RPA Interacts with HIRA and Regulates H3.3 Deposition at Gene Regulatory Elements in Mammalian Cells

Mol Cell. 2017 Jan 19;65(2):272-284. doi: 10.1016/j.molcel.2016.11.030.

Abstract

The histone chaperone HIRA is involved in depositing histone variant H3.3 into distinct genic regions, including promoters, enhancers, and gene bodies. However, how HIRA deposits H3.3 to these regions remains elusive. Through a short hairpin RNA (shRNA) screening, we identified single-stranded DNA binding protein replication protein A (RPA) as a regulator of the deposition of newly synthesized H3.3 into chromatin. We show that RPA physically interacts with HIRA to form RPA-HIRA-H3.3 complexes, and it co-localizes with HIRA and H3.3 at gene promoters and enhancers. Depletion of RPA1, the largest subunit of the RPA complex, dramatically reduces both HIRA association with chromatin and the deposition of newly synthesized H3.3 at promoters and enhancers and leads to altered transcription at gene promoters. These results support a model whereby RPA, best known for its role in DNA replication and repair, recruits HIRA to promoters and enhancers and regulates deposition of newly synthesized H3.3 to these regulatory elements for gene regulation.

Keywords: H3.3 deposition; HIRA; R-loop; RPA; enhancer; histone chaperone; nucleosome assembly; promoter.

MeSH terms

  • Binding Sites
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Chromatin / genetics
  • Chromatin / metabolism*
  • DNA / genetics
  • DNA / metabolism*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Enhancer Elements, Genetic*
  • G1 Phase
  • HEK293 Cells
  • HeLa Cells
  • Histone Chaperones / genetics
  • Histone Chaperones / metabolism*
  • Histones / metabolism*
  • Humans
  • Promoter Regions, Genetic*
  • Protein Binding
  • Protein Interaction Domains and Motifs
  • RNA Interference
  • Replication Protein A / genetics
  • Replication Protein A / metabolism*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Transcription, Genetic*
  • Transfection

Substances

  • Cell Cycle Proteins
  • Chromatin
  • DNA-Binding Proteins
  • HIRA protein, human
  • Histone Chaperones
  • Histones
  • RPA1 protein, human
  • RPA3 protein, human
  • Replication Protein A
  • Transcription Factors
  • DNA
  • RPA2 protein, human