Oxidative Medicine and Cellular Longevity

Review Article

Exercise Modulates Oxidative Stress and Inflammation in Aging and Cardiovascular Diseases

Table 3

Effects of exercise training on expression and activity of antioxidant and prooxidant enzymes.


Enzyme	Species		Tissue	Exercise mode	Effect of physical activity/exercise	Reference

SOD	Human	Untrained males = 9	Erythrocytes	High-intensity endurance training for 12 weeks	Activity increased after training	[354]
		Healthy young men and women = 17	Erythrocytes	16 weeks of training then an acute bout of aerobic exercise for 30 min	Transient increase in activity after acute exercise	[355]
		Athletes = 18 and sedentary control = 6	Erythrocyte	Marathon or sprint training	Higher activity in sprint-trained athletes and marathon runners	[352]
		Winter swimmers = 40 and controls = 36	Erythrocyte	Regular winter swimming	Higher activity in winter swimmers	[353]
	Rats	Males, young and aged (17 months)	Lung, heart, and liver	Regular swimming exercise for 1 year	Increased activity in lung and heart of old rats relative to sedentary controls	[356]
		Males, young and aged	Heart	Treadmill endurance exercise for 2 months	Increased activity in young and aged rats	[316]
		Male, young, adult, and aged	Skeletal muscles	Exercise training for 10 weeks	Increased activity in deep vastus lateralis muscle of young rats only	[311]
		Males, 16-17 weeks	Heart and skeletal muscle	Sprint training on a treadmill for 6 weeks	Unchanged activity	[383]
		Females, 4 months	Ventricles	Endurance exercise training for 10 weeks	Increased activity	[293]
		Females, 17 weeks	Ventricles	High-intensity exercise treadmill for 10 weeks	Increased activity	[357]
		Males, adults	Heart	Treadmill training for 12 or 24 weeks	Increased activity after 24 but not 12 weeks	[292]
		Males, myocardial infarcted	Aorta	Treadmill training 5 times per week, 60 min/day for 11 weeks	Increased activity but not expression	[359]
	Mice	Males, aged 29–32 months	Aorta	Voluntary wheel running for 10–14 weeks	Increased activity	[360]
		Males and females, aged 28, 52, and 78 weeks	Bain, heart, liver, and kidney	Long term moderate-intensity treadmill exercise	Increased activity in all tissues at 52 but not 78 weeks old	[23]
		Females, 3 months	Kidney, heart, and skeletal muscle	Treadmill exercise for 8 weeks	Increased activity	[136]
		Males (6–8 weeks)	Ventricles	Swimming training for 14 weeks	No change in activity	[298]
	Microtus	Short-tailed field vole Microtus agrestis	Skeletal muscle and heart	Voluntary running over 1 or 7 days	Reduced activity in the heart	[401]

SOD-1	Human		Umbilical vein endothelial cells	Laminar fluid shear stress	mRNA and protein levels increased after 24 hours	[350]
			Endothelial progenitor cells	Shear stress	Increased mRNA expression and activity	[349]
			Aortic endothelial cells	Fluid shear stress	Increased protein expression	[351]
		Patients with congestive heart failure = 14	Skeletal muscle	12 weeks of training	Increased gene expression	[361]
	Rats	Young (3 months) and aged (30 months)	Skeletal muscles	4.5 weeks of resistance exercise	Protein expression increased in young rats but decreased in old rats	[222]
		Males, young (3–5 months) and aged (24–27 months)	Skeletal muscles and heart	Exhausting treadmill running	Increased activity in skeletal muscles and heart of young rats and hearts of old rats	[358]
		Males, aged 24 months	Hearts	Treadmill training 30 m/min, 45 min/day, 5 days/week for 6 weeks	Protein expression increased	[295]
		Males, young (2 months) and old (22 months)	Soleus muscle feed arteries	Exercise training for 10–12 weeks	No change in protein expression	[366]
		Females, 12 months old	Hippocampus	Treadmill training for 15 weeks	Protein expression increased	[307]
		Females	Skeletal muscle	Acute bout of exhaustive treadmill exercise	Increased protein level but not mRNA or activity	[362]
		Males, adults	Heart	Acute session of treadmill running for 25–30 min	No change	[230]
		Females, adults	Ventricles	20 weeks of training	Increased protein expression	[363]
		Males, high caloric fed	Aorta and mesenteric artery	Running 60 min, 5 days/week for 12 weeks	Increased expression relative to sedentary controls	[364]
	Mice		Aorta	Treadmill running 15 m/min, 30 min/day, 5 days/week for 3 weeks	No change in protein expression	[367]
		Males, diabetic young	Aorta	Treadmill exercise for 10 weeks	Increased protein expression	[194]
	Pigs	Females	Aortic endothelial cells	Chronic exercise training for 16–19 weeks	Protein and activity increased	[365]

SOD-2	Human	Men = 18	Plasma	Swimming or running for 3 months then a bout of acute exercise	Protein level increased by acute exercise	[373]
		Men 62 ± 3 years Physically active = 13 and sedentary = 26	Vascular endothelial cells from the brachial artery	Habitual aerobic exercise	Higher protein expression than sedentary men	[133]
	Rats	Males, 10-11 weeks	Cardiac mitochondria	Long term voluntary wheel running	Reduced activity	[402]
		Males, adults	Heart	Treadmill training for 12 or 24 weeks	Increased activity after 24 but not 12 weeks	[292]
		Males, adults	Heart	Acute session of treadmill running for 25–30 min	Activity increased at 0.5 and 48 h, and protein content increased at 48 h after exercise	[230]
		Females, 4 months	Heart	3–5 consecutive days of treadmill exercise [60 min/day at 60–70% maximal O₂ uptake]	Increased activity	[368]
		Females, 4 months	Ventricles	Treadmill exercise (60 min/day) at 25 degrees for 3 days	Increased activity	[369]
		Females, adults	Ventricles	20 weeks of training	Increased protein expression	[363]
		Males subjected to IR	Ventricles	3 consecutive days of intensive treadmill exercise 60 min/day, at 30 m/min	Increased activity of SOD-2 but not SOD-1	[370]
		Males, aged 24 months	Heart	Treadmill training 30 m/min, 45 min/day, 5 days/week for 6 weeks	Protein expression increased	[295]
		Males, young (4 months) and aged (21 months)	Heart	Acute exercise 60 min at 70–75% of maximum oxygen consumption	Activity increased in old rats	[297]
		Young (6 months) and aged 27 months	Left ventricle	Treadmill for 60 min/day, 5 days/week for a total of 12 weeks	Protein expression and activity increased in the aged group compared with sedentary control	[296]
		Females	Skeletal muscle	Treadmill running for 10 weeks	Increased activity and protein expression	[371]
		Females	Skeletal muscles	Acute bout of exhaustive treadmill exercise	Increased mRNA level in deep vastus lateralis muscle. Increased protein level in superficial vastus lateralis	[362]
		Male Zucker diabetic fatty rats (18 weeks)	Skeletal muscles	Swimming training for 6 weeks	Protein expression increased	[375]
		Males, 2 months	Plasma	Treadmill training 3 days/week for 14 weeks	Increased activity	[137]
		Males, obese Zucker	Liver	Treadmill running at 20 m/min for 1 h/day, 7 days/week, for 8 weeks	mRNA and protein levels and activity increased	[372]
		Male, young (3 months) and aged (23 months)	Aorta	Treadmill training for 12 weeks	Increased protein expression in aged rats	[138]
	Mice	Male, diabetic and young	Heart	Motorized exercise-wheel for 1 h/day, 5 days/week for 8 weeks	Increased protein expression	[374]
		Male, diabetic and young	Aorta	Motorized exercise-wheel for 1 h/day, 5 days/week for 8 weeks	Increased protein expression	[376]
	Pigs	Females	Aortic endothelial cells	Chronic exercise training for 16–19 weeks	No change in protein levels	[365]

SOD-3	Human	Men 62 ± 3 years Physically active = 13 and sedentary = 26	Vascular endothelial cells from the brachial artery	Habitual aerobic exercise	Higher activity than sedentary men	[133]
		Men = 18	Plasma	Swimming or running for 3 months then a bout of acute exercise	Reduced protein level after endurance training but increased by acute exercise	[373]
	Rats	Males, young (2 months) and old (22 months)	Soleus muscle feed arteries	Exercise training for 10–12 weeks	Increased protein expression in old rats	[366]
	Mice		Aorta	Treadmill running 15 m/min, 30 min/day, 5 days/ week for 3 weeks	Increased protein expression	[367]

CAT	Human	Athletes = 18 and sedentary control = 6	Erythrocytes	Marathon or sprint training	Lower activity than controls in sprint-trained athletes	[352]
		Winter swimmers = 40 and controls = 36	Erythrocytes	Regular winter swimming	Higher activity in winter swimmers	[353]
	Rats	Males, young and aged (17 months)	Lung, heart and liver	Regular swimming exercise for 1 year	Increased activity in liver of old rats relative to sedentary controls	[356]
		Aged	Brain, liver, lung, muscle, and testes	Regular exercise	Increased activity in all tissues	[377]
		Males, young (4 months) and aged (21 months)	Heart	Acute exercise 60 min at 70–75% of maximum oxygen consumption	Activity increased in young and old rats	[297]
		Male, young and aged	Heart	Treadmill exercise for 2 months	Increased activity in young and aged rats	[316]
		Males, young (9 months) and aged (20 months)	Liver	Regular exercise	Increased activity	[126]
		Male, young (8 months) and aged (22 months)	Brain	Swimming 30 min/day, 5 days/week for 12 weeks	Increased activity in hippocampus in young and old rats	[378]
		Male, young (8 weeks), adult (12 months), and old (24 months)	Skeletal muscles	Exercise training for 10 weeks	Decreased activity in soleus muscle of adult and old rats	[311]
		Males (4 months)	Cardiac mitochondria	Treadmill for 16 weeks (5 days/week, 60 min/day, 25 m/min)	Increased activity	[379]
		Males, adults	Heart	Treadmill training for 12 or 24 weeks	Reduced activity after 24 but not 12 weeks	[292]
		Females, 4 months	Ventricles	Endurance exercise training for 10 weeks	No change in activity	[293]
		Males subjected to IR	Ventricles	3 consecutive days of intensive treadmill exercise 60 min/day, at 30 m/min	Increased activity	[370]
		Females	Skeletal muscle	Treadmill running for 10 weeks	Increased activity in deep vastus lateralis muscle	[371]
		Male, normotensive and hypertensive (11-12 weeks)	Liver, kidney, skeletal muscles, and heart	Treadmill running for 10 weeks	Reduced activity in all tissues in hypertensive and normotensive rats	[380]
	Mice	Males and females, aged 28, 52, and 78 weeks	Brain, heart, liver, and kidney	Long term moderate-intensity treadmill exercise	Increased activity in all issues at 52- but not 78-week-old mice	[23]
		Females, 3 months	Liver, heart, skeletal muscle, and salivary gland	Treadmill for a total of 8 weeks	Increased activity	[136]
	Pigs	Females	Aortic endothelial cells	Exercise training for 16–19 weeks	No change in protein level	[365]

GPX	Human	Untrained males = 9	Erythrocytes	High-intensity endurance training for 12 weeks	Increased activity after training	[354]
		Healthy young = 17	Blood	16 weeks of training then an acute bout of aerobic exercise for 30 min	Activity increased after regular training and transiently reduced following acute exercise	[355]
		Exercising and sedentary, young (21–38 years) and old (65–75 years) = 50	Erythrocyte	Regular exercise	Higher activity in the exercising elderly compared to the sedentary elderly	[381]
		Athletes = 18 and sedentary control = 6	Erythrocyte	Marathon or sprint training	Higher activity in sprint-trained athletes	[352]
		Patients with CHF = 14	Skeletal muscle	Moderate-intensity semirecumbent bicycle training for 12 weeks	Increased gene expression	[361]
	Rats	Males, young and aged (17 months)	Lung, heart, and liver	Regular swimming for 1 year	Activity increased in liver, lung, and heart of old rats relative to sedentary controls	[356]
		Aged	Brain liver, lung, muscle, and testes	Regular exercise	Increased activity in brain, liver, lung, and testes	[377]
		Male, young (8 months) and aged (22 months)	Brain	Swimming 30 min/day, 5 days/week for 12 weeks	Increased activity in hippocampus in young and aged	[378]
		Females, 12 months old	Hippocampus	Treadmill for a period of 15 weeks	Protein expression increased	[307]
		Females (24 months)	Skeletal muscles	Treadmill training (60 min, 5 days/week for 10 weeks)	Increased activity	[313]
		Male, young (8 weeks), adult (12 months), and old (24 months)	Skeletal muscles	Exercise training for 10 weeks	Increased activity in deep vastus lateralis muscle of young rats only	[311]
		Young (5 months) and aged (27.5 months)	Skeletal muscles	Treadmill training for 10 weeks	Increased activity in deep vastus lateralis muscle of old rats only	[384]
		Males, young (9 months) and aged (20 months)	liver	Regular exercise	Increased activity	[126]
		Males, obese Zucker	Liver	Treadmill running at 20 m/min for 1 h/day, 7 days/week for 8 weeks	mRNA and protein levels and activity increased	[372]
		Males, young	Liver, heart, and muscle	Swim training for 10 weeks	Increased activity in all tissues	[382]
		Females, 4 months	Ventricles	Endurance training for 10 weeks	No change in activity	[293]
		Males, adult	Heart	Treadmill training for 12 or 24 weeks	No change in activity	[292]
		Males, 16-17 weeks	Skeletal muscle and heart	Sprint training on a treadmill for 6 weeks	Increased activity in heart and some skeletal muscle fibres	[383]
		Females	Skeletal muscle	Treadmill running for 10 weeks	Increased activity in deep vastus lateralis muscle	[371]
		Male, normotensive and hypertensive (11-12 weeks)	Liver, kidney, skeletal muscles, and heart	Treadmill running for 10 weeks	Reduced activity in all tissues in hypertensive and normotensive rats	[380]
	Mice	Females, 3 months	Liver, kidney, and heart	Treadmill for a total of 8 weeks	Increased activity	[136]
		Males (6–8 weeks)	Ventricles	Swimming training for 14 weeks	No change in activity	[298]

GSR	Human	Healthy young = 17	Plasma	16 weeks of training then an acute bout of aerobic exercise for 30 min	Activity increased after regular training	[355]
	Mice	Males (6–8 weeks)	Ventricles	Swimming training for 14 weeks	No change in activity	[298]
	Rats	Males, adults	Heart	Treadmill training for 12 or 24 weeks	No change in activity	[292]
		Males, 16-17 weeks	Skeletal muscle and heart	Sprint training on a treadmill for 6 weeks	Increased activity in heart and some skeletal muscle fibres	[383]
		Males, young	Liver, heart, and muscle	Swim training for 10 weeks	Increased activity in all tissues	[382]
		Aged	Brain liver, lung, muscle, and testes	Regular exercise	Increased activity in testes	[377]
		Males, young (8 weeks), adult (12 months), and old (24 months)	Skeletal muscles	Exercise training for 10 weeks	Activity increased in deep vastus lateralis muscle of young rats and decreased in soleus muscle of adult rats only	[311]

GST	Mice	Females, 3 months	Liver and salivary gland	Treadmill for a total of 8 weeks	Increased activity	[136]

NAD(P)H oxidase	Human	Patients with symptomatic coronary artery disease = 45	Internal mammary artery	Aerobic training for 4 weeks	Reduced protein and gene expression and activity	[386]
		Men, 62 ± 3 years, physically active = 13 and sedentary = 26	Vascular endothelial cells from the brachial artery	Habitual aerobic exercise	Lower level of p47(phox) compared with sedentary men	[133]
	Rats	Males, young and myocardial infarcted	Aorta	Treadmill training 5 times per week, 60 min/day for 11 weeks	Reduced activity	[359]
		Male, adult (6 months) and aged (24 months)	Aorta	Swim training (60 min/day, 5 days/week for 10 weeks)	Decreased expression of gp91(phox)	[387]
	Pigs	Females	Aortic endothelial cells	Chronic exercise training for 16–19 weeks	Reduced protein expression of p67(phox)	[365]
	Mice	Young (6–8 months) and aged (29–32 months)	Aorta	Voluntary wheel running for 10–14 weeks	Reduced expression and activity	[360]
		Males, diabetic and young	Aorta	Treadmill exercise for 10 weeks	Decreased protein expression of gp91(phox)	[194]