Chromatin Remodeling in Heart Failure

  • Pei Han
  • Jin Yang
  • Ching Shang
  • Ching-Pin ChangEmail author
Part of the Cardiac and Vascular Biology book series (Abbreviated title: Card. vasc. biol.)


Chromatin provides a dynamic DNA scaffold that reacts to physiological and pathological signals to control the accessibility of DNA sequence and the genomic responses to environmental stimuli. Chromatin can be regulated by nucleosome remodeling, histone modification, and DNA methylation. Histone and DNA modifications occur by covalent alterations of the side chains of histone or bases of DNA, catalyzed by specific histone- and DNA-modifying enzymes, whereas nucleosome or chromatin-remodeling controls noncovalent changes of nucleosomes, including their position and histone composition, effected by adenosine triphosphate (ATP)-dependent chromatin-remodeling complexes. Within the nucleosome, the chromatin remodelers can replace canonical histones with variant forms of histones, which are involved in cardiac stress response. In addition, chromatin remodelers can interact with histone- and DNA-modifying enzymes to control chromatin structure and reprogram gene expression in pathologically stressed hearts. More recently, a chromatin-remodeling factor was found to interact with a cardiac-specific long noncoding RNA to control gene expression and maintain cardiac homeostasis. These functional aspects of chromatin remodelers are critical for the pathogenesis of cardiomyopathy and heart failure. This chapter is focused on the recent progress in understanding the roles of chromatin-remodeling factors in heart failure, new chromatin-based mechanisms, and potential therapeutic strategies for heart failure.


Chromatin Remodeler Histone Variant ATPase Subunit Heart Failure Therapy Repressive Chromatin 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Compliance with Ethical Standards


C.P.C. is the Charles Fisch Scholar of Cardiology and was supported by National Institutes of Health (NIH; HL118087, HL121197, HL085345), the American Heart Association (National Scientist Development Award, Established Investigator Award 12EIA8960018), Oak Foundation, Baxter Foundation, Lucile Packard Heart Center Research Program, California Institute of Regenerative Medicine New Faculty Award, Children’s Heart Foundation, the CHARGE Syndrome Foundation, March of Dimes Foundation (#6-FY11-260), Indiana University (IU) School of Medicine—IU Health Strategic Research Initiative, and the IU Physician-Scientist Initiative, endowed by Lilly Endowment.

Conflict of Interest

The authors declare that they have no conflict of interest.


  1. Abraham WT et al (2002) Coordinate changes in Myosin heavy chain isoform gene expression are selectively associated with alterations in dilated cardiomyopathy phenotype. Mol Med 8:750–760PubMedPubMedCentralGoogle Scholar
  2. Ahmad K, Henikoff S (2002) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9:1191–1200PubMedCrossRefGoogle Scholar
  3. Anand P et al (2013) BET bromodomains mediate transcriptional pause release in heart failure. Cell 154:569–582PubMedPubMedCentralCrossRefGoogle Scholar
  4. Backs J, Olson EN (2006) Control of cardiac growth by histone acetylation/deacetylation. Circ Res 98:15–24PubMedCrossRefGoogle Scholar
  5. Billon P, Cote J (2013) Precise deposition of histone H2A.Z in chromatin for genome expression and maintenance. Biochim Biophys Acta 1819:290–302PubMedCrossRefGoogle Scholar
  6. Blaxall BC, Tschannen-Moran BM, Milano CA, Koch WJ (2003) Differential gene expression and genomic patient stratification following left ventricular assist device support. J Am Coll Cardiol 41:1096–1106PubMedCrossRefGoogle Scholar
  7. Bultman S et al (2000) A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol Cell 6:1287–1295PubMedCrossRefGoogle Scholar
  8. Burnett JC, Rossi JJ (2012) RNA-based therapeutics: current progress and future prospects. Chem Biol 19:60–71PubMedPubMedCentralCrossRefGoogle Scholar
  9. Byrd AK, Raney KD (2012) Superfamily 2 helicases. Front Biosci (Landmark Ed) 17:2070–2088CrossRefGoogle Scholar
  10. Byrd AK et al (2012) Dda helicase tightly couples translocation on single-stranded DNA to unwinding of duplex DNA: Dda is an optimally active helicase. J Mol Biol 420:141–154PubMedPubMedCentralCrossRefGoogle Scholar
  11. Callis TE et al (2009) MicroRNA-208a is a regulator of cardiac hypertrophy and conduction in mice. J Clin Invest 119:2772–2786PubMedPubMedCentralCrossRefGoogle Scholar
  12. Chang CP, Bruneau BG (2012) Epigenetics and cardiovascular development. Annu Rev Physiol 74:41–68PubMedCrossRefGoogle Scholar
  13. Chang L, Kiriazis H, Gao XM, Du XJ, El-Osta A (2011) Cardiac genes show contextual SWI/SNF interactions with distinguishable gene activities. Epigenetics 6:760–768PubMedCrossRefGoogle Scholar
  14. Chen H et al (2004) BMP10 is essential for maintaining cardiac growth during murine cardiogenesis. Development 131:2219–2231PubMedPubMedCentralCrossRefGoogle Scholar
  15. Chen IY et al (2006) Histone H2A.z is essential for cardiac myocyte hypertrophy but opposed by silent information regulator 2alpha. J Biol Chem 281:19369–19377PubMedCrossRefGoogle Scholar
  16. Clapier CR, Cairns BR (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78:273–304PubMedCrossRefGoogle Scholar
  17. Dallas PB et al (2000) The human SWI-SNF complex protein p270 is an ARID family member with non-sequence-specific DNA binding activity. Mol Cell Biol 20:3137–3146PubMedPubMedCentralCrossRefGoogle Scholar
  18. Delmore JE et al (2011) BET bromodomain inhibition as a therapeutic strategy to target c-Myc. Cell 146:904–917PubMedPubMedCentralCrossRefGoogle Scholar
  19. Devaux Y et al (2015) Long noncoding RNAs in cardiac development and ageing. Nat Rev Cardiol 12:415–425PubMedCrossRefGoogle Scholar
  20. Eissenberg JC (2012) Structural biology of the chromodomain: form and function. Gene 496:69–78PubMedCrossRefGoogle Scholar
  21. Emery P, Durand B, Mach B, Reith W (1996) RFX proteins, a novel family of DNA binding proteins conserved in the eukaryotic kingdom. Nucleic Acids Res 24:803–807PubMedPubMedCentralCrossRefGoogle Scholar
  22. Fairman-Williams ME, Guenther UP, Jankowsky E (2010) SF1 and SF2 helicases: family matters. Curr Opin Struct Biol 20:313–324PubMedPubMedCentralCrossRefGoogle Scholar
  23. Filippakopoulos P, Knapp S (2014) Targeting bromodomains: epigenetic readers of lysine acetylation. Nat Rev Drug Discov 13:337–356PubMedCrossRefGoogle Scholar
  24. Filippakopoulos P et al (2010) Selective inhibition of BET bromodomains. Nature 468:1067–1073PubMedPubMedCentralCrossRefGoogle Scholar
  25. Filippakopoulos P et al (2012) Histone recognition and large-scale structural analysis of the human bromodomain family. Cell 149:214–231PubMedPubMedCentralCrossRefGoogle Scholar
  26. Finley A, Copeland RA (2014) Small molecule control of chromatin remodeling. Chem Biol 21:1196–1210PubMedCrossRefGoogle Scholar
  27. Foltz DR et al (2006) The human CENP-A centromeric nucleosome-associated complex. Nat Cell Biol 8:458–469PubMedCrossRefGoogle Scholar
  28. Franklin S et al (2011) Specialized compartments of cardiac nuclei exhibit distinct proteomic anatomy. Mol Cell Proteomics 10:M110 000703PubMedPubMedCentralCrossRefGoogle Scholar
  29. Frick DN (2003) Helicases as antiviral drug targets. Drug News Perspect 16:355–362PubMedPubMedCentralCrossRefGoogle Scholar
  30. Garnier JM, Sharp PP, Burns CJ (2014) BET bromodomain inhibitors: a patent review. Expert Opin Ther Pat 24:185–199PubMedCrossRefGoogle Scholar
  31. Gilsbach R et al (2014) Dynamic DNA methylation orchestrates cardiomyocyte development, maturation and disease. Nat Commun 5:5288PubMedPubMedCentralCrossRefGoogle Scholar
  32. Goldberg AD et al (2010) Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140:678–691PubMedPubMedCentralCrossRefGoogle Scholar
  33. Grote P et al (2013) The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse. Dev Cell 24:206–214PubMedPubMedCentralCrossRefGoogle Scholar
  34. Gupta RM, Pilbrow AP, Weeke PE (2015) Top advances in functional genomics and translational biology for 2014. Circ Cardiovasc Genet 8:207–210PubMedCrossRefGoogle Scholar
  35. Haas J et al (2013) Alterations in cardiac DNA methylation in human dilated cardiomyopathy. EMBO Mol Med 5:413–429PubMedPubMedCentralCrossRefGoogle Scholar
  36. Han P, Chang CP (2015) Myheart hits the core of chromatin. Cell Cycle 14:787–788PubMedPubMedCentralCrossRefGoogle Scholar
  37. Han P, Hang CT, Yang J, Chang CP (2011) Chromatin remodeling in cardiovascular development and physiology. Circ Res 108:378–396PubMedPubMedCentralCrossRefGoogle Scholar
  38. Han P et al (2014) A long noncoding RNA protects the heart from pathological hypertrophy. Nature 514:102–106PubMedPubMedCentralCrossRefGoogle Scholar
  39. Han P et al (2016) Epigenetic response to environmental stress: assembly of BRG1-G9a/GLP-DNMT3 repressive chromatin complex on Myh6 promoter in pathologically stressed hearts. Biochim Biophys Acta 1863:1772–1781PubMedCrossRefGoogle Scholar
  40. Hang CT et al (2010) Chromatin regulation by Brg1 underlies heart muscle development and disease. Nature 466:62–67PubMedPubMedCentralCrossRefGoogle Scholar
  41. He L et al (2014) BAF200 is required for heart morphogenesis and coronary artery development. PLoS One 9:e109493PubMedPubMedCentralCrossRefGoogle Scholar
  42. Henikoff S, Ahmad K (2005) Assembly of variant histones into chromatin. Annu Rev Cell Dev Biol 21:133–153PubMedCrossRefGoogle Scholar
  43. Herron TJ, McDonald KS (2002) Small amounts of alpha-myosin heavy chain isoform expression significantly increase power output of rat cardiac myocyte fragments. Circ Res 90:1150–1152PubMedCrossRefGoogle Scholar
  44. Ho L, Crabtree GR (2010) Chromatin remodelling during development. Nature 463:474–484PubMedPubMedCentralCrossRefGoogle Scholar
  45. Huang X, Gao X, Diaz-Trelles R, Ruiz-Lozano P, Wang Z (2008) Coronary development is regulated by ATP-dependent SWI/SNF chromatin remodeling component BAF180. Dev Biol 319:258–266PubMedCrossRefGoogle Scholar
  46. Hurd EA et al (2007) Loss of Chd7 function in gene-trapped reporter mice is embryonic lethal and associated with severe defects in multiple developing tissues. Mamm Genome 18:94–104PubMedCrossRefGoogle Scholar
  47. James J et al (2005) Forced expression of alpha-myosin heavy chain in the rabbit ventricle results in cardioprotection under cardiomyopathic conditions. Circulation 111:2339–2346PubMedPubMedCentralCrossRefGoogle Scholar
  48. Jankowsky E (2011) RNA helicases at work: binding and rearranging. Trends Biochem Sci 36:19–29PubMedPubMedCentralCrossRefGoogle Scholar
  49. Jenni R, Rojas J, Oechslin E (1999) Isolated noncompaction of the myocardium. N Engl J Med 340:966–967PubMedCrossRefGoogle Scholar
  50. Kadam S, Emerson BM (2003) Transcriptional specificity of human SWI/SNF BRG1 and BRM chromatin remodeling complexes. Mol Cell 11:377–389PubMedCrossRefGoogle Scholar
  51. Kadoch C, Crabtree GR (2013) Reversible disruption of mSWI/SNF (BAF) complexes by the SS18-SSX oncogenic fusion in synovial sarcoma. Cell 153:71–85PubMedPubMedCentralCrossRefGoogle Scholar
  52. Kadoch C et al (2013) Proteomic and bioinformatic analysis of mammalian SWI/SNF complexes identifies extensive roles in human malignancy. Nat Genet 45:592–601PubMedPubMedCentralCrossRefGoogle Scholar
  53. Kamakaka RT, Biggins S (2005) Histone variants: deviants? Genes Dev 19:295–310PubMedCrossRefGoogle Scholar
  54. Kasten M et al (2004) Tandem bromodomains in the chromatin remodeler RSC recognize acetylated histone H3 Lys14. EMBO J 23:1348–1359PubMedPubMedCentralCrossRefGoogle Scholar
  55. Klattenhoff CA et al (2013) Braveheart, a long noncoding RNA required for cardiovascular lineage commitment. Cell 152:570–583PubMedPubMedCentralCrossRefGoogle Scholar
  56. Krenz M, Robbins J (2004) Impact of beta-myosin heavy chain expression on cardiac function during stress. J Am Coll Cardiol 44:2390–2397PubMedCrossRefGoogle Scholar
  57. Kwong AD, Rao BG, Jeang KT (2005) Viral and cellular RNA helicases as antiviral targets. Nat Rev Drug Discov 4:845–853PubMedCrossRefGoogle Scholar
  58. Lange M et al (2008) Regulation of muscle development by DPF3, a novel histone acetylation and methylation reader of the BAF chromatin remodeling complex. Genes Dev 22:2370–2384PubMedPubMedCentralCrossRefGoogle Scholar
  59. Lee HS, Park JH, Kim SJ, Kwon SJ, Kwon J (2010) A cooperative activation loop among SWI/SNF, gamma-H2AX and H3 acetylation for DNA double-strand break repair. EMBO J 29:1434–1445PubMedPubMedCentralCrossRefGoogle Scholar
  60. Lessard J et al (2007) An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron 55:201–215PubMedPubMedCentralCrossRefGoogle Scholar
  61. Li W et al (2013) Brg1 governs distinct pathways to direct multiple aspects of mammalian neural crest cell development. Proc Natl Acad Sci U S A 110:1738–1743PubMedPubMedCentralCrossRefGoogle Scholar
  62. Lickert H et al (2004) Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature 432:107–112PubMedCrossRefGoogle Scholar
  63. Linder P, Jankowsky E (2011) From unwinding to clamping—the DEAD box RNA helicase family. Nat Rev Mol Cell Biol 12:505–516PubMedCrossRefGoogle Scholar
  64. Liu J, Wang DZ (2014) An epigenetic “LINK(RNA)” to pathological cardiac hypertrophy. Cell Metab 20:555–557PubMedPubMedCentralCrossRefGoogle Scholar
  65. Liu Y et al (2014a) CHD7 interacts with BMP R-SMADs to epigenetically regulate cardiogenesis in mice. Hum Mol Genet 23:2145–2156PubMedCrossRefGoogle Scholar
  66. Liu M et al (2014b) AG-690/11026014, a novel PARP-1 inhibitor, protects cardiomyocytes from AngII-induced hypertrophy. Mol Cell Endocrinol 392:14–22PubMedCrossRefGoogle Scholar
  67. Lompre AM et al (1979) Myosin isoenzyme redistribution in chronic heart overload. Nature 282:105–107PubMedCrossRefGoogle Scholar
  68. Lowes BD et al (2002) Myocardial gene expression in dilated cardiomyopathy treated with beta-blocking agents. N Engl J Med 346:1357–1365PubMedCrossRefGoogle Scholar
  69. Mack GS (2010) To selectivity and beyond. Nat Biotechnol 28:1259–1266PubMedCrossRefGoogle Scholar
  70. Mallam AL, Del Campo M, Gilman B, Sidote DJ, Lambowitz AM (2012) Structural basis for RNA-duplex recognition and unwinding by the DEAD-box helicase Mss116p. Nature 490:121–125PubMedPubMedCentralCrossRefGoogle Scholar
  71. Marfella CG et al (2006) Mutation of the SNF2 family member Chd2 affects mouse development and survival. J Cell Physiol 209:162–171PubMedCrossRefGoogle Scholar
  72. Masternak K et al (1998) A gene encoding a novel RFX-associated transactivator is mutated in the majority of MHC class II deficiency patients. Nat Genet 20:273–277PubMedCrossRefGoogle Scholar
  73. McKinsey TA, Kass DA (2007) Small-molecule therapies for cardiac hypertrophy: moving beneath the cell surface. Nat Rev Drug Discov 6:617–635PubMedCrossRefGoogle Scholar
  74. McKinsey TA, Olson EN (2004) Cardiac histone acetylation—therapeutic opportunities abound. Trends Genet 20:206–213PubMedCrossRefGoogle Scholar
  75. Miyata S, Minobe W, Bristow MR, Leinwand LA (2000) Myosin heavy chain isoform expression in the failing and nonfailing human heart. Circ Res 86:386–390PubMedCrossRefGoogle Scholar
  76. Mizuguchi G et al (2004) ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303:343–348PubMedCrossRefGoogle Scholar
  77. Montgomery RL et al (2011) Therapeutic inhibition of miR-208a improves cardiac function and survival during heart failure. Circulation 124:1537–1547PubMedPubMedCentralCrossRefGoogle Scholar
  78. Movassagh M et al (2011) Distinct epigenomic features in end-stage failing human hearts. Circulation 124:2411–2422PubMedPubMedCentralCrossRefGoogle Scholar
  79. Mozaffarian D et al (2015) Heart disease and stroke statistics—2015 update: a report from the American Heart Association. Circulation 131:e29–e322PubMedCrossRefGoogle Scholar
  80. Natarajan K, Jackson BM, Zhou H, Winston F, Hinnebusch AG (1999) Transcriptional activation by Gcn4p involves independent interactions with the SWI/SNF complex and the SRB/mediator. Mol Cell 4:657–664PubMedCrossRefGoogle Scholar
  81. Olson EN (2006) Gene regulatory networks in the evolution and development of the heart. Science 313:1922–1927PubMedPubMedCentralCrossRefGoogle Scholar
  82. Olson EN, Backs J, McKinsey TA (2006) Control of cardiac hypertrophy and heart failure by histone acetylation/deacetylation. Novartis Found Symp 274: 3–12; discussion 13–19, 152–155, 272–156Google Scholar
  83. Pang B et al (2013) Drug-induced histone eviction from open chromatin contributes to the chemotherapeutic effects of doxorubicin. Nat Commun 4:1908PubMedPubMedCentralCrossRefGoogle Scholar
  84. Papait R et al (2013) Genome-wide analysis of histone marks identifying an epigenetic signature of promoters and enhancers underlying cardiac hypertrophy. Proc Natl Acad Sci U S A 110:20164–20169PubMedPubMedCentralCrossRefGoogle Scholar
  85. Papamichos-Chronakis M, Watanabe S, Rando OJ, Peterson CL (2011) Global regulation of H2A.Z localization by the INO80 chromatin-remodeling enzyme is essential for genome integrity. Cell 144:200–213PubMedPubMedCentralCrossRefGoogle Scholar
  86. Paull TT et al (2000) A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 10:886–895PubMedCrossRefGoogle Scholar
  87. Randall V et al (2009) Great vessel development requires biallelic expression of Chd7 and Tbx1 in pharyngeal ectoderm in mice. J Clin Invest 119:3301–3310PubMedPubMedCentralGoogle Scholar
  88. Reyes JC et al (1998) Altered control of cellular proliferation in the absence of mammalian brahma (SNF2alpha). EMBO J 17:6979–6991PubMedPubMedCentralCrossRefGoogle Scholar
  89. Saha A, Wittmeyer J, Cairns BR (2006) Chromatin remodelling: the industrial revolution of DNA around histones. Nat Rev Mol Cell Biol 7:437–447PubMedCrossRefGoogle Scholar
  90. Sanchez R, Zhou MM (2011) The PHD finger: a versatile epigenome reader. Trends Biochem Sci 36:364–372PubMedPubMedCentralGoogle Scholar
  91. Santoro R, Li J, Grummt I (2002) The nucleolar remodeling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription. Nat Genet 32:393–396PubMedCrossRefGoogle Scholar
  92. Sarma K, Reinberg D (2005) Histone variants meet their match. Nat Rev Mol Cell Biol 6:139–149PubMedCrossRefGoogle Scholar
  93. Schuettengruber B, Martinez AM, Iovino N, Cavalli G (2011) Trithorax group proteins: switching genes on and keeping them active. Nat Rev Mol Cell Biol 12:799–814PubMedCrossRefGoogle Scholar
  94. Shen W et al (2007) Solution structure of human Brg1 bromodomain and its specific binding to acetylated histone tails. Biochemistry 46:2100–2110PubMedCrossRefGoogle Scholar
  95. Singh AP, Archer TK (2014) 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 42:2958–2975PubMedCrossRefGoogle Scholar
  96. Spiltoir JI et al (2013) BET acetyl-lysine binding proteins control pathological cardiac hypertrophy. J Mol Cell Cardiol 63:175–179PubMedPubMedCentralCrossRefGoogle Scholar
  97. Stankunas K et al (2008) Endocardial Brg1 represses ADAMTS1 to maintain the microenvironment for myocardial morphogenesis. Dev Cell 14:298–311PubMedPubMedCentralCrossRefGoogle Scholar
  98. Stopka T, Skoultchi AI (2003) The ISWI ATPase Snf2h is required for early mouse development. Proc Natl Acad Sci U S A 100:14097–14102PubMedPubMedCentralCrossRefGoogle Scholar
  99. Stros M, Launholt D, Grasser KD (2007) The HMG-box: a versatile protein domain occurring in a wide variety of DNA-binding proteins. Cell Mol Life Sci 64:2590–2606PubMedCrossRefGoogle Scholar
  100. Swynghedauw B (1999) Molecular mechanisms of myocardial remodeling. Physiol Rev 79:215–262PubMedGoogle Scholar
  101. Szabo G et al (2002) Poly(ADP-ribose) polymerase inhibition reduces reperfusion injury after heart transplantation. Circ Res 90:100–106PubMedCrossRefGoogle Scholar
  102. Takeuchi JK et al (2007) Baf60c is a nuclear Notch signaling component required for the establishment of left-right asymmetry. Proc Natl Acad Sci U S A 104:846–851PubMedPubMedCentralCrossRefGoogle Scholar
  103. Takeuchi JK et al (2011) Chromatin remodelling complex dosage modulates transcription factor function in heart development. Nat Commun 2:187PubMedPubMedCentralCrossRefGoogle Scholar
  104. Tang L, Nogales E, Ciferri C (2010) Structure and function of SWI/SNF chromatin remodeling complexes and mechanistic implications for transcription. Prog Biophys Mol Biol 102:122–128PubMedPubMedCentralCrossRefGoogle Scholar
  105. Terme JM et al (2011) Histone H1 variants are differentially expressed and incorporated into chromatin during differentiation and reprogramming to pluripotency. J Biol Chem 286:35347–35357PubMedPubMedCentralCrossRefGoogle Scholar
  106. van Rooij E et al (2007) Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 316:575–579PubMedCrossRefGoogle Scholar
  107. van Rooij E et al (2009) A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev Cell 17:662–673PubMedPubMedCentralCrossRefGoogle Scholar
  108. Von Hoff DD et al (1979) Risk factors for doxorubicin-induced congestive heart failure. Ann Intern Med 91:710–717CrossRefGoogle Scholar
  109. Wang Z, Wang Y (2015) Dawn of the Epi-LncRNAs: new path from Myheart. Circ Res 116:235–236PubMedPubMedCentralCrossRefGoogle Scholar
  110. Wang Z et al (2004) Polybromo protein BAF180 functions in mammalian cardiac chamber maturation. Genes Dev 18:3106–3116PubMedPubMedCentralCrossRefGoogle Scholar
  111. Wei JQ et al (2008) Quantitative control of adaptive cardiac hypertrophy by acetyltransferase p300. Circulation 118:934–946PubMedPubMedCentralCrossRefGoogle Scholar
  112. Wu C, Arora P (2015) Long noncoding Mhrt RNA: molecular crowbar unravel insights into heart failure treatment. Circ Cardiovasc Genet 8:213–215PubMedCrossRefGoogle Scholar
  113. Wu JI, Lessard J, Crabtree GR (2009) Understanding the words of chromatin regulation. Cell 136:200–206PubMedPubMedCentralCrossRefGoogle Scholar
  114. Wu M et al (2014) Baf250a orchestrates an epigenetic pathway to repress the Nkx2.5-directed contractile cardiomyocyte program in the sinoatrial node. Cell Res 24:1201–1213PubMedPubMedCentralCrossRefGoogle Scholar
  115. Yang KC et al (2014) Deep RNA sequencing reveals dynamic regulation of myocardial noncoding RNAs in failing human heart and remodeling with mechanical circulatory support. Circulation 129:1009–1021PubMedPubMedCentralCrossRefGoogle Scholar
  116. Zeng L et al (2010) Mechanism and regulation of acetylated histone binding by the tandem PHD finger of DPF3b. Nature 466:258–262PubMedPubMedCentralCrossRefGoogle Scholar
  117. Zhang W, Chen H, Qu X, Chang CP, Shou W (2013) Molecular mechanism of ventricular trabeculation/compaction and the pathogenesis of the left ventricular noncompaction cardiomyopathy (LVNC). Am J Med Genet C Semin Med Genet 163C:144–156PubMedCrossRefGoogle Scholar
  118. Zhou Y, Santoro R, Grummt I (2002) The chromatin remodeling complex NoRC targets HDAC1 to the ribosomal gene promoter and represses RNA polymerase I transcription. EMBO J 21:4632–4640PubMedPubMedCentralCrossRefGoogle Scholar
  119. Zhu JG et al (2014) Long noncoding RNAs expression profile of the developing mouse heart. J Cell Biochem 115:910–918PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Pei Han
    • 1
    • 2
  • Jin Yang
    • 1
  • Ching Shang
    • 1
    • 2
  • Ching-Pin Chang
    • 1
    • 3
    • 4
    Email author
  1. 1.Department of Medicine, Krannert Institute of Cardiology and Division of CardiologyIndiana University School of MedicineIndianapolisUSA
  2. 2.Division of Cardiovascular MedicineStanford University School of MedicineStanfordUSA
  3. 3.Department of Biochemistry and Molecular BiologyIndiana University School of MedicineIndianapolisUSA
  4. 4.Department of Medical and Molecular GeneticsIndiana University School of MedicineIndianapolisUSA

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