Histone locus regulation by the Drosophila dosage compensation adaptor protein CLAMP

  1. Erica N. Larschan1
  1. 1Department of Molecular Biology, Cellular Biology, and Biochemistry, Brown University, Providence, Rhode Island 02912, USA;
  2. 2Curriculum in Genetics and Molecular Biology, University of North Carolina, Chapel Hill, North Carolina 27599, USA;
  3. 3Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina 27599, USA;
  4. 4Integrative Program for Biological and Genome Sciences, University of North Carolina, Chapel Hill, North Carolina 27599, USA;
  5. 5Department of Molecular Biology, Massachusetts General Hospital, Boston, Massachusetts 02114, USA;
  6. 6Department of Biochemistry and Biophysics, University of North Carolina, Chapel Hill, North Carolina 27599, USA;
  7. 7Department of Biology, University of North Carolina at Chapel Hill, University of North Carolina, Chapel Hill, North Carolina 27599, USA;
  8. 8Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599, USA
  1. Corresponding authors: leila_rieder{at}brown.edu, erica_larschan{at}brown.edu

  1. ↵13 These authors contributed equally to this work.

  • ↵Present addresses: 9Department of Entomology, North Carolina State University, Raleigh, NC 27695, USA; 10Center for Eukaryotic Gene Regulation, Department of Biochemistry and Molecular Biology, Pennsylvania State University, State College, PA 16801, USA; 11Directed Genomics, Ipswitch, MA 01938, USA; 12Science Outreach Program, The Rockefeller University, New York, NY 10065, USA

Abstract

The conserved histone locus body (HLB) assembles prior to zygotic gene activation early during development and concentrates factors into a nuclear domain of coordinated histone gene regulation. Although HLBs form specifically at replication-dependent histone loci, the cis and trans factors that target HLB components to histone genes remained unknown. Here we report that conserved GA repeat cis elements within the bidirectional histone3–histone4 promoter direct HLB formation in Drosophila. In addition, the CLAMP (chromatin-linked adaptor for male-specific lethal [MSL] proteins) zinc finger protein binds these GA repeat motifs, increases chromatin accessibility, enhances histone gene transcription, and promotes HLB formation. We demonstrated previously that CLAMP also promotes the formation of another domain of coordinated gene regulation: the dosage-compensated male X chromosome. Therefore, CLAMP binding to GA repeat motifs promotes the formation of two distinct domains of coordinated gene activation located at different places in the genome.

Keywords

Footnotes

  • Received April 27, 2017.
  • Accepted July 25, 2017.

This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genesdev.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.

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  1. Published in Advance August 24, 2017, doi: 10.1101/gad.300855.117 Genes & Dev. 31: 1494-1508 © 2017 Rieder et al.; Published by Cold Spring Harbor Laboratory Press

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