Impaired oxidative phosphorylation in overtrained rat myocardium

Experimental and Clinical Cardiology

Volumn 15, Issue 4, 2010, Pages

  Kadaja, Lumme ^a   Eimre, Margus ^a   Paju, Kalju ^a   Roosimaa, Mart ^a   Põdramägi, Taavi ^a   Kaasik, Priit ^a   Pehme, Ando ^a   Orlova, Ehte ^a   Mudist, Margareeta ^a   Peet, Nadezhda ^a   Piirsoo, Andres ^a   Seene, Teet ^a   Gellerich, Frank N ^b   Seppet, Enn K ^a  

^a UNIVERSITY OF TARTU   (Estonia)

^b LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

Author keywords

Mitochondria; Overtraining; Oxidative phosphorylation; Rat myocardium

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENYLATE KINASE; CYTOCHROME C; SAPONIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CATABOLISM; CELL SWELLING; ELECTRON MICROSCOPY; ENERGY METABOLISM; HEART MUSCLE; HEART MUSCLE CELL; MALE; MITOCHONDRION; NONHUMAN; OVEREXERTION; OXIDATIVE PHOSPHORYLATION; PEROXISOME; RAT; RESPIROMETRY; SKELETAL MUSCLE; TREADMILL EXERCISE;

EID: 79952539543     PISSN: 12056626     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (95)

1. Holloszy JO. Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J Biol Chem 1967;242:2278-82.
2. Holloszy JO. Regulation by exercise of skeletal muscle content of mitochondria and GLU4. J Physiol Pharmacol 2008;59:5-18.
3. Pereira B, Costa Rosa LFB, Safi DA, Medeiros MHG, Curi R, Bechara EJH. Superoxide dismutase, catalase, and glutathione peroxidase activities in muscle and lymphoid organs of sedentary and exercise-trained rats. Physiol Behav 1994;56:1095-9.
4. Oh-ishi S, Kizaki T, Ookawara T, et al. Endurance training improves the resistance of rat diaphragm to exercise-induced oxidative stress. Am J Respir Crit Care Med 1997;156:1579-85.
5. Radák Z, Kaneko T, Tahara S, et al. The effect of exercise training on oxidative damage of lipids, proteins, and DNA in rat skeletal muscle: evidence for beneficial outcomes. Free Radic Biol Med 1999;27:69-74.
6. Pinho RA, Andrades ME, Oliveira MR, et al. Imbalance in SOD/CAT activities in rat skeletal muscles submitted to treadmill training exercise. Cell Biol Int 2006;30:848-53.
7. Navarro A, Gomez C, López-Cepero JM, 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 2004;286:R505-11.
8. Ventura-Clapier R. Exercise training, energy metabolism, and heart failure. Appl Physiol Nutr Metab 2009;34:336-9.
9. Ascensão A, Magalhães JF, Soares JM, et al. Cardiac mitochondrial respiratory function and oxidative stress: The role of exercise. Int J Sports Med 2005;26:258-67.
10. Tonkonogi M, Walsh B, Svensson M, Sahlin K. Mitochondrial function and antioxidative defence in human muscle: Effects of endurance training and oxidative stress. J Physiol 2000;528:379-88.
11. Ljubicic V, Joseph A-M, Saleem A, et al. Transcriptional and post-transcriptional regulation of mitochondrial biogenesis in skeletal muscle: Effect of exercise and aging. Biochim Biophys Acta 2010;1800:223-34.
12. 2+- induced dysfunction. J Appl Physiol 2007;102:1793-8.
13. Seene T, Kaasik P, Alev K, Pehme A, Riso EM. Composition and turnover of contractile proteins in volume-overtrained skeletal muscle. Int J Sports Med 2004;25:438-45.
14. Seene T, Umnova M, Kaasik P. The exercise myopathy. In: Lehman M, et al, eds. Overload, Perfomance Incompetence, and Regeneration in Sport. New York: Kluwer Academic Plenum, 1999:119-30.
15. Hooper S, Mackinnon L, Howard A, et al. Markers for monitoring overtraining and recovery. Med Sci Sports Exerc 1995;27:106-12.
16. Di Meo S, Venditti P. Mitochondria in exercise-induced oxidative stress. Biol Signals Recept 2001;10:125-40.
17. Bejma J, Ji LL. Aging and acute exercise enhance free radical generation in rat skeletal muscle. J Appl Physiol 1999;87:465-70.
18. Ashton T, Rowlands CC, Jones E, et al. Electron spin resonance spectroscopic detection of oxygen-centred radicals in human serum following exhaustive exercise. Eur J Appl Physiol Occup Physiol 1998;77:498-502.
19. Powers SK, Jackson MJ. Exercise-induced oxidative stress: Cellular mechanisms and impact on muscle force production. Physiol Rev 2008;88:1243-76.
20. Herrero A, Barja G. Localization of the site of oxygen radical generation inside the complex I of heart and nonsynaptic brain mammalian mitochondria. J Bioenerg Biomembr 2000;32:609-15.
21. Muller FL, Liu Y, Van Remmen H. Complex III releases superoxide to both sides of the inner mitochondrial membrane. J Biol Chem 2004;279:49064-73.
22. Molnar AM, Alves AA, Pereira-da-Silva L, Macedo DV, Dabbeni-Sala F. Evaluation by blue native polyacrylamide electrophoresis colorimetric staining of the effects of physical exercise on the activities of mitochondrial complexes in rat muscle. Braz J Med Biol Res 2004;37:939-47.
23. Arslan S, Erdem S, Kilinç K, Sivri A, Tan E, Hasçelik HZ. Free radical changes in rat muscle tissue after exercise. Rheumatol Int 2001;3:109-12.
24. Armstrong RB, Warren GL, Warren JA. Mechanisms of exercise-induced muscle fibre injury. Sports Med 1991;12:184-207.
25. Tate CA, Bonner HW, Leslie SW. Calcium uptake in skeletal muscle mitochondria. II. The effects of long-term chronic and acute exercise. Eur J Appl Physiol Occup Physiol 1978;39:117-22.
26. King DW, Gollnick PD. Ultrastructure of rat heart and liver after exhaustive exercise. Am J Physiol 1970;218:1150-5.
27. Ji LL, Mitchell EW. Effects of adriamycin on heart mitochondrial function in rested and exercised rats. Biochem Pharmacol 1994;47:877-85.
28. Leichtweiss SB, Leeuwenburgh C, Parmelee DJ, Fiebig R, Ji LL. Rigorous swim training impairs mitochondrial function in post-ischemic rat heart. Acta Physiol Scand 1997;160:139-48.
29. Terblanche SE, Gohil K, Packer L, Henderson S, Brooks GA. The effects of endurance training and exhaustive exercise on mitochondrial enzymes in tissues of the rat (Rattus norvegicus). Comp Biochem Physiol A Mol Integr Physiol 2001;128:889-96.
30. Kemi OJ, Høydal MA, Haram PM, et al. Exercise training restores aerobic capacity and enenrgy transfer systems in heart failure treated with losartan. Cardiovasc Res 2007;76:91-9.
31. Sun B, Wang JH, Lv YY, Zhu SS, Yang J, Ma JZ. Proteomic adaptation to chronic high intensity swimming training in the rat heart. Comp Biochem Physiol 2008;3:108-17.
32. Bo H, Jiang N, Ma G, et al. Regulation of mitochondrial uncoupling respiration during exercise in rat heart: Role of reactive oxygen species (ROS) and uncoupling protein 2. Free Rad Biol Med 2008;44:1373-81.
33. Ascensão A, Magalhães J, Soares JMC, et al. Endurance training limits the functional alterations of heart rat mitochondria submitted to in vitro anoxia-reoxygenation. Int J Cardiol 2006;109:169-78.
34. Kavazis AN, McClung JM, Hood DA, Powers SK. Exercise induces a cardiac mitochondrial phenotype that resists apoptotic stimuli. Am J Physiol 2008;294:H928-35.
35. Kavazis AN, Alvarez S, Talbert E, Lee Y, Powers SK. Exercise training induces a cardioprotective phenotype and alterations in cardiac subsarcolemmal and intermyofibrillar mitochondrial proteins. Am J Physiol 2009;297:H144-52.
36. Pierce GN, Kutryk MJ, Dhalla KS, Beamish RE, Dhalla NS. Biochemical alterations in heart after exhaustive swimming in rats. J Appl Physiol 1984;57:326-31.
37. Huang C-C, Lin T-J, Chen C-C, Lin W-T. Endurance training accelerates exhaustive exercise-induced mitochondrial DNA deletion and apoptosis of left ventricle myocardium in rats. Eur J Appl Physiol 2009;107:697-706.
38. Seppet EK, Kaambre T, Sikk P, et al. Functional complexes of mitochondria with Ca,MgATPases of myofibrils and sarcoplasmic reticulum in muscle cells. Biochim Biophys Acta 2001;504:379-95.
39. Saks VA, Kaambre T, Sikk P, et al. Intracellular energetic units in red muscle cells. Biochem J 2001;356:643-57.
40. Anmann T, Eimre M, Kuznetsov AV, et al. Structure-function relationships in the regulation of energy transfer between mitochondria and ATPases in cardiac cells. Exp Clin Cardiol 2006;1:189-94.
41. Braun U, Paju K, Eimre M, et al. Lack of dystrophin is associated with altered integration of the mitochondria and ATPases in slow-twitch muscle cells of MDX mice. Biochim Biophys Acta 2001;1505:258-70.
42. Kadaja L, Kisand KE, Peet N, et al. IgG from patients with liver diseases inhibit mitochondrial respiration in permeabilized oxidative muscle cells: impaired function of intracellular energetic units? Mol Cell Biochem 2004;256-257:291-303.
43. Seppet E, Eimre M, Peet N, et al. Compartmentation of energy metabolism in atrial myocardium of patients undergoing cardiac surgery. Mol Cell Biochem 2005;270:49-61.
44. Schlattner U, Tokarska-Schlattner M, Wallimann T. Mitochondrial creatine kinase in human health and disease. Biochim Biophys Acta 2006;1762:164-80.
45. Eimre M, Puhke R, Alev K, et al. Altered mitochondrial apparent affinity for ADP and impaired function of mitochondrial creatine kinase in gluteus medius of patients with hip osteoarthritis. Am J Physiol Regul Integr Comp Physiol 2006;290:R1271-75.
46. Kaasik P, Alev K, Seene T. The effect of activity on the rat skeletal muscle contractile apparatus. Scand J Lab Anim Sci 1996;23:35-9.
47. Seene T, Alev K. Effect of glucocorticoids on the turnover rate of actin and myosin heavy and light chains on different types of skeletal muscle fibres. J Steroid Biochem 1985;22:767-71.
48. Saks VA, Veksler VI, Kuznetsov AV, et al. Permeabilized cell and skinned fiber techniques in studies of mitochondrial function in vivo. Mol Cell Biochem 1998;184:81-100.
49. Eimre M, Paju K, Pelloux S, et al. Distinct organization of energy metabolism in HL-1 cardiac cell line and cardiomyocytes. Biochim Biophys Acta 2008;1777:514-24.
50. Fuller EO, Goldberg DI, Starnes JW, Sacks LM, Delivoria-Papadopoulos M. Mitochondrial respiration following acute hypoxia in the perfused rat heart. J Mol Cell Cardiol 1985;17:71-81.
51. Maguire JJ, Davies KJA, Dallman, PR, Packer L. Effects of dietary iron efficiency on iron-sulfur proteins and bioenergetic function on skeletal muscle mitochondria. Biochim Biophys Acta 1982;679:210-20.
52. Bradford M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-54.
53. Ostadal B, Schiebler TH. The development of capillaries in the rat heart: An electron microscopic study. Z Anat Entwicklungsgesh 1971;133:288-304.
54. Laguens RP, Gómez-Dumm CLA. Fine-structure of myocardial mitochondria in rats after exercise for one-half to two hours. Circ Res 1967;21:271-9.
55. Nozaki T, Kagaya Y, Ishide N, et al. Interaction between sarcomere and mitochondrial length in normoxic and hypoxic rat ventricular papillary muscles. Cardiovasc Pathol 2001;10:125-32.
56. Vendelin M, Béraud N, Guerrero K, et al. Mitochondrial regular arrangement in muscle cells: A "crystal-like" pattern. Am J Physiol 2005;288:757-67.
57. Capetanaki Y. Desmin cytoskeleton: A potential regulator of muscle mitochondrial behaviour and function. Trends Cardiovasc Med 2002;12:339-48.
58. Herzog V, Fahimi HD. Identification of peroxisomes (microbodies) in mouse myocardium. J Mol Cell Cardiol 1976;8:271-2.
59. Fahimi HD, Kino M, Hicks L, Thorp KA, Abelman WH. Increased myocardial catalase in rats fed ethanol. Am J Pathol 1979;96:373-90.
60. Goldfischer S. Peroxisomes in disease. J Histochem Cytochem 1979;27:1371-3.
61. Zipper J. Proliferation of myocardial peroxisomes caused by several agents and conditions. J Mol Cell Cardiol 1997;29:149-61.
62. De Craemer D, Vamecq J, Roels F, et al. Peroxisomes in liver, heart, and kidney of mice fed a commercial fish oil preparation: Original data and review on peroxisomal changes induced by high-fat diets. J Lipid Res 1994;35:1241-50.
63. Zhou Z, Kang YJ. Cellular and subcellular localization of catalase in the heart of transgenic mice. J Histochem Cytochem 2000;48:585-94.
64. McKenna O, Arnold G, Holtzman E. Microperoxisome distribution in the central nervous system of the rat. Brain Res 1976;117:181-94.
65. Hicks L, Fahimi HD. Peroxisomes (microbodies) in the myocardium of rodents and primates. A comparative ultrastructural cytochemical study. Cell Tissue Res 1977;175:467-81.
66. Kainulainen H, Ahomäki E, Vihko V. Selected enzyme activities in mouse cardiac muscle during training and terminated training. Basic Res Cardiol 1984;79:110-23.
67. Mohr M, Krustrup P, Nielsen JJ, et al. Effect of two different intense training regimes on skeletal muscle ion transport proteins and fatigue development. Am J Physiol 2007;292:R1594-602.
68. Brancaccio P, Maffulli N, Limongelli FM. Creatine kinase monitoring in sport medicine. Br Med Bull 2007;81-82:209-30.
69. Bronheimer JF, Lau F. Effects of treadmill exercise on total and myocardial creatine phosphokinase. Chest 1981;80:146-8
70. Jaffe AS, Garfinkel BT, Ritter CS, Sobel BE. Plasma MB creatine kinase after vigorous exercise in professional athletes. Am J Cardiol 1984;53:856-8.
71. Young A. Plasma creatine kinase after the marathon - a diagnostic dilemma. Brit J Sports Med 1984;18:269-72.
72. Apple FS, Billadello JJ. Expression of creatine kinase M and B mRNAs in treadmill trained rat skeletal muscle. Life Sci 1994;55:585-92.
73. Cummins P, Young A, Auckland ML, Michie CA, Stone PC, Shepstone BJ. Comparison of serum cardiac specific troponin-I with creatine kinase, creatine kinase-MB isoenzyme, tropomyosin, myoglobin and C-reactive protein release in marathon runners: Cardiac or skeletal muscle trauma? Eur J Clin Invest 1987;17:317-24.
74. Siegel AJ, Sholar M, Yang J, Dhanak E, Lewandrowsky KB. Elevated serum cardiac markers in asymptomatic marathon runners after competition: Is the myocardium stunned? Cardiology 1997;88:487-91.
75. Nie J, Tong TK, George K, Fu FH, Lin H, Shi Q. Resting and post-exercise serum biomarkers of cardiac and skeletal muscle damage in adolescent runners. Scand J Med Sci Sports 2010. (In press)
76. Nanji AA. Serum creatine kinase isoenzymes: A review. Muscle Nerve 1983;6:83-90.
77. Apple FS. Tesch PA. CK and LD isoenzymes in human single muscle fibers in trained athletes. J Appl Physiol 1989;66:2717-20.
78. Stuewe SR, Gwirtz PA, Mallet RT. Exercise training increases creatine kinase capacity in canine myocardium. Med Sci Sports Exerc 2001;33:92-8.
79. Chen YJ, Serfass RC, Apple FS. Loss of myocardial CK-MB into the circulation following 3.5 hours of swimming in a rat model. Int J Sports Med. 2000;21:561-5.
80. Miller TD, Rogers PJ, Bauer BA, et al. Does exercise training alter myocardial creatine kinase MB isoenzyme content? Med Sci Sports Exerc 1989;21:437-40.
81. Borutaite V. Mitochondria as decision-makers in cell death. Environ Mol Mutagen 2010;51:406-16.
82. Rossignol R, Letellier T, Malgat M, Rocher C, Mazat J-P. T issue variation in the control of oxidative phosphorylation: Implication for mitochondrial diseases. Biochem J 2000;347:45-53.
83. Rasmussen HN, Rasmussen UF. Small scale preparation of skeletal muscle mitochondria, criteria for integrity, and assays with reference to tissue function. Mol Cell Biochem 1997;174:55-60.
84. Hood DA. Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle. Appl Physiol Nutr Metab 2009;34:465-72.
85. Pan SS. Alterations of atrial natriuretic peptide in cardiomyocytes and plasma of rats after different intensity exercise. Scan J Med Sci Sports 2008;18:346-53.
86. Korshunov SS, Skulachev VP, Starkov AA. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 1997; 416:15-8.
87. Malinska D, Kulawiak B, Kudin AP, et al. Complex III-dependent superoxide production of brain mitochondria contributes to seizure-related ROS formation. Biochim Biophys Acta 2010;1797:1163-70.
88. Echtay KS, Roussel D, St-Pierre J, et al. Superoxide activates mitochondrial uncoupling proteins. Nature 2002;415:96-9.
89. Boveris A, Navarro A. Systemic and mitochondrial adaptive responses to moderate exercise in rodents. Free Rad Biol Med 2008;44:224-9.
90. Fry AC, Kraemer WJ. Resistance exercise overtraining and overreaching. Sports Med 1997;23:106-29.
91. Kreider R, Fry AC, O'Toole M. Over-training in sports: Terms, definitions, and prevalence. In: Kreider R, Fry AC, O'Toole M, eds. Over-training in Sport. Champaign: Human Kinetics, 1998:47-66.
92. Seene T, Umnova M, Kaasik P, Alev K, Pehme A. Overtraining injuries in athletic population. In: Tiidus PM, ed. Skeletal Muscle Damage and Repair. Windsor: Human Kinetics, 2008:173-84.
93. Seene T, Kaasik P, Umnova M. Structural rearrangements in contractile apparatus and resulting skeletal muscle remodelling: Effect of exercise training. J Sports Med Phys Fitness 2009;49:410-23.
94. Ding H, Jiang N, Liu H, et al. Response of mitochondrial fusion and fission protein gene expression to exercise in rat skeletal muscle. Biochim Biophys Acta 2010;1800:250-6.
95. Margonis K, Fatouros IG, Jamurtas AZ, et al. Oxidative stress biomarkers responses to physical overtraining: Implications for diagnosis. Free Rad Biol Med 2007;43:901-10.