Identification of the Drosophila X Chromosome: The Long and Short of It

Overview

Journal RNA Biol

Specialty Molecular Biology

Date 2015 Sep 15

PMID 26367502

Citations 11

Authors

Debashish U Menon

Victoria H Meller

Affiliations

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Abstract

The different dose of X chromosomes in males and females produces a potentially fatal imbalance in X-linked gene products. This imbalance is addressed by dosage compensation, a process that modulates expression from an entire X chromosome in one sex. Dosage compensation acts on thousands of genes with disparate expression patterns. Both flies and mammals accomplish this with remarkable specificity by targeting epigenetic chromatin modifications to a single chromosome. Long noncoding RNAs that are expressed from the X chromosome are essential elements of the targeting mechanism in both lineages. We recently discovered that the siRNA pathway, as well as small RNA from satellite repeats that are strikingly enriched on the fly X chromosome, also promote X recognition. In this article we review the current understanding of X recognition in flies and discuss potential mechanisms by which the siRNA pathway, repetitive elements and long noncoding RNAs might cooperate to promote X recognition.

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References

Kuhn G, Kuttler H, Moreira-Filho O, Heslop-Harrison J . The 1.688 repetitive DNA of Drosophila: concerted evolution at different genomic scales and association with genes. Mol Biol Evol. 2011; 29(1):7-11. DOI: 10.1093/molbev/msr173. View

Menon D, Meller V . A role for siRNA in X-chromosome dosage compensation in Drosophila melanogaster. Genetics. 2012; 191(3):1023-8. PMC: 3389965. DOI: 10.1534/genetics.112.140236. View

Conrad T, Cavalli F, Vaquerizas J, Luscombe N, Akhtar A . Drosophila dosage compensation involves enhanced Pol II recruitment to male X-linked promoters. Science. 2012; 337(6095):742-6. DOI: 10.1126/science.1221428. View

Horakova A, Moseley S, McLaughlin C, Tremblay D, Chadwick B . The macrosatellite DXZ4 mediates CTCF-dependent long-range intrachromosomal interactions on the human inactive X chromosome. Hum Mol Genet. 2012; 21(20):4367-77. PMC: 3459461. DOI: 10.1093/hmg/dds270. View

Wang C, Alekseyenko A, LeRoy G, Elia A, Gorchakov A, Britton L . Chromatin proteins captured by ChIP-mass spectrometry are linked to dosage compensation in Drosophila. Nat Struct Mol Biol. 2013; 20(2):202-9. PMC: 3674866. DOI: 10.1038/nsmb.2477. View

Soruco M, Chery J, Bishop E, Siggers T, Tolstorukov M, Leydon A . The CLAMP protein links the MSL complex to the X chromosome during Drosophila dosage compensation. Genes Dev. 2013; 27(14):1551-6. PMC: 3731544. DOI: 10.1101/gad.214585.113. View

Rival-Gervier S, Lo M, Khattak S, Pasceri P, Lorincz M, Ellis J . Kinetics and epigenetics of retroviral silencing in mouse embryonic stem cells defined by deletion of the D4Z4 element. Mol Ther. 2013; 21(8):1536-50. PMC: 3734652. DOI: 10.1038/mt.2013.131. View

Mousavi K, Zare H, DellOrso S, Grontved L, Gutierrez-Cruz G, Derfoul A . eRNAs promote transcription by establishing chromatin accessibility at defined genomic loci. Mol Cell. 2013; 51(5):606-17. PMC: 3786356. DOI: 10.1016/j.molcel.2013.07.022. View

Gu T, Elgin S . Maternal depletion of Piwi, a component of the RNAi system, impacts heterochromatin formation in Drosophila. PLoS Genet. 2013; 9(9):e1003780. PMC: 3777992. DOI: 10.1371/journal.pgen.1003780. View

10.

Smith E, Pannuti A, Gu W, Steurnagel A, Cook R, Allis C . The drosophila MSL complex acetylates histone H4 at lysine 16, a chromatin modification linked to dosage compensation. Mol Cell Biol. 1999; 20(1):312-8. PMC: 85086. DOI: 10.1128/MCB.20.1.312-318.2000. View

11.

Bell O, Conrad T, Kind J, Wirbelauer C, Akhtar A, Schubeler D . Transcription-coupled methylation of histone H3 at lysine 36 regulates dosage compensation by enhancing recruitment of the MSL complex in Drosophila melanogaster. Mol Cell Biol. 2008; 28(10):3401-9. PMC: 2423169. DOI: 10.1128/MCB.00006-08. View

12.

Portnoy V, Huang V, Place R, Li L . Small RNA and transcriptional upregulation. Wiley Interdiscip Rev RNA. 2011; 2(5):748-60. PMC: 3154074. DOI: 10.1002/wrna.90. View

13.

Moshkovich N, Nisha P, Boyle P, Thompson B, Dale R, Lei E . RNAi-independent role for Argonaute2 in CTCF/CP190 chromatin insulator function. Genes Dev. 2011; 25(16):1686-701. PMC: 3165934. DOI: 10.1101/gad.16651211. View

14.

Deng X, Hiatt J, Nguyen D, Ercan S, Sturgill D, Hillier L . Evidence for compensatory upregulation of expressed X-linked genes in mammals, Caenorhabditis elegans and Drosophila melanogaster. Nat Genet. 2011; 43(12):1179-85. PMC: 3576853. DOI: 10.1038/ng.948. View

15.

Liu Y, Lu C, Yang Y, Fan Y, Yang R, Liu C . Influence of histone tails and H4 tail acetylations on nucleosome-nucleosome interactions. J Mol Biol. 2011; 414(5):749-64. DOI: 10.1016/j.jmb.2011.10.031. View

16.

Ferrari F, Plachetka A, Alekseyenko A, Jung Y, Ozsolak F, Kharchenko P . "Jump start and gain" model for dosage compensation in Drosophila based on direct sequencing of nascent transcripts. Cell Rep. 2013; 5(3):629-36. PMC: 3852897. DOI: 10.1016/j.celrep.2013.09.037. View

17.

Leung K, Panning B . X-inactivation: Xist RNA uses chromosome contacts to coat the X. Curr Biol. 2014; 24(2):R80-R82. PMC: 4465072. DOI: 10.1016/j.cub.2013.11.052. View

18.

Lam M, Li W, Rosenfeld M, Glass C . Enhancer RNAs and regulated transcriptional programs. Trends Biochem Sci. 2014; 39(4):170-82. PMC: 4266492. DOI: 10.1016/j.tibs.2014.02.007. View

19.

Su M, Han D, Boyd-Kirkup J, Yu X, Han J . Evolution of Alu elements toward enhancers. Cell Rep. 2014; 7(2):376-385. DOI: 10.1016/j.celrep.2014.03.011. View

20.

Gallach M . Recurrent turnover of chromosome-specific satellites in Drosophila. Genome Biol Evol. 2014; 6(6):1279-86. PMC: 4079201. DOI: 10.1093/gbe/evu104. View