Induction of an unregulated channel by mutations in adenine nucleotide translocase suggests an explanation for human ophthalmoplegia

Hum Mol Genet. 2002 Aug 1;11(16):1835-43. doi: 10.1093/hmg/11.16.1835.

Abstract

Adenine nucleotide translocase (Ant) is primarily involved in ATP/ADP exchange across the mitochondrial inner membrane. Recently, the A114P missense mutation in the human Ant1 protein was found to be associated with autosomal dominant progressive external ophthalmoplegia (adPEO). Ant1(A114P) was proposed to cause an imbalance of the mitochondrial deoxynucleotide pool that subsequently affects the accuracy of mtDNA replication, thereby leading to accumulation of mutant mtDNA. In the present study, it has been shown that the A128P mutation of the Saccharomyces cerevisiae Aac2 protein, equivalent to A114P in human Ant1p, does not always affect respiratory growth. However, expression of aac2(A128P) results in depolarization, structural swelling and disintegration of mitochondria, and ultimately an arrest of cell growth in a dominant-negative manner. The aac2(A128P) mutation likely induces an unregulated channel allowing free passage of solutes across the inner membrane. These data raise the possibility that the formation of an unregulated channel, rather than a defect in ATP/ADP exchange, is a direct pathogenic factor in human adPEO. The accumulation of mtDNA mutations might be a consequence of mitochondrial dysfunction.

MeSH terms

  • Adenine Nucleotide Translocator 1 / genetics*
  • Alleles
  • DNA, Mitochondrial / genetics
  • Genes, Dominant
  • Genes, Fungal
  • Humans
  • Membrane Potentials
  • Mitochondria / metabolism
  • Mitochondrial ADP, ATP Translocases / genetics
  • Mitochondrial Swelling
  • Mutation, Missense*
  • Ophthalmoplegia, Chronic Progressive External / enzymology*
  • Ophthalmoplegia, Chronic Progressive External / genetics*
  • Saccharomyces cerevisiae / enzymology
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae Proteins / genetics

Substances

  • Adenine Nucleotide Translocator 1
  • DNA, Mitochondrial
  • PET9 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • Mitochondrial ADP, ATP Translocases