Bioenergetic consequences of accumulating the common 4977-bp mitochondrial DNA deletion

Eur J Biochem. 1998 Oct 1;257(1):192-201. doi: 10.1046/j.1432-1327.1998.2570192.x.

Abstract

Mutations and deletions in mitochondrial DNA (mtDNA) lead to a number of human diseases characterized by neuromuscular degeneration. Accumulation of truncated mtDNA molecules (delta-mtDNA) lacking a specific 4977-bp fragment, the common deletion, leads to three related mtDNA diseases: Pearson's syndrome; Kearns-Sayre syndrome; and chronic progressive external ophthalmoplegia (CPEO). In addition, the proportion of delta-mtDNA present increases with age in a range of tissues. Consequently, there is considerable interest in the effects of the accumulation of delta-mtDNA on cell function. The 4977-bp deletion affects genes encoding 7 polypeptide components of the mitochondrial respiratory chain, and 5 of the 22 tRNAs necessary for mitochondrial protein synthesis. To determine how the accumulation of delta-mtDNA affects oxidative phosphorylation we constructed a series of cybrids by fusing a human osteosarcoma cell line depleted of mtDNA (rho0) with enucleated skin fibroblasts from a CPEO patient. The ensuing cybrids contained 0-86% delta-mtDNA and all had volumes, protein contents, plasma-membrane potentials and mitochondrial contents similar to those of the parental cell line. The bioenergetic consequences of accumulating delta-mtDNA were assessed by measuring the mitochondrial membrane potential, rate of ATP synthesis and ATP/ADP ratio. In cybrids containing less than 50-55% delta-mtDNA, these bioenergetic functions were equivalent to those of cybrids with intact mtDNA. However, once the proportion of delta-mtDNA exceeded this threshold, the mitochondrial membrane potential, rate of ATP synthesis, and cellular ATP/ADP ratio decreased. These bioenergetic deficits will contribute to the cellular pathology associated with the accumulation of delta-mtDNA in the target tissues of patients with mtDNA diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Diphosphate / metabolism
  • Adenosine Triphosphate / biosynthesis
  • Adenosine Triphosphate / metabolism
  • DNA, Mitochondrial / genetics*
  • DNA, Mitochondrial / metabolism
  • Energy Metabolism
  • Humans
  • Intracellular Membranes / metabolism
  • Intracellular Membranes / physiology
  • Kinetics
  • Membrane Potentials
  • Microscopy, Electron
  • Mitochondria / metabolism
  • Mitochondria / ultrastructure
  • Sequence Deletion*
  • Tumor Cells, Cultured

Substances

  • DNA, Mitochondrial
  • Adenosine Diphosphate
  • Adenosine Triphosphate