CTCF counter-regulates cardiomyocyte development and maturation programs in the embryonic heart

PLoS Genetics

Volumn 13, Issue 8, 2017, Pages

  Gomez Velazquez, Melisa ^a   Badia Careaga, Claudio ^a   Lechuga Vieco, Ana Victoria ^a   Nieto Arellano, Rocio ^a   Tena, Juan J ^b   Rollan, Isabel ^a   Alvarez, Alba ^a   Torroja, Carlos ^a   Caceres, Eva F ^a,g   Roy, Anna ^c,d   Galjart, Niels ^e   Delgado Olguin, Paul ^c,d,f   Sanchez Cabo, Fatima ^a   Enriquez, Jose Antonio ^a   Gomez Skarmeta, Jose Luis ^b   Manzanares, Miguel ^a  

^a CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^b UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e ERASMUS MEDICAL CENTER   (Netherlands)

^f HEART AND STROKE FOUNDATION OF CANADA   (Canada)

^g UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR CTCF; CCCTC-BINDING FACTOR; CHROMATIN; PROTEIN BINDING; REPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARDIAC MUSCLE CELL; CELL DIFFERENTIATION; CELL MATURATION; CHROMATIN; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONTROLLED STUDY; CTCF GENE; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; ENHANCER REGION; GENE; GENE EXPRESSION; HEART DEVELOPMENT; HEART MITOCHONDRION; IRX4 GENE; MOUSE; NONHUMAN; PROMOTER REGION; UPREGULATION; ANIMAL; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEART; HEART VENTRICLE; METABOLISM; MITOCHONDRION; ORGANOGENESIS; TRANSCRIPTION INITIATION;

ANIMALS; CELL DIFFERENTIATION; CHROMATIN; EMBRYONIC DEVELOPMENT; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; HEART VENTRICLES; MICE; MITOCHONDRIA; ORGANOGENESIS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REPRESSOR PROTEINS; TRANSCRIPTIONAL ACTIVATION;

EID: 85028885948     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1006985     Document Type: Article

References (58)

1. Olson EN, Gene regulatory networks in the evolution and development of the heart. Science. 2006;313(5795):1922–7. doi: 10.1126/science.1132292 17008524
2. Hirschy A, Schatzmann F, Ehler E, Perriard JC, Establishment of cardiac cytoarchitecture in the developing mouse heart. Dev Biol. 2006;289(2):430–41. doi: 10.1016/j.ydbio.2005.10.046 16337936
3. Hom JR, Quintanilla RA, Hoffman DL, de Mesy Bentley KL, Molkentin JD, Sheu SS, et al. The permeability transition pore controls cardiac mitochondrial maturation and myocyte differentiation. Dev Cell. 2011;21(3):469–78. doi: 10.1016/j.devcel.2011.08.008 21920313
4. Beutner G, Eliseev RA, Porter GA, JrInitiation of electron transport chain activity in the embryonic heart coincides with the activation of mitochondrial complex 1 and the formation of supercomplexes. PLoS One. 2014;9(11):e113330. doi: 10.1371/journal.pone.0113330 25427064
5. Soonpaa MH, Kim KK, Pajak L, Franklin M, Field LJ, Cardiomyocyte DNA synthesis and binucleation during murine development. Am J Physiol. 1996;271(5 Pt 2):H2183–9. 8945939
6. Bruneau BG, Transcriptional regulation of vertebrate cardiac morphogenesis. Circ Res. 2002;90(5):509–19. 11909814
7. Paige SL, Thomas S, Stoick-Cooper CL, Wang H, Maves L, Sandstrom R, et al. A temporal chromatin signature in human embryonic stem cells identifies regulators of cardiac development. Cell. 2012;151(1):221–32. doi: 10.1016/j.cell.2012.08.027 22981225
8. Wamstad JA, Alexander JM, Truty RM, Shrikumar A, Li F, Eilertson KE, et al. Dynamic and coordinated epigenetic regulation of developmental transitions in the cardiac lineage. Cell. 2012;151(1):206–20. doi: 10.1016/j.cell.2012.07.035 22981692
9. Consortium EP, An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489(7414):57–74. doi: 10.1038/nature11247 22955616
10. Shen Y, Yue F, McCleary DF, Ye Z, Edsall L, Kuan S, et al. A map of the cis-regulatory sequences in the mouse genome. Nature. 2012;488(7409):116–20. doi: 10.1038/nature11243 22763441
11. de Wit E, de Laat W, A decade of 3C technologies: insights into nuclear organization. Genes Dev. 2012;26(1):11–24. doi: 10.1101/gad.179804.111 22215806
12. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature. 2012;485(7398):376–80. doi: 10.1038/nature11082 22495300
13. Jin F, Li Y, Dixon JR, Selvaraj S, Ye Z, Lee AY, et al. A high-resolution map of the three-dimensional chromatin interactome in human cells. Nature. 2013;503(7475):290–4. doi: 10.1038/nature12644 24141950
14. Bonora G, Plath K, Denholtz M, A mechanistic link between gene regulation and genome architecture in mammalian development. Curr Opin Genet Dev. 2014;27:92–101. doi: 10.1016/j.gde.2014.05.002 24998386
15. Ong CT, Corces VG, CTCF: an architectural protein bridging genome topology and function. Nat Rev Genet. 2014;15(4):234–46. doi: 10.1038/nrg3663 24614316
16. Rao SS, Huntley MH, Durand NC, Stamenova EK, Bochkov ID, Robinson JT, et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell. 2014;159(7):1665–80. doi: 10.1016/j.cell.2014.11.021 25497547
17. Heath H, Ribeiro de Almeida C, Sleutels F, Dingjan G, van de Nobelen S, Jonkers I, et al. CTCF regulates cell cycle progression of alphabeta T cells in the thymus. EMBO J. 2008;27(21):2839–50. doi: 10.1038/emboj.2008.214 18923423
18. Wan LB, Pan H, Hannenhalli S, Cheng Y, Ma J, Fedoriw A, et al. Maternal depletion of CTCF reveals multiple functions during oocyte and preimplantation embryo development. Development. 2008;135(16):2729–38. doi: 10.1242/dev.024539 18614575
19. Moore JM, Rabaia NA, Smith LE, Fagerlie S, Gurley K, Loukinov D, et al. Loss of maternal CTCF is associated with peri-implantation lethality of Ctcf null embryos. PLoS One. 2012;7(4):e34915. doi: 10.1371/journal.pone.0034915 22532833
20. Soshnikova N, Montavon T, Leleu M, Galjart N, Duboule D, Functional analysis of CTCF during mammalian limb development. Dev Cell. 2010;19(6):819–30. doi: 10.1016/j.devcel.2010.11.009 21145498
21. Watson LA, Wang X, Elbert A, Kernohan KD, Galjart N, Berube NG, Dual effect of CTCF loss on neuroprogenitor differentiation and survival. J Neurosci. 2014;34(8):2860–70. doi: 10.1523/JNEUROSCI.3769-13.2014 24553927
22. Hirayama T, Tarusawa E, Yoshimura Y, Galjart N, Yagi T, CTCF is required for neural development and stochastic expression of clustered Pcdh genes in neurons. Cell Rep. 2012;2(2):345–57. doi: 10.1016/j.celrep.2012.06.014 22854024
23. Stanley EG, Biben C, Elefanty A, Barnett L, Koentgen F, Robb L, et al. Efficient Cre-mediated deletion in cardiac progenitor cells conferred by a 3'UTR-ires-Cre allele of the homeobox gene Nkx2-5. Int J Dev Biol. 2002;46(4):431–9. 12141429
24. Quitschke WW, Taheny MJ, Fochtmann LJ, Vostrov AA, Differential effect of zinc finger deletions on the binding of CTCF to the promoter of the amyloid precursor protein gene. Nucleic Acids Res. 2000;28(17):3370–8. 10954607
25. Nikolic T, Movita D, Lambers ME, Ribeiro de Almeida C, Biesta P, Kreefft K, et al. The DNA-binding factor Ctcf critically controls gene expression in macrophages. Cell Mol Immunol. 2014;11(1):58–70. doi: 10.1038/cmi.2013.41 24013844
26. Nora EP, Goloborodko A, Valton A-L, Gibcus JH, Uebersohn A, Abdennur N, et al. Targeted Degradation of CTCF Decouples Local Insulation of Chromosome Domains from Genomic Compartmentalization. Cell. 2017;169(5):930–44.e22. doi: 10.1016/j.cell.2017.05.004 28525758
27. Kemp CJ, Moore JM, Moser R, Bernard B, Teater M, Smith LE, et al. CTCF haploinsufficiency destabilizes DNA methylation and predisposes to cancer. Cell Rep. 2014;7(4):1020–9. doi: 10.1016/j.celrep.2014.04.004 24794443
28. Huang da W, Sherman BT, Lempicki RA, Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44–57. doi: 10.1038/nprot.2008.211 19131956
29. Dorn GW, 2ndVega RB, Kelly DP, Mitochondrial biogenesis and dynamics in the developing and diseased heart. Genes Dev. 2015;29(19):1981–91. doi: 10.1101/gad.269894.115 26443844
30. Phillips JE, Corces VG, CTCF: master weaver of the genome. Cell. 2009;137(7):1194–211. doi: 10.1016/j.cell.2009.06.001 19563753
31. Yaguchi T, Aida S, Kaul SC, Wadhwa R, Involvement of mortalin in cellular senescence from the perspective of its mitochondrial import, chaperone, and oxidative stress management functions. Ann N Y Acad Sci. 2007;1100:306–11. doi: 10.1196/annals.1395.032 17460192
32. Falkenberg M, Larsson NG, Gustafsson CM, DNA replication and transcription in mammalian mitochondria. Annu Rev Biochem. 2007;76:679–99. doi: 10.1146/annurev.biochem.76.060305.152028 17408359
33. Guaras A, Perales-Clemente E, Calvo E, Acin-Perez R, Loureiro-Lopez M, Pujol C, et al. The CoQH2/CoQ Ratio Serves as a Sensor of Respiratory Chain Efficiency. Cell Rep. 2016;15(1):197–209. doi: 10.1016/j.celrep.2016.03.009 27052170
34. Bruneau BG, Bao ZZ, Fatkin D, Xavier-Neto J, Georgakopoulos D, Maguire CT, et al. Cardiomyopathy in Irx4-deficient mice is preceded by abnormal ventricular gene expression. Mol Cell Biol. 2001;21(5):1730–6. doi: 10.1128/MCB.21.5.1730-1736.2001 11238910
35. Bao ZZ, Bruneau BG, Seidman JG, Seidman CE, Cepko CL, Regulation of chamber-specific gene expression in the developing heart by Irx4. Science. 1999;283(5405):1161–4. 10024241
36. Gomez-Skarmeta JL, Modolell J, Iroquois genes: genomic organization and function in vertebrate neural development. Curr Opin Genet Dev. 2002;12(4):403–8. 12100884
37. Kim KH, Rosen A, Bruneau BG, Hui CC, Backx PH, Iroquois homeodomain transcription factors in heart development and function. Circ Res. 2012;110(11):1513–24. doi: 10.1161/CIRCRESAHA.112.265041 22628575
38. Tena JJ, Alonso ME, de la Calle-Mustienes E, Splinter E, de Laat W, Manzanares M, et al. An evolutionarily conserved three-dimensional structure in the vertebrate Irx clusters facilitates enhancer sharing and coregulation. Nat Commun. 2011;2:310. doi: 10.1038/ncomms1301 21556064
39. Simonis M, Kooren J, de Laat W, An evaluation of 3C-based methods to capture DNA interactions. Nat Methods. 2007;4(11):895–901. doi: 10.1038/nmeth1114 17971780
40. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, et al. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339(6121):819–23. doi: 10.1126/science.1231143 23287718
41. Dowen JM, Fan ZP, Hnisz D, Ren G, Abraham BJ, Zhang LN, et al. Control of cell identity genes occurs in insulated neighborhoods in mammalian chromosomes. Cell. 2014;159(2):374–87. doi: 10.1016/j.cell.2014.09.030 25303531
42. Zuin J, Dixon JR, van der Reijden MI, Ye Z, Kolovos P, Brouwer RW, et al. Cohesin and CTCF differentially affect chromatin architecture and gene expression in human cells. Proc Natl Acad Sci U S A. 2014;111(3):996–1001. doi: 10.1073/pnas.1317788111 24335803
43. Smallwood A, Ren B, Genome organization and long-range regulation of gene expression by enhancers. Curr Opin Cell Biol. 2013;25(3):387–94. doi: 10.1016/j.ceb.2013.02.005 23465541
44. Martin D, Pantoja C, Fernandez Minan A, Valdes-Quezada C, Molto E, Matesanz F, et al. Genome-wide CTCF distribution in vertebrates defines equivalent sites that aid the identification of disease-associated genes. Nat Struct Mol Biol. 2011;18(6):708–14. doi: 10.1038/nsmb.2059 21602820
45. Sams DS, Nardone S, Getselter D, Raz D, Tal M, Rayi PR, et al. Neuronal CTCF Is Necessary for Basal and Experience-Dependent Gene Regulation, Memory Formation, and Genomic Structure of BDNF and Arc. Cell Rep. 2016;17(9):2418–30. doi: 10.1016/j.celrep.2016.11.004 27880914
46. Brand NJ, Lara-Pezzi E, Rosenthal N, Barton PJ, Analysis of cardiac myocyte biology in transgenic mice: a protocol for preparation of neonatal mouse cardiac myocyte cultures. Methods Mol Biol. 2010;633:113–24. doi: 10.1007/978-1-59745-019-5_9 20204624
47. Luna-Zurita L, Prados B, Grego-Bessa J, Luxan G, del Monte G, Benguria A, et al. Integration of a Notch-dependent mesenchymal gene program and Bmp2-driven cell invasiveness regulates murine cardiac valve formation. J Clin Invest. 2010;120(10):3493–507. doi: 10.1172/JCI42666 20890042
48. Bosse A, Zulch A, Becker MB, Torres M, Gomez-Skarmeta JL, Modolell J, et al. Identification of the vertebrate Iroquois homeobox gene family with overlapping expression during early development of the nervous system. Mech Dev. 1997;69(1–2):169–81. 9486539
49. Huang da W, Sherman BT, Lempicki RA, Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009;37(1):1–13. doi: 10.1093/nar/gkn923 19033363
50. Pohl A, Beato M, bwtool: a tool for bigWig files. Bioinformatics. 2014;30(11):1618–9. doi: 10.1093/bioinformatics/btu056 24489365
51. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010;38(4):576–89. doi: 10.1016/j.molcel.2010.05.004 20513432
52. Fernandez-Vizarra E, Lopez-Perez MJ, Enriquez JA, Isolation of biogenetically competent mitochondria from mammalian tissues and cultured cells. Methods. 2002;26(4):292–7. doi: 10.1016/S1046-2023(02)00034-8 12054919
53. Schagger H, Native electrophoresis for isolation of mitochondrial oxidative phosphorylation protein complexes. Methods Enzymol. 1995;260:190–202. 8592444
54. Latorre-Pellicer A, Moreno-Loshuertos R, Lechuga-Vieco AV, Sanchez-Cabo F, Torroja C, Acin-Perez R, et al. Mitochondrial and nuclear DNA matching shapes metabolism and healthy ageing. Nature. 2016;535(7613):561–5. doi: 10.1038/nature18618 27383793
55. van de Werken HJ, Landan G, Holwerda SJ, Hoichman M, Klous P, Chachik R, et al. Robust 4C-seq data analysis to screen for regulatory DNA interactions. Nat Methods. 2012;9(10):969–72. doi: 10.1038/nmeth.2173 22961246
56. van Weerd JH, Badi I, van den Boogaard M, Stefanovic S, van de Werken HJ, Gomez-Velazquez M, et al. A large permissive regulatory domain exclusively controls Tbx3 expression in the cardiac conduction system. Circ Res. 2014;115(4):432–41. doi: 10.1161/CIRCRESAHA.115.303591 24963028
57. Robinson MD, McCarthy DJ, Smyth GK, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139–40. doi: 10.1093/bioinformatics/btp616 19910308
58. Klein FA, Pakozdi T, Anders S, Ghavi-Helm Y, Furlong EE, Huber W, FourCSeq: analysis of 4C sequencing data. Bioinformatics. 2015;31(19):3085–91. doi: 10.1093/bioinformatics/btv335 26034064