Home LiteratureArticle Details
PMID: 16079233 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

The Drosophila dosage compensation complex binds to polytene chromosomes independently of developmental changes in transcription.

Genetics ·Vol. 172 ·No. 2 ·2006-02-00 ·Pages 963-74

Kotlikova IV, Demakova OV, Semeshin VF, Shloma VV, Boldyreva LV, Kuroda MI, Zhimulev IF

Abstract

In Drosophila, the dosage compensation complex (DCC) mediates upregulation of transcription from the single male X chromosome. Despite coating the polytene male X, the DCC pattern looks discontinuous and probably reflects DCC dynamic associations with genes active at a given moment of development in a salivary gland. To test this hypothesis, we compared binding patterns of the DCC and of the elongating form of RNA polymerase II (PolIIo). We found that, unlike PolIIo, the DCC demonstrates a stable banded pattern throughout larval development and escapes binding to a subset of transcriptionally active areas, including developmental puffs. Moreover, these proteins are not completely colocalized at the electron microscopy level. These data combined imply that simple recognition of PolII machinery or of general features of active chromatin is either insufficient or not involved in DCC recruitment to its targets. We propose that DCC-mediated site-specific upregulation of transcription is not the fate of all active X-linked genes in males. Additionally, we found that DCC subunit MLE associates dynamically with developmental and heat-shock-induced puffs and, surprisingly, with those developing within DCC-devoid regions of the male X, thus resembling the PolIIo pattern. These data imply that, independently of other MSL proteins, the RNA-helicase MLE might participate in general transcriptional regulation or RNA processing.

MeSH Terms
Animals Animals, Genetically Modified Chromosomes/metabolism Dosage Compensation, Genetic/physiology Drosophila/genetics Drosophila Proteins/genetics Fluorescent Antibody Technique Gene Expression Regulation, Developmental/physiology Larva/genetics Male RNA Polymerase II/genetics Transcription Factors/genetics Transcription, Genetic Transgenes X Chromosome/metabolism
Chemicals
Drosophila Proteins Transcription Factors roX1 protein, Drosophila RNA Polymerase II
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Kotlikova I V
Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russia.
Demakova O V
Semeshin V F
Shloma V V
Boldyreva L V
Kuroda M I
Zhimulev I F
References (70)
70 references, click to expand
  1. Dosage compensation regulatory proteins and the evolution of sex chromosomes in Drosophila.
    Genetics. 1996 Oct;144(2):705-13 PMID: 8889531
  2. RNA-dependent association of the Drosophila maleless protein with the male X chromosome.
    Genes Cells. 1996 Mar;1(3):325-36 PMID: 9133666
  3. The NTPase/helicase activities of Drosophila maleless, an essential factor in dosage compensation.
    EMBO J. 1997 May 15;16(10):2671-81 PMID: 9184214
  4. 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
  5. Targeting of MOF, a putative histone acetyl transferase, to the X chromosome of Drosophila melanogaster.
    Dev Genet. 1998;22(1):56-64 PMID: 9499580
  6. An analysis of maleless and histone H4 acetylation in Drosophila melanogaster spermatogenesis.
    Mech Dev. 1998 Feb;71(1-2):107-17 PMID: 9507080
  7. 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
  8. X chromosome sites autonomously recruit the dosage compensation complex in Drosophila males.
    PLoS Biol. 2004 Nov;2(11):e341 PMID: 15502872
  9. Transcriptional activation triggers deposition and removal of the histone variant H3.3.
    Genes Dev. 2005 Apr 1;19(7):804-14 PMID: 15774717
  10. Gene expression analysis of the function of the male-specific lethal complex in Drosophila.
    Genetics. 2005 Apr;169(4):2061-74 PMID: 15716510
  11. Recycling to remodel: evolution of dosage-compensation complexes.
    Curr Opin Genet Dev. 2000 Dec;10(6):644-50 PMID: 11088015
  12. Evolution of dosage compensation in Diptera: the gene maleless implements dosage compensation in Drosophila (Brachycera suborder) but its homolog in Sciara (Nematocera suborder) appears to play no role in dosage compensation.
    Genetics. 2000 Dec;156(4):1853-65 PMID: 11102379
  13. 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
  14. The JIL-1 tandem kinase mediates histone H3 phosphorylation and is required for maintenance of chromatin structure in Drosophila.
    Cell. 2001 May 18;105(4):433-43 PMID: 11371341
  15. Recruitment of the male-specific lethal (MSL) dosage compensation complex to an autosomally integrated roX chromatin entry site correlates with an increased expression of an adjacent reporter gene in male Drosophila.
    J Biol Chem. 2001 Aug 24;276(34):31953-8 PMID: 11402038
  16. 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
  17. Drosophila ELL is associated with actively elongating RNA polymerase II on transcriptionally active sites in vivo.
    EMBO J. 2001 Nov 1;20(21):6104-14 PMID: 11689450
  18. Isolation and characterization of novel mutations of the Broad-Complex, a key regulatory gene of ecdysone induction in Drosophila melanogaster.
    Insect Biochem Mol Biol. 2002 Feb;32(2):121-32 PMID: 11755053
  19. Sex and the single chromosome.
    Adv Genet. 2002;46:1-24 PMID: 11931222
  20. Nucleosome remodeling induced by RNA polymerase II: loss of the H2A/H2B dimer during transcription.
    Mol Cell. 2002 Mar;9(3):541-52 PMID: 11931762
  21. Dosage compensation and intercalary heterochromatin in X chromosomes of Drosophila melanogaster.
    Chromosoma. 2002 Jul;111(2):106-13 PMID: 12111333
  22. Immunogold electron microscope localization of proteins in Drosophila polytene chromosomes: applications and limitations of the method.
    Chromosome Res. 2002;10(5):429-33 PMID: 12296526
  23. Extent of chromatin spreading determined by roX RNA recruitment of MSL proteins.
    Science. 2002 Nov 22;298(5598):1620-3 PMID: 12446910
  24. RNA polymerase II accumulation in the promoter-proximal region of the dihydrofolate reductase and gamma-actin genes.
    Mol Cell Biol. 2003 Mar;23(6):1961-7 PMID: 12612070
  25. Tails of intrigue: phosphorylation of RNA polymerase II mediates histone methylation.
    Cell. 2003 May 16;113(4):429-32 PMID: 12757703
  26. 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
  27. Tracking FACT and the RNA polymerase II elongation complex through chromatin in vivo.
    Science. 2003 Aug 22;301(5636):1094-6 PMID: 12934007
  28. Cdk7 is required for full activation of Drosophila heat shock genes and RNA polymerase II phosphorylation in vivo.
    Mol Cell Biol. 2003 Oct;23(19):6876-86 PMID: 12972606
  29. Investigating RNA polymerase II carboxyl-terminal domain (CTD) phosphorylation.
    Eur J Biochem. 2003 Oct;270(19):3859-70 PMID: 14511368
  30. 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
  31. Study of dosage compensation in Drosophila.
    Genetics. 2003 Nov;165(3):1167-81 PMID: 14668373
  32. 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
  33. Lifting a chromosome: dosage compensation in Drosophila melanogaster.
    FEBS Lett. 2004 Jun 1;567(1):8-14 PMID: 15165886
  34. Multiple functions of nuclear DNA helicase II (RNA helicase A) in nucleic acid metabolism.
    Acta Biochim Biophys Sin (Shanghai). 2004 Mar;36(3):177-83 PMID: 15202501
  35. Sequence-specific targeting of MSL complex regulates transcription of the roX RNA genes.
    EMBO J. 2004 Jul 21;23(14):2853-61 PMID: 15229655
  36. Temporal control of puffing activity in polytene chromosomes.
    Cold Spring Harb Symp Quant Biol. 1974;38:655-62 PMID: 4208797
  37. Deletion mapping of two D. melanogaster loci that code for the 70,000 dalton heat-induced protein.
    Cell. 1979 Jul;17(3):565-71 PMID: 113104
  38. Cloning and characterization of nine heat-shock-induced mRNAs of Drosophila melanogaster.
    Gene. 1981 Oct;15(1):67-80 PMID: 6795091
  39. Analysis of the dosage compensation of a specific transcript in Drosophila melanogaster.
    Genetics. 1986 Mar;112(3):483-91 PMID: 3082711
  40. Dosage compensation at the sgs4 locus of Drosophila melanogaster.
    J Mol Biol. 1986 Feb 20;187(4):529-36 PMID: 3012092
  41. Characterization of a Drosophila protein associated with boundaries of transcriptionally active chromatin.
    Genes Dev. 1991 Sep;5(9):1611-21 PMID: 1885003
  42. The maleless protein associates with the X chromosome to regulate dosage compensation in Drosophila.
    Cell. 1991 Sep 6;66(5):935-47 PMID: 1653648
  43. napts, a mutation affecting sodium channel activity in Drosophila, is an allele of mle, a regulator of X chromosome transcription.
    Cell. 1991 Sep 6;66(5):949-59 PMID: 1653649
  44. The non-dosage compensated LSP1-alpha gene of Drosophila melanogaster lies immediately downstream of the dosage compensated L12 gene.
    Mol Gen Genet. 1992 May;233(1-2):49-52 PMID: 1376406
  45. Dense cluster of genes is located at the ecdysone-regulated 3C puff of Drosophila melanogaster.
    J Mol Biol. 1993 May 20;231(2):531-8 PMID: 8510164
  46. Molecular analysis of the initiation of insect metamorphosis: a comparative study of Drosophila ecdysteroid-regulated transcription.
    Dev Biol. 1993 Dec;160(2):388-404 PMID: 8253272
  47. Locus-specific variation in phosphorylation state of RNA polymerase II in vivo: correlations with gene activity and transcript processing.
    Genes Dev. 1993 Dec;7(12A):2329-44 PMID: 8253380
  48. 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
  49. Dosage compensation in Drosophila.
    Annu Rev Genet. 1994;28:491-521 PMID: 7893138
  50. 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
  51. Expression of msl-2 causes assembly of dosage compensation regulators on the X chromosomes and female lethality in Drosophila.
    Cell. 1995 Jun 16;81(6):867-77 PMID: 7781064
  52. In situ quantification of hsp70 and alpha-beta transcripts at 87A and 87C loci in relation to hsr-omega gene activity in polytene cells of Drosophila melanogaster.
    Chromosome Res. 1995 Sep;3(6):386-93 PMID: 7551555
  53. The evolutionary dynamics of sex determination.
    Science. 1998 Sep 25;281(5385):1990-4 PMID: 9748152
  54. Modulation of MSL1 abundance in female Drosophila contributes to the sex specificity of dosage compensation.
    Genetics. 1998 Oct;150(2):699-709 PMID: 9755201
  55. Electron microscopic in situ hybridization of digoxigenin-dUTP-labelled DNA probes with Drosophila melanogaster polytene chromosomes.
    Chromosome Res. 1998 Aug;6(5):405-10 PMID: 9872670
  56. Role of the male specific lethal (msl) genes in modifying the effects of sex chromosomal dosage in Drosophila.
    Genetics. 1999 May;152(1):249-68 PMID: 10224258
  57. Genetic organization of polytene chromosomes.
    Adv Genet. 1999;39:1-589 PMID: 10319426
  58. JIL-1: a novel chromosomal tandem kinase implicated in transcriptional regulation in Drosophila.
    Mol Cell. 1999 Jul;4(1):129-35 PMID: 10445035
  59. Guilt by association: non-coding RNAs, chromosome-specific proteins and dosage compensation in Drosophila.
    Trends Genet. 1999 Nov;15(11):454-8 PMID: 10529808
  60. 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
  61. Ordered assembly of roX RNAs into MSL complexes on the dosage-compensated X chromosome in Drosophila.
    Curr Biol. 2000 Feb 10;10(3):136-43 PMID: 10679323
  62. The mle(napts) RNA helicase mutation in drosophila results in a splicing catastrophe of the para Na+ channel transcript in a region of RNA editing.
    Neuron. 2000 Jan;25(1):139-49 PMID: 10707979
  63. 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
  64. Chromodomains are protein-RNA interaction modules.
    Nature. 2000 Sep 21;407(6802):405-9 PMID: 11014199
  65. Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription.
    Genes Dev. 2000 Oct 1;14(19):2452-60 PMID: 11018013
  66. RNA polymerase II elongation through chromatin.
    Nature. 2000 Sep 28;407(6803):471-5 PMID: 11028991
  67. Spt5 and spt6 are associated with active transcription and have characteristics of general elongation factors in D. melanogaster.
    Genes Dev. 2000 Oct 15;14(20):2623-34 PMID: 11040216
  68. Targeting the chromatin-remodeling MSL complex of Drosophila to its sites of action on the X chromosome requires both acetyl transferase and ATPase activities.
    EMBO J. 2000 Oct 2;19(19):5202-11 PMID: 11013222
  69. X chromosome dosage compensation in Drosophila.
    Science. 1996 May 24;272(5265):1190-1 PMID: 8638167
  70. CHD1 is concentrated in interbands and puffed regions of Drosophila polytene chromosomes.
    Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):7137-42 PMID: 8692958
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
2006-02-00
Epub
2005-00-03
Pages
963-74
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1456256
Subset
IM
Grants
FIC NIH HHS · N1 R03TW05669-01 · 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