TIP48/Reptin and H2A.Z Requirement for Initiating Chromatin Remodeling in Estrogen-Activated Transcription

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Histone variants, including histone H2A.Z, are incorporated into specific genomic sites and participate in transcription regulation. The role of H2A.Z at these sites remains poorly characterized. Our study investigates changes in the chromatin environment at the Cyclin D1 gene (CCND1) during transcriptional initiation in response to estradiol in estrogen receptor positive mammary tumour cells. We show that H2A.Z is present at the transcription start-site and downstream enhancer sequences of CCND1 when the gene is poorly transcribed. Stimulation of CCND1 expression required release of H2A.Z concomitantly from both these DNA elements. The AAA+ family members TIP48/reptin and the histone variant H2A.Z are required to remodel the chromatin environment at CCND1 as a prerequisite for binding of the estrogen receptor (ERα) in the presence of hormone. TIP48 promotes acetylation and exchange of H2A.Z, which triggers a dissociation of the CCND1 3′ enhancer from the promoter, thereby releasing a repressive intragenic loop. This release then enables the estrogen receptor to bind to the CCND1 promoter. Our findings provide new insight into the priming of chromatin required for transcription factor access to their target sequence. Dynamic release of gene loops could be a rapid means to remodel chromatin and to stimulate transcription in response to hormones.

Vyšlo v časopise: TIP48/Reptin and H2A.Z Requirement for Initiating Chromatin Remodeling in Estrogen-Activated Transcription. PLoS Genet 9(4): e32767. doi:10.1371/journal.pgen.1003387
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003387

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Zdroje

1. BhaumikSR, SmithE, ShilatifardA (2007) Covalent modifications of histones during development and disease pathogenesis. Nat Struct Mol Biol 14: 1008–1016.

2. DalvaiM, BystrickyK (2010) The role of histone modifications and variants in regulating gene expression in breast cancer. J Mammary Gland Biol Neoplasia 15: 19–33.

3. HenikoffS, AhmadK (2005) Assembly of variant histones into chromatin. Annu Rev Cell Dev Biol 21: 133–153.

4. StrahlBD, AllisCD (2000) The language of covalent histone modifications. Nature 403: 41–45.

5. VinckeviciusA, ChakravartiD (2012) Chromatin immunoprecipitation: advancing analysis of nuclear hormone signaling. J Mol Endocrinol 49: R113–123.

6. McKennaNJ, LanzRB, O'MalleyBW (1999) Nuclear receptor coregulators: cellular and molecular biology. Endocr Rev 20: 321–344.

7. EeckhouteJ, CarrollJS, GeistlingerTR, Torres-ArzayusMI, BrownM (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.

8. MetivierR, PenotG, HubnerMR, 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. MetivierR, StarkA, FlouriotG, HubnerMR, BrandH, et al. (2002) A dynamic structural model for estrogen receptor-alpha activation by ligands, emphasizing the role of interactions between distant A and E domains. Mol Cell 10: 1019–1032.

10. ShangY, HuX, DiRenzoJ, LazarMA, BrownM (2000) Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103: 843–852.

11. GuillemetteB, BatailleAR, GevryN, AdamM, BlanchetteM, et al. (2005) Variant histone H2A.Z is globally localized to the promoters of inactive yeast genes and regulates nucleosome positioning. PLoS Biol 3: e384.

12. LiB, PattendenSG, LeeD, GutierrezJ, ChenJ, et al. (2005) Preferential occupancy of histone variant H2AZ at inactive promoters influences local histone modifications and chromatin remodeling. Proc Natl Acad Sci U S A 102: 18385–18390.

13. Valdes-MoraF, SongJZ, StathamAL, StrbenacD, RobinsonMD, et al. (2011) Acetylation of H2A.Z is a key epigenetic modification associated with gene deregulation and epigenetic remodeling in cancer. Genome Res 22: 307–321.

14. ZhangH, RobertsDN, CairnsBR (2005) Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell 123: 219–231.

15. JohnS, SaboPJ, JohnsonTA, SungMH, BiddieSC, et al. (2008) Interaction of the glucocorticoid receptor with the chromatin landscape. Mol Cell 29: 611–624.

16. FarrisSD, RubioED, MoonJJ, GombertWM, NelsonBH, et al. (2005) Transcription-induced chromatin remodeling at the c-myc gene involves the local exchange of histone H2A.Z. J Biol Chem 280: 25298–25303.

17. MorrisonAJ, ShenX (2009) Chromatin remodelling beyond transcription: the INO80 and SWR1 complexes. Nat Rev Mol Cell Biol 10: 373–384.

18. ZhangH, RichardsonDO, RobertsDN, UtleyR, Erdjument-BromageH, et al. (2004) The Yaf9 component of the SWR1 and NuA4 complexes is required for proper gene expression, histone H4 acetylation, and Htz1 replacement near telomeres. Mol Cell Biol 24: 9424–9436.

19. BillonP, CoteJ (2012) Precise deposition of histone H2A.Z in chromatin for genome expression and maintenance. Biochim Biophys Acta 1819: 290–302.

20. CaiY, JinJ, FlorensL, SwansonSK, KuschT, et al. (2005) The mammalian YL1 protein is a shared subunit of the TRRAP/TIP60 histone acetyltransferase and SRCAP complexes. J Biol Chem 280: 13665–13670.

21. IkuraT, OgryzkoVV, GrigorievM, GroismanR, WangJ, et al. (2000) Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 102: 463–473.

22. KuschT, FlorensL, MacdonaldWH, SwansonSK, GlaserRL, et al. (2004) Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 306: 2084–2087.

23. GevryN, ChanHM, LaflammeL, LivingstonDM, GaudreauL (2007) p21 transcription is regulated by differential localization of histone H2A.Z. Genes Dev 21: 1869–1881.

24. GevryN, HardyS, JacquesPE, LaflammeL, SvotelisA, et al. (2009) Histone H2A.Z is essential for estrogen receptor signaling. Genes Dev

25. ChoiJ, HeoK, AnW (2009) Cooperative action of TIP48 and TIP49 in H2A.Z exchange catalyzed by acetylation of nucleosomal H2A. Nucleic Acids Res 37: 5993–6007.

26. JhaS, ShibataE, DuttaA (2008) Human Rvb1/Tip49 is required for the histone acetyltransferase activity of Tip60/NuA4 and for the downregulation of phosphorylation on H2AX after DNA damage. Mol Cell Biol 28: 2690–2700.

27. ArnoldA, PapanikolaouA (2005) Cyclin D1 in breast cancer pathogenesis. J Clin Oncol 23: 4215–4224.

28. LehnS, TobinNP, BerglundP, NilssonK, SimsAH, et al. (2010) Down-regulation of the oncogene cyclin D1 increases migratory capacity in breast cancer and is linked to unfavorable prognostic features. Am J Pathol 177: 2886–2897.

29. TobinNP, SimsAH, LundgrenKL, LehnS, LandbergG (2011) Cyclin D1, Id1 and EMT in breast cancer. BMC Cancer 11: 417.

30. DalvaiM, BystrickyK (2010) Cell cycle and anti-estrogen effects synergize to regulate cell proliferation and ER target gene expression. PLoS One 5: e11011.

31. SutherlandRL, PrallOW, WattsCK, MusgroveEA (1998) Estrogen and progestin regulation of cell cycle progression. J Mammary Gland Biol Neoplasia 3: 63–72.

32. SerandourAA, AvnerS, PercevaultF, DemayF, BizotM, et al. (2011) Epigenetic switch involved in activation of pioneer factor FOXA1-dependent enhancers. Genome Res 21: 555–565.

33. GrigolettoA, LestienneP, RosenbaumJ (2011) The multifaceted proteins Reptin and Pontin as major players in cancer. Biochim Biophys Acta 1815: 147–157.

34. JeongKW, KimK, SituAJ, UlmerTS, AnW, et al. (2011) Recognition of enhancer element-specific histone methylation by TIP60 in transcriptional activation. Nat Struct Mol Biol 18: 1358–1365.

35. SvotelisA, GevryN, GaudreauL (2009) Regulation of gene expression and cellular proliferation by histone H2A.Z. Biochem Cell Biol 87: 179–188.

36. KimuraA, HorikoshiM (1998) Tip60 acetylates six lysines of a specific class in core histones in vitro. Genes Cells 3: 789–800.

37. MillarCB, XuF, ZhangK, GrunsteinM (2006) Acetylation of H2AZ Lys 14 is associated with genome-wide gene activity in yeast. Genes Dev 20: 711–722.

38. FullwoodMJ, LiuMH, PanYF, LiuJ, XuH, et al. (2009) An oestrogen-receptor-alpha-bound human chromatin interactome. Nature 462: 58–64.

39. Tan-WongSM, FrenchJD, ProudfootNJ, BrownMA (2008) Dynamic interactions between the promoter and terminator regions of the mammalian BRCA1 gene. Proc Natl Acad Sci U S A 105: 5160–5165.

40. DalvaiM, BellucciL, FleuryL, LavigneAC, MoutahirF, et al. (2012) H2A.Z-dependent crosstalk between enhancer and promoter regulates Cyclin D1 expression. Oncogene

41. DekkerJ (2006) The three 'C' s of chromosome conformation capture: controls, controls, controls. Nat Methods 3: 17–21.

42. HagegeH, KlousP, BraemC, SplinterE, DekkerJ, et al. (2007) Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat Protoc 2: 1722–1733.

43. MatteraL, EscaffitF, PillaireMJ, SelvesJ, TytecaS, et al. (2009) The p400/Tip60 ratio is critical for colorectal cancer cell proliferation through DNA damage response pathways. Oncogene 28: 1506–1517.

44. BallareC, CastellanoG, GavegliaL, AlthammerS, Gonzalez-VallinasJ, et al. (2013) Nucleosome-driven transcription factor binding and gene regulation. Mol Cell 49: 67–79.

45. KocanovaS, KerrEA, RafiqueS, BoyleS, KatzE, et al. (2010) Activation of estrogen-responsive genes does not require their nuclear co-localization. PLoS Genet 6: e1000922.

46. IacovoniJS, CaronP, LassadiI, NicolasE, MassipL, et al. (2010) High-resolution profiling of gammaH2AX around DNA double strand breaks in the mammalian genome. EMBO J 29: 1446–1457.

47. LegubeG, LinaresLK, TytecaS, CaronC, ScheffnerM, et al. (2004) Role of the histone acetyl transferase Tip60 in the p53 pathway. J Biol Chem 279: 44825–44833.

48. LiG, ThomasAM, HartSN, ZhongX, WuD, et al. (2010) Farnesoid X receptor activation mediates head-to-tail chromatin looping in the Nr0b2 gene encoding small heterodimer partner. Mol Endocrinol 24: 1404–1412.

49. SplinterE, GrosveldF, de LaatW (2004) 3C technology: analyzing the spatial organization of genomic loci in vivo. Methods Enzymol 375: 493–507.

50. DeschenesJ, BourdeauV, WhiteJH, MaderS (2007) Regulation of GREB1 transcription by estrogen receptor alpha through a multipartite enhancer spread over 20 kb of upstream flanking sequences. J Biol Chem 282: 17335–17339.