Chromatin Sampling—An Emerging Perspective on Targeting Polycomb Repressor Proteins

1. RingroseL, ParoR (2004) Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu Rev Genet 38: 413–443.

2. StruhlG, AkamM (1985) Altered distributions of Ultrabithorax transcripts in extra sex combs mutant embryos of Drosophila. EMBO J 4: 3259–3264.

3. ChanCS, RastelliL, PirrottaV (1994) A Polycomb response element in the Ubx gene that determines an epigenetically inherited state of repression. EMBO J 13: 2553–2564.

4. SchwartzYB, KahnTG, StenbergP, OhnoK, BourgonR, et al. (2010) Alternative epigenetic chromatin states of polycomb target genes. PLoS Genet 6: e1000805 doi:10.1371/journal.pgen.1000805

5. MikkelsenTS, KuM, JaffeDB, IssacB, LiebermanE, et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553–560.

6. XieR, EverettLJ, LimHW, PatelNA, SchugJ, et al. (2013) Dynamic chromatin remodeling mediated by polycomb proteins orchestrates pancreatic differentiation of human embryonic stem cells. Cell Stem Cell 12: 224–237.

7. MohnF, WeberM, RebhanM, RoloffTC, RichterJ, et al. (2008) Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell 30: 755–766.

8. KohlmaierA, SavareseF, LachnerM, MartensJ, JenuweinT, et al. (2004) A chromosomal memory triggered by Xist regulates histone methylation in X inactivation. PLoS Biol 2: e171 doi:10.1371/journal.pbio.0020171

9. SimonJA, KingstonRE (2013) Occupying chromatin: polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put. Mol Cell 49: 808–824.

10. TavaresL, DimitrovaE, OxleyD, WebsterJ, PootR, et al. (2012) RYBP-PRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3. Cell 148: 664–678.

11. GaoZ, ZhangJ, BonasioR, StrinoF, SawaiA, et al. (2012) PCGF homologs, CBX proteins, and RYBP define functionally distinct PRC1 family complexes. Mol Cell 45: 344–356.

12. FischleW, WangY, JacobsSA, KimY, AllisCD, et al. (2003) Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev 17: 1870–1881.

13. MinJ, ZhangY, XuRM (2003) Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev 17: 1823–1828.

14. SchuettengruberB, MartinezAM, IovinoN, CavalliG (2011) Trithorax group proteins: switching genes on and keeping them active. Nat Rev Mol Cell Biol 12: 799–814.

15. PouxS, MelfiR, PirrottaV (2001) Establishment of Polycomb silencing requires a transient interaction between PC and ESC. Genes Dev 15: 2509–2514.

16. Mohd-SaripA, VenturiniF, ChalkleyGE, VerrijzerCP (2002) Pleiohomeotic can link polycomb to DNA and mediate transcriptional repression. Mol Cell Biol 22: 7473–7483.

17. Mohd-SaripA, CleardF, MishraRK, KarchF, VerrijzerCP (2005) Synergistic recognition of an epigenetic DNA element by Pleiohomeotic and a Polycomb core complex. Genes Dev 19: 1755–1760.

18. WangL, BrownJL, CaoR, ZhangY, KassisJA, et al. (2004) Hierarchical recruitment of polycomb group silencing complexes. Mol Cell 14: 637–646.

19. WooCJ, KharchenkoPV, DaheronL, ParkPJ, KingstonRE (2010) A region of the human HOXD cluster that confers polycomb-group responsiveness. Cell 140: 99–110.

20. DietrichN, LerdrupM, LandtE, Agrawal-SinghS, BakM, et al. (2012) REST-mediated recruitment of polycomb repressor complexes in mammalian cells. PLoS Genet 8: e1002494 doi:10.1371/journal.pgen.1002494

21. RenX, KerppolaTK (2011) REST interacts with Cbx proteins and regulates polycomb repressive complex 1 occupancy at RE1 elements. Mol Cell Biol 31: 2100–2110.

22. ArnoldP, ScholerA, PachkovM, BalwierzPJ, JorgensenH, et al. (2013) Modeling of epigenome dynamics identifies transcription factors that mediate Polycomb targeting. Genome Res 23: 60–73.

23. YuM, MazorT, HuangH, HuangHT, KathreinKL, et al. (2012) Direct recruitment of polycomb repressive complex 1 to chromatin by core binding transcription factors. Mol Cell 45: 330–343.

24. KuM, KocheRP, RheinbayE, MendenhallEM, EndohM, et al. (2008) Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet 4: e1000242 doi:10.1371/journal.pgen.1000242

25. MakW, BaxterJ, SilvaJ, NewallAE, OtteAP, et al. (2002) Mitotically stable association of polycomb group proteins eed and enx1 with the inactive x chromosome in trophoblast stem cells. Curr Biol 12: 1016–1020.

26. ZhaoJ, SunBK, ErwinJA, SongJJ, LeeJT (2008) Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322: 750–756.

27. BrockdorffN (2013) Noncoding RNA and Polycomb recruitment. RNA 19: 429–442.

28. SaboPJ, HumbertR, HawrylyczM, WallaceJC, DorschnerMO, et al. (2004) Genome-wide identification of DNaseI hypersensitive sites using active chromatin sequence libraries. Proc Natl Acad Sci U S A 101: 4537–4542.

29. BlackledgeNP, KloseR (2011) CpG island chromatin: a platform for gene regulation. Epigenetics 6: 147–152.

30. DeatonAM, BirdA (2011) CpG islands and the regulation of transcription. Genes Dev 25: 1010–1022.

31. ThomsonJP, SkenePJ, SelfridgeJ, ClouaireT, GuyJ, et al. (2010) CpG islands influence chromatin structure via the CpG-binding protein Cfp1. Nature 464: 1082–1086.

32. BlackledgeNP, ZhouJC, TolstorukovMY, FarcasAM, ParkPJ, et al. (2010) CpG islands recruit a histone H3 lysine 36 demethylase. Mol Cell 38: 179–190.

33. LongHK, SimsD, HegerA, BlackledgeNP, KutterC, et al. (2013) Epigenetic conservation at gene regulatory elements revealed by non-methylated DNA profiling in seven vertebrates. Elife 2: e00348.

34. MendenhallEM, KocheRP, TruongT, ZhouVW, IssacB, et al. (2010) GC-rich sequence elements recruit PRC2 in mammalian ES cells. PLoS Genet 6: e1001244 doi:10.1371/journal.pgen.1001244

35. LynchMD, SmithAJ, De GobbiM, FlenleyM, HughesJR, et al. (2012) An interspecies analysis reveals a key role for unmethylated CpG dinucleotides in vertebrate Polycomb complex recruitment. EMBO J 31: 317–329.

36. LindrothAM, ParkYJ, McLeanCM, DokshinGA, PerssonJM, et al. (2008) Antagonism between DNA and H3K27 methylation at the imprinted Rasgrf1 locus. PLoS Genet 4: e1000145 doi:10.1371/journal.pgen.1000145

37. BrinkmanAB, GuH, BartelsSJ, ZhangY, MatareseF, et al. (2012) Sequential ChIP-bisulfite sequencing enables direct genome-scale investigation of chromatin and DNA methylation cross-talk. Genome Res 22: 1128–1138.

38. HagarmanJA, MotleyMP, KristjansdottirK, SolowayPD (2013) Coordinate regulation of DNA methylation and H3K27me3 in mouse embryonic stem cells. PLoS ONE 8: e53880 doi:10.1371/journal.pone.0053880

39. HeJ, ShenL, WanM, TaranovaO, WuH, et al. (2013) Kdm2b maintains murine embryonic stem cell status by recruiting PRC1 complex to CpG islands of developmental genes. Nat Cell Biol 15: 373–384.

40. WuX, JohansenJV, HelinK (2013) Fbxl10/Kdm2b recruits Polycomb repressive complex 1 to CpG islands and regulates H2A ubiquitylation. Mol Cell 49: 1134–1146.

41. FarcasAM, BlackledgeNP, SudberyI, LongHK, McGouranJF, et al. (2012) KDM2B links the Polycomb Repressive Complex 1 (PRC1) to recognition of CpG islands. Elife 1: e00205.

42. PengJC, ValouevA, SwigutT, ZhangJ, ZhaoY, et al. (2009) Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. Cell 139: 1290–1302.

43. LiG, MargueronR, KuM, ChambonP, BernsteinBE, et al. (2010) Jarid2 and PRC2, partners in regulating gene expression. Genes Dev 24: 368–380.

44. YuanW, WuT, FuH, DaiC, WuH, et al. (2012) Dense chromatin activates Polycomb repressive complex 2 to regulate H3 lysine 27 methylation. Science 337: 971–975.

45. SchmitgesFW, PrustyAB, FatyM, StutzerA, LingarajuGM, et al. (2011) Histone methylation by PRC2 is inhibited by active chromatin marks. Mol Cell 42: 330–341.

46. HeJ, KallinEM, TsukadaY, ZhangY (2008) The H3K36 demethylase Jhdm1b/Kdm2b regulates cell proliferation and senescence through p15(Ink4b). Nat Struct Mol Biol 15: 1169–1175.

47. WuH, CoskunV, TaoJ, XieW, GeW, et al. (2010) Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 329: 444–448.

48. ReddingtonJP, PerriconeSM, NestorCE, ReichmannJ, YoungsonNA, et al. (2013) Redistribution of H3K27me3 upon DNA hypomethylation results in de-repression of Polycomb-target genes. Genome Biol 14: R25.

49. WeinhoferI, HehenbergerE, RoszakP, HennigL, KöhlerC (2010) H3K27me3 profiling of the endosperm implies exclusion of polycomb group protein targeting by DNA methylation. PLoS Genet 6: e1001152 doi:10.1371/journal.pgen.1001152

50. DelerisA, StroudH, BernatavichuteY, JohnsonE, KleinG, et al. (2012) Loss of the DNA methyltransferase MET1 Induces H3K9 hypermethylation at PcG target genes and redistribution of H3K27 trimethylation to transposons in Arabidopsis thaliana. PLoS Genet 8: e1003062 doi:10.1371/journal.pgen.1003062

51. GaydosLJ, RechtsteinerA, EgelhoferTA, CarrollCR, StromeS (2012) Antagonism between MES-4 and Polycomb repressive complex 2 promotes appropriate gene expression in C. elegans germ cells. Cell Rep 2: 1169–1177.

52. GuentherMG, LevineSS, BoyerLA, JaenischR, YoungRA (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130: 77–88.

53. LeeJH, SkalnikDG (2008) Wdr82 is a C-terminal domain-binding protein that recruits the Setd1A Histone H3-Lys4 methyltransferase complex to transcription start sites of transcribed human genes. Mol Cell Biol 28: 609–618.

54. NgHH, RobertF, YoungRA, StruhlK (2003) Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell 11: 709–719.

55. KarlicR, ChungHR, LasserreJ, VlahovicekK, VingronM (2010) Histone modification levels are predictive for gene expression. Proc Natl Acad Sci U S A 107: 2926–2931.

56. ReynoldsN, Salmon-DivonM, DvingeH, Hynes-AllenA, BalasooriyaG, et al. (2012) NuRD-mediated deacetylation of H3K27 facilitates recruitment of Polycomb Repressive Complex 2 to direct gene repression. EMBO J 31: 593–605.

57. LeeMG, VillaR, TrojerP, NormanJ, YanKP, et al. (2007) Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science 318: 447–450.

58. EndohM, EndoTA, EndohT, FujimuraY, OharaO, et al. (2008) Polycomb group proteins Ring1A/B are functionally linked to the core transcriptional regulatory circuitry to maintain ES cell identity. Development 135: 1513–1524.

59. LeebM, PasiniD, NovatchkovaM, JaritzM, HelinK, et al. (2010) Polycomb complexes act redundantly to repress genomic repeats and genes. Genes Dev 24: 265–276.

60. BrackenAP, DietrichN, PasiniD, HansenKH, HelinK (2006) Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev 20: 1123–1136.

61. KlymenkoT, MullerJ (2004) The histone methyltransferases Trithorax and Ash1 prevent transcriptional silencing by Polycomb group proteins. EMBO Rep 5: 373–377.

62. AzuaraV, PerryP, SauerS, SpivakovM, JorgensenHF, et al. (2006) Chromatin signatures of pluripotent cell lines. Nat Cell Biol 8: 532–538.

63. BernsteinBE, MikkelsenTS, XieX, KamalM, HuebertDJ, et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315–326.

64. StockJK, GiadrossiS, CasanovaM, BrookesE, VidalM, et al. (2007) Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat Cell Biol 9: 1428–1435.

65. BinderH, SteinerL, PrzybillaJ, RohlfT, ProhaskaS, et al. (2013) Transcriptional regulation by histone modifications: towards a theory of chromatin re-organization during stem cell differentiation. Phys Biol 10: 026006.

66. RohlfT, SteinerL, PrzybillaJ, ProhaskaS, BinderH, et al. (2012) Modeling the dynamic epigenome: from histone modifications towards self-organizing chromatin. Epigenomics 4: 205–219.

67. AngelA, SongJ, DeanC, HowardM (2011) A Polycomb-based switch underlying quantitative epigenetic memory. Nature 476: 105–108.

68. RingroseL, ParoR (2001) Remembering silence. Bioessays 23: 566–570.

69. VoigtP, TeeWW, ReinbergD (2013) A double take on bivalent promoters. Genes Dev 27: 1318–1338.