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

S Judge, Y M Jang, A Smith, C Selman, T Phillips, J R Speakman, T Hagen, C Leeuwenburgh

Research output: Contribution to journalArticle

96 Citations (Scopus)

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 ( FM) 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 similar to 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.

Original languageEnglish
Number of pages9
JournalAmerican Journal of Physiology-Regulatory Integrative and Comparative Physiology
Volume289
DOIs
Publication statusPublished - 2005

Keywords

  • aging
  • superoxide anion
  • longevity
  • postmitotic
  • calorie restriction
  • RAT SKELETAL-MUSCLE
  • OXIDATIVE STRESS
  • CALORIC RESTRICTION
  • ANTIOXIDANT DEFENSES
  • INTERMYOFIBRILLAR MITOCHONDRIA
  • RADICAL GENERATION
  • LIVER-MITOCHONDRIA
  • LIPID-PEROXIDATION
  • FOOD RESTRICTION
  • CARDIAC-MUSCLE

Cite this

Exercise by lifelong voluntary wheel running reduces subsarcolemmal and interfibrillar mitochondrial hydrogen peroxide production in the heart. / Judge, S ; Jang, Y M ; Smith, A ; Selman, C ; Phillips, T ; Speakman, J R ; Hagen, T ; Leeuwenburgh, C .

In: American Journal of Physiology-Regulatory Integrative and Comparative Physiology, Vol. 289, 2005.

Research output: Contribution to journalArticle

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T1 - Exercise by lifelong voluntary wheel running reduces subsarcolemmal and interfibrillar mitochondrial hydrogen peroxide production in the heart

AU - Judge, S

AU - Jang, Y M

AU - Smith, A

AU - Selman, C

AU - Phillips, T

AU - Speakman, J R

AU - Hagen, T

AU - Leeuwenburgh, C

PY - 2005

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N2 - 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 ( FM) 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 similar to 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.

AB - 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 ( FM) 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 similar to 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.

KW - aging

KW - superoxide anion

KW - longevity

KW - postmitotic

KW - calorie restriction

KW - RAT SKELETAL-MUSCLE

KW - OXIDATIVE STRESS

KW - CALORIC RESTRICTION

KW - ANTIOXIDANT DEFENSES

KW - INTERMYOFIBRILLAR MITOCHONDRIA

KW - RADICAL GENERATION

KW - LIVER-MITOCHONDRIA

KW - LIPID-PEROXIDATION

KW - FOOD RESTRICTION

KW - CARDIAC-MUSCLE

U2 - 10.1152/ajpregu.00396.2005

DO - 10.1152/ajpregu.00396.2005

M3 - Article

VL - 289

JO - American Journal of Physiology-Regulatory Integrative and Comparative Physiology

JF - American Journal of Physiology-Regulatory Integrative and Comparative Physiology

SN - 0363-6119

ER -