HIRA complex deposition of histone H3.3 is driven by histone tetramerization and histone-DNA binding

J Biol Chem. 2024 Sep;300(9):107604. doi: 10.1016/j.jbc.2024.107604. Epub 2024 Jul 24.

Abstract

The HIRA histone chaperone complex is comprised of four protein subunits: HIRA, UBN1, CABIN1, and transiently associated ASF1a. All four subunits have been demonstrated to play a role in the deposition of the histone variant H3.3 onto areas of actively transcribed euchromatin in cells. The mechanism by which these subunits function together to drive histone deposition has remained poorly understood. Here we present biochemical and biophysical data supporting a model whereby ASF1a delivers histone H3.3/H4 dimers to the HIRA complex, H3.3/H4 tetramerization drives the association of two HIRA/UBN1 complexes, and the affinity of the histones for DNA drives release of ASF1a and subsequent histone deposition. These findings have implications for understanding how other histone chaperone complexes may mediate histone deposition.

Keywords: ASF1a; CABIN1; HIRA; UBN1; chromatin regulation; histone H3.3; histone deposition.

MeSH terms

  • Cell Cycle Proteins* / chemistry
  • Cell Cycle Proteins* / genetics
  • Cell Cycle Proteins* / metabolism
  • DNA* / chemistry
  • DNA* / metabolism
  • Histone Chaperones* / chemistry
  • Histone Chaperones* / metabolism
  • Histones* / metabolism
  • Humans
  • Molecular Chaperones
  • Nuclear Proteins
  • Protein Binding
  • Protein Multimerization*
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism

Substances

  • Histones
  • Cell Cycle Proteins
  • Transcription Factors
  • Histone Chaperones
  • DNA
  • HIRA protein, human
  • ASF1A protein, human
  • UBN1 protein, human
  • Nuclear Proteins
  • Molecular Chaperones