Protein structure, amino acid composition and sequence determine proteome vulnerability to oxidation-induced damage

EMBO J. 2020 Dec 1;39(23):e104523. doi: 10.15252/embj.2020104523. Epub 2020 Oct 19.

Abstract

Oxidative stress alters cell viability, from microorganism irradiation sensitivity to human aging and neurodegeneration. Deleterious effects of protein carbonylation by reactive oxygen species (ROS) make understanding molecular properties determining ROS susceptibility essential. The radiation-resistant bacterium Deinococcus radiodurans accumulates less carbonylation than sensitive organisms, making it a key model for deciphering properties governing oxidative stress resistance. We integrated shotgun redox proteomics, structural systems biology, and machine learning to resolve properties determining protein damage by γ-irradiation in Escherichia coli and D. radiodurans at multiple scales. Local accessibility, charge, and lysine enrichment accurately predict ROS susceptibility. Lysine, methionine, and cysteine usage also contribute to ROS resistance of the D. radiodurans proteome. Our model predicts proteome maintenance machinery, and proteins protecting against ROS are more resistant in D. radiodurans. Our findings substantiate that protein-intrinsic protection impacts oxidative stress resistance, identifying causal molecular properties.

Keywords: Deinococcus radiodurans; oxidative stress; protein carbonyl; radioresistance; structural systems biology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aging / metabolism
  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / metabolism*
  • Computational Biology
  • Deinococcus / metabolism
  • Escherichia coli
  • Humans
  • Machine Learning
  • Neurodegenerative Diseases / metabolism
  • Oxidation-Reduction
  • Oxidative Stress / physiology*
  • Protein Conformation
  • Protein Processing, Post-Translational
  • Proteome / metabolism*
  • Proteomics / methods
  • Reactive Oxygen Species / metabolism
  • Sequence Analysis, Protein

Substances

  • Bacterial Proteins
  • Proteome
  • Reactive Oxygen Species