The histone variant H2A.Z is an important regulator of enhancer activity

Nucleic Acids Research

Volumn 43, Issue 20, 2015, Pages 9742-9756

  Brunelle, Mylène ^a   Nordell Markovits, Alexei ^a,b   Rodrigue, Sébastien ^a   Lupien, Mathieu ^a   Jacques, Pierre Étienne ^a,b,c   Gévry, Nicolas ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

^b PRINCESS MARGARET HOSPITAL   (Canada)

^c CENTRE HOSPITALIER UNIVERSITAIRE DE SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COHESIN; DNA; ENHANCER RNA; ESTROGEN; ESTROGEN RECEPTOR ALPHA; HISTONE H2AZ; HISTONE H3; PROTEIN RAD21; RNA; RNA POLYMERASE II; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; CHROMATIN; ESTRADIOL; HISTONE; HISTONE H2A.F-Z; NONHISTONE PROTEIN; NUCLEOSOME;

ARTICLE; CHROMATIN; CONTROLLED STUDY; DNA METHYLATION; ENHANCER REGION; HUMAN; HUMAN CELL; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN FUNCTION; RNA TRANSCRIPTION; SEQUENCE ANALYSIS; GENOMICS; HISTONE CODE; MCF-7 CELL LINE; METABOLISM; TRANSCRIPTION INITIATION;

CELL CYCLE PROTEINS; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA METHYLATION; ENHANCER ELEMENTS, GENETIC; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; GENOMICS; HISTONE CODE; HISTONES; MCF-7 CELLS; NUCLEOSOMES; RNA POLYMERASE II; TRANSCRIPTIONAL ACTIVATION;

EID: 84950111512     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv825     Document Type: Article

References (92)

1. Lupien, M. , Eeckhoute, J. , Meyer, C. A. , Wang, Q. , Zhang, Y. , Li, W. , Carroll, J. S. , Liu, X. S. and Brown, M. (2008) FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell, 132, 958-970.
2. Heintzman, N. D. , Hon, G. C. , Hawkins, R. D. , Kheradpour, P. , Stark, A. , Harp, L. F. , Ye, Z. , Lee, L. K. , Stuart, R. K. , Ching, C. W. et al. (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature, 459, 108-112.
3. Ernst, J. , Kheradpour, P. , Mikkelsen, T. S. , Shoresh, N. , Ward, L. D. , Epstein, C. B. , Zhang, X. , Wang, L. , Issner, R. , Coyne, M. et al. (2011) Mapping and analysis of chromatin state dynamics in nine human cell types. Nature, 473, 43-49.
4. Akhtar-Zaidi, B. , Cowper-Sal-lari, R. , Corradin, O. , Saiakhova, A. , Bartels, C. F. , Balasubramanian, D. , Myeroff, L. , Lutterbaugh, J. , Jarrar, A. , Kalady, M. F. et al. (2012) Epigenomic enhancer profiling defines a signature of colon cancer. Science, 336, 736-739.
5. Heintzman, N. D. , Stuart, R. K. , Hon, G. , Fu, Y. , Ching, C. W. , Hawkins, R. D. , Barrera, L. O. , Calcar, S. V. , Qu, C. , Ching, K. A. et al. (2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. , 39, 311-318.
6. Ernst, J. and Kellis, M. (2010) Discovery and characterization of chromatin states for systematic annotation of the human genome. Nat. Biotechnol. , 28, 817-825.
7. Creyghton, M. P. , Cheng, A. W. , Welstead, G. G. , Kooistra, T. , Carey, B. W. , Steine, E. J. , Hanna, J. , Lodato, M. A. , Frampton, G. M. , Sharp, P. A. et al. (2010) Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl. Acad. Sci. U. S. A. , 107, 21931-21936.
8. Rada-Iglesias, A. , Bajpai, R. , Swigut, T. , Brugmann, S. A. , Flynn, R. A. and Wysocka, J. (2011) A unique chromatin signature uncovers early developmental enhancers in humans. Nature, 470, 279-283.
9. Zentner, G. E. , Tesar, P. J. and Scacheri, P. C. (2011) Epigenetic signatures distinguish multiple classes of enhancers with distinct cellular functions. Genome Res, 21, 1273-1283.
10. Visel, A. , Blow, M. J. , Li, Z. , Zhang, T. , Akiyama, J. A. , Holt, A. , Plajzer-Frick, I. , Shoukry, M. , Wright, C. , Chen, F. et al. (2009) ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature, 457, 854-858.
11. Gross, D. S. and Garrard, W. T. (1988) Nuclease hypersensitive sites in chromatin. Annu. Rev. Biochem. , 57, 159-197.
12. Thurman, R. E. , Rynes, E. , Humbert, R. , Vierstra, J. , Maurano, M. T. , Haugen, E. , Sheffield, N. C. , Stergachis, A. B. , Wang, H. , Vernot, B. et al. (2012) The accessible chromatin landscape of the human genome. Nature, 489, 75-82.
13. Tillo, D. , Kaplan, N. , Moore, I. K. , Fondufe-Mittendorf, Y. , Gossett, A. J. , Field, Y. , Lieb, J. D. , Widom, J. , Segal, E. and Hughes, T. R. (2010) High nucleosome occupancy is encoded at human regulatory sequences. PLoS One, 5, e9129.
14. Nili, E. L. , Field, Y. , Lubling, Y. , Widom, J. , Oren, M. and Segal, E. (2010) p53 binds preferentially to genomic regions with high DNA-encoded nucleosome occupancy. Genome Res. , 20, 1361-1368.
15. Mito, Y. , Henikoff, J. G. and Henikoff, S. (2007) Histone replacement marks the boundaries of cis-regulatory domains. Science, 315, 1408-1411.
16. Jin, C. and Felsenfeld, G. (2007) Nucleosome stability mediated by histone variants H3. 3 and H2A. Z. Genes Dev. , 21, 1519-1529.
17. Jin, C. , Zang, C. , Wei, G. , Cui, K. , Peng, W. , Zhao, K. and Felsenfeld, G. (2009) H3. 3/H2A. Z double variant-containing nucleosomes mark nucleosome-free regions of active promoters and other regulatory regions. Nat. Genet. , 41, 941-945.
18. Henikoff, S. , Henikoff, J. G. , Sakai, A. , Loeb, G. B. and Ahmad, K. (2009) Genome-wide profiling of salt fractions maps physical properties of chromatin. Genome Res. , 19, 460-469.
19. Kundaje, A. , Kyriazopoulou-Panagiotopoulou, S. , Libbrecht, M. , Smith, C. L. , Raha, D. , Winters, E. E. , Johnson, S. M. , Snyder, M. , Batzoglou, S. and Sidow, A. (2012) Ubiquitous heterogeneity and asymmetry of the chromatin environment at regulatory elements. Genome Res. , 22, 1735-1747.
20. Schones, D. E. , Cui, K. , Cuddapah, S. , Roh, T.-Y. , Barski, A. , Wang, Z. , Wei, G. and Zhao, K. (2008) Dynamic regulation of nucleosome positioning in the human genome. Cell, 132, 887-898.
21. He, H. H. , Meyer, C. A. , Shin, H. , Bailey, S. T. , Wei, G. , Wang, Q. , Zhang, Y. , Xu, K. , Ni, M. , Lupien, M. et al. (2010) Nucleosome dynamics define transcriptional enhancers. Nat. Genet. , 42, 343-347.
22. Hu, G. , Schones, D. E. , Cui, K. , Ybarra, R. , Northrup, D. , Tang, Q. , Gattinoni, L. , Restifo, N. P. , Huang, S. and Zhao, K. (2011) Regulation of nucleosome landscape and transcription factor targeting at tissue-specific enhancers by BRG1. Genome Res. , 21, 1650-1658.
23. Wang, D. , Garcia-Bassets, I. , Benner, C. , Li, W. , Su, X. , Zhou, Y. , Qiu, J. , Liu, W. , Kaikkonen, M. U. , Ohgi, K. A. et al. (2011) Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA. Nature, 474, 390-394.
24. He, H. H. , Meyer, C. A. , Chen, M. W. , Jordan, V. C. , Brown, M. and Liu, X. S. (2012) Differential DNase I hypersensitivity reveals factor-dependent chromatin dynamics. Genome Res. , 22, 1015-1025.
25. Barski, A. , Cuddapah, S. , Cui, K. , Roh, T.-Y. , Schones, D. E. , Wang, Z. , Wei, G. , Chepelev, I. and Zhao, K. (2007) High-resolution profiling of histone methylations in the human genome. Cell, 129, 823-837.
26. Ruhl, D. D. , Jin, J. , Cai, Y. , Swanson, S. , Florens, L. , Washburn, M. P. , Conaway, R. C. , Conaway, J. W. and Chrivia, J. C. (2006) Purification of a human SRCAP complex that remodels chromatin by incorporating the histone variant H2A. Z into nucleosomes. Biochemistry, 45, 5671-5677.
27. Gévry, N. , Chan, H. M. , Laflamme, L. , Livingston, D. M. and Gaudreau, L. (2007) p21 transcription is regulated by differential localization of histone H2A. Z. Genes Dev. , 21, 1869-1881.
28. Tolstorukov, M. Y. , Kharchenko, P. V. , Goldman, J. A. , Kingston, R. E. and Park, P. J. (2009) Comparative analysis of H2A. Z nucleosome organization in the human and yeast genomes. Genome Res. , 19, 967-977.
29. Hu, G. , Cui, K. , Northrup, D. , Liu, C. , Wang, C. , Tang, Q. , Ge, K. , Levens, D. , Crane-Robinson, C. and Zhao, K. (2013) H2A. Z facilitates access of active and repressive complexes to chromatin in embryonic stem cell self-renewal and differentiation. Cell Stem Cell, 12, 180-192.
30. Joseph, R. , Orlov, Y. L. , Huss, M. , Sun, W. , Kong, S. L. , Ukil, L. , Pan, Y. F. , Li, G. , Lim, M. , Thomsen, J. S. et al. (2010) Integrative model of genomic factors for determining binding site selection by estrogen receptor. Mol. Syst. Biol. , 6, 456.
31. John, S. , Sabo, P. J. , Thurman, R. E. , Sung, M.-H. , Biddie, S. C. , Johnson, T. A. , Hager, G. L. and Stamatoyannopoulos, J. A. (2011) Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nat. Genet. , 43, 264-268.
32. Gertz, J. , Savic, D. , Varley, K. E. , Partridge, E. C. , Safi, A. , Jain, P. , Cooper, G. M. , Reddy, T. E. , Crawford, G. E. and Myers, R. M. (2013) Distinct properties of cell-type-specific and shared transcription factor binding sites. Mol. Cell, 52, 25-36.
33. John, S. , Sabo, P. J. , Johnson, T. A. , Sung, M.-H. , Biddie, S. C. , Lightman, S. L. , Voss, T. C. , Davis, S. R. , Meltzer, P. S. , Stamatoyannopoulos, J. A. et al. (2008) Interaction of the glucocorticoid receptor with the chromatin landscape. Mol. Cell, 29, 611-624.
34. Gévry, N. , Hardy, S. , Jacques, P.-E. , Laflamme, L. , Svotelis, A. , Robert, F. and Gaudreau, L. (2009) Histone H2A. Z is essential for estrogen receptor signaling. Genes Dev. , 23, 1522-1533.
35. Dalvai, M. , Fleury, L. , Bellucci, L. , Kocanova, S. and Bystricky, K. (2013) TIP48/Reptin and H2A. Z requirement for initiating chromatin remodeling in estrogen-activated transcription. PLoS Genet. , 9, e1003387.
36. Eeckhoute, J. , Carroll, J. S. , Geistlinger, T. R. , Torres-Arzayus, M. I. and Brown, M. (2006) A cell-type-specific transcriptional network required for estrogen regulation of cyclin D1 and cell cycle progression in breast cancer. Genes Dev. , 20, 2513-2526.
37. Pekowska, A. , Benoukraf, T. , Zacarias-Cabeza, J. , Belhocine, M. , Koch, F. , Holota, H. , Imbert, J. , Andrau, J.-C. , Ferrier, P. and Spicuglia, S. (2011) H3K4 tri-methylation provides an epigenetic signature of active enhancers. EMBO J, 30, 4198-4210.
38. Carroll, J. S. , Meyer, C. A. , Song, J. , Li, W. , Geistlinger, T. R. , Eeckhoute, J. , Brodsky, A. S. , Keeton, E. K. , Fertuck, K. C. , Hall, G. F. et al. (2006) Genome-wide analysis of estrogen receptor binding sites. Nat. Genet. , 38, 1289-1297.
39. Svotelis, A. , Gévry, N. and Gaudreau, L. (2009) Chromatin immunoprecipitation in mammalian cells. Methods Mol. Biol. , 543, 243-251.
40. Rodrigue, S. , Materna, A. C. , Timberlake, S. C. , Blackburn, M. C. , Malmstrom, R. R. , Alm, E. J. and Chisholm, S. W. (2010) Unlocking short read sequencing for metagenomics. PLoS One, 5, e11840.
41. Li, H. and Durbin, R. (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754-1760.
42. Hoffman, M. M. , Ernst, J. , Wilder, S. P. , Kundaje, A. , Harris, R. S. , Libbrecht, M. , Giardine, B. , Ellenbogen, P. M. , Bilmes, J. A. , Birney, E. et al. (2013) Integrative annotation of chromatin elements from ENCODE data. Nucleic Acids Res. , 41, 827-841.
43. Zhang, Y. , Liu, T. , Meyer, C. A. , Eeckhoute, J. , Johnson, D. S. , Bernstein, B. E. , Nusbaum, C. , Myers, R. M. , Brown, M. , Li, W. et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol. , 9, R137.
44. Ye, T. , Krebs, A. R. , Choukrallah, M.-A. , Keime, C. , Plewniak, F. , Davidson, I. and Tora, L. (2011) seqMINER: an integrated ChIP-seq data interpretation platform. Nucleic Acids Res. , 39, e35.
45. Schmidt, D. , Schwalie, P. C. , Ross-Innes, C. S. , Hurtado, A. , Brown, G. D. , Carroll, J. S. , Flicek, P. and Odom, D. T. (2010) A CTCF-independent role for cohesin in tissue-specific transcription. Genome Res. , 20, 578-588.
46. Carroll, J. S. , Liu, X. S. , Brodsky, A. S. , Li, W. , Meyer, C. A. , Szary, A. J. , Eeckhoute, J. , Shao, W. , Hestermann, E. V. , Geistlinger, T. R. et al. (2005) Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell, 122, 33-43.
47. Magnani, L. , Ballantyne, E. B. , Zhang, X. and Lupien, M. (2011) PBX1 genomic pioneer function drives ER- signaling underlying progression in breast cancer. PLoS Genet. , 7, e1002368.
48. Tan, S. K. , Lin, Z. H. , Chang, C. W. , Varang, V. , Chng, K. R. , Pan, Y. F. , Yong, E. L. , Sung, W. K. , Sung, W. K. and Cheung, E. (2011) AP-2- regulates oestrogen receptor-mediated long-range chromatin interaction and gene transcription. EMBO J, 30, 2569-2581.
49. Sérandour, A. A. , Avner, S. , Percevault, F. , Demay, F. , Bizot, M. , Lucchetti-Miganeh, C. , Barloy-Hubler, F. , Brown, M. , Lupien, M. , Métivier, R. et al. (2011) Epigenetic switch involved in activation of pioneer factor FOXA1-dependent enhancers. Genome Res. , 21, 555-565.
50. Tang, Q. , Chen, Y. , Meyer, C. , Geistlinger, T. , Lupien, M. , Wang, Q. , Liu, T. , Zhang, Y. , Brown, M. and Liu, X. S. (2011) A comprehensive view of nuclear receptor cancer cistromes. Cancer Res. , 71, 6940-6947.
51. Hardy, S. , Jacques, P.-E. , Gévry, N. , Forest, A. , Fortin, M.-E. , Laflamme, L. , Gaudreau, L. and Robert, F. (2009) The euchromatic and heterochromatic landscapes are shaped by antagonizing effects of transcription on H2A. Z deposition. PLoS Genet. , 5, e1000687.
52. Fullwood, M. J. , Liu, M. H. , Pan, Y. F. , Liu, J. , Xu, H. , Mohamed, Y. B. , Orlov, Y. L. , Velkov, S. , Ho, A. , Mei, P. H. et al. (2009) An oestrogen-receptor-alpha-bound human chromatin interactome. Nature, 462, 58-64.
53. Tropberger, P. , Pott, S. , Keller, C. , Kamieniarz-Gdula, K. , Caron, M. , Richter, F. , Li, G. , Mittler, G. , Liu, E. T. , Bühler, M. et al. (2013) Regulation of transcription through acetylation of H3K122 on the lateral surface of the histone octamer. Cell, 152, 859-872.
54. Zwart, W. , Theodorou, V. , Kok, M. , Canisius, S. , Linn, S. and Carroll, J. S. (2011) Oestrogen receptor-co-factor-chromatin specificity in the transcriptional regulation of breast cancer. EMBO J, 30, 4764-4776.
55. Neph, S. , Vierstra, J. , Stergachis, A. B. , Reynolds, A. P. , Haugen, E. , Vernot, B. , Thurman, R. E. , John, S. , Sandstrom, R. , Johnson, A. K. et al. (2012) An expansive human regulatory lexicon encoded in transcription factor footprints. Nature, 489, 83-90.
56. Métivier, R. , Gallais, R. , Tiffoche, C. , Péron, C. L. , Jurkowska, R. Z. , Carmouche, R. P. , Ibberson, D. , Barath, P. , Demay, F. , Reid, G. et al. (2008) Cyclical DNA methylation of a transcriptionally active promoter. Nature, 452, 45-50.
57. Wiench, M. , John, S. , Baek, S. , Johnson, T. A. , Sung, M.-H. , Escobar, T. , Simmons, C. A. , Pearce, K. H. , Biddie, S. C. , Sabo, P. J. et al. (2011) DNA methylation status predicts cell type-specific enhancer activity. EMBO J, 30, 3028-3039.
58. Zilberman, D. , Coleman-Derr, D. , Ballinger, T. and Henikoff, S. (2008) Histone H2A. Z and DNA methylation are mutually antagonistic chromatin marks. Nature, 456, 125-129.
59. Conerly, M. L. , Teves, S. S. , Diolaiti, D. , Ulrich, M. , Eisenman, R. N. and Henikoff, S. (2010) Changes in H2A. Z occupancy and DNA methylation during B-cell lymphomagenesis. Genome Res. , 20, 1383-1390.
60. Lister, R. , Pelizzola, M. , Dowen, R. H. , Hawkins, R. D. , Hon, G. , Tonti-Filippini, J. , Nery, J. R. , Lee, L. , Ye, Z. , Ngo, Q.-M. et al. (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature, 462, 315-322.
61. Stadler, M. B. , Murr, R. , Burger, L. , Ivanek, R. , Lienert, F. , Schöer, A. , van Nimwegen, E. , Wirbelauer, C. , Oakeley, E. J. , Gaidatzis, D. et al. (2011) DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature, 480, 490-495.
62. Varley, K. E. , Gertz, J. , Bowling, K. M. , Parker, S. L. , Reddy, T. E. , Pauli-Behn, F. , Cross, M. K. , Williams, B. A. , Stamatoyannopoulos, J. A. , Crawford, G. E. et al. (2013) Dynamic DNA methylation across diverse human cell lines and tissues. Genome Res. , 23, 555-567.
63. Lupien, M. , Meyer, C. A. , Bailey, S. T. , Eeckhoute, J. , Cook, J. , Westerling, T. , Zhang, X. , Carroll, J. S. , Rhodes, D. R. , Liu, X. S. et al. (2010) Growth factor stimulation induces a distinct ER(alpha) cistrome underlying breast cancer endocrine resistance. Genes Dev. , 24, 2219-2227.
64. McLean, C. Y. , Bristor, D. , Hiller, M. , Clarke, S. L. , Schaar, B. T. , Lowe, C. B. , Wenger, A. M. and Bejerano, G. (2010) GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. , 28, 495-501.
65. Kim, T.-K. , Hemberg, M. , Gray, J. M. , Costa, A. M. , Bear, D. M. , Wu, J. , Harmin, D. A. , Laptewicz, M. , Barbara-Haley, K. , Kuersten, S. et al. (2010) Widespread transcription at neuronal activity-regulated enhancers. Nature, 465, 182-187.
66. Santa, F. D. , Barozzi, I. , Mietton, F. , Ghisletti, S. , Polletti, S. , Tusi, B. K. , Muller, H. , Ragoussis, J. , Wei, C.-L. and Natoli, G. (2010) A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biol. , 8, e1000384.
67. Hah, N. , Danko, C. G. , Core, L. , Waterfall, J. J. , Siepel, A. , Lis, J. T. and Kraus, W. L. (2011) A rapid, extensive, and transient transcriptional response to estrogen signaling in breast cancer cells. Cell, 145, 622-634.
68. Mousavi, K. , Zare, H. , Dellorso, S. , Grontved, L. , Gutierrez-Cruz, G. , Derfoul, A. , Hager, G. L. and Sartorelli, V. (2013) eRNAs promote transcription by establishing chromatin accessibility at defined genomic loci. Mol. Cell, 51, 606-617.
69. Lai, F. , Orom, U. A. , Cesaroni, M. , Beringer, M. , Taatjes, D. J. , Blobel, G. A. and Shiekhattar, R. (2013) Activating RNAs associate with Mediator to enhance chromatin architecture and transcription. Nature, 494, 497-501.
70. Li, W. , Notani, D. , Ma, Q. , Tanasa, B. , Nunez, E. , Chen, A. Y. , Merkurjev, D. , Zhang, J. , Ohgi, K. , Song, X. et al. (2013) Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation. Nature, 498, 516-520.
71. Hah, N. , Murakami, S. , Nagari, A. , Danko, C. G. and Kraus, W. L. (2013) Enhancer transcripts mark active estrogen receptor binding sites. Genome Res. , 23, 1210-1223.
72. Core, L. J. , Waterfall, J. J. and Lis, J. T. (2008) Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science, 322, 1845-1848.
73. Kagey, M. H. , Newman, J. J. , Bilodeau, S. , Zhan, Y. , Orlando, D. A. , van Berkum, N. L. , Ebmeier, C. C. , Goossens, J. , Rahl, P. B. , Levine, S. S. et al. (2010) Mediator and cohesin connect gene expression and chromatin architecture. Nature, 467, 430-435.
74. Li, G. , Ruan, X. , Auerbach, R. K. , Sandhu, K. S. , Zheng, M. , Wang, P. , Poh, H. M. , Goh, Y. , Lim, J. , Zhang, J. et al. (2012) Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell, 148, 84-98.
75. Li, Z. , Gadue, P. , Chen, K. , Jiao, Y. , Tuteja, G. , Schug, J. , Li, W. and Kaestner, K. H. (2012) Foxa2 and H2A. Z mediate nucleosome depletion during embryonic stem cell differentiation. Cell, 151, 1608-1616.
76. Simon, M. , North, J. A. , Shimko, J. C. , Forties, R. A. , Ferdinand, M. B. , Manohar, M. , Zhang, M. , Fishel, R. , Ottesen, J. J. and Poirier, M. G. (2011) Histone fold modifications control nucleosome unwrapping and disassembly. Proc. Natl. Acad. Sci. U. S. A. , 108, 12711-12716.
77. Stenoien, D. L. , Patel, K. , Mancini, M. G. , Dutertre, M. , Smith, C. L. , OMalley, B. W. and Mancini, M. A. (2001) FRAP reveals that mobility of oestrogen receptor-alpha is ligand- and proteasome-dependent. Nat. Cell Biol. , 3, 15-23.
78. Kraushaar, D. C. , Jin, W. , Maunakea, A. , Abraham, B. , Ha, M. and Zhao, K. (2013) Genome-wide incorporation dynamics reveal distinct categories of turnover for the histone variant H3. 3. Genome Biol. , 14, R121.
79. Li, G. and Widom, J. (2004) Nucleosomes facilitate their own invasion. Nat. Struct. Mol. Biol. , 11, 763-769.
80. Li, G. , Levitus, M. , Bustamante, C. and Widom, J. (2005) Rapid spontaneous accessibility of nucleosomal DNA. Nat. Struct. Mol. Biol. , 12, 46-53.
81. Poirier, M. G. , Bussiek, M. , Langowski, J. and Widom, J. (2008) Spontaneous access to DNA target sites in folded chromatin fibers. J. Mol. Biol. , 379, 772-786.
82. Shimko, J. C. , North, J. A. , Bruns, A. N. , Poirier, M. G. and Ottesen, J. J. (2011) Preparation of fully synthetic histone H3 reveals that acetyl-lysine 56 facilitates protein binding within nucleosomes. J. Mol. Biol. , 408, 187-204.
83. Neumann, H. , Hancock, S. M. , Buning, R. , Routh, A. , Chapman, L. , Somers, J. , Owen-Hughes, T. , van Noort, J. , Rhodes, D. and Chin, J. W. (2009) A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation. Mol. Cell, 36, 153-163.
84. North, J. A. , Shimko, J. C. , Javaid, S. , Mooney, A. M. , Shoffner, M. A. , Rose, S. D. , Bundschuh, R. , Fishel, R. , Ottesen, J. J. and Poirier, M. G. (2012) Regulation of the nucleosome unwrapping rate controls DNA accessibility. Nucleic Acids Res. , 40, 10215-10227.
85. Watanabe, S. , Radman-Livaja, M. , Rando, O. J. and Peterson, C. L. (2013) A histone acetylation switch regulates H2A. Z deposition by the SWR-C remodeling enzyme. Science, 340, 195-199.
86. Henikoff, J. G. , Belsky, J. A. , Krassovsky, K. , MacAlpine, D. M. and Henikoff, S. (2011) Epigenome characterization at single base-pair resolution. Proc. Natl. Acad. Sci. U. S. A. , 108, 18318-18323.
87. Hua, S. , Kallen, C. B. , Dhar, R. , Baquero, M. T. , Mason, C. E. , Russell, B. A. , Shah, P. K. , Liu, J. , Khramtsov, A. , Tretiakova, M. S. et al. (2008) Genomic analysis of estrogen cascade reveals histone variant H2A. Z associated with breast cancer progression. Mol. Syst. Biol. , 4, 188.
88. Svotelis, A. , Gévry, N. , Grondin, G. and Gaudreau, L. (2010) H2A. Z overexpression promotes cellular proliferation of breast cancer cells. Cell Cycle, 9, 364-370.
89. Ruike, Y. , Imanaka, Y. , Sato, F. , Shimizu, K. and Tsujimoto, G. (2010) Genome-wide analysis of aberrant methylation in human breast cancer cells using methyl-DNA immunoprecipitation combined with high-throughput sequencing. BMC Genomics, 11, 137.
90. Hon, G. C. , Hawkins, R. D. , Caballero, O. L. , Lo, C. , Lister, R. , Pelizzola, M. , Valsesia, A. , Ye, Z. , Kuan, S. , Edsall, L. E. et al. (2012) Global DNA hypomethylation coupled to repressive chromatin domain formation and gene silencing in breast cancer. Genome Res. , 22, 246-258.
91. Aran, D. , Sabato, S. and Hellman, A. (2013) DNA methylation of distal regulatory sites characterizes dysregulation of cancer genes. Genome Biol. , 14, R21.
92. Edgar, R. , Domrachev, M. and Lash, A. E. (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. , 30, 207-210.