Up-regulation of avian uncoupling protein in cold-acclimated and hyperthyroid ducklings prevents reactive oxygen species production by skeletal muscle mitochondria

BMC Physiol. 2010 Apr 28:10:5. doi: 10.1186/1472-6793-10-5.

Abstract

Background: Although identified in several bird species, the biological role of the avian homolog of mammalian uncoupling proteins (avUCP) remains extensively debated. In the present study, the functional properties of isolated mitochondria were examined in physiological or pharmacological situations that induce large changes in avUCP expression in duckling skeletal muscle.

Results: The abundance of avUCP mRNA, as detected by RT-PCR in gastrocnemius muscle but not in the liver, was markedly increased by cold acclimation (CA) or pharmacological hyperthyroidism but was down-regulated by hypothyroidism. Activators of UCPs, such as superoxide with low doses of fatty acids, stimulated a GDP-sensitive proton conductance across the inner membrane of muscle mitochondria from CA or hyperthyroid ducklings. The stimulation was much weaker in controls and not observed in hypothyroid ducklings or in any liver mitochondrial preparations. The production of endogenous mitochondrial reactive oxygen species (ROS) was much lower in muscle mitochondria from CA and hyperthyroid ducklings than in the control or hypothyroid groups. The addition of GDP markedly increased the mitochondrial ROS production of CA or hyperthyroid birds up to, or above, the level of control or hypothyroid ducklings. Differences in ROS production among groups could not be attributed to changes in antioxidant enzyme activities (superoxide dismutase or glutathione peroxidase).

Conclusion: This work provides the first functional in vitro evidence that avian UCP regulates mitochondrial ROS production in situations of enhanced metabolic activity.

MeSH terms

  • Acclimatization / physiology*
  • Animals
  • Cold Temperature
  • Ducks / growth & development
  • Ducks / metabolism*
  • Energy Metabolism / physiology
  • Glutathione Peroxidase / metabolism
  • Hydrogen Peroxide / metabolism
  • Hyperthyroidism / metabolism*
  • Hyperthyroidism / physiopathology
  • Ion Channels / genetics
  • Ion Channels / metabolism*
  • Lipids / blood
  • Male
  • Membrane Potential, Mitochondrial / physiology
  • Mitochondria / metabolism
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism*
  • Muscle, Skeletal / metabolism*
  • Oxidative Stress / physiology
  • Oxygen Consumption / physiology
  • RNA, Messenger / metabolism
  • Reactive Oxygen Species / metabolism
  • Species Specificity
  • Superoxide Dismutase / metabolism
  • Triiodothyronine / blood
  • Uncoupling Protein 1
  • Up-Regulation / physiology

Substances

  • Ion Channels
  • Lipids
  • Mitochondrial Proteins
  • RNA, Messenger
  • Reactive Oxygen Species
  • Uncoupling Protein 1
  • Triiodothyronine
  • Hydrogen Peroxide
  • Glutathione Peroxidase
  • Superoxide Dismutase