The ubiquitous transcription factor CTCF promotes lineage-specific epigenomic remodeling and establishment of transcriptional networks driving cell differentiation

References

• Jin F, Li Y, Dixon JR, Selvaraj S, Ye Z, Lee AY, Yen C, Schmitt AD, Espinoza CA, Ren B. A high-resolution map of the three-dimensional chromatin interactome in human cells. Nature 2013; 503: 290-4; PMID:24141950
   PubMed Web of Science ®Google Scholar
• Heidari N, Phanstiel DH, He C, Grubert F, Jahanbanian F, Kasowski M, Zhang MQ, Snyder MP. Genome-wide map of regulatory interactions in the human genome. Genome Res 2014; PMID:25228660
   PubMedGoogle Scholar
• Magnani L, Eeckhoute J, Lupien M. Pioneer factors: directing transcriptional regulators within the chromatin environment. Trends Genet 2011; 27: 465-74; PMID:21885149; http://dx.doi.org/10.1016/j.tig.2011.07.002
   PubMed Web of Science ®Google Scholar
• Zaret KS, Carroll JS. Pioneer transcription factors: establishing competence for gene expression. Genes Dev 2011; 25: 2227-41; PMID:22056668; http://dx.doi.org/10.1101/gad.176826.111
   PubMed Web of Science ®Google Scholar
• Siersbæk R, Rabiee A, Nielsen R, Sidoli S, Traynor S, Loft A, La Cour Poulsen L, Rogowska-Wrzesinska A, Jensen ON, Mandrup S. Transcription factor cooperativity in early adipogenic hotspots and super-enhancers. Cell Rep 2014; 7: 1443-55; PMID:24857652; http://dx.doi.org/10.1016/j.celrep.2014.04.042
   PubMed Web of Science ®Google Scholar
• Madsen MS, Siersbæk R, Boergesen M, Nielsen R, Mandrup S. Peroxisome proliferator-activated receptor γ and C/EBPα synergistically activate key metabolic adipocyte genes by assisted loading. Mol Cell Biol 2014; 34: 939-54; PMID:24379442; http://dx.doi.org/10.1128/MCB.01344-13
   PubMed Web of Science ®Google Scholar
• Voss TC, Schiltz RL, Sung M, Yen PM, Stamatoyannopoulos JA, Biddie SC, Johnson TA, Miranda TB, John S, Hager GL. Dynamic exchange at regulatory elements during chromatin remodeling underlies assisted loading mechanism. Cell 2011; 146: 544-54; PMID:21835447; http://dx.doi.org/10.1016/j.cell.2011.07.006
   PubMed Web of Science ®Google Scholar
• Mikkelsen TS, Xu Z, Zhang X, Wang L, Gimble JM, Lander ES, Rosen ED. Comparative epigenomic analysis of murine and human adipogenesis. Cell 2010; 143: 156-69; PMID:20887899; http://dx.doi.org/10.1016/j.cell.2010.09.006
   PubMed Web of Science ®Google Scholar
• Steger DJ, Grant GR, Schupp M, Tomaru T, Lefterova MI, Schug J, Manduchi E, Stoeckert CJJ, Lazar MA. Propagation of adipogenic signals through an epigenomic transition state. Genes Dev 2010; 24: 1035-44; PMID:20478996; http://dx.doi.org/10.1101/gad.1907110
   PubMed Web of Science ®Google Scholar
• Siersbæk R, Nielsen R, John S, Sung M, Baek S, Loft A, Hager GL, Mandrup S. Extensive chromatin remodelling and establishment of transcription factor 'hotspots' during early adipogenesis. EMBO J 2011; 30: 1459-72; PMID:21427703; http://dx.doi.org/10.1038/emboj.2011.65
   PubMed Web of Science ®Google Scholar
• Sérandour AA, Avner S, Percevault F, Demay F, Bizot M, Lucchetti-Miganeh C, Barloy-Hubler F, Brown M, Lupien M, Métivier R, et al. Epigenetic switch involved in activation of pioneer factor FOXA1-dependent enhancers. Genome Res 2011; 21: 555-65; PMID:21233399; http://dx.doi.org/10.1101/gr.111534.110
   PubMed Web of Science ®Google Scholar
• Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, Schöler A, van Nimwegen E, Wirbelauer C, Oakeley EJ, Gaidatzis D, et al. DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 2011; 480: 490-5; PMID:22170606
   PubMed Web of Science ®Google Scholar
• Oger F, Dubois-Chevalier J, Gheeraert C, Avner S, Durand E, Froguel P, Salbert G, Staels B, Lefebvre P, Eeckhoute J. Peroxisome proliferator-activated receptor γ (PPARγ) regulates genes involved in insulin/IGF signalling and lipid metabolism during adipogenesis through functionally distinct enhancer classes. J Biol Chem 2014; 289: 708-722; PMID:24288131; http://dx.doi.org/10.1074/jbc.M113.526996
   PubMedGoogle Scholar
• Sérandour AA, Avner S, Oger F, Bizot M, Percevault F, Lucchetti-Miganeh C, Palierne G, Gheeraert C, Barloy-Hubler F, Péron CL, et al. Dynamic hydroxymethylation of deoxyribonucleic acid marks differentiation-associated enhancers. Nucleic Acids Res 2012; 40: 8255-65; PMID:22730288; http://dx.doi.org/10.1093/nar/gks595
   PubMed Web of Science ®Google Scholar
• Pastor WA, Aravind L, Rao A. TETonic shift: biological roles of TET proteins in DNA demethylation and transcription. Nat Rev Mol Cell Biol 2013; 14: 341-56; PMID:23698584; http://dx.doi.org/10.1038/nrm3589
   PubMed Web of Science ®Google Scholar
• Hon GC, Song C, Du T, Jin F, Selvaraj S, Lee AY, Yen C, Ye Z, Mao S, Wang B, et al. 5mC Oxidation by Tet2 Modulates Enhancer Activity and Timing of Transcriptome Reprogramming during Differentiation. Mol Cell 2014; 56: 286-97; PMID:25263596; http://dx.doi.org/10.1016/j.molcel.2014.08.026
   PubMed Web of Science ®Google Scholar
• Bachman M, Uribe-Lewis S, Yang X, Williams M, Murrel A, Balasubramanian S. 5-Hydroxymethylcytosine is a predominantly stable DNA modification. Nat Chem 2014; PMID:25411882; http://dx.doi.org/10.1038/nchem.2064
   PubMedGoogle Scholar
• Spruijt CG, Gnerlich F, Smits AH, Pfaffeneder T, Jansen PWTC, Bauer C, Münzel M, Wagner M, Müller M, Khan F, et al. Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell 2013; 152: 1146-59; PMID:23434322; http://dx.doi.org/10.1016/j.cell.2013.02.004
   PubMed Web of Science ®Google Scholar
• Lu F, Liu Y, Jiang L, Yamaguchi S, Zhang Y. Role of Tet proteins in enhancer activity and telomere elongation. Genes Dev 2014; 28:2103-19; PMID:25223896; http://dx.doi.org/10.1101/gad.248005.114
   PubMed Web of Science ®Google Scholar
• Fujiki K, Shinoda A, Kano F, Sato R, Shirahige K, Murata M. PPARγ-induced PARylation promotes local DNA demethylation by production of 5-hydroxymethylcytosine. Nat Commun 2013; 4: 2262; PMID:23912449; http://dx.doi.org/10.1038/ncomms3262
   PubMedGoogle Scholar
• Vaquerizas JM, Kummerfeld SK, Teichmann SA, Luscombe NM. A census of human transcription factors: function, expression and evolution. Nat. Rev. Genet. 2009; 10: 252-63; PMID:19274049; http://dx.doi.org/10.1038/nrg2538
   PubMed Web of Science ®Google Scholar
• Dubois-Chevalier J, Oger F, Dehondt H, Firmin FF, Gheeraert C, Staels B, Lefebvre P, Eeckhoute J. A dynamic CTCF chromatin binding landscape promotes DNA hydroxymethylation and transcriptional induction of adipocyte differentiation. Nucleic Acids Res. 2014; 42: 10943-59; PMID:25183525; http://dx.doi.org/10.1093/nar/gku780
   PubMed Web of Science ®Google Scholar
• Zlatanova J, Caiafa P. CTCF and its protein partners: divide and rule?. J. Cell. Sci. 2009; 122: 1275-84; PMID:19386894; http://dx.doi.org/10.1242/jcs.039990
   PubMedGoogle Scholar
• Fu Y, Sinha M, Peterson CL, Weng Z. The insulator binding protein CTCF positions 20 nucleosomes around its binding sites across the human genome. PLoS Genet. 2008; 4: e1000138; PMID:18654629; http://dx.doi.org/10.1371/journal.pgen.1000138
   PubMed Web of Science ®Google Scholar
• Shen Y, Yue F, McCleary DF, Ye Z, Edsall L, Kuan S, Wagner U, Dixon J, Lee L, Lobanenkov VV, et al. A map of the cis-regulatory sequences in the mouse genome. Nature 2012; 488: 116-20; PMID:22763441; http://dx.doi.org/10.1038/nature11243
   PubMed Web of Science ®Google Scholar
• Lee B, Bhinge AA, Battenhouse A, McDaniell RM, Liu Z, Song L, Ni Y, Birney E, Lieb JD, Furey TS, et al. Cell-type specific and combinatorial usage of diverse transcription factors revealed by genome-wide binding studies in multiple human cells. Genome Res. 2012; 22: 9-24; PMID:22090374; http://dx.doi.org/10.1101/gr.127597.111
   PubMed Web of Science ®Google Scholar
• Calero-Nieto FJ, Ng FS, Wilson NK, Hannah R, Moignard V, Leal-Cervantes AI, Jimenez-Madrid I, Diamanti E, Wernisch L, Göttgens B. Key regulators control distinct transcriptional programmes in blood progenitor and mast cells. EMBO J. 2014; 33: 1212-26; PMID:24760698
   PubMed Web of Science ®Google Scholar
• Sheffield NC, Thurman RE, Song L, Safi A, Stamatoyannopoulos JA, Lenhard B, Crawford GE, Furey TS. Patterns of regulatory activity across diverse human cell types predict tissue identity, transcription factor binding, and long-range interactions. Genome Res. 2013; 23: 777-88; PMID:23482648; http://dx.doi.org/10.1101/gr.152140.112
   PubMed Web of Science ®Google Scholar
• Herold M, Bartkuhn M, Renkawitz R. CTCF: insights into insulator function during development. Development 2012; 139: 1045-57; PMID:22354838; http://dx.doi.org/10.1242/dev.065268
   PubMed Web of Science ®Google Scholar
• Wang H, Maurano MT, Qu H, Varley KE, Gertz J, Pauli F, Lee K, Canfield T, Weaver M, Sandstrom R, et al. Widespread plasticity in CTCF occupancy linked to DNA methylation. Genome Res. 2012; 22: 1680-8; PMID:22955980; http://dx.doi.org/10.1101/gr.136101.111
   PubMed Web of Science ®Google Scholar
• Essien K, Vigneau S, Apreleva S, Singh LN, Bartolomei MS, Hannenhalli S. CTCF binding site classes exhibit distinct evolutionary, genomic, epigenomic and transcriptomic features. Genome Biol. 2009; 10: R131; PMID:19922652
   PubMed Web of Science ®Google Scholar
• Oldfield AJ, Yang P, Conway AE, Cinghu S, Freudenberg JM, Yellaboina S, Jothi R. Histone-Fold Domain Protein NF-Y Promotes Chromatin Accessibility for Cell Type-Specific Master Transcription Factors. Mol Cell 2014; 55: 708-22; PMID:25132174; http://dx.doi.org/10.1016/j.molcel.2014.07.005
   PubMedGoogle Scholar
• Nakahashi H, Kwon KK, Resch W, Vian L, Dose M, Stavreva D, Hakim O, Pruett N, Nelson S, Yamane A, et al. A genome-wide map of CTCF multivalency redefines the CTCF code. Cell Rep 2013; 3: 1678-89; PMID:23707059; http://dx.doi.org/10.1016/j.celrep.2013.04.024
   PubMed Web of Science ®Google Scholar
• Schmidt D, Schwalie PC, Wilson MD, Ballester B, Gonçalves A, Kutter C, Brown GD, Marshall A, Flicek P, Odom DT. Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell 2012; 148: 335-48; PMID:22244452; http://dx.doi.org/10.1016/j.cell.2011.11.058
   PubMed Web of Science ®Google Scholar
• Weth O, Renkawitz R. CTCF function is modulated by neighboring DNA binding factors. Biochem. Cell Biol. 2011; 89: 459-68; PMID:21895576; http://dx.doi.org/10.1139/o11-033
   PubMedGoogle Scholar
• Davidson EH. The uncommon roles of common gene regulatory factors in the genomes of differentiating cells. EMBO J 2014; 33: 1193-4; PMID:24788410; http://dx.doi.org/10.1002/embj.201488693
   PubMedGoogle Scholar
• Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 2010; 38: 576-89
   PubMed Web of Science ®Google Scholar
• Métivier R, Penot G, Hübner MR, Reid G, Brand H, Kos M, Gannon F. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 2003; 115: 751-63; PMID:14675539; http://dx.doi.org/10.1016/S0092-8674(03)00934-6
   PubMed Web of Science ®Google Scholar
• Quintin J, Le Péron C, Palierne G, Bizot M, Cunha S, Sérandour AA, Avner S, Henry C, Percevault F, Belaud-Rotureau M, et al. Dynamic estrogen receptor interactomes control estrogen-responsive trefoil Factor (TFF) locus cell-specific activities. Mol Cell Biol 2014; 34: 2418-36; PMID:24752895; http://dx.doi.org/10.1128/MCB.00918-13
   PubMedGoogle Scholar
• Weth O, Paprotka C, Günther K, Schulte A, Baierl M, Leers J, Galjart N, Renkawitz R. CTCF induces histone variant incorporation, erases the H3K27me3 histone mark and opens chromatin. Nucleic Acids Res 2014; 42: 11941-51; PMID:25294833; http://dx.doi.org/10.1093/nar/gku937
   PubMedGoogle Scholar
• Magbanua JP, Runneburger E, Russell S, White R. A variably occupied CTCF binding site in the Ultrabithorax gene in the Drosophila Bithorax Complex. Mol Cell Biol 2014; PMID:25368383
   PubMedGoogle Scholar
• Feldmann A, Ivanek R, Murr R, Gaidatzis D, Burger L, Schübeler D. Transcription factor occupancy can mediate active turnover of DNA methylation at regulatory regions. PLoS Genet. 2013; 9: e1003994; PMID:24367273
   PubMed Web of Science ®Google Scholar
• Teif VB, Beshnova DA, Vainshtein Y, Marth C, Mallm J, Höfer T, Rippe K. Nucleosome repositioning links DNA (de)methylation and differential CTCF binding during stem cell development. Genome Res. 2014; 24: 1285-95; PMID:24812327; http://dx.doi.org/10.1101/gr.164418.113
   PubMed Web of Science ®Google Scholar
• Odom DT, Dowell RD, Jacobsen ES, Nekludova L, Rolfe PA, Danford TW, Gifford DK, Fraenkel E, Bell GI, Young RA. Core transcriptional regulatory circuitry in human hepatocytes. Mol. Syst. Biol. 2006; 2: 2006.0017; PMID:16738562; http://dx.doi.org/10.1038/msb4100059
   PubMedGoogle Scholar
• Eeckhoute J, Oger F, Staels B, Lefebvre P. Coordinated regulation of PPARγ expression and activity through control of chromatin structure in adipogenesis and obesity. PPAR Res 2012; 2012: 164140; PMID:22991504; http://dx.doi.org/10.1155/2012/164140
   PubMedGoogle Scholar
• Siersbæk R, Nielsen R, Mandrup S. Transcriptional networks and chromatin remodeling controlling adipogenesis. Trends Endocrinol. Metab. 2011; 23: 56-64; PMID:22079269; http://dx.doi.org/10.1016/j.tem.2011.10.001
   PubMedGoogle Scholar
• Delgado-Olguín P, Brand-Arzamendi K, Scott IC, Jungblut B, Stainier DY, Bruneau BG, Recillas-Targa F. CTCF promotes muscle differentiation by modulating the activity of myogenic regulatory factors. J. Biol. Chem. 2011; 286: 12483-94; PMID:21288905; http://dx.doi.org/10.1074/jbc.M110.164574
   PubMedGoogle Scholar
• Neph S, Stergachis AB, Reynolds A, Sandstrom R, Borenstein E, Stamatoyannopoulos JA. Circuitry and dynamics of human transcription factor regulatory networks. Cell 2012; 150: 1274-86; PMID:22959076; http://dx.doi.org/10.1016/j.cell.2012.04.040
   PubMed Web of Science ®Google Scholar