1932

Abstract

Genome function, replication, integrity, and propagation rely on the dynamic structural organization of chromosomes during the cell cycle. Genome folding in interphase provides regulatory segmentation for appropriate transcriptional control, facilitates ordered genome replication, and contributes to genome integrity by limiting illegitimate recombination. Here, we review recent high-resolution chromosome conformation capture and functional studies that have informed models of the spatial and regulatory compartmentalization of mammalian genomes, and discuss mechanistic models for how CTCF and cohesin control the functional architecture of mammalian chromosomes.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genom-083115-022339
2016-08-31
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/genom/17/1/annurev-genom-083115-022339.html?itemId=/content/journals/10.1146/annurev-genom-083115-022339&mimeType=html&fmt=ahah

Literature Cited

  1. Alipour E, Marko JF. 1.  2012. Self-organization of domain structures by DNA-loop-extruding enzymes. Nucleic Acids Res. 40:11202–12 [Google Scholar]
  2. Austenaa LM, Barozzi I, Simonatto M, Masella S, Della Chiara G. 2.  et al. 2015. Transcription of mammalian cis-regulatory elements is restrained by actively enforced early termination. Mol. Cell 60:460–74 [Google Scholar]
  3. Battulin N, Fishman VS, Mazur AM, Pomaznoy M, Khabarova AA. 3.  et al. 2015. Comparison of the three-dimensional organization of sperm and fibroblast genomes using the Hi-C approach. Genome Biol. 16:77 [Google Scholar]
  4. Baù D, Sanyal A, Lajoie BR, Capriotti E, Byron M. 4.  et al. 2011. The three-dimensional folding of the α-globin gene domain reveals formation of chromatin globules. Nat. Struct. Mol. Biol. 18:107–14 [Google Scholar]
  5. Bell AC, Felsenfeld G. 5.  2000. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405:482–85 [Google Scholar]
  6. Bell AC, West AG, Felsenfeld G. 6.  1999. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 98:387–96 [Google Scholar]
  7. Benner C, Isoda T, Murre C. 7.  2015. New roles for DNA cytosine modification, eRNA, anchors, and superanchors in developing B cell progenitors. PNAS 112:12776–81 [Google Scholar]
  8. Beygo J, Citro V, Sparago A, De Crescenzo A, Cerrato F. 8.  et al. 2013. The molecular function and clinical phenotype of partial deletions of the IGF2/H19 imprinting control region depends on the spatial arrangement of the remaining CTCF-binding sites. Hum. Mol. Genet. 22:544–57 [Google Scholar]
  9. Bickmore WA, van Steensel B. 9.  2013. Genome architecture: domain organization of interphase chromosomes. Cell 152:1270–84 [Google Scholar]
  10. Blewitt ME, Gendrel AV, Pang Z, Sparrow DB, Whitelaw N. 10.  et al. 2008. SmcHD1, containing a structural-maintenance-of-chromosomes hinge domain, has a critical role in X inactivation. Nat. Genet. 40:663–69 [Google Scholar]
  11. Burcin M, Arnold R, Lutz M, Kaiser B, Runge D. 11.  et al. 1997. Negative protein 1, which is required for function of the chicken lysozyme gene silencer in conjunction with hormone receptors, is identical to the multivalent zinc finger repressor CTCF. Mol. Cell. Biol. 17:1281–88 [Google Scholar]
  12. Calabrese JM, Sun W, Song L, Mugford JW, Williams L. 12.  et al. 2012. Site-specific silencing of regulatory elements as a mechanism of X inactivation. Cell 151:951–63 [Google Scholar]
  13. Cornacchia D, Dileep V, Quivy JP, Foti R, Tili F. 13.  et al. 2012. Mouse Rif1 is a key regulator of the replication-timing programme in mammalian cells. EMBO J. 31:3678–90 [Google Scholar]
  14. Cremer T, Cremer M, Dietzel S, Muller S, Solovei I, Fakan S. 14.  2006. Chromosome territories—a functional nuclear landscape. Curr. Opin. Cell Biol. 18:307–16 [Google Scholar]
  15. Cuddapah S, Jothi R, Schones DE, Roh TY, Cui K, Zhao K. 15.  2009. Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains. Genome Res. 19:24–32 [Google Scholar]
  16. de Laat W, Duboule D. 16.  2013. Topology of mammalian developmental enhancers and their regulatory landscapes. Nature 502:499–506 [Google Scholar]
  17. de Wit E, Bouwman BA, Zhu Y, Klous P, Splinter E. 17.  et al. 2013. The pluripotent genome in three dimensions is shaped around pluripotency factors. Nature 501:227–31 [Google Scholar]
  18. de Wit E, Vos ES, Holwerda SJ, Valdes-Quezada C, Verstegen MJ. 18.  et al. 2015. CTCF binding polarity determines chromatin looping. Mol. Cell 60:676–84 [Google Scholar]
  19. Dekker J. 19.  2014. Two ways to fold the genome during the cell cycle: insights obtained with chromosome conformation capture. Epigenetics Chromatin 7:25 [Google Scholar]
  20. Dekker J, Heard E. 20.  2015. Structural and functional diversity of Topologically Associating Domains. FEBS Lett 589:2877–84 [Google Scholar]
  21. Deng W, Lee J, Wang H, Miller J, Reik A. 21.  et al. 2012. Controlling long-range genomic interactions at a native locus by targeted tethering of a looping factor. Cell 149:1233–44 [Google Scholar]
  22. Deng X, Ma W, Ramani V, Hill A, Yang F. 22.  et al. 2015. Bipartite structure of the inactive mouse X chromosome. Genome Biol. 16:152 [Google Scholar]
  23. Denholtz M, Bonora G, Chronis C, Splinter E, de Laat W. 23.  et al. 2013. Long-range chromatin contacts in embryonic stem cells reveal a role for pluripotency factors and polycomb proteins in genome organization. Cell Stem Cell 13:602–16 [Google Scholar]
  24. Dileep V, Ay F, Sima J, Vera DL, Noble WS, Gilbert DM. 24.  2015. Topologically associating domains and their long-range contacts are established during early G1 coincident with the establishment of the replication-timing program. Genome Res. 25:1104–13 [Google Scholar]
  25. Dixon JR, Jung I, Selvaraj S, Shen Y, Antosiewicz-Bourget JE. 25.  et al. 2015. Chromatin architecture reorganization during stem cell differentiation. Nature 518:331–36 [Google Scholar]
  26. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y. 26.  et al. 2012. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485:376–80 [Google Scholar]
  27. Dong J, Panchakshari RA, Zhang T, Zhang Y, Hu J. 27.  et al. 2015. Orientation-specific joining of AID-initiated DNA breaks promotes antibody class switching. Nature 525:134–39 [Google Scholar]
  28. Dorsett D, Merkenschlager M. 28.  2013. Cohesin at active genes: a unifying theme for cohesin and gene expression from model organisms to humans. Curr. Opin. Cell Biol. 25:327–33 [Google Scholar]
  29. Dowen JM, Bilodeau S, Orlando DA, Hübner MR, Abraham BJ. 29.  et al. 2013. Multiple structural maintenance of chromosome complexes at transcriptional regulatory elements. Stem Cell Rep 1:371–78 [Google Scholar]
  30. Dowen JM, Fan ZP, Hnisz D, Ren G, Abraham BJ. 30.  et al. 2014. Control of cell identity genes occurs in insulated neighborhoods in mammalian chromosomes. Cell 159:374–87 [Google Scholar]
  31. Doyle B, Fudenberg G, Imakaev M, Mirny LA. 31.  2014. Chromatin loops as allosteric modulators of enhancer-promoter interactions. PLOS Comput. Biol. 10:e1003867 [Google Scholar]
  32. Eagen KP, Hartl TA, Kornberg RD. 32.  2015. Stable chromosome condensation revealed by chromosome conformation capture. Cell 163:934–46 [Google Scholar]
  33. Engreitz JM, Pandya-Jones A, McDonel P, Shishkin A, Sirokman K. 33.  et al. 2013. The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Science 341:1237973 [Google Scholar]
  34. Fabre PJ, Benke A, Joye E, Nguyen Huynh TH, Manley S, Duboule D. 34.  2015. Nanoscale spatial organization of the HoxD gene cluster in distinct transcriptional states. PNAS 112:13964–69 [Google Scholar]
  35. Faure AJ, Schmidt D, Watt S, Schwalie PC, Wilson MD. 35.  et al. 2012. Cohesin regulates tissue-specific expression by stabilising highly occupied cis-regulatory modules. Genome Res. 22:2163–75 [Google Scholar]
  36. Fedoriw AM, Stein P, Svoboda P, Schultz RM, Bartolomei MS. 36.  2004. Transgenic RNAi reveals essential function for CTCF in H19 gene imprinting. Science 303:238–40 [Google Scholar]
  37. Feldmann A, Ivanek R, Murr R, Gaidatzis D, Burger L, Schübeler D. 37.  2013. Transcription factor occupancy can mediate active turnover of DNA methylation at regulatory regions. PLOS Genet. 9:e1003994 [Google Scholar]
  38. Filippova D, Patro R, Duggal G, Kingsford C. 38.  2014. Identification of alternative topological domains in chromatin. Algorithms Mol. Biol. 9:14 [Google Scholar]
  39. Flavahan WA, Drier Y, Liau BB, Gillespie SM, Venteicher AS. 39.  et al. 2016. Insulator dysfunction and oncogene activation in IDH mutant gliomas. Nature 529:110–14 [Google Scholar]
  40. Foti R, Gnan S, Cornacchia D, Dileep V, Bulut-Karslioglu A. 40.  et al. 2016. Nuclear architecture organized by Rif1 underpins the replication-timing program. Mol. Cell 61:260–73 [Google Scholar]
  41. Fudenberg G, Imakaev M, Lu C, Goloborodko A, Abdennur N, Mirny LA. 41.  2015. Formation of chromosomal domains by loop extrusion. bioRxiv. doi: 10.1101/024620
  42. Fudenberg G, Mirny LA. 42.  2012. Higher-order chromatin structure: bridging physics and biology. Curr. Opin. Genet. Dev. 22:115–24 [Google Scholar]
  43. Gerlich D, Koch B, Dupeux F, Peters JM, Ellenberg J. 43.  2006. Live-cell imaging reveals a stable cohesin-chromatin interaction after but not before DNA replication. Curr. Biol. 16:1571–78 [Google Scholar]
  44. Gibcus JH, Dekker J. 44.  2013. The hierarchy of the 3D genome. Mol. Cell 49:773–82 [Google Scholar]
  45. Giles KE, Gowher H, Ghirlando R, Jin C, Felsenfeld G. 45.  2010. Chromatin boundaries, insulators, and long-range interactions in the nucleus. Cold Spring Harb. Symp. Quant. Biol. 75:79–85 [Google Scholar]
  46. Giorgetti L, Galupa R, Nora EP, Piolot T, Lam F. 46.  et al. 2014. Predictive polymer modeling reveals coupled fluctuations in chromosome conformation and transcription. Cell 157:950–63 [Google Scholar]
  47. Goetze S, Mateos-Langerak J, Gierman HJ, de Leeuw W, Giromus O. 47.  et al. 2007. The three-dimensional structure of human interphase chromosomes is related to the transcriptome map. Mol. Cell. Biol. 2:4475–87 [Google Scholar]
  48. Gómez-Marín C, Tena JJ, Acemal RD, Lopez-Mayorga M, Naranjo S. 48.  et al. 2015. Evolutionary comparison reveals that diverging CTCF sites are signatures of ancestral topological associating domains borders. PNAS 112:7542–47 [Google Scholar]
  49. Gröschel S, Sanders MA, Hoogenboezem R, de Wit E, Bouwman BA. 49.  et al. 2014. A single oncogenic enhancer rearrangement causes concomitant EVI1 and GATA2 deregulation in leukemia. Cell 157:369–81 [Google Scholar]
  50. Gruber S. 50.  2014. Multilayer chromosome organization through DNA bending, bridging and extrusion. Curr. Opin. Microbiol. 22:102–10 [Google Scholar]
  51. Gullerova M, Proudfoot NJ. 51.  2008. Cohesin complex promotes transcriptional termination between convergent genes in S. pombe. Cell 132:983–95 [Google Scholar]
  52. Guo C, Yoon HS, Franklin A, Jain S, Ebert A. 52.  et al. 2011. CTCF-binding elements mediate control of V(D)J recombination. Nature 477:424–30 [Google Scholar]
  53. Guo Y, Xu Q, Canzio D, Shou J, Li J. 53.  et al. 2015. CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function. Cell 162:900–10 [Google Scholar]
  54. Hadjur S, Williams LM, Ryan NK, Cobb BS, Sexton T. 54.  et al. 2009. Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus. Nature 460:410–13 [Google Scholar]
  55. Handoko L, Xu H, Li G, Ngan CY, Chew E. 55.  et al. 2011. CTCF-mediated functional chromatin interactome in pluripotent cells. Nat. Genet. 43:630–38 [Google Scholar]
  56. Hark AT, Schoenherr CJ, Katz DJ, Ingram RS, Levorse JM, Tilghman SM. 56.  2000. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 405:486–89 [Google Scholar]
  57. Heger P, Marin B, Bartkuhn M, Schierenberg E, Wiehe T. 57.  2012. The chromatin insulator CTCF and the emergence of metazoan diversity. PNAS 109:17507–12 [Google Scholar]
  58. Heidari N, Phanstiel DH, He C, Grubert F, Jahanbanian F. 58.  et al. 2014. Genome-wide map of regulatory interactions in the human genome. Genome Res. 24:1905–17 [Google Scholar]
  59. Hnisz D, Weintraub AS, Day DS, Valton AL, Bak RO. 59.  et al. 2016. Activation of proto-oncogenes by disruption of chromosome neighborhoods. Science 351:1454–58 [Google Scholar]
  60. Hu J, Zhang Y, Zhao L, Frock RL, Du Z. 60.  et al. 2015. Chromosomal loop domains direct the recombination of antigen receptor genes. Cell 163:947–59 [Google Scholar]
  61. Hughes JR, Roberts N, McGowan S, Hay D, Giannoulatou E. 61.  et al. 2014. Analysis of hundreds of cis-regulatory landscapes at high resolution in a single, high-throughput experiment. Nat. Genet. 46:205–12 [Google Scholar]
  62. Imakaev MV, Fudenberg G, Mirny LA. 62.  2015. Modeling chromosomes: beyond pretty pictures. FEBS Lett. 589:3031–36 [Google Scholar]
  63. Ing-Simmons E, Seitan VC, Faure AJ, Flicek P, Carroll T. 63.  et al. 2015. Spatial enhancer clustering and regulation of enhancer-proximal genes by cohesin. Genome Res. 25:504–13 [Google Scholar]
  64. Jin F, Li Y, Dixon JR, Selvaraj S, Ye Z. 64.  et al. 2013. A high-resolution map of the three-dimensional chromatin interactome in human cells. Nature 503:290–94 [Google Scholar]
  65. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA. 65.  et al. 2010. Mediator and cohesin connect gene expression and chromatin architecture. Nature 467:430–35 [Google Scholar]
  66. Kanduri C, Pant V, Loukinov D, Pugacheva E, Qi CF. 66.  et al. 2000. Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive. Curr. Biol. 10:853–56 [Google Scholar]
  67. Katainen R, Dave K, Pitkänen E, Palin K, Kivioja T. 67.  et al. 2015. CTCF/cohesin-binding sites are frequently mutated in cancer. Nat. Genet. 47:818–21 [Google Scholar]
  68. Kemp CJ, Moore JM, Moser R, Bernard B, Teater M. 68.  et al. 2014. CTCF haploinsufficiency destabilizes DNA methylation and predisposes to cancer. Cell Rep. 7:1020–29 [Google Scholar]
  69. Klenova EM, Nicolas RH, Paterson HF, Carne AF, Heath CM. 69.  et al. 1993. CTCF, a conserved nuclear factor required for optimal transcriptional activity of the chicken c-myc gene, is an 11-Zn-finger protein differentially expressed in multiple forms. Mol. Cell. Biol. 13:7612–24 [Google Scholar]
  70. Kung JT, Kesner B, An JY, Ahn JY, Cifuentes-Rojas C. 70.  et al. 2015. Locus-specific targeting to the X chromosome revealed by the RNA interactome of CTCF. Mol. Cell 57:361–75 [Google Scholar]
  71. Lavagnolli T, Gupta P, Hörmanseder E, Mira-Bontenbal H, Dharmalingam G. 71.  et al. 2015. Initiation and maintenance of pluripotency gene expression in the absence of cohesin. Genes Dev. 29:23–38 [Google Scholar]
  72. Le Dily F, Baù D, Pohl A, Vicent GP, Soronellas D. 72.  et al. 2014. Distinct structural transitions of chromatin topological domains correlate with coordinated hormone-induced gene regulation. Genes Dev. 28:2151–62 [Google Scholar]
  73. Lengronne A, Katou Y, Mori S, Yokobayashi S, Kelly GP. 73.  et al. 2004. Cohesin relocation from sites of chromosomal loading to places of convergent transcription. Nature 430:573–78 [Google Scholar]
  74. Lesterlin C, Ball G, Schermelleh L, Sherratt DJ. 74.  2014. RecA bundles mediate homology pairing between distant sisters during DNA break repair. Nature 506:249–53 [Google Scholar]
  75. Li G, Ruan X, Auerbach RK, Sandhu KS, Zheng M. 75.  et al. 2012. Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell 148:84–98 [Google Scholar]
  76. Li L, Lyu X, Hou C, Takenaka N, Nguyen HQ. 76.  et al. 2015. Widespread rearrangement of 3D chromatin organization underlies Polycomb-mediated stress-induced silencing. Mol. Cell 58:216–31 [Google Scholar]
  77. Li W, Notani D, Ma Q, Tanasa B, Nunez E. 77.  et al. 2013. Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation. Nature 498:516–20 [Google Scholar]
  78. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T. 78.  et al. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–93 [Google Scholar]
  79. Ling JQ, Li T, Hu JF, Vu TH, Chen HL. 79.  et al. 2006. CTCF mediates interchromosomal colocalization between Igf2/H19 and Wsb1/Nf1. Science 312:269–72 [Google Scholar]
  80. Lopez-Serra L, Kelly G, Patel H, Stewart A, Uhlmann F. 80.  2014. The Scc2-Scc4 complex acts in sister chromatid cohesion and transcriptional regulation by maintaining nucleosome-free regions. Nat. Genet. 46:1147–51 [Google Scholar]
  81. Losada A. 81.  2014. Cohesin in cancer: chromosome segregation and beyond. Nat. Rev. Cancer 14:389–93 [Google Scholar]
  82. Lupianez DG, Kraft K, Heinrich V, Krawitz P, Brancati F. 82.  et al. 2015. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161:1012–25 [Google Scholar]
  83. MacPherson MJ, Sadowski PD. 83.  2010. The CTCF insulator protein forms an unusual DNA structure. BMC Mol. Biol. 11:101 [Google Scholar]
  84. Matthews AG, Kuo AJ, Ramón-Maiques S, Han S, Champagne KS. 84.  et al. 2007. RAG2 PHD finger couples histone H3 lysine 4 trimethylation with V(D)J recombination. Nature 450:1106–10 [Google Scholar]
  85. Maurano MT, Wang H, John S, Shafer A, Canfield T. 85.  et al. 2015. Role of DNA methylation in modulating transcription factor occupancy. Cell Rep. 12:1184–95 [Google Scholar]
  86. Mazumdar C, Shen Y, Xavy S, Zhao F, Reinisch A. 86.  et al. 2015. Leukemia-associated cohesin mutants dominantly enforce stem cell programs and impair human hematopoietic progenitor differentiation. Cell Stem Cell 17:675–88 [Google Scholar]
  87. McCord RP, Nazario-Toole A, Zhang H, Chines PS, Zhan Y. 87.  et al. 2013. Correlated alterations in genome organization, histone methylation, and DNA-lamin A/C interactions in Hutchinson-Gilford progeria syndrome. Genome Res. 23:260–69 [Google Scholar]
  88. Merkenschlager M, Odom DT. 88.  2013. CTCF and cohesin: linking gene regulatory elements with their targets. Cell 152:1285–97 [Google Scholar]
  89. Mifsud B, Tavares-Cadete F, Young AN, Sugar R, Schoenfelder S. 89.  et al. 2015. Mapping long-range promoter contacts in human cells with high-resolution capture Hi-C. Nat. Genet. 47:598–606 [Google Scholar]
  90. Minajigi A, Froberg JE, Wei C, Sunwoo H, Kesner B. 90.  et al. 2015. A comprehensive Xist interactome reveals cohesin repulsion and an RNA-directed chromosome conformation. Science 349:aab2276 [Google Scholar]
  91. Mishiro T, Ishihara K, Hino S, Tsutsumi S, Aburatani H. 91.  et al. 2009. Architectural roles of multiple chromatin insulators at the human apolipoprotein gene cluster. EMBO J. 28:1234–45 [Google Scholar]
  92. Mizuguchi T, Fudenberg G, Mehta S, Belton JM, Taneja N. 92.  et al. 2014. Cohesin-dependent globules and heterochromatin shape 3D genome architecture in S. pombe. Nature 516:432–35 [Google Scholar]
  93. Mullenders J, Aranda-Orgilles B, Lhoumaud P, Keller M, Pae J. 93.  et al. 2015. Cohesin loss alters adult hematopoietic stem cell homeostasis, leading to myeloproliferative neoplasms. J. Exp. Med. 212:1833–50 [Google Scholar]
  94. Murayama Y, Uhlmann F. 94.  2015. DNA entry into and exit out of the cohesin ring by an interlocking gate mechanism. Cell 163:1628–40 [Google Scholar]
  95. Nagano T, Lubling Y, Stevens TJ, Schoenfelder S, Yaffe E. 95.  et al. 2013. Single-cell Hi-C reveals cell-to-cell variability in chromosome structure. Nature 502:59–64 [Google Scholar]
  96. Nakahashi H, Kwon KR, Resch W, Vian L, Dose M. 96.  et al. 2013. A genome-wide map of CTCF multivalency redefines the CTCF code. Cell Rep. 3:1678–89 [Google Scholar]
  97. Narendra V, Rocha PP, An D, Raviram R, Skok JA. 97.  et al. 2015. CTCF establishes discrete functional chromatin domains at the Hox clusters during differentiation. Science 347:1017–21 [Google Scholar]
  98. Nasmyth K. 98.  2001. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu. Rev. Genet. 35:673–745 [Google Scholar]
  99. Nasmyth K, Haering CH. 99.  2009. Cohesin: its roles and mechanisms. Annu. Rev. Genet. 43:525–58 [Google Scholar]
  100. Nativio R, Wendt KS, Ito Y, Huddleston JE, Uribe-Lewis S. 100.  et al. 2009. Cohesin is required for higher-order chromatin conformation at the imprinted IGF2-H19 locus. PLOS Genet. 5:e1000739 [Google Scholar]
  101. Naumova N, Imakaev M, Fudenberg G, Zhan Y, Lajoie BR. 101.  et al. 2013. Organization of the mitotic chromosome. Science 342:948–53 [Google Scholar]
  102. Nichols MH, Corces VG. 102.  2015. A CTCF code for 3D genome architecture. Cell 162:703–5 [Google Scholar]
  103. Nora EP, Dekker J, Heard E. 103.  2013. Segmental folding of chromosomes: a basis for structural and regulatory chromosomal neighborhoods?. BioEssays 35:818–28 [Google Scholar]
  104. Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I. 104.  et al. 2012. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485:381–85 [Google Scholar]
  105. Pant V, Kurukuti S, Pugacheva E, Shamsuddin S, Mariano P. 105.  et al. 2004. Mutation of a single CTCF target site within the H19 imprinting control region leads to loss of Igf2 imprinting and complex patterns of de novo methylation upon maternal inheritance. Mol. Cell. Biol. 24:3497–504 [Google Scholar]
  106. Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S. 106.  et al. 2008. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132:422–33 [Google Scholar]
  107. Peric-Hupkes D, Meuleman W, Pagie L, Bruggeman SW, Solovei I. 107.  et al. 2010. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol. Cell 38:603–13 [Google Scholar]
  108. Phillips JE, Corces VG. 108.  2009. CTCF: master weaver of the genome. Cell 137:1194–211 [Google Scholar]
  109. Pope BD, Ryba T, Dileep V, Yue F, Wu W. 109.  et al. 2014. Topologically associating domains are stable units of replication-timing regulation. Nature 515:402–5 [Google Scholar]
  110. Rao SSP, Huntley MH, Durand NC, Stamenova EK, Bochkov ID. 110.  et al. 2014. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159:1665–80 [Google Scholar]
  111. Remeseiro S, Cuadrado A, Gómez-López G, Pisano DG, Losada A. 111.  2012. A unique role of cohesin-SA1 in gene regulation and development. EMBO J. 31:2090–102 [Google Scholar]
  112. Rowley JD. 112.  1973. A new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature 243:290–93 [Google Scholar]
  113. Rubio ED, Reiss DJ, Welcsh PL, Disteche CM, Filippova GN. 113.  et al. 2008. CTCF physically links cohesin to chromatin. PNAS 105:8309–14 [Google Scholar]
  114. Saldaña-Meyer R, González-Buendía E, Guerrero G, Narendra V, Bonasio R. 114.  et al. 2014. CTCF regulates the human p53 gene through direct interaction with its natural antisense transcript, Wrap53. Genes Dev. 28:723–34 [Google Scholar]
  115. Sanborn AL, Rao SSP, Huang S-C, Durand NC, Huntley MH. 115.  et al. 2015. Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. PNAS 112:E6456–65 [Google Scholar]
  116. Sandhu KS, Li G, Poh HM, Quek YL, Sia YY. 116.  et al. 2012. Large-scale functional organization of long-range chromatin interaction networks. Cell Rep. 2:1207–19 [Google Scholar]
  117. Sanyal A, Lajoie BR, Jain G, Dekker J. 117.  2012. The long-range interaction landscape of gene promoters. Nature 489:109–13 [Google Scholar]
  118. Schmidt D, Schwalie PC, Ross-Innes CS, Hurtado A, Brown GD. 118.  et al. 2010. A CTCF-independent role for cohesin in tissue-specific transcription. Genome Res. 20:578–88 [Google Scholar]
  119. Schoenfelder S, Furlan-Magaril M, Mifsud B, Tavares-Cadete F, Sugar R. 119.  et al. 2015. The pluripotent regulatory circuitry connecting promoters to their long-range interacting elements. Genome Res. 25:582–97 [Google Scholar]
  120. Seitan VC, Faure AJ, Zhan Y, McCord RP, Lajoie BR. 120.  et al. 2013. Cohesin-based chromatin interactions enable regulated gene expression within preexisting architectural compartments. Genome Res. 23:2066–77 [Google Scholar]
  121. Seitan VC, Hao B, Tachibana-Konwalski K, Lavagnolli T, Mira-Bontenbal H. 121.  et al. 2011. A role for cohesin in T cell receptor rearrangement and thymocyte differentiation. Nature 476:467–71 [Google Scholar]
  122. Shrimali S, Srivastava S, Varma G, Grinberg A, Pfeifer K, Srivastava M. 122.  2012. An ectopic CTCF-dependent transcriptional insulator influences the choice of Vβ gene segments for VDJ recombination at TCRβ locus. Nucleic Acids Res. 40:7753–65 [Google Scholar]
  123. Shukla S, Kavak E, Gregory M, Imashimizu M, Shutinoski B. 123.  et al. 2011. CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 479:74–79 [Google Scholar]
  124. Skibbens RV. 124.  2010. Buck the establishment: reinventing sister chromatid cohesion. Trends Cell Biol. 20:507–13 [Google Scholar]
  125. Sleutels F, Soochit W, Bartkuhn M, Heath H, Dienstbach S. 125.  et al. 2012. The male germ cell gene regulator CTCFL is functionally different from CTCF and binds CTCF-like consensus sites in a nucleosome composition-dependent manner. Epigenetics Chromatin 5:8 [Google Scholar]
  126. Sofueva S, Yaffe E, Chan WC, Georgopoulou D, Vietri Rudan M. 126.  et al. 2013. Cohesin-mediated interactions organize chromosomal domain architecture. EMBO J. 32:3119–29 [Google Scholar]
  127. Soh YM, Bürmann F, Shin HC, Oda T, Jin KS. 127.  et al. 2015. Molecular basis for SMC rod formation and its dissolution upon DNA binding. Mol. Cell 57:290–303 [Google Scholar]
  128. Solovei I, Kreysing M, Lanctôt C, Kösem S, Peichl L. 128.  et al. 2009. Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution. Cell 137:356–68 [Google Scholar]
  129. Soshnikova N, Montavon T, Leleu M, Galjart N, Duboule D. 129.  2010. Functional analysis of CTCF during mammalian limb development. Dev. Cell 19:819–30 [Google Scholar]
  130. Splinter E, de Wit E, Nora EP, Klous P, van de Werken HJ. 130.  et al. 2011. The inactive X chromosome adopts a unique three-dimensional conformation that is dependent on Xist RNA. Genes Dev. 25:1371–83 [Google Scholar]
  131. Splinter E, Heath H, Kooren J, Palstra RJ, Klous P. 131.  et al. 2006. CTCF mediates long-range chromatin looping and local histone modification in the β-globin locus. Genes Dev. 20:2349–54 [Google Scholar]
  132. Stanhope-Baker P, Hudson KM, Shaffer AL, Constantinescu A, Schlissel MS. 132.  1996. Cell type-specific chromatin structure determines the targeting of V(D)J recombinase activity in vitro. Cell 85:887–97 [Google Scholar]
  133. Stark WM, Sherratt DJ, Boocock MR. 133.  1989. Site-specific recombination by Tn3 resolvase: topological changes in the forward and reverse reactions. Cell 58:779–90 [Google Scholar]
  134. Stedman W, Kang H, Lin S, Kissil JL, Bartolomei MS, Lieberman PM. 134.  2008. Cohesins localize with CTCF at the KSHV latency control region and at cellular c-myc and H19/Igf2 insulators. EMBO J. 27:654–66 [Google Scholar]
  135. Stegle O, Teichmann SA, Marioni JC. 135.  2015. Computational and analytical challenges in single-cell transcriptomics. Nat. Rev. Genet. 16:133–45 [Google Scholar]
  136. Suter DM, Molina N, Gatfield D, Schneider K, Schibler U, Naef F. 136.  2011. Mammalian genes are transcribed with widely different bursting kinetics. Science 332:472–74 [Google Scholar]
  137. Symmons O, Uslu VV, Tsujimura T, Ruf S, Nassari S. 137.  et al. 2014. Functional and topological characteristics of mammalian regulatory domains. Genome Res. 24:390–400 [Google Scholar]
  138. Tang Z, Luo OJ, Li X, Zheng M, Zhu JJ. 138.  et al. 2015. CTCF-mediated human 3D genome architecture reveals chromatin topology for transcription. Cell 163:1611–27 [Google Scholar]
  139. Tark-Dame M, Jerabek H, Manders EMM, Heermann DW, van Driel R. 139.  2014. Depletion of the chromatin looping proteins CTCF and cohesin causes chromatin compaction: insight into chromatin folding by polymer modelling. PLOS Comput. Biol. 10:e1003877 [Google Scholar]
  140. Tsujimoto Y, Finger LR, Yunis J, Nowell PC, Croce CM. 140.  1984. Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science 226:1097–99 [Google Scholar]
  141. van de Corput MP, de Boer E, Knoch TA, van Cappellen WA, Quintanilla A. 141.  et al. 2012. Super-resolution imaging reveals three-dimensional folding dynamics of the β-globin locus upon gene activation. J. Cell Sci. 125:4630–39 [Google Scholar]
  142. van Steensel B. 142.  2011. Chromatin: constructing the big picture. EMBO J. 30:1885–95 [Google Scholar]
  143. Vietri Rudan M, Barrington C, Henderson S, Ernst C, Odom DT. 143.  et al. 2015. Comparative Hi-C reveals that CTCF underlies evolution of chromosomal domain architecture. Cell Rep. 10:1297–309 [Google Scholar]
  144. Viny AD, Ott CJ, Spitzer B, Rivas M, Meydan C. 144.  et al. 2015. Dose-dependent role of the cohesin complex in normal and malignant hematopoiesis. J. Exp. Med. 212:1819–32 [Google Scholar]
  145. Wan LB, Pan H, Hannenhalli S, Cheng Y, Ma J. 145.  et al. 2008. Maternal depletion of CTCF reveals multiple functions during oocyte and preimplantation embryo development. Development 135:2729–38 [Google Scholar]
  146. Wang H, Maurano MT, Qu H, Varley KE, Gertz J. 146.  et al. 2012. Widespread plasticity in CTCF occupancy linked to DNA methylation. Genome Res. 22:1680–88 [Google Scholar]
  147. Wendt KS, Yoshida K, Itoh T, Bando M, Koch B. 147.  et al. 2008. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451:796–801 [Google Scholar]
  148. Whyte WA, Orlando DA, Hnisz D, Abraham BJ, Lin CY. 148.  et al. 2013. Master transcription factors and Mediator establish super-enhancers at key cell identity genes. Cell 153:307–19 [Google Scholar]
  149. Wijchers PJ, Krijger PH, Geeven G, Zhu Y, Denker A. 149.  et al. 2016. Cause and consequence of tethering a subTAD to different nuclear compartments. Mol. Cell 61:461–73 [Google Scholar]
  150. Wu LJ, Errington J. 150.  1994. Bacillus subtilis SpoIIIE protein required for DNA segregation during asymmetric cell division. Science 264:572–75 [Google Scholar]
  151. Xiao T, Wallace J, Felsenfeld G. 151.  2011. Specific sites in the C terminus of CTCF interact with the SA2 subunit of the cohesin complex and are required for cohesin-dependent insulation activity. Mol. Cell. Biol. 31:2174–83 [Google Scholar]
  152. Xu C, Corces VG. 152.  2016. Towards a predictive model of chromatin 3D organization. Semin. Cell Dev. Biol. In press. doi: 10.1016/j.semcdb.2015.11.013
  153. Xu N, Donohoe ME, Silva SS, Lee JT. 153.  2007. Evidence that homologous X-chromosome pairing requires transcription and Ctcf protein. Nat. Genet. 39:1390–96 [Google Scholar]
  154. Yan J, Enge M, Whitington T, Dave K, Liu J. 154.  et al. 2013. Transcription factor binding in human cells occurs in dense clusters formed around cohesin anchor sites. Cell 154:801–3 [Google Scholar]
  155. Yang F, Deng X, Ma W, Berletch JB, Rabaia N. 155.  et al. 2015. The lncRNA Firre anchors the inactive X chromosome to the nucleolus by binding CTCF and maintains H3K27me3 methylation. Genome Biol. 16:52 [Google Scholar]
  156. Zhang N, Pati D. 156.  2009. Handcuff for sisters: a new model for sister chromatid cohesion. Cell Cycle 8:399–402 [Google Scholar]
  157. Zhang Y, Wong C-H, Birnbaum RY, Li G, Favaro R. 157.  et al. 2013. Chromatin connectivity maps reveal dynamic promoter-enhancer long-range associations. Nature 504:306–10 [Google Scholar]
  158. Zhao H, Sifakis EG, Sumida N, Millán-Ariño L, Scholz BA. 158.  et al. 2015. PARP1- and CTCF-mediated interactions between active and repressed chromatin at the lamina promote oscillating transcription. Mol. Cell 59:984–97 [Google Scholar]
  159. Zhao Z, Tavoosidana G, Sjölinder M, Göndör A, Mariano P. 159.  et al. 2006. Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions. Nat. Genet. 38:1341–47 [Google Scholar]
  160. Zuin J, Dixon JR, van der Reijden MI, Ye Z, Kolovos P. 160.  et al. 2014. Cohesin and CTCF differentially affect chromatin architecture and gene expression in human cells. PNAS 111:996–1001 [Google Scholar]
/content/journals/10.1146/annurev-genom-083115-022339
Loading
/content/journals/10.1146/annurev-genom-083115-022339
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error