Mitochondrial topoisomerase I is critical for mitochondrial integrity and cellular energy metabolism

PLoS One. 2012;7(7):e41094. doi: 10.1371/journal.pone.0041094. Epub 2012 Jul 20.

Abstract

Background: Mitochondria contain their own DNA genome (mtDNA), as well as specific DNA replication and protein synthesis machineries. Relaxation of the circular, double-stranded mtDNA relies on the presence of topoisomerase activity. Three different topoisomerases have been identified in mitochondria: Top1mt, Top3α and a truncated form of Top2β.

Methodology/principal findings: The present study shows the importance of Top1mt in mitochondrial homeostasis. Here we show that Top1mt-/- murine embryonic fibroblasts (MEF) exhibit dysfunctional mitochondrial respiration, which leads decreased ATP production and compensation by increased glycolysis and fatty acid oxidation. ROS production in Top1mt-/- MEF cells is involved in nuclear DNA damage and induction of autophagy. Lack of Top1mt also triggers oxidative stress and DNA damage associated with lipid peroxidation and mitophagy in Top1mt-/- mice.

Conclusion/significance: Together, our data implicate Top1mt for mitochondrial integrity and energy metabolism. The compensation mechanism described here contributes to the survival of Top1mt-/- cells and mice despite alterations of mitochondrial functions and metabolism. Therefore, this study supports a novel model for cellular adaptation to mitochondrial damage.

Publication types

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

MeSH terms

  • Animals
  • Autophagy / genetics
  • DNA Damage
  • DNA Topoisomerases, Type I / genetics
  • DNA Topoisomerases, Type I / metabolism*
  • DNA, Mitochondrial
  • Energy Metabolism* / genetics
  • Fatty Acids / metabolism
  • Glycolysis
  • Lipogenesis / genetics
  • Mice
  • Mice, Knockout
  • Mitochondria / genetics
  • Mitochondria / metabolism*
  • Oxidation-Reduction
  • Oxidative Stress
  • Signal Transduction

Substances

  • DNA, Mitochondrial
  • Fatty Acids
  • DNA Topoisomerases, Type I