PcG-Mediated Higher-Order Chromatin Structures Modulate Replication Programs at the BX-C

English version České info

Polycomb group proteins (PcG) exert conserved epigenetic functions that convey maintenance of repressed transcriptional states, via post-translational histone modifications and high order structure formation. During S-phase, in order to preserve cell identity, in addition to DNA information, PcG-chromatin-mediated epigenetic signatures need to be duplicated requiring a tight coordination between PcG proteins and replication programs. However, the interconnection between replication timing control and PcG functions remains unknown. Using Drosophila embryonic cell lines, we find that, while presence of specific PcG complexes and underlying transcription state are not the sole determinants of cellular replication timing, PcG-mediated higher-order structures appear to dictate the timing of replication and maintenance of the silenced state. Using published datasets we show that PRC1, PRC2, and PhoRC complexes differently correlate with replication timing of their targets. In the fully repressed BX-C, loss of function experiments revealed a synergistic role for PcG proteins in the maintenance of replication programs through the mediation of higher-order structures. Accordingly, replication timing analysis performed on two Drosophila cell lines differing for BX-C gene expression states, PcG distribution, and chromatin domain conformation revealed a cell-type-specific replication program that mirrors lineage-specific BX-C higher-order structures. Our work suggests that PcG complexes, by regulating higher-order chromatin structure at their target sites, contribute to the definition and the maintenance of genomic structural domains where genes showing the same epigenetic state replicate at the same time.

Vyšlo v časopise: PcG-Mediated Higher-Order Chromatin Structures Modulate Replication Programs at the BX-C. PLoS Genet 9(2): e32767. doi:10.1371/journal.pgen.1003283
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003283

Souhrn

Zdroje

1. HirataniI, GilbertDM (2009) Replication timing as an epigenetic mark. Epigenetics 4: 93–97.

2. LanzuoloC, OrlandoV (2012) Memories from the Polycomb Group Proteins. Annu Rev Genet

3. MihalyJ, MishraRK, KarchF (1998) A conserved sequence motif in Polycomb-response elements. Mol Cell 1: 1065–1066.

4. BeiselC, ParoR (2011) Silencing chromatin: comparing modes and mechanisms. Nat Rev Genet 12: 123–135.

5. EnderleD, BeiselC, StadlerMB, GerstungM, AthriP, et al. (2011) Polycomb preferentially targets stalled promoters of coding and noncoding transcripts. Genome Res 21: 216–226.

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

7. CzerminB, MelfiR, McCabeD, SeitzV, ImhofA, et al. (2002) Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111: 185–196.

8. KuzmichevA, NishiokaK, Erdjument-BromageH, TempstP, ReinbergD (2002) Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 16: 2893–2905.

9. MullerJ, HartCM, FrancisNJ, VargasML, SenguptaA, et al. (2002) Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111: 197–208.

10. CaoR, WangL, WangH, XiaL, Erdjument-BromageH, et al. (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298: 1039–1043.

11. BantigniesF, RoureV, CometI, LeblancB, SchuettengruberB, et al. (2011) Polycomb-dependent regulatory contacts between distant Hox loci in Drosophila. Cell 144: 214–226.

12. CometI, SchuettengruberB, SextonT, CavalliG (2011) A chromatin insulator driving three-dimensional Polycomb response element (PRE) contacts and Polycomb association with the chromatin fiber. Proc Natl Acad Sci U S A 108: 2294–2299.

13. LanzuoloC, RoureV, DekkerJ, BantigniesF, OrlandoV (2007) Polycomb response elements mediate the formation of chromosome higher-order structures in the bithorax complex. Nat Cell Biol 9: 1167–1174.

14. BerezneyR, DubeyDD, HubermanJA (2000) Heterogeneity of eukaryotic replicons, replicon clusters, and replication foci. Chromosoma 108: 471–484.

15. EaswaranHP, LeonhardtH, CardosoMC (2007) Distribution of DNA replication proteins in Drosophila cells. BMC Cell Biol 8: 42.

16. KitamuraE, BlowJJ, TanakaTU (2006) Live-cell imaging reveals replication of individual replicons in eukaryotic replication factories. Cell 125: 1297–1308.

17. HansenRS, ThomasS, SandstromR, CanfieldTK, ThurmanRE, et al. (2010) Sequencing newly replicated DNA reveals widespread plasticity in human replication timing. Proc Natl Acad Sci U S A 107: 139–144.

18. SchwaigerM, StadlerMB, BellO, KohlerH, OakeleyEJ, et al. (2009) Chromatin state marks cell-type- and gender-specific replication of the Drosophila genome. Genes Dev 23: 589–601.

19. ZhouJ, ErmakovaOV, RibletR, BirshteinBK, SchildkrautCL (2002) Replication and subnuclear location dynamics of the immunoglobulin heavy-chain locus in B-lineage cells. Mol Cell Biol 22: 4876–4889.

20. HirataniI, RybaT, ItohM, RathjenJ, KulikM, et al. (2010) Genome-wide dynamics of replication timing revealed by in vitro models of mouse embryogenesis. Genome Res 20: 155–169.

21. PerryP, SauerS, BillonN, RichardsonWD, SpivakovM, et al. (2004) A dynamic switch in the replication timing of key regulator genes in embryonic stem cells upon neural induction. Cell Cycle 3: 1645–1650.

22. SimonI, TenzenT, MostoslavskyR, FibachE, LandeL, et al. (2001) Developmental regulation of DNA replication timing at the human beta globin locus. EMBO J 20: 6150–6157.

23. BellO, SchwaigerM, OakeleyEJ, LienertF, BeiselC, et al. (2010) Accessibility of the Drosophila genome discriminates PcG repression, H4K16 acetylation and replication timing. Nat Struct Mol Biol 17: 894–900.

24. Casas-DelucchiCS, van BemmelJG, HaaseS, HerceHD, NowakD, et al. (2011) Histone hypoacetylation is required to maintain late replication timing of constitutive heterochromatin. Nucleic Acids Res

25. JorgensenHF, AzuaraV, AmoilsS, SpivakovM, TerryA, et al. (2007) The impact of chromatin modifiers on the timing of locus replication in mouse embryonic stem cells. Genome Biol 8: R169.

26. YinS, DengW, HuL, KongX (2009) The impact of nucleosome positioning on the organization of replication origins in eukaryotes. Biochem Biophys Res Commun 385: 363–368.

27. Lande-DinerL, ZhangJM, CedarH (2009) Shifts in Replication Timing Actively Affect Histone Acetylation during Nucleosome Reassembly. Molecular Cell 34: 767–774.

28. LanzuoloC, Lo SardoF, DiamantiniA, OrlandoV (2011) PcG complexes set the stage for epigenetic inheritance of gene silencing in early S phase before replication. PLoS Genet 7: e1002370 doi: 10.1371/journal.pgen.1002370

29. KarnaniN, TaylorC, MalhotraA, DuttaA (2007) Pan-S replication patterns and chromosomal domains defined by genome-tiling arrays of ENCODE genomic areas. Genome Res 17: 865–876.

30. KlochkovDB, GavrilovAA, VassetzkyYS, RazinSV (2009) Early replication timing of the chicken alpha-globin gene domain correlates with its open chromatin state in cells of different lineages. Genomics 93: 481–486.

31. LanzuoloC, Lo SardoF, OrlandoV (2012) Concerted epigenetic signatures inheritance at PcG targets through replication. Cell Cycle 11.

32. MacAlpineDM, RodriguezHK, BellSP (2004) Coordination of replication and transcription along a Drosophila chromosome. Genes Dev 18: 3094–3105.

33. SchubelerD, ScalzoD, KooperbergC, van SteenselB, DelrowJ, et al. (2002) Genome-wide DNA replication profile for Drosophila melanogaster: a link between transcription and replication timing. Nat Genet 32: 438–442.

34. EatonML, PrinzJA, MacAlpineHK, TretyakovG, KharchenkoPV, et al. (2011) Chromatin signatures of the Drosophila replication program. Genome Res 21: 164–174.

35. AspP, BlumR, VethanthamV, ParisiF, MicsinaiM, et al. (2011) Genome-wide remodeling of the epigenetic landscape during myogenic differentiation. Proc Natl Acad Sci U S A 108: E149–158.

36. 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

37. SchwartzYB, KahnTG, NixDA, LiXY, BourgonR, et al. (2006) Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nat Genet 38: 700–705.

38. BeiselC, BunessA, Roustan-EspinosaIM, KochB, SchmittS, et al. (2007) Comparing active and repressed expression states of genes controlled by the Polycomb/Trithorax group proteins. Proc Natl Acad Sci U S A 104: 16615–16620.

39. BrookesE, de SantiagoI, HebenstreitD, MorrisKJ, CarrollT, et al. (2012) Polycomb Associates Genome-wide with a Specific RNA Polymerase II Variant, and Regulates Metabolic Genes in ESCs. Cell Stem Cell 10: 157–170.

40. PappB, MullerJ (2006) Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes Dev 20: 2041–2054.

41. Kheradmand KiaS, Solaimani KartalaeiP, FarahbakhshianE, PourfarzadF, von LindernM, et al. (2009) EZH2-dependent chromatin looping controls INK4a and INK4b, but not ARF, during human progenitor cell differentiation and cellular senescence. Epigenetics & Chromatin 2.

42. TiwariVK, McGarveyKM, LicchesiJD, OhmJE, HermanJG, et al. (2008) PcG proteins, DNA methylation, and gene repression by chromatin looping. PLoS Biol 6: e306 doi:10.1371/journal.pbio.0060306

43. BeuchleD, StruhlG, MullerJ (2001) Polycomb group proteins and heritable silencing of Drosophila Hox genes. Development 128: 993–1004.

44. BreilingA, O'NeillLP, D'EliseoD, TurnerBM, OrlandoV (2004) Epigenome changes in active and inactive polycomb-group-controlled regions. EMBO Rep 5: 976–982.

45. HirataniI, TakebayashiS, LuJ, GilbertDM (2009) Replication timing and transcriptional control: beyond cause and effect–part II. Curr Opin Genet Dev 19: 142–149.

46. SchwaigerM, SchubelerD (2006) A question of timing: emerging links between transcription and replication. Curr Opin Genet Dev 16: 177–183.

47. HirataniI, RybaT, ItohM, YokochiT, SchwaigerM, et al. (2008) Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol 6: e245 doi:10.1371/journal.pbio.0060245

48. KimSM, DubeyDD, HubermanJA (2003) Early-replicating heterochromatin. Genes Dev 17: 330–335.

49. SantosJ, PereiraCF, Di-GregorioA, SpruceT, AlderO, et al. (2010) Differences in the epigenetic and reprogramming properties of pluripotent and extra-embryonic stem cells implicate chromatin remodelling as an important early event in the developing mouse embryo. Epigenetics Chromatin 3: 1.

50. TakebayashiS, DileepV, RybaT, DennisJH, GilbertDM (2012) Chromatin-interaction compartment switch at developmentally regulated chromosomal domains reveals an unusual principle of chromatin folding. Proc Natl Acad Sci U S A 109: 12574–12579.

51. CornacchiaD, DileepV, QuivyJP, FotiR, TiliF, et al. (2012) Mouse Rif1 is a key regulator of the replication-timing programme in mammalian cells. EMBO J 31: 3678–3690.

52. Hassan-ZadehV, ChilakaS, CadoretJC, MaMK, BoggettoN, et al. (2012) USF binding sequences from the HS4 insulator element impose early replication timing on a vertebrate replicator. PLoS Biol 10: e1001277 doi:10.1371/journal.pbio.1001277

53. LiJ, SantoroR, KobernaK, GrummtI (2005) The chromatin remodeling complex NoRC controls replication timing of rRNA genes. EMBO J 24: 120–127.

54. SchwaigerM, KohlerH, OakeleyEJ, StadlerMB, SchubelerD (2010) Heterochromatin protein 1 (HP1) modulates replication timing of the Drosophila genome. Genome Res 20: 771–780.

55. TazumiA, FukuuraM, NakatoR, KishimotoA, TakenakaT, et al. (2012) Telomere-binding protein Taz1 controls global replication timing through its localization near late replication origins in fission yeast. Genes Dev 26: 2050–2062.

56. YamazakiS, IshiiA, KanohY, OdaM, NishitoY, et al. (2012) Rif1 regulates the replication timing domains on the human genome. EMBO J 31: 3667–3677.

57. RybaT, HirataniI, LuJ, ItohM, KulikM, et al. (2010) Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. Genome Res 20: 761–770.

58. YaffeE, Farkash-AmarS, PoltenA, YakhiniZ, TanayA, et al. (2010) Comparative analysis of DNA replication timing reveals conserved large-scale chromosomal architecture. PLoS Genet 6: e1001011 doi:10.1371/journal.pgen.1001011

59. GuillouE, IbarraA, CoulonV, Casado-VelaJ, RicoD, et al. (2010) Cohesin organizes chromatin loops at DNA replication factories. Genes Dev 24: 2812–2822.

60. MacAlpineHK, GordanR, PowellSK, HarteminkAJ, MacAlpineDM (2010) Drosophila ORC localizes to open chromatin and marks sites of cohesin complex loading. Genome Res 20: 201–211.

61. LupoR, BreilingA, BianchiME, OrlandoV (2001) Drosophila chromosome condensation proteins Topoisomerase II and Barren colocalize with Polycomb and maintain Fab-7 PRE silencing. Mol Cell 7: 127–136.

62. AgherbiH, Gaussmann-WengerA, VerthuyC, ChassonL, SerranoM, et al. (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

63. SextonT, YaffeE, KenigsbergE, BantigniesF, LeblancB, et al. (2012) Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148: 458–472.

64. SextonT, YaffeE, KenigsbergE, BantigniesF, LeblancB, et al. (2012) Three-Dimensional Folding and Functional Organization Principles of the Drosophila Genome. Cell

65. LemaitreJM, DanisE, PaseroP, VassetzkyY, MechaliM (2005) Mitotic remodeling of the replicon and chromosome structure. Cell 123: 787–801.

66. ShufaroY, Lacham-KaplanO, TzuberiBZ, McLaughlinJ, TrounsonA, et al. (2010) Reprogramming of DNA Replication Timing. Stem Cells 28: 443–449.

67. HolohanEE, KwongC, AdryanB, BartkuhnM, HeroldM, et al. (2007) CTCF genomic binding sites in Drosophila and the organisation of the bithorax complex. PLoS Genet 3: e112 doi:10.1371/journal.pgen.0030112

68. EfronBTR (1986) Bootsrtrap Methods for Standard Errors, Confdence Intervals, and Other Measures of Statistical Accuracy. Statistical Science 1: 54–75.

69. BreilingA, TurnerBM, BianchiME, OrlandoV (2001) General transcription factors bind promoters repressed by Polycomb group proteins. Nature 412: 651–655.

70. AzuaraV (2006) Profiling of DNA replication timing in unsynchronized cell populations. Nat Protoc 1: 2171–2177.