Targeted H3R26 Deimination Specifically Facilitates Estrogen Receptor Binding by Modifying Nucleosome Structure

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Transcription factors bind to DNA to activate and repress gene transcription. Many transcription factors, particularly nuclear receptors, associate with their cognate DNA element in a highly dynamic manner in vivo. Highly acetylated histone tails and DNase sensitive chromatin are amenable to the initial binding of transcription factors. Upon binding to DNA, transcription factor binding recruits remodelers and coactivators that can cause a concomitant increase in accessibility and acetylation. Herein, we show that estrogen receptor recruitment of a histone deiminase causes the positively charged H3R26 residue to be neutralized. This modification changes the fine structure of the nucleosome particle and facilitates estrogen receptor binding. Lastly, we find that high deiminase expression is associated with increased survival in estrogen receptor-positive breast cancer patients.

Vyšlo v časopise: Targeted H3R26 Deimination Specifically Facilitates Estrogen Receptor Binding by Modifying Nucleosome Structure. PLoS Genet 10(9): e32767. doi:10.1371/journal.pgen.1004613
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004613

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Zdroje

1. LugerK, MäderAW, RichmondRK, SargentDF, RichmondTJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251–260 doi:10.1038/38444

2. GuertinMJ, LisJT (2013) Mechanisms by which transcription factors gain access to target sequence elements in chromatin. Current Opinion in Genetics & Development 23: 116–123 doi:10.1016/j.gde.2012.11.008

3. HeHH, MeyerCA, ChenMW, JordanVC, BrownM, et al. (2012) Differential DNase I hypersensitivity reveals factor-dependent chromatin dynamics. Genome Res 22: 1015–1025 doi:10.1101/gr.133280.111

4. JohnS, SaboPJ, ThurmanRE, SungM-H, BiddieSC, et al. (2011) Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nat Genet 43: 264–268 doi:10.1038/ng.759

5. VossTC, SchiltzRL, SungM-H, YenPM, StamatoyannopoulosJA, et al. (2011) Dynamic Exchange at Regulatory Elements during Chromatin Remodeling Underlies Assisted Loading Mechanism. Cell 146: 544–554 doi:10.1016/j.cell.2011.07.006

6. BallaréC, CastellanoG, GavegliaL, AlthammerS, González-VallinasJ, et al. (2013) Nucleosome-driven transcription factor binding and gene regulation. Mol Cell 49: 67–79 doi:10.1016/j.molcel.2012.10.019

7. GiamarchiC, SolanasM, ChailleuxC, AugereauP, VignonF, et al. (1999) Chromatin structure of the regulatory regions of pS2 and cathepsin D genes in hormone-dependent and -independent breast cancer cell lines. Oncogene 18: 533–541 doi:10.1038/sj.onc.1202317

8. MétivierR, PenotG, HübnerMR, ReidG, BrandH, et al. (2003) Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 115: 751–763.

9. HahN, KolkmanA, RuhlDD, PijnappelWWMP, HeckAJR, et al. (2010) A role for BAF57 in cell cycle-dependent transcriptional regulation by the SWI/SNF chromatin remodeling complex. Cancer Res 70: 4402–4411 doi:10.1158/0008-5472.CAN-09-2767

10. CuthbertGL, DaujatS, SnowdenAW, Erdjument-BromageH, HagiwaraT, et al. (2004) Histone deimination antagonizes arginine methylation. Cell 118: 545–553 doi:10.1016/j.cell.2004.08.020

11. WangY, WysockaJ, SayeghJ, LeeY-H, PerlinJR, et al. (2004) Human PAD4 regulates histone arginine methylation levels via demethylimination. Science 306: 279–283 doi:10.1126/science.1101400

12. ZhangX, BoltM, GuertinMJ, ChenW, ZhangS, et al. (2012) Peptidylarginine deiminase 2-catalyzed histone H3 arginine 26 citrullination facilitates estrogen receptor α target gene activation. Proc Natl Acad Sci 109: 13331–6.

13. CherringtonBD, ZhangX, McElweeJL, MorencyE, AnguishLJ, et al. (2012) Potential role for PAD2 in gene regulation in breast cancer cells. PLoS ONE 7: e41242 doi:10.1371/journal.pone.0041242

14. WelborenW-J, van DrielMA, Janssen-MegensEM, van HeeringenSJ, SweepFC, et al. (2009) ChIP-Seq of ERalpha and RNA polymerase II defines genes differentially responding to ligands. EMBO J 28: 1418–1428 doi:10.1038/emboj.2009.88

15. Ross-InnesCS, StarkR, HolmesKA, SchmidtD, SpyrouC, et al. (2010) Cooperative interaction between retinoic acid receptor-alpha and estrogen receptor in breast cancer. Genes Dev 24: 171–182 doi:10.1101/gad.552910

16. ENCODE Project Consortium (2012) BernsteinBE, BirneyE, DunhamI, GreenED, et al. (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57–74 doi:10.1038/nature11247

17. NephS, VierstraJ, StergachisAB, ReynoldsAP, HaugenE, et al. (2012) An expansive human regulatory lexicon encoded in transcription factor footprints. Nature 489: 83–90 doi:10.1038/nature11212

18. GentlemanR, CareyV, HuberW, HahneF (2011) Bioconductor - genefilter. R package version

19. AndersS, HuberW (2010) Differential expression analysis for sequence count data. Genome Biology 11: R106 doi:10.1186/gb-2010-11-10-r106

20. GrøntvedL, JohnS, BaekS, LiuY, BuckleyJR, et al. (2013) C/EBP maintains chromatin accessibility in liver and facilitates glucocorticoid receptor recruitment to steroid response elements. EMBO J 32: 1568–1583 doi:10.1038/emboj.2013.106

21. GertzJ, SavicD, VarleyKE, PartridgeEC, SafiA, et al. (2013) Distinct properties of cell-type-specific and shared transcription factor binding sites. Mol Cell 52: 25–36 doi:10.1016/j.molcel.2013.08.037

22. LeeDY, HayesJJ, PrussD, WolffeAP (1993) A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell 72: 73–84.

23. TseC, SeraT, WolffeAP, HansenJC (1998) Disruption of higher-order folding by core histone acetylation dramatically enhances transcription of nucleosomal arrays by RNA polymerase III. Molecular and cellular biology 18: 4629–4638.

24. HenikoffJG, BelskyJA, KrassovskyK, MacAlpineDM, HenikoffS (2011) Epigenome characterization at single base-pair resolution. Proc Natl Acad Sci 108: 18318–18323 doi:10.1073/pnas.1110731108

25. Cancer Genome Atlas Network (2012) Comprehensive molecular portraits of human breast tumours. Nature 490: 61–70 doi:10.1038/nature11412

26. ClineMS, CraftB, SwatloskiT, GoldmanM, MaS, et al. (2013) Exploring TCGA Pan-Cancer data at the UCSC Cancer Genomics Browser. Sci Rep 3: 2652 doi:10.1038/srep02652

27. GyörffyB, LanczkyA, EklundAC, DenkertC, BudcziesJ, et al. (2010) An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res Treat 123: 725–731 doi:10.1007/s10549-009-0674-9

28. GaoJ, AksoyBA, DogrusozU, DresdnerG, GrossB, et al. (2013) Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 6: pl1 doi:10.1126/scisignal.2004088

29. FerreiraH, SomersJ, WebsterR, FlausA, Owen-HughesT (2007) Histone tails and the H3 alphaN helix regulate nucleosome mobility and stability. Molecular and cellular biology 27: 4037–4048 doi:10.1128/MCB.02229-06

30. WangX, HayesJJ (2008) Acetylation mimics within individual core histone tail domains indicate distinct roles in regulating the stability of higher-order chromatin structure. Mol Cell Biol 28: 227–236 doi:10.1128/MCB.01245-07

31. ChristophorouMA, Castelo-BrancoG, Halley-StottRP, OliveiraCS, LoosR, et al. (2014) Citrullination regulates pluripotency and histone H1 binding to chromatin. Nature 507: 104–108 doi:10.1038/nature12942

32. WangY, LiM, StadlerS, CorrellS, LiP, et al. (2009) Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol 184: 205–213 doi:10.1083/jcb.200806072

33. GuertinMJ, LisJT (2010) Chromatin landscape dictates HSF binding to target DNA elements. PLoS Genet 6: e1001114 doi:10.1371/journal.pgen.1001114

34. GuertinMJ, MartinsAL, SiepelA, LisJT (2012) Accurate prediction of inducible transcription factor binding intensities in vivo. PLoS Genet 8: e1002610 doi:10.1371/journal.pgen.1002610

35. LangmeadB, TrapnellC, PopM, SalzbergSL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology 10: R25 doi:10.1186/gb-2009-10-3-r25

36. ZhangY, LiuT, MeyerCA, EeckhouteJ, JohnsonDS, et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biology 9: R137 doi:10.1186/gb-2008-9-9-r137

37. BaileyTL, BodenM, BuskeFA, FrithM, GrantCE, et al. (2009) MEME Suite: tools for motif discovery and searching. Nucleic Acids Res 37: W202–W208 doi:10.1093/nar/gkp335

38. GuertinMJ, ZhangX, CoonrodSA, HagerGL (2014) Transient ER binding and p300 redistribution support a squelching mechanism for E2-repressed genes. Molecular Endocrinology doi:10.1210/me.2014-1130