AIFM1 is a component of the mitochondrial disulfide relay that drives complex I assembly through efficient import of NDUFS5

EMBO J. 2022 Sep 1;41(17):e110784. doi: 10.15252/embj.2022110784. Epub 2022 Jul 20.

Abstract

The mitochondrial intermembrane space protein AIFM1 has been reported to mediate the import of MIA40/CHCHD4, which forms the import receptor in the mitochondrial disulfide relay. Here, we demonstrate that AIFM1 and MIA40/CHCHD4 cooperate beyond this MIA40/CHCHD4 import. We show that AIFM1 and MIA40/CHCHD4 form a stable long-lived complex in vitro, in different cell lines, and in tissues. In HEK293 cells lacking AIFM1, levels of MIA40 are unchanged, but the protein is present in the monomeric form. Monomeric MIA40 neither efficiently interacts with nor mediates the import of specific substrates. The import defect is especially severe for NDUFS5, a subunit of complex I of the respiratory chain. As a consequence, NDUFS5 accumulates in the cytosol and undergoes rapid proteasomal degradation. Lack of mitochondrial NDUFS5 in turn results in stalling of complex I assembly. Collectively, we demonstrate that AIFM1 serves two overlapping functions: importing MIA40/CHCHD4 and constituting an integral part of the disulfide relay that ensures efficient interaction of MIA40/CHCHD4 with specific substrates.

Keywords: AIFM1; MIA40-CHCHD4; NDUFS5; complex I; mitochondrial disulfide relay.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis Inducing Factor* / metabolism
  • Disulfides / metabolism
  • Electron Transport Complex I* / metabolism
  • HEK293 Cells
  • Humans
  • Mitochondrial Membrane Transport Proteins* / genetics
  • Mitochondrial Membrane Transport Proteins* / metabolism
  • Mitochondrial Precursor Protein Import Complex Proteins
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism
  • Oxidation-Reduction
  • Protein Transport

Substances

  • AIFM1 protein, human
  • Apoptosis Inducing Factor
  • Disulfides
  • Mitochondrial Membrane Transport Proteins
  • Mitochondrial Precursor Protein Import Complex Proteins
  • Mitochondrial Proteins
  • NDUFS5 protein, human
  • Electron Transport Complex I