Home LiteratureArticle Details
PMID: 22406341 Published · ppublish English Journal Article Research Support, N.I.H., Intramural Review

Coupling polymerase pausing and chromatin landscapes for precise regulation of transcription.

Biochimica et biophysica acta ·Vol. 1819 ·No. 7 ·2012-07-00 ·Pages 700-6

Gilchrist DA, Adelman K

Abstract

Altering gene expression in response to stimuli is a pivotal mechanism through which organisms execute developmental programs and respond to changes in their environment. Packaging of promoter DNA into chromatin can greatly impact the ability of RNA polymerase II to access and transcribe a gene. Promoter chromatin environments thus play a central role in establishing transcriptional output appropriate for specific environmental conditions or developmental states. Recent genomic studies have illuminated general principles of chromatin organization and deepened our understanding of how promoter sequence and nucleosome architecture may impact gene expression. Concurrently, pausing of polymerase during early elongation has been recognized as an important event influencing transcription of genes within stimulus-responsive networks. Promoters regulated by pausing are now recognized to possess a distinct chromatin architecture that may facilitate the plasticity of gene expression in response to signaling events. Here we review advances in understanding chromatin and pausing, and explore how coupling Pol II pausing to distinct promoter architectures may help organisms achieve flexible yet precise transcriptional control. This article is part of a Special Issue entitled: Chromatin in time and space.

MeSH Terms
Animals Base Sequence Chromatin/genetics,metabolism DNA/genetics,metabolism Gene Expression Regulation Humans Nucleic Acid Conformation Promoter Regions, Genetic RNA Polymerase II/metabolism,physiology Transcription, Genetic
Chemicals
Chromatin DNA RNA Polymerase II
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Gilchrist Daniel A
Laboratory of Molecular Carcinogenesis, National Institute of Environmental Health Sciences, NIH, Research Triangle Park, NC 27709, USA. gilchristd@niehs.nih.gov
Adelman Karen
References (52)
52 references, click to expand
  1. G+C content dominates intrinsic nucleosome occupancy.
    BMC Bioinformatics. 2009 Dec 22;10:442 PMID: 20028554
  2. The RNA polymerase II molecule at the 5' end of the uninduced hsp70 gene of D. melanogaster is transcriptionally engaged.
    Cell. 1988 Sep 9;54(6):795-804 PMID: 3136931
  3. NELF and GAGA factor are linked to promoter-proximal pausing at many genes in Drosophila.
    Mol Cell Biol. 2008 May;28(10):3290-300 PMID: 18332113
  4. Promoter elements associated with RNA Pol II stalling in the Drosophila embryo.
    Proc Natl Acad Sci U S A. 2008 Jun 3;105(22):7762-7 PMID: 18505835
  5. Rapid, transcription-independent loss of nucleosomes over a large chromatin domain at Hsp70 loci.
    Cell. 2008 Jul 11;134(1):74-84 PMID: 18614012
  6. Facilitated binding of TATA-binding protein to nucleosomal DNA.
    Nature. 1994 Aug 11;370(6489):481-5 PMID: 8047170
  7. Nucleosomes are not necessary for promoter-proximal pausing in vitro on the Drosophila hsp70 promoter.
    Nucleic Acids Res. 1998 Feb 15;26(4):1051-5 PMID: 9461467
  8. Mapping and analysis of chromatin state dynamics in nine human cell types.
    Nature. 2011 May 5;473(7345):43-9 PMID: 21441907
  9. Determinants of nucleosome organization in primary human cells.
    Nature. 2011 May 22;474(7352):516-20 PMID: 21602827
  10. Removal of promoter nucleosomes by disassembly rather than sliding in vivo.
    Mol Cell. 2004 Jun 4;14(5):667-73 PMID: 15175161
  11. Nucleosome positioning as a determinant of exon recognition.
    Nat Struct Mol Biol. 2009 Sep;16(9):996-1001 PMID: 19684599
  12. ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor.
    Nature. 1994 Feb 10;367(6463):525-32 PMID: 8107823
  13. H3.3/H2A.Z double variant-containing nucleosomes mark 'nucleosome-free regions' of active promoters and other regulatory regions.
    Nat Genet. 2009 Aug;41(8):941-5 PMID: 19633671
  14. c-Myc regulates transcriptional pause release.
    Cell. 2010 Apr 30;141(3):432-45 PMID: 20434984
  15. Promoter-associated pausing in promoter architecture and postinitiation transcriptional regulation.
    Cold Spring Harb Symp Quant Biol. 1998;63:347-56 PMID: 10384299
  16. Biased chromatin signatures around polyadenylation sites and exons.
    Mol Cell. 2009 Oct 23;36(2):245-54 PMID: 19854133
  17. Nucleosome positioning modulates accessibility of regulatory proteins to the mouse mammary tumor virus promoter.
    Cell. 1990 Mar 9;60(5):719-31 PMID: 2155706
  18. Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome.
    Nature. 2007 Mar 29;446(7135):572-6 PMID: 17392789
  19. The 5' ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I.
    Nature. 1980 Aug 28;286(5776):854-60 PMID: 6774262
  20. 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
  21. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters.
    Science. 2008 Dec 19;322(5909):1845-8 PMID: 19056941
  22. Chromatin disassembly from the PHO5 promoter is essential for the recruitment of the general transcription machinery and coactivators.
    Mol Cell Biol. 2007 Sep;27(18):6372-82 PMID: 17620413
  23. RNA polymerase II interacts with the promoter region of the noninduced hsp70 gene in Drosophila melanogaster cells.
    Mol Cell Biol. 1986 Nov;6(11):3984-9 PMID: 3099167
  24. Structure and function of the human transcription elongation factor DSIF.
    J Biol Chem. 1999 Mar 19;274(12):8085-92 PMID: 10075709
  25. Unlocking the secrets of the genome.
    Nature. 2009 Jun 18;459(7249):927-30 PMID: 19536255
  26. Chromatin structure of hsp 70 genes, activated by heat shock: selective removal of histones from the coding region and their absence from the 5' region.
    Cell. 1984 Feb;36(2):423-31 PMID: 6420075
  27. Chromatin organization marks exon-intron structure.
    Nat Struct Mol Biol. 2009 Sep;16(9):990-5 PMID: 19684600
  28. High-resolution nucleosome mapping reveals transcription-dependent promoter packaging.
    Genome Res. 2010 Jan;20(1):90-100 PMID: 19846608
  29. Comprehensive analysis of the chromatin landscape in Drosophila melanogaster.
    Nature. 2011 Mar 24;471(7339):480-5 PMID: 21179089
  30. RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo.
    Nat Genet. 2007 Dec;39(12):1512-6 PMID: 17994019
  31. RNA polymerase is poised for activation across the genome.
    Nat Genet. 2007 Dec;39(12):1507-11 PMID: 17994021
  32. Nucleosomes are well positioned in exons and carry characteristic histone modifications.
    Genome Res. 2009 Oct;19(10):1732-41 PMID: 19687145
  33. DNase I hypersensitive sites in Drosophila chromatin occur at the 5' ends of regions of transcription.
    Proc Natl Acad Sci U S A. 1981 Jan;78(1):143-6 PMID: 6264428
  34. 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
  35. Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo.
    Nat Struct Mol Biol. 2009 Aug;16(8):847-52 PMID: 19620965
  36. Pausing of RNA polymerase II disrupts DNA-specified nucleosome organization to enable precise gene regulation.
    Cell. 2010 Nov 12;143(4):540-51 PMID: 21074046
  37. Dynamic regulation of nucleosome positioning in the human genome.
    Cell. 2008 Mar 7;132(5):887-98 PMID: 18329373
  38. Role of nucleosome remodeling factor NURF in transcriptional activation of chromatin.
    Mol Cell. 1997 Dec;1(1):141-50 PMID: 9659911
  39. Two strategies for gene regulation by promoter nucleosomes.
    Genome Res. 2008 Jul;18(7):1084-91 PMID: 18448704
  40. Global analysis of short RNAs reveals widespread promoter-proximal stalling and arrest of Pol II in Drosophila.
    Science. 2010 Jan 15;327(5963):335-8 PMID: 20007866
  41. The DNA-encoded nucleosome organization of a eukaryotic genome.
    Nature. 2009 Mar 19;458(7236):362-6 PMID: 19092803
  42. Systematic protein location mapping reveals five principal chromatin types in Drosophila cells.
    Cell. 2010 Oct 15;143(2):212-24 PMID: 20888037
  43. NELF-mediated stalling of Pol II can enhance gene expression by blocking promoter-proximal nucleosome assembly.
    Genes Dev. 2008 Jul 15;22(14):1921-33 PMID: 18628398
  44. Regulating RNA polymerase pausing and transcription elongation in embryonic stem cells.
    Genes Dev. 2011 Apr 1;25(7):742-54 PMID: 21460038
  45. High nucleosome occupancy is encoded at human regulatory sequences.
    PLoS One. 2010 Feb 09;5(2):e9129 PMID: 20161746
  46. A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling.
    Cell. 2009 Jul 10;138(1):114-28 PMID: 19596239
  47. Nucleosome organization in the Drosophila genome.
    Nature. 2008 May 15;453(7193):358-62 PMID: 18408708
  48. Anatomy of a hypersensitive site.
    Biochim Biophys Acta. 2004 Mar 15;1677(1-3):24-9 PMID: 15020042
  49. Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter.
    Mol Cell. 2003 Jun;11(6):1599-607 PMID: 12820972
  50. All and only CpG containing sequences are enriched in promoters abundantly bound by RNA polymerase II in multiple tissues.
    BMC Genomics. 2008 Feb 05;9:67 PMID: 18252004
  51. Purification and properties of an ATP-dependent nucleosome remodeling factor.
    Cell. 1995 Dec 15;83(6):1011-20 PMID: 8521501
  52. Transcriptional regulation by chromatin disassembly and reassembly.
    Curr Opin Genet Dev. 2007 Apr;17(2):88-93 PMID: 17307351
Article Info
Journal
Biochimica et biophysica acta
Abbr.
Biochim Biophys Acta
ISSN
0006-3002
Published
2012-07-00
Epub
2012-00-02
Pages
700-6
Language
English
Region
Netherlands
NLM ID
0217513
PMCID
PMC3371112
Subset
IM
Grants
Intramural NIH HHS · Z01 ES101987 · United States
Intramural NIH HHS · ZIA ES101987-06 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com