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PMID: 22749399 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

A bridging model for persistence of a polycomb group protein complex through DNA replication in vitro.

Molecular cell ·Vol. 46 ·No. 6 ·2012-06-29 ·Pages 784-96

Lo SM, Follmer NE, Lengsfeld BM, Madamba EV, Seong S, Grau DJ, Francis NJ

Abstract

Epigenetic regulation may involve heritable chromatin states, but how chromatin features can be inherited through DNA replication is incompletely understood. We address this question using cell-free replication of chromatin. Previously, we showed that a Polycomb group complex, PRC1, remains continuously associated with chromatin through DNA replication. Here we investigate the mechanism of persistence. We find that a single PRC1 subunit, Posterior sex combs (PSC), can reconstitute persistence through DNA replication. PSC binds nucleosomes and self-interacts, bridging nucleosomes into a stable, oligomeric structure. Within these structures, individual PSC-chromatin contacts are dynamic. Stable association of PSC with chromatin, including through DNA replication, depends on PSC-PSC interactions. Our data suggest that labile individual PSC-chromatin contacts allow passage of the DNA replication machinery while PSC-PSC interactions prevent PSC from dissociating, allowing it to rebind to replicated chromatin. This mechanism may allow inheritance of chromatin proteins including PRC1 through DNA replication to maintain chromatin states.

MeSH Terms
Animals Chromatin/metabolism Chromatin Assembly and Disassembly DNA/metabolism DNA Replication Drosophila/metabolism Drosophila Proteins/metabolism Humans Nucleosomes/metabolism Polycomb-Group Proteins Repressor Proteins/chemistry,metabolism
Chemicals
Chromatin Drosophila Proteins Nucleosomes Polycomb-Group Proteins Repressor Proteins DNA
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Lo Stanley M
Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA.
Follmer Nicole E
Lengsfeld Bettina M
Madamba Egbert V
Seong Samuel
Grau Daniel J
Francis Nicole J
References (48)
48 references, click to expand
  1. Simian virus 40 (SV40) DNA replication: SV40 large T antigen unwinds DNA containing the SV40 origin of replication.
    Proc Natl Acad Sci U S A. 1987 Jan;84(1):16-20 PMID: 3025851
  2. In vitro replication of duplex circular DNA containing the simian virus 40 DNA origin site.
    Proc Natl Acad Sci U S A. 1985 Sep;82(17):5710-4 PMID: 2994044
  3. Analysis of a polycomb group protein defines regions that link repressive activity on nucleosomal templates to in vivo function.
    Mol Cell Biol. 2005 Aug;25(15):6578-91 PMID: 16024794
  4. Transcriptional regulation by Pol II(G) involving mediator and competitive interactions of Gdown1 and TFIIF with Pol II.
    Mol Cell. 2012 Jan 13;45(1):51-63 PMID: 22244332
  5. Functional association of Gdown1 with RNA polymerase II poised on human genes.
    Mol Cell. 2012 Jan 13;45(1):38-50 PMID: 22244331
  6. RAWUL: a new ubiquitin-like domain in PRC1 ring finger proteins that unveils putative plant and worm PRC1 orthologs.
    BMC Genomics. 2008 Jun 27;9:308 PMID: 18588675
  7. SV40 DNA replication: from the A gene to a nanomachine.
    Virology. 2009 Feb 20;384(2):352-9 PMID: 19101707
  8. Native and recombinant polycomb group complexes establish a selective block to template accessibility to repress transcription in vitro.
    Mol Cell Biol. 2002 Nov;22(22):7919-28 PMID: 12391159
  9. Polycomb response elements mediate the formation of chromosome higher-order structures in the bithorax complex.
    Nat Cell Biol. 2007 Oct;9(10):1167-74 PMID: 17828248
  10. Molecular genetic analysis of Suppressor 2 of zeste identifies key functional domains.
    Genetics. 2009 Aug;182(4):999-1013 PMID: 19528329
  11. Imprinting a determined state into the chromatin of Drosophila.
    Trends Genet. 1990 Dec;6(12):416-21 PMID: 1982376
  12. PcG complexes set the stage for epigenetic inheritance of gene silencing in early S phase before replication.
    PLoS Genet. 2011 Nov;7(11):e1002370 PMID: 22072989
  13. Association of BMI1 with polycomb bodies is dynamic and requires PRC2/EZH2 and the maintenance DNA methyltransferase DNMT1.
    Mol Cell Biol. 2005 Dec;25(24):11047-58 PMID: 16314526
  14. Biochemical mechanisms of gene regulation by polycomb group protein complexes.
    Curr Opin Genet Dev. 2009 Apr;19(2):150-8 PMID: 19345089
  15. Insulators, not Polycomb response elements, are required for long-range interactions between Polycomb targets in Drosophila melanogaster.
    Mol Cell Biol. 2011 Feb;31(4):616-25 PMID: 21135119
  16. Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro.
    Nature. 1994 May 19;369(6477):207-12 PMID: 7910375
  17. Reconstitution of a functional core polycomb repressive complex.
    Mol Cell. 2001 Sep;8(3):545-56 PMID: 11583617
  18. Reconstitution of complete SV40 DNA replication with purified replication factors.
    J Biol Chem. 1994 Apr 8;269(14):10923-34 PMID: 8144677
  19. Chromatin architectural proteins.
    Chromosome Res. 2006;14(1):39-51 PMID: 16506095
  20. A core subunit of Polycomb repressive complex 1 is broadly conserved in function but not primary sequence.
    Proc Natl Acad Sci U S A. 2012 May 1;109(18):E1063-71 PMID: 22517748
  21. Propagation of silencing; recruitment and repression of naive chromatin in trans by polycomb repressed chromatin.
    Mol Cell. 2004 Feb 13;13(3):415-25 PMID: 14967148
  22. A gene complex controlling segmentation in Drosophila.
    Nature. 1978 Dec 7;276(5688):565-70 PMID: 103000
  23. Chromatin assembly during SV40 DNA replication in vitro.
    Cell. 1986 May 23;45(4):555-65 PMID: 3011272
  24. Mechanisms of polycomb gene silencing: knowns and unknowns.
    Nat Rev Mol Cell Biol. 2009 Oct;10(10):697-708 PMID: 19738629
  25. Inhibition of chromatin remodeling by polycomb group protein posterior sex combs is mechanistically distinct from nucleosome binding.
    Biochemistry. 2010 Nov 9;49(44):9438-48 PMID: 20873869
  26. A gene product required for correct initiation of segmental determination in Drosophila.
    Nature. 1981 Sep 3;293(5827):36-41 PMID: 7266657
  27. Replication of simian virus 40 origin-containing DNA in vitro with purified proteins.
    Proc Natl Acad Sci U S A. 1987 Apr;84(7):1834-8 PMID: 3031654
  28. Epigenetic inheritance during the cell cycle.
    Nat Rev Mol Cell Biol. 2009 Mar;10(3):192-206 PMID: 19234478
  29. Expression of simian virus 40 T antigen in insect cells using a baculovirus expression vector.
    Virology. 1988 Nov;167(1):72-81 PMID: 3055666
  30. Stabilization of chromatin structure by PRC1, a Polycomb complex.
    Cell. 1999 Jul 9;98(1):37-46 PMID: 10412979
  31. DNA helicase activity of SV40 large tumor antigen.
    EMBO J. 1986 Aug;5(8):1939-44 PMID: 3019672
  32. Compaction of chromatin by diverse Polycomb group proteins requires localized regions of high charge.
    Genes Dev. 2011 Oct 15;25(20):2210-21 PMID: 22012622
  33. Chromatin compaction by a polycomb group protein complex.
    Science. 2004 Nov 26;306(5701):1574-7 PMID: 15567868
  34. Drosophila genes Posterior Sex Combs and Suppressor two of zeste encode proteins with homology to the murine bmi-1 oncogene.
    Nature. 1991 Sep 26;353(6342):351-3 PMID: 1833647
  35. Polycomb group proteins: repression in 3D.
    Trends Genet. 2011 Nov;27(11):454-64 PMID: 21794944
  36. Chromatin structure and the inheritance of epigenetic information.
    Nat Rev Genet. 2010 Apr;11(4):285-96 PMID: 20300089
  37. Polycomb proteins remain bound to chromatin and DNA during DNA replication in vitro.
    Cell. 2009 Apr 3;137(1):110-22 PMID: 19303136
  38. Polycomb group protein-associated chromatin is reproduced in post-mitotic G1 phase and is required for S phase progression.
    J Biol Chem. 2008 Jul 4;283(27):18905-15 PMID: 18453536
  39. Simian virus 40 DNA replication in vitro.
    Proc Natl Acad Sci U S A. 1984 Nov;81(22):6973-7 PMID: 6095264
  40. Replication and supercoiling of simian virus 40 DNA in cell extracts from human cells.
    Mol Cell Biol. 1985 Aug;5(8):2051-60 PMID: 3018548
  41. Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro.
    Cell. 1989 Jul 14;58(1):15-25 PMID: 2546672
  42. CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing.
    Nature. 2011 Nov 3;479(7371):74-9 PMID: 21964334
  43. Phenotypic plasticity and the epigenetics of human disease.
    Nature. 2007 May 24;447(7143):433-40 PMID: 17522677
  44. A chromatin insulator driving three-dimensional Polycomb response element (PRE) contacts and Polycomb association with the chromatin fiber.
    Proc Natl Acad Sci U S A. 2011 Feb 8;108(6):2294-9 PMID: 21262819
  45. A genetic analysis of the Suppressor 2 of zeste complex of Drosophila melanogaster.
    Genetics. 1995 May;140(1):139-81 PMID: 7635282
  46. Chromatin as a potential carrier of heritable information.
    Curr Opin Cell Biol. 2010 Jun;22(3):284-90 PMID: 20299197
  47. Chromodomain-mediated oligomerization of HP1 suggests a nucleosome-bridging mechanism for heterochromatin assembly.
    Mol Cell. 2011 Jan 7;41(1):67-81 PMID: 21211724
  48. Architecture of a polycomb nucleoprotein complex.
    Mol Cell. 2006 Oct 6;24(1):91-100 PMID: 17018295
Article Info
Journal
Molecular cell
Abbr.
Mol Cell
ISSN
1097-4164
Published
2012-06-29
Pages
784-96
Language
English
Region
United States
NLM ID
9802571
PMCID
PMC3389374
Subset
IM
Grants
NIGMS NIH HHS · R01 GM078456 · United States
NIGMS NIH HHS · GM78456 · United States
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