The 3D genome in transcriptional regulation and pluripotency

Cell Stem Cell

Volumn 14, Issue 6, 2014, Pages 762-775

  Gorkin, David U ^a   Leung, Danny ^a   Ren, Bing ^a,b  

^a LUDWIG INSTITUTE FOR CANCER RESEARCH   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME; GENE EXPRESSION; GENE LOCUS; GENOME; GENOME ANALYSIS; MAMMAL CELL; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVIEW; TRANSCRIPTION REGULATION; CELL DIFFERENTIATION; CHROMATIN STRUCTURE; COMPARATIVE STUDY; DAUGHTER CELL; GENE CLUSTER; GENETIC TRANSCRIPTION; HEK293 CELL LINE; HISTONE MODIFICATION; NUCLEAR LAMINA; PROMOTER REGION; PROTEIN DOMAIN; REGULATOR GENE; ANIMAL; CELL LINEAGE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM;

COHESIN;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; GENE EXPRESSION REGULATION; GENOME; HUMANS; PLURIPOTENT STEM CELLS; TRANSCRIPTION, GENETIC;

EID: 84902212007     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2014.05.017     Document Type: Review

References (149)

1. W. Akhtar, J. de Jong, A.V. Pindyurin, L. Pagie, W. Meuleman, J. de Ridder, A. Berns, L.F. Wessels, M. van Lohuizen, and B. van Steensel Chromatin position effects assayed by thousands of reporters integrated in parallel Cell 154 2013 914 927
2. G. Andrey, T. Montavon, B. Mascrez, F. Gonzalez, D. Noordermeer, M. Leleu, D. Trono, F. Spitz, and D. Duboule A switch between topological domains underlies HoxD genes collinearity in mouse limbs Science 340 2013 1234167
3. E. Apostolou, and K. Hochedlinger Chromatin dynamics during cellular reprogramming Nature 502 2013 462 471
4. E. Apostolou, F. Ferrari, R.M. Walsh, O. Bar-Nur, M. Stadtfeld, S. Cheloufi, H.T. Stuart, J.M. Polo, T.K. Ohsumi, and M.L. Borowsky et al. Genome-wide chromatin interactions of the Nanog locus in pluripotency, differentiation, and reprogramming Cell Stem Cell 12 2013 699 712
5. A. Barski, S. Cuddapah, K. Cui, T.Y. Roh, D.E. Schones, Z. Wang, G. Wei, I. Chepelev, and K. Zhao High-resolution profiling of histone methylations in the human genome Cell 129 2007 823 837
6. A.C. Bell, and G. Felsenfeld Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene Nature 405 2000 482 485
7. A.C. Bell, A.G. West, and G. Felsenfeld The protein CTCF is required for the enhancer blocking activity of vertebrate insulators Cell 98 1999 387 396
8. S. Benko, J.A. Fantes, J. Amiel, D.J. Kleinjan, S. Thomas, J. Ramsay, N. Jamshidi, A. Essafi, S. Heaney, and C.T. Gordon et al. Highly conserved non-coding elements on either side of SOX9 associated with Pierre Robin sequence Nat. Genet. 41 2009 359 364
9. B.E. Bernstein, J.A. Stamatoyannopoulos, J.F. Costello, B. Ren, A. Milosavljevic, A. Meissner, M. Kellis, M.A. Marra, A.L. Beaudet, and J.R. Ecker et al. The NIH Roadmap Epigenomics Mapping Consortium Nat. Biotechnol. 28 2010 1045 1048
10. B.E. Bernstein, E. Birney, I. Dunham, E.D. Green, C. Gunter, M. Snyder ENCODE Project Consortium An integrated encyclopedia of DNA elements in the human genome Nature 489 2012 57 74
11. W.A. Bickmore The spatial organization of the human genome Annu. Rev. Genomics Hum. Genet. 14 2013 67 84
12. A. Bolzer, G. Kreth, I. Solovei, D. Koehler, K. Saracoglu, C. Fauth, S. Müller, R. Eils, C. Cremer, M.R. Speicher, and T. Cremer Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes PLoS Biol. 3 2005 e157
13. H. Bornfleth, P. Edelmann, D. Zink, T. Cremer, and C. Cremer Quantitative motion analysis of subchromosomal foci in living cells using four-dimensional microscopy Biophys. J. 77 1999 2871 2886
14. S. Boyle, M.J. Rodesch, H.A. Halvensleben, J.A. Jeddeloh, and W.A. Bickmore Fluorescence in situ hybridization with high-complexity repeat-free oligonucleotide probes generated by massively parallel synthesis Chromosome Res. 19 2011 901 909
15. M.R. Branco, and A. Pombo Intermingling of chromosome territories in interphase suggests role in translocations and transcription-dependent associations PLoS Biol. 4 2006 e138
16. S. Cai, C.C. Lee, and T. Kohwi-Shigematsu SATB1 packages densely looped, transcriptionally active chromatin for coordinated expression of cytokine genes Nat. Genet. 38 2006 1278 1288
17. J.O. Carlsten, X. Zhu, and C.M. Gustafsson The multitalented Mediator complex Trends Biochem. Sci. 38 2013 531 537
18. D. Carter, L. Chakalova, C.S. Osborne, Y.F. Dai, and P. Fraser Long-range chromatin regulatory interactions in vivo Nat. Genet. 32 2002 623 626
19. G. Cavalli, and T. Misteli Functional implications of genome topology Nat. Struct. Mol. Biol. 20 2013 290 299
20. S. Chambeyron, and W.A. Bickmore Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription Genes Dev. 18 2004 1119 1130
21. X. Chen, H. Xu, P. Yuan, F. Fang, M. Huss, V.B. Vega, E. Wong, Y.L. Orlov, W. Zhang, and J. Jiang et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells Cell 133 2008 1106 1117
22. H. Chen, Y. Tian, W. Shu, X. Bo, and S. Wang Comprehensive identification and annotation of cell type-specific and ubiquitous CTCF-binding sites in the human genome PLoS ONE 7 2012 e41374
23. T. Cheutin, and G. Cavalli Polycomb silencing: from linear chromatin domains to 3D chromosome folding Curr. Opin. Genet. Dev. 25C 2014 30 37
24. R. Chien, W. Zeng, S. Kawauchi, M.A. Bender, R. Santos, H.C. Gregson, J.A. Schmiesing, D.A. Newkirk, X. Kong, and A.R. Ball Jr. et al. Cohesin mediates chromatin interactions that regulate mammalian β-globin expression J. Biol. Chem. 286 2011 17870 17878
25. E.J. Clowney, M.A. LeGros, C.P. Mosley, F.G. Clowney, E.C. Markenskoff-Papadimitriou, M. Myllys, G. Barnea, C.A. Larabell, and S. Lomvardas Nuclear aggregation of olfactory receptor genes governs their monogenic expression Cell 151 2012 724 737
26. T. Cremer, and M. Cremer Chromosome territories Cold Spring Harb. Perspect. Biol. 2 2010 a003889
27. S. Cuddapah, R. Jothi, D.E. Schones, T.Y. Roh, K. Cui, and K. Zhao Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains Genome Res. 19 2009 24 32
28. W. de Laat, and J. Dekker 3C-based technologies to study the shape of the genome Methods 58 2012 189 191
29. W. de Laat, and D. Duboule Topology of mammalian developmental enhancers and their regulatory landscapes Nature 502 2013 499 506
30. E. de Wit, and W. de Laat A decade of 3C technologies: insights into nuclear organization Genes Dev. 26 2012 11 24
31. E. de Wit, B.A. Bouwman, Y. Zhu, P. Klous, E. Splinter, M.J. Verstegen, P.H. Krijger, N. Festuccia, E.P. Nora, and M. Welling et al. The pluripotent genome in three dimensions is shaped around pluripotency factors Nature 501 2013 227 231
32. J. Dekker, K. Rippe, M. Dekker, and N. Kleckner Capturing chromosome conformation Science 295 2002 1306 1311
33. J. Dekker, M.A. Marti-Renom, and L.A. Mirny Exploring the three-dimensional organization of genomes: interpreting chromatin interaction data Nat. Rev. Genet. 14 2013 390 403
34. L.E. DeMare, J. Leng, J. Cotney, S.K. Reilly, J. Yin, R. Sarro, and J.P. Noonan The genomic landscape of cohesin-associated chromatin interactions Genome Res. 23 2013 1224 1234
35. W. Deng, J. Lee, H. Wang, J. Miller, A. Reik, P.D. Gregory, A. Dean, and G.A. Blobel Controlling long-range genomic interactions at a native locus by targeted tethering of a looping factor Cell 149 2012 1233 1244
36. M. Denholtz, and K. Plath Pluripotency in 3D: genome organization in pluripotent cells Curr. Opin. Cell Biol. 24 2012 793 801
37. M. Denholtz, G. Bonora, C. Chronis, E. Splinter, W. de Laat, J. Ernst, M. Pellegrini, and K. Plath Long-range chromatin contacts in embryonic stem cells reveal a role for pluripotency factors and polycomb proteins in genome organization Cell Stem Cell 13 2013 602 616
38. J.R. Dixon, S. Selvaraj, F. Yue, A. Kim, Y. Li, Y. Shen, M. Hu, J.S. Liu, and B. Ren Topological domains in mammalian genomes identified by analysis of chromatin interactions Nature 485 2012 376 380
39. J. Dostie, T.A. Richmond, R.A. Arnaout, R.R. Selzer, W.L. Lee, T.A. Honan, E.D. Rubio, A. Krumm, J. Lamb, and C. Nusbaum et al. Chromosome Conformation Capture Carbon Copy (5C): a massively parallel solution for mapping interactions between genomic elements Genome Res. 16 2006 1299 1309
40. C.C. Ebmeier, and D.J. Taatjes Activator-Mediator binding regulates Mediator-cofactor interactions Proc. Natl. Acad. Sci. USA 107 2010 11283 11288
41. L.B. Edelman, and P. Fraser Transcription factories: genetic programming in three dimensions Curr. Opin. Genet. Dev. 22 2012 110 114
42. A. Eijkelenboom, M. Mokry, E. de Wit, L.M. Smits, P.E. Polderman, M.H. van Triest, R. van Boxtel, A. Schulze, W. de Laat, E. Cuppen, and B.M. Burgering Genome-wide analysis of FOXO3 mediated transcription regulation through RNA polymerase II profiling Mol. Syst. Biol. 9 2013 638
43. J.M. Engreitz, A. Pandya-Jones, P. McDonel, A. Shishkin, K. Sirokman, C. Surka, S. Kadri, J. Xing, A. Goren, and E.S. Lander et al. The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome Science 341 2013 1237973
44. R. Eskeland, M. Leeb, G.R. Grimes, C. Kress, S. Boyle, D. Sproul, N. Gilbert, Y. Fan, A.I. Skoultchi, A. Wutz, and W.A. Bickmore Ring1B compacts chromatin structure and represses gene expression independent of histone ubiquitination Mol. Cell 38 2010 452 464
45. A.J. Faure, D. Schmidt, S. Watt, P.C. Schwalie, M.D. Wilson, H. Xu, R.G. Ramsay, D.T. Odom, and P. Flicek Cohesin regulates tissue-specific expression by stabilizing highly occupied cis-regulatory modules Genome Res. 22 2012 2163 2175
46. L.E. Finlan, D. Sproul, I. Thomson, S. Boyle, E. Kerr, P. Perry, B. Ylstra, J.R. Chubb, and W.A. Bickmore Recruitment to the nuclear periphery can alter expression of genes in human cells PLoS Genet. 4 2008 e1000039
47. N.J. Fuda, M.B. Ardehali, and J.T. Lis Defining mechanisms that regulate RNA polymerase II transcription in vivo Nature 461 2009 186 192
48. M.J. Fullwood, M.H. Liu, Y.F. Pan, J. Liu, H. Xu, Y.B. Mohamed, Y.L. Orlov, S. Velkov, A. Ho, and P.H. Mei et al. An oestrogen-receptor-alpha-bound human chromatin interactome Nature 462 2009 58 64
49. A. Gaspar-Maia, A. Alajem, E. Meshorer, and M. Ramalho-Santos Open chromatin in pluripotency and reprogramming Nat. Rev. Mol. Cell Biol. 12 2011 36 47
50. J.H. Gibcus, and J. Dekker The hierarchy of the 3D genome Mol. Cell 49 2013 773 782
51. L. Giorgetti, R. Galupa, E.P. Nora, T. Piolot, F. Lam, J. Dekker, G. Tiana, and E. Heard Predictive polymer modeling reveals coupled fluctuations in chromosome conformation and transcription Cell 157 2014 950 963
52. L. Guelen, L. Pagie, E. Brasset, W. Meuleman, M.B. Faza, W. Talhout, B.H. Eussen, A. de Klein, L. Wessels, W. de Laat, and B. van Steensel Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions Nature 453 2008 948 951
53. S. Hadjur, L.M. Williams, N.K. Ryan, B.S. Cobb, T. Sexton, P. Fraser, A.G. Fisher, and M. Merkenschlager Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus Nature 460 2009 410 413
54. O. Hakim, M.H. Sung, T.C. Voss, E. Splinter, S. John, P.J. Sabo, R.E. Thurman, J.A. Stamatoyannopoulos, W. de Laat, and G.L. Hager Diverse gene reprogramming events occur in the same spatial clusters of distal regulatory elements Genome Res. 21 2011 697 706
55. L. Handoko, H. Xu, G. Li, C.Y. Ngan, E. Chew, M. Schnapp, C.W. Lee, C. Ye, J.L. Ping, and F. Mulawadi et al. CTCF-mediated functional chromatin interactome in pluripotent cells Nat. Genet. 43 2011 630 638
56. A.T. Hark, C.J. Schoenherr, D.J. Katz, R.S. Ingram, J.M. Levorse, and S.M. Tilghman CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus Nature 405 2000 486 489
57. R.D. Hawkins, G.C. Hon, L.K. Lee, Q. Ngo, R. Lister, M. Pelizzola, L.E. Edsall, S. Kuan, Y. Luu, and S. Klugman et al. Distinct epigenomic landscapes of pluripotent and lineage-committed human cells Cell Stem Cell 6 2010 479 491
58. L.A. Hindorff, P. Sethupathy, H.A. Junkins, E.M. Ramos, J.P. Mehta, F.S. Collins, and T.A. Manolio Potential etiologic and functional implications of genome-wide association loci for human diseases and traits Proc. Natl. Acad. Sci. USA 106 2009 9362 9367
59. D. Hnisz, B.J. Abraham, T.I. Lee, A. Lau, V. Saint-André, A.A. Sigova, H.A. Hoke, and R.A. Young Super-enhancers in the control of cell identity and disease Cell 155 2013 934 947
60. D. Huang, Z. Wei, and W. Lu Genome organization by Klf4 regulates transcription in pluripotent stem cells Cell Cycle 12 2013 3351 3352
61. J.R. Hughes, N. Roberts, S. McGowan, D. Hay, E. Giannoulatou, M. Lynch, M. De Gobbi, S. Taylor, R. Gibbons, and D.R. Higgs Analysis of hundreds of cis-regulatory landscapes at high resolution in a single, high-throughput experiment Nat. Genet. 46 2014 205 212
62. K. Isono, T.A. Endo, M. Ku, D. Yamada, R. Suzuki, J. Sharif, T. Ishikura, T. Toyoda, B.E. Bernstein, and H. Koseki SAM domain polymerization links subnuclear clustering of PRC1 to gene silencing Dev. Cell 26 2013 565 577
63. F. Jin, Y. Li, B. Ren, and R. Natarajan PU.1 and C/EBP(alpha) synergistically program distinct response to NF-kappaB activation through establishing monocyte specific enhancers Proc. Natl. Acad. Sci. USA 108 2011 5290 5295
64. F. Jin, Y. Li, J.R. Dixon, S. Selvaraj, Z. Ye, A.Y. Lee, C.A. Yen, A.D. Schmitt, C.A. Espinoza, and B. Ren A high-resolution map of the three-dimensional chromatin interactome in human cells Nature 503 2013 290 294
65. D.O. Jones, I.G. Cowell, and P.B. Singh Mammalian chromodomain proteins: their role in genome organisation and expression Bioessays 22 2000 124 137
66. M.H. Kagey, J.J. Newman, S. Bilodeau, Y. Zhan, D.A. Orlando, N.L. van Berkum, C.C. Ebmeier, J. Goossens, P.B. Rahl, and S.S. Levine et al. Mediator and cohesin connect gene expression and chromatin architecture Nature 467 2010 430 435
67. K.R. Kieffer-Kwon, Z. Tang, E. Mathe, J. Qian, M.H. Sung, G. Li, W. Resch, S. Baek, N. Pruett, and L. Grøntved et al. Interactome maps of mouse gene regulatory domains reveal basic principles of transcriptional regulation Cell 155 2013 1507 1520
68. T.H. Kim, Z.K. Abdullaev, A.D. Smith, K.A. Ching, D.I. Loukinov, R.D. Green, M.Q. Zhang, V.V. Lobanenkov, and B. Ren Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome Cell 128 2007 1231 1245
69. J. Kind, L. Pagie, H. Ortabozkoyun, S. Boyle, S.S. de Vries, H. Janssen, M. Amendola, L.D. Nolen, W.A. Bickmore, and B. van Steensel Single-cell dynamics of genome-nuclear lamina interactions Cell 153 2013 178 192
70. E.M. Klenova, R.H. Nicolas, H.F. Paterson, A.F. Carne, C.M. Heath, G.H. Goodwin, P.E. Neiman, and V.V. Lobanenkov 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 1993 7612 7624
71. S.T. Kosak, J.A. Skok, K.L. Medina, R. Riblet, M.M. Le Beau, A.G. Fisher, and H. Singh Subnuclear compartmentalization of immunoglobulin loci during lymphocyte development Science 296 2002 158 162
72. F. Lai, U.A. Orom, M. Cesaroni, M. Beringer, D.J. Taatjes, G.A. Blobel, and R. Shiekhattar Activating RNAs associate with Mediator to enhance chromatin architecture and transcription Nature 494 2013 497 501
73. L. Larivière, M. Seizl, and P. Cramer A structural perspective on Mediator function Curr. Opin. Cell Biol. 24 2012 305 313
74. M.S. Lawrence, P. Stojanov, C.H. Mermel, J.T. Robinson, L.A. Garraway, T.R. Golub, M. Meyerson, S.B. Gabriel, E.S. Lander, and G. Getz Discovery and saturation analysis of cancer genes across 21 tumour types Nature 505 2014 495 501
75. L.A. Lettice, S.J. Heaney, L.A. Purdie, L. Li, P. de Beer, B.A. Oostra, D. Goode, G. Elgar, R.E. Hill, and E. de Graaff A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly Hum. Mol. Genet. 12 2003 1725 1735
76. D.N. Levasseur, J. Wang, M.O. Dorschner, J.A. Stamatoyannopoulos, and S.H. Orkin Oct4 dependence of chromatin structure within the extended Nanog locus in ES cells Genes Dev. 22 2008 575 580
77. G. Li, X. Ruan, R.K. Auerbach, K.S. Sandhu, M. Zheng, P. Wang, H.M. Poh, Y. Goh, J. Lim, and J. Zhang et al. Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation Cell 148 2012 84 98
78. E. Lieberman-Aiden, N.L. van Berkum, L. Williams, M. Imakaev, T. Ragoczy, A. Telling, I. Amit, B.R. Lajoie, P.J. Sabo, and M.O. Dorschner et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome Science 326 2009 289 293
79. W.F. Marshall, A. Straight, J.F. Marko, J. Swedlow, A. Dernburg, A. Belmont, A.W. Murray, D.A. Agard, and J.W. Sedat Interphase chromosomes undergo constrained diffusional motion in living cells Curr. Biol. 7 1997 930 939
80. M.T. Maurano, R. Humbert, E. Rynes, R.E. Thurman, E. Haugen, H. Wang, A.P. Reynolds, R. Sandstrom, H. Qu, and J. Brody et al. Systematic localization of common disease-associated variation in regulatory DNA Science 337 2012 1190 1195
81. S. Melcer, and E. Meshorer Chromatin plasticity in pluripotent cells Essays Biochem. 48 2010 245 262
82. M. Merkenschlager, and D.T. Odom CTCF and cohesin: linking gene regulatory elements with their targets Cell 152 2013 1285 1297
83. E. Meshorer, D. Yellajoshula, E. George, P.J. Scambler, D.T. Brown, and T. Misteli Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells Dev. Cell 10 2006 105 116
84. T. Misteli Self-organization in the genome Proc. Natl. Acad. Sci. USA 106 2009 6885 6886
85. T. Misteli Higher-order genome organization in human disease Cold Spring Harb. Perspect. Biol. 2 2010 a000794
86. T. Montavon, N. Soshnikova, B. Mascrez, E. Joye, L. Thevenet, E. Splinter, W. de Laat, F. Spitz, and D. Duboule A regulatory archipelago controls Hox genes transcription in digits Cell 147 2011 1132 1145
87. C. Morey, N.R. Da Silva, P. Perry, and W.A. Bickmore Nuclear reorganisation and chromatin decondensation are conserved, but distinct, mechanisms linked to Hox gene activation Development 134 2007 909 919
88. W.G. Müller, J.B. Heymann, K. Nagashima, P. Guttmann, S. Werner, S. Rehbein, G. Schneider, and J.G. McNally Towards an atlas of mammalian cell ultrastructure by cryo soft X-ray tomography J. Struct. Biol. 177 2012 179 192
89. T. Nagano, Y. Lubling, T.J. Stevens, S. Schoenfelder, E. Yaffe, W. Dean, E.D. Laue, A. Tanay, and P. Fraser Single-cell Hi-C reveals cell-to-cell variability in chromosome structure Nature 502 2013 59 64
90. N. Naumova, M. Imakaev, G. Fudenberg, Y. Zhan, B.R. Lajoie, L.A. Mirny, and J. Dekker Organization of the mitotic chromosome Science 342 2013 948 953
91. S. Neph, J. Vierstra, A.B. Stergachis, A.P. Reynolds, E. Haugen, B. Vernot, R.E. Thurman, S. John, R. Sandstrom, and A.K. Johnson et al. An expansive human regulatory lexicon encoded in transcription factor footprints Nature 489 2012 83 90
92. A. Nitzsche, M. Paszkowski-Rogacz, F. Matarese, E.M. Janssen-Megens, N.C. Hubner, H. Schulz, I. de Vries, L. Ding, N. Huebner, and M. Mann et al. RAD21 cooperates with pluripotency transcription factors in the maintenance of embryonic stem cell identity PLoS ONE 6 2011 e19470
93. D. Noordermeer, and W. de Laat Joining the loops: beta-globin gene regulation IUBMB Life 60 2008 824 833
94. E.P. Nora, B.R. Lajoie, E.G. Schulz, L. Giorgetti, I. Okamoto, N. Servant, T. Piolot, N.L. van Berkum, J. Meisig, and J. Sedat et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre Nature 485 2012 381 385
95. E.P. Nora, J. Dekker, and E. Heard Segmental folding of chromosomes: a basis for structural and regulatory chromosomal neighborhoods? Bioessays 35 2013 818 828
96. C.T. Ong, and V.G. Corces CTCF: an architectural protein bridging genome topology and function Nat. Rev. Genet. 15 2014 234 246
97. U.A. rom, and R. Shiekhattar Long noncoding RNAs usher in a new era in the biology of enhancers Cell 154 2013 1190 1193
98. U.A. rom, T. Derrien, M. Beringer, K. Gumireddy, A. Gardini, G. Bussotti, F. Lai, M. Zytnicki, C. Notredame, and Q. Huang et al. Long noncoding RNAs with enhancer-like function in human cells Cell 143 2010 46 58
99. C.S. Osborne, L. Chakalova, K.E. Brown, D. Carter, A. Horton, E. Debrand, B. Goyenechea, J.A. Mitchell, S. Lopes, W. Reik, and P. Fraser Active genes dynamically colocalize to shared sites of ongoing transcription Nat. Genet. 36 2004 1065 1071
100. J. Padeken, and P. Heun Nucleolus and nuclear periphery: Velcro for heterochromatin Curr. Opin. Cell Biol. 28C 2014 54 60
101. R.J. Palstra, M. Simonis, P. Klous, E. Brasset, B. Eijkelkamp, and W. de Laat Maintenance of long-range DNA interactions after inhibition of ongoing RNA polymerase II transcription PLoS One 3 2008 e1661
102. A. Papantonis, and P.R. Cook Transcription factories: genome organization and gene regulation Chem. Rev. 113 2013 8683 8705
103. L.A. Parada, J.J. Roix, and T. Misteli An uncertainty principle in chromosome positioning Trends Cell Biol. 13 2003 393 396
104. V. Parelho, S. Hadjur, M. Spivakov, M. Leleu, S. Sauer, H.C. Gregson, A. Jarmuz, C. Canzonetta, Z. Webster, and T. Nesterova et al. Cohesins functionally associate with CTCF on mammalian chromosome arms Cell 132 2008 422 433
105. D. Peric-Hupkes, W. Meuleman, L. Pagie, S.W. Bruggeman, I. Solovei, W. Brugman, S. Gräf, P. Flicek, R.M. Kerkhoven, and M. van Lohuizen et al. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation Mol. Cell 38 2010 603 613
106. J.E. Phillips, and V.G. Corces CTCF: master weaver of the genome Cell 137 2009 1194 1211
107. J.E. Phillips-Cremins, M.E. Sauria, A. Sanyal, T.I. Gerasimova, B.R. Lajoie, J.S. Bell, C.T. Ong, T.A. Hookway, C. Guo, and Y. Sun et al. Architectural protein subclasses shape 3D organization of genomes during lineage commitment Cell 153 2013 1281 1295
108. H. Pickersgill, B. Kalverda, E. de Wit, W. Talhout, M. Fornerod, and B. van Steensel Characterization of the Drosophila melanogaster genome at the nuclear lamina Nat. Genet. 38 2006 1005 1014
109. C. Praetorius, C. Grill, S.N. Stacey, A.M. Metcalf, D.U. Gorkin, K.C. Robinson, E. Van Otterloo, R.S. Kim, K. Bergsteinsdottir, and M.H. Ogmundsdottir et al. A polymorphism in IRF4 affects human pigmentation through a tyrosinase-dependent MITF/TFAP2A pathway Cell 155 2013 1022 1033
110. K.L. Reddy, J.M. Zullo, E. Bertolino, and H. Singh Transcriptional repression mediated by repositioning of genes to the nuclear lamina Nature 452 2008 243 247
111. S. Remeseiro, A. Cuadrado, and A. Losada Cohesin in development and disease Development 140 2013 3715 3718
112. V. Roukos, T.C. Voss, C.K. Schmidt, S. Lee, D. Wangsa, and T. Misteli Spatial dynamics of chromosome translocations in living cells Science 341 2013 660 664
113. E.D. Rubio, D.J. Reiss, P.L. Welcsh, C.M. Disteche, G.N. Filippova, N.S. Baliga, R. Aebersold, J.A. Ranish, and A. Krumm CTCF physically links cohesin to chromatin Proc. Natl. Acad. Sci. USA 105 2008 8309 8314
114. T. Sagai, M. Hosoya, Y. Mizushina, M. Tamura, and T. Shiroishi Elimination of a long-range cis-regulatory module causes complete loss of limb-specific Shh expression and truncation of the mouse limb Development 132 2005 797 803
115. A. Sanyal, B.R. Lajoie, G. Jain, and J. Dekker The long-range interaction landscape of gene promoters Nature 489 2012 109 113
116. S. Schoenfelder, T. Sexton, L. Chakalova, N.F. Cope, A. Horton, S. Andrews, S. Kurukuti, J.A. Mitchell, D. Umlauf, and D.S. Dimitrova et al. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells Nat. Genet. 42 2010 53 61
117. V.C. Seitan, B. Hao, K. Tachibana-Konwalski, T. Lavagnolli, H. Mira-Bontenbal, K.E. Brown, G. Teng, T. Carroll, A. Terry, and K. Horan et al. A role for cohesin in T-cell-receptor rearrangement and thymocyte differentiation Nature 476 2011 467 471
118. V.C. Seitan, A.J. Faure, Y. Zhan, R.P. McCord, B.R. Lajoie, E. Ing-Simmons, B. Lenhard, L. Giorgetti, E. Heard, and A.G. Fisher et al. Cohesin-based chromatin interactions enable regulated gene expression within preexisting architectural compartments Genome Res. 23 2013 2066 2077
119. S. Selvaraj, J. R Dixon, V. Bansal, and B. Ren Whole-genome haplotype reconstruction using proximity-ligation and shotgun sequencing Nat. Biotechnol. 31 2013 1111 1118
120. T. Sexton, E. Yaffe, E. Kenigsberg, F. Bantignies, B. Leblanc, M. Hoichman, H. Parrinello, A. Tanay, and G. Cavalli Three-dimensional folding and functional organization principles of the Drosophila genome Cell 148 2012 458 472
121. Y. Shen, F. Yue, D.F. McCleary, Z. Ye, L. Edsall, S. Kuan, U. Wagner, J. Dixon, L. Lee, V.V. Lobanenkov, and B. Ren A map of the cis-regulatory sequences in the mouse genome Nature 488 2012 116 120
122. M. Simonis, P. Klous, E. Splinter, Y. Moshkin, R. Willemsen, E. de Wit, B. van Steensel, and W. de Laat Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C) Nat. Genet. 38 2006 1348 1354
123. A. Smallwood, and B. Ren Genome organization and long-range regulation of gene expression by enhancers Curr. Opin. Cell Biol. 25 2013 387 394
124. S. Smemo, J.J. Tena, K.H. Kim, E.R. Gamazon, N.J. Sakabe, C. Gómez-Marín, I. Aneas, F.L. Credidio, D.R. Sobreira, and N.F. Wasserman et al. Obesity-associated variants within FTO form long-range functional connections with IRX3 Nature 507 2014 371 375
125. S. Sofueva, E. Yaffe, W.C. Chan, D. Georgopoulou, M. Vietri Rudan, H. Mira-Bontenbal, S.M. Pollard, G.P. Schroth, A. Tanay, and S. Hadjur Cohesin-mediated interactions organize chromosomal domain architecture EMBO J. 32 2013 3119 3129
126. E. Soler, C. Andrieu-Soler, E. de Boer, J.C. Bryne, S. Thongjuea, R. Stadhouders, R.J. Palstra, M. Stevens, C. Kockx, and W. van Ijcken et al. The genome-wide dynamics of the binding of Ldb1 complexes during erythroid differentiation Genes Dev. 24 2010 277 289
127. F. Song, P. Chen, D. Sun, M. Wang, L. Dong, D. Liang, R.M. Xu, P. Zhu, and G. Li Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units Science 344 2014 376 380
128. O. Symmons, V.V. Uslu, T. Tsujimura, S. Ruf, S. Nassari, W. Schwarzer, L. Ettwiller, and F. Spitz Functional and topological characteristics of mammalian regulatory domains Genome Res. 24 2014 390 400
129. I. Thomson, S. Gilchrist, W.A. Bickmore, and J.R. Chubb The radial positioning of chromatin is not inherited through mitosis but is established de novo in early G1 Curr. Biol. 14 2004 166 172
130. V.K. Tiwari, L. Cope, K.M. McGarvey, J.E. Ohm, and S.B. Baylin A novel 6C assay uncovers Polycomb-mediated higher order chromatin conformations Genome Res. 18 2008 1171 1179
131. B. Tolhuis, R.J. Palstra, E. Splinter, F. Grosveld, and W. de Laat Looping and interaction between hypersensitive sites in the active beta-globin locus Mol. Cell 10 2002 1453 1465
132. A.V. Tutter, M.P. Kowalski, G.A. Baltus, V. Iourgenko, M. Labow, E. Li, and S. Kadam Role for Med12 in regulation of Nanog and Nanog target genes J. Biol. Chem. 284 2009 3709 3718
133. C.R. Vakoc, D.L. Letting, N. Gheldof, T. Sawado, M.A. Bender, M. Groudine, M.J. Weiss, J. Dekker, and G.A. Blobel Proximity among distant regulatory elements at the beta-globin locus requires GATA-1 and FOG-1 Mol. Cell 17 2005 453 462
134. B. van Steensel, and S. Henikoff Identification of in vivo DNA targets of chromatin proteins using tethered dam methyltransferase Nat. Biotechnol. 18 2000 424 428
135. A. Visel, E.M. Rubin, and L.A. Pennacchio Genomic views of distant-acting enhancers Nature 461 2009 199 205
136. M. Visser, M. Kayser, and R.J. Palstra HERC2 rs12913832 modulates human pigmentation by attenuating chromatin-loop formation between a long-range enhancer and the OCA2 promoter Genome Res. 22 2012 446 455
137. J. Walter, L. Schermelleh, M. Cremer, S. Tashiro, and T. Cremer Chromosome order in HeLa cells changes during mitosis and early G1, but is stably maintained during subsequent interphase stages J. Cell Biol. 160 2003 685 697
138. M.N. Weedon, I. Cebola, A.M. Patch, S.E. Flanagan, E. De Franco, R. Caswell, S.A. Rodríguez-Seguí, C. Shaw-Smith, C.H. Cho, H. Lango Allen International Pancreatic Agenesis Consortium Recessive mutations in a distal PTF1A enhancer cause isolated pancreatic agenesis Nat. Genet. 46 2014 61 64
139. Z. Wei, F. Gao, S. Kim, H. Yang, J. Lyu, W. An, K. Wang, and W. Lu Klf4 organizes long-range chromosomal interactions with the oct4 locus in reprogramming and pluripotency Cell Stem Cell 13 2013 36 47
140. K.S. Wendt, K. Yoshida, T. Itoh, M. Bando, B. Koch, E. Schirghuber, S. Tsutsumi, G. Nagae, K. Ishihara, and T. Mishiro et al. Cohesin mediates transcriptional insulation by CCCTC-binding factor Nature 451 2008 796 801
141. R.R. Williams, V. Azuara, P. Perry, S. Sauer, M. Dvorkina, H. Jørgensen, J. Roix, P. McQueen, T. Misteli, M. Merkenschlager, and A.G. Fisher Neural induction promotes large-scale chromatin reorganisation of the Mash1 locus J. Cell Sci. 119 2006 132 140
142. N. Xu, M.E. Donohoe, S.S. Silva, and J.T. Lee Evidence that homologous X-chromosome pairing requires transcription and Ctcf protein Nat. Genet. 39 2007 1390 1396
143. J. Yan, M. Enge, T. Whitington, K. Dave, J. Liu, I. Sur, B. Schmierer, A. Jolma, T. Kivioja, M. Taipale, and J. Taipale Transcription factor binding in human cells occurs in dense clusters formed around cohesin anchor sites Cell 154 2013 801 813
144. Y. Zhang, R.P. McCord, Y.J. Ho, B.R. Lajoie, D.G. Hildebrand, A.C. Simon, M.S. Becker, F.W. Alt, and J. Dekker Spatial organization of the mouse genome and its role in recurrent chromosomal translocations Cell 148 2012 908 921
145. H. Zhang, W. Jiao, L. Sun, J. Fan, M. Chen, H. Wang, X. Xu, A. Shen, T. Li, and B. Niu et al. Intrachromosomal looping is required for activation of endogenous pluripotency genes during reprogramming Cell Stem Cell 13 2013 30 35
146. Y. Zhang, C.H. Wong, R.Y. Birnbaum, G. Li, R. Favaro, C.Y. Ngan, J. Lim, E. Tai, H.M. Poh, and E. Wong et al. Chromatin connectivity maps reveal dynamic promoter-enhancer long-range associations Nature 504 2013 306 310
147. J. Zhu, M. Adli, J.Y. Zou, G. Verstappen, M. Coyne, X. Zhang, T. Durham, M. Miri, V. Deshpande, and P.L. De Jager et al. Genome-wide chromatin state transitions associated with developmental and environmental cues Cell 152 2013 642 654
148. D. Zink, M.D. Amaral, A. Englmann, S. Lang, L.A. Clarke, C. Rudolph, F. Alt, K. Luther, C. Braz, and N. Sadoni et al. Transcription-dependent spatial arrangements of CFTR and adjacent genes in human cell nuclei J. Cell Biol. 166 2004 815 825
149. J. Zuin, J.R. Dixon, M.I. van der Reijden, Z. Ye, P. Kolovos, R.W. Brouwer, M.P. van de Corput, H.J. van de Werken, T.A. Knoch, and W.F. van IJcken et al. Cohesin and CTCF differentially affect chromatin architecture and gene expression in human cells Proc. Natl. Acad. Sci. USA 111 2014 996 1001