Functional and mechanistic diversity of distal transcription enhancers

Cell

Volumn 144, Issue 3, 2011, Pages 327-339

  Bulger, Michael ^a   Groudine, Mark ^b,c  

^a UNIVERSITY OF ROCHESTER   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR;

BACTERIAL CELL; CELL INTERACTION; CELL NUCLEUS; CELL SPECIFICITY; CELL TYPE; CHROMATIN; ENHANCER REGION; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENE STRUCTURE; GENETIC REGULATION; GENETIC VARIABILITY; HUMAN; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; MOLECULAR MECHANICS; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY DNA SEQUENCE; REVIEW; TRANSCRIPTION REGULATION; YEAST CELL;

METAZOA;

EID: 79551655285     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2011.01.024     Document Type: Review

References (126)

1. T. Amano, T. Sagai, H. Tanabe, Y. Mizushina, H. Nakazawa, and T. Shiroishi Chromosomal dynamics at the Shh locus: limb bud-specific differential regulation of competence and active transcription Dev. Cell 16 2009 47 57
2. E.D. Andrulis, A.M. Neiman, D.C. Zappulla, and R. Sternglanz Perinuclear localization of chromatin facilitates transcriptional silencing Nature 394 1998 592 595
3. J. Banerji, S. Rusconi, and W. Schaffner Expression of a beta-globin gene is enhanced by remote SV40 DNA sequences Cell 27 1981 299 308
4. J. Banerji, L. Olson, and W. Schaffner A lymphocyte-specific cellular enhancer is located downstream of the joining region in immunoglobulin heavy chain genes Cell 33 1983 729 740
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. M.A. Bender, M. Bulger, J. Close, and M. Groudine Beta-globin gene switching and DNase I sensitivity of the endogenous beta-globin locus in mice do not require the locus control region Mol. Cell 5 2000 387 393
7. E.M. Blackwood, and J.T. Kadonaga Going the distance: a current view of enhancer action Science 281 1998 60 63
8. M.J. Blow, D.J. McCulley, Z. Li, T. Zhang, J.A. Akiyama, A. Holt, I. Plajzer-Frick, M. Shoukry, C. Wright, and F. Chen ChIP-Seq identification of weakly conserved heart enhancers Nat. Genet. 42 2010 806 810
9. M.R. Branco, and A. Pombo Chromosome organization: new facts, new models Trends Cell Biol. 17 2007 127 134
10. J.M. Brown, J. Green, R.P. das Neves, H.A. Wallace, A.J. Smith, J. Hughes, N. Gray, S. Taylor, W.G. Wood, and D.R. Higgs Association between active genes occurs at nuclear speckles and is modulated by chromatin environment J. Cell Biol. 182 2008 1083 1097
11. M. Bulger, and M. Groudine Looping versus linking: toward a model for long-distance gene activation Genes Dev. 13 1999 2465 2477
12. J.E. Butler, and J.T. Kadonaga Enhancer-promoter specificity mediated by DPE or TATA core promoter motifs Genes Dev. 15 2001 2515 2519
13. S. Cai, H.J. Han, and T. Kohwi-Shigematsu Tissue-specific nuclear architecture and gene expression regulated by SATB1 Nat. Genet. 34 2003 42 51
14. 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
15. V.C. Calhoun, and M. Levine Long-range enhancer-promoter interactions in the Scr-Antp interval of the Drosophila Antennapedia complex Proc. Natl. Acad. Sci. USA 100 2003 9878 9883
16. V.C. Calhoun, A. Stathopoulos, and M. Levine Promoter-proximal tethering elements regulate enhancer-promoter specificity in the Drosophila Antennapedia complex Proc. Natl. Acad. Sci. USA 99 2002 9243 9247
17. Y.F. Chan, M.E. Marks, F.C. Jones, G. Villarreal Jr.; M.D. Shapiro, S.D. Brady, A.M. Southwick, D.M. Absher, J. Grimwood, and J. Schmutz Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer Science 327 2010 302 305
18. C.P. Chaturvedi, A.M. Hosey, C. Palii, C. Perez-Iratxeta, Y. Nakatani, J.A. Ranish, F.J. Dilworth, and M. Brand Dual role for the methyltransferase G9a in the maintenance of beta-globin gene transcription in adult erythroid cells Proc. Natl. Acad. Sci. USA 106 2009 18303 18308
19. M.P. Cosma, T. Tanaka, and K. Nasmyth Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle- and developmentally regulated promoter Cell 97 1999 299 311
20. T. Cremer, and M. Cremer Chromosome territories Cold Spring Harb. Perspect. Biol. 2 2010 a003889
21. G.E. Crawford, S. Davis, P.C. Scacheri, G. Renaud, M.J. Halawi, M.R. Erdos, R. Green, P.S. Meltzer, T.G. Wolfsberg, and F.S. Collins DNase-chip: a high-resolution method to identify DNase I hypersensitive sites using tiled microarrays Nat. Methods 3 2006 503 509
22. M.P. Creyghton, A.W. Cheng, G.G. Welstead, T. Kooistra, B.W. Carey, E.J. Steine, J. Hanna, M.A. Lodato, G.M. Frampton, and P.A. Sharp Histone H3K27ac separates active from poised enhancers and predicts developmental state Proc. Natl. Acad. Sci. USA 107 2010 21931 21936
23. K.E. Cullen, M.P. Kladde, and M.A. Seyfred Interaction between transcription regulatory regions of prolactin chromatin Science 261 1993 203 206
24. D. de Bruin, Z. Zaman, R.A. Liberatore, and M. Ptashne Telomere looping permits gene activation by a downstream UAS in yeast Nature 409 2001 109 113
25. J. Dekker, K. Rippe, M. Dekker, and N. Kleckner Capturing chromosome conformation Science 295 2002 1306 1311
26. Y.J. de Kok, E.R. Vossenaar, C.W. Cremers, N. Dahl, J. Laporte, L.J. Hu, D. Lacombe, N. Fischel-Ghodsian, R.A. Friedman, and L.S. Parnes Identification of a hot spot for microdeletions in patients with X-linked deafness type 3 (DFN3) 900 kb proximal to the DFN3 gene POU3F4 Hum. Mol. Genet. 5 1996 1229 1235
27. W. de Laat, P. Klous, J. Kooren, D. Noordermeer, R.J. Palstra, M. Simonis, E. Splinter, and F. Grosveld Three-dimensional organization of gene expression in erythroid cells Curr. Top. Dev. Biol. 82 2008 117 139
28. C. Demers, C.P. Chaturvedi, J.A. Ranish, G. Juban, P. Lai, F. Morle, R. Aebersold, F.J. Dilworth, M. Groudine, and M. Brand Activator-mediated recruitment of the MLL2 methyltransferase complex to the beta-globin locus Mol. Cell 27 2007 573 584
29. F. De Santa, I. Barozzi, F. Mietton, S. Ghisletti, S. Polletti, B.K. Tusi, H. Muller, J. Ragoussis, C.L. Wei, and G. Natoli A large fraction of extragenic RNA pol II transcription sites overlap enhancers PLoS Biol. 8 2010 e1000384
30. K.C. Dobi, and F. Winston Analysis of transcriptional activation at a distance in Saccharomyces cerevisiae Mol. Cell. Biol. 27 2007 5575 5586
31. D. Dorsett Distant liaisons: long-range enhancer-promoter interactions in Drosophila Curr. Opin. Genet. Dev. 9 1999 505 514
32. 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 Chromosome Conformation Capture Carbon Copy (5C): a massively parallel solution for mapping interactions between genomic elements Genome Res. 16 2006 1299 1309
33. R. Drissen, R.J. Palstra, N. Gillemans, E. Splinter, F. Grosveld, S. Philipsen, and W. de Laat The active spatial organization of the beta-globin locus requires the transcription factor EKLF Genes Dev. 18 2004 2485 2490
34. S.C. Elgin The formation and function of DNase I hypersensitive sites in the process of gene activation J. Biol. Chem. 263 1988 19259 19262
35. E.S. Emison, A.S. McCallion, C.S. Kashuk, R.T. Bush, E. Grice, S. Lin, M.E. Portnoy, D.J. Cutler, E.D. Green, and A. Chakravarti A common sex-dependent mutation in a RET enhancer underlies Hirschsprung disease risk Nature 434 2005 857 863
36. ENCODE Project Consortium Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project Nature 447 2007 799 816
37. C. Ferrai, I.J. de Castro, L. Lavitas, M. Chotalia, and A. Pombo Gene positioning Cold Spring Harbor Perspect. Biol. 2 2010 a000588
38. 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
39. C. Francastel, M.C. Walters, M. Groudine, and D.I. Martin A functional enhancer suppresses silencing of a transgene and prevents its localization close to centrometric heterochromatin Cell 99 1999 259 269
40. S. Ghisletti, I. Barozzi, F. Mietton, S. Polletti, F. De Santa, E. Venturini, L. Gregory, L. Lonie, A. Chew, and C.L. Wei Identification and characterization of enhancers controlling the inflammatory gene expression program in macrophages Immunity 32 2010 317 328
41. S.D. Gillies, S.L. Morrison, V.T. Oi, and S. Tonegawa A tissue-specific transcription enhancer element is located in the major intron of a rearranged immunoglobulin heavy chain gene Cell 33 1983 717 728
42. D.S. Gross, and W.T. Garrard Nuclease hypersensitive sites in chromatin Annu. Rev. Biochem. 57 1988 159 197
43. F. Grosveld, G.B. van Assendelft, D.R. Greaves, and G. Kollias Position-independent, high-level expression of the human beta-globin gene in transgenic mice Cell 51 1987 975 985
44. R. Hardison, J.L. Slightom, D.L. Gumucio, M. Goodman, N. Stojanovic, and W. Miller Locus control regions of mammalian beta-globin gene clusters: combining phylogenetic analyses and experimental results to gain functional insights Gene 205 1997 73 94
45. E.E. Hare, B.K. Peterson, V.N. Iyer, R. Meier, and M.B. Eisen Sepsid even-skipped enhancers are functionally conserved in Drosophila despite lack of sequence conservation PLoS Genet. 4 2008 e1000106
46. N.D. Heintzman, R.K. Stuart, G. Hon, Y. Fu, C.W. Ching, R.D. Hawkins, L.O. Barrera, S. Van Calcar, C. Qu, and K.A. Ching Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome Nat. Genet. 39 2007 311 318
47. N.D. Heintzman, G.C. Hon, R.D. Hawkins, P. Kheradpour, A. Stark, L.F. Harp, Z. Ye, L.K. Lee, R.K. Stuart, and C.W. Ching Histone modifications at human enhancers reflect global cell-type-specific gene expression Nature 459 2009 108 112
48. Y. Ho, F. Elefant, N. Cooke, and S. Liebhaber A defined locus control region determinant links chromatin domain acetylation with long-range gene activation Mol. Cell 9 2002 291 302
49. Y. Ho, F. Elefant, S.A. Liebhaber, and N.E. Cooke Locus control region transcription plays an active role in long-range gene activation Mol. Cell 23 2006 365 375
50. S.G. Holmes, and J.R. Broach Silencers are required for inheritance of the repressed state in yeast Genes Dev. 10 1996 1021 1032
51. C. Hou, R. Dale, and A. Dean Cell type specificity of chromatin organization mediated by CTCF and cohesin Proc. Natl. Acad. Sci. USA 107 2010 3651 3656
52. F.J. Iborra, A. Pombo, D.A. Jackson, and P.R. Cook Active RNA polymerases are localized within discrete transcription "factories" in human nuclei J. Cell Sci. 109 1996 1427 1436
53. T. Juven-Gershon, J.Y. Hsu, and J.T. Kadonaga Caudal, a key developmental regulator, is a DPE-specific transcriptional factor Genes Dev. 22 2008 2823 2830
54. 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 Mediator and cohesin connect gene expression and chromatin architecture Nature 467 2010 430 435
55. E. Kim, A. Magen, and G. Ast Different levels of alternative splicing among eukaryotes Nucleic Acids Res. 35 2007 125 131
56. A. Kim, H. Zhao, I. Ifrim, and A. Dean Beta-globin intergenic transcription and histone acetylation dependent on an enhancer Mol. Cell. Biol. 27 2007 2980 2986
57. T.K. Kim, M. Hemberg, J.M. Gray, A.M. Costa, D.M. Bear, J. Wu, D.A. Harmin, M. Laptewicz, K. Barbara-Haley, and S. Kuersten Widespread transcription at neuronal activity-regulated enhancers Nature 465 2010 182 187
58. D.A. Kleinjan, and V. van Heyningen Long-range control of gene expression: emerging mechanisms and disruption in disease Am. J. Hum. Genet. 76 2005 8 32
59. C.M. Koch, R.M. Andrews, P. Flicek, S.C. Dillon, U. Karaöz, G.K. Clelland, S. Wilcox, D.M. Beare, J.C. Fowler, and P. Couttet The landscape of histone modifications across 1% of the human genome in five human cell lines Genome Res. 17 2007 691 707
60. F. Koch, F. Jourquin, P. Ferrier, and J.C. Andrau Genome-wide RNA polymerase II: not genes only! Trends Biochem. Sci. 33 2008 265 273
61. J.E. Krebs, M.H. Kuo, C.D. Allis, and C.L. Peterson Cell cycle-regulated histone acetylation required for expression of the yeast HO gene Genes Dev. 13 1999 1412 1421
62. S. Kurukuti, V.K. Tiwari, G. Tavoosidana, E. Pugacheva, A. Murrell, Z. Zhao, V. Lobanenkov, W. Reik, and R. Ohlsson CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2 Proc. Natl. Acad. Sci. USA 103 2006 10684 10689
63. K.M. Leach, K. Nightingale, K. Igarashi, P.P. Levings, J.D. Engel, P.B. Becker, and J. Bungert Reconstitution of human beta-globin locus control region hypersensitive sites in the absence of chromatin assembly Mol. Cell. Biol. 21 2001 2629 2640
64. 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.A. 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
65. M. Levine Transcriptional enhancers in animal development and evolution Curr. Biol. 20 2010 R754 R763
66. D. Liber, R. Domaschenz, P.H. Holmqvist, L. Mazzarella, A. Georgiou, M. Leleu, A.G. Fisher, P.A. Labosky, and N. Dillon Epigenetic priming of a pre-B cell-specific enhancer through binding of Sox2 and Foxd3 at the ESC stage Cell Stem Cell 7 2010 114 126
67. 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 Comprehensive mapping of long-range interactions reveals folding principles of the human genome Science 326 2009 289 293
68. L. Melnikova, M. Kostuchenko, M. Silicheva, and P. Georgiev Drosophila gypsy insulator and yellow enhancers regulate activity of yellow promoter through the same regulatory element Chromosoma 117 2008 137 145
69. A. Miele, and J. Dekker Long-range chromosomal interactions and gene regulation Mol. Biosyst. 4 2008 1046 1057
70. A. Miele, and J. Dekker Mapping cis- and trans- chromatin interaction networks using chromosome conformation capture (3C) Methods Mol. Biol. 464 2009 105 121
71. A.M. Moon, and T.J. Ley Conservation of the primary structure, organization, and function of the human and mouse beta-globin locus-activating regions Proc. Natl. Acad. Sci. USA 87 1990 7693 7697
72. D.M. McGaughey, R.M. Vinton, J. Huynh, A. Al-Saif, M.A. Beer, and A.S. McCallion Metrics of sequence constraint overlook regulatory sequences in an exhaustive analysis at phox2b Genome Res. 18 2008 252 260
73. P.T. Moen Jr.; C.V. Johnson, M. Byron, L.S. Shopland, I.L. de la Serna, A.N. Imbalzano, and J.B. Lawrence Repositioning of muscle-specific genes relative to the periphery of SC-35 domains during skeletal myogenesis Mol. Biol. Cell 15 2004 197 206
74. P. Moreau, R. Hen, B. Wasylyk, R. Everett, M.P. Gaub, and P. Chambon The SV40 72 base repair repeat has a striking effect on gene expression both in SV40 and other chimeric recombinants Nucleic Acids Res. 9 1981 6047 6068
75. B.E. Morrow, S.P. Johnson, and J.R. Warner The rRNA enhancer regulates rRNA transcription in Saccharomyces cerevisiae Mol. Cell. Biol. 13 1993 1283 1289
76. L. Neigeborn, and J.R. Warner Expression of yeast 5S RNA is independent of the rDNA enhancer region Nucleic Acids Res. 18 1990 4179 4184
77. J.P. Noonan Regulatory DNAs and the evolution of human development Curr. Opin. Genet. Dev. 19 2009 557 564
78. J.P. Noonan, and A.S. McCallion Genomics of long-range regulatory elements Annu. Rev. Genomics Hum. Genet. 11 2010 1 23
79. D. Noordermeer, M.R. Branco, E. Splinter, P. Klous, W. van Ijcken, S. Swagemakers, M. Koutsourakis, P. van der Spek, A. Pombo, and W. de Laat Transcription and chromatin organization of a housekeeping gene cluster containing an integrated beta-globin locus control region PLoS Genet. 4 2008 e1000016
80. D.T. Odom, R.D. Dowell, E.S. Jacobsen, W. Gordon, T.W. Danford, K.D. MacIsaac, P.A. Rolfe, C.M. Conboy, D.K. Gifford, and E. Fraenkel Tissue-specific transcriptional regulation has diverged significantly between human and mouse Nat. Genet. 39 2007 730 732
81. S. Ohtsuki, M. Levine, and H.N. Cai Different core promoters possess distinct regulatory activities in the Drosophila embryo Genes Dev. 12 1998 547 556
82. U.A. Ørom, T. Derrien, M. Beringer, K. Gumireddy, A. Gardini, G. Bussotti, F. Lai, M. Zytnicki, C. Notredame, and Q. Huang Long noncoding RNAs with enhancer-like function in human cells Cell 143 2010 46 58
83. 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
84. V. Pant, S. Kurukuti, E. Pugacheva, S. Shamsuddin, P. Mariano, R. Renkawitz, E. Klenova, V. Lobanenkov, and R. Ohlsson 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 2004 3497 3504
85. M. Petrascheck, D. Escher, T. Mahmoudi, C.P. Verrijzer, W. Schaffner, and A. Barberis DNA looping induced by a transcriptional enhancer in vivo Nucleic Acids Res. 33 2005 3743 3750
86. J.E. Phillips, and V.G. Corces CTCF: master weaver of the genome Cell 137 2009 1194 1211
87. K.S. Pollard, S.R. Salama, N. Lambert, M.A. Lambot, S. Coppens, J.S. Pedersen, S. Katzman, B. King, C. Onodera, and A. Siepel An RNA gene expressed during cortical development evolved rapidly in humans Nature 443 2006 167 172
88. S. Prabhakar, J.P. Noonan, S. Pääbo, and E.M. Rubin Accelerated evolution of conserved noncoding sequences in humans Science 314 2006 786
89. S. Prabhakar, A. Visel, J.A. Akiyama, M. Shoukry, K.D. Lewis, A. Holt, I. Plajzer-Frick, H. Morrison, D.R. Fitzpatrick, and V. Afzal Human-specific gain of function in a developmental enhancer Science 321 2008 1346 1350
90. M. Ptashne Gene regulation by proteins acting nearby and at a distance Nature 322 1986 697 701
91. A. Rada-Iglesias, R. Bajpai, T. Swigut, S.A. Brugmann, R.A. Flynn, and J. Wysocka A unique chromatin signature uncovers early developmental enhancers in humans Nature 2010 10.1038/nature09692 in press. Published online December 15, 2010
92. T. Ragoczy, A. Telling, T. Sawado, M. Groudine, and S.T. Kosak A genetic analysis of chromosome territory looping: diverse roles for distal regulatory elements Chromosome Res. 11 2003 513 525
93. T. Ragoczy, M.A. Bender, A. Telling, R. Byron, and M. Groudine The locus control region is required for association of the murine beta-globin locus with engaged transcription factories during erythroid maturation Genes Dev. 20 2006 1447 1457
94. M. Rebeiz, J.E. Pool, V.A. Kassner, C.F. Aquadro, and S.B. Carroll Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population Science 326 2009 1663 1667
95. 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
96. R.A. Rollins, P. Morcillo, and D. Dorsett Nipped-B, a Drosophila homologue of chromosomal adherins, participates in activation by remote enhancers in the cut and Ultrabithorax genes Genetics 152 1999 577 593
97. 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
98. L.N. Rusche, A.L. Kirchmaier, and J. Rine The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae Annu. Rev. Biochem. 72 2003 481 516
99. 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
100. T. Sawado, J. Halow, M.A. Bender, and M. Groudine The beta -globin locus control region (LCR) functions primarily by enhancing the transition from transcription initiation to elongation Genes Dev. 17 2003 1009 1018
101. D. Schmidt, M.D. Wilson, B. Ballester, P.C. Schwalie, G.D. Brown, A. Marshall, C. Kutter, S. Watt, C.P. Martinez-Jimenez, and S. Mackay Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding Science 328 2010 1036 1040
102. S. Schoenfelder, T. Sexton, L. Chakalova, N.F. Cope, A. Horton, S. Andrews, S. Kurukuti, J.A. Mitchell, D. Umlauf, and D.S. Dimitrova Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells Nat. Genet. 42 2010 53 61
103. 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
104. E. Splinter, H. Heath, J. Kooren, R.J. Palstra, P. Klous, F. Grosveld, N. Galjart, and W. de Laat CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus Genes Dev. 20 2006 2349 2354
105. J.A. Stamatoyannopoulos, A. Goodwin, T. Joyce, and C.H. Lowrey NF-E2 and GATA binding motifs are required for the formation of DNase I hypersensitive site 4 of the human beta-globin locus control region EMBO J. 14 1995 106 116
106. H. Sutherland, and W.A. Bickmore Transcription factories: gene expression in unions? Nat. Rev. Genet. 10 2009 457 466
107. C.I. Swanson, N.C. Evans, and S. Barolo Structural rules and complex regulatory circuitry constrain expression of a Notch- and EGFR-regulated eye enhancer Dev. Cell 18 2010 359 370
108. A. Taddei Active genes at the nuclear pore complex Curr. Opin. Cell Biol. 19 2007 305 310
109. P.B. Talbert, and S. Henikoff Spreading of silent chromatin: inaction at a distance Nat. Rev. Genet. 7 2006 793 803
110. 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
111. L. Valenzuela, N. Dhillon, R.N. Dubey, M.R. Gartenberg, and R.T. Kamakaka Long-range communication between the silencers of HMR Mol. Cell. Biol. 28 2008 1924 1935
112. A. Visel, M.J. Blow, Z. Li, T. Zhang, J.A. Akiyama, A. Holt, I. Plajzer-Frick, M. Shoukry, C. Wright, and F. Chen ChIP-seq accurately predicts tissue-specific activity of enhancers Nature 457 2009 854 858
113. A. Visel, E.M. Rubin, and L.A. Pennacchio Genomic views of distant-acting enhancers Nature 461 2009 199 205
114. H. Wai, K. Johzuka, L. Vu, K. Eliason, T. Kobayashi, T. Horiuchi, and M. Nomura Yeast RNA polymerase I enhancer is dispensable for transcription of the chromosomal rRNA gene and cell growth, and its apparent transcription enhancement from ectopic promoters requires Fob1 protein Mol. Cell. Biol. 21 2001 5541 5553
115. Z. Wang, C. Zang, J.A. Rosenfeld, D.E. Schones, A. Barski, S. Cuddapah, K. Cui, T.Y. Roh, W. Peng, M.Q. Zhang, and K. Zhao Combinatorial patterns of histone acetylations and methylations in the human genome Nat. Genet. 40 2008 897 903
116. K.S. Wendt, K. Yoshida, T. Itoh, M. Bando, B. Koch, E. Schirghuber, S. Tsutsumi, G. Nagae, K. Ishihara, and T. Mishiro Cohesin mediates transcriptional insulation by CCCTC-binding factor Nature 451 2008 796 801
117. M.D. Wilson, N.L. Barbosa-Morais, D. Schmidt, C.M. Conboy, L. Vanes, V.L.J. Tybulewicz, E.M.C. Fisher, S. Tavaré, and D.T. Odom Species-specific transcription in mice carrying human chromosome 21 Science 322 2008 434 438
118. C. Wu The 5′ ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I Nature 286 1980 854 860
119. H. Xi, H.P. Shulha, J.M. Lin, T.R. Vales, Y. Fu, D.M. Bodine, R.D. McKay, J.G. Chenoweth, P.J. Tesar, and T.S. Furey Identification and characterization of cell type-specific and ubiquitous chromatin regulatory structures in the human genome PLoS Genet. 3 2007 e136
120. H. Xu, and T.R. Hoover Transcriptional regulation at a distance in bacteria Curr. Opin. Microbiol. 4 2001 138 144
121. M. Xu, and P.R. Cook Similar active genes cluster in specialized transcription factories J. Cell Biol. 181 2008 615 623
122. J. Xu, J.A. Watts, S.D. Pope, P. Gadue, M. Kamps, K. Plath, K.S. Zaret, and S.T. Smale Transcriptional competence and the active marking of tissue-specific enhancers by defined transcription factors in embryonic and induced pluripotent stem cells Genes Dev. 23 2009 2824 2838
123. T.M. Yusufzai, H. Tagami, Y. Nakatani, and G. Felsenfeld CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species Mol. Cell 13 2004 291 298
124. Z. Zhao, G. Tavoosidana, M. Sjölinder, A. Göndör, P. Mariano, S. Wang, C. Kanduri, M. Lezcano, K.S. Sandhu, and U. Singh Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions Nat. Genet. 38 2006 1341 1347
125. X. Zhu, J. Ling, L. Zhang, W. Pi, M. Wu, and D. Tuan A facilitated tracking and transcription mechanism of long-range enhancer function Nucleic Acids Res. 35 2007 5532 5544
126. R.P. Zinzen, C. Girardot, J. Gagneur, M. Braun, and E.E. Furlong Combinatorial binding predicts spatio-temporal cis-regulatory activity Nature 462 2009 65 70