Impaired Bioenergetics in Mutant Mitochondrial DNA Determines Cell Fate During Seizure-Like Activity

Mol Neurobiol. 2019 Jan;56(1):321-334. doi: 10.1007/s12035-018-1078-9. Epub 2018 Apr 27.

Abstract

Mutations in genes affecting mitochondrial proteins are increasingly recognised in patients with epilepsy, but the factors determining cell fate during seizure activity in these mutations remain unknown. Fluorescent dye imaging techniques were applied to fibroblast cell lines from patients suffering from common mitochondrial mutations and to age-matched controls. Using live cell imaging techniques in fibroblasts, we show that fibroblasts with mutations in the mitochondrial genome had reduced mitochondrial membrane potential and NADH pools and higher redox indices, indicative of respiratory chain dysfunction. Increasing concentrations of ferutinin, a Ca2+ ionophore, led to oscillatory Ca2+ signals in fibroblasts resembling dynamic Ca2+ changes that occur during seizure-like activity. Co-monitoring of mitochondrial membrane potential (ΔΨm) changes induced by ferutinin showed accelerated membrane depolarisation and cell collapse in fibroblasts with mutations in the mitochondrial genome when compared to controls. Ca2+ flash photolysis using caged Ca2+ confirmed impaired Ca2+ handling in fibroblasts with mitochondrial mutations. Findings indicate that intracellular Ca2+ levels cannot be compensated during periods of hyperexcitability, leading to Ca2+ overload and subsequent cell death in mitochondrial diseases.

Keywords: Ca2+; Epilepsy; Fibroblasts; Mitochondrial mutation; PTP opening.

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Calcium / metabolism
  • Calcium Signaling
  • Cell Line
  • Cell Lineage / genetics*
  • Cell Respiration
  • DNA, Mitochondrial / genetics*
  • Energy Metabolism*
  • Fibroblasts / metabolism
  • Fibroblasts / pathology
  • Humans
  • Membrane Potential, Mitochondrial
  • Mitochondria / metabolism
  • Mutation / genetics*
  • NAD / metabolism
  • Oxidation-Reduction
  • Seizures / genetics*
  • Seizures / pathology*

Substances

  • DNA, Mitochondrial
  • NAD
  • Adenosine Triphosphate
  • Calcium