Protein lysine-Nζ alkylation and O-phosphorylation mediated by DTT-generated reactive oxygen species

Protein Sci. 2013 Mar;22(3):327-46. doi: 10.1002/pro.2214. Epub 2013 Jan 27.

Abstract

Reactive oxygen species (ROS) play crucial roles in physiology and pathology. In this report, we use NMR spectroscopy and mass spectrometry (MS) to demonstrate that proteins (galectin-1, ubiquitin, RNase, cytochrome c, myoglobin, and lysozyme) under reducing conditions with dithiothreitol (DTT) become alkylated at lysine-N(ζ) groups and O-phosphorylated at serine and threonine residues. These adduction reactions only occur in the presence of monophosphate, potassium, trace metals Fe/Cu, and oxygen, and are promoted by reactive oxygen species (ROS) generated via DTT oxidation. Superoxide mediates the chemistry, because superoxide dismutase inhibits the reaction, and hydroxyl and phosphoryl radicals are also likely involved. While lysine alkylation accounts for most of the adduction, low levels of phosphorylation are also observed at some serine and threonine residues, as determined by western blotting and MS fingerprinting. The adducted alkyl group is found to be a fragment of DTT that forms a Schiff base at lysine N(ζ) groups. Although its exact chemical structure remains unknown, the DTT fragment includes a SH group and a --CHOH--CH₂-- group. Chemical adduction appears to be promoted in the context of a well-folded protein, because some adducted sites in the proteins studied are considerably more reactive than others and the reaction occurs to a lesser extent with shorter, unfolded peptides and not at all with small organic molecules. A structural signature involving clusters of positively charged and other polar groups appears to facilitate the reaction. Overall, our findings demonstrate a novel reaction for DTT-mediated ROS chemistry with proteins.

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

  • Alkylation / drug effects
  • Animals
  • Catalysis / drug effects
  • Dithiothreitol / chemistry*
  • Humans
  • Lysine / chemistry*
  • Mutant Proteins / chemistry
  • Oxidation-Reduction
  • Phosphorylation / drug effects
  • Protein Conformation / drug effects
  • Protein Folding / drug effects
  • Proteins / chemistry*
  • Reactive Oxygen Species / chemistry*
  • Reducing Agents / chemistry*
  • Schiff Bases / chemistry
  • Serine / chemistry
  • Threonine / chemistry

Substances

  • Mutant Proteins
  • Proteins
  • Reactive Oxygen Species
  • Reducing Agents
  • Schiff Bases
  • Threonine
  • Serine
  • Lysine
  • Dithiothreitol