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PMID: 16547173 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

High-resolution ChIP-chip analysis reveals that the Drosophila MSL complex selectively identifies active genes on the male X chromosome.

Genes & development ·Vol. 20 ·No. 7 ·2006-04-01 ·Pages 848-57

Alekseyenko AA, Larschan E, Lai WR, Park PJ, Kuroda MI

Abstract

X-chromosome dosage compensation in Drosophila requires the male-specific lethal (MSL) complex, which up-regulates gene expression from the single male X chromosome. Here, we define X-chromosome-specific MSL binding at high resolution in two male cell lines and in late-stage embryos. We find that the MSL complex is highly enriched over most expressed genes, with binding biased toward the 3' end of transcription units. The binding patterns are largely similar in the distinct cell types, with approximately 600 genes clearly bound in all three cases. Genes identified as clearly bound in one cell type and not in another indicate that attraction of MSL complex correlates with expression state. Thus, sequence alone is not sufficient to explain MSL targeting. We propose that the MSL complex recognizes most X-linked genes, but only in the context of chromatin factors or modifications indicative of active transcription. Distinguishing expressed genes from the bulk of the genome is likely to be an important function common to many chromatin organizing and modifying activities.

MeSH Terms
Animals Animals, Genetically Modified Base Sequence Binding Sites/genetics Chromatin Immunoprecipitation DNA/genetics,metabolism Dosage Compensation, Genetic Drosophila/genetics,metabolism Drosophila Proteins/chemistry,genetics,metabolism Female Gene Expression Profiling Genes, Insect Male Multiprotein Complexes Nuclear Proteins/chemistry,genetics,metabolism Oligonucleotide Array Sequence Analysis Recombinant Fusion Proteins/chemistry,genetics,metabolism Sex Chromosomes/genetics,metabolism Transcription Factors/chemistry,genetics,metabolism
Chemicals
Drosophila Proteins Multiprotein Complexes Nuclear Proteins Recombinant Fusion Proteins Transcription Factors msl-3 protein, Drosophila DNA
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Alekseyenko Artyom A
Howard Hughes Medical Institute, Brigham and Women's Hospital, Boston, Massachusetts 02115, USA.
Larschan Erica
Lai Weil R
Park Peter J
Kuroda Mitzi I
References (36)
36 references, click to expand
  1. Male-specific lethal complex of Drosophila targets activated regions of the X chromosome for chromatin remodeling.
    Proc Natl Acad Sci U S A. 2003 Jul 8;100(14):8287-91 PMID: 12829796
  2. The MSL complex levels are critical for its correct targeting to the chromosomes in Drosophila melanogaster.
    Chromosoma. 2003 Oct;112(3):103-15 PMID: 14579126
  3. Multiple classes of MSL binding sites target dosage compensation to the X chromosome of Drosophila.
    Curr Biol. 2004 Mar 23;14(6):481-7 PMID: 15043812
  4. Lifting a chromosome: dosage compensation in Drosophila melanogaster.
    FEBS Lett. 2004 Jun 1;567(1):8-14 PMID: 15165886
  5. Sequence-specific targeting of MSL complex regulates transcription of the roX RNA genes.
    EMBO J. 2004 Jul 21;23(14):2853-61 PMID: 15229655
  6. Transposition of cloned P elements into Drosophila germ line chromosomes.
    Science. 1982 Oct 22;218(4570):341-7 PMID: 6289435
  7. Histone H4 isoforms acetylated at specific lysine residues define individual chromosomes and chromatin domains in Drosophila polytene nuclei.
    Cell. 1992 Apr 17;69(2):375-84 PMID: 1568251
  8. Acetylated histone H4 on the male X chromosome is associated with dosage compensation in Drosophila.
    Genes Dev. 1994 Jan;8(1):96-104 PMID: 8288132
  9. Molecular characterization of the male-specific lethal-3 gene and investigations of the regulation of dosage compensation in Drosophila.
    Development. 1995 Feb;121(2):463-75 PMID: 7768187
  10. mof, a putative acetyl transferase gene related to the Tip60 and MOZ human genes and to the SAS genes of yeast, is required for dosage compensation in Drosophila.
    EMBO J. 1997 Apr 15;16(8):2054-60 PMID: 9155031
  11. Co-localization of Polycomb protein and GAGA factor on regulatory elements responsible for the maintenance of homeotic gene expression.
    EMBO J. 1997 Jun 16;16(12):3621-32 PMID: 9218803
  12. Complex formation by the Drosophila MSL proteins: role of the MSL2 RING finger in protein complex assembly.
    EMBO J. 1998 Sep 15;17(18):5409-17 PMID: 9736618
  13. Epigenetic spreading of the Drosophila dosage compensation complex from roX RNA genes into flanking chromatin.
    Cell. 1999 Aug 20;98(4):513-22 PMID: 10481915
  14. X chromosome sites autonomously recruit the dosage compensation complex in Drosophila males.
    PLoS Biol. 2004 Nov;2(11):e341 PMID: 15502872
  15. A novel domain in Set2 mediates RNA polymerase II interaction and couples histone H3 K36 methylation with transcript elongation.
    Mol Cell Biol. 2005 Apr;25(8):3305-16 PMID: 15798214
  16. Involvement of human MOF in ATM function.
    Mol Cell Biol. 2005 Jun;25(12):5292-305 PMID: 15923642
  17. hMOF histone acetyltransferase is required for histone H4 lysine 16 acetylation in mammalian cells.
    Mol Cell Biol. 2005 Aug;25(15):6798-810 PMID: 16024812
  18. A high-resolution map of active promoters in the human genome.
    Nature. 2005 Aug 11;436(7052):876-80 PMID: 15988478
  19. Genome-scale profiling of histone H3.3 replacement patterns.
    Nat Genet. 2005 Oct;37(10):1090-7 PMID: 16155569
  20. The Drosophila MSL complex activates the transcription of target genes.
    Genes Dev. 2005 Oct 1;19(19):2284-8 PMID: 16204179
  21. Global regulation of X chromosomal genes by the MSL complex in Drosophila melanogaster.
    Genes Dev. 2005 Oct 1;19(19):2289-94 PMID: 16204180
  22. A human protein complex homologous to the Drosophila MSL complex is responsible for the majority of histone H4 acetylation at lysine 16.
    Mol Cell Biol. 2005 Nov;25(21):9175-88 PMID: 16227571
  23. Dimethylation of histone H3 at lysine 36 demarcates regulatory and nonregulatory chromatin genome-wide.
    Mol Cell Biol. 2005 Nov;25(21):9447-59 PMID: 16227595
  24. Chipper: discovering transcription-factor targets from chromatin immunoprecipitation microarrays using variance stabilization.
    Genome Biol. 2005;6(11):R96 PMID: 16277751
  25. Chromatin remodeling in dosage compensation.
    Annu Rev Genet. 2005;39:615-51 PMID: 16285873
  26. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription.
    Cell. 2005 Nov 18;123(4):581-92 PMID: 16286007
  27. Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex.
    Cell. 2005 Nov 18;123(4):593-605 PMID: 16286008
  28. The Drosophila dosage compensation complex binds to polytene chromosomes independently of developmental changes in transcription.
    Genetics. 2006 Feb;172(2):963-74 PMID: 16079233
  29. Genome-wide location and function of DNA binding proteins.
    Science. 2000 Dec 22;290(5500):2306-9 PMID: 11125145
  30. Association and spreading of the Drosophila dosage compensation complex from a discrete roX1 chromatin entry site.
    EMBO J. 2001 May 1;20(9):2236-45 PMID: 11331589
  31. The tandem affinity purification (TAP) method: a general procedure of protein complex purification.
    Methods. 2001 Jul;24(3):218-29 PMID: 11403571
  32. Linking global histone acetylation to the transcription enhancement of X-chromosomal genes in Drosophila males.
    J Biol Chem. 2001 Aug 24;276(34):31483-6 PMID: 11445559
  33. Extent of chromatin spreading determined by roX RNA recruitment of MSL proteins.
    Science. 2002 Nov 22;298(5598):1620-3 PMID: 12446910
  34. Chromatin remodeling protein Chd1 interacts with transcription elongation factors and localizes to transcribed genes.
    EMBO J. 2003 Apr 15;22(8):1846-56 PMID: 12682017
  35. Local spreading of MSL complexes from roX genes on the Drosophila X chromosome.
    Genes Dev. 2003 Jun 1;17(11):1334-9 PMID: 12782651
  36. The Drosophila roX1 RNA gene can overcome silent chromatin by recruiting the male-specific lethal dosage compensation complex.
    Genetics. 2003 Jun;164(2):565-74 PMID: 12807777
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
0890-9369
Published
2006-04-01
Epub
2006-00-17
Pages
848-57
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC1472287
Subset
IM
Grants
NIGMS NIH HHS · GM67825 · United States
NIGMS NIH HHS · R01 GM045744 · United States
NIGMS NIH HHS · GM45744 · United States
NIGMS NIH HHS · K25 GM067825 · United States
NIGMS NIH HHS · R37 GM045744 · United States
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