A System for Genome-Wide Histone Variant Dynamics In ES Cells Reveals Dynamic MacroH2A2 Replacement at Promoters

English version České info

The ability of cells to remember the correct cell fate is at least partly dependent on how the genome is packaged. Embryonic stem (ES) cells, which have the ability to become any cell type in the body, are a particularly well-studied system for understanding how the packaging of the genome – chromatin – controls cell state. One of the more curious aspects of ES cell chromatin is its “hyperdynamic” nature, as the histone proteins that comprise chromatin have been reported to exchange rapidly on and off the DNA in these cells. Here, we report a pulse chase system for studying histone dynamics in mouse ES cells, and report on the dynamics of two histone variants, H3.3 and MacroH2A2. Notably, MacroH2A2 is highly dynamic in ES cells, with rapid exchange occurring over gene promoters, alongside much more stably-bound domains that cover large blocks of the genome. Upon differentiation to fibroblasts MacroH2A2 becomes much more stably-bound to the genome, consistent with the idea that this histone variant plays a role in “locking down” repressed regions the genome. These results provide further evidence for a key role of histone dynamics in control of cell state inheritance.

Vyšlo v časopise: A System for Genome-Wide Histone Variant Dynamics In ES Cells Reveals Dynamic MacroH2A2 Replacement at Promoters. PLoS Genet 10(8): e32767. doi:10.1371/journal.pgen.1004515
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004515

Souhrn

Zdroje

1. KimuraH, CookPR (2001) Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. J Cell Biol 153: 1341–1353.

2. AhmadK, HenikoffS (2002) Epigenetic consequences of nucleosome dynamics. Cell 111: 281–284.

3. AhmadK, HenikoffS (2002) Histone H3 variants specify modes of chromatin assembly. Proc Natl Acad Sci U S A 99 Suppl 4: 16477–16484.

4. AhmadK, HenikoffS (2002) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9: 1191–1200.

5. DionMF, KaplanT, KimM, BuratowskiS, FriedmanN, et al. (2007) Dynamics of replication-independent histone turnover in budding yeast. Science 315: 1405–1408.

6. MitoY, HenikoffJG, HenikoffS (2005) Genome-scale profiling of histone H3.3 replacement patterns. Nat Genet 37: 1090–1097.

7. MitoY, HenikoffJG, HenikoffS (2007) Histone replacement marks the boundaries of cis-regulatory domains. Science 315: 1408–1411.

8. RufiangeA, JacquesPE, BhatW, RobertF, NouraniA (2007) Genome-wide replication-independent histone H3 exchange occurs predominantly at promoters and implicates H3 K56 acetylation and Asf1. Mol Cell 27: 393–405.

9. GoldbergAD, BanaszynskiLA, NohKM, LewisPW, ElsaesserSJ, et al. (2010) Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140: 678–691.

10. StroudH, OteroS, DesvoyesB, Ramirez-ParraE, JacobsenSE, et al. (2012) Genome-wide analysis of histone H3.1 and H3.3 variants in Arabidopsis thaliana. Proc Natl Acad Sci U S A 109: 5370–5375.

11. JinC, ZangC, WeiG, CuiK, PengW, et al. (2009) H3.3/H2A.Z double variant-containing nucleosomes mark ‘nucleosome-free regions’ of active promoters and other regulatory regions. Nat Genet 41: 941–945.

12. AygunO, MehtaS, GrewalSI (2013) HDAC-mediated suppression of histone turnover promotes epigenetic stability of heterochromatin. Nat Struct Mol Biol 20: 547–554.

13. XuM, LongC, ChenX, HuangC, ChenS, et al. (2010) Partitioning of histone H3-H4 tetramers during DNA replication-dependent chromatin assembly. Science 328: 94–98.

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

15. FazzioTG, HuffJT, PanningB (2008) An RNAi screen of chromatin proteins identifies Tip60-p400 as a regulator of embryonic stem cell identity. Cell 134: 162–174.

16. ChristophersenNS, HelinK (2010) Epigenetic control of embryonic stem cell fate. J Exp Med 207: 2287–2295.

17. BoyerLA, PlathK, ZeitlingerJ, BrambrinkT, MedeirosLA, et al. (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349–353.

18. CreyghtonMP, MarkoulakiS, LevineSS, HannaJ, LodatoMA, et al. (2008) H2AZ is enriched at polycomb complex target genes in ES cells and is necessary for lineage commitment. Cell 135: 649–661.

19. KajiK, CaballeroIM, MacLeodR, NicholsJ, WilsonVA, et al. (2006) The NuRD component Mbd3 is required for pluripotency of embryonic stem cells. Nat Cell Biol 8: 285–292.

20. MeshorerE, YellajoshulaD, GeorgeE, ScamblerPJ, BrownDT, et al. (2006) Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev Cell 10: 105–116.

21. CreppeC, PosavecM, DouetJ, BuschbeckM (2012) MacroH2A in stem cells: a story beyond gene repression. Epigenomics 4: 221–227.

22. ChangolkarLN, CostanziC, LeuNA, ChenD, McLaughlinKJ, et al. (2007) Developmental changes in histone macroH2A1-mediated gene regulation. Mol Cell Biol 27: 2758–2764.

23. ChangolkarLN, PehrsonJR (2006) macroH2A1 histone variants are depleted on active genes but concentrated on the inactive X chromosome. Mol Cell Biol 26: 4410–4420.

24. ChangCC, GaoS, SungLY, CorryGN, MaY, et al. (2010) Rapid elimination of the histone variant MacroH2A from somatic cell heterochromatin after nuclear transfer. Cell Reprogram 12: 43–53.

25. Gaspar-MaiaA, QadeerZA, HassonD, RatnakumarK, LeuNA, et al. (2012) MacroH2A histone variants act as a barrier upon reprogramming towards pluripotency. Nat Commun 4: 1565.

26. PasqueV, GillichA, GarrettN, GurdonJB (2011) Histone variant macroH2A confers resistance to nuclear reprogramming. Embo J 30: 2373–2387.

27. PasqueV, RadzisheuskayaA, GillichA, Halley-StottRP, PanamarovaM, et al. (2012) Histone variant macroH2A marks embryonic differentiation in vivo and acts as an epigenetic barrier to induced pluripotency. J Cell Sci 6094–6104.

28. BarreroMJ, SeseB, KueblerB, BilicJ, BoueS, et al. (2013) Macrohistone Variants Preserve Cell Identity by Preventing the Gain of H3K4me2 during Reprogramming to Pluripotency. Cell Rep 3: 1005–1011.

29. CostanziC, PehrsonJR (1998) Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature 393: 599–601.

30. ChadwickBP, WillardHF (2001) Histone H2A variants and the inactive X chromosome: identification of a second macroH2A variant. Hum Mol Genet 10: 1101–1113.

31. CsankovszkiG, PanningB, BatesB, PehrsonJR, JaenischR (1999) Conditional deletion of Xist disrupts histone macroH2A localization but not maintenance of X inactivation. Nat Genet 22: 323–324.

32. CreppeC, JanichP, CantarinoN, NogueraM, ValeroV, et al. (2012) MacroH2A1 regulates the balance between self-renewal and differentiation commitment in embryonic and adult stem cells. Mol Cell Biol 32: 1442–1452.

33. DealRB, HenikoffS (2010) Capturing the dynamic epigenome. Genome Biol 11: 218.

34. SchermerUJ, KorberP, HorzW (2005) Histones are incorporated in trans during reassembly of the yeast PHO5 promoter. Mol Cell 19: 279–285.

35. JamaiA, ImoberdorfRM, StrubinM (2007) Continuous Histone H2B and Transcription-Dependent Histone H3 Exchange in Yeast Cells outside of Replication. Mol Cell 25: 345–355.

36. KraushaarDC, JinW, MaunakeaA, AbrahamB, HaM, et al. (2013) Genome-wide incorporation dynamics reveal distinct categories of turnover for the histone variant H3.3. Genome Biol 14: R121.

37. DealRB, HenikoffJG, HenikoffS (2010) Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328: 1161–1164.

38. BeardC, HochedlingerK, PlathK, WutzA, JaenischR (2006) Efficient method to generate single-copy transgenic mice by site-specific integration in embryonic stem cells. Genesis 44: 23–28.

39. HuG, CuiK, NorthrupD, LiuC, WangC, et al. (2013) H2A.Z facilitates access of active and repressive complexes to chromatin in embryonic stem cell self-renewal and differentiation. Cell Stem Cell 12: 180–192.

40. GambleMJ, FrizzellKM, YangC, KrishnakumarR, KrausWL (2010) The histone variant macroH2A1 marks repressed autosomal chromatin, but protects a subset of its target genes from silencing. Genes Dev 24: 21–32.

41. TakahashiK, YamanakaS (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663–676.

42. YildirimO, LiR, HungJH, ChenPB, DongX, et al. (2011) Mbd3/NURD complex regulates expression of 5-hydroxymethylcytosine marked genes in embryonic stem cells. Cell 147: 1498–1510.

43. YangF, KempCJ, HenikoffS (2013) Doxorubicin enhances nucleosome turnover around promoters. Curr Biol 23: 782–787.

44. CoreLJ, LisJT (2008) Transcription regulation through promoter-proximal pausing of RNA polymerase II. Science 319: 1791–1792.

45. KimJ, WooAJ, ChuJ, SnowJW, FujiwaraY, et al. (2010) A Myc network accounts for similarities between embryonic stem and cancer cell transcription programs. Cell 143: 313–324.