Dioxin increases reactive oxygen production in mouse liver mitochondria

Toxicol Appl Pharmacol. 2002 Jan 1;178(1):15-21. doi: 10.1006/taap.2001.9314.

Abstract

Dioxin (2,3,7,8-tetrachlorodibenzo-p-dioxin; TCDD) causes an oxidative stress response in liver and several extrahepatic tissues. The subcellular sources and underlying mechanisms of dioxin-induced reactive oxygen, however, are not well understood. In this study, we examined whether mitochondria, organelles that consume the majority of cellular oxygen, might be a source of dioxin-induced reactive oxygen. Female C57BL/6 mice were treated with dioxin (15 microg/kg body wt ip) on 3 consecutive days, and liver mitochondria were examined at 1, 4, and 8 weeks after the first treatment. Mitochondrial aconitase activity, an enzyme inactivated by superoxide, was decreased by 44% at 1 week, 22% at 4 weeks, and returned to control levels at 8 weeks. Dioxin elevated succinate-stimulated mitochondrial H2O2 production twofold at 1 and 4 weeks; H2O2 production remained significantly elevated at 8 weeks. The enhanced H2O2 production was due to neither increased Mn-superoxide dismutase activity nor decreased mitochondrial glutathione peroxidase activity. Dioxin treatment augmented mitochondrial glutathione, but not glutathione disulfide levels, a result that might be explained by increased mitochondrial glutathione reductase activity. Liver ATP levels were significantly lowered at 1 and 4 weeks, the peak times of mitochondrial reactive oxygen production. Increased dioxin-stimulated reactive oxygen at 1 and 4 weeks did not appear to be related to the observed decrease in cytochrome oxidase activity, since State 3 and State 4 respiration were not diminished. To our knowledge, this is the first report to show that dioxin increases mitochondrial respiration-dependent reactive oxygen production, which may play an important role in dioxin-induced toxicity and disease.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Aconitate Hydratase / metabolism
  • Adenosine Triphosphate / metabolism
  • Animals
  • Dioxins / pharmacology*
  • Energy Metabolism / drug effects
  • Female
  • Glutathione / metabolism
  • Glutathione Peroxidase / metabolism
  • Glutathione Reductase / metabolism
  • Hydrogen Peroxide / metabolism
  • Indicators and Reagents
  • Luminol
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria, Liver / drug effects
  • Mitochondria, Liver / enzymology
  • Mitochondria, Liver / metabolism*
  • Oxidation-Reduction
  • Oxidative Stress / drug effects
  • Proteins / metabolism
  • Reactive Oxygen Species / metabolism*
  • Superoxide Dismutase / metabolism

Substances

  • Dioxins
  • Indicators and Reagents
  • Proteins
  • Reactive Oxygen Species
  • Luminol
  • Adenosine Triphosphate
  • Hydrogen Peroxide
  • Glutathione Peroxidase
  • Superoxide Dismutase
  • Glutathione Reductase
  • Aconitate Hydratase
  • Glutathione