Impaired adaptability of in vivo mitochondrial energetics to acute oxidative insult in aged skeletal muscle

Mech Ageing Dev. 2012 Sep-Oct;133(9-10):620-8. doi: 10.1016/j.mad.2012.08.002. Epub 2012 Aug 19.

Abstract

Periods of elevated reactive oxygen species (ROS) production are a normal part of mitochondrial physiology. However, little is known about age-related changes in the mitochondrial response to elevated ROS in vivo. Significantly, ROS-induced uncoupling of oxidative phosphorylation has received attention as a negative feedback mechanism to reduce mitochondrial superoxide production. Here we use a novel in vivo spectroscopy system to test the hypothesis that ROS-induced uncoupling is diminished in aged mitochondria. This system simultaneously acquires (31)P magnetic resonance and near-infrared optical spectra to non-invasively measure phosphometabolite and O(2) concentrations in mouse skeletal muscle. Using low dose paraquat to elevate intracellular ROS we assess in vivo mitochondrial function in young, middle aged, and old mice. Oxidative phosphorylation was uncoupled to the same degree in response to ROS at each age, but this uncoupling was associated with loss of phosphorylation capacity and total ATP in old mice only. Using mice lacking UCP3 we demonstrate that this in vivo uncoupling is independent of this putative uncoupler of skeletal muscle mitochondria. These data indicate that ROS-induced uncoupling persists throughout life, but that oxidative stress leads to mitochondrial deficits and loss of ATP in aged organisms that may contribute to impaired function and degeneration.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / genetics
  • Adenosine Triphosphate / metabolism
  • Aging / genetics
  • Aging / metabolism*
  • Aging / pathology
  • Animals
  • Female
  • Ion Channels / genetics
  • Ion Channels / metabolism
  • Mice
  • Mice, Knockout
  • Mitochondria, Muscle / genetics
  • Mitochondria, Muscle / metabolism*
  • Mitochondria, Muscle / pathology
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism
  • Muscle, Skeletal / metabolism*
  • Muscle, Skeletal / pathology
  • Oxidative Phosphorylation*
  • Oxidative Stress*
  • Oxygen / metabolism
  • Reactive Oxygen Species / metabolism
  • Regeneration / genetics
  • Uncoupling Protein 3

Substances

  • Ion Channels
  • Mitochondrial Proteins
  • Reactive Oxygen Species
  • Ucp3 protein, mouse
  • Uncoupling Protein 3
  • Adenosine Triphosphate
  • Oxygen