Stabilization of the hexasome intermediate during histone exchange by yeast SWR1 complex

Mol Cell. 2024 Oct 17;84(20):3871-3884.e9. doi: 10.1016/j.molcel.2024.08.015. Epub 2024 Sep 2.

Abstract

The yeast SWR1 complex catalyzes the exchange of histone H2A/H2B dimers in nucleosomes with Htz1/H2B dimers. We use cryoelectron microscopy to determine the structure of an enzyme-bound hexasome intermediate in the reaction pathway of histone exchange, in which an H2A/H2B dimer has been extracted from a nucleosome prior to the insertion of a dimer comprising Htz1/H2B. The structure reveals a key role for the Swc5 subunit in stabilizing the unwrapping of DNA from the histone core of the hexasome. By engineering a crosslink between an Htz1/H2B dimer and its chaperone protein Chz1, we show that this blocks histone exchange by SWR1 but allows the incoming chaperone-dimer complex to insert into the hexasome. We use this reagent to trap an SWR1/hexasome complex with an incoming Htz1/H2B dimer that shows how the reaction progresses to the next step. Taken together the structures reveal insights into the mechanism of histone exchange by SWR1 complex.

Keywords: SWR1 complex; chromatin remodeling; histone exchange.

MeSH terms

  • Adenosine Triphosphatases / chemistry
  • Adenosine Triphosphatases / genetics
  • Adenosine Triphosphatases / metabolism
  • Chromosomal Proteins, Non-Histone / chemistry
  • Chromosomal Proteins, Non-Histone / genetics
  • Chromosomal Proteins, Non-Histone / metabolism
  • Cryoelectron Microscopy*
  • Histone Chaperones
  • Histones* / chemistry
  • Histones* / genetics
  • Histones* / metabolism
  • Models, Molecular
  • Nucleosomes* / genetics
  • Nucleosomes* / metabolism
  • Nucleosomes* / ultrastructure
  • Protein Binding
  • Protein Multimerization*
  • Saccharomyces cerevisiae Proteins* / chemistry
  • Saccharomyces cerevisiae Proteins* / genetics
  • Saccharomyces cerevisiae Proteins* / metabolism
  • Saccharomyces cerevisiae* / genetics
  • Saccharomyces cerevisiae* / metabolism

Substances

  • Histones
  • Saccharomyces cerevisiae Proteins
  • Nucleosomes
  • Swr1 protein, S cerevisiae
  • Chz1 protein, S cerevisiae
  • Htz1 protein, S cerevisiae
  • Adenosine Triphosphatases
  • Chromosomal Proteins, Non-Histone
  • Histone Chaperones