential for the neurulation and cardiac development of mouse embryos with a C3H/He background. Mech Dev 1999 86 29 38
37. Ohtani K, Zhao C, Dobreva G, Manavski Y, Kluge B, Braun T, Rieger MA, Zeiher AM, Dimmeler S, Jmjd3 controls mesodermal and cardiovascular differentiation of embryonic stem cells. Circ Res 2013; 113: 856-862. doi: 10.1161/CIRCRESAHA.113.302035.
38. Lee S, Lee JW, Lee SK, UTX, a histone H3-lysine 27 demethylase, acts as a critical switch to activate the cardiac developmental program. Dev Cell 2012; 22: 25-37. doi: 10.1016/j.devcel.2011.11.009.
39. Hill JA, Olson EN, Cardiac plasticity. N Engl J Med 2008; 358: 1370-1380. doi: 10.1056/NEJMra072139.
40. Schiattarella GG, Hill JA, Inhibition of hypertrophy is a good therapeutic strategy in ventricular pressure overload. Circulation 2015
41. Burchfield JS, Xie M, Hill JA, Pathological ventricular remodeling: mechanisms: part 1 of 2. Circulation 2013; 128: 388-400. doi: 10.1161/CIRCULATIONAHA.113.001878.
42. Han P, Li W, Lin CH, A long noncoding RNA protects the heart from pathological hypertrophy. Nature 2014 514 102 106
43. Krenz M, Robbins J, Impact of beta-myosin heavy chain expression on cardiac function during stress. J Am Coll Cardiol 2004; 44: 2390-2397. doi: 10.1016/j.jacc.2004.09.044.
44. Herron TJ, McDonald KS, Small amounts of alpha-myosin heavy chain isoform expression significantly increase power output of rat cardiac myocyte fragments. Circ Res 2002 90 1150 1152
45. Razeghi P, Young ME, Alcorn JL, Moravec CS, Frazier OH, Taegtmeyer H, Metabolic gene expression in fetal and failing human heart. Circulation 2001 104 2923 2931
46. Zhang CL, McKinsey TA, Chang S, Antos CL, Hill JA, Olson EN, Class II histone deacetylases act as signal-responsive repressors of cardiac hypertrophy. Cell 2002 110 479 488
47. Black BL, Cripps RM, Rosenthal N, Harvey RP, Myocyte enhancer factor 2 transcription factors in heart development and disease. In: Heart Development and Regeneration 2010 Oxford Elsevier Inc, Academic Press 673 699
48. Molkentin JD, Black BL, Martin JF, Olson EN, Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell 1995 83 1125 1136
49. Naya FJ, Black BL, Wu H, Bassel-Duby R, Richardson JA, Hill JA, Olson EN, Mitochondrial deficiency and cardiac sudden death in mice lacking the MEF2A transcription factor. Nat Med 2002; 8: 1303-1309. doi: 10.1038/nm789.
50. Kim Y, Phan D, van Rooij E, Wang DZ, McAnally J, Qi X, Richardson JA, Hill JA, Bassel-Duby R, Olson EN, The MEF2D transcription factor mediates stress-dependent cardiac remodeling in mice. J Clin Invest 2008; 118: 124-132. doi: 10.1172/JCI33255.
51. Lu J, McKinsey TA, Nicol RL, Olson EN, Signal-dependent activation of the MEF2 transcription factor by dissociation from histone deacetylases. Proc Natl Acad Sci U S A 2000; 97: 4070-4075. doi: 10.1073/pnas.080064097.
52. Antos CL, McKinsey TA, Dreitz M, Hollingsworth LM, Zhang CL, Schreiber K, Rindt H, Gorczynski RJ, Olson EN, Dose-dependent blockade to cardiomyocyte hypertrophy by histone deacetylase inhibitors. J Biol Chem 2003; 278: 28930-28937. doi: 10.1074/jbc.M303113200.
53. Kong Y, Tannous P, Lu G, Berenji K, Rothermel BA, Olson EN, Hill JA, Suppression of class I and II histone deacetylases blunts pressure-overload cardiac hypertrophy. Circulation 2006; 113: 2579-2588. doi: 10.1161/CIRCULATIONAHA.106.625467.
54. Kee HJ, Sohn IS, Nam KI, Park JE, Qian YR, Yin Z, Ahn Y, Jeong MH, Bang YJ, Kim N, Kim JK, Kim KK, Epstein JA, Kook H, Inhibition of histone deacetylation blocks cardiac hypertrophy induced by angiotensin II infusion and aortic banding. Circulation 2006; 113: 51-59. doi: 10.1161/CIRCULATIONAHA.105.559724.
55. Gallo P, Latronico MV, Gallo P, Grimaldi S, Borgia F, Todaro M, Jones P, Gallinari P, De Francesco R, Ciliberto G, Steinkühler C, Esposito G, Condorelli G, Inhibition of class I histone deacetylase with an apicidin derivative prevents cardiac hypertrophy and failure. Cardiovasc Res 2008; 80: 416-424. doi: 10.1093/cvr/cvn215.
56. Cao DJ, Wang ZV, Battiprolu PK, Jiang N, Morales CR, Kong Y, Rothermel BA, Gillette TG, Hill JA, Histone deacetylase (HDAC) inhibitors attenuate cardiac hypertrophy by suppressing autophagy. Proc Natl Acad Sci U S A 2011; 108: 4123-4128. doi: 10.1073/pnas.1015081108.
57. Fischle W, Dequiedt F, Hendzel MJ, Guenther MG, Lazar MA, Voelter W, Verdin E, Enzymatic activity associated with class II HDACs is dependent on a multiprotein complex containing HDAC3 and SMRT/N-CoR. Mol Cell 2002 9 45 57
58. Eom GH, Nam YS, Oh JG, Choe N, Min HK, Yoo EK, Kang G, Nguyen VH, Min JJ, Kim JK, Lee IK, Bassel-Duby R, Olson EN, Park WJ, Kook H, Regulation of acetylation of histone deacetylase 2 by p300/CBP-associated factor/histone deacetylase 5 in the development of cardiac hypertrophy. Circ Res 2014; 114: 1133-1143. doi: 10.1161/CIRCRESAHA.114.303429.
59. Trivedi CM, Luo Y, Yin Z, Zhang M, Zhu W, Wang T, Floss T, Goettlicher M, Noppinger PR, Wurst W, Ferrari VA, Abrams CS, Gruber PJ, Epstein JA, HDAC2 regulates the cardiac hypertrophic response by modulating Gsk3 beta activity. Nat Med 2007; 13: 324-331. doi: 10.1038/nm1552.
60. Sun Z, Singh N, Mullican SE, Everett LJ, Li L, Yuan L, Liu X, Epstein JA, Lazar MA, Diet-induced lethality due to deletion of the HDAC3 gene in heart and skeletal muscle. J Biol Chem 2011; 286: 33301-33309. doi: 10.1074/jbc.M111.277707.
61. Lavandero S, Chiong M, Rothermel BA, Hill JA, Autophagy in cardiovascular biology. J Clin Invest 2015; 125: 55-64. doi: 10.1172/JCI73943.
62. Blakeslee WW, Wysoczynski CL, Fritz KS, Nyborg JK, Churchill ME, McKinsey TA, Class I HDAC inhibition stimulates cardiac protein SUMOylation through a post-translational mechanism. Cell Signal 2014; 26: 2912-2920. doi: 10.1016/j.cellsig.2014.09.005.
63. Gusterson RJ, Jazrawi E, Adcock IM, Latchman DS, The transcriptional co-activators CREB-binding protein (CBP) and p300 play a critical role in cardiac hypertrophy that is dependent on their histone acetyltransferase activity. J Biol Chem 2003; 278: 6838-6847. doi: 10.1074/jbc.M211762200.
64. Dawson MA, Kouzarides T, Huntly BJ, Targeting epigenetic readers in cancer. N Engl J Med 2012; 367: 647-657. doi: 10.1056/NEJMra1112635.
65. Anand P, Brown JD, Lin CY, Qi J, Zhang R, Artero PC, Alaiti MA, Bullard J, Alazem K, Margulies KB, Cappola TP, Lemieux M, Plutzky J, Bradner JE, Haldar SM, BET bromodomains mediate transcriptional pause release in heart failure. Cell 2013; 154: 569-582. doi: 10.1016/j.cell.2013.07.013.
66. Spiltoir JI, Stratton MS, Cavasin MA, Demos-Davies K, Reid BG, Qi J, Bradner JE, McKinsey TA, BET acetyl-lysine binding proteins control pathological cardiac hypertrophy. J Mol Cell Cardiol 2013; 63: 175-179. doi: 10.1016/j.yjmcc.2013.07.017.
67. Papait R, Cattaneo P, Kunderfranco P, Greco C, Carullo P, Guffanti A, Viganò V, Stirparo GG, Latronico MV, Hasenfuss G, Chen J, Condorelli G, Genome-wide analysis of histone marks identifying an epigenetic signature of promoters and enhancers underlying cardiac hypertrophy. Proc Natl Acad Sci U S A 2013; 110: 20164-20169. doi: 10.1073/pnas.1315155110.
68. Movassagh M, Choy MK, Knowles DA, Cordeddu L, Haider S, Down T, Siggens L, Vujic A, Simeoni I, Penkett C, Goddard M, Lio P, Bennett MR, Foo RS, Distinct epigenomic features in end-stage failing human hearts. Circulation 2011; 124: 2411-2422. doi: 10.1161/CIRCULATIONAHA.111.040071.
69. Delgado-Olguín P, Huang Y, Li X, Christodoulou D, Seidman CE, Seidman JG, Tarakhovsky A, Bruneau BG, Epigenetic repression of cardiac progenitor gene expression by Ezh2 is required for postnatal cardiac homeostasis. Nat Genet 2012; 44: 343-347. doi: 10.1038/ng.1068.
70. Nguyen AT, Xiao B, Neppl RL, Kallin EM, Li J, Chen T, Wang DZ, Xiao X, Zhang Y, DOT1L regulates dystrophin expression and is critical for cardiac function. Genes Dev 2011; 25: 263-274. doi: 10.1101/gad.2018511.
71. Maeda M, Biro S, Kamogawa Y, Hirakawa T, Setoguchi M, Tei C, Dystrophin upregulation in pressure-overloaded cardiac hypertrophy in rats. Cell Motil Cytoskeleton 2003; 55: 26-35. doi: 10.1002/cm.10110.
72. Kamogawa Y, Biro S, Maeda M, Setoguchi M, Hirakawa T, Yoshida H, Tei C, Dystrophin-deficient myocardium is vulnerable to pressure overload in vivo. Cardiovasc Res 2001 50 509 515
73. Gray SG, Iglesias AH, Lizcano F, Villanueva R, Camelo S, Jingu H, Teh BT, Koibuchi N, Chin WW, Kokkotou E, Dangond F, Functional characterization of JMJD2A, a histone deacetylase- and retinoblastoma-binding protein. J Biol Chem 2005; 280: 28507-28518. doi: 10.1074/jbc.M413687200.
74. Shin S, Janknecht R, Activation of androgen receptor by histone demethylases JMJD2A and JMJD2D. Biochem Biophys Res Commun 2007; 359: 742-746. doi: 10.1016/j.bbrc.2007.05.179.
75. Zhang QJ, Chen HZ, Wang L, Liu DP, Hill JA, Liu ZP, The histone trimethyllysine demethylase JMJD2A promotes cardiac hypertrophy in response to hypertrophic stimuli in mice. J Clin Invest 2011; 121: 2447-2456. doi: 10.1172/JCI46277.
76. Hohl M, Wagner M, Reil JC, Müller SA, Tauchnitz M, Zimmer AM, Lehmann LH, Thiel G, Böhm M, Backs J, Maack C, HDAC4 controls histone methylation in response to elevated cardiac load. J Clin Invest 2013; 123: 1359-1370. doi: 10.1172/JCI61084.
77. Backs J, Song K, Bezprozvannaya S, Chang S, Olson EN, CaM kinase II selectively signals to histone deacetylase 4 during cardiomyocyte hypertrophy. J Clin Invest 2006; 116: 1853-1864. doi: 10.1172/JCI27438.
78. Awad S, Al-Haffar KM, Marashly Q, Quijada P, Kunhi M, Al-Yacoub N, Wade FS, Mohammed SF, Al-Dayel F, Sutherland G, Assiri A, Sussman M, Bers D, Al-Habeeb W, Poizat C, Control of histone H3 phosphorylation by CaMKIIδ in response to haemodynamic cardiac stress. J Pathol 2015; 235: 606-618. doi: 10.1002/path.4489.
79. Awad S, Kunhi M, Little GH, Bai Y, An W, Bers D, Kedes L, Poizat C, Nuclear CaMKII enhances histone H3 phosphorylation and remodels chromatin during cardiac hypertrophy. Nucleic Acids Res 2013; 41: 7656-7672. doi: 10.1093/nar/gkt500.
80. Wang Z, Zang C, Cui K, Schones DE, Barski A, Peng W, Zhao K, Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 2009; 138: 1019-1031. doi: 10.1016/j.cell.2009.06.049.
81. Chiang CM, Brd4 engagement from chromatin targeting to transcriptional regulation: selective contact with acetylated histone H3 and H4. F1000 Biol Rep 2009 1 98. doi: 10.3410/B1-98.
82. Ai N, Hu X, Ding F, Yu B, Wang H, Lu X, Zhang K, Li Y, Han A, Lin W, Liu R, Chen R, Signal-induced Brd4 release from chromatin is essential for its role transition from chromatin targeting to transcriptional regulation. Nucleic Acids Res 2011; 39: 9592-9604. doi: 10.1093/nar/gkr698.
83. Lee TM, Lin MS, Chang NC, Inhibition of histone deacetylase on ventricular remodeling in infarcted rats. Am J Physiol Heart Circ Physiol 2007 293 H968 H977. doi: 10.1152/ajpheart.00891.2006.
84. Granger A, Abdullah I, Huebner F, Stout A, Wang T, Huebner T, Epstein JA, Gruber PJ, Histone deacetylase inhibition reduces myocardial ischemia-reperfusion injury in mice. FASEB J 2008; 22: 3549-3560. doi: 10.1096/fj.08-108548.
85. Xie M, Kong Y, Tan W, Histone deacetylase inhibition blunts ischemia/reperfusion injury by inducing cardiomyocyte autophagy. Circulation 2014 129 1139 1151
86. Williams SM, Golden-Mason L, Ferguson BS, Schuetze KB, Cavasin MA, Demos-Davies K, Yeager ME, Stenmark KR, McKinsey TA, Class I HDACs regulate angiotensin II-dependent cardiac fibrosis via fibroblasts and circulating fibrocytes. J Mol Cell Cardiol 2014; 67: 112-125. doi: 10.1016/j.yjmcc.2013.12.013.
87. McKinsey TA, Targeting inflammation in heart failure with histone deacetylase inhibitors. Mol Med 2011; 17: 434-441. doi: 10.2119/molmed.2011.00022.
88. Ma X, Liu H, Foyil SR, Godar RJ, Weinheimer CJ, Hill JA, Diwan A, Impaired autophagosome clearance contributes to cardiomyocyte death in ischemia/reperfusion injury. Circulation 2012; 125: 3170-3181. doi: 10.1161/CIRCULATIONAHA.111.041814.
89. Ma X, Liu H, Foyil SR, Godar RJ, Weinheimer CJ, Diwan A, Autophagy is impaired in cardiac ischemia-reperfusion injury. Autophagy 2012; 8: 1394-1396. doi: 10.4161/auto.21036.
90. Bánréti A, Sass M, Graba Y, The emerging role of acetylation in the regulation of autophagy. Autophagy 2013; 9: 819-829. doi: 10.4161/auto.23908.
91. Gibson CL, Murphy SP, Benefits of histone deacetylase inhibitors for acute brain injury: a systematic review of animal studies. J Neurochem 2010; 115: 806-813. doi: 10.1111/j.1471-4159.2010.06993.x.
92. Yang B, Yang J, Bai J, Pu P, Liu J, Wang F, Ruan B, Suv39h1 protects from myocardial ischemia-reperfusion injury in diabetic rats. Cell Physiol Biochem 2014; 33: 1176-1185. doi: 10.1159/000358686.
93. Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, Wood JG, Zipkin RE, Chung P, Kisielewski A, Zhang LL, Scherer B, Sinclair DA, Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 2003; 425: 191-196. doi: 10.1038/nature01960.
94. Michan S, Sinclair D, Sirtuins in mammals: insights into their biological function. Biochem J 2007; 404: 1-13. doi: 10.1042/BJ20070140.
95. Hsu CP, Zhai P, Yamamoto T, Maejima Y, Matsushima S, Hariharan N, Shao D, Takagi H, Oka S, Sadoshima J, Silent information regulator 1 protects the heart from ischemia/reperfusion. Circulation 2010; 122: 2170-2182. doi: 10.1161/CIRCULATIONAHA.110.958033.
96. Oka S, Alcendor R, Zhai P, Park JY, Shao D, Cho J, Yamamoto T, Tian B, Sadoshima J, PPARα-Sirt1 complex mediates cardiac hypertrophy and failure through suppression of the ERR transcriptional pathway. Cell Metab 2011; 14: 598-611. doi: 10.1016/j.cmet.2011.10.001.