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TRANSLATIONAL PHYSIOLOGY

Exercise by lifelong voluntary wheel running reduces subsarcolemmal and interfibrillar mitochondrial hydrogen peroxide production in the heart

¹Biochemistry of Aging Laboratory, Genomics and Biomarkers Core of the Institute on Aging, Department of Aging and Geriatric Research, College of Medicine, University of Florida, Gainesville, Florida; ²Linus Pauling Institute and Department of Biochemistry and Biophysics, Oregon State University, Corvallis, Oregon; ³Department of Medicine (Centre for Diabetes and Endocrinology), University College London Centre for Research on Ageing, London, United Kingdom; and ⁴Aberdeen Centre for Energy Regulation and Obesity, School of Biological Sciences, University of Aberdeen, and Division of Energy Balance and Obesity, Rowett Research Institute, Bucksburn, Aberdeen, Scotland, United Kingdom

Submitted 3 June 2005 ; accepted in final form 15 July 2005

ABSTRACT

Evidence suggests that mitochondrial dysfunction and oxidant production, in association with an accumulation of oxidative damage, contribute to the aging process. Regular physical activity can delay the onset of morbidity, increase mean lifespan, and reduce the risk of developing several pathological states. No studies have examined age-related changes in oxidant production and oxidative stress in both subsarcolemmal (SSM) and interfibrillar (IFM) mitochondria in combination with lifelong exercise. Therefore, we investigated whether long-term voluntary wheel running in Fischer 344 rats altered hydrogen peroxide (H₂O₂) production, antioxidant defenses, and oxidative damage in cardiac SSM and IFM. At 10–11 wk of age, rats were randomly assigned to one of two groups: sedentary and 8% food restriction (sedentary; n = 20) or wheel running and 8% food restriction (runners; n = 20); rats were killed at 24 mo of age. After the age of 6 mo, running activity was maintained at an average of 1,145 ± 248 m/day. Daily energy expenditure determined by doubly labeled water technique showed that runners expended on average 70% more energy per day than the sedentary rats. Long-term voluntary wheel running significantly reduced H₂O₂ production from both SSM (–10.0%) and IFM (–9.6%) and increased daily energy expenditure (kJ/day) significantly in runners compared with sedentary controls. Additionally, MnSOD activity was significantly lowered in SSM and IFM from wheel runners, which may reflect a reduction in mitochondrial superoxide production. Activities of the other major antioxidant enzymes (glutathione peroxidase and catalase) and glutathione levels were not altered by wheel running. Despite the reduction in mitochondrial oxidant production, no significant differences in oxidative stress levels (4-hydroxy-2-nonenal-modified proteins, protein carbonyls, and malondialdehyde) were detected between the two groups. The health benefits of chronic exercise may be, at least partially, due to a reduction in mitochondrial oxidant production; however, we could not detect a significant reduction in several selected parameters of oxidative stress.

aging; superoxide anion; longevity; postmitotic; calorie restriction

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