Minireview: Conversing with chromatin: The language of nuclear receptors

Molecular Endocrinology

Volumn 28, Issue 1, 2014, Pages 3-15

  Biddie, Simon C ^a   John, Sam ^b  

^a ADDENBROOKE S HOSPITAL   (United Kingdom)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS RECEPTOR; STAT3 PROTEIN; TRANSCRIPTION FACTOR;

CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CIRCADIAN RHYTHM; DEACETYLATION; DNA METHYLATION; DNA SEQUENCE; HISTONE ACETYLATION; HISTONE MODIFICATION; PRIORITY JOURNAL; PROTEIN BINDING; RECEPTOR BINDING; REVIEW;

ANIMALS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; HISTONES; HUMANS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION;

EID: 84891511859     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2013-1247     Document Type: Review

References (168)

1. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997;389(6648):251-260.
2. Lee DY, Hayes JJ, Pruss D, Wolffe AP. A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell. 1993;72(1):73-84.
3. Miller KM, Tjeertes JV, Coates J, et al. Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining. Nat Struct Mol Biol. 2010;17(9): 1144-1151.
4. Xu M, Long C, Chen X, Huang C, Chen S, Zhu B. Partitioning of histone H3-H4 tetramers during DNA replication-dependent chromatin assembly. Science. 2010;328(5974):94-98.
5. Tachiwana H, Kagawa W, Shiga T, et al. Crystal structure of the human centromeric nucleosome containing CENP-A. Nature. 2011;476(7359):232-235.
6. Arrowsmith CH, Bountra C, Fish PV, Lee K, Schapira M. Epigenetic protein families: a new frontier for drug discovery. Nat Rev Drug Discov. 2012;1(5):384-400.
7. Scheidereit C, Geisse S, Westphal HM, Beato M. The glucocorticoid receptor binds to defined nucleotide sequences near the promoter of mouse mammary tumour virus. Nature. 1983;304(5928):749-752.
8. Zaret KS, Yamamoto KR. Reversible and persistent changes in chromatin structure accompany activation of a glucocorticoid-dependent enhancer element. Cell. 1984;38(1):29-38.
9. Wu C, Bingham PM, Livak KJ, Holmgren R, Elgin SC. The chromatin structure of specific genes: I. Evidence for higher order domains of defined DNA sequence. Cell. 1979;16(4):797-806.
10. Dorigo B, Schalch T, Kulangara A, Duda S, Schroeder RR, Richmond TJ. Nucleosome arrays reveal the two-start organization of the chromatin fiber. Science. 2004;306(5701):1571-1573.
11. Teif VB, Vainshtein Y, Caudron-Herger M, et al. Genome-wide nucleosome positioning during embryonic stem cell development. Nat Struct Mol Biol. 2012;19(11):1185-1192.
12. Valouev A, Johnson SM, Boyd SD, Smith CL, Fire AZ, Sidow A. Determinants of nucleosome organization in primary human cells. Nature. 2011;474(7352):516-520.
13. Grewal SI, Moazed D. Heterochromatin and epigenetic control of gene expression. Science. 2003;301(5634):798-802.
14. Peters AH, Kubicek S, Mechtler K, et al. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol Cell. 2003;12(6):1577-1589.
15. Mikkelsen TS, Ku M, Jaffe DB, et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature. 2007;448(7153):553-560.
16. Heintzman ND, Stuart RK, Hon G, et al. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet. 2007;39(3):311-318.
17. Bell O, Schwaiger M, Oakeley EJ, et al. Accessibility of the Drosophila genome discriminates PcG repression, H4K16 acetylation and replication timing. Nat Struct Mol Biol. 2010;17(7):894-900.
18. Payvar F, DeFranco D, Firestone GL, et al. Sequence-specific binding of glucocorticoid receptor to MTV DNA at sites within and upstream of the transcribed region. Cell. 1983;35(2 Pt 1):381-392.
19. Jongstra J, Reudelhuber TL, Oudet P, et al. Induction of altered chromatin structures by simian virus 40 enhancer and promoter elements. Nature. 1984;307(5953):708-714.
20. Lyko F, Brenton JD, Surani MA, Paro R. An imprinting element from the mouse H19 locus functions as a silencer in Drosophila. Nat Genet. 1997;16(2):171-173.
21. Boyle AP, Davis S, Shulha HP, et al. High-resolution mapping and characterization of open chromatin across the genome. Cell. 2008; 132(2):311-322.
22. Sabo PJ, Kuehn MS, Thurman R, et al. Genome-scale mapping of DNase I sensitivity in vivo using tiling DNA microarrays. Nat Methods. 2006;3(7):511-518.
23. Thurman RE, Rynes E, Humbert R, et al. The accessible chromatin landscape of the human genome. Nature. 2012;488(7414):75-82.
24. Grontved L, Bandle R, John S, et al. Rapid genome-scale mapping of chromatin accessibility in tissue. Epigenetics Chromatin. 2012; 5(1):10.
25. Kouzarides T. Chromatin modifications and their function. Cell. 2007;128(4):693-705.
26. Barski A, Cuddapah S, Cui K, et al. High-resolution profiling of histone methylations in the human genome. Cell. 2007;129(4): 823-837.
27. Wang Z, Zang C, Rosenfeld JA, et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet. 2008;40(7):897-903.
28. Kan PY, Lu X, Hansen JC, Hayes JJ. The H3 tail domain participates in multiple interactions during folding and self-association of nucleosome arrays. Mol Cell Biol. 2007;27(6):2084-2091.
29. Zhu Y, van Essen D, Saccani S. Cell-type-specific control of enhancer activity by H3K9 trimethylation. Mol Cell. 2012;46(4): 408-423.
30. Jones PL, Veenstra GJ, Wade PA, et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet. 1998;19(2):187-191.
31. Surani MA. Imprinting and the initiation of gene silencing in the germ line. Cell. 1998;93(3):309-312.
32. Sado T, Hoki Y, Sasaki H. Tsix silences Xist through modification of chromatin structure. Dev Cell. 2005;9(1):159-165.
33. John S, Sabo PJ, Thurman RE, et al. Chromatin accessibility predetermines glucocorticoid receptor binding patterns. Nat Genet. 2011;43(3):264-268.
34. Lefterova MI, Zhang Y, Steger DJ, et al. PPARγ and C/EBP factors orchestrate adipocyte biology via adjacent binding on a genomewide scale. Genes Dev. 2008;22(21):2941-2952.
35. Nielsen R, Pedersen TA, Hagenbeek D, et al. Genome-wide profiling of PPARγ:RXR and RNA polymerase II occupancy reveals temporal activation of distinct metabolic pathways and changes in RXR dimer composition during adipogenesis. Genes Dev. 2008; 22(21):2953-2967.
36. Lupien M, Eeckhoute J, Meyer CA, et al. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell. 2008;132(6):958-970.
37. Reddy TE, Pauli F, Sprouse RO, et al. Genomic determination of the glucocorticoid response reveals unexpected mechanisms of gene regulation. Genome Res. 2009;19(12):2163-2171.
38. Lefterova MI, Steger DJ, Zhuo D, et al. Cell-specific determinants of peroxisome proliferator-activated receptor γ function in adipocytes and macrophages. Mol Cell Biol. 2010;30(9):2078-2089.
39. Fryer CJ, Archer TK. Chromatin remodelling by the glucocorticoid receptor requires the BRG1 complex. Nature. 1998;393(6680):88-91.
40. John S, Sabo PJ, Johnson TA, et al. Interaction of the glucocorticoid receptor with the chromatin landscape. Mol Cell. 2008;29(5):611-624.
41. Reddy TE, Gertz J, Crawford GE, Garabedian MJ, Myers RM. The hypersensitive glucocorticoid response specifically regulates period 1 and expression of circadian genes. Mol Cell Biol. 2012;32(18): 3756-3767.
42. Grøntved L, John S, Baek S, et al. C/EBP maintains chromatin accessibility in liver and facilitates glucocorticoid receptor recruitment to steroid response elements. EMBO J. 2013;32(11):1568-1583.
43. Gertz J, Savic D, Varley KE, et al. Distinct properties of cell-typespecific and shared transcription factor binding sites. Mol Cell. 2013;52(1):25-36.
44. He HH, Meyer CA, Shin H, et al. Nucleosome dynamics define transcriptional enhancers. Nat Genet. 2010;42(4):343-347.
45. Jin C, Zang C, Wei G, et al. H3.3/H2A. Z double variant-containing nucleosomes mark 'nucleosome-free regions' of active promoters and other regulatory regions. Nat Genet. 2009;41(8):941-945.
46. Neph S, Vierstra J, Stergachis AB, et al. An expansive human regulatory lexicon encoded in transcription factor footprints. Nature. 2012;488(7414):83-90.
47. Burd CJ, Ward JM, Crusselle-Davis VJ, et al. Analysis of chromatin dynamics during glucocorticoid receptor activation. Mol Cell Biol. 2012;32(10):1805-1817.
48. Ballaré C, Castellano G, Gaveglia L, et al. Nucleosome-driven transcription factor binding and gene regulation. Mol Cell. 2013;49(1): 67-79.
49. Foulds CE, Feng Q, Ding C, et al. Proteomic analysis of coregulators bound to ERα on DNA and nucleosomes reveals coregulator dynamics. Mol Cell. 2013;51(2):185-199.
50. He HH, Meyer CA, Chen MW, Jordan VC, Brown M, Liu XS. Differential DNase I hypersensitivity reveals factor-dependent chromatin dynamics. Genome Res. 2012;22(6):1015-1025.
51. Louie MC, Yang HQ, MaAH, et al. Androgen-induced recruitment of RNA polymerase II to a nuclear receptor-p160 coactivator complex. Proc Natl Acad Sci USA. 2003;100(5):2226-2230.
52. Chakravarti D, LaMorte VJ, Nelson MC, et al. Role of CBP/P300 in nuclear receptor signalling. Nature. 1996;383(6595):99-103.
53. Wiench M, John S, Baek S, et al. DNA methylation status predicts cell type-specific enhancer activity. EMBO J. 2011;30(15):3028-3039.
54. Métivier R, Gallais R, Tiffoche C, et al. Cyclical DNA methylation of a transcriptionally active promoter. Nature. 2008;452(7183): 45-50.
55. Kangaspeska S, Stride B, Métivier R, et al. Transient cyclical methylation of promoter DNA. Nature. 2008;452(7183):112-115.
56. Shen Y, Yue F, McCleary DF, et al. A map of the cis-regulatory sequences in the mouse genome. Nature. 2012;488(7409):116-120.
57. Heintzman ND, Hon GC, Hawkins RD, et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature. 2009;459(7243):108-112.
58. Norris JD, Chang CY, Wittmann BM, et al. The homeodomain protein HOXB13 regulates the cellular response to androgens. Mol Cell. 2009;36(3):405-416.
59. York B, O'Malley BW. Steroid receptor coactivator (SRC) family: masters of systems biology. J Biol Chem. 2010;285(50):38743-38750.
60. Nagy L, Kao HY, Chakravarti D, et al. Nuclear receptor repression mediated by a complex containing SMRT, mSin3A, and histone deacetylase. Cell. 1997;89(3):373-380.
61. Heinz S, Benner C, Spann N, et al. Simple combinations of lineagedetermining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010;38(4): 576-589.
62. Lupien M, Eeckhoute J, Meyer CA, et al. Coactivator function defines the active estrogen receptor α cistrome. Mol Cell Biol. 2009; 29(12):3413-3423.
63. Louet JF, Chopra AR, Sagen JV, et al. The coactivator SRC-1 is an essential coordinator of hepatic glucose production. Cell Metab. 2010;12(6):606-618.
64. Winnay JN, Xu J, O'Malley BW, Hammer GD. Steroid receptor coactivator-1-deficient mice exhibit altered hypothalamic-pituitary-adrenal axis function. Endocrinology. 2006;147(3):1322-1332.
65. Han SJ, Hawkins SM, Begum K, et al. A new isoform of steroid receptor coactivator-1 is crucial for pathogenic progression of endometriosis. Nat Med. 2012;18(7):1102-1111.
66. Anzick SL, Kononen J, Walker RL, et al. AIB1, a steroid receptor coactivator amplified in breast and ovarian cancer. Science. 1997; 277(5328):965-968.
67. Liu Z, Wong J, Tsai SY, Tsai MJ, O'Malley BW. Sequential recruitment of steroid receptor coactivator-1 (SRC-1) and p300 enhances progesterone receptor-dependent initiation and reinitiation of transcription from chromatin. Proc Natl Acad Sci USA. 2001;98(22): 12426-12431.
68. Heery DM, Kalkhoven E, Hoare S, Parker MG. A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature. 1997;387(6634):733-736.
69. Feng W, Ribeiro RC, Wagner RL, et al. Hormone-dependent coactivator binding to a hydrophobic cleft on nuclear receptors. Science. 1998;280(5370):1747-1749.
70. Conway-Campbell BL, George CL, Pooley JR, et al. The HSP90 molecular chaperone cycle regulates cyclical transcriptional dynamics of the glucocorticoid receptor and its coregulatory molecules CBP/p300 during ultradian ligand treatment. Mol Endocrinol. 2011;25(6):944-954.
71. Zwart W, Theodorou V, Kok M, Canisius S, Linn S, Carroll JS. Oestrogen receptor-co-factor-chromatin specificity in the transcriptional regulation of breast cancer. EMBO J. 2011;30(23):4764-4776.
72. Ianculescu I, Wu DY, Siegmund KD, Stallcup MR. Selective roles for cAMP response element-binding protein binding protein and p300 protein as coregulators for androgen-regulated gene expression in advanced prostate cancer cells. J Biol Chem. 2012;287(6): 4000-4013.
73. Chen D, Ma H, Hong H, et al. Regulation of transcription by a protein methyltransferase. Science. 1999;284(5423):2174-2177.
74. Bauer UM, Daujat S, Nielsen SJ, Nightingale K, Kouzarides T. Methylation at arginine 17 of histone H3 is linked to gene activation. EMBO Rep. 2002;3(1):39-44.
75. Lee DY, Northrop JP, Kuo MH, Stallcup MR. Histone H3 lysine 9 methyltransferase G9a is a transcriptional coactivator for nuclear receptors. J Biol Chem. 2006;281(13):8476-8485.
76. Bittencourt D, Wu DY, Jeong KW, et al. G9a functions as a molecular scaffold for assembly of transcriptional coactivators on a subset of glucocorticoid receptor target genes. Proc Natl Acad Sci USA. 2012;109(48):19673-19678.
77. Yamane K, Toumazou C, Tsukada Y, et al. JHDM2A, a JmjCcontaining H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell. 2006;125(3):483-495.
78. Svotelis A, Bianco S, Madore J, et al. H3K27 demethylation by JMJD3 at a poised enhancer of anti-apoptotic gene BCL2 determines ER-α ligand dependency. EMBO J. 2011;30(19):3947-3946.
79. Ceschin DG, Walia M, Wenk SS, et al. Methylation specifies distinct estrogen-induced binding site repertoires of CBP to chromatin. Genes Dev. 2011;25(11):1132-1146.
80. Jeong KW, Kim K, Situ AJ, Ulmer TS, An W, Stallcup MR. Recognition of enhancer element-specific histone methylation by TIP60 in transcriptional activation. Nat Struct Mol Biol. 2011;18(12): 1358-1365.
81. Duplessis TT, Williams CC, Hill SM, Rowan BG. Phosphorylation of estrogen receptor α at serine 118 directs recruitment of promoter complexes and gene-specific transcription. Endocrinology. 2011; 152(6):2517-2526.
82. Galliher-Beckley AJ, Williams JG, Cidlowski JA. Ligand-independent phosphorylation of the glucocorticoid receptor integrates cellular stress pathways with nuclear receptor signaling. Mol Cell Biol. 2011;31(23):4663-4675.
83. Voss TC, John S, Hager GL. Single-cell analysis of glucocorticoid receptor action reveals that stochastic post-chromatin association mechanisms regulate ligand-specific transcription. Mol Endocrinol. 2006;20(11):2641-2655.
84. Biddie SC, John S, Sabo PJ, et al. Transcription factor AP1 potentiates chromatin accessibility and glucocorticoid receptor binding. Mol Cell. 2011;43(1):145-155.
85. Phillips-Cremins JE, Sauria ME, Sanyal A, et al. Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell. 2013;153(6):1281-1295.
86. Zhang J, Chalmers MJ, Stayrook KR, et al. DNA binding alters coactivator interaction surfaces of the intact VDR-RXR complex. Nat Struct Mol Biol. 2011;18(5):556-563.
87. Meijsing SH, Pufall MA, So AY, Bates DL, Chen L, Yamamoto KR. DNA binding site sequence directs glucocorticoid receptor structure and activity. Science. 2009;324(5925):407-410.
88. Surjit M, Ganti KP, Mukherji A, et al. Widespread negative response elements mediate direct repression by agonist-liganded glucocorticoid receptor. Cell. 2011;145(2):224-241.
89. Kasowski M, Grubert F, Heffelfinger C, et al. Variation in transcription factor binding among humans. Science. 2010;328(5975): 232-235.
90. McDaniell R, Lee BK, Song L, et al. Heritable individual-specific and allele-specific chromatin signatures in humans. Science. 2010; 328(5975):235-239.
91. Maurano MT, Humbert R, Rynes E, et al. Systematic localization of common disease-associated variation in regulatory DNA. Science. 2012;337(6099):1190-1195.
92. Perissi V, Jepsen K, Glass CK, Rosenfeld MG. Deconstructing repression: evolving models of co-repressor action. Nat Rev Genet. 2010;11(2):109-123.
93. Bilodeau S, Vallette-Kasic S, Gauthier Y, et al. Role of Brg1 and HDAC2 in GR trans-repression of the pituitary POMC gene and misexpression in Cushing disease. Genes Dev. 2006;20(20):2871-2886.
94. Phelan CA, Gampe RT Jr, Lambert MH, et al. Structure of Reverb α bound to N-CoR reveals a unique mechanism of nuclear receptor-co-repressor interaction. Nat Struct Mol Biol. 2010;17(7): 808-814.
95. Feng D, Liu T, Sun Z, et al. A circadian rhythm orchestrated by histone deacetylase 3 controls hepatic lipid metabolism. Science. 2011;331(6022):1315-1319.
96. Li MD, Ruan HB, Singh JP, et al. O-GlcNAc transferase is involved in glucocorticoid receptor-mediated transrepression. J Biol Chem. 2012;287(16):12904-12912.
97. Yang X, Zhang F, Kudlow JE. Recruitment of O-GlcNAc transferase to promoters by corepressor mSin3A: coupling protein OGlcNAcylation to transcriptional repression. Cell. 2002;110(1): 69-80.
98. Fujiki R, Hashiba W, Sekine H, et al. GlcNAcylation of histone H2B facilitates its monoubiquitination. Nature. 2011;480(7378): 557-560.
99. Robertson KD, Ait-Si-Ali S, Yokochi T, Wade PA, Jones PL, Wolffe AP. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat Genet. 2000;25(3):338-342.
100. Yen K, Vinayachandran V, Batta K, Koerber RT, Pugh BF. Genome-wide nucleosome specificity and directionality of chromatin remodelers. Cell. 2012;149(7):1461-1473.
101. Wiegand KC, Shah SP, Al-Agha OM, et al. ARID1A mutations in endometriosis-associated ovarian carcinomas. N Engl J Med. 2010;363(16):1532-1543.
102. Gui Y, Guo G, Huang Y, et al. Frequent mutations of chromatin remodeling genes in transitional cell carcinoma of the bladder. Nat Genet. 2011;43(9):875-878.
103. Li M, Zhao H, Zhang X, et al. Inactivating mutations of the chromatin remodeling gene ARID2 in hepatocellular carcinoma. Nat Genet. 2011;43(9):828-829.
104. Landry JW, Banerjee S, Taylor B, Aplan PD, Singer A, Wu C. Chromatin remodeling complex NURF regulates thymocyte maturation. Genes Dev. 2011;25(3):275-286.
105. Takeuchi JK, Lou X, Alexander JM, et al. Chromatin remodelling complex dosage modulates transcription factor function in heart development. Nat Commun. 2011;2:187.
106. Chia NY, Chan YS, Feng B, et al. A genome-wide RNAi screen reveals determinants of human embryonic stem cell identity. Nature. 2010;468(7321):316-320.
107. Jones S, Wang TL, Shih IM, et al. Frequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinoma. Science. 2010;330(6001):228-231.
108. Romero OA, Setien F, John S, et al. The tumour suppressor and chromatin remodelling factor BRG1 antagonizes Myc activity and promotes cell differentiation in human cancer. EMBO Mol Med. 2012;4(7):603-616.
109. Gaspar-Maia A, Alajem A, Polesso F, et al. Chd1 regulates open chromatin and pluripotency of embryonic stem cells. Nature. 2009;460(7257):863-868.
110. Rowbotham SP, Barki L, Neves-Costa A, et al. Maintenance of silent chromatin through replication requires SWI/SNF-like chromatin remodeler SMARCAD1. Mol Cell. 2011;42(3):285-296.
111. Ho L, Miller EL, Ronan JL, Ho WQ, Jothi R, Crabtree GR. esBAF facilitates pluripotency by conditioning the genome for LIF/ STAT3 signalling and by regulating polycomb function. Nat Cell Biol. 2011;13(8):903-913.
112. Watanabe H, Mizutani T, Haraguchi T, et al. SWI/SNF complex is essential for NRSF-mediated suppression of neuronal genes in human nonsmall cell lung carcinoma cell lines. Oncogene. 2006; 25(3):470-479.
113. Battaglioli E, Andrés ME, Rose DW, et al. REST repression of neuronal genes requires components of the HSWI. SNF complex. J Biol Chem. 2002;277(43):41038-41045.
114. Liu CL, Kaplan T, Kim M, Buratowski S, et al. Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol. 2005;3(10):e328.
115. Hauk G, McKnight JN, Nodelman IM, Bowman GD. The chromodomains of the Chd1 chromatin remodeler regulate DNA access to the ATPase motor. Mol Cell. 2010;39(5):711-723.
116. Hassan AH, Prochasson P, Neely KE, et al. Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes. Cell. 2002;111(3):369-379.
117. Junion G, Spivakov M, Girardot C, et al. A transcription factor collective defines cardiac cell fate and reflects lineage history. Cell. 2012;148(3):473-486.
118. Mullen AC, Orlando DA, Newman JJ, et al. Master transcription factors determine cell-type-specific responses to TGF-β signaling. Cell. 2011;147(3):565-576.
119. Ravasi T, Suzuki H, Cannistraci CV, et al. An atlas of combinatorial transcriptional regulation in mouse and man. Cell. 2010; 140(5):744-752.
120. Zinzen RP, Girardot C, Gagneur J, Braun M, Furlong EE. Combinatorial binding predicts spatio-temporal cis-regulatory activity. Nature. 2009;462(7269):65-70.
121. Kim J, Chu J, Shen X, Wang J, Orkin SH. An extended transcriptional network for pluripotency of embryonic stem cells. Cell. 2008;132(6):1049-1061.
122. Neph S, Stergachis AB, Reynolds A, Sandstrom R, Borenstein E, Stamatoyannopoulos JA. Circuitry and dynamics of human transcription factor regulatory networks. Cell. 2012;150(6):1274-1286.
123. Schüle R, Muller M, Kaltschmidt C, Renkawitz R. Many transcription factors interact synergistically with steroid receptors. Science. 1988;242(4884):1418-1420.
124. Shemshedini L, Knauthe R, Sassone-Corsi P, Pornon A, Gronemeyer H. Cell-specific inhibitory and stimulatory effects of Fos and Jun on transcription activation by nuclear receptors. EMBOJ. 1991;10(12):3839-3849.
125. Sakai DD, Helms S, Carlstedt-Duke J, Gustafsson JA, Rottman FM, Yamamoto KR. Hormone-mediated repression: a negative glucocorticoid response element from the bovine prolactin gene. Genes Dev. 1988;2(9):1144-1154.
126. Schüle R, Rangarajan P, Kliewer S, et al. Functional antagonism between oncoprotein c-Jun and the glucocorticoid receptor. Cell. 1990;62(6):1217-1226.
127. Diamond MI, Miner JN, Yoshinaga SK, Yamamoto KR. Transcription factor interactions: selectors of positive or negative regulation from a single DNA element. Science. 1990;249(4974): 1266-1272.
128. Langlais D, Couture C, Balsalobre A, Drouin J. The Stat3/GR interaction code: predictive value of direct/indirect DNA recruitment for transcription outcome. Mol Cell. 2012;47(1):38-49.
129. Adler S, Waterman ML, He X, Rosenfeld MG. Steroid receptormediated inhibition of rat prolactin gene expression does not require the receptor DNA-binding domain. Cell. 1988;52(5):685-695.
130. Reichardt HM, Kaestner KH, Tuckermann J, et al. DNA binding of the glucocorticoid receptor is not essential for survival. Cell. 1998;93(4):531-541.
131. Nissen RM, Yamamoto KR. The glucocorticoid receptor inhibits NFκB by interfering with serine-2 phosphorylation of the RNA polymerase II carboxy-terminal domain. Genes Dev. 2000; 14(18):2314-2329.
132. Chandra V, Huang P, Hamuro Y, et al. Structure of the intact PPAR-γ-RXR-nuclear receptor complex on DNA. Nature. 2008; 456(7220):350-356.
133. Shen Q, Bai Y, Chang KC, et al. Liver X receptor-retinoid X receptor (LXR-RXR) heterodimer cistrome reveals coordination of LXR and AP1 signaling in keratinocytes. J Biol Chem. 2011; 286(16):14554-14563.
134. Szanto A, Balint BL, Nagy ZS, et al. STAT6 transcription factor is a facilitator of the nuclear receptor PPARγ-regulated gene expression in macrophages and dendritic cells. Immunity. 2010;33(5): 699-712.
135. Voss TC, Schiltz RL, Sung MH, et al. Dynamic exchange at regulatory elements during chromatin remodeling underlies assisted loading mechanism. Cell. 2011;146(4):544-554.
136. Miranda TB, Voss TC, Sung MH, et al. Reprogramming the chromatin landscape: interplay of the estrogen and glucocorticoid receptors at the genomic level. Cancer Res. 2013;73:5130-5139.
137. Hurtado A, Holmes KA, Ross-Innes CS, Schmidt D, Carroll JS. FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat Genet. 2011;43(1):27-33.
138. Wang D, Garcia-Bassets I, Benner C, et al. Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA. Nature. 2011;474(7351):390-394.
139. Ross-Innes CS, Stark R, Teschendorff AE, et al. Differential oestrogen receptor binding is associated with clinical outcome in breast cancer. Nature. 2012;481(7381):389-393.
140. Lupien M, Meyer CA, Bailey ST, et al. Growth factor stimulation induces a distinct ERα cistrome underlying breast cancer endocrine resistance. Genes Dev. 2010;24(19):2219-2227.
141. Rao NA, McCalman MT, Moulos P, et al. Coactivation ofGRand NFKB alters the repertoire of their binding sites and target genes. Genome Res. 2011;21(9):1404-1416.
142. Novershtern N, Subramanian A, Lawton LN, et al. Densely interconnected transcriptional circuits control cell states in human hematopoiesis. Cell. 2011;144(2):296-309.
143. Xu J, Shao Z, Glass K, et al. Combinatorial assembly of developmental stage-specific enhancers controls gene expression programs during human erythropoiesis. Dev Cell. 2012;23(4):796-811.
144. Samstein RM, Arvey A, Josefowicz SZ, et al. Foxp3 exploits a pre-existent enhancer landscape for regulatory T cell lineage specification. Cell. 2012;151(1):153-166.
145. Paige SL, Thomas S, Stoick-Cooper CL, et al. A temporal chromatin signature in human embryonic stem cells identifies regulators of cardiac development. Cell. 2012;151(1):221-232.
146. Siersbaek R, Nielsen R, John S, et al. Extensive chromatin remodelling and establishment of transcription factor 'hotspots' during early adipogenesis. EMBO J. 2011;30(8):1459-1472.
147. Steger DJ, Grant GR, Schupp M, et al. Propagation of adipogenic signals through an epigenomic transition state. Genes Dev. 2010; 24(10):1035-1044.
148. Stavreva DA, Wiench M, John S, et al. Ultradian hormone stimu-lation induces glucocorticoid receptor-mediated pulses of gene transcription. Nat Cell Biol. 2009;11(9):1093-1102.
149. Chng KR, Chang CW, Tan SK, et al. A transcriptional repressor co-regulatory network governing androgen response in prostate cancers. EMBO J. 2012;31(12):2810-2823.
150. Barbieri CE, Baca SC, Lawrence MS, et al. Exome sequencing identifies recurrent SPOP, FOXA1 and MED12 mutations in prostate cancer. Nat Genet. 2012;44(6):685-689.
151. Fujimoto A, Totoki Y, Abe T, et al. Whole-genome sequencing of liver cancers identifies etiological influences on mutation patterns and recurrent mutations in chromatin regulators. Nat Genet. 2012;44(7):760-764.
152. Jagani Z, Mora-Blanco EL, Sansam CG, et al. Loss of the tumor suppressor Snf5 leads to aberrant activation of the Hedgehog-Gli pathway. Nat Med. 2010;16:1429-1433.
153. Nie Z, Xue Y, Yang D, et al. A specificity and targeting subunit of a human SWI/SNF family-related chromatin-remodeling complex. Mol Cell Biol. 2000;20(23):8879-8888.
154. Yan Z. PBAF chromatin-remodeling complex requires a novel specificity subunit, BAF200, to regulate expression of selective interferon-responsive genes. Genes Dev. 2005;19(14):1662-1667.
155. Lemon B, Inouye C, King DS, Tjian R. Selectivity of chromatinremodelling cofactors for ligand-activated transcription. Nature. 2001;414(6866):924-928.
156. Debril MB, Gelman L, Fayard E, Annicotte JS, Rocchi S, Auwerx J. Transcription factors and nuclear receptors interact with the SWI/SNF complex through the BAF60c subunit. J Biol Chem. 2004;279(16):16677-16686.
157. Link KA, Burd CJ, Williams E, et al. BAF57 governs androgen receptor action and androgen-dependent proliferation through SWI/SNF. Mol Cell Biol. 2005;25(6):2200-2215.
158. Nik-Zainal S, Alexandrov LB, Wedge DC, et al. Mutational processes molding the genomes of 21 breast cancers. Cell. 2012; 149(5):979-993.
159. Pasqualucci L, Dominguez-Sola D, Chiarenza A, Fabbri G, Grunn A, Trifonov V, et al. Inactivating mutations of acetyltransferase genes in B-cell lymphoma. Nature. 2011;471(7337):189-195.
160. Lonard DM, O'Malley BW. Nuclear receptor coregulators: modulators of pathology and therapeutic targets. Nat Rev Endocrinol. 2012;8(10):598-604.
161. Petrij F, Giles RH, Dauwerse HG, et al. Rubinstein-Taybi syndrome caused by mutations in the transcriptional co-activator CBP. Nature. 1995;376:348-351.
162. Santen GW, Aten E, Sun Y, et al. Mutations in SWI/SNF chromatin remodeling complex gene ARID1B cause Coffin-Siris syndrome. Nat Genet. 2012;44(4):379-380.
163. Tsurusaki Y, Okamoto N, Ohashi H, et al. Mutations affecting components of the SWI/SNF complex cause Coffin-Siris syndrome. Nat Genet. 2012;44(4):376-378.
164. Van Houdt JK, Nowakowska BA, Sousa SB, et al. Heterozygous missense mutations in SMARCA2 cause Nicolaides-Baraitser syndrome. Nat Genet. 2012;44(4):445-449.
165. Malovannaya A, Lanz RB, Jung SY, et al. Analysis of the human endogenous coregulator complexome. Cell. 2011;145(5):787-799.
166. Dawson MA, Prinjha RK, Dittmann A, et al. Inhibition of BET recruitment to chromatin as an effective treatment for MLL-fusion leukaemia. Nature. 2011;478(7370):529-533.
167. Filippakopoulos P, Qi J, Picaud S, et al. Selective inhibition of BET bromodomains. Nature. 2010;468(7327):1067-1073.
168. Delmore JE, Issa GC, Lemieux ME, et al. BET bromodomain inhibition as a therapeutic strategy to target c-Myc. Cell. 2011; 146(6):904-917.