Cohesin and Polycomb Proteins Functionally Interact to Control Transcription at Silenced and Active Genes

Overview

Journal PLoS Genet

Specialty Genetics

Date 2013 Jul 3

PMID 23818863

Citations 75

Authors

Cheri A Schaaf

Ziva Misulovin

Maria Gause

Amanda Koenig

David W Gohara

Audrey Watson

Dale Dorsett

Affiliations

Soon will be listed here.

Abstract

Cohesin is crucial for proper chromosome segregation but also regulates gene transcription and organism development by poorly understood mechanisms. Using genome-wide assays in Drosophila developing wings and cultured cells, we find that cohesin functionally interacts with Polycomb group (PcG) silencing proteins at both silenced and active genes. Cohesin unexpectedly facilitates binding of Polycomb Repressive Complex 1 (PRC1) to many active genes, but their binding is mutually antagonistic at silenced genes. PRC1 depletion decreases phosphorylated RNA polymerase II and mRNA at many active genes but increases them at silenced genes. Depletion of cohesin reduces long-range interactions between Polycomb Response Elements in the invected-engrailed gene complex where it represses transcription. These studies reveal a previously unrecognized role for PRC1 in facilitating productive gene transcription and provide new insights into how cohesin and PRC1 control development.

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References

Dorsett D, Strom L . The ancient and evolving roles of cohesin in gene expression and DNA repair. Curr Biol. 2012; 22(7):R240-50. PMC: 3327610. DOI: 10.1016/j.cub.2012.02.046. View

Liu T, Ortiz J, Taing L, Meyer C, Lee B, Zhang Y . Cistrome: an integrative platform for transcriptional regulation studies. Genome Biol. 2011; 12(8):R83. PMC: 3245621. DOI: 10.1186/gb-2011-12-8-r83. View

Klebes A, Sustar A, Kechris K, Li H, Schubiger G, Kornberg T . Regulation of cellular plasticity in Drosophila imaginal disc cells by the Polycomb group, trithorax group and lama genes. Development. 2005; 132(16):3753-65. DOI: 10.1242/dev.01927. View

Schwartz Y, Kahn T, Stenberg P, Ohno K, Bourgon R, Pirrotta V . Alternative epigenetic chromatin states of polycomb target genes. PLoS Genet. 2010; 6(1):e1000805. PMC: 2799325. DOI: 10.1371/journal.pgen.1000805. View

Buratowski S . Progression through the RNA polymerase II CTD cycle. Mol Cell. 2009; 36(4):541-6. PMC: 3232742. DOI: 10.1016/j.molcel.2009.10.019. View

Beisel C, Buness A, Roustan-Espinosa I, Koch B, Schmitt S, Haas S . Comparing active and repressed expression states of genes controlled by the Polycomb/Trithorax group proteins. Proc Natl Acad Sci U S A. 2007; 104(42):16615-20. PMC: 2001164. DOI: 10.1073/pnas.0701538104. View

Johnson D, Li W, Gordon D, Bhattacharjee A, Curry B, Ghosh J . Systematic evaluation of variability in ChIP-chip experiments using predefined DNA targets. Genome Res. 2008; 18(3):393-403. PMC: 2259103. DOI: 10.1101/gr.7080508. View

Papp B, Muller J . Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes Dev. 2006; 20(15):2041-54. PMC: 1536056. DOI: 10.1101/gad.388706. View

Sawarkar R, Paro R . Interpretation of developmental signaling at chromatin: the Polycomb perspective. Dev Cell. 2010; 19(5):651-61. DOI: 10.1016/j.devcel.2010.10.012. View

10.

Negre N, Hennetin J, Sun L, Lavrov S, Bellis M, White K . Chromosomal distribution of PcG proteins during Drosophila development. PLoS Biol. 2006; 4(6):e170. PMC: 1440717. DOI: 10.1371/journal.pbio.0040170. View

11.

Gause M, Webber H, Misulovin Z, Haller G, Rollins R, Eissenberg J . Functional links between Drosophila Nipped-B and cohesin in somatic and meiotic cells. Chromosoma. 2007; 117(1):51-66. PMC: 2258212. DOI: 10.1007/s00412-007-0125-5. View

12.

Quinlan A, Hall I . BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010; 26(6):841-2. PMC: 2832824. DOI: 10.1093/bioinformatics/btq033. View

13.

Tabata T, Schwartz C, Gustavson E, Ali Z, Kornberg T . Creating a Drosophila wing de novo, the role of engrailed, and the compartment border hypothesis. Development. 1995; 121(10):3359-69. DOI: 10.1242/dev.121.10.3359. View

14.

Dorsett D . Cohesin: genomic insights into controlling gene transcription and development. Curr Opin Genet Dev. 2011; 21(2):199-206. PMC: 3070859. DOI: 10.1016/j.gde.2011.01.018. View

15.

Rollins R, Korom M, Aulner N, Martens A, Dorsett D . Drosophila nipped-B protein supports sister chromatid cohesion and opposes the stromalin/Scc3 cohesion factor to facilitate long-range activation of the cut gene. Mol Cell Biol. 2004; 24(8):3100-11. PMC: 381657. DOI: 10.1128/MCB.24.8.3100-3111.2004. View

16.

Muller J, Verrijzer P . Biochemical mechanisms of gene regulation by polycomb group protein complexes. Curr Opin Genet Dev. 2009; 19(2):150-8. DOI: 10.1016/j.gde.2009.03.001. View

17.

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

18.

Schaaf C, Kwak H, Koenig A, Misulovin Z, Gohara D, Watson A . Genome-wide control of RNA polymerase II activity by cohesin. PLoS Genet. 2013; 9(3):e1003382. PMC: 3605059. DOI: 10.1371/journal.pgen.1003382. View

19.

Gambetta M, Oktaba K, Muller J . Essential role of the glycosyltransferase sxc/Ogt in polycomb repression. Science. 2009; 325(5936):93-6. DOI: 10.1126/science.1169727. View

20.

Young M, Willson T, Wakefield M, Trounson E, Hilton D, Blewitt M . ChIP-seq analysis reveals distinct H3K27me3 profiles that correlate with transcriptional activity. Nucleic Acids Res. 2011; 39(17):7415-27. PMC: 3177187. DOI: 10.1093/nar/gkr416. View