Differential DNase I Hypersensitivity Reveals Factor-dependent Chromatin Dynamics

Overview

Journal Genome Res

Specialty Genetics

Date 2012 Apr 18

PMID 22508765

Citations 117

Authors

Housheng Hansen He

Clifford A Meyer

Mei Wei Chen

V Craig Jordan

Myles Brown

X Shirley Liu

Affiliations

Soon will be listed here.

Abstract

Transcription factor cistromes are highly cell-type specific. Chromatin accessibility, histone modifications, and nucleosome occupancy have all been found to play a role in defining these binding locations. Here, we show that hormone-induced DNase I hypersensitivity changes (ΔDHS) are highly predictive of androgen receptor (AR) and estrogen receptor 1 (ESR1) binding in prostate cancer and breast cancer cells, respectively. While chromatin structure prior to receptor binding and nucleosome occupancy after binding are strikingly different for ESR1 and AR, ΔDHS is highly predictive for both. AR binding is associated with changes in both local nucleosome occupancy and DNase I hypersensitivity. In contrast, while global ESR1 binding is unrelated to changes in nucleosome occupancy, DNase I hypersensitivity dynamics are also predictive of the ESR1 cistrome. These findings suggest that AR and ESR1 have distinct modes of interaction with chromatin and that DNase I hypersensitivity dynamics provides a general approach for predicting cell-type specific cistromes.

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References

Verzi M, Shin H, He H, Sulahian R, Meyer C, Montgomery R . Differentiation-specific histone modifications reveal dynamic chromatin interactions and partners for the intestinal transcription factor CDX2. Dev Cell. 2010; 19(5):713-26. PMC: 3001591. DOI: 10.1016/j.devcel.2010.10.006. View

Joseph R, Orlov Y, Huss M, Sun W, Kong S, Ukil L . Integrative model of genomic factors for determining binding site selection by estrogen receptor-α. Mol Syst Biol. 2010; 6:456. PMC: 3018168. DOI: 10.1038/msb.2010.109. View

Irizarry R, Hobbs B, Collin F, Beazer-Barclay Y, Antonellis K, Scherf U . Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003; 4(2):249-64. DOI: 10.1093/biostatistics/4.2.249. View

Lanz R, Bulynko Y, Malovannaya A, Labhart P, Wang L, Li W . Global characterization of transcriptional impact of the SRC-3 coregulator. Mol Endocrinol. 2010; 24(4):859-72. PMC: 2852354. DOI: 10.1210/me.2009-0499. View

Siersbaek R, Nielsen R, John S, Sung M, Baek S, Loft A . Extensive chromatin remodelling and establishment of transcription factor 'hotspots' during early adipogenesis. EMBO J. 2011; 30(8):1459-72. PMC: 3102274. DOI: 10.1038/emboj.2011.65. View

Song L, Zhang Z, Grasfeder L, Boyle A, Giresi P, Lee B . Open chromatin defined by DNaseI and FAIRE identifies regulatory elements that shape cell-type identity. Genome Res. 2011; 21(10):1757-67. PMC: 3202292. DOI: 10.1101/gr.121541.111. View

Zhang Z, Wippo C, Wal M, Ward E, Korber P, Pugh B . A packing mechanism for nucleosome organization reconstituted across a eukaryotic genome. Science. 2011; 332(6032):977-80. PMC: 4852979. DOI: 10.1126/science.1200508. View

Dai Y, Ngo D, Jacob J, Forman L, Faller D . Prohibitin and the SWI/SNF ATPase subunit BRG1 are required for effective androgen antagonist-mediated transcriptional repression of androgen receptor-regulated genes. Carcinogenesis. 2008; 29(9):1725-33. PMC: 2722849. DOI: 10.1093/carcin/bgn117. View

DiRenzo J, Shang Y, Phelan M, Sif S, Myers M, Kingston R . BRG-1 is recruited to estrogen-responsive promoters and cooperates with factors involved in histone acetylation. Mol Cell Biol. 2000; 20(20):7541-9. PMC: 86306. DOI: 10.1128/MCB.20.20.7541-7549.2000. View

10.

Smyth G, Speed T . Normalization of cDNA microarray data. Methods. 2003; 31(4):265-73. DOI: 10.1016/s1046-2023(03)00155-5. View

11.

Wang Q, Li W, Zhang Y, Yuan X, Xu K, Yu J . Androgen receptor regulates a distinct transcription program in androgen-independent prostate cancer. Cell. 2009; 138(2):245-56. PMC: 2726827. DOI: 10.1016/j.cell.2009.04.056. View

12.

John S, Sabo P, Thurman R, Sung M, Biddie S, Johnson T . Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nat Genet. 2011; 43(3):264-8. PMC: 6386452. DOI: 10.1038/ng.759. View

13.

Jin C, Zang C, Wei G, Cui K, Peng W, Zhao K . H3.3/H2A.Z double variant-containing nucleosomes mark 'nucleosome-free regions' of active promoters and other regulatory regions. Nat Genet. 2009; 41(8):941-5. PMC: 3125718. DOI: 10.1038/ng.409. View

14.

Zhang Y, Shin H, Song J, Lei Y, Liu X . Identifying positioned nucleosomes with epigenetic marks in human from ChIP-Seq. BMC Genomics. 2008; 9:537. PMC: 2596141. DOI: 10.1186/1471-2164-9-537. View

15.

Lupien M, Eeckhoute J, Meyer C, Wang Q, Zhang Y, Li W . FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell. 2008; 132(6):958-70. PMC: 2323438. DOI: 10.1016/j.cell.2008.01.018. View

16.

Meyer M, Gronemeyer H, TURCOTTE B, Bocquel M, Tasset D, Chambon P . Steroid hormone receptors compete for factors that mediate their enhancer function. Cell. 1989; 57(3):433-42. DOI: 10.1016/0092-8674(89)90918-5. View

17.

Wang Q, Carroll J, Brown M . Spatial and temporal recruitment of androgen receptor and its coactivators involves chromosomal looping and polymerase tracking. Mol Cell. 2005; 19(5):631-42. DOI: 10.1016/j.molcel.2005.07.018. View

18.

Wu C . The 5' ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I. Nature. 1980; 286(5776):854-60. DOI: 10.1038/286854a0. View

19.

Dai M, Wang P, Boyd A, Kostov G, Athey B, Jones E . Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res. 2005; 33(20):e175. PMC: 1283542. DOI: 10.1093/nar/gni179. View

20.

Meyer C, He H, Brown M, Liu X . BINOCh: binding inference from nucleosome occupancy changes. Bioinformatics. 2011; 27(13):1867-8. PMC: 3117357. DOI: 10.1093/bioinformatics/btr279. View