Baf250a orchestrates an epigenetic pathway to repress the Nkx2.5-directed contractile cardiomyocyte program in the sinoatrial node

Cell Research

Volumn 24, Issue 10, 2014, Pages 1201-1213

  Wu, Meng ^a,b   Peng, Siwu ^a,b   Yang, Jialiang ^b   Tu, Zhidong ^b   Cai, Xiaoqiang ^a   Cai, Chen Leng ^a   Wang, Zhong ^c   Zhao, Yong ^a,b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b Department of Genetics and Genomic Sciences ^*  (China)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC HORMONE AGONISTS AND ANTAGONISTS; ARID1A PROTEIN, MOUSE; DNA BINDING PROTEIN; GATA4 PROTEIN, MOUSE; HISTONE DEACETYLASE; HISTONE DEACETYLASE 3; HOMEODOMAIN PROTEIN; NKX2-5 PROTEIN, MOUSE; NUCLEAR PROTEIN; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR 5; TAMOXIFEN; TBX3 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 4;

ANIMAL; C57BL MOUSE; CARDIAC MUSCLE CELL; CHROMATIN IMMUNOPRECIPITATION; CLUSTER ANALYSIS; DEFICIENCY; DRUG EFFECTS; GENETIC EPIGENESIS; GENETICS; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; METABOLISM; MOUSE; MUSCLE CONTRACTION; SINUS NODE;

ANIMALS; ANTINEOPLASTIC AGENTS, HORMONAL; CHROMATIN IMMUNOPRECIPITATION; CLUSTER ANALYSIS; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; GATA4 TRANSCRIPTION FACTOR; HEK293 CELLS; HISTONE DEACETYLASES; HOMEODOMAIN PROTEINS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE CONTRACTION; MYOCYTES, CARDIAC; NUCLEAR PROTEINS; SINOATRIAL NODE; T-BOX DOMAIN PROTEINS; TAMOXIFEN; TRANSCRIPTION FACTORS;

EID: 84961368033     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2014.113     Document Type: Article

References (54)

1. Boyett MR, Honjo H, Kodama I. The sinoatrial node, a heterogeneous pacemaker structure. Cardiovasc Res 2000; 47;658-687.
2. Mangoni ME, Nargeot J. Genesis and regulation of the heart automaticity. Physiol Rev 2008; 88:919-982.
3. Park DS, Fishman GI. The cardiac conduction system. Circulation 2011; 123:904-915.
4. Dobrzynski H, Boyett MR, Anderson RH. New insights into pacemaker activity: promoting understanding of sick sinus syndrome. Circulation 2007; 115:1921-1932.
5. Kumar P, Kusumoto FM, Goldschlager N. Bradyarrhythmias in the elderly. Clin Geriatr Med 2012; 28:703-715.
6. Lakatta EG, Maltsev VA, Vinogradova TM. A coupled SYSTEM of intracellular Ca2+ clocks and surface membrane voltage clocks controls the timekeeping mechanism of the heart's pacemaker. Circ Res 2010; 106:659-673.
7. DiFrancesco D. The role of the funny current in pacemaker activity. Circ Res 2010; 106:434-446.
8. Chen B, Wu Y, Mohler PJ, et al. Local control of Ca2+-induced Ca2+ release in mouse sinoatrial node cells. J Mol Cell Cardiol 2009; 47:706-715.
9. Milanesi R, Baruscotti M, Gnecchi-Ruscone T, et al. Familial sinus bradycardia associated with a mutation in the cardiac pacemaker channel. N Engl J Med 2006; 354:151-157.
10. Le Scouarnec S, Bhasin N, Vieyres C, et al. Dysfunction in ankyrin-B-dependent ion channel and transporter targeting causes human sinus node disease. Proc Natl Acad Sci USA 2008; 105:15617-15622.
11. Benson DW, Wang DW, Dyment M, et al. Congenital sick sinus syndrome caused by recessive mutations in the cardiac sodium channel gene (SCN5A). J Clin Invest 2003; 112:1019-1028.
12. Blaschke RJ, Hahurij ND, Kuijper S, et al. Targeted mutation reveals essential functions of the homeodomain transcription factor Shox2 in sinoatrial and pacemaking development. Circulation 2007; 115:1830-1838.
13. Espinoza-Lewis RA, Yu L, He F, et al. Shox2 is essential for the differentiation of cardiac pacemaker cells by repressing Nkx2-5. Dev Biol 2009; 327:376-385.
14. Wiese C, Grieskamp T, Airik R, et al. Formation of the sinus node head and differentiation of sinus node myocardium are independently regulated by Tbx18 and Tbx3. Circ Res 2009; 104:388-397.
15. Hoogaars WM, Engel A, Brons JF, et al. Tbx3 controls the sinoatrial node gene program and imposes pacemaker function on the atria. Genes Dev 2007; 21:1098-1112.
16. Frank DU, Carter KL, Thomas KR, et al. Lethal arrhythmias in Tbx3-deficient mice reveal extreme dosage sensitivity of cardiac conduction system function and homeostasis. Proc Natl Acad Sci USA 2012; 109:E154-E163.
17. Chang CP, Bruneau BG. Epigenetics and cardiovascular development. Annu Rev Physiol 2012; 74:41-68.
18. Bruneau BG. Chromatin remodeling in heart development. Curr Opin Genet Dev 2010; 20:505-511.
19. Backs J, Olson EN. Control of cardiac growth by histone acetylation/deacetylation. Circ Res 2006; 98:15-24.
20. Paige SL, Thomas S, Stoick-Cooper CL, et al. A temporal chromatin signature in human embryonic stem cells identifies regulators of cardiac development. Cell 2012; 151:221-232.
21. Roy K, de la Serna IL, Imbalzano AN. The myogenic basic helix-loop-helix family of transcription factors shows similar requirements for SWI/SNF chromatin remodeling enzymes during muscle differentiation in culture. J Biol Chem 2002; 277:33818-33824.
22. Metivier R, Penot G, Hubner MR, et al. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 2003; 115:751-763.
23. Lei I, Gao X, Sham MH, et al. SWI/SNF protein component BAF250a regulates cardiac progenitor cell differentiation by modulating chromatin accessibility during second heart field development. J Biol Chem 2012; 287:24255-24262.
24. Gao X, Tate P, Hu P, et al. ES cell pluripotency and germ-layer formation require the SWI/SNF chromatin remodeling component BAF250a. Proc Natl Acad Sci USA 2008; 105:6656-6661.
25. Wu M, Peng S, Zhao Y. Inducible gene deletion in the entire cardiac conduction system using Hcn4-CreERT2 BAC transgenic mice. Genesis 2014; 52:134-140.
26. Park EJ, Sun X, Nichol P, et al. System for tamoxifen-inducible expression of cre-recombinase from the Foxa2 locus in mice. Dev Dyn 2008; 237:447-453.
27. Ernst J, Bar-Joseph Z. STEM: a tool for the analysis of short time series gene expression data. BMC Bioinformatics 2006; 7:191.
28. McCulley DJ, Black BL. Transcription factor pathways and congenital heart disease. Curr Top Dev Biol 2012; 100:253-277.
29. Wilsker D, Patsialou A, Zumbrun SD, et al. The DNA-binding properties of the ARID-containing subunits of yeast and mammalian SWI/SNF complexes. Nucleic Acids Res 2004; 32:1345-1353.
30. Clapier CR, Cairns BR. The biology of chromatin remodeling complexes. Annu Rev Biochem 2009; 78:273-304.
31. Montgomery RL, Potthoff MJ, Haberland M, et al. Maintenance of cardiac energy metabolism by histone deacetylase 3 in mice. J Clin Invest 2008; 118:3588-3597.
32. Singh N, Trivedi CM, Lu M, et al Histone deacetylase 3 regulates smooth muscle differentiation in neural crest cells and development of the cardiac outflow tract. Circ Res 2011; 109:1240-1249.
33. Bernstein BE, Kamal M, Lindblad-Toh K, et al. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 2005; 120:169-181.
34. Wang Z, Zang C, Cui K, et al. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 2009; 138:1019-1031.
35. Liu R, Liu H, Chen X, et al. Regulation of CSF1 promoter by the SWI/SNF-like BAF complex. Cell 2001; 106:309-318.
36. Srivastava D. Making or breaking the heart: from lineage determination to morphogenesis. Cell 2006; 126:1037-1048.
37. Bruneau BG, Nemer G, Schmitt JP, et al. A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell 2001; 106:709-721.
38. Prall OW, Menon MK, Solloway MJ, et al. An Nkx2-5/Bmp2/Smad1 negative feedback loop controls heart progenitor specification and proliferation. Cell 2007; 128:947-959.
39. Risebro CA, Riley PR. Formation of the ventricles. ScientificWorldJournal 2006; 6:1862-1880.
40. He A, Kong SW, Ma Q, et al. Co-occupancy by multiple cardiac transcription factors identifies transcriptional enhancers active in heart. Proc Natl Acad Sci USA 2011; 108:5632-5637.
41. Xie L, Hoffmann AD, Burnicka-Turek O, et al. Tbx5-hedgehog molecular networks are essential in the second heart field for atrial septation. Dev Cell 2012; 23:280-291.
42. Watanabe Y, Zaffran S, Kuroiwa A, et al. Fibroblast growth factor 10 gene regulation in the second heart field by Tbx1, Nkx2-5, and Islet1 reveals a genetic switch for down-regulation in the myocardium. Proc Natl Acad Sci USA 2012; 109:18273-18280.
43. Bakker ML, Christoffels VM, Moorman AF. The cardiac pacemaker and conduction system develops from embryonic myocardium that retains its primitive phenotype. J Cardiovasc Pharmacol 2010; 56:6-15.
44. Liang X, Wang G, Lin L, et al. HCN4 dynamically marks the first heart field and conduction system precursors. Circ Res 2013; 113:399-407.
45. Spater D, Abramczuk MK, Buac K, et al. A HCN4+ cardiomyogenic progenitor derived from the first heart field and human pluripotent stem cells. Nat Cell Biol 2013; 15:1098-1106.
46. Miquerol L, Moreno-Rascon N, Beyer S, et al. Biphasic development of the mammalian ventricular conduction system. Circ Res 2010; 107:153-161.
47. Dhamoon AS, Jalife J. The inward rectifier current (IK1) controls cardiac excitability and is involved in arrhythmogenesis. Heart Rhythm 2005; 2:316-324.
48. Miake J, Marban E, Nuss HB. Biological pacemaker created by gene transfer. Nature 2002; 419:132-133.
49. Jones SA, Lancaster MK, Boyett MR. Ageing-related changes of connexins and conduction within the sinoatrial node. J Physiol 2004; 560(Part 2):429-437.
50. Kapoor N, Liang W, Marban E, et al. Direct conversion of quiescent cardiomyocytes to pacemaker cells by expression of Tbx18. Nat Biotechnol 2013; 31:54-62.
51. Bakker ML, Boink GJ, Boukens BJ, et al. T-box transcription factor TBX3 reprogrammes mature cardiac myocytes into pacemaker-like cells. Cardiovasc Res 2012; 94:439-449.
52. den Hoed M, Eijgelsheim M, Esko T, et al. Identification of heart rate-associated loci and their effects on cardiac conduction and rhythm disorders. Nat Genet 2013; 45:621-631.
53. Holm H, Gudbjartsson DF, Arnar DO, et al. Several common variants modulate heart rate, PR interval and QRS duration. Nat Genet 2010; 42:117-122.
54. Pfeufer A, van Noord C, Marciante KD, et al. Genome-wide association study of PR interval. Nat Genet 2010; 42:153-159.