Home LiteratureArticle Details
PMID: 16547172 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Chromosome-wide gene-specific targeting of the Drosophila dosage compensation complex.

Genes & development ·Vol. 20 ·No. 7 ·2006-04-01 ·Pages 858-70

Gilfillan GD, Straub T, de Wit E, Greil F, Lamm R, van Steensel B, Becker PB

Abstract

The dosage compensation complex (DCC) of Drosophila melanogaster is capable of distinguishing the single male X from the other chromosomes in the nucleus. It selectively interacts in a discontinuous pattern with much of the X chromosome. How the DCC identifies and binds the X, including binding to the many genes that require dosage compensation, is currently unknown. To identify bound genes and attempt to isolate the targeting cues, we visualized male-specific lethal 1 (MSL1) protein binding along the X chromosome by combining chromatin immunoprecipitation with high-resolution microarrays. More than 700 binding regions for the DCC were observed, encompassing more than half the genes found on the X chromosome. In addition, several rare autosomal binding sites were identified. Essential genes are preferred targets, and genes binding high levels of DCC appear to experience the most compensation (i.e., greatest increase in expression). DCC binding clearly favors genes over intergenic regions, and binds most strongly to the 3' end of transcription units. Within the targeted genes, the DCC exhibits a strong preference for exons and coding sequences. Our results demonstrate gene-specific binding of the DCC, and identify several sequence elements that may partly direct its targeting.

MeSH Terms
Animals Binding Sites/genetics Dosage Compensation, Genetic Drosophila Proteins/metabolism Drosophila melanogaster/genetics,metabolism Genes, Insect Male Models, Genetic Nuclear Proteins/metabolism Protein Binding RNA Polymerase II/metabolism Sex Chromosomes/genetics,metabolism Transcription Factors/metabolism Transcription, Genetic
Chemicals
Drosophila Proteins Nuclear Proteins Transcription Factors msl-1 protein, Drosophila RNA Polymerase II
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Gilfillan Gregor D
Adolf-Butenandt-Institut, Molekularbiologie, Ludwig-Maximilians-Universität München, 80336 München, Germany.
Straub Tobias
de Wit Elzo
Greil Frauke
Lamm Rosemarie
van Steensel Bas
Becker Peter B
References (58)
58 references, click to expand
  1. High-resolution ChIP-chip analysis reveals that the Drosophila MSL complex selectively identifies active genes on the male X chromosome.
    Genes Dev. 2006 Apr 1;20(7):848-57 PMID: 16547173
  2. The Drosophila dosage compensation complex binds to polytene chromosomes independently of developmental changes in transcription.
    Genetics. 2006 Feb;172(2):963-74 PMID: 16079233
  3. JIL-1, a chromosomal kinase implicated in regulation of chromatin structure, associates with the male specific lethal (MSL) dosage compensation complex.
    J Cell Biol. 2000 May 29;149(5):1005-10 PMID: 10831604
  4. Activation of transcription through histone H4 acetylation by MOF, an acetyltransferase essential for dosage compensation in Drosophila.
    Mol Cell. 2000 Feb;5(2):367-75 PMID: 10882077
  5. The role of chromosomal RNAs in marking the X for dosage compensation.
    Curr Opin Genet Dev. 2000 Oct;10(5):555-61 PMID: 10980435
  6. RNA polymerase II elongation through chromatin.
    Nature. 2000 Sep 28;407(6803):471-5 PMID: 11028991
  7. 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
  8. A Bayesian framework for the analysis of microarray expression data: regularized t -test and statistical inferences of gene changes.
    Bioinformatics. 2001 Jun;17(6):509-19 PMID: 11395427
  9. 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
  10. Interactions between natural selection, recombination and gene density in the genes of Drosophila.
    Genetics. 2002 Feb;160(2):595-608 PMID: 11861564
  11. Gene expression during the life cycle of Drosophila melanogaster.
    Science. 2002 Sep 27;297(5590):2270-5 PMID: 12351791
  12. Sequence-specific targeting of Drosophila roX genes by the MSL dosage compensation complex.
    Mol Cell. 2003 Apr;11(4):977-86 PMID: 12718883
  13. 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
  14. 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
  15. Genome-wide RNAi analysis of growth and viability in Drosophila cells.
    Science. 2004 Feb 6;303(5659):832-5 PMID: 14764878
  16. 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
  17. Lifting a chromosome: dosage compensation in Drosophila melanogaster.
    FEBS Lett. 2004 Jun 1;567(1):8-14 PMID: 15165886
  18. Functional integration of the histone acetyltransferase MOF into the dosage compensation complex.
    EMBO J. 2004 Jun 2;23(11):2258-68 PMID: 15141166
  19. Evidence for large domains of similarly expressed genes in the Drosophila genome.
    J Biol. 2002;1(1):5 PMID: 12144710
  20. Cohesin relocation from sites of chromosomal loading to places of convergent transcription.
    Nature. 2004 Jul 29;430(6999):573-8 PMID: 15229615
  21. Gene loops juxtapose promoters and terminators in yeast.
    Nat Genet. 2004 Sep;36(9):1014-8 PMID: 15314641
  22. Elongation by RNA polymerase II: the short and long of it.
    Genes Dev. 2004 Oct 15;18(20):2437-68 PMID: 15489290
  23. Dosage compensation of serine-4 transfer RNA in Drosophila melanogaster.
    Genetics. 1982 Nov;102(3):525-37 PMID: 6816678
  24. (dC-dA)n.(dG-dT)n sequences have evolutionarily conserved chromosomal locations in Drosophila with implications for roles in chromosome structure and function.
    EMBO J. 1987 Jun;6(6):1781-9 PMID: 3111846
  25. Nonrandom distribution of long mono- and dinucleotide repeats in Drosophila chromosomes: correlations with dosage compensation, heterochromatin, and recombination.
    Mol Cell Biol. 1989 Mar;9(3):1173-82 PMID: 2725493
  26. 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
  27. Dosage compensation in Drosophila.
    Annu Rev Genet. 1994;28:491-521 PMID: 7893138
  28. Male-specific lethal 2, a dosage compensation gene of Drosophila, undergoes sex-specific regulation and encodes a protein with a RING finger and a metallothionein-like cysteine cluster.
    EMBO J. 1995 Jun 15;14(12):2884-95 PMID: 7796814
  29. The msl-2 dosage compensation gene of Drosophila encodes a putative DNA-binding protein whose expression is sex specifically regulated by Sex-lethal.
    Development. 1995 Oct;121(10):3245-58 PMID: 7588059
  30. The evolution of chromosomal sex determination and dosage compensation.
    Curr Biol. 1996 Feb 1;6(2):149-62 PMID: 8673462
  31. roX1 RNA paints the X chromosome of male Drosophila and is regulated by the dosage compensation system.
    Cell. 1997 Feb 21;88(4):445-57 PMID: 9038336
  32. 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
  33. Drosophila male-specific lethal-2 protein: structure/function analysis and dependence on MSL-1 for chromosome association.
    Genetics. 1997 Dec;147(4):1743-53 PMID: 9409833
  34. 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
  35. Dosage compensation in flies and worms: the ups and downs of X-chromosome regulation.
    Curr Opin Genet Dev. 1998 Apr;8(2):179-84 PMID: 9610408
  36. Facilitation of chromatin dynamics by SARs.
    Curr Opin Genet Dev. 1998 Oct;8(5):519-25 PMID: 9794825
  37. The rox1 and rox2 RNAs are essential components of the compensasome, which mediates dosage compensation in Drosophila.
    Mol Cell. 1999 Jul;4(1):117-22 PMID: 10445033
  38. The drosophila MSL complex acetylates histone H4 at lysine 16, a chromatin modification linked to dosage compensation.
    Mol Cell Biol. 2000 Jan;20(1):312-8 PMID: 10594033
  39. The genome sequence of Drosophila melanogaster.
    Science. 2000 Mar 24;287(5461):2185-95 PMID: 10731132
  40. 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
  41. X chromosome sites autonomously recruit the dosage compensation complex in Drosophila males.
    PLoS Biol. 2004 Nov;2(11):e341 PMID: 15502872
  42. Coordination of replication and transcription along a Drosophila chromosome.
    Genes Dev. 2004 Dec 15;18(24):3094-105 PMID: 15601823
  43. Characteristic low density and shear sensitivity of cross-linked chromatin containing polycomb complexes.
    Mol Cell Biol. 2005 Jan;25(1):432-9 PMID: 15601863
  44. X-inactivation profile reveals extensive variability in X-linked gene expression in females.
    Nature. 2005 Mar 17;434(7031):400-4 PMID: 15772666
  45. Chromatin mechanisms in Drosophila dosage compensation.
    Prog Mol Subcell Biol. 2005;38:123-49 PMID: 15881893
  46. Developmental regulation of the beta-globin gene locus.
    Prog Mol Subcell Biol. 2005;38:183-206 PMID: 15881896
  47. Dosage compensation in flies: mechanism, models, mystery.
    FEBS Lett. 2005 Jun 13;579(15):3258-63 PMID: 15943970
  48. Long-distance interactions between enhancers and promoters.
    FEBS J. 2005 Jul;272(13):3253-9 PMID: 15978032
  49. Sequence signature analysis of chromosome identity in three Drosophila species.
    BMC Bioinformatics. 2005;6:158 PMID: 15975141
  50. Targeting dosage compensation to the X chromosome of Drosophila males.
    Cold Spring Harb Symp Quant Biol. 2004;69:81-8 PMID: 16117636
  51. A topological interaction between cohesin rings and a circular minichromosome.
    Cell. 2005 Sep 23;122(6):849-60 PMID: 16179255
  52. X-linked genes evolve higher codon bias in Drosophila and Caenorhabditis.
    Genetics. 2005 Sep;171(1):145-55 PMID: 15965246
  53. Genome-scale profiling of histone H3.3 replacement patterns.
    Nat Genet. 2005 Oct;37(10):1090-7 PMID: 16155569
  54. The Drosophila MSL complex activates the transcription of target genes.
    Genes Dev. 2005 Oct 1;19(19):2284-8 PMID: 16204179
  55. Global regulation of X chromosomal genes by the MSL complex in Drosophila melanogaster.
    Genes Dev. 2005 Oct 1;19(19):2289-94 PMID: 16204180
  56. Stable chromosomal association of MSL2 defines a dosage-compensated nuclear compartment.
    Chromosoma. 2005 Nov;114(5):352-64 PMID: 16179989
  57. Chromatin remodeling in dosage compensation.
    Annu Rev Genet. 2005;39:615-51 PMID: 16285873
  58. Targeting determinants of dosage compensation in Drosophila.
    PLoS Genet. 2006 Feb;2(2):e5 PMID: 16462942
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
0890-9369
Published
2006-04-01
Epub
2006-00-17
Pages
858-70
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC1475731
Subset
IM
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