Mitochondrial DNA deletions inhibit proteasomal activity and stimulate an autophagic transcript

Free Radic Biol Med. 2007 Jan 1;42(1):32-43. doi: 10.1016/j.freeradbiomed.2006.09.014. Epub 2006 Sep 19.

Abstract

Deletions within the mitochondrial DNA (mtDNA) cause Kearns Sayre syndrome (KSS) and chronic progressive external opthalmoplegia (CPEO). The clinical signs of KSS include muscle weakness, heart block, pigmentary retinopathy, ataxia, deafness, short stature, and dementia. The identical deletions occur and rise exponentially as humans age, particularly in substantia nigra. Deletions at >30% concentration cause deficits in basic bioenergetic parameters, including membrane potential and ATP synthesis, but it is poorly understood how these alterations cause the pathologies observed in patients. To better understand the consequences of mtDNA deletions, we microarrayed six cell types containing mtDNA deletions from KSS and CPEO patients. There was a prominent inhibition of transcripts encoding ubiquitin-mediated proteasome activity, and a prominent induction of transcripts involved in the AMP kinase pathway, macroautophagy, and amino acid degradation. In mutant cells, we confirmed a decrease in proteasome biochemical activity, significantly lower concentration of several amino acids, and induction of an autophagic transcript. An interpretation consistent with the data is that mtDNA deletions increase protein damage, inhibit the ubiquitin-proteasome system, decrease amino acid salvage, and activate autophagy. This provides a novel pathophysiological mechanism for these diseases, and suggests potential therapeutic strategies.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Autophagy*
  • Biomarkers / metabolism*
  • Cells, Cultured
  • DNA, Mitochondrial / genetics*
  • Gene Expression Profiling
  • Humans
  • Kearns-Sayre Syndrome / genetics*
  • Kearns-Sayre Syndrome / metabolism
  • Oligonucleotide Array Sequence Analysis
  • Ophthalmoplegia, Chronic Progressive External / genetics*
  • Ophthalmoplegia, Chronic Progressive External / metabolism
  • Proteasome Endopeptidase Complex / metabolism
  • Proteasome Inhibitors*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sequence Deletion*
  • Transcription, Genetic
  • Ubiquitin / metabolism

Substances

  • Biomarkers
  • DNA, Mitochondrial
  • Proteasome Inhibitors
  • RNA, Messenger
  • Ubiquitin
  • Proteasome Endopeptidase Complex