The Chromatin Remodeler CHD8 Is Required for Activation of Progesterone Receptor-Dependent Enhancers


A lot of research has been devoted during the last decades to understand the mechanisms that control gene promoters activity, however, much less is known about enhancers. Only recently, the use of genome-wide chromatin immunoprecipitation techniques has revealed the existence of more than 400,000 enhancers in the human genome. We are starting to understand the importance of these regulatory elements and how they are activated or repressed. In this work we discover that the chromatin remodeler CHD8 is recruited to Progesteron Receptor-dependent enhancers upon hormone treatment. CHD8 is required for late steps in the activation of these enhancers, including transcription of the enhancers and synthesis of eRNA (long noncoding RNAs derived form the enhancers).


Vyšlo v časopise: The Chromatin Remodeler CHD8 Is Required for Activation of Progesterone Receptor-Dependent Enhancers. PLoS Genet 11(4): e32767. doi:10.1371/journal.pgen.1005174
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pgen.1005174

Souhrn

A lot of research has been devoted during the last decades to understand the mechanisms that control gene promoters activity, however, much less is known about enhancers. Only recently, the use of genome-wide chromatin immunoprecipitation techniques has revealed the existence of more than 400,000 enhancers in the human genome. We are starting to understand the importance of these regulatory elements and how they are activated or repressed. In this work we discover that the chromatin remodeler CHD8 is recruited to Progesteron Receptor-dependent enhancers upon hormone treatment. CHD8 is required for late steps in the activation of these enhancers, including transcription of the enhancers and synthesis of eRNA (long noncoding RNAs derived form the enhancers).


Zdroje

1. Lenhard B, Sandelin A, Carninci P (2012) Metazoan promoters: emerging characteristics and insights into transcriptional regulation. Nat Rev Genet 13: 233–245. doi: 10.1038/nrg3163 22392219

2. Calo E, Wysocka J (2013) Modification of enhancer chromatin: what, how, and why? Mol Cell 49: 825–837. doi: 10.1016/j.molcel.2013.01.038 23473601

3. Maston GA, Landt SG, Snyder M, Green MR (2012) Characterization of enhancer function from genome-wide analyses. Annu Rev Genomics Hum Genet 13: 29–57. doi: 10.1146/annurev-genom-090711-163723 22703170

4. Voss TC, Hager GL (2014) Dynamic regulation of transcriptional states by chromatin and transcription factors. Nat Rev Genet 15: 69–81. doi: 10.1038/nrg3623 24342920

5. Maston GA, Evans SK, Green MR (2006) Transcriptional regulatory elements in the human genome. Annu Rev Genomics Hum Genet 7: 29–59. 16719718

6. Hargreaves DC, Crabtree GR (2011) ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res 21: 396–420. doi: 10.1038/cr.2011.32 21358755

7. Narlikar GJ, Sundaramoorthy R, Owen-Hughes T (2013) Mechanisms and Functions of ATP-Dependent Chromatin-Remodeling Enzymes. Cell 154: 490–503. doi: 10.1016/j.cell.2013.07.011 23911317

8. Marfella CG, Imbalzano AN (2007) The Chd family of chromatin remodelers. Mutat Res 618: 30–40. 17350655

9. Thompson BA, Tremblay V, Lin G, Bochar DA (2008) CHD8 is an ATP-dependent chromatin remodeling factor that regulates beta-catenin target genes. Mol Cell Biol 28: 3894–3904. doi: 10.1128/MCB.00322-08 18378692

10. Nishiyama M, Nakayama K, Tsunematsu R, Tsukiyama T, Kikuchi A, et al. (2004) Early embryonic death in mice lacking the beta-catenin-binding protein Duplin. Mol Cell Biol 24: 8386–8394. 15367660

11. Ishihara K, Oshimura M, Nakao M (2006) CTCF-dependent chromatin insulator is linked to epigenetic remodeling. Mol Cell 23: 733–742. 16949368

12. Sakamoto I, Kishida S, Fukui A, Kishida M, Yamamoto H, et al. (2000) A novel beta-catenin-binding protein inhibits beta-catenin-dependent Tcf activation and axis formation. J Biol Chem 275: 32871–32878. 10921920

13. Nishiyama M, Oshikawa K, Tsukada Y, Nakagawa T, Iemura S, et al. (2009) CHD8 suppresses p53-mediated apoptosis through histone H1 recruitment during early embryogenesis. Nat Cell Biol 11: 172–182. doi: 10.1038/ncb1831 19151705

14. Nishiyama M, Skoultchi AI, Nakayama KI (2012) Histone H1 recruitment by CHD8 is essential for suppression of the Wnt-beta-catenin signaling pathway. Mol Cell Biol 32: 501–512. doi: 10.1128/MCB.06409-11 22083958

15. Fang M, Ou J, Hutchinson L, Green MR (2014) The BRAF oncoprotein functions through the transcriptional repressor MAFG to mediate the CpG Island Methylator phenotype. Mol Cell 55: 904–915. doi: 10.1016/j.molcel.2014.08.010 25219500

16. Rodriguez-Paredes M, Ceballos-Chavez M, Esteller M, Garcia-Dominguez M, Reyes JC (2009) The chromatin remodeling factor CHD8 interacts with elongating RNA polymerase II and controls expression of the cyclin E2 gene. Nucleic Acids Res 37: 2449–2460. doi: 10.1093/nar/gkp101 19255092

17. Subtil-Rodriguez A, Vazquez-Chavez E, Ceballos-Chavez M, Rodriguez-Paredes M, Martin-Subero JI, et al. (2014) The chromatin remodeller CHD8 is required for E2F-dependent transcription activation of S-phase genes. Nucleic Acids Res 42: 2185–2196. doi: 10.1093/nar/gkt1161 24265227

18. Caldon CE, Sergio CM, Schutte J, Boersma MN, Sutherland RL, et al. (2009) Estrogen regulation of cyclin E2 requires cyclin D1 but not c-Myc. Mol Cell Biol 29: 4623–4639. doi: 10.1128/MCB.00269-09 19564413

19. Menon T, Yates JA, Bochar DA (2010) Regulation of androgen-responsive transcription by the chromatin remodeling factor CHD8. Mol Endocrinol 24: 1165–1174. doi: 10.1210/me.2009-0421 20308527

20. Beato M, Vicent GP (2012) Impact of chromatin structure and dynamics on PR signaling. The initial steps in hormonal gene regulation. Mol Cell Endocrinol 357: 37–42. doi: 10.1016/j.mce.2011.09.004 21945605

21. Vicent GP, Nacht AS, Font-Mateu J, Castellano G, Gaveglia L, et al. (2011) Four enzymes cooperate to displace histone H1 during the first minute of hormonal gene activation. Genes Dev 25: 845–862. doi: 10.1101/gad.621811 21447625

22. Vicent GP, Zaurin R, Nacht AS, Li A, Font-Mateu J, et al. (2009) Two chromatin remodeling activities cooperate during activation of hormone responsive promoters. PLoS Genet 5: e1000567. doi: 10.1371/journal.pgen.1000567 19609353

23. Vicent GP, Ballare C, Nacht AS, Clausell J, Subtil-Rodriguez A, et al. (2006) Induction of progesterone target genes requires activation of Erk and Msk kinases and phosphorylation of histone H3. Mol Cell 24: 367–381. 17081988

24. Pedram A, Razandi M, Sainson RC, Kim JK, Hughes CC, et al. (2007) A conserved mechanism for steroid receptor translocation to the plasma membrane. J Biol Chem 282: 22278–22288. 17535799

25. Ballaré C, Castellano G, Gaveglia L, Althammer S, Gonzalez-Vallinas J, et al. (2013) Nucleosome-driven transcription factor binding and gene regulation. Mol Cell 49: 67–79. doi: 10.1016/j.molcel.2012.10.019 23177737

26. Yin P, Roqueiro D, Huang L, Owen JK, Xie A, et al. (2012) Genome-wide progesterone receptor binding: cell type-specific and shared mechanisms in T47D breast cancer cells and primary leiomyoma cells. PLoS One 7: e29021. doi: 10.1371/journal.pone.0029021 22272226

27. Clarke CL, Graham JD (2012) Non-overlapping progesterone receptor cistromes contribute to cell-specific transcriptional outcomes. PLoS One 7: e35859. doi: 10.1371/journal.pone.0035859 22545144

28. Truss M, Bartsch J, Schelbert A, Hache RJ, Beato M (1995) Hormone induces binding of receptors and transcription factors to a rearranged nucleosome on the MMTV promoter in vivo. Embo J 14: 1737–1751. 7737125

29. Visel A, Blow MJ, Li Z, Zhang T, Akiyama JA, et al. (2009) ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457: 854–858. doi: 10.1038/nature07730 19212405

30. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, et al. (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459: 108–112. doi: 10.1038/nature07829 19295514

31. Cuddapah S, Jothi R, Schones DE, Roh TY, Cui K, et al. (2009) Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains. Genome Res 19: 24–32. doi: 10.1101/gr.082800.108 19056695

32. Sartorius CA, Groshong SD, Miller LA, Powell RL, Tung L, et al. (1994) New T47D breast cancer cell lines for the independent study of progesterone B- and A-receptors: only antiprogestin-occupied B-receptors are switched to transcriptional agonists by cAMP. Cancer Res 54: 3868–3877. 8033109

33. Zaret KS, Carroll JS (2011) Pioneer transcription factors: establishing competence for gene expression. Genes Dev 25: 2227–2241. doi: 10.1101/gad.176826.111 22056668

34. Lupien M, Eeckhoute J, Meyer CA, Wang Q, Zhang Y, et al. (2008) FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 132: 958–970. doi: 10.1016/j.cell.2008.01.018 18358809

35. Hurtado A, Holmes KA, Ross-Innes CS, Schmidt D, Carroll JS (2011) FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat Genet 43: 27–33. doi: 10.1038/ng.730 21151129

36. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, et al. (2010) Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci U S A 107: 21931–21936. doi: 10.1073/pnas.1016071107 21106759

37. Rada-Iglesias A, Bajpai R, Prescott S, Brugmann SA, Swigut T, et al. (2012) Epigenomic annotation of enhancers predicts transcriptional regulators of human neural crest. Cell Stem Cell 11: 633–648. doi: 10.1016/j.stem.2012.07.006 22981823

38. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, et al. (2011) A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470: 279–283. doi: 10.1038/nature09692 21160473

39. Tie F, Banerjee R, Stratton CA, Prasad-Sinha J, Stepanik V, et al. (2009) CBP-mediated acetylation of histone H3 lysine 27 antagonizes Drosophila Polycomb silencing. Development 136: 3131–3141. doi: 10.1242/dev.037127 19700617

40. Di Stefano B, Sardina JL, van Oevelen C, Collombet S, Kallin EM, et al. (2014) C/EBPalpha poises B cells for rapid reprogramming into induced pluripotent stem cells. Nature 506: 235–239. doi: 10.1038/nature12885 24336202

41. De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S, et al. (2010) A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biol 8: e1000384. doi: 10.1371/journal.pbio.1000384 20485488

42. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, et al. (2012) Landscape of transcription in human cells. Nature 489: 101–108. doi: 10.1038/nature11233 22955620

43. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM, et al. (2010) Widespread transcription at neuronal activity-regulated enhancers. Nature 465: 182–187. doi: 10.1038/nature09033 20393465

44. Wang D, Garcia-Bassets I, Benner C, Li W, Su X, et al. (2011) Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA. Nature 474: 390–394. doi: 10.1038/nature10006 21572438

45. Hah N, Murakami S, Nagari A, Danko CG, Kraus WL (2013) Enhancer transcripts mark active estrogen receptor binding sites. Genome Res 23: 1210–1223. doi: 10.1101/gr.152306.112 23636943

46. Yuan CC, Zhao X, Florens L, Swanson SK, Washburn MP, et al. (2007) CHD8 associates with human Staf and contributes to efficient U6 RNA polymerase III transcription. Mol Cell Biol 27: 8729–8738. 17938208

47. Sugathan A, Biagioli M, Golzio C, Erdin S, Blumenthal I, et al. (2014) CHD8 regulates neurodevelopmental pathways associated with autism spectrum disorder in neural progenitors. Proc Natl Acad Sci U S A 111: E4468–4477. doi: 10.1073/pnas.1405266111 25294932

48. Batsukh T, Pieper L, Koszucka AM, von Velsen N, Hoyer-Fender S, et al. (2010) CHD8 interacts with CHD7, a protein which is mutated in CHARGE syndrome. Hum Mol Genet 19: 2858–2866. doi: 10.1093/hmg/ddq189 20453063

49. Schnetz MP, Bartels CF, Shastri K, Balasubramanian D, Zentner GE, et al. (2009) Genomic distribution of CHD7 on chromatin tracks H3K4 methylation patterns. Genome Res 19: 590–601. doi: 10.1101/gr.086983.108 19251738

50. Schnetz MP, Handoko L, Akhtar-Zaidi B, Bartels CF, Pereira CF, et al. (2010) CHD7 targets active gene enhancer elements to modulate ES cell-specific gene expression. PLoS Genet 6: e1001023. doi: 10.1371/journal.pgen.1001023 20657823

51. Melgar MF, Collins FS, Sethupathy P (2011) Discovery of active enhancers through bidirectional expression of short transcripts. Genome Biol 12: R113. doi: 10.1186/gb-2011-12-11-r113 22082242

52. Degner SC, Verma-Gaur J, Wong TP, Bossen C, Iverson GM, et al. (2011) CCCTC-binding factor (CTCF) and cohesin influence the genomic architecture of the Igh locus and antisense transcription in pro-B cells. Proc Natl Acad Sci U S A 108: 9566–9571. doi: 10.1073/pnas.1019391108 21606361

53. Dawson MA, Prinjha RK, Dittmann A, Giotopoulos G, Bantscheff M, et al. (2011) Inhibition of BET recruitment to chromatin as an effective treatment for MLL-fusion leukaemia. Nature 478: 529–533. doi: 10.1038/nature10509 21964340

54. Ho L, Jothi R, Ronan JL, Cui K, Zhao K, et al. (2009) An embryonic stem cell chromatin remodeling complex, esBAF, is an essential component of the core pluripotency transcriptional network. Proc Natl Acad Sci U S A 106: 5187–5191. doi: 10.1073/pnas.0812888106 19279218

55. Bajpai R, Chen DA, Rada-Iglesias A, Zhang J, Xiong Y, et al. (2010) CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature 463: 958–962. doi: 10.1038/nature08733 20130577

56. Nagl NG Jr., Wang X, Patsialou A, Van Scoy M, Moran E (2007) Distinct mammalian SWI/SNF chromatin remodeling complexes with opposing roles in cell-cycle control. Embo J 26: 752–763. 17255939

57. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, et al. (2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39: 311–318. 17277777

58. Kaikkonen MU, Spann NJ, Heinz S, Romanoski CE, Allison KA, et al. (2013) Remodeling of the enhancer landscape during macrophage activation is coupled to enhancer transcription. Mol Cell 51: 310–325. doi: 10.1016/j.molcel.2013.07.010 23932714

59. Pekowska A, Benoukraf T, Zacarias-Cabeza J, Belhocine M, Koch F, et al. (2011) H3K4 tri-methylation provides an epigenetic signature of active enhancers. Embo J 30: 4198–4210. doi: 10.1038/emboj.2011.295 21847099

60. Mousavi K, Zare H, Dell'orso S, Grontved L, Gutierrez-Cruz G, et al. (2013) eRNAs Promote Transcription by Establishing Chromatin Accessibility at Defined Genomic Loci. Mol Cell 51: 606–617. doi: 10.1016/j.molcel.2013.07.022 23993744

61. Melo CA, Drost J, Wijchers PJ, van de Werken H, de Wit E, et al. (2013) eRNAs are required for p53-dependent enhancer activity and gene transcription. Mol Cell 49: 524–535. doi: 10.1016/j.molcel.2012.11.021 23273978

62. Li W, Notani D, Ma Q, Tanasa B, Nunez E, et al. (2013) Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation. Nature 498: 516–520. doi: 10.1038/nature12210 23728302

63. Lam MT, Cho H, Lesch HP, Gosselin D, Heinz S, et al. (2013) Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription. Nature 498: 511–515. doi: 10.1038/nature12209 23728303

64. Lai F, Orom UA, Cesaroni M, Beringer M, Taatjes DJ, et al. (2013) Activating RNAs associate with Mediator to enhance chromatin architecture and transcription. Nature 494: 497–501. doi: 10.1038/nature11884 23417068

65. Srinivasan S, Armstrong JA, Deuring R, Dahlsveen IK, McNeill H, et al. (2005) The Drosophila trithorax group protein Kismet facilitates an early step in transcriptional elongation by RNA Polymerase II. Development 132: 1623–1635. 15728673

66. Garel A, Axel R (1976) Selective digestion of transcriptionally active ovalbumin genes from oviduct nuclei. Proc Natl Acad Sci U S A 73: 3966–3970. 1069279

67. Weintraub H, Groudine M (1976) Chromosomal subunits in active genes have an altered conformation. Science 193: 848–856. 948749

68. Marom R, Shur I, Hager GL, Benayahu D (2006) Expression and regulation of CReMM, a chromodomain helicase-DNA-binding (CHD), in marrow stroma derived osteoprogenitors. J Cell Physiol 207: 628–635. 16523501

69. Surapureddi S, Viswakarma N, Yu S, Guo D, Rao MS, et al. (2006) PRIC320, a transcription coactivator, isolated from peroxisome proliferator-binding protein complex. Biochem Biophys Res Commun 343: 535–543. 16554032

70. Jacobsen BM, Richer JK, Schittone SA, Horwitz KB (2002) New human breast cancer cells to study progesterone receptor isoform ratio effects and ligand-independent gene regulation. J Biol Chem 277: 27793–27800. 12021276

71. Strutt H, Paro R (1999) Mapping DNA target sites of chromatin proteins in vivo by formaldehyde crosslinking. Methods Mol Biol 119: 455–467. 10804532

72. Giannopoulou EG, Elemento O (2011) An integrated ChIP-seq analysis platform with customizable workflows. BMC Bioinformatics 12: 277. doi: 10.1186/1471-2105-12-277 21736739

73. Elemento O, Slonim N, Tavazoie S (2007) A universal framework for regulatory element discovery across all genomes and data types. Mol Cell 28: 337–350. 17964271

74. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, et al. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202–208. doi: 10.1093/nar/gkp335 19458158

75. Pavesi G, Mereghetti P, Mauri G, Pesole G (2004) Weeder Web: discovery of transcription factor binding sites in a set of sequences from co-regulated genes. Nucleic Acids Res 32: W199–203. 15215380

76. Matys V, Kel-Margoulis OV, Fricke E, Liebich I, Land S, et al. (2006) TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res 34: D108–110. 16381825

77. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, et al. (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31: e15. 12582260

78. Sanges R, Cordero F, Calogero RA (2007) oneChannelGUI: a graphical interface to Bioconductor tools, designed for life scientists who are not familiar with R language. Bioinformatics 23: 3406–3408. 17875544

79. Huang da W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44–57. doi: 10.1038/nprot.2008.211 19131956

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 4
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Eozinofilní granulomatóza s polyangiitidou
nový kurz

Betablokátory a Ca antagonisté z jiného úhlu
Autori: prof. MUDr. Michal Vrablík, Ph.D., MUDr. Petr Janský

Autori: doc. MUDr. Petr Čáp, Ph.D.

Farmakoterapie akutní a chronické bolesti

Získaná hemofilie - Povědomí o nemoci a její diagnostika

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Nemáte účet?  Registrujte sa

Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa