CTCF Binding Polarity Determines Chromatin Looping

Molecular Cell

Volumn 60, Issue 4, 2015, Pages 676-684

  de Wit, Elzo ^a   Vos, Erica S M ^a   Holwerda, Sjoerd J B ^a   Valdes Quezada, Christian ^a   Verstegen, Marjon J A M ^a   Teunissen, Hans ^a   Splinter, Erik ^a   Wijchers, Patrick J ^a   Krijger, Peter H L ^a   de Laat, Wouter ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

COHESIN; HEMOGLOBIN BETA CHAIN; NUCLEOTIDE; TRANSCRIPTION FACTOR CTCF; TRANSCRIPTION FACTOR SOX2; CCCTC-BINDING FACTOR; CELL CYCLE PROTEIN; CHROMATIN; NONHISTONE PROTEIN; PROTEIN BINDING; REPRESSOR PROTEIN;

ANIMAL CELL; ARTICLE; BINDING SITE; CHROMATIN; CHROMATIN STRUCTURE; CONTROLLED STUDY; CRISPR CAS SYSTEM; GENE EXPRESSION; GENE LOCUS; MOLECULAR RECOGNITION; NONHUMAN; PROMOTER REGION; PROTEIN BINDING; TRANSCRIPTION INITIATION SITE; ANIMAL; CELL LINE; CHEMISTRY; CYTOLOGY; EMBRYONIC STEM CELL; METABOLISM; MOUSE;

ANIMALS; BINDING SITES; CELL CYCLE PROTEINS; CELL LINE; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; CRISPR-CAS SYSTEMS; EMBRYONIC STEM CELLS; MICE; PROTEIN BINDING; REPRESSOR PROTEINS;

EID: 84947765898     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.09.023     Document Type: Article

References (40)

1. Bickmore W.A., van Steensel B. Genome architecture: domain organization of interphase chromosomes. Cell 2013, 152:1270-1284.
2. Chen H., Tian Y., Shu W., Bo X., Wang S. Comprehensive identification and annotation of cell type-specific and ubiquitous CTCF-binding sites in the human genome. PLoS ONE 2012, 7:e41374.
3. de Laat W., Duboule D. Topology of mammalian developmental enhancers and their regulatory landscapes. Nature 2013, 502:499-506.
4. de Leeuw J., Hornik K., Mair P. Isotone Optimization in R: Pool-Adjacent-Violators Algorithm (PAVA) and Active Set Methods. J. Stat. Softw. 2009, 32:1-24.
5. Deng W., Lee J., Wang H., Miller J., Reik A., Gregory P.D., Dean A., Blobel G.A. Controlling long-range genomic interactions at a native locus by targeted tethering of a looping factor. Cell 2012, 149:1233-1244.
6. Dixon J.R., Selvaraj S., Yue F., Kim A., Li Y., Shen Y., Hu M., Liu J.S., Ren B. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 2012, 485:376-380.
7. Dowen J.M., Fan Z.P., Hnisz D., Ren G., Abraham B.J., Zhang L.N., Weintraub A.S., Schuijers J., Lee T.I., Zhao K., Young R.A. Control of cell identity genes occurs in insulated neighborhoods in mammalian chromosomes. Cell 2014, 159:374-387.
8. Faure A.J., Schmidt D., Watt S., Schwalie P.C., Wilson M.D., Xu H., Ramsay R.G., Odom D.T., Flicek P. Cohesin regulates tissue-specific expression by stabilizing highly occupied cis-regulatory modules. Genome Res. 2012, 22:2163-2175.
9. Gómez-Marín C., Tena J.J., Acemel R.D., López-Mayorga M., Naranjo S., de la Calle-Mustienes E., Maeso I., Beccari L., Aneas I., Vielmas E., et al. Evolutionary comparison reveals that diverging CTCF sites are signatures of ancestral topological associating domains borders. Proc. Natl. Acad. Sci. USA 2015, 112:7542-7547.
10. Guo Y., Xu Q., Canzio D., Shou J., Li J., Gorkin D.U., Jung I., Wu H., Zhai Y., Tang Y., et al. CRISPR Inversion of CTCF Sites Alters Genome Topology and Enhancer/Promoter Function. Cell 2015, 162:900-910.
11. Hadjur S., Williams L.M., Ryan N.K., Cobb B.S., Sexton T., Fraser P., Fisher A.G., Merkenschlager M. Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus. Nature 2009, 460:410-413.
12. Handoko L., Xu H., Li G., Ngan C.Y., Chew E., Schnapp M., Lee C.W., Ye C., Ping J.L., Mulawadi F., et al. CTCF-mediated functional chromatin interactome in pluripotent cells. Nat. Genet. 2011, 43:630-638.
13. Heath H., Ribeiro de Almeida C., Sleutels F., Dingjan G., van de Nobelen S., Jonkers I., Ling K.W., Gribnau J., Renkawitz R., Grosveld F., et al. CTCF regulates cell cycle progression of alphabeta T cells in the thymus. EMBO J. 2008, 27:2839-2850.
14. Kagey M.H., Newman J.J., Bilodeau S., Zhan Y., Orlando D.A., van Berkum N.L., Ebmeier C.C., Goossens J., Rahl P.B., Levine S.S., et al. Mediator and cohesin connect gene expression and chromatin architecture. Nature 2010, 467:430-435.
15. Kim T.H., Abdullaev Z.K., Smith A.D., Ching K.A., Loukinov D.I., Green R.D., Zhang M.Q., Lobanenkov V.V., Ren B. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 2007, 128:1231-1245.
16. Klein F.A., Pakozdi T., Anders S., Ghavi-Helm Y., Furlong E.E., Huber W. FourCSeq: analysis of 4C sequencing data. Bioinformatics 2015, 31:3085-3091.
17. Li Y., Rivera C.M., Ishii H., Jin F., Selvaraj S., Lee A.Y., Dixon J.R., Ren B. CRISPR reveals a distal super-enhancer required for Sox2 expression in mouse embryonic stem cells. PLoS ONE 2014, 9:e114485.
18. Nakahashi H., Kwon K.R., 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, 3:1678-1689.
19. Narendra V., Rocha P.P., An D., Raviram R., Skok J.A., Mazzoni E.O., Reinberg D. Transcription. CTCF establishes discrete functional chromatin domains at the Hox clusters during differentiation. Science 2015, 347:1017-1021.
20. Nora E.P., Lajoie B.R., Schulz E.G., Giorgetti L., Okamoto I., Servant N., Piolot T., van Berkum N.L., Meisig J., Sedat J., et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 2012, 485:381-385.
21. Ong C.T., Corces V.G. CTCF: an architectural protein bridging genome topology and function. Nat. Rev. Genet. 2014, 15:234-246.
22. Parelho V., Hadjur S., Spivakov M., Leleu M., Sauer S., Gregson H.C., Jarmuz A., Canzonetta C., Webster Z., Nesterova T., et al. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 2008, 132:422-433.
23. Phillips-Cremins J.E., Sauria M.E., Sanyal A., Gerasimova T.I., Lajoie B.R., Bell J.S., Ong C.T., Hookway T.A., Guo C., Sun Y., et al. Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 2013, 153:1281-1295.
24. Pugacheva E.M., Rivero-Hinojosa S., Espinoza C.A., Méndez-Catalá C.F., Kang S., Suzuki T., Kosaka-Suzuki N., Robinson S., Nagarajan V., Ye Z., et al. Comparative analyses of CTCF and BORIS occupancies uncover two distinct classes of CTCF binding genomic regions. Genome Biol. 2015, 16:161.
25. Ran F.A., Hsu P.D., Wright J., Agarwala V., Scott D.A., Zhang F. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 2013, 8:2281-2308.
26. Rao S.S., Huntley M.H., Durand N.C., Stamenova E.K., Bochkov I.D., Robinson J.T., Sanborn A.L., Machol I., Omer A.D., Lander E.S., Aiden E.L. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 2014, 159:1665-1680.
27. Rippe K., von Hippel P.H., Langowski J. Action at a distance: DNA-looping and initiation of transcription. Trends Biochem. Sci. 1995, 20:500-506.
28. Schmidt D., Schwalie P.C., Wilson M.D., Ballester B., Gonçalves A., Kutter C., Brown G.D., Marshall A., Flicek P., Odom D.T. Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell 2012, 148:335-348.
29. Seitan V.C., Faure A.J., Zhan Y., McCord R.P., Lajoie B.R., Ing-Simmons E., Lenhard B., Giorgetti L., Heard E., Fisher A.G., et al. Cohesin-based chromatin interactions enable regulated gene expression within preexisting architectural compartments. Genome Res. 2013, 23:2066-2077.
30. Sexton T., Yaffe E., Kenigsberg E., Bantignies F., Leblanc B., Hoichman M., Parrinello H., Tanay A., Cavalli G. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 2012, 148:458-472.
31. Sofueva S., Yaffe E., Chan W.C., Georgopoulou D., Vietri Rudan M., Mira-Bontenbal H., Pollard S.M., Schroth G.P., Tanay A., Hadjur S. Cohesin-mediated interactions organize chromosomal domain architecture. EMBO J. 2013, 32:3119-3129.
32. Splinter E., Heath H., Kooren J., Palstra R.J., Klous P., Grosveld F., Galjart N., de Laat W. CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus. Genes Dev. 2006, 20:2349-2354.
33. Splinter E., de Wit E., van de Werken H.J., Klous P., de Laat W. Determining long-range chromatin interactions for selected genomic sites using 4C-seq technology: from fixation to computation. Methods 2012, 58:221-230.
34. Symmons O., Uslu V.V., Tsujimura T., Ruf S., Nassari S., Schwarzer W., Ettwiller L., Spitz F. Functional and topological characteristics of mammalian regulatory domains. Genome Res. 2014, 24:390-400.
35. Vietri Rudan M., Barrington C., Henderson S., Ernst C., Odom D.T., Tanay A., Hadjur S. Comparative Hi-C reveals that CTCF underlies evolution of chromosomal domain architecture. Cell Rep. 2015, 10:1297-1309.
36. Wendt K.S., Yoshida K., Itoh T., Bando M., Koch B., Schirghuber E., Tsutsumi S., Nagae G., Ishihara K., Mishiro T., et al. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 2008, 451:796-801.
37. Whyte W.A., Orlando D.A., Hnisz D., Abraham B.J., Lin C.Y., Kagey M.H., Rahl P.B., Lee T.I., Young R.A. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 2013, 153:307-319.
38. Yaffe E., Tanay A. Probabilistic modeling of Hi-C contact maps eliminates systematic biases to characterize global chromosomal architecture. Nat. Genet. 2011, 43:1059-1065.
39. Zhou H.Y., Katsman Y., Dhaliwal N.K., Davidson S., Macpherson N.N., Sakthidevi M., Collura F., Mitchell J.A. A Sox2 distal enhancer cluster regulates embryonic stem cell differentiation potential. Genes Dev. 2014, 28:2699-2711.
40. Zuin J., Dixon J.R., van der Reijden M.I.J.A., Ye Z., Kolovos P., Brouwer R.W.W., van de Corput M.P.C., van de Werken H.J.G., Knoch T.A., van IJcken W.F.J., et al. Cohesin and CTCF differentially affect chromatin architecture and gene expression in human cells. Proc. Natl. Acad. Sci. USA 2014, 111:996-1001.