Sequence-Specific Targeting of Dosage Compensation in Drosophila Favors an Active Chromatin Context

Alekseyenko, Artyom A.; Ho, Joshua W.  K.; Peng, Shouyong; Gelbart, Marnie; Tolstorukov, Michael Y.; Plachetka, Annette; Kharchenko, Peter V.; Jung, Youngsook L.; Gorchakov, Andrey A.; Larschan, Erica; Gu, Tingting; Minoda, Aki; Riddle, Nicole C.; Schwartz, Yuri B.; Elgin, Sarah C.  R.; Karpen, Gary H.; Pirrotta, Vincenzo; Kuroda, Mitzi I.; Park, Peter J.

doi:10.1371/journal.pgen.1002646

Sequence-Specific Targeting of Dosage Compensation in Drosophila Favors an Active Chromatin Context

Journal Article · Thu Apr 26 00:00:00 EDT 2012 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1002646· OSTI ID:1627296

Alekseyenko, Artyom A. ^[1]; Ho, Joshua W. K. ^[2]; Peng, Shouyong ^[2]; Gelbart, Marnie ^[3]; Tolstorukov, Michael Y. ^[2]; Plachetka, Annette ^[3]; Kharchenko, Peter V. ^[2]; Jung, Youngsook L. ^[2]; Gorchakov, Andrey A. ^[3]; Larschan, Erica ^[4]; Gu, Tingting ^[5]; Minoda, Aki ^[6]; Riddle, Nicole C. ^[5]; Schwartz, Yuri B. ^[7]; Elgin, Sarah C. R. ^[5]; Karpen, Gary H. ^[8]; Pirrotta, Vincenzo ^[9]; Kuroda, Mitzi I. ^[3]; Park, Peter J. ^[2]

Harvard Medical School, Boston, MA (United States). Brigham and Women's Hospital. Dept. of Medicine. Division of Genetics; Harvard Medical School, Boston, MA (United States). Dept. of Genetics; DOE/OSTI
Harvard Medical School, Boston, MA (United States). Brigham and Women's Hospital. Dept. of Medicine. Division of Genetics; Harvard Medical School, Boston, MA (United States). Center for Biomedical Informatics
Harvard Medical School, Boston, MA (United States). Brigham and Women's Hospital. Dept. of Medicine. Division of Genetics; Harvard Medical School, Boston, MA (United States). Dept. of Genetics
Brown Univ., Providence, RI (United States). Dept. of Molecular Biology, Cell Biology and Biochemistry
Washington Univ., St. Louis, MO (United States). Dept. of Biology
Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Dept. of Genome Dynamics
Umea Univ. (Sweden). Dept. of Molecular Biology
Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology
Rutgers Univ., Piscataway, NJ (United States). Dept. of Molecular Biology and Biochemistry

The Drosophila MSL complex mediates dosage compensation by increasing transcription of the single X chromosome in males approximately two-fold. This is accomplished through recognition of the X chromosome and subsequent acetylation of histone H4K16 on X-linked genes. Initial binding to the X is thought to occur at ‘‘entry sites’’ that contain a consensus sequence motif (‘‘MSL recognition element’’ or MRE). However, this motif is only ~2 fold enriched on X, and only a fraction of the motifs on X are initially targeted. Here we ask whether chromatin context could distinguish between utilized and non-utilized copies of the motif, by comparing their relative enrichment for histone modifications and chromosomal proteins mapped in the modENCODE project. Through a comparative analysis of the chromatin features in male S2 cells (which contain MSL complex) and female Kc cells (which lack the complex), we find that the presence of active chromatin modifications, together with an elevated local GC content in the surrounding sequences, has strong predictive value for functional MSL entry sites, independent of MSL binding. We tested these sites for function in Kc cells by RNAi knockdown of Sxl, resulting in induction of MSL complex. We show that ectopic MSL expression in Kc cells leads to H4K16 acetylation around these sites and a relative increase in X chromosome transcription. Collectively, our results support a model in which a pre-existing active chromatin environment, coincident with H3K36me3, contributes to MSL entry site selection. The consequences of MSL targeting of the male X chromosome include increase in nucleosome lability, enrichment for H4K16 acetylation and JIL-1 kinase, and depletion of linker histone H1 on active X-linked genes. Our analysis can serve as a model for identifying chromatin and local sequence features that may contribute to selection of functional protein binding sites in the genome.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Institutes of Health (NIH)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1627296

Journal Information:: PLoS Genetics, Journal Name: PLoS Genetics Journal Issue: 4 Vol. 8; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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