Comparing Active and Repressed Expression States of Genes Controlled by the Polycomb/Trithorax Group Proteins

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2007 Oct 9

PMID 17921257

Citations 39

Authors

Christian Beisel

Andreas Buness

Ian M Roustan-Espinosa

Britta Koch

Sabine Schmitt

Stefan A Haas

Marc Hild

Tomonori Katsuyama

Renato Paro

Affiliations

Soon will be listed here.

Abstract

Drosophila Polycomb group (PcG) and Trithorax group (TrxG) proteins are responsible for the maintenance of stable transcription patterns of many developmental regulators, such as the homeotic genes. We have used ChIP-on-chip to compare the distribution of several PcG/TrxG proteins, as well as histone modifications in active and repressed genes across the two homeotic complexes ANT-C and BX-C. Our data indicate the colocalization of the Polycomb repressive complex 1 (PRC1) with Trx and the DNA binding protein Pleiohomeotic (Pho) at discrete sequence elements as well as significant chromatin assembly differences in active and inactive regions. Trx binds to the promoters of active genes and noncoding transcripts. Most strikingly, in the active state, Pho covers extended chromatin domains over many kilobases. This feature of Pho, observed on many polytene chromosome puffs, reflects a previously undescribed function. At the hsp70 gene, we demonstrate in mutants that Pho is required for transcriptional recovery after heat shock. Besides its presumptive function in recruiting PcG complexes to their site of action, our results now uncover that Pho plays an additional role in the repression of already induced genes.

Citing Articles

Transcriptionally active chromatin loops contain both 'active' and 'inactive' histone modifications that exhibit exclusivity at the level of nucleosome clusters.

Koestler S, Ball M, Muresan L, Dinakaran V, White R Epigenetics Chromatin. 2024; 17(1):8.

PMID: 38528624 PMC: 10962081. DOI: 10.1186/s13072-024-00535-9.

Kinome-Wide RNAi Screen Uncovers Role of Ballchen in Maintenance of Gene Activation by Trithorax Group in .

Khan M, Akhtar J, Umer Z, Shaheen N, Shaukat A, Munir M Front Cell Dev Biol. 2021; 9:637873.

PMID: 33748127 PMC: 7973098. DOI: 10.3389/fcell.2021.637873.

Genome-wide RNAi screen in Drosophila reveals Enok as a novel trithorax group regulator.

Umer Z, Akhtar J, Khan M, Shaheen N, Abdul Haseeb M, Mazhar K Epigenetics Chromatin. 2019; 12(1):55.

PMID: 31547845 PMC: 6757429. DOI: 10.1186/s13072-019-0301-x.

Signalling crosstalk during early tumorigenesis in the absence of Polycomb silencing.

Beira J, Torres J, Paro R PLoS Genet. 2018; 14(1):e1007187.

PMID: 29357360 PMC: 5794193. DOI: 10.1371/journal.pgen.1007187.

Pho dynamically interacts with Spt5 to facilitate transcriptional switches at the hsp70 locus.

Pereira A, Paro R Epigenetics Chromatin. 2017; 10(1):57.

PMID: 29208012 PMC: 5718073. DOI: 10.1186/s13072-017-0166-9.

References

Petruk S, Sedkov Y, Riley K, Hodgson J, Schweisguth F, Hirose S . Transcription of bxd noncoding RNAs promoted by trithorax represses Ubx in cis by transcriptional interference. Cell. 2006; 127(6):1209-21. PMC: 1866366. DOI: 10.1016/j.cell.2006.10.039. View

Guenther M, Jenner R, Chevalier B, Nakamura T, Croce C, Canaani E . Global and Hox-specific roles for the MLL1 methyltransferase. Proc Natl Acad Sci U S A. 2005; 102(24):8603-8. PMC: 1150839. DOI: 10.1073/pnas.0503072102. View

Mohd-Sarip A, Cleard F, Mishra R, Karch F, Verrijzer C . Synergistic recognition of an epigenetic DNA element by Pleiohomeotic and a Polycomb core complex. Genes Dev. 2005; 19(15):1755-60. PMC: 1182336. DOI: 10.1101/gad.347005. View

Rastelli L, Chan C, Pirrotta V . Related chromosome binding sites for zeste, suppressors of zeste and Polycomb group proteins in Drosophila and their dependence on Enhancer of zeste function. EMBO J. 1993; 12(4):1513-22. PMC: 413364. DOI: 10.1002/j.1460-2075.1993.tb05795.x. View

Klymenko T, Papp B, Fischle W, Kocher T, Schelder M, Fritsch C . A Polycomb group protein complex with sequence-specific DNA-binding and selective methyl-lysine-binding activities. Genes Dev. 2006; 20(9):1110-22. PMC: 1472471. DOI: 10.1101/gad.377406. View

Cao R, Tsukada Y, Zhang Y . Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol Cell. 2005; 20(6):845-54. DOI: 10.1016/j.molcel.2005.12.002. View

Klymenko T, Muller J . The histone methyltransferases Trithorax and Ash1 prevent transcriptional silencing by Polycomb group proteins. EMBO Rep. 2004; 5(4):373-7. PMC: 1299022. DOI: 10.1038/sj.embor.7400111. View

Schmitt S, Prestel M, Paro R . Intergenic transcription through a polycomb group response element counteracts silencing. Genes Dev. 2005; 19(6):697-708. PMC: 1065723. DOI: 10.1101/gad.326205. View

Lavrov S, Dejardin J, Cavalli G . Combined immunostaining and FISH analysis of polytene chromosomes. Methods Mol Biol. 2004; 247:289-303. DOI: 10.1385/1-59259-665-7:289. View

10.

Ringrose L, Rehmsmeier M, Dura J, Paro R . Genome-wide prediction of Polycomb/Trithorax response elements in Drosophila melanogaster. Dev Cell. 2003; 5(5):759-71. DOI: 10.1016/s1534-5807(03)00337-x. View

11.

Orlando V, Jane E, Chinwalla V, Harte P, Paro R . Binding of trithorax and Polycomb proteins to the bithorax complex: dynamic changes during early Drosophila embryogenesis. EMBO J. 1998; 17(17):5141-50. PMC: 1170842. DOI: 10.1093/emboj/17.17.5141. View

12.

Schwartz Y, Kahn T, Nix D, Li X, Bourgon R, Biggin M . Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nat Genet. 2006; 38(6):700-5. DOI: 10.1038/ng1817. View

13.

Ringrose L, Ehret H, Paro R . Distinct contributions of histone H3 lysine 9 and 27 methylation to locus-specific stability of polycomb complexes. Mol Cell. 2004; 16(4):641-53. DOI: 10.1016/j.molcel.2004.10.015. View

14.

Levine S, King I, Kingston R . Division of labor in polycomb group repression. Trends Biochem Sci. 2004; 29(9):478-85. DOI: 10.1016/j.tibs.2004.07.007. View

15.

Francis N, Saurin A, Shao Z, Kingston R . Reconstitution of a functional core polycomb repressive complex. Mol Cell. 2001; 8(3):545-56. DOI: 10.1016/s1097-2765(01)00316-1. View

16.

Hsieh J, Cheng E, Korsmeyer S . Taspase1: a threonine aspartase required for cleavage of MLL and proper HOX gene expression. Cell. 2003; 115(3):293-303. DOI: 10.1016/s0092-8674(03)00816-x. View

17.

Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P . Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science. 2002; 298(5595):1039-43. DOI: 10.1126/science.1076997. View

18.

Cavalli G, Paro R . Epigenetic inheritance of active chromatin after removal of the main transactivator. Science. 1999; 286(5441):955-8. DOI: 10.1126/science.286.5441.955. View

19.

Kahn T, Schwartz Y, Dellino G, Pirrotta V . Polycomb complexes and the propagation of the methylation mark at the Drosophila ubx gene. J Biol Chem. 2006; 281(39):29064-75. DOI: 10.1074/jbc.M605430200. View

20.

Ng H, Robert F, Young R, Struhl K . Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell. 2003; 11(3):709-19. DOI: 10.1016/s1097-2765(03)00092-3. View