DNA binding by Sgf11 protein affects histone H2B deubiquitination by Spt-Ada-Gcn5-acetyltransferase (SAGA)

J Biol Chem. 2014 Mar 28;289(13):8989-99. doi: 10.1074/jbc.M113.500868. Epub 2014 Feb 7.

Abstract

The yeast Spt-Ada-Gcn5-acetyltransferase (SAGA) complex is a transcription coactivator that contains a histone H2B deubiquitination activity mediated by its Ubp8 subunit. Full enzymatic activity requires the formation of a quaternary complex, the deubiquitination module (DUBm) of SAGA, which is composed of Ubp8, Sus1, Sgf11, and Sgf73. The crystal structures of the DUBm have shed light on the structure/function relationship of this complex. Specifically, both Sgf11 and Sgf73 contain zinc finger domains (ZnF) that appear essential for the DUBm activity. Whereas Sgf73 N-terminal ZnF is important for DUBm stability, Sgf11 C-terminal ZnF appears to be involved in DUBm function. To further characterize the role of these two zinc fingers, we have solved their structure by NMR. We show that, contrary to the previously reported structures, Sgf73 ZnF adopts a C2H2 coordination with unusual tautomeric forms for the coordinating histidines. We further report that the Sgf11 ZnF, but not the Sgf73 ZnF, binds to nucleosomal DNA with a binding interface composed of arginine residues located within the ZnF α-helix. Mutational analyses both in vitro and in vivo provide evidence for the functional relevance of our structural observations. The combined interpretation of our results leads to an uncommon ZnF-DNA interaction between the SAGA DUBm and nucleosomes, thus providing further functional insights into SAGA's epigenetic modulation of the chromatin structure.

Keywords: DNA-Protein Interaction; Deubiquitination; Epigenetics; NMR; Zinc Finger.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Base Sequence
  • Binding Sites
  • DNA / genetics
  • DNA / metabolism*
  • HeLa Cells
  • Histone Acetyltransferases / chemistry
  • Histone Acetyltransferases / metabolism
  • Histones / metabolism*
  • Humans
  • Models, Molecular
  • Molecular Sequence Data
  • Mutation
  • Nucleosomes / metabolism
  • Protein Binding
  • Protein Structure, Tertiary
  • Saccharomyces cerevisiae / cytology
  • Saccharomyces cerevisiae / metabolism*
  • Saccharomyces cerevisiae Proteins / chemistry
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism*
  • Trans-Activators / metabolism*
  • Transcription Factors / chemistry
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Ubiquitination*
  • Zinc Fingers

Substances

  • Histones
  • Nucleosomes
  • SAGA complex, S cerevisiae
  • SGF11 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • Trans-Activators
  • Transcription Factors
  • DNA
  • Histone Acetyltransferases
  • Sgf73 protein, S cerevisiae

Associated data

  • PDB/2LO2
  • PDB/2LO3