Human NARP mitochondrial mutation metabolism corrected with alpha-ketoglutarate/aspartate: a potential new therapy

Arch Neurol. 2009 Aug;66(8):951-7. doi: 10.1001/archneurol.2009.134.

Abstract

Objective: To verify whether enhanced substrate-level phosphorylation increases viability and adenosine 5'-triphosphate (ATP) content of cells with neuropathy, ataxia, and retinitis pigmentosa/maternally inherited Leigh syndrome (NARP/MILS) mitochondrial DNA mutations and ATP synthase dysfunction.

Design: We used cell lines "poisoned" with oligomycin, the specific inhibitor of ATP synthase, and "natural" models, including transmitochondrial human cell lines (cybrids) harboring 2 different pathogenic mutations associated with the NARP/MILS phenotypes.

Main outcome measures: Cell survival, morphology, and ATP content.

Results: When normal human fibroblasts cultured in glucose-free medium were forced to increase energy consumption by exposure to the ionophore gramicidin or were energy challenged by oligomycin inhibition, their survival at 72 hours was 5%, but this increased to 70% when the medium was supplemented with alpha-ketoglutarate/aspartate to boost mitochondrial substrate-level phosphorylation. Homoplasmic cybrids harboring the 8993T-->G NARP mutation were also protected from death (75% vs 15% survival at 72 hours) by the supplemented medium and their ATP content was similar to controls.

Conclusions: These results show that ATP synthase-deficient cells can be rescued by increasing mitochondrial substrate-level phosphorylation and suggest potential dietary or pharmacological therapeutic approaches based on the supplementation of alpha-ketoglutarate/aspartate to patients with impaired ATP synthase activity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism*
  • Anti-Infective Agents, Local / pharmacology
  • Aspartic Acid / pharmacology*
  • C-Reactive Protein / genetics*
  • Cell Line
  • Cell Survival / drug effects*
  • Cell Survival / genetics*
  • DNA, Mitochondrial / genetics*
  • Energy Metabolism / drug effects*
  • Energy Metabolism / genetics*
  • Gramicidin / pharmacology
  • Humans
  • Ketoglutaric Acids / pharmacology*
  • Leigh Disease / genetics
  • Mitochondria / drug effects*
  • Mitochondria / genetics*
  • Mitochondrial Proton-Translocating ATPases / antagonists & inhibitors*
  • Mitochondrial Proton-Translocating ATPases / genetics*
  • Mutation*
  • Nerve Tissue Proteins / genetics*
  • Oligomycins / pharmacology*
  • Oxidative Phosphorylation / drug effects
  • Retinitis Pigmentosa / genetics
  • Spinocerebellar Degenerations / genetics

Substances

  • Anti-Infective Agents, Local
  • DNA, Mitochondrial
  • Ketoglutaric Acids
  • Nerve Tissue Proteins
  • Oligomycins
  • neuronal pentraxin
  • Gramicidin
  • Aspartic Acid
  • Adenosine Triphosphate
  • C-Reactive Protein
  • Mitochondrial Proton-Translocating ATPases