COX19 mediates the transduction of a mitochondrial redox signal from SCO1 that regulates ATP7A-mediated cellular copper efflux

Mol Biol Cell. 2013 Mar;24(6):683-91. doi: 10.1091/mbc.E12-09-0705. Epub 2013 Jan 23.

Abstract

SCO1 and SCO2 are metallochaperones whose principal function is to add two copper ions to the catalytic core of cytochrome c oxidase (COX). However, affected tissues of SCO1 and SCO2 patients exhibit a combined deficiency in COX activity and total copper content, suggesting additional roles for these proteins in the regulation of cellular copper homeostasis. Here we show that both the redox state of the copper-binding cysteines of SCO1 and the abundance of SCO2 correlate with cellular copper content and that these relationships are perturbed by mutations in SCO1 or SCO2, producing a state of apparent copper overload. The copper deficiency in SCO patient fibroblasts is rescued by knockdown of ATP7A, a trans-Golgi, copper-transporting ATPase that traffics to the plasma membrane during copper overload to promote efflux. To investigate how a signal from SCO1 could be relayed to ATP7A, we examined the abundance and subcellular distribution of several soluble COX assembly factors. We found that COX19 partitions between mitochondria and the cytosol in a copper-dependent manner and that its knockdown partially rescues the copper deficiency in patient cells. These results demonstrate that COX19 is necessary for the transduction of a SCO1-dependent mitochondrial redox signal that regulates ATP7A-mediated cellular copper efflux.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphatases / genetics
  • Adenosine Triphosphatases / metabolism*
  • Carrier Proteins / metabolism
  • Cation Transport Proteins / genetics
  • Cation Transport Proteins / metabolism*
  • Cell Line
  • Cell Membrane / metabolism
  • Copper / metabolism*
  • Copper-Transporting ATPases
  • Fibroblasts
  • Humans
  • Ion Transport
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Mitochondria / genetics
  • Mitochondria / metabolism*
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism*
  • Molecular Chaperones
  • Oxidation-Reduction
  • RNA Interference
  • RNA, Small Interfering
  • Signal Transduction

Substances

  • COX19 protein, human
  • Carrier Proteins
  • Cation Transport Proteins
  • Membrane Proteins
  • Mitochondrial Proteins
  • Molecular Chaperones
  • RNA, Small Interfering
  • SCO1 protein, human
  • SCO2 protein, human
  • Copper
  • Adenosine Triphosphatases
  • ATP7A protein, human
  • Copper-Transporting ATPases