Targeted degradation of extracellular mitochondrial aspartyl-tRNA synthetase modulates immune responses

Nat Commun. 2024 Jul 22;15(1):6172. doi: 10.1038/s41467-024-50031-7.

Abstract

The severity of bacterial pneumonia can be worsened by impaired innate immunity resulting in ineffective pathogen clearance. We describe a mitochondrial protein, aspartyl-tRNA synthetase (DARS2), which is released in circulation during bacterial pneumonia in humans and displays intrinsic innate immune properties and cellular repair properties. DARS2 interacts with a bacterial-induced ubiquitin E3 ligase subunit, FBXO24, which targets the synthetase for ubiquitylation and degradation, a process that is inhibited by DARS2 acetylation. During experimental pneumonia, Fbxo24 knockout mice exhibit elevated DARS2 levels with an increase in pulmonary cellular and cytokine levels. In silico modeling identified an FBXO24 inhibitory compound with immunostimulatory properties which extended DARS2 lifespan in cells. Here, we show a unique biological role for an extracellular, mitochondrially derived enzyme and its molecular control by the ubiquitin apparatus, which may serve as a mechanistic platform to enhance protective host immunity through small molecule discovery.

MeSH terms

  • Acetylation
  • Animals
  • Aspartate-tRNA Ligase* / genetics
  • Aspartate-tRNA Ligase* / metabolism
  • Cytokines / metabolism
  • F-Box Proteins / genetics
  • F-Box Proteins / metabolism
  • Female
  • HEK293 Cells
  • Humans
  • Immunity, Innate*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • Mitochondria* / metabolism
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism
  • Proteolysis
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / metabolism
  • Ubiquitination*

Substances

  • Aspartate-tRNA Ligase
  • F-Box Proteins
  • Ubiquitin-Protein Ligases
  • Cytokines
  • Mitochondrial Proteins