Preparation of fully synthetic histone H3 reveals that acetyl-lysine 56 facilitates protein binding within nucleosomes

J Mol Biol. 2011 Apr 29;408(2):187-204. doi: 10.1016/j.jmb.2011.01.003. Epub 2011 Feb 15.

Abstract

Posttranslational modification (PTM) of histones plays a central role in genome regulation. Engineering histones with defined PTMs on one residue or on multiple residues is crucial for understanding their function within nucleosomes and chromatin. We introduce a sequential native chemical ligation strategy that is suitable for the preparation of fully synthetic histone proteins, allowing for site-specific incorporation of varied PTMs throughout the sequence. We demonstrate this method with the generation of histone H3 acetylated at lysine 56 [H3(K56ac)]. H3(K56ac) is essential for transcription, replication, and repair. We examined the influence of H3(K56ac) on the targeting of a model DNA binding factor (LexA) to a site ∼30 bp within the nucleosome. We find that H3(K56ac) increases LexA binding to its DNA target site by 3-fold at physiological ionic strength. We then demonstrate that H3(K56ac) facilitates LexA binding by increasing DNA unwrapping, not by nucleosome repositioning. Furthermore, we find that H3(K56Q) quantitatively imitates H3(K56ac) function. Together, these studies introduce powerful tools for the analysis of histone PTM functions.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Acetylation
  • Amino Acid Sequence
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • DNA / genetics
  • DNA / metabolism*
  • Fluorescence Resonance Energy Transfer
  • Histones / chemical synthesis*
  • Histones / metabolism*
  • Lysine / chemistry*
  • Lysine / genetics
  • Lysine / metabolism
  • Molecular Sequence Data
  • Nucleosomes / genetics
  • Nucleosomes / metabolism*
  • Peptide Fragments / genetics
  • Peptide Fragments / metabolism
  • Protein Binding
  • Protein Conformation
  • Protein Processing, Post-Translational
  • Serine Endopeptidases / genetics
  • Serine Endopeptidases / metabolism*
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization

Substances

  • Bacterial Proteins
  • Histones
  • LexA protein, Bacteria
  • Nucleosomes
  • Peptide Fragments
  • DNA
  • Serine Endopeptidases
  • Lysine