Oxidation of hemoproteins by Streptococcus pneumoniae collapses the cell cytoskeleton and disrupts mitochondrial respiration leading to the cytotoxicity of human lung cells

Microbiol Spectr. 2024 Jan 11;12(1):e0291223. doi: 10.1128/spectrum.02912-23. Epub 2023 Dec 12.

Abstract

Streptococcus pneumoniae (Spn) colonizes the lungs, killing millions every year. During its metabolism, Spn produces abundant amounts of hydrogen peroxide. When produced in the lung parenchyma, Spn-hydrogen peroxide (H2O2) causes the death of lung cells, and details of the mechanism are studied here. We found that Spn-H2O2 targets intracellular proteins, resulting in the contraction of the cell cytoskeleton and disruption of mitochondrial function, ultimately contributing to cell death. Intracellular proteins targeted by Spn-H2O2 included cytochrome c and, surprisingly, a protein of the cell cytoskeleton, beta-tubulin. To study the details of oxidative reactions, we used, as a surrogate model, the oxidation of another hemoprotein, hemoglobin. Using the surrogate model, we specifically identified a highly reactive radical whose creation was catalyzed by Spn-H2O2. In sum, we demonstrated that the oxidation of intracellular targets by Spn-H2O2 plays an important role in the cytotoxicity caused by Spn, thus providing new targets for interventions.

Keywords: Streptococcus pneumoniae; cytoskeleton; hemoproteins; mitochondria; oxidation.

MeSH terms

  • Cytoskeleton / metabolism
  • Humans
  • Hydrogen Peroxide* / metabolism
  • Hydrogen Peroxide* / toxicity
  • Lung / metabolism
  • Mitochondria / metabolism
  • Respiration
  • Streptococcus pneumoniae* / metabolism

Substances

  • Hydrogen Peroxide