Exercise-induced cardioprotection - biochemical, morphological and functional evidence in whole tissue and isolated mitochondria

International Journal of Cardiology

Volumn 117, Issue 1, 2007, Pages 16-30

  Ascensão, António ^a   Ferreira, Rita ^a   Magalhães, José ^a  

^a UNIVERSITY OF PORTO   (Portugal)

Author keywords

Antioxidants; Damage; Heart; Oxidative stress; Physical activity

Indexed keywords

ALPHA TOCOPHEROL; ANTIOXIDANT; CREATINE KINASE; DOXORUBICIN; ESTROGEN; FREE RADICAL; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 10; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 72; HEAT SHOCK PROTEIN 90; MANGANESE SUPEROXIDE DISMUTASE; TROPONIN I;

AGING; ANIMAL CELL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; BIOCHEMISTRY; BREATHING RATE; CALCIUM HOMEOSTASIS; CARDIOMYOPATHY; CARDIOTOXICITY; CORE TEMPERATURE; CROSS TOLERANCE; DIABETES MELLITUS; ENDURANCE; EXERCISE; GENE EXPRESSION; GUINEA PIG; HEART LEFT VENTRICLE PRESSURE; HEART MITOCHONDRION; HEART MUSCLE; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PROTECTION; HEART VENTRICLE; HEAT STRESS; HEMODYNAMICS; HEMOSTASIS; HYPOXIA; LIPID PEROXIDATION; MEMBRANE TRANSPORT; MITOCHONDRIAL RESPIRATION; MORPHOLOGY; MOUSE STRAIN; NONHUMAN; OVARIECTOMY; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT STRAIN; REVIEW; SARCOPLASMIC RETICULUM; SEX DIFFERENCE; STREPTOZOCIN DIABETES; TREADMILL;

ANIMALS; ANTIOXIDANTS; BIOLOGICAL MARKERS; EXERCISE; HEART; HEART DISEASES; HEART FUNCTION TESTS; HEAT-SHOCK PROTEINS; HUMANS; MYOCARDIUM; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHYSICAL ENDURANCE;

EID: 33947235594     PISSN: 01675273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijcard.2006.04.076     Document Type: Review

References (139)

1. Paffenbarger Jr. R.S., Hyde R.T., Wing A.L., and Hsieh C.C. Physical activity, all-cause mortality, and longevity of college alumni. N Engl J Med 10 (1986) 605-613
2. Paffenbarger Jr. R.S., Hyde R.T., Hsieh C.C., and Wing A.L. Physical activity, other life-style patterns, cardiovascular disease and longevity. Acta Med Scand Suppl (1986) 85-91
3. Penckofer S., Schwertz D., and Florczak K. Oxidative stress and cardiovascular disease in type 2 diabetes: the role of antioxidants and pro-oxidants. J Cardiovasc Nurs 2 (2002) 68-85
4. Thompson P.D., Buchner D., Pina I.L., et al. Exercise and physical activity in the prevention and treatment of atherosclerotic cardiovascular disease: a statement from the Council on Clinical Cardiology (Subcommittee on Exercise, Rehabilitation, and Prevention) and the Council on Nutrition, Physical Activity, and Metabolism (Subcommittee on Physical Activity). Circulation 24 (2003) 3109-3116
5. Pearson T.A., Blair S.N., Daniels S.R., et al. AHA guidelines for primary prevention of cardiovascular disease and stroke: 2002 update: consensus panel guide to comprehensive risk reduction for adult patients without coronary or other atherosclerotic vascular diseases. American Heart Association Science Advisory and Coordinating Committee. Circulation 3 (2002) 388-391
6. Ji L., and Leichtweis S. Exercise and oxidative stress: sources of free radicals and their impact on antioxidant systems. Age (1997) 91-106
7. Jenkins R.R. Free radical chemistry. Relationship to exercise. Sports Med 3 (1988) 156-170
8. Jackson M. Exercise and oxygen radical production by the muscle. In: Sen C.K., Packer L., Hanninen O., Sen C.K., Packer L., and Hanninens O. (Eds). Handbook of oxidants and antioxidants in exercise (2000), Elsevier B.V., Basel 57-68
9. Halliwell B., and Gutteridge J.M. Free radicals in biology and medicine (1999), Clarendon Press, Oxford
10. Phaneuf S., and Leeuwenburgh C. Apoptosis and exercise. Med Sci Sports Exerc 3 (2001) 393-396
11. Siu P.M., Bryner R.W., Martyn J.K., and Alway S.E. Apoptotic adaptations from exercise training in skeletal and cardiac muscles. FASEB J 10 (2004) 1150-1152
12. Lajoie C., Calderone A., and Beliveau L. Exercise training enhanced the expression of myocardial proteins related to cell protection in spontaneously hypertensive rats. Pflugers Arch 1 (2004) 26-32
13. Ji L.L. Exercise and oxidative stress: role of the cellular antioxidant systems. Exerc Sport Sci Rev (1995) 135-166
14. Ji L. Exercise-induced oxidative stress in the heart. In: Sen C.K., Packer L., Hanninen O., Sen C.K., Packer L., and Hanninens O. (Eds). Handbook of oxidants and antioxidants in exercise (2000), Elsevier B.V., Basel 689-712
15. Ji L.L. Antioxidants and oxidative stress in exercise. Proc Soc Exp Biol Med 3 (1999) 283-292
16. Atalay M., and Sen C.K. Physical exercise and antioxidant defenses in the heart. Ann N Y Acad Sci (1999) 169-177
17. Powers S.K., and Demirel H.A. Exercise, heat shock proteins, and myocardial protection from I-R injury. Med Sci Sports Exerc 3 (2001) 386-392
18. Powers S.K., Lennon S.L., Quindry J., and Mehta J.L. Exercise and cardioprotection. Curr Opin Cardiol 5 (2002) 495-502
19. Nemoto S., Takeda K., Yu Z.X., Ferrans V.J., and Finkel T. Role for mitochondrial oxidants as regulators of cellular metabolism. Mol Cell Biol 19 (2000) 7311-7318
20. Finkel T. Reactive oxygen species and signal transduction. IUBMB Life 1-2 (2001) 3-6
21. Hancock J.T., Desikan R., and Neill S.J. Role of reactive oxygen species in cell signalling pathways. Biochem Soc Trans Pt 2 (2001) 345-350
22. Cadenas E. Mitochondrial free radical production and cell signaling. Mol Aspects Med 1-2 (2004) 17-26
23. Dalton T.P., Shertzer H.G., and Puga A. Regulation of gene expression by reactive oxygen. Annu Rev Pharmacol Toxicol (1999) 67-101
24. Shern-Brewer R., Santanam N., Wetzstein C., et al. The paradoxical relationship of aerobic exercise and the oxidative theory of atherosclerosis. In: Sen C.K., Packer L., Hanninen O., Sen C.K., Packer L., and Hanninens O. (Eds). Handbook of oxidants and antioxidants in exercise (2000), Elsevier B.V., Basel 1053-1067
25. Venditti P., and Di Meo S. Antioxidants, tissue damage, and endurance in trained and untrained young male rats. Arch Biochem Biophys 1 (1996) 63-68
26. Somani S.M., Frank S., and Rybak L.P. Responses of antioxidant system to acute and trained exercise in rat heart subcellular fractions. Pharmacol Biochem Behav 4 (1995) 627-634
27. Lew H., and Quintanilha A. Effects of endurance training and exercise on tissue antioxidative capacity and acetaminophen detoxification. Eur J Drug Metab Pharmacokinet 1 (1991) 59-68
28. Ji L.L., Fu R.G., Mitchell E.W., Griffiths M., Waldrop T.G., and Swartz H.M. Cardiac hypertrophy alters myocardial response to ischaemia and reperfusion in vivo. Acta Physiol Scand 3 (1994) 279-290
29. Ramires P.R., and Ji L.L. Glutathione supplementation and training increases myocardial resistance to ischemia-reperfusion in vivo. Am J Physiol Heart Circ Physiol 2 (2001) H679-H688
30. Demirel H.A., Powers S.K., Caillaud C., et al. Exercise training reduces myocardial lipid peroxidation following short-term ischemia-reperfusion. Med Sci Sports Exerc 8 (1998) 1211-1216
31. Powers S.K., Demirel H.A., Vincent H.K., et al. Exercise training improves myocardial tolerance to in vivo ischemia-reperfusion in the rat. Am J Physiol 5 Pt 2 (1998) R1468-R1477
32. Ascensao A., Magalhaes J., Soares J., et al. Endurance training attenuates doxorubicin-induced cardiac oxidative damage in mice. Int J Cardiol 3 (2005) 451-460
33. Acensao A., Magallanes J., Soares J., et al. Endurance exercise training attenuates morphological signs of cardiac muscle damage induced by doxorubicin in mice. Basic Appl Myol 1 (2006) 27-35
34. Ascensao A., Magalhaes J., Soares J.M., et al. Moderate endurance training prevents doxorubicin-induced in vivo mitochondriopathy and reduces the development of cardiac apoptosis. Am J Physiol Heart Circ Physiol 2 (2005) H722-H731
35. Korte F.S., Mokelke E.A., Sturek M., and McDonald K.S. Exercise improves impaired ventricular function and alterations of cardiac myofibrillar proteins in diabetic dyslipidemic pigs. J Appl Physiol 2 (2005) 461-467
36. Ji L.L. Exercise, oxidative stress, and antioxidants. Am J Sports Med 6 (1996) S20-S24 [Suppl]
37. Bejma J., Ramires P., and Ji L.L. Free radical generation and oxidative stress with ageing and exercise: differential effects in the myocardium and liver. Acta Physiol Scand 4 (2000) 343-351
38. Ohkuwa T., Sato Y., and Naoi M. Glutathione status and reactive oxygen generation in tissues of young and old exercised rats. Acta Physiol Scand 3 (1997) 237-244
39. Khanna S., Atalay M., Laaksonen D.E., Gul M., Roy S., and Sen C.K. Alpha-lipoic acid supplementation: tissue glutathione homeostasis at rest and after exercise. J Appl Physiol 4 (1999) 1191-1196
40. Aydin C., Ince E., Koparan S., Cangul I.T., Naziroglu M., and Ak F. Protective effects of long term dietary restriction on swimming exercise-induced oxidative stress in the liver, heart and kidney of rat. Cell Biochem Funct (2005)
41. Venditti P., and Di Meo S. Effect of training on antioxidant capacity, tissue damage, and endurance of adult male rats. Int J Sports Med 7 (1997) 497-502
42. Venditti P., Piro M.C., Artiaco G., and Di Meo S. Effect of exercise on tissue anti-oxidant capacity and heart electrical properties in male and female rats. Eur J Appl Physiol Occup Physiol 4 (1996) 322-329
43. Powers S., and Sen C.K. Physiological antioxidants and exercise training. In: Sen C.K., Packer L., Hanninen O., Sen C.K., Packer L., and Hanninens O. (Eds). Handbook of oxidants and antioxidants in exercise (2000), Elsevier B.V., Basel 221-242
44. Powers S.K., Ji L.L., and Leeuwenburgh C. Exercise training-induced alterations in skeletal muscle antioxidant capacity: a brief review. Med Sci Sports Exerc 7 (1999) 987-997
45. Ji L.L., and Leeuwenburgh C. Glutathione and exercise. In: Somani S., and Somanis S. (Eds). Pharmacology in exercise and sports (1996), CRC Press, Boca Raton (FL) 97-123
46. Liu J., Yeo H.C., Overvik-Douki E., et al. Chronically and acutely exercised rats: biomarkers of oxidative stress and endogenous antioxidants. J Appl Physiol 1 (2000) 21-28
47. Demirel H.A., Powers S.K., Zergeroglu M.A., et al. Short-term exercise improves myocardial tolerance to in vivo ischemia-reperfusion in the rat. J Appl Physiol 5 (2001) 2205-2212
48. Leeuwenburgh C., Leichtweis S., Hollander J., Fiebig R., Gore M., and Ji L.L. Effect of acute exercise on glutathione deficient heart. Mol Cell Biochem 1 (1996) 17-24
49. Atalay M., Marnila P., Lilius E.M., Hanninen O., and Sen C.K. Glutathione-dependent modulation of exhausting exercise-induced changes in neutrophil function of rats. Eur J Appl Physiol Occup Physiol 4 (1996) 342-347
50. Sen C.K., Atalay M., and Hanninen O. Exercise-induced oxidative stress: glutathione supplementation and deficiency. J Appl Physiol 5 (1994) 2177-2187
51. Benderitter M., Hadj-Saad F., Lhuissier M., Maupoil V., Guilland J.C., and Rochette L. Effects of exhaustive exercise and vitamin B6 deficiency on free radical oxidative process in male trained rats. Free Radic Biol Med 4 (1996) 541-549
52. Locke M., Tanguay R.M., Klabunde R.E., and Ianuzzo C.D. Enhanced postischemic myocardial recovery following exercise induction of HSP 72. Am J Physiol 1 Pt 2 (1995) H320-H325
53. Starnes J.W., Taylor R.P., and Park Y. Exercise improves postischemic function in aging hearts. Am J Physiol Heart Circ Physiol 1 (2003) H347-H351
54. Kim J.D., Yu B.P., McCarter R.J., Lee S.Y., and Herlihy J.T. Exercise and diet modulate cardiac lipid peroxidation and antioxidant defenses. Free Radic Biol Med 1 (1996) 83-88
55. Suzuki K., Sawa Y., Ichikawa H., Kaneda Y., and Matsuda H. Myocardial protection with endogenous overexpression of manganese superoxide dismutase. Ann Thorac Surg 4 (1999) 1266-1271
56. 2 toxicity. Am J Physiol 1 Pt 2 (1999) H167-H175
57. Leichtweis S., and Ji L.L. Glutathione deficiency intensifies ischaemia-reperfusion induced cardiac dysfunction and oxidative stress. Acta Physiol Scand 1 (2001) 1-10
58. Vaziri N.D., Wang X.Q., Oveisi F., and Rad B. Induction of oxidative stress by glutathione depletion causes severe hypertension in normal rats. Hypertension 1 (2000) 142-146
59. Atalay M., Seene T., Hanninen O., and Sen C.K. Skeletal muscle and heart antioxidant defences in response to sprint training. Acta Physiol Scand 2 (1996) 129-134
60. Hong H., and Johnson P. Antioxidant enzyme activities and lipid peroxidation levels in exercised and hypertensive rat tissues. Int J Biochem Cell Biol 9 (1995) 923-931
61. Powers S.K., Criswell D., Lawler J., et al. Rigorous exercise training increases superoxide dismutase activity in ventricular myocardium. Am J Physiol 6 Pt 2 (1993) H2094-H2098
62. Leeuwenburgh C., Hollander J., Leichtweis S., Griffiths M., Gore M., and Ji L.L. Adaptations of glutathione antioxidant system to endurance training are tissue and muscle fiber specific. Am J Physiol 1 Pt 2 (1997) R363-R369
63. Hamilton K.L., Staib J.L., Phillips T., Hess A., Lennon S.L., and Powers S.K. Exercise, antioxidants, and HSP72: protection against myocardial ischemia/reperfusion. Free Radic Biol Med 7 (2003) 800-809
64. Lennon S.L., Quindry J., Hamilton K.L., et al. Loss of exercise-induced cardioprotection after cessation of exercise. J Appl Physiol 4 (2004) 1299-1305
65. Kanter M.M., Hamlin R.L., Unverferth D.V., Davis H.W., and Merola A.J. Effect of exercise training on antioxidant enzymes and cardiotoxicity of doxorubicin. J Appl Physiol 4 (1985) 1298-1303
66. Chicco A.J., Schneider C.M., and Hayward R. Voluntary exercise protects against acute doxorubicin cardiotoxicity in the isolated perfused rat heart. Am J Physiol Regul Integr Comp Physiol 2 (2005) R31-R424
67. Atalay M., Oksala N.K., Laaksonen D.E., et al. Exercise training modulates heat shock protein response in diabetic rats. J Appl Physiol 2 (2004) 605-611
68. Bupha-Intr T., and Wattanapermpool J. Cardioprotective effects of exercise training on myofilament calcium activation in ovariectomized rats. J Appl Physiol 5 (2004) 1755-1760
69. Paulson D.J., Kopp S.J., Peace D.G., and Tow J.P. Myocardial adaptation to endurance exercise training in diabetic rats. Am J Physiol 6 Pt 2 (1987) R1073-R1081
70. Chicco A.J., Hydock D.S., Schneider C.M., and Hayward R. Low-intensity exercise training during doxorubicin treatment protects against cardiotoxicity. J Appl Physiol 2 (2006) 519-527
71. Selman C., McLaren J.S., Collins A.R., Duthie G.G., and Speakman J.R. Antioxidant enzyme activities, lipid peroxidation, and DNA oxidative damage: the effects of short-term voluntary wheel running. Arch Biochem Biophys 2 (2002) 255-261
72. Bronikowski A.M., Carter P.A., Morgan T.J., et al. Lifelong voluntary exercise in the mouse prevents age-related alterations in gene expression in the heart. Physiol Genomics 2 (2003) 129-138
73. Navarro A., Gomez C., Lopez-Cepero J.M., and Boveris A. Beneficial effects of moderate exercise on mice aging: survival, behavior, oxidative stress, and mitochondrial electron transfer. Am J Physiol Regul Integr Comp Physiol 3 (2004) R505-R511
74. Quindry J., French J., Hamilton K., Lee Y., Mehta J.L., and Powers S. Exercise training provides cardioprotection against ischemia-reperfusion induced apoptosis in young and old animals. Exp Gerontol 5 (2005) 416-425
75. Lennon S.L., Quindry J.C., French J.P., Kim S., Mehta J.L., and Powers S.K. Exercise and myocardial tolerance to ischaemia-reperfusion. Acta Physiol Scand 2 (2004) 161-169
76. Ascensao A., Magalhaes J., Soares J.M., et al. Endurance training limits the functional alterations of heart rat mitochondria submitted to in vitro anoxia-reoxygenation. Int J Cardiol 2 (2006) 169-178
77. Taylor R.P., Ciccolo J.T., and Starnes J.W. Effect of exercise training on the ability of the rat heart to tolerate hydrogen peroxide. Cardiovasc Res 3 (2003) 575-581
78. Mogk A., Mayer M.P., and Deuerling E. Mechanisms of protein folding: molecular chaperones and their application in biotechnology. Chembiochem 9 (2002) 807-814
79. Paroo Z., Meredith M.J., Locke M., Haist J.V., Karmazyn M., and Noble E.G. Redox signaling of cardiac HSF1 DNA binding. Am J Physiol Cell Physiol 2 (2002) C404-C411
80. Locke M., Noble E.G., Tanguay R.M., Feild M.R., Ianuzzo S.E., and Ianuzzo C.D. Activation of heat-shock transcription factor in rat heart after heat shock and exercise. Am J Physiol 6 Pt 1 (1995) C1387-C1394
81. Ho J., and Westwood J. Transcriptional regulation of the mammalian heat shock genes. In: Locke M., Noble E., Locke M., and Nobles E. (Eds). Exercise and stress response - the role of stress proteins (2002), CRC Press, Boca Raton (FL) 13-41
82. Chi N.C., and Karliner J.S. Molecular determinants of responses to myocardial ischemia/reperfusion injury: focus on hypoxia-inducible and heat shock factors. Cardiovasc Res 3 (2004) 437-447
83. Melling C.W., Thorp D.B., and Noble E.G. Regulation of myocardial heat shock protein 70 gene expression following exercise. J Mol Cell Cardiol 4 (2004) 847-855
84. Latchman D.S. Heat shock proteins and cardiac protection. Cardiovasc Res 4 (2001) 637-646
85. Snoeckx L.H., Cornelussen R.N., Van Nieuwenhoven F.A., Reneman R.S., and Van Der Vusse G.J. Heat shock proteins and cardiovascular pathophysiology. Physiol Rev 4 (2001) 1461-1497
86. Sammut I.A., and Harrison J.C. Cardiac mitochondrial complex activity is enhanced by heat shock proteins. Clin Exp Pharmacol Physiol 1-2 (2003) 110-115
87. Papp E., Nardai G., Soti C., and Csermely P. Molecular chaperones, stress proteins and redox homeostasis. Biofactors 1-4 (2003) 249-257
88. Benjamin I.J., and McMillan D.R. Stress (heat shock) proteins: molecular chaperones in cardiovascular biology and disease. Circ Res 2 (1998) 117-132
89. Hamilton K.L., Powers S.K., Sugiura T., et al. Short-term exercise training can improve myocardial tolerance to I/R without elevation in heat shock proteins. Am J Physiol Heart Circ Physiol 3 (2001) H1346-H1352
90. Taylor R.P., Harris M.B., and Starnes J.W. Acute exercise can improve cardioprotection without increasing heat shock protein content. Am J Physiol 3 Pt 2 (1999) H1098-H1102
91. Harris M.B., and Starnes J.W. Effects of body temperature during exercise training on myocardial adaptations. Am J Physiol Heart Circ Physiol 5 (2001) H2271-H2280
92. Kim K.B., Kim M.H., and Lee D.J. The effect of exercise in cool, control and hot environments on cardioprotective HSP70 induction. J Physiol Anthropol Appl Human Sci 6 (2004) 225-230
93. Paroo Z., Tiidus P.M., and Noble E.G. Estrogen attenuates HSP 72 expression in acutely exercised male rodents. Eur J Appl Physiol Occup Physiol 3 (1999) 180-184
94. Paroo Z., Haist J.V., Karmazyn M., and Noble E.G. Exercise improves postischemic cardiac function in males but not females: consequences of a novel sex-specific heat shock protein 70 response. Circ Res 8 (2002) 911-917
95. Xi L. Exercise does not protect the female heart: an unconvincing conclusion?. Circ Res 3 (2002) e2
96. Benjamin I.J., and Christians E. Exercise, estrogen, and ischemic cardioprotection by heat shock protein 70. Circ Res 8 (2002) 833-835
97. Knowlton A.A., and Sun L. Heat-shock factor-1, steroid hormones, and regulation of heat-shock protein expression in the heart. Am J Physiol Heart Circ Physiol 1 (2001) H455-H464
98. Noble E.G., Moraska A., Mazzeo R.S., et al. Differential expression of stress proteins in rat myocardium after free wheel or treadmill run training. J Appl Physiol 5 (1999) 1696-1701
99. Noble E. Heat shock proteins and their induction with exercise. In: Locke M., Noble E., Locke M., and Nobles E. (Eds). Exercise and stress response. The role of stress proteins (2002), CRC Press, Boca Raton 43-78
100. Suzuki K., Murtuza B., Sammut I.A., et al. Heat shock protein 72 enhances manganese superoxide dismutase activity during myocardial ischemia-reperfusion injury, associated with mitochondrial protection and apoptosis reduction. Circulation 12 Suppl. 1 (2002) I270-I276
101. Jayakumar J., Suzuki K., Sammut I.A., et al. Heat shock protein 70 gene transfection protects mitochondrial and ventricular function against ischemia-reperfusion injury. Circulation 12 Suppl. 1 (2001) I303-I307
102. Sen C.K., and Goldfarb A. Antioxidants and physical exercise. In: Sen C.K., Packer L., Hanninen O., Sen C.K., Packer L., and Hanninens O. (Eds). Handbook of oxidants and antioxidants in exercise (2000), Elsevier B.V., Basel 297-320
103. Brookes P.S., Yoon Y., Robotham J.L., Anders M.W., and Sheu S.S. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 4 (2004) C817-C833
104. Brookes P.S. Mitochondrial H(+) leak and ROS generation: an odd couple. Free Radic Biol Med 1 (2005) 12-23
105. Skulachev V.P. Mitochondrial physiology and pathology; concepts of programmed death of organelles, cells and organisms. Mol Aspects Med 3 (1999) 139-184
106. Brown G.C., and Borutaite V. Nitric oxide inhibition of mitochondrial respiration and its role in cell death. Free Radic Biol Med 11 (2002) 1440-1450
107. Vercesi A.E., Kowaltowski A.J., Grijalba M.T., Meinicke A.R., and Castilho R.F. The role of reactive oxygen species in mitochondrial permeability transition. Biosci Rep 1 (1997) 43-52
108. Ji L.L., and Mitchell E.W. Effects of Adriamycin on heart mitochondrial function in rested and exercised rats. Biochem Pharmacol 5 (1994) 877-885
109. Taylor P.B., Lamb D.R., and Budd G.C. Structure and function of cardiac mitochondria in exhausted guinea pigs. Eur J Appl Physiol Occup Physiol 2 (1976) 111-118
110. Leichtweis S.B., Leeuwenburgh C., Parmelee D.J., Fiebig R., and Ji L.L. Rigorous swim training impairs mitochondrial function in post-ischaemic rat heart. Acta Physiol Scand 2 (1997) 139-148
111. Tiidus P.M., and Houston M.E. Vitamin E status and response to exercise training. Sports Med 1 (1995) 12-23
112. Asha Devi S., Prathima S., and Subramanyam M.V. Dietary vitamin E and physical exercise: II. Antioxidant status and lipofuscin-like substances in aging rat heart. Exp Gerontol 3 (2003) 291-297
113. Perez A.C., Cabral de Oliveira A.C., Estevez E., Molina A.J., Prieto J.G., and Alvarez A.I. Mitochondrial, sarcoplasmic membrane integrity and protein degradation in heart and skeletal muscle in exercised rats. Comp Biochem Physiol C Toxicol Pharmacol 2 (2003) 199-206
114. Jin H., Yang R., Li W., et al. Effects of exercise training on cardiac function, gene expression, and apoptosis in rats. Am J Physiol Heart Circ Physiol 6 (2000) H2994-H3002
115. Zhou S., Starkov A., Froberg M.K., Leino R.L., and Wallace K.B. Cumulative and irreversible cardiac mitochondrial dysfunction induced by doxorubicin. Cancer Res 2 (2001) 771-777
116. Oliveira P.J., Bjork J.A., Santos M.S., et al. Carvedilol-mediated antioxidant protection against doxorubicin-induced cardiac mitochondrial toxicity. Toxicol Appl Pharmacol 2 (2004) 159-168
117. Santos D.L., Moreno A.J., Leino R.L., Froberg M.K., and Wallace K.B. Carvedilol protects against doxorubicin-induced mitochondrial cardiomyopathy. Toxicol Appl Pharmacol 3 (2002) 218-227
118. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem J (1999) 233-249
119. Skulachev V.P. Membrane-linked systems preventing superoxide formation. Biosci Rep 3 (1997) 347-366
120. Kowaltowski A.J., Castilho R.F., and Vercesi A.E. Mitochondrial permeability transition and oxidative stress. FEBS Lett 1-2 (2001) 12-15
121. Judge S., Jang Y.M., Smith A., et al. Exercise by lifelong voluntary wheel running reduces subsarcolemmal and interfibrillar mitochondrial hydrogen peroxide production in the heart. Am J Physiol Regul Integr Comp Physiol 6 (2006) R1564-R1572
122. Mokhtar N., Lavoie J.P., Rousseau-Migneron S., and Nadeau A. Physical training reverses defect in mitochondrial energy production in heart of chronically diabetic rats. Diabetes 5 (1993) 682-687
123. Wallace K.B. Doxorubicin-induced cardiac mitochondrionopathy. Pharmacol Toxicol 3 (2003) 105-115
124. Searls Y.M., Smirnova I.V., Fegley B.R., and Stehno-Bittel L. Exercise attenuates diabetes-induced ultrastructural changes in rat cardiac tissue. Med Sci Sports Exerc 11 (2004) 1863-1870
125. Wallace K.B., Hausner E., Herman E., et al. Serum troponins as biomarkers of drug-induced cardiac toxicity. Toxicol Pathol 1 (2004) 106-121
126. Bertinchant J.P., Robert E., Polge A., et al. Comparison of the diagnostic value of cardiac troponin I and T determinations for detecting early myocardial damage and the relationship with histological findings after isoprenaline-induced cardiac injury in rats. Clin Chim Acta 1-2 (2000) 13-28
127. Shave R., Dawson E., Whyte G., et al. The cardiospecificity of the third-generation cTnT assay after exercise-induced muscle damage. Med Sci Sports Exerc 4 (2002) 651-654
128. Fredericks S., Merton G.K., Lerena M.J., Heining P., Carter N.D., and Holt D.W. Cardiac troponins and creatine kinase content of striated muscle in common laboratory animals. Clin Chim Acta 1-2 (2001) 65-74
129. Bertinchant J.P., Polge A., Juan J.M., et al. Evaluation of cardiac troponin I and T levels as markers of myocardial damage in doxorubicin-induced cardiomyopathy rats, and their relationship with echocardiographic and histological findings. Clin Chim Acta 1-2 (2003) 39-51
130. Kihlstrom M. Protection effect of endurance training against reoxygenation-induced injuries in rat heart. J Appl Physiol 4 (1990) 1672-1678
131. Husain K. Interaction of physical training and chronic nitroglycerin treatment on blood pressure, nitric oxide, and oxidants/antioxidants in the rat heart. Pharmacol Res 3 (2003) 253-261
132. Husain K., and Hazelrigg S.R. Oxidative injury due to chronic nitric oxide synthase inhibition in rat: effect of regular exercise on the heart. Biochim Biophys Acta 1 (2002) 75-82
133. Moran M., Blazquez I., Saborido A., and Megias A. Antioxidants and ecto-5′-nucleotidase are not involved in the training-induced cardioprotection against ischaemia-reperfusion injury. Exp Physiol 4 (2005) 507-517
134. Moran M., Delgado J., Gonzalez B., Manso R., and Megias A. Responses of rat myocardial antioxidant defences and heat shock protein HSP72 induced by 12 and 24-week treadmill training. Acta Physiol Scand 2 (2004) 157-166
135. Kihlstrom M.T. Lipid peroxidation capacities in the myocardium of endurance-trained rats and mice in vitro. Acta Physiol Scand 2 (1992) 177-183
136. Husain K., and Somani S.M. Response of cardiac antioxidant system to alcohol and exercise training in the rat. Alcohol 3 (1997) 301-307
137. Gunduz F., Senturk U.K., Kuru O., Aktekin B., and Aktekin M.R. The effect of one year's swimming exercise on oxidant stress and antioxidant capacity in aged rats. Physiol Res 2 (2004) 171-176
138. Gore M., Fiebig R., Hollander J., Leeuwenburgh C., Ohno H., and Ji L.L. Endurance training alters antioxidant enzyme gene expression in rat skeletal muscle. Can J Physiol Pharmacol 12 (1998) 1139-1145
139. Tiidus P.M., and Houston M.E. Antioxidant and oxidative enzyme adaptations to vitamin E deprivation and training. Med Sci Sports Exerc 3 (1994) 354-359