Home LiteratureArticle Details
PMID: 18408708 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Nucleosome organization in the Drosophila genome.

Nature ·Vol. 453 ·No. 7193 ·2008-05-15 ·Pages 358-62

Mavrich TN, Jiang C, Ioshikhes IP, Li X, Venters BJ, Zanton SJ, Tomsho LP, Qi J, Glaser RL, Schuster SC, Gilmour DS, Albert I, Pugh BF

Abstract

Comparative genomics of nucleosome positions provides a powerful means for understanding how the organization of chromatin and the transcription machinery co-evolve. Here we produce a high-resolution reference map of H2A.Z and bulk nucleosome locations across the genome of the fly Drosophila melanogaster and compare it to that from the yeast Saccharomyces cerevisiae. Like Saccharomyces, Drosophila nucleosomes are organized around active transcription start sites in a canonical -1, nucleosome-free region, +1 arrangement. However, Drosophila does not incorporate H2A.Z into the -1 nucleosome and does not bury its transcriptional start site in the +1 nucleosome. At thousands of genes, RNA polymerase II engages the +1 nucleosome and pauses. How the transcription initiation machinery contends with the +1 nucleosome seems to be fundamentally different across major eukaryotic lines.

MeSH Terms
Animals Conserved Sequence/genetics Drosophila melanogaster/embryology,enzymology,genetics Gene Expression Regulation/genetics Genes, Insect/genetics Genome, Insect/genetics Histones/metabolism Nucleosomes/genetics,metabolism Promoter Regions, Genetic/genetics RNA Polymerase II/metabolism Saccharomyces cerevisiae/genetics Transcription Initiation Site Transcription, Genetic/genetics
Chemicals
Histones Nucleosomes RNA Polymerase II
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
Mavrich Travis N
Center for Gene Regulation, Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, Pennsylvania 16802, USA.
Jiang Cizhong
Ioshikhes Ilya P
Li Xiaoyong
Venters Bryan J
Zanton Sara J
Tomsho Lynn P
Qi Ji
Glaser Robert L
Schuster Stephan C
Gilmour David S
Albert Istvan
Pugh B Franklin
References (46)
46 references, click to expand
  1. Direct cloning of DNA that interacts in vivo with a specific protein: application to RNA polymerase II and sites of pausing in Drosophila.
    Nucleic Acids Res. 1998 Feb 15;26(4):919-24 PMID: 9461448
  2. Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome.
    Nature. 2007 Mar 29;446(7135):572-6 PMID: 17392789
  3. Control of transcription through intragenic patterns of nucleosome composition.
    Cell. 2005 Dec 29;123(7):1187-90 PMID: 16377560
  4. 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
  5. Genome-scale identification of nucleosome positions in S. cerevisiae.
    Science. 2005 Jul 22;309(5734):626-30 PMID: 15961632
  6. Histone replacement marks the boundaries of cis-regulatory domains.
    Science. 2007 Mar 9;315(5817):1408-11 PMID: 17347439
  7. Genome sequencing in microfabricated high-density picolitre reactors.
    Nature. 2005 Sep 15;437(7057):376-80 PMID: 16056220
  8. Nucleosome positions predicted through comparative genomics.
    Nat Genet. 2006 Oct;38(10):1210-5 PMID: 16964265
  9. Imaging Drosophila gene activation and polymerase pausing in vivo.
    Nature. 2007 Nov 8;450(7167):198-202 PMID: 17994086
  10. Transcription factors that activate the Ultrabithorax promoter in developmentally staged extracts.
    Cell. 1988 Jun 3;53(5):699-711 PMID: 2897243
  11. Statistical distributions of nucleosomes: nonrandom locations by a stochastic mechanism.
    Nucleic Acids Res. 1988 Jul 25;16(14A):6677-90 PMID: 3399412
  12. Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures.
    Nature. 2007 Nov 8;450(7167):219-32 PMID: 17994088
  13. Structural basis of transcription: an RNA polymerase II elongation complex at 3.3 A resolution.
    Science. 2001 Jun 8;292(5523):1876-82 PMID: 11313499
  14. The role of histone H2Av variant replacement and histone H4 acetylation in the establishment of Drosophila heterochromatin.
    Genes Dev. 2005 Jan 1;19(1):65-76 PMID: 15630020
  15. TFIID sequence recognition of the initiator and sequences farther downstream in Drosophila class II genes.
    Genes Dev. 1994 Apr 1;8(7):830-42 PMID: 7926771
  16. Isolation of cDNAs encoding the Drosophila GAGA transcription factor.
    Mol Cell Biol. 1993 Dec;13(12):7961-70 PMID: 7504178
  17. Preferential occupancy of histone variant H2AZ at inactive promoters influences local histone modifications and chromatin remodeling.
    Proc Natl Acad Sci U S A. 2005 Dec 20;102(51):18385-90 PMID: 16344463
  18. 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
  19. Temporal regulation of foregut development by HTZ-1/H2A.Z and PHA-4/FoxA.
    PLoS Genet. 2006 Sep 29;2(9):e161 PMID: 17009877
  20. A high-resolution atlas of nucleosome occupancy in yeast.
    Nat Genet. 2007 Oct;39(10):1235-44 PMID: 17873876
  21. Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss.
    Cell. 2005 Oct 21;123(2):219-31 PMID: 16239141
  22. Global analysis of patterns of gene expression during Drosophila embryogenesis.
    Genome Biol. 2007;8(7):R145 PMID: 17645804
  23. NELF and DSIF cause promoter proximal pausing on the hsp70 promoter in Drosophila.
    Genes Dev. 2003 Jun 1;17(11):1402-14 PMID: 12782658
  24. A chromatin landmark and transcription initiation at most promoters in human cells.
    Cell. 2007 Jul 13;130(1):77-88 PMID: 17632057
  25. Genome-scale profiling of histone H3.3 replacement patterns.
    Nat Genet. 2005 Oct;37(10):1090-7 PMID: 16155569
  26. RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo.
    Nat Genet. 2007 Dec;39(12):1512-6 PMID: 17994019
  27. RNA polymerase is poised for activation across the genome.
    Nat Genet. 2007 Dec;39(12):1507-11 PMID: 17994021
  28. The MTE, a new core promoter element for transcription by RNA polymerase II.
    Genes Dev. 2004 Jul 1;18(13):1606-17 PMID: 15231738
  29. High-resolution profiling of histone methylations in the human genome.
    Cell. 2007 May 18;129(4):823-37 PMID: 17512414
  30. Sequence structure of human nucleosome DNA.
    J Biomol Struct Dyn. 2006 Aug;24(1):43-8 PMID: 16780374
  31. Activator-dependent regulation of transcriptional pausing on nucleosomal templates.
    Genes Dev. 1996 Jun 15;10(12):1479-90 PMID: 8666232
  32. The location of nucleosomes in chromatin: specific or statistical.
    Nature. 1981 Aug 13;292(5824):579-80 PMID: 7254354
  33. Cluster analysis and display of genome-wide expression patterns.
    Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):14863-8 PMID: 9843981
  34. Anything else but GAGA: a nonhistone protein complex reshapes chromatin structure.
    Trends Genet. 2004 Jan;20(1):15-22 PMID: 14698615
  35. RSC exploits histone acetylation to abrogate the nucleosomal block to RNA polymerase II elongation.
    Mol Cell. 2006 Nov 3;24(3):481-7 PMID: 17081996
  36. A highly purified RNA polymerase II elongation control system.
    J Biol Chem. 2001 Nov 9;276(45):42601-9 PMID: 11553615
  37. The replacement histone H2A.Z in a hyperacetylated form is a feature of active genes in the chicken.
    Nucleic Acids Res. 2005 Oct 04;33(17):5633-9 PMID: 16204459
  38. Disruption of downstream chromatin directed by a transcriptional activator.
    Genes Dev. 1997 Dec 1;11(23):3116-21 PMID: 9389644
  39. An integrated gene annotation and transcriptional profiling approach towards the full gene content of the Drosophila genome.
    Genome Biol. 2003;5(1):R3 PMID: 14709175
  40. Histone H2A.Z is widely but nonrandomly distributed in chromosomes of Drosophila melanogaster.
    J Biol Chem. 2000 Jul 28;275(30):23267-72 PMID: 10801889
  41. The downstream promoter element DPE appears to be as widely used as the TATA box in Drosophila core promoters.
    Mol Cell Biol. 2000 Jul;20(13):4754-64 PMID: 10848601
  42. Nucleosomes can form a polar barrier to transcript elongation by RNA polymerase II.
    Mol Cell. 2006 Nov 3;24(3):469-79 PMID: 17081995
  43. Genome-wide map of nucleosome acetylation and methylation in yeast.
    Cell. 2005 Aug 26;122(4):517-27 PMID: 16122420
  44. Histone variant H2A.Z marks the 5' ends of both active and inactive genes in euchromatin.
    Cell. 2005 Oct 21;123(2):233-48 PMID: 16239142
  45. Nucleosome DNA sequence pattern revealed by multiple alignment of experimentally mapped sequences.
    J Mol Biol. 1996 Sep 20;262(2):129-39 PMID: 8831784
  46. Flexibility and constraint in the nucleosome core landscape of Caenorhabditis elegans chromatin.
    Genome Res. 2006 Dec;16(12):1505-16 PMID: 17038564
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
DOI
10.1038/nature06929
Published
2008-05-15
Epub
2008-00-13
Pages
358-62
Language
English
Region
England
NLM ID
0410462
PMCID
PMC2735122
Subset
IM
Grants
NHGRI NIH HHS · HG004160 · United States
NIGMS NIH HHS · GM47477 · United States
NHGRI NIH HHS · R01 HG004160 · United States
NIGMS NIH HHS · R01 GM047477 · United States
NHGRI NIH HHS · R01 HG004160-01A1 · United States
External Links
PubMed source DOI: 10.1038/nature06929 PMC Full Text View journal details
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: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2