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PMID: 19620965 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo.

Nature structural & molecular biology ·Vol. 16 ·No. 8 ·2009-08-00 ·Pages 847-52

Zhang Y, Moqtaderi Z, Rattner BP, Euskirchen G, Snyder M, Kadonaga JT, Liu XS, Struhl K

Abstract

We assess the role of intrinsic histone-DNA interactions by mapping nucleosomes assembled in vitro on genomic DNA. Nucleosomes strongly prefer yeast DNA over Escherichia coli DNA, indicating that the yeast genome evolved to favor nucleosome formation. Many yeast promoter and terminator regions intrinsically disfavor nucleosome formation, and nucleosomes assembled in vitro show strong rotational positioning. Nucleosome arrays generated by the ACF assembly factor have fewer nucleosome-free regions, reduced rotational positioning and less translational positioning than obtained by intrinsic histone-DNA interactions. Notably, nucleosomes assembled in vitro have only a limited preference for specific translational positions and do not show the pattern observed in vivo. Our results argue against a genomic code for nucleosome positioning, and they suggest that the nucleosomal pattern in coding regions arises primarily from statistical positioning from a barrier near the promoter that involves some aspect of transcriptional initiation by RNA polymerase II.

MeSH Terms
Chromatin/metabolism DNA, Bacterial/chemistry,genetics,metabolism DNA, Fungal/chemistry,genetics,metabolism Endodeoxyribonucleases/metabolism Escherichia coli/genetics Escherichia coli Proteins/genetics,metabolism Histones/genetics,metabolism Nucleosomes/metabolism Protein Binding Saccharomyces cerevisiae/genetics Saccharomyces cerevisiae Proteins/genetics,metabolism Sequence Analysis, DNA Transcription Initiation Site Transcription, Genetic
Chemicals
Chromatin DNA, Bacterial DNA, Fungal Escherichia coli Proteins Histones Nucleosomes Saccharomyces cerevisiae Proteins Endodeoxyribonucleases
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Zhang Yong
Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute and Harvard School of Public Health, Boston, Massachusetts, USA.
Moqtaderi Zarmik
Rattner Barbara P
Euskirchen Ghia
Snyder Michael
Kadonaga James T
Liu X Shirley
Struhl Kevin
References (34)
34 references, click to expand
  1. Evidence for distinct mechanisms facilitating transcript elongation through chromatin in vivo.
    EMBO J. 2004 Oct 27;23(21):4243-52 PMID: 15457216
  2. DNA bending and its relation to nucleosome positioning.
    J Mol Biol. 1985 Dec 20;186(4):773-90 PMID: 3912515
  3. Antagonistic forces that position nucleosomes in vivo.
    Nat Struct Mol Biol. 2006 Jul;13(7):633-40 PMID: 16819518
  4. Dynamics of replication-independent histone turnover in budding yeast.
    Science. 2007 Mar 9;315(5817):1405-8 PMID: 17347438
  5. Whole-genome comparison of Leu3 binding in vitro and in vivo reveals the importance of nucleosome occupancy in target site selection.
    Genome Res. 2006 Dec;16(12):1517-28 PMID: 17053089
  6. Structure of chromatin.
    Annu Rev Biochem. 1977;46:931-54 PMID: 332067
  7. A high-resolution atlas of nucleosome occupancy in yeast.
    Nat Genet. 2007 Oct;39(10):1235-44 PMID: 17873876
  8. Role of DNA sequence in nucleosome stability and dynamics.
    Q Rev Biophys. 2001 Aug;34(3):269-324 PMID: 11838235
  9. Genome-scale identification of nucleosome positions in S. cerevisiae.
    Science. 2005 Jul 22;309(5734):626-30 PMID: 15961632
  10. Histone acetylation at promoters is differentially affected by specific activators and repressors.
    Mol Cell Biol. 2001 Apr;21(8):2726-35 PMID: 11283252
  11. RNA polymerase is poised for activation across the genome.
    Nat Genet. 2007 Dec;39(12):1507-11 PMID: 17994021
  12. Dynamic regulation of nucleosome positioning in the human genome.
    Cell. 2008 Mar 7;132(5):887-98 PMID: 18329373
  13. The Swi/Snf complex is important for histone eviction during transcriptional activation and RNA polymerase II elongation in vivo.
    Mol Cell Biol. 2007 Oct;27(20):6987-95 PMID: 17709398
  14. Dynamic remodeling of individual nucleosomes across a eukaryotic genome in response to transcriptional perturbation.
    PLoS Biol. 2008 Mar 18;6(3):e65 PMID: 18351804
  15. The DNA-encoded nucleosome organization of a eukaryotic genome.
    Nature. 2009 Mar 19;458(7236):362-6 PMID: 19092803
  16. Sequence specific cleavage of DNA by micrococcal nuclease.
    Nucleic Acids Res. 1981 Jun 25;9(12):2643-58 PMID: 7279658
  17. Sequence periodicities in chicken nucleosome core DNA.
    J Mol Biol. 1986 Oct 20;191(4):659-75 PMID: 3806678
  18. Statistical positioning of nucleosomes by specific protein-binding to an upstream activating sequence in yeast.
    J Mol Biol. 1988 Nov 5;204(1):109-27 PMID: 3063825
  19. A high-resolution, nucleosome position map of C. elegans reveals a lack of universal sequence-dictated positioning.
    Genome Res. 2008 Jul;18(7):1051-63 PMID: 18477713
  20. Relationships between p63 binding, DNA sequence, transcription activity, and biological function in human cells.
    Mol Cell. 2006 Nov 17;24(4):593-602 PMID: 17188034
  21. Evidence for nucleosome depletion at active regulatory regions genome-wide.
    Nat Genet. 2004 Aug;36(8):900-5 PMID: 15247917
  22. Genome-wide distribution of yeast RNA polymerase II and its control by Sen1 helicase.
    Mol Cell. 2006 Dec 8;24(5):735-746 PMID: 17157256
  23. Chromatin assembly in vitro with purified recombinant ACF and NAP-1.
    Methods Enzymol. 2003;371:499-515 PMID: 14712724
  24. Poly(dA:dT), a ubiquitous promoter element that stimulates transcription via its intrinsic DNA structure.
    EMBO J. 1995 Jun 1;14(11):2570-9 PMID: 7781610
  25. Transcriptional noise and the fidelity of initiation by RNA polymerase II.
    Nat Struct Mol Biol. 2007 Feb;14(2):103-5 PMID: 17277804
  26. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning.
    J Mol Biol. 1998 Feb 13;276(1):19-42 PMID: 9514715
  27. Nucleosomes unfold completely at a transcriptionally active promoter.
    Mol Cell. 2003 Jun;11(6):1587-98 PMID: 12820971
  28. Yeast transcriptional regulatory mechanisms.
    Annu Rev Genet. 1995;29:651-74 PMID: 8825489
  29. Nucleosome organization in the Drosophila genome.
    Nature. 2008 May 15;453(7193):358-62 PMID: 18408708
  30. A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome.
    Genome Res. 2008 Jul;18(7):1073-83 PMID: 18550805
  31. Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter.
    Mol Cell. 2003 Jun;11(6):1599-607 PMID: 12820972
  32. Intrinsic histone-DNA interactions and low nucleosome density are important for preferential accessibility of promoter regions in yeast.
    Mol Cell. 2005 Jun 10;18(6):735-48 PMID: 15949447
  33. A genomic code for nucleosome positioning.
    Nature. 2006 Aug 17;442(7104):772-8 PMID: 16862119
  34. Evidence for eviction and rapid deposition of histones upon transcriptional elongation by RNA polymerase II.
    Mol Cell Biol. 2004 Dec;24(23):10111-7 PMID: 15542822
Article Info
Journal
Nature structural & molecular biology
Abbr.
Nat Struct Mol Biol
ISSN
1545-9985
DOI
10.1038/nsmb.1636
Published
2009-08-00
Epub
2009-00-20
Pages
847-52
Language
English
Region
United States
NLM ID
101186374
PMCID
PMC2823114
Subset
IM
Grants
NIGMS NIH HHS · R01 GM030186-27 · United States
NIGMS NIH HHS · GM 30186 · United States
NIGMS NIH HHS · GM 58272 · United States
NIGMS NIH HHS · R01 GM030186-25 · United States
NHGRI NIH HHS · R01 HG004069-03 · United States
NHGRI NIH HHS · R01 HG004069 · United States
NIGMS NIH HHS · R01 GM030186-25S1 · United States
NHGRI NIH HHS · HG 4069 · United States
NIGMS NIH HHS · R01 GM030186 · United States
NIGMS NIH HHS · R37 GM030186 · United States
NIGMS NIH HHS · R01 GM030186-28 · United States
NIGMS NIH HHS · R01 GM030186-26A1 · United States
NIGMS NIH HHS · R01 GM058272 · United States
Databases
GEO
GSE15188
Corrections
CommentIn
PMID: 20683473
External Links
PubMed source DOI: 10.1038/nsmb.1636 PMC Full Text View journal details
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