The histone chaperone Vps75 forms multiple oligomeric assemblies capable of mediating exchange between histone H3-H4 tetramers and Asf1-H3-H4 complexes

Nucleic Acids Res. 2016 Jul 27;44(13):6157-72. doi: 10.1093/nar/gkw209. Epub 2016 Apr 1.

Abstract

Vps75 is a histone chaperone that has been historically characterized as homodimer by X-ray crystallography. In this study, we present a crystal structure containing two related tetrameric forms of Vps75 within the crystal lattice. We show Vps75 associates with histones in multiple oligomers. In the presence of equimolar H3-H4 and Vps75, the major species is a reconfigured Vps75 tetramer bound to a histone H3-H4 tetramer. However, in the presence of excess histones, a Vps75 dimer bound to a histone H3-H4 tetramer predominates. We show the Vps75-H3-H4 interaction is compatible with the histone chaperone Asf1 and deduce a structural model of the Vps75-Asf1-H3-H4 (VAH) co-chaperone complex using the Pulsed Electron-electron Double Resonance (PELDOR) technique and cross-linking MS/MS distance restraints. The model provides a molecular basis for the involvement of both Vps75 and Asf1 in Rtt109 catalysed histone H3 K9 acetylation. In the absence of Asf1 this model can be used to generate a complex consisting of a reconfigured Vps75 tetramer bound to a H3-H4 tetramer. This provides a structural explanation for many of the complexes detected biochemically and illustrates the ability of Vps75 to interact with dimeric or tetrameric H3-H4 using the same interaction surface.

MeSH terms

  • Acetylation
  • Cell Cycle Proteins / chemistry*
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Crystallography, X-Ray
  • Histone Acetyltransferases / genetics
  • Histone Acetyltransferases / metabolism
  • Histone Chaperones / chemistry*
  • Histone Chaperones / genetics
  • Histone Chaperones / metabolism
  • Histones / chemistry*
  • Histones / genetics
  • Histones / metabolism
  • Molecular Chaperones / chemistry*
  • Molecular Chaperones / genetics
  • Molecular Chaperones / metabolism
  • Multiprotein Complexes
  • Protein Binding
  • Protein Multimerization
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae Proteins / chemistry*
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism

Substances

  • ASF1 protein, S cerevisiae
  • Cell Cycle Proteins
  • Histone Chaperones
  • Histones
  • Molecular Chaperones
  • Multiprotein Complexes
  • Saccharomyces cerevisiae Proteins
  • Vps75 protein, S cerevisiae
  • Histone Acetyltransferases