Dynamic Regulation of Mitochondrial Import by the Ubiquitin System

Mol Cell. 2020 Mar 5;77(5):1107-1123.e10. doi: 10.1016/j.molcel.2020.02.012.

Abstract

Mitochondria import nearly their entire proteome from the cytoplasm by translocating precursor proteins through the translocase of the outer membrane (TOM) complex. Here, we show dynamic regulation of mitochondrial import by the ubiquitin system. Acute pharmacological inhibition or genetic ablation of the mitochondrial deubiquitinase (DUB) USP30 triggers accumulation of Ub-substrates that are normally localized inside the mitochondria. Mitochondrial import of USP30 substrates is impaired in USP30 knockout (KO) cells, suggesting that deubiquitination promotes efficient import. Upstream of USP30, the E3 ligase March5 ubiquitinates mitochondrial proteins whose eventual import depends on USP30. In USP30 KOs, exogenous March5 expression induces accumulation of unimported translocation intermediates that are degraded by the proteasomes. In USP30 KO mice, TOM subunits have reduced abundance across multiple tissues. Together these data highlight how protein import into a subcellular compartment can be regulated by ubiquitination and deubiquitination by E3 ligase and DUB machinery positioned at the gate.

Keywords: Deubiquitinase; E3 Ubiquitin Ligase; Mitochondria; Mitochondrial Import; TOM complex; Ubiquitin System.

MeSH terms

  • Animals
  • Biological Transport
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Female
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mitochondria / enzymology*
  • Mitochondria / genetics
  • Mitochondrial Precursor Protein Import Complex Proteins
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism*
  • Proteasome Endopeptidase Complex / genetics
  • Proteasome Endopeptidase Complex / metabolism
  • Proteolysis
  • Thiolester Hydrolases / genetics
  • Thiolester Hydrolases / metabolism*
  • Time Factors
  • Ubiquitin / metabolism*
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / metabolism*
  • Ubiquitination

Substances

  • Carrier Proteins
  • Membrane Proteins
  • Mitochondrial Precursor Protein Import Complex Proteins
  • Mitochondrial Proteins
  • Ubiquitin
  • Usp30 protein, human
  • MARCHF5 protein, human
  • Marchf5 protein, mouse
  • Ubiquitin-Protein Ligases
  • Thiolester Hydrolases
  • Usp30 protein, mouse
  • Proteasome Endopeptidase Complex