The mitochondrial metallochaperone SCO1 maintains CTR1 at the plasma membrane to preserve copper homeostasis in the murine heart

Hum Mol Genet. 2017 Dec 1;26(23):4617-4628. doi: 10.1093/hmg/ddx344.

Abstract

SCO1 is a ubiquitously expressed, mitochondrial protein with essential roles in cytochrome c oxidase (COX) assembly and the regulation of copper homeostasis. SCO1 patients present with severe forms of early onset disease, and ultimately succumb from liver, heart or brain failure. However, the inherent susceptibility of these tissues to SCO1 mutations and the clinical heterogeneity observed across SCO1 pedigrees remain poorly understood phenomena. To further address this issue, we generated Sco1hrt/hrt and Sco1stm/stm mice in which Sco1 was specifically deleted in heart and striated muscle, respectively. Lethality was observed in both models due to a combined COX and copper deficiency that resulted in a dilated cardiomyopathy. Left ventricular dilation and loss of heart function was preceded by a temporal decrease in COX activity and copper levels in the longer-lived Sco1stm/stm mice. Interestingly, the reduction in copper content of Sco1stm/stm cardiomyocytes was due to the mislocalisation of CTR1, the high affinity transporter that imports copper into the cell. CTR1 was similarly mislocalized to the cytosol in the heart of knockin mice carrying a homozygous G115S substitution in Sco1, which in humans causes a hypertrophic cardiomyopathy. Our current findings in the heart are in marked contrast to our prior observations in the liver, where Sco1 deletion results in a near complete absence of CTR1 protein. These data collectively argue that mutations perturbing SCO1 function have tissue-specific consequences for the machinery that ultimately governs copper homeostasis, and further establish the importance of aberrant mitochondrial signaling to the etiology of copper handling disorders.

MeSH terms

  • Animals
  • Cardiomyopathy, Hypertrophic / genetics
  • Cardiomyopathy, Hypertrophic / metabolism
  • Cation Transport Proteins / metabolism*
  • Cell Membrane / metabolism
  • Copper / deficiency
  • Copper / metabolism*
  • Copper Transporter 1
  • Disease Models, Animal
  • Electron Transport Complex IV / genetics
  • Electron Transport Complex IV / metabolism*
  • Homeostasis
  • Ion Transport
  • Metallochaperones / genetics
  • Metallochaperones / metabolism
  • Mice
  • Mice, Transgenic
  • Mitochondria, Heart / metabolism*
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism
  • Molecular Chaperones
  • Myocardium / metabolism*
  • Myocytes, Cardiac / metabolism
  • Oxidation-Reduction
  • Signal Transduction

Substances

  • Cation Transport Proteins
  • Copper Transporter 1
  • Metallochaperones
  • Mitochondrial Proteins
  • Molecular Chaperones
  • SCO1 protein, mouse
  • Slc31a1 protein, mouse
  • Copper
  • Electron Transport Complex IV

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