1,227
Views
8
CrossRef citations to date
0
Altmetric
Brief Communication

Bivalency in Drosophila embryos is associated with strong inducibility of Polycomb target genes

, &
Pages 42-50 | Received 15 Mar 2019, Accepted 09 May 2019, Published online: 25 May 2019

References

  • Torres J, Monti R, Moore AL, et al. A switch in transcription and cell fate governs the onset of an epigenetically-deregulated tumor in Drosophila. eLife. 2018;7:e32697.
  • Hariharan IK, Serras F. Imaginal disc regeneration takes flight. Curr Opin Cell Biol. 2017;48:10–16.
  • Lee N, Maurange C, Ringrose L, et al. Suppression of Polycomb group proteins by JNK signalling induces transdetermination in Drosophila imaginal discs. Nature. 2005;438:234–237.
  • Shaw T, Martin P. Epigenetic reprogramming during wound healing: loss of polycomb-mediated silencing may enable upregulation of repair genes. EMBO Rep. 2009;10:881–886.
  • Cao R, Wang L, Wang H, et al. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science. 2002;298:1039–1043.
  • Czermin B, Melfi R, McCabe D, et al. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell. 2002;111:185–196.
  • Müller J, Hart CM, Francis NJ, et al. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell. 2002;111:197–208.
  • Messmer S, Franke A, Paro R. Analysis of the functional role of the Polycomb chromo domain in Drosophila melanogaster. Genes Dev. 1992;6:1241–1254.
  • Wang L, Brown JL, Cao R, et al. Hierarchical recruitment of polycomb group silencing complexes. Mol Cell. 2004;14:637–646.
  • King IFG, Emmons RB, Francis NJ, et al. Analysis of a polycomb group protein defines regions that link repressive activity on nucleosomal templates to in vivo function. Mol Cell Biol. 2005;25:6578–6591.
  • Petruk S, Sedkov Y, Smith S, et al. Trithorax and dCBP acting in a complex to maintain expression of a homeotic gene. Science. 2001;294:1331–1334.
  • Smith ST, Petruk S, Sedkov Y, et al. Modulation of heat shock gene expression by the TAC1 chromatin-modifying complex. Nat Cell Biol. 2004;6:162–167.
  • Bernstein BE, Mikkelsen TS, Xie X, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell. 2006;125:315–326.
  • Azuara V, Perry P, Sauer S, et al. Chromatin signatures of pluripotent cell lines. Nat Cell Biol. 2006;8:532–538.
  • Liu X, Wang C, Liu W, et al. Distinct features of H3K4me3 and H3K27me3 chromatin domains in pre-implantation embryos. Nature. 2016;537:558–562.
  • Weiner A, Lara-Astiaso D, Krupalnik V, et al. Co-ChIP enables genome-wide mapping of histone mark co-occurrence at single-molecule resolution. Nat Biotechnol. 2016;34:953–961.
  • Jadhav U, Nalapareddy K, Saxena M, et al. Acquired tissue-specific promoter bivalency is a basis for PRC2 necessity in adult cells. Cell. 2016;165:1389–1400.
  • Lesch BJ, Silber SJ, McCarrey JR, et al. Parallel evolution of male germline epigenetic poising and somatic development in animals. Nat Genet. 2016;48:888–894.
  • Mas G, Blanco E, Ballaré C, et al. Promoter bivalency favors an open chromatin architecture in embryonic stem cells. Nat Genet. 2018;50:1452–1462.
  • Minoux M, Holwerda S, Vitobello A, et al. Gene bivalency at Polycomb domains regulates cranial neural crest positional identity. Science. 2017;355:eaal2913.
  • Lomniczi A, Loche A, Castellano JM, et al. Epigenetic control of female puberty. Nat Neurosci. 2013;16:281–289.
  • Muotri AR, Chu VT, Marchetto MCN, et al. Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition. Nature. 2005;435:903–910.
  • Hoffmann A, Zimmermann CA, Spengler D. Molecular epigenetic switches in neurodevelopment in health and disease. Front Behav Neurosci. 2015;9:Article 120.
  • Voigt P, Tee -W-W, Reinberg D. A double take on bivalent promoters. Genes Dev. 2013;27:1318–1338.
  • Denissov S, Hofemeister H, Marks H, et al. Mll2 is required for H3K4 trimethylation on bivalent promoters in embryonic stem cells, whereas Mll1 is redundant. Development. 2014;141:526–537.
  • Beisel C, Paro R. Silencing chromatin: comparing modes and mechanisms. Nat Rev Genet. 2011;12:123–135.
  • Gan Q, Schones DE, Ho Eun S, et al. Monovalent and unpoised status of most genes in undifferentiated cell-enriched Drosophila testis. Genome Biol. 2010;11:R42.
  • McKearin DM, Spradling AC. bag-of-marbles: a Drosophila gene required to initiate both male and female gametogenesis. Genes Dev. 1990;4:2242–2251.
  • Gönczy P, Matunis E, DiNardo S. bag-of-marbles and benign gonial cell neoplasm act in the germline to restrict proliferation during Drosophila spermatogenesis. Dev Camb Engl. 1997;124:4361–4371.
  • Schuettengruber B, Ganapathi M, Leblanc B, et al. Functional anatomy of polycomb and trithorax chromatin landscapes in drosophila embryos. PLoS Biol. 2009;7:e1000013.
  • Kang H, Jung YL, McElroy KA, et al. Bivalent complexes of PRC1 with orthologs of BRD4 and MOZ/MORF target developmental genes in Drosophila. Genes Dev. 2017;31:1988–2002.
  • Ho JWK, Jung YL, Liu T, et al. Comparative analysis of metazoan chromatin organization. Nature. 2014;512:449–452.
  • Schertel C, Albarca M, Rockel-Bauer C, et al. A large-scale, in vivo transcription factor screen defines bivalent chromatin as a key property of regulatory factors mediating Drosophila wing development. Genome Res. 2015;25:514–523.
  • Schuettengruber B, Bourbon H-M, Di Croce L, et al. Genome regulation by Polycomb and Trithorax: 70 years and counting. Cell. 2017;171:34–57.
  • Choate LA, Danko CG. Poised for development. Nat Genet. 2016;48:822–823.
  • Ringrose L. Noncoding RNAs in Polycomb and Trithorax regulation: a quantitative perspective. Annu Rev Genet. 2017;51:385–411.
  • Kassis JA, Kennison JA, Tamkun JW. Polycomb and Trithorax group genes in drosophila. Genetics. 2017;206:1699–1725.
  • Akmammedov A, Geigges M, Paro R. Single vector non-leaky gene expression system for Drosophila melanogaster. Sci Rep. 2017;7:6899.
  • Sandmann T, Jakobsen JS, Furlong EEM. ChIP-on-chip protocol for genome-wide analysis of transcription factor binding in Drosophila melanogaster embryos. Nat Protoc. 2006;1:2839–2855.
  • Truax AD, Greer SF. ChIP and Re-ChIP assays: investigating interactions between regulatory proteins, histone modifications, and the DNA sequences to which they bind. In: Vancura A, editor. Transcriptional regulation. New York (NY): Springer New York; 2012. p. 175–188.
  • Cavalli G, Paro R. The Drosophila Fab-7 chromosomal element conveys epigenetic inheritance during mitosis and meiosis. Cell. 1998;93:505–518.
  • Cavalli G, Paro R. Epigenetic inheritance of active chromatin after removal of the main transactivator. Science. 1999;286:955–958.
  • Schwartz YB, Pirrotta V. Polycomb silencing mechanisms and the management of genomic programmes. Nat Rev Genet. 2007;8:9–22.
  • Gates LA, Shi J, Rohira AD, et al. Acetylation on histone H3 lysine 9 mediates a switch from transcription initiation to elongation. J Biol Chem. 2017;292:14456–14472.
  • Ng J, Hart CM, Morgan K, et al. A drosophila ESC-E(Z) protein complex is distinct from other polycomb group complexes and contains covalently modified ESC. Mol Cell Biol. 2000;20:3069–3078.
  • Casas-Vila N, Bluhm A, Sayols S, et al. The developmental proteome of Drosophila melanogaster. Genome Res. 2017;27:1273–1285.
  • Nekrasov M, Klymenko T, Fraterman S, et al. Pcl-PRC2 is needed to generate high levels of H3-K27 trimethylation at Polycomb target genes. Embo J. 2007;26:4078–4088.
  • Tie F, Prasad-Sinha J, Birve A, et al. A 1-megadalton ESC/E(Z) complex from Drosophila that contains polycomblike and RPD3. Mol Cell Biol. 2003;23:3352–3362.
  • Savla U, Benes J, Zhang J, et al. Recruitment of Drosophila Polycomb-group proteins by Polycomblike, a component of a novel protein complex in larvae. Dev Camb Engl. 2008;135:813–817.
  • O’Connell S, Wang L, Robert S, et al. Polycomblike PHD fingers mediate conserved interaction with enhancer of zeste protein. J Biol Chem. 2001;276:43065–43073.
  • Furuyama T, Banerjee R, Breen TR, et al. SIR2 is required for polycomb silencing and is associated with an E(Z) histone methyltransferase complex. Curr Biol CB. 2004;14:1812–1821.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.