Human mitochondrial cytochrome c oxidase assembly factor COX18 acts transiently as a membrane insertase within the subunit 2 maturation module

J Biol Chem. 2017 May 12;292(19):7774-7783. doi: 10.1074/jbc.M117.778514. Epub 2017 Mar 22.

Abstract

Defects in mitochondrial cytochrome c oxidase or respiratory chain complex IV (CIV) assembly are a frequent cause of human mitochondrial disorders. Specifically, mutations in four conserved assembly factors impinging the biogenesis of the mitochondrion-encoded catalytic core subunit 2 (COX2) result in myopathies. These factors afford stability of newly synthesized COX2 (the dystonia-ataxia syndrome protein COX20), a protein with two transmembrane domains, and maturation of its copper center, CuA (cardiomyopathy proteins SCO1, SCO2, and COA6). COX18 is an additional COX2 assembly factor that belongs to the Oxa1 family of membrane protein insertases. Here, we used a gene-editing approach to generate a human COX18 knock-out HEK293T cell line that displays isolated complete CIV deficiency. We demonstrate that COX20 stabilizes COX2 during insertion of its N-proximal transmembrane domain, and subsequently, COX18 transiently interacts with COX2 to promote translocation across the inner membrane of the COX2 C-tail that contains the apo-CuA site. The release of COX18 from this complex coincides with the binding of the SCO1-SCO2-COA6 copper metallation module to COX2-COX20 to finalize COX2 biogenesis. Therefore, COX18 is a new candidate when screening for mitochondrial disorders associated with isolated CIV deficiency.

Keywords: COX18; COX2; COX20; SCO1; SCO2; cardiomyopathy; cytochrome c oxidase (complex IV); mitochondrial metabolism; mitochondrial respiratory chain complex; transcription activator-like effector nuclease (TALEN).

MeSH terms

  • Cardiomyopathies / metabolism
  • Carrier Proteins / metabolism
  • Catalytic Domain
  • Cell Line
  • Cell Membrane / metabolism
  • Citrate (si)-Synthase / metabolism
  • Copper / chemistry
  • Cyclooxygenase 2 / metabolism
  • Electron Transport Complex IV / metabolism*
  • Endopeptidase K / metabolism
  • Gene Editing
  • Gene Knockout Techniques
  • HEK293 Cells
  • Humans
  • Immunohistochemistry
  • Membrane Proteins / metabolism*
  • Mitochondria / metabolism
  • Mitochondrial Proteins / metabolism*
  • Molecular Chaperones
  • Muscular Diseases / metabolism
  • Mutation
  • Nuclear Proteins / metabolism
  • Plasmids / metabolism
  • Protein Transport

Substances

  • COA6 protein, human
  • COX18 protein, human
  • Carrier Proteins
  • Membrane Proteins
  • Mitochondrial Proteins
  • Molecular Chaperones
  • Nuclear Proteins
  • OXA1 protein
  • SCO1 protein, human
  • SCO2 protein, human
  • Copper
  • Cyclooxygenase 2
  • PTGS2 protein, human
  • COX20 protein, human
  • Electron Transport Complex IV
  • Citrate (si)-Synthase
  • Endopeptidase K