Chromatin modifications remodel cardiac gene expression

Tabibiazar, 2003, Transcriptional profiling of the heart reveals chamber-specific gene expression patterns, Circ Res, 93, 1193, 10.1161/01.RES.0000103171.42654.DD

Bruneau, 1999, Chamber-specific cardiac expression of Tbx5 and heart defects in Holt–Oram syndrome, Dev Biol, 211, 100, 10.1006/dbio.1999.9298

Bruneau, 2002, Transcriptional regulation of vertebrate cardiac morphogenesis, Circ Res, 90, 509, 10.1161/01.RES.0000013072.51957.B7

Akazawa, 2005, Cardiac transcription factor Csx/Nkx2-5: its role in cardiac development and diseases, Pharmacol Ther, 107, 252, 10.1016/j.pharmthera.2005.03.005

Anversa, 2006, Cardiac regeneration, J Am Coll Cardiol, 47, 1769, 10.1016/j.jacc.2006.02.003

He, 2011, Co-occupancy by multiple cardiac transcription factors identifies transcriptional enhancers active in heart, Proc Natl Acad Sci USA, 108, 5632, 10.1073/pnas.1016959108

Wolffe, 1994, The transcription of chromatin templates, Curr Opin Genet Dev, 4, 245, 10.1016/S0959-437X(05)80051-6

Jenuwein, 2001, Translating the histone code, Science, 293, 1074, 10.1126/science.1063127

Stein, 2011, Loss of H3K4 methylation destabilizes gene expression patterns and physiological functions in adult murine cardiomyocytes, J Clin Invest, 121, 2641, 10.1172/JCI44641

Delgado-Olguin, 2012, Epigenetic repression of cardiac progenitor gene expression by Ezh2 is required for postnatal cardiac homeostasis, Nat Genet, 44, 343, 10.1038/ng.1068

Zaidi, 2013, De novo mutations in histone-modifying genes in congenital heart disease, Nature, 498, 220, 10.1038/nature12141

Chang, 2011, Cardiac genes show contextual SWI/SNF interactions with distinguishable gene activities, Epigenetics, 6, 760, 10.4161/epi.6.6.16007

Hang, 2010, Chromatin regulation by Brg1 underlies heart muscle development and disease, Nature, 466, 62, 10.1038/nature09130

Matsuoka, 2014, Noninvasive and quantitative live imaging reveals a potential stress-responsive enhancer in the failing heart, FASEB J, 28, 1870, 10.1096/fj.13-245522

Schonrock, 2012, Long noncoding RNAs in cardiac development and pathophysiology, Circ Res, 111, 1349, 10.1161/CIRCRESAHA.112.268953

Mathiyalagan, 2013, Interplay of chromatin modifications and non-coding RNAs in the heart, Epigenetics, 9, 101, 10.4161/epi.26405

Mathiyalagan, 2014, The primary microRNA-208b interacts with polycomb-group protein, Ezh2, to regulate gene expression in the heart, Nucleic Acids Res, 42, 790, 10.1093/nar/gkt896

Klattenhoff, 2013, Braveheart, a long noncoding RNA required for cardiovascular lineage commitment, Cell, 152, 570, 10.1016/j.cell.2013.01.003

Grote, 2013, The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse, Dev Cell, 24, 206, 10.1016/j.devcel.2012.12.012

Kehat, 2010, Molecular pathways underlying cardiac remodeling during pathophysiological stimulation, Circulation, 122, 2727, 10.1161/CIRCULATIONAHA.110.942268

Cohn, 2000, Cardiac remodeling—concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling. Behalf of an International Forum on Cardiac Remodeling, J Am Coll Cardiol, 35, 569, 10.1016/S0735-1097(99)00630-0

Gardin, 2004, Left ventricular hypertrophy: the next treatable, silent killer?, JAMA, 292, 2396, 10.1001/jama.292.19.2396

Frey, 2003, Cardiac hypertrophy: the good, the bad, and the ugly, Annu Rev Physiol, 65, 45, 10.1146/annurev.physiol.65.092101.142243

Li, 2008, Curcumin prevents and reverses murine cardiac hypertrophy, J Clin Invest, 118, 879

Heineke, 2006, Regulation of cardiac hypertrophy by intracellular signalling pathways, Nat Rev Mol Cell Biol, 7, 589, 10.1038/nrm1983

Insel, 1993, Beta-adrenergic receptors in heart failure, J Clin Invest, 92, 2564, 10.1172/JCI116867

Sipido, 2002, Altered Na/Ca exchange activity in cardiac hypertrophy and heart failure: a new target for therapy?, Cardiovasc Res, 53, 782, 10.1016/S0008-6363(01)00470-9

Han, 2011, Chromatin remodeling in cardiovascular development and physiology, Circ Res, 108, 378, 10.1161/CIRCRESAHA.110.224287

McKinsey, 2012, Therapeutic potential for HDAC inhibitors in the heart, Annu Rev Pharmacol Toxicol, 52, 303, 10.1146/annurev-pharmtox-010611-134712

Backs, 2006, Control of cardiac growth by histone acetylation/deacetylation, Circ Res, 98, 15, 10.1161/01.RES.0000197782.21444.8f

Movassagh, 2011, Distinct epigenomic features in end-stage failing human hearts, Circulation, 124, 2411, 10.1161/CIRCULATIONAHA.111.040071

Kaneda, 2009, Genome-wide histone methylation profile for heart failure, Genes Cells, 14, 69, 10.1111/j.1365-2443.2008.01252.x

McKinsey, 2002, MEF2: a calcium-dependent regulator of cell division, differentiation and death, Trends Biochem Sci, 27, 40, 10.1016/S0968-0004(01)02031-X

McKinsey, 2000, Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation, Nature, 408, 106, 10.1038/35040593

Dai, 2001, p300 Functions as a coactivator of transcription factor GATA-4, J Biol Chem, 276, 37178, 10.1074/jbc.M103731200

Saha, 2006, Chromatin remodelling: the industrial revolution of DNA around histones, Nat Rev Mol Cell Biol, 7, 437, 10.1038/nrm1945

Clapier, 2009, The biology of chromatin remodeling complexes, Annu Rev Biochem, 78, 273, 10.1146/annurev.biochem.77.062706.153223

Campos, 2009, Histones: annotating chromatin, Annu Rev Genet, 43, 559, 10.1146/annurev.genet.032608.103928

Takeuchi, 2011, Chromatin remodelling complex dosage modulates transcription factor function in heart development, Nat Commun, 2, 187, 10.1038/ncomms1187

Gupta, 2007, Factors controlling cardiac myosin-isoform shift during hypertrophy and heart failure, J Mol Cell Cardiol, 43, 388, 10.1016/j.yjmcc.2007.07.045

Lai, 2012, Maintenance of adult cardiac function requires the chromatin factor Asxl2, J Mol Cell Cardiol, 53, 734, 10.1016/j.yjmcc.2012.08.014

Wolffe, 1989, Initiation of transcription on nucleosomal templates, Proc Natl Acad Sci USA, 86, 9817, 10.1073/pnas.86.24.9817

Sayed, 2013, Transcriptional regulation patterns revealed by high resolution chromatin immunoprecipitation during cardiac hypertrophy, J Biol Chem, 288, 2546, 10.1074/jbc.M112.429449

Schlesinger, 2011, The cardiac transcription network modulated by Gata4, Mef2a, Nkx2.5, Srf, histone modifications, and microRNAs, PLoS Genet, 7, e1001313, 10.1371/journal.pgen.1001313

Papait, 2013, Genome-wide analysis of histone marks identifying an epigenetic signature of promoters and enhancers underlying cardiac hypertrophy, Proc Natl Acad Sci USA, 110, 20164, 10.1073/pnas.1315155110

Mathiyalagan, 2010, Cardiac ventricular chambers are epigenetically distinguishable, Cell Cycle, 9, 612, 10.4161/cc.9.3.10612

Yao, 1998, Gene dosage-dependent embryonic development and proliferation defects in mice lacking the transcriptional integrator p300, Cell, 93, 361, 10.1016/S0092-8674(00)81165-4

Gusterson, 2003, 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, 278, 6838, 10.1074/jbc.M211762200

Yanazume, 2003, Cardiac p300 is involved in myocyte growth with decompensated heart failure, Mol Cell Biol, 23, 3593, 10.1128/MCB.23.10.3593-3606.2003

Slepak, 2001, Control of cardiac-specific transcription by p300 through myocyte enhancer factor-2D, J Biol Chem, 276, 7575, 10.1074/jbc.M004625200

Sartorelli, 1997, Molecular mechanisms of myogenic coactivation by p300: direct interaction with the activation domain of MyoD and with the MADS box of MEF2C, Mol Cell Biol, 17, 1010, 10.1128/MCB.17.2.1010

Chandrasekaran, 2009, Histone deacetylases facilitate sodium/calcium exchanger up-regulation in adult cardiomyocytes, FASEB J, 23, 3851, 10.1096/fj.09-132415

Sunagawa, 2010, Cyclin-dependent kinase-9 is a component of the p300/GATA4 complex required for phenylephrine-induced hypertrophy in cardiomyocytes, J Biol Chem, 285, 9556, 10.1074/jbc.M109.070458

Morimoto, 2008, The dietary compound curcumin inhibits p300 histone acetyltransferase activity and prevents heart failure in rats, J Clin Invest, 118, 868

Sunagawa, 2011, A natural p300-specific histone acetyltransferase inhibitor, curcumin, in addition to angiotensin-converting enzyme inhibitor, exerts beneficial effects on left ventricular systolic function after myocardial infarction in rats, Circ J, 75, 2151, 10.1253/circj.CJ-10-1072

McKinsey, 2007, Small-molecule therapies for cardiac hypertrophy: moving beneath the cell surface, Nat Rev Drug Discov, 6, 617, 10.1038/nrd2193

Kee, 2006, Inhibition of histone deacetylation blocks cardiac hypertrophy induced by angiotensin II infusion and aortic banding, Circulation, 113, 51, 10.1161/CIRCULATIONAHA.105.559724

Glenn, 2009, Endothelin-stimulated human B-type natriuretic peptide gene expression is mediated by Yin Yang 1 in association with histone deacetylase 2, Hypertension, 53, 549, 10.1161/HYPERTENSIONAHA.108.125088

Choudhary, 2009, Lysine acetylation targets protein complexes and co-regulates major cellular functions, Science, 325, 834, 10.1126/science.1175371

de Ruijter, 2003, Histone deacetylases (HDACs): characterization of the classical HDAC family, Biochem J, 370, 737, 10.1042/bj20021321

Marks, 2009, Histone deacetylase inhibitors: potential in cancer therapy, J Cell Biochem, 107, 600, 10.1002/jcb.22185

Gregoretti, 2004, Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis, J Mol Biol, 338, 17, 10.1016/j.jmb.2004.02.006

Dokmanovic, 2007, Histone deacetylase inhibitors: overview and perspectives, Mol Cancer Res, 5, 981, 10.1158/1541-7786.MCR-07-0324

Kee, 2011, Roles and targets of class I and IIa histone deacetylases in cardiac hypertrophy, J Biomed Biotechnol, 2011, 928326, 10.1155/2011/928326

Chang, 2004, 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, 24, 8467, 10.1128/MCB.24.19.8467-8476.2004

Zhang, 2002, Class II histone deacetylases act as signal-responsive repressors of cardiac hypertrophy, Cell, 110, 479, 10.1016/S0092-8674(02)00861-9

Antos, 2003, Dose-dependent blockade to cardiomyocyte hypertrophy by histone deacetylase inhibitors, J Biol Chem, 278, 28930, 10.1074/jbc.M303113200

Cao, 2011, Histone deacetylase (HDAC) inhibitors attenuate cardiac hypertrophy by suppressing autophagy, Proc Natl Acad Sci USA, 108, 4123, 10.1073/pnas.1015081108

Kee, 2009, Kruppel-like factor 4 mediates histone deacetylase inhibitor-induced prevention of cardiac hypertrophy, J Mol Cell Cardiol, 47, 770, 10.1016/j.yjmcc.2009.08.022

Trivedi, 2007, Hdac2 regulates the cardiac hypertrophic response by modulating Gsk3 beta activity, Nat Med, 13, 324, 10.1038/nm1552

Kee, 2008, Activation of histone deacetylase 2 by inducible heat shock protein 70 in cardiac hypertrophy, Circ Res, 103, 1259, 10.1161/01.RES.0000338570.27156.84

Zhu, 2010, Histone deacetylase-3 activation promotes tumor necrosis factor-alpha (TNF-alpha) expression in cardiomyocytes during lipopolysaccharide stimulation, J Biol Chem, 285, 9429, 10.1074/jbc.M109.071274

Hohl, 2013, HDAC4 controls histone methylation in response to elevated cardiac load, J Clin Invest, 123, 1359, 10.1172/JCI61084

Granger, 2008, Histone deacetylase inhibition reduces myocardial ischemia-reperfusion injury in mice, FASEB J, 22, 3549, 10.1096/fj.08-108548

Sucharov, 2008, YY1 protects cardiac myocytes from pathologic hypertrophy by interacting with HDAC5, Mol Biol Cell, 19, 4141, 10.1091/mbc.E07-12-1217

Tao, 2007, Deacetylase inhibition promotes the generation and function of regulatory T cells, Nat Med, 13, 1299, 10.1038/nm1652

Giles, 2006, A phase I study of intravenous LBH589, a novel cinnamic hydroxamic acid analogue histone deacetylase inhibitor, in patients with refractory hematologic malignancies, Clin Cancer Res, 12, 4628, 10.1158/1078-0432.CCR-06-0511

Klimek, 2008, Tolerability, pharmacodynamics, and pharmacokinetics studies of depsipeptide (romidepsin) in patients with acute myelogenous leukemia or advanced myelodysplastic syndromes, Clin Cancer Res, 14, 826, 10.1158/1078-0432.CCR-07-0318

Kong, 2006, Suppression of class I and II histone deacetylases blunts pressure-overload cardiac hypertrophy, Circulation, 113, 2579, 10.1161/CIRCULATIONAHA.106.625467

Haberland, 2009, The many roles of histone deacetylases in development and physiology: implications for disease and therapy, Nat Rev Genet, 10, 32, 10.1038/nrg2485

Montgomery, 2007, Histone deacetylases 1 and 2 redundantly regulate cardiac morphogenesis, growth, and contractility, Genes Dev, 21, 1790, 10.1101/gad.1563807

Steele, 2008, A phase 1 pharmacokinetic and pharmacodynamic study of the histone deacetylase inhibitor belinostat in patients with advanced solid tumors, Clin Cancer Res, 14, 804, 10.1158/1078-0432.CCR-07-1786

Neal, 2012, Complex role of histone deacetylase inhibitors in the treatment of non-small-cell lung cancer, J Clin Oncol, 30, 2280, 10.1200/JCO.2011.41.0860

Vojinovic, 2011, HDAC inhibition in rheumatoid arthritis and juvenile idiopathic arthritis, Mol Med, 17, 397, 10.2119/molmed.2011.00030

Bush, 2010, Protein acetylation in the cardiorenal axis: the promise of histone deacetylase inhibitors, Circ Res, 106, 272, 10.1161/CIRCRESAHA.109.209338

West, 2014, New and emerging HDAC inhibitors for cancer treatment, J Clin Invest, 124, 30, 10.1172/JCI69738

Xie, 2014, HDAC inhibition blunts ischemia/reperfusion injury by inducing cardiomyocyte autophagy, Circulation, 129, 1139, 10.1161/CIRCULATIONAHA.113.002416

Zhang, 2011, The histone trimethyllysine demethylase JMJD2A promotes cardiac hypertrophy in response to hypertrophic stimuli in mice, J Clin Invest, 121, 2447, 10.1172/JCI46277

Wamstad, 2012, Dynamic and coordinated epigenetic regulation of developmental transitions in the cardiac lineage, Cell, 151, 206, 10.1016/j.cell.2012.07.035

Paige, 2012, A temporal chromatin signature in human embryonic stem cells identifies regulators of cardiac development, Cell, 151, 221, 10.1016/j.cell.2012.08.027

Sirinupong, 2010, Crystal structure of cardiac-specific histone methyltransferase SmyD1 reveals unusual active site architecture, J Biol Chem, 285, 40635, 10.1074/jbc.M110.168187

Das, 2012, Caveolin induces cardioprotection through epigenetic regulation, J Cell Mol Med, 16, 888, 10.1111/j.1582-4934.2011.01372.x

Chen, 2012, Conditional ablation of Ezh2 in murine hearts reveals its essential roles in endocardial cushion formation, cardiomyocyte proliferation and survival, PLoS ONE, 7, e31005, 10.1371/journal.pone.0031005

Dixit, 2007, DUX4, a candidate gene of facioscapulohumeral muscular dystrophy, encodes a transcriptional activator of PITX1, Proc Natl Acad Sci USA, 104, 18157, 10.1073/pnas.0708659104

Ohtani, 2011, Epigenetic regulation of endothelial lineage committed genes in pro-angiogenic hematopoietic and endothelial progenitor cells, Circ Res, 109, 1219, 10.1161/CIRCRESAHA.111.247304

Borlak, 2003, Hallmarks of ion channel gene expression in end-stage heart failure, FASEB J, 17, 1592, 10.1096/fj.02-0889com

Costantini, 2005, The homeodomain transcription factor Irx5 establishes the mouse cardiac ventricular repolarization gradient, Cell, 123, 347, 10.1016/j.cell.2005.08.004

Diehl, 2010, Cardiac deletion of Smyd2 is dispensable for mouse heart development, PLoS ONE, 5, e9748, 10.1371/journal.pone.0009748

Nguyen, 2011, DOT1L regulates dystrophin expression and is critical for cardiac function, Genes Dev, 25, 263, 10.1101/gad.2018511

Shi, 2004, Histone demethylation mediated by the nuclear amine oxidase homolog LSD1, Cell, 119, 941, 10.1016/j.cell.2004.12.012

Sheikh, 2008, An FHL1-containing complex within the cardiomyocyte sarcomere mediates hypertrophic biomechanical stress responses in mice, J Clin Invest, 118, 3870, 10.1172/JCI34472

Simon, 2009, Mechanisms of polycomb gene silencing: knowns and unknowns, Nat Rev Mol Cell Biol, 10, 697, 10.1038/nrm2763

Margueron, 2011, The polycomb complex PRC2 and its mark in life, Nature, 469, 343, 10.1038/nature09784

He, 2012, Polycomb repressive complex 2 regulates normal development of the mouse heart, Circ Res, 110, 406, 10.1161/CIRCRESAHA.111.252205

Rada-Iglesias, 2011, A unique chromatin signature uncovers early developmental enhancers in humans, Nature, 470, 279, 10.1038/nature09692

Yan, 2006, Histone H3 acetylation and H3 K4 methylation define distinct chromatin regions permissive for transgene expression, Mol Cell Biol, 26, 6357, 10.1128/MCB.00311-06

Liang, 2004, Distinct localization of histone H3 acetylation and H3-K4 methylation to the transcription start sites in the human genome, Proc Natl Acad Sci USA, 101, 7357, 10.1073/pnas.0401866101

Jiang, 2007, Global assessment of combinatorial post-translational modification of core histones in yeast using contemporary mass spectrometry. LYS4 trimethylation correlates with degree of acetylation on the same H3 tail, J Biol Chem, 282, 27923, 10.1074/jbc.M704194200

Martin, 2006, Methylation of histone H3 mediates the association of the NuA3 histone acetyltransferase with chromatin, Mol Cell Biol, 26, 3018, 10.1128/MCB.26.8.3018-3028.2006

Vakoc, 2006, Profile of histone lysine methylation across transcribed mammalian chromatin, Mol Cell Biol, 26, 9185, 10.1128/MCB.01529-06

Zhang, 2001, Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails, Genes Dev, 15, 2343, 10.1101/gad.927301

Zhang, 2002, Association of class II histone deacetylases with heterochromatin protein 1: potential role for histone methylation in control of muscle differentiation, Mol Cell Biol, 22, 7302, 10.1128/MCB.22.20.7302-7312.2002

Lehnertz, 2003, Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin, Curr Biol, 13, 1192, 10.1016/S0960-9822(03)00432-9

Mahdavi, 1984, Cardiac alpha- and beta-myosin heavy chain genes are organized in tandem, Proc Natl Acad Sci USA, 81, 2626, 10.1073/pnas.81.9.2626

Rundell, 2005, Impact of beta-myosin heavy chain isoform expression on cross-bridge cycling kinetics, Am J Physiol Heart Circ Physiol, 288, H896, 10.1152/ajpheart.00407.2004

Krenz, 2004, Impact of beta-myosin heavy chain expression on cardiac function during stress, J Am Coll Cardiol, 44, 2390, 10.1016/j.jacc.2004.09.044

Lowes, 1997, Changes in gene expression in the intact human heart. Downregulation of alpha-myosin heavy chain in hypertrophied, failing ventricular myocardium, J Clin Invest, 100, 2315, 10.1172/JCI119770

Miyata, 2000, Myosin heavy chain isoform expression in the failing and nonfailing human heart, Circ Res, 86, 386, 10.1161/01.RES.86.4.386

Haddad, 2003, Role of antisense RNA in coordinating cardiac myosin heavy chain gene switching, J Biol Chem, 278, 37132, 10.1074/jbc.M305911200

Haddad, 2006, Regulation of antisense RNA expression during cardiac MHC gene switching in response to pressure overload, Am J Physiol Heart Circ Physiol, 290, H2351, 10.1152/ajpheart.01111.2005

Huang, 1997, A conserved GATA motif in a tissue-specific DNase I hypersensitive site of the cardiac alpha-myosin heavy chain gene, Biochem J, 325, 47, 10.1042/bj3250047

Huang, 1998, Chromatin remodelling of the cardiac beta-myosin heavy chain gene, Biochem J, 330, 871, 10.1042/bj3300871

Knutson, 2012, A selective inhibitor of EZH2 blocks H3K27 methylation and kills mutant lymphoma cells, Nat Chem Biol, 8, 890, 10.1038/nchembio.1084

McCabe, 2012, EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations, Nature, 492, 108, 10.1038/nature11606

Takawa, 2011, Validation of the histone methyltransferase EZH2 as a therapeutic target for various types of human cancer and as a prognostic marker, Cancer Sci, 102, 1298, 10.1111/j.1349-7006.2011.01958.x

Varambally, 2008, Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer, Science, 322, 1695, 10.1126/science.1165395

Varambally, 2002, The polycomb group protein EZH2 is involved in progression of prostate cancer, Nature, 419, 624, 10.1038/nature01075

Kleer, 2003, EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells, Proc Natl Acad Sci USA, 100, 11606, 10.1073/pnas.1933744100

Daigle, 2011, Selective killing of mixed lineage leukemia cells by a potent small-molecule DOT1L inhibitor, Cancer Cell, 20, 53, 10.1016/j.ccr.2011.06.009

Copeland, 2013, Molecular pathways: protein methyltransferases in cancer, Clin Cancer Res, 19, 6344, 10.1158/1078-0432.CCR-13-0223

Wee, 2014, Targeting epigenetic regulators for cancer therapy, Ann N Y Acad Sci, 1309, 30, 10.1111/nyas.12356