Mutations in valosin-containing protein (VCP) decrease ADP/ATP translocation across the mitochondrial membrane and impair energy metabolism in human neurons

J Biol Chem. 2017 May 26;292(21):8907-8917. doi: 10.1074/jbc.M116.762898. Epub 2017 Mar 30.

Abstract

Mutations in the gene encoding valosin-containing protein (VCP) lead to multisystem proteinopathies including frontotemporal dementia. We have previously shown that patient-derived VCP mutant fibroblasts exhibit lower mitochondrial membrane potential, uncoupled respiration, and reduced ATP levels. This study addresses the underlying basis for mitochondrial uncoupling using VCP knockdown neuroblastoma cell lines, induced pluripotent stem cells (iPSCs), and iPSC-derived cortical neurons from patients with pathogenic mutations in VCP Using fluorescent live cell imaging and respiration analysis we demonstrate a VCP mutation/knockdown-induced dysregulation in the adenine nucleotide translocase, which results in a slower rate of ADP or ATP translocation across the mitochondrial membranes. This deregulation can explain the mitochondrial uncoupling and lower ATP levels in VCP mutation-bearing neurons via reduced ADP availability for ATP synthesis. This study provides evidence for a role of adenine nucleotide translocase in the mechanism underlying altered mitochondrial function in VCP-related degeneration, and this new insight may inform efforts to better understand and manage neurodegenerative disease and other proteinopathies.

Keywords: ADP; ANT; ATP; VCP; amyotrophic lateral sclerosis (ALS) (Lou Gehrig disease); induced pluripotent stem cell (iPS cell) (iPSC); mitochondria.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Diphosphate / genetics
  • Adenosine Diphosphate / metabolism*
  • Adenosine Triphosphatases* / genetics
  • Adenosine Triphosphatases* / metabolism
  • Adenosine Triphosphate / genetics
  • Adenosine Triphosphate / metabolism*
  • Biological Transport, Active / physiology
  • Cell Cycle Proteins* / genetics
  • Cell Cycle Proteins* / metabolism
  • Cell Line, Tumor
  • Humans
  • Induced Pluripotent Stem Cells / metabolism
  • Induced Pluripotent Stem Cells / pathology
  • Mitochondrial ADP, ATP Translocases / genetics
  • Mitochondrial ADP, ATP Translocases / metabolism
  • Mitochondrial Membranes / metabolism*
  • Mutation*
  • Neurodegenerative Diseases / genetics
  • Neurodegenerative Diseases / metabolism
  • Neurons / metabolism*
  • Neurons / pathology
  • Proteostasis Deficiencies / genetics
  • Proteostasis Deficiencies / metabolism
  • Valosin Containing Protein

Substances

  • Cell Cycle Proteins
  • Adenosine Diphosphate
  • Adenosine Triphosphate
  • Mitochondrial ADP, ATP Translocases
  • Adenosine Triphosphatases
  • VCP protein, human
  • Valosin Containing Protein