Sex-specific phenotypes of histone H4 point mutants establish dosage compensation as the critical function of H4K16 acetylation in Drosophila

Proc Natl Acad Sci U S A. 2018 Dec 26;115(52):13336-13341. doi: 10.1073/pnas.1817274115. Epub 2018 Dec 10.

Abstract

Acetylation of histone H4 at lysine 16 (H4K16) modulates nucleosome-nucleosome interactions and directly affects nucleosome binding by certain proteins. In Drosophila, H4K16 acetylation by the dosage compensation complex subunit Mof is linked to increased transcription of genes on the single X chromosome in males. Here, we analyzed Drosophila containing different H4K16 mutations or lacking Mof protein. An H4K16A mutation causes embryonic lethality in both sexes, whereas an H4K16R mutation permits females to develop into adults but causes lethality in males. The acetyl-mimic mutation H4K16Q permits both females and males to develop into adults. Complementary analyses reveal that males lacking maternally deposited and zygotically expressed Mof protein arrest development during gastrulation, whereas females of the same genotype develop into adults. Together, this demonstrates the causative role of H4K16 acetylation by Mof for dosage compensation in Drosophila and uncovers a previously unrecognized requirement for this process already during the onset of zygotic gene transcription.

Keywords: Drosophila; H4K16 acetylation; chromatin; dosage compensation complex; histone modification.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylation
  • Animals
  • Dosage Compensation, Genetic / genetics*
  • Drosophila Proteins / genetics
  • Drosophila melanogaster / genetics
  • Female
  • Histone Acetyltransferases / metabolism
  • Histones / genetics*
  • Histones / metabolism
  • Lysine / genetics
  • Male
  • Nuclear Proteins / metabolism
  • Nucleosomes / metabolism
  • Phenotype
  • Point Mutation / genetics
  • Protein Processing, Post-Translational / genetics
  • Sex
  • Sex Factors
  • Transcription Factors / metabolism
  • X Chromosome / metabolism

Substances

  • Drosophila Proteins
  • Histones
  • Nuclear Proteins
  • Nucleosomes
  • Transcription Factors
  • Histone Acetyltransferases
  • Lysine