Defective mitochondrial fusion, altered respiratory function, and distorted cristae structure in skin fibroblasts with heterozygous OPA1 mutations

Biochim Biophys Acta. 2012 Oct;1822(10):1570-80. doi: 10.1016/j.bbadis.2012.07.002. Epub 2012 Jul 16.

Abstract

Deleterious consequences of heterozygous OPA1 mutations responsible for autosomal dominant optic atrophy remain a matter of debate. Primary skin fibroblasts derived from patients have shown diverse mitochondrial alterations that were however difficult to resolve in a unifying scheme. To address the potential use of these cells as disease model, we undertook parallel and quantitative analyses of the diverse reported alterations in four fibroblast lines harboring different OPA1 mutations, nonsense or missense, in the guanosine triphosphatase or the C-terminal coiled-coil domains. We tackled several factors potentially underlying discordant reports and showed that fibroblasts with heterozygous OPA1 mutations present with several mitochondrial alterations. These included defective mitochondrial fusion during pharmacological challenge with the protonophore carbonyl cyanide m-chlorophenyl hydrazone, significant mitochondrial elongation with decreased OPA1 and DRP1 proteins, and abnormal mitochondrial fragmentation during glycolysis shortage or exogenous oxidative stress. Respiratory complex IV activity and subunits steady-state were decreased without alteration of the mitochondrial deoxyribonucleic acid size, amount or transcription. Physical link between OPA1 protein and oxidative phosphorylation was shown by reciprocal immunoprecipitation. Altered cristae structure coexisted with normal response to pro-apoptotic stimuli and expression of Bax or Bcl2 proteins. Skin fibroblasts with heterozygous OPA1 mutations thus share significant mitochondrial remodeling, and may therefore be useful for analyzing disease pathophysiology. Identifying whether the observed alterations are also present in ganglion retinal cells, and which of them underlies their degeneration process remains however an essential goal for therapeutic strategy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis / drug effects
  • Apoptosis / genetics
  • Carbonyl Cyanide m-Chlorophenyl Hydrazone / pharmacology
  • Cell Respiration / drug effects
  • Cell Respiration / genetics*
  • Cell Respiration / physiology
  • Cells, Cultured
  • DNA, Mitochondrial / genetics
  • Dynamins
  • Electron Transport Complex IV / genetics
  • Electron Transport Complex IV / metabolism
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • GTP Phosphohydrolases / genetics*
  • GTP Phosphohydrolases / metabolism
  • Glycolysis / drug effects
  • Glycolysis / genetics
  • Heterozygote
  • Humans
  • Membrane Fusion / drug effects
  • Membrane Fusion / genetics*
  • Membrane Fusion / physiology
  • Microtubule-Associated Proteins / genetics*
  • Microtubule-Associated Proteins / metabolism
  • Mitochondria / drug effects
  • Mitochondria / genetics*
  • Mitochondria / metabolism
  • Mitochondrial Proteins / genetics*
  • Mitochondrial Proteins / metabolism
  • Optic Atrophy, Autosomal Dominant / genetics
  • Optic Atrophy, Autosomal Dominant / metabolism
  • Oxidative Phosphorylation / drug effects
  • Oxidative Stress / drug effects
  • Oxidative Stress / genetics
  • Protein Structure, Tertiary / drug effects
  • Protein Structure, Tertiary / genetics
  • Skin / cytology
  • Skin / drug effects
  • Skin / metabolism
  • Skin Physiological Phenomena / drug effects
  • Skin Physiological Phenomena / genetics*
  • bcl-2-Associated X Protein / genetics
  • bcl-2-Associated X Protein / metabolism
  • bcl-Associated Death Protein / genetics
  • bcl-Associated Death Protein / metabolism

Substances

  • DNA, Mitochondrial
  • Microtubule-Associated Proteins
  • Mitochondrial Proteins
  • bcl-2-Associated X Protein
  • bcl-Associated Death Protein
  • Carbonyl Cyanide m-Chlorophenyl Hydrazone
  • Electron Transport Complex IV
  • GTP Phosphohydrolases
  • OPA1 protein, human
  • DNM1L protein, human
  • Dynamins