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PcG Complexes Set the Stage for Epigenetic Inheritance of Gene Silencing in Early S Phase before Replication


Polycomb group (PcG) proteins are part of a conserved cell memory system that conveys epigenetic inheritance of silenced transcriptional states through cell division. Despite the considerable amount of information about PcG mechanisms controlling gene silencing, how PcG proteins maintain repressive chromatin during epigenome duplication is still unclear. Here we identified a specific time window, the early S phase, in which PcG proteins are recruited at BX-C PRE target sites in concomitance with H3K27me3 repressive mark deposition. Notably, these events precede and are uncoupled from PRE replication timing, which occurs in late S phase when most epigenetic signatures are reduced. These findings shed light on one of the key mechanisms for PcG–mediated epigenetic inheritance during S phase, suggesting a conserved model in which the PcG–dependent H3K27me3 mark is inherited by dilution and not by de novo methylation occurring at the time of replication.


Vyšlo v časopise: PcG Complexes Set the Stage for Epigenetic Inheritance of Gene Silencing in Early S Phase before Replication. PLoS Genet 7(11): e32767. doi:10.1371/journal.pgen.1002370
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002370

Souhrn

Polycomb group (PcG) proteins are part of a conserved cell memory system that conveys epigenetic inheritance of silenced transcriptional states through cell division. Despite the considerable amount of information about PcG mechanisms controlling gene silencing, how PcG proteins maintain repressive chromatin during epigenome duplication is still unclear. Here we identified a specific time window, the early S phase, in which PcG proteins are recruited at BX-C PRE target sites in concomitance with H3K27me3 repressive mark deposition. Notably, these events precede and are uncoupled from PRE replication timing, which occurs in late S phase when most epigenetic signatures are reduced. These findings shed light on one of the key mechanisms for PcG–mediated epigenetic inheritance during S phase, suggesting a conserved model in which the PcG–dependent H3K27me3 mark is inherited by dilution and not by de novo methylation occurring at the time of replication.


Zdroje

1. MoreyLHelinK 2010 Polycomb group protein-mediated repression of transcription. Trends Biochem Sci 35 323 332

2. FritschCBrownJLKassisJAMullerJ 1999 The DNA-binding polycomb group protein pleiohomeotic mediates silencing of a Drosophila homeotic gene. Development 126 3905 3913

3. MihalyJMishraRKKarchF 1998 A conserved sequence motif in Polycomb-response elements. Mol Cell 1 1065 1066

4. WangLBrownJLCaoRZhangYKassisJA 2004 Hierarchical recruitment of polycomb group silencing complexes. Mol Cell 14 637 646

5. CaoRWangLWangHXiaLErdjument-BromageH 2002 Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298 1039 1043

6. CzerminBMelfiRMcCabeDSeitzVImhofA 2002 Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111 185 196

7. KuzmichevANishiokaKErdjument-BromageHTempstPReinbergD 2002 Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 16 2893 2905

8. MullerJHartCMFrancisNJVargasMLSenguptaA 2002 Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111 197 208

9. FrancisNJKingstonREWoodcockCL 2004 Chromatin compaction by a polycomb group protein complex. Science 306 1574 1577

10. WangHWangLErdjument-BromageHVidalMTempstP 2004 Role of histone H2A ubiquitination in Polycomb silencing. Nature 431 873 878

11. ScheuermannJCde Ayala AlonsoAGOktabaKLy-HartigNMcGintyRK 2010 Histone H2A deubiquitinase activity of the Polycomb repressive complex PR-DUB. Nature 465 243 247

12. BantigniesFGrimaudCLavrovSGabutMCavalliG 2003 Inheritance of Polycomb-dependent chromosomal interactions in Drosophila. Genes Dev 17 2406 2420

13. BantigniesFRoureVCometILeblancBSchuettengruberB 2011 Polycomb-Dependent Regulatory Contacts between Distant Hox Loci in Drosophila. Cell 144 214 226

14. CleardFMoshkinYKarchFMaedaRK 2006 Probing long-distance regulatory interactions in the Drosophila melanogaster bithorax complex using Dam identification. Nat Genet 38 931 935

15. CometISavitskayaESchuettengruberBNegreNLavrovS 2006 PRE-mediated bypass of two Su(Hw) insulators targets PcG proteins to a downstream promoter. Dev Cell 11 117 124

16. LanzuoloCRoureVDekkerJBantigniesFOrlandoV 2007 Polycomb response elements mediate the formation of chromosome higher-order structures in the bithorax complex. Nat Cell Biol 9 1167 1174

17. SingAPannellDKaraiskakisASturgeonKDjabaliM 2009 A vertebrate Polycomb response element governs segmentation of the posterior hindbrain. Cell 138 885 897

18. WooCJKharchenkoPVDaheronLParkPJKingstonRE 2010 A region of the human HOXD cluster that confers polycomb-group responsiveness. Cell 140 99 110

19. HansenKHBrackenAPPasiniDDietrichNGehaniSS 2008 A model for transmission of the H3K27me3 epigenetic mark. Nat Cell Biol 10 1291 1300

20. MargueronRJustinNOhnoKSharpeMLSonJ 2009 Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 461 762 767

21. FrancisNJFollmerNESimonMDAghiaGButlerJD 2009 Polycomb proteins remain bound to chromatin and DNA during DNA replication in vitro. Cell 137 110 122

22. SchubelerDScalzoDKooperbergCvan SteenselBDelrowJ 2002 Genome-wide DNA replication profile for Drosophila melanogaster: a link between transcription and replication timing. Nat Genet 32 438 442

23. SchwaigerMStadlerMBBellOKohlerHOakeleyEJ 2009 Chromatin state marks cell-type- and gender-specific replication of the Drosophila genome. Genes Dev 23 589 601

24. Kheradmand KiaSSolaimani KartalaeiPFarahbakhshianEPourfarzadFvon LindernM 2009 EZH2-dependent chromatin looping controls INK4a and INK4b, but not ARF, during human progenitor cell differentiation and cellular senescence. Epigenetics & Chromatin 2

25. TiwariVKMcGarveyKMLicchesiJDOhmJEHermanJG 2008 PcG proteins, DNA methylation, and gene repression by chromatin looping. PLoS Biol 6 e306 doi:10.1371/journal.pbio.0060306

26. LupoRBreilingABianchiMEOrlandoV 2001 Drosophila chromosome condensation proteins Topoisomerase II and Barren colocalize with Polycomb and maintain Fab-7 PRE silencing. Mol Cell 7 127 136

27. BreilingAO'NeillLPD'EliseoDTurnerBMOrlandoV 2004 Epigenome changes in active and inactive polycomb-group-controlled regions. EMBO Rep 5 976 982

28. PappBMullerJ 2006 Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes Dev 20 2041 2054

29. GehaniSSAgrawal-SinghSDietrichNChristophersenNSHelinK 2010 Polycomb group protein displacement and gene activation through MSK-dependent H3K27me3S28 phosphorylation. Mol Cell 39 886 900

30. LauPNCheungP 2011 Histone code pathway involving H3 S28 phosphorylation and K27 acetylation activates transcription and antagonizes polycomb silencing. Proc Natl Acad Sci U S A 108 2801 2806

31. Perez-CadahiaBDrobicBDavieJR 2009 H3 phosphorylation: dual role in mitosis and interphase. Biochem Cell Biol 87 695 709

32. BuchenauPHodgsonJStruttHArndt-JovinDJ 1998 The distribution of polycomb-group proteins during cell division and development in Drosophila embryos: impact on models for silencing. J Cell Biol 141 469 481

33. FiczGHeintzmannRArndt-JovinDJ 2005 Polycomb group protein complexes exchange rapidly in living Drosophila. Development

34. AgherbiHGaussmann-WengerAVerthuyCChassonLSerranoM 2009 Polycomb mediated epigenetic silencing and replication timing at the INK4a/ARF locus during senescence. PLoS ONE 4 e5622 doi:10.1371/journal.pone.0005622

35. BirneyEStamatoyannopoulosJADuttaAGuigoRGingerasTR 2007 Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447 799 816

36. ThurmanREDayNNobleWSStamatoyannopoulosJA 2007 Identification of higher-order functional domains in the human ENCODE regions. Genome Res 17 917 927

37. EnglishCMAdkinsMWCarsonJJChurchillMETylerJK 2006 Structural basis for the histone chaperone activity of Asf1. Cell 127 495 508

38. EnglishCMMalufNKTripetBChurchillMETylerJK 2005 ASF1 binds to a heterodimer of histones H3 and H4: a two-step mechanism for the assembly of the H3-H4 heterotetramer on DNA. Biochemistry 44 13673 13682

39. GrothACorpetACookAJRocheDBartekJ 2007 Regulation of replication fork progression through histone supply and demand. Science 318 1928 1931

40. GrothARochaWVerreaultAAlmouzniG 2007 Chromatin challenges during DNA replication and repair. Cell 128 721 733

41. NatsumeREitokuMAkaiYSanoNHorikoshiM 2007 Structure and function of the histone chaperone CIA/ASF1 complexed with histones H3 and H4. Nature 446 338 341

42. QuivyJPRocheDKirschnerDTagamiHNakataniY 2004 A CAF-1 dependent pool of HP1 during heterochromatin duplication. Embo J 23 3516 3526

43. ChenESZhangKNicolasECamHPZofallM 2008 Cell cycle control of centromeric repeat transcription and heterochromatin assembly. Nature 451 734 737

44. KlocAZaratieguiMNoraEMartienssenR 2008 RNA interference guides histone modification during the S phase of chromosomal replication. Curr Biol 18 490 495

45. ChenSBohrerLRRaiANPanYGanL 2010 Cyclin-dependent kinases regulate epigenetic gene silencing through phosphorylation of EZH2. Nat Cell Biol 12 1108 1114

46. KanekoSLiGSonJXuCFMargueronR 2010 Phosphorylation of the PRC2 component Ezh2 is cell cycle-regulated and up-regulates its binding to ncRNA. Genes Dev 24 2615 2620

47. ScharfANBarthTKImhofA 2009 Establishment of histone modifications after chromatin assembly. Nucleic Acids Res 37 5032 5040

48. WeiYChenYHLiLYLangJYehSP 2011 CDK1-dependent phosphorylation of EZH2 suppresses methylation of H3K27 and promotes osteogenic differentiation of human mesenchymal stem cells. Nat Cell Biol 13 87 94

49. DealRBHenikoffJGHenikoffS 2010 Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328 1161 1164

50. HenikoffSFuruyamaTAhmadK 2004 Histone variants, nucleosome assembly and epigenetic inheritance. Trends Genet 20 320 326

51. LoyolaAAlmouzniG 2007 Marking histone H3 variants: how, when and why? Trends Biochem Sci 32 425 433

52. MillsAA 2010 Throwing the cancer switch: reciprocal roles of polycomb and trithorax proteins. Nat Rev Cancer 10 669 682

53. SawarkarRParoR 2010 Interpretation of developmental signaling at chromatin: the Polycomb perspective. Dev Cell 19 651 661

54. BreilingATurnerBMBianchiMEOrlandoV 2001 General transcription factors bind promoters repressed by Polycomb group proteins. Nature 412 651 655

55. ParoRZinkB 1993 The Polycomb gene is differentially regulated during oogenesis and embryogenesis of Drosophila melanogaster. Mech Dev 40 37 46

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