Limited exercise capacity in heterozygous manganese superoxide dismutase gene-knockout mice: roles of superoxide anion and nitric oxide

Circulation. 2005 Mar 29;111(12):1480-6. doi: 10.1161/01.CIR.0000159261.11520.63. Epub 2005 Mar 21.

Abstract

Background: We have reported that there is a limitation of exercise capacity in mice with defects in the expression of endothelial nitric oxide (NO) synthase, which is associated with a greater increase in whole-body oxygen consumption (VO2). We hypothesized that in states in which superoxide anion (O2-) is increased, especially in the mitochondria, whole-body VO2 will be increased because of the inactivation of NO, and consequently, exercise capacity will be reduced.

Methods and results: Heterozygous manganese superoxide anion dismutase (SOD2) gene-knockout mice (SOD2+/-), in which SOD2 activity is reduced by 30% to 80%, and wild-type control mice (SOD2+/+) were treadmill-tested to measure indices defining exercise capacity. Tempol was given to each mouse for 7 days by an intraperitoneal injection to scavenge O2- before a second treadmill testing. VO2 and carbon dioxide production (VCO2) at rest were increased in SOD2+/-. The work (vertical distance run x body weight) to exhaustion was decreased in SOD2+/-. When the maximum VO2 and VCO2 were corrected to per work unit, they were increased in SOD2+/-. Tempol normalized basal VO2 and VCO2 and improved the work to exhaustion and corrected VO2 and VCO2 in SOD2+/-. VO2 of skeletal muscle was measured in vitro. Bradykinin-induced reduction in VO2 in vitro was attenuated in SOD2+/-, and was acutely restored by Tempol. There was a decrease in SOD2 protein level and a concomitant increase in lucigenin-detectable O2- production in skeletal muscle from SOD2+/-.

Conclusions: These results suggest that exercise capacity is reduced in conditions in which superoxide anion is increased, and this is associated with a greater increase in whole-body oxygen consumption in SOD2+/- compared with SOD2+/+.

Publication types

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

MeSH terms

  • Animals
  • Carbon Dioxide / metabolism
  • Cyclic N-Oxides / administration & dosage
  • Cyclic N-Oxides / pharmacology
  • Exercise Test
  • Free Radical Scavengers / administration & dosage
  • Free Radical Scavengers / pharmacology
  • Heterozygote
  • Male
  • Mice
  • Mice, Knockout
  • Muscle, Skeletal / enzymology
  • Muscle, Skeletal / metabolism
  • Nerve Tissue Proteins / analysis
  • Nitric Oxide / analysis
  • Nitric Oxide Synthase / analysis
  • Nitric Oxide Synthase Type I
  • Nitric Oxide Synthase Type II
  • Nitric Oxide Synthase Type III
  • Oxygen Consumption / drug effects
  • Physical Endurance / drug effects
  • Physical Endurance / genetics*
  • Spin Labels
  • Superoxide Dismutase / deficiency
  • Superoxide Dismutase / genetics*
  • Superoxide Dismutase / physiology*
  • Superoxides / analysis

Substances

  • Cyclic N-Oxides
  • Free Radical Scavengers
  • Nerve Tissue Proteins
  • Spin Labels
  • Superoxides
  • Carbon Dioxide
  • Nitric Oxide
  • Nitric Oxide Synthase
  • Nitric Oxide Synthase Type I
  • Nitric Oxide Synthase Type II
  • Nitric Oxide Synthase Type III
  • Nos1 protein, mouse
  • Nos3 protein, mouse
  • Superoxide Dismutase
  • tempol