TrxG and PcG Proteins but Not Methylated Histones Remain Associated with DNA Through Replication

Overview

Journal Cell

Publisher Cell Press

Specialty Cell Biology

Date 2012 Aug 28

PMID 22921915

Citations 150

Authors

Svetlana Petruk

Yurii Sedkov

Danika M Johnston

Jacob W Hodgson

Kathryn L Black

Sina K Kovermann

Samantha Beck

Eli Canaani

Hugh W Brock

Alexander Mazo

Affiliations

Soon will be listed here.

Abstract

Propagation of gene-expression patterns through the cell cycle requires the existence of an epigenetic mark that re-establishes the chromatin architecture of the parental cell in the daughter cells. We devised assays to determine which potential epigenetic marks associate with epigenetic maintenance elements during DNA replication in Drosophila embryos. Histone H3 trimethylated at lysines 4 or 27 is present during transcription but, surprisingly, is replaced by nonmethylated H3 following DNA replication. Methylated H3 is detected on DNA only in nuclei not in S phase. In contrast, the TrxG and PcG proteins Trithorax and Enhancer-of-Zeste, which are H3K4 and H3K27 methylases, and Polycomb continuously associate with their response elements on the newly replicated DNA. We suggest that histone modification enzymes may re-establish the histone code on newly assembled unmethylated histones and thus may act as epigenetic marks.

Citing Articles

Increased levels of lagging strand polymerase α in an adult stem cell lineage affect replication-coupled histone incorporation.

Davis B, Snedeker J, Ranjan R, Wooten M, Barton S, Blundon J Sci Adv. 2025; 11(9):eadu6799.

PMID: 40020063 PMC: 11870066. DOI: 10.1126/sciadv.adu6799.

Developmental signals control chromosome segregation fidelity during pluripotency and neurogenesis by modulating replicative stress.

De Jaime-Soguero A, Hattemer J, Bufe A, Haas A, van den Berg J, van Batenburg V Nat Commun. 2024; 15(1):7404.

PMID: 39191776 PMC: 11350214. DOI: 10.1038/s41467-024-51821-9.

Reduced Levels of Lagging Strand Polymerases Shape Stem Cell Chromatin.

Snedeker J, Davis B, Ranjan R, Wooten M, Blundon J, Chen X bioRxiv. 2024; .

PMID: 38746451 PMC: 11092439. DOI: 10.1101/2024.04.26.591383.

An emerging paradigm in epigenetic marking: coordination of transcription and replication.

Fenstermaker T, Petruk S, Mazo A Transcription. 2024; 15(1-2):22-37.

PMID: 38378467 PMC: 11093037. DOI: 10.1080/21541264.2024.2316965.

RNA polymerase II associates with active genes during DNA replication.

Fenstermaker T, Petruk S, Kovermann S, Brock H, Mazo A Nature. 2023; 620(7973):426-433.

PMID: 37468626 DOI: 10.1038/s41586-023-06341-9.

References

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

Fonseca J, Steffen P, Muller S, Lu J, Sawicka A, Seiser C . In vivo Polycomb kinetics and mitotic chromatin binding distinguish stem cells from differentiated cells. Genes Dev. 2012; 26(8):857-71. PMC: 3337459. DOI: 10.1101/gad.184648.111. View

Fanti L, Perrini B, Piacentini L, Berloco M, Marchetti E, Palumbo G . The trithorax group and Pc group proteins are differentially involved in heterochromatin formation in Drosophila. Chromosoma. 2007; 117(1):25-39. DOI: 10.1007/s00412-007-0123-7. View

Krajewski W, Nakamura T, Mazo A, Canaani E . A motif within SET-domain proteins binds single-stranded nucleic acids and transcribed and supercoiled DNAs and can interfere with assembly of nucleosomes. Mol Cell Biol. 2005; 25(5):1891-9. PMC: 549386. DOI: 10.1128/MCB.25.5.1891-1899.2005. 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

Deal R, Henikoff J, Henikoff S . Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science. 2010; 328(5982):1161-4. PMC: 2879085. DOI: 10.1126/science.1186777. View

Floer M, Wang X, Prabhu V, Berrozpe G, Narayan S, Spagna D . A RSC/nucleosome complex determines chromatin architecture and facilitates activator binding. Cell. 2010; 141(3):407-18. PMC: 3032599. DOI: 10.1016/j.cell.2010.03.048. View

Shermoen A, McCleland M, OFarrell P . Developmental control of late replication and S phase length. Curr Biol. 2010; 20(23):2067-77. PMC: 3108027. DOI: 10.1016/j.cub.2010.10.021. View

Henikoff S, Shilatifard A . Histone modification: cause or cog?. Trends Genet. 2011; 27(10):389-96. DOI: 10.1016/j.tig.2011.06.006. View

10.

Lanzuolo C, Lo Sardo F, Diamantini A, Orlando V . PcG complexes set the stage for epigenetic inheritance of gene silencing in early S phase before replication. PLoS Genet. 2011; 7(11):e1002370. PMC: 3207895. DOI: 10.1371/journal.pgen.1002370. View

11.

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

12.

Corpet A, Almouzni G . Making copies of chromatin: the challenge of nucleosomal organization and epigenetic information. Trends Cell Biol. 2008; 19(1):29-41. DOI: 10.1016/j.tcb.2008.10.002. View

13.

Jackson V, Shires A, Tanphaichitr N, Chalkley R . Modifications to histones immediately after synthesis. J Mol Biol. 1976; 104(2):471-83. DOI: 10.1016/0022-2836(76)90282-5. View

14.

Sharif J, Muto M, Takebayashi S, Suetake I, Iwamatsu A, Endo T . The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature. 2007; 450(7171):908-12. DOI: 10.1038/nature06397. View

15.

Hernandez-Munoz I, Taghavi P, Kuijl C, Neefjes J, van Lohuizen M . Association of BMI1 with polycomb bodies is dynamic and requires PRC2/EZH2 and the maintenance DNA methyltransferase DNMT1. Mol Cell Biol. 2005; 25(24):11047-58. PMC: 1316945. DOI: 10.1128/MCB.25.24.11047-11058.2005. View

16.

Ng R, Gurdon J . Epigenetic inheritance of cell differentiation status. Cell Cycle. 2008; 7(9):1173-7. DOI: 10.4161/cc.7.9.5791. View

17.

Ringrose L, Paro R . Polycomb/Trithorax response elements and epigenetic memory of cell identity. Development. 2006; 134(2):223-32. DOI: 10.1242/dev.02723. View

18.

Huen M, Sy S, van Deursen J, Chen J . Direct interaction between SET8 and proliferating cell nuclear antigen couples H4-K20 methylation with DNA replication. J Biol Chem. 2008; 283(17):11073-7. PMC: 2431066. DOI: 10.1074/jbc.C700242200. View

19.

Dietzel S, Niemann H, Bruckner B, Maurange C, Paro R . The nuclear distribution of Polycomb during Drosophila melanogaster development shown with a GFP fusion protein. Chromosoma. 1999; 108(2):83-94. DOI: 10.1007/s004120050355. View

20.

Muller J, Hart C, Francis N, Vargas M, Sengupta A, Wild B . Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell. 2002; 111(2):197-208. DOI: 10.1016/s0092-8674(02)00976-5. View