Stress oxidativo e dano oxidativo muscular esquelético: influência do exercício agudo inabitual e do treino físico

 

Filipe Ferreira

Rita Ferreira

José Alberto Duarte

Centro de Investigação em Actividade Física, Saúde e Lazer

Faculdade de Desporto

Universidade do Porto

Portugal

 

Resumo

A designação “espécies reactivas” (ER) é utilizada para englobar os radicais livres e outras moléculas, as quais, apesar de não possuírem átomos com electrões desemparelhados, são potencialmente geradoras desses radicais. Estas substâncias, naturalmente formadas em situações basais pelo metabolismo celular, são capazes, devido à sua elevada reactividade, de modificar a maioria das moléculas biológicas, colocando em risco a funcionalidade e a viabilidade celular. Particularmente a nível muscular esquelético, a mitocôndria parece constituir a principal fonte e, simultaneamente, o principal alvo das ER. No entanto, a Xantina Oxidase, a Fosfolipase A2, a desaminação das catecolaminas, assim como a infiltração tecidual pós-exercício de leucócitos, poderão contribuir também como fontes adicionais de ER nos músculos exercitados. A ocorrência e a intensidade do resultante dano oxidativo, tanto no músculo esquelético, como nos restantes órgãos e tecidos corporais, para além da taxa de síntese de ER, estão também dependente da capacidade antioxidante que o tecido expressa, quer à custa de antioxidantes endógenos, quer exógenos provenientes da dieta. Essa capacidade antioxidante depende não só do papel específico de cada um dos mecanismos antioxidantes, enzimáticos e não enzimáticos, como também da cooperação entre os mesmos. Como resultado do exercício físico agudo, as taxas de produção de ER de oxigénio aumentam, tal como o dano muscular causado por estes mesmos compostos. Contudo, com a repetição regular do exercício físico (treino), os resultados da literatura mostram que os músculos aumentam a sua capacidade antioxidante, tornando-os mais protegidos contra as ER formadas, não só em repouso, como também durante os exercícios agudos subsequentes.

Palavras-chave: radicais livres, espécies reactivas, antioxidantes, lesão oxidativa, exercício exaustivo, exercício regular

 

Abstract

Oxidative stress and damage in skeletal muscle: Influence of unusual acute exercise and physical conditioning

The designation “reactive species” (RS) is currently used to classify the free radicals and other kind of molecules that despite not containing atoms with unpaired electrons are potentially producers of those radicals. These substances are naturally created at basal conditions by the cellular metabolism, and due to its high reactivity are able of modifying the structure of most of the biological molecules, placing in risk the cellular functionality and viability. Particularly in the skeletal muscle, the mitochondria seem to be the main source of RS and, simultaneously, the main target of these compounds. Xanthine Oxidase, the Phospholipase A2, the catecholamine deamination, as well as the tissue infiltration by leukocytes after exercise, may also contribute as additional sources of RS in exercised muscles. The occurrence and the intensity of the RS-induced oxidative damage in the skeletal muscle or in the remaining organs and tissues, behind the rate of RS synthesis, are also dependent of the antioxidant capacity of the tissue carried out by endogenous and exogenous substances. This antioxidant capacity, performed by enzymatic and non-enzymatic mechanisms, is dependent of the specific paper of each antioxidant and, moreover, also depends of the cooperation between them. As a consequence of the acute and unusual exercise, the production rate of RS of oxygen in skeletal muscle increases severely as well as the oxidative damage caused by these compounds. However, with the regular practice of physical exercise the recruited skeletal muscles increase their antioxidant capacity, becoming more protected against RS, not only at rest conditions but also during the subsequent practice of acute exercises.

Key-words: free radicals, reactive species, antioxidants, oxidative damage, exhaustive exercise, physical training

 

Texto completo disponível apenas em PDF.

Full text only available in PDF format.

 

 

 

Bibliografia

1. Agostinelli E, Arancia G, Vedova L, Belli F, Marra M, Salvi M, Toninello A (2004). The biological functions of polyamine oxidation products by amine oxidases: perspectives of clinical applications. Amino Acids. 27: 347-358.        [ Links ]

2. Ames B, Shigenaga M, Hagen T (1993). Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci USA. 90(17): 7915-7922.

3. Appell HJ, Duarte JA, Glöser S, Remi‹o F, Carvalho F, Bastos M, Soares J. (1997). Administration of tourniquet. II. Prevention of postischemic oxidative stress can reduce muscle edema. Arch Orthop Trauma Surg. 116(1-2): 101-105.

4. Appell HJ, Soares J, Duarte JA (1992). Exercise, muscle damage and fatigue. Sports Med. 13(2): 108-115.

5. Arai M, Imai H, Koumura T, Yoshida M, Emoto K, Umeda M, Chiba M, Nakagawa Y (1999).Mitochondrial phospholipid hydroperoxide glutathione peroxidase plays a major role in preventing oxidative injury to cells. J Biol Chem. 274(8): 4924-4933.

6. Armstrong RB, Warren GL, Warren JA (1991). Mechanisms of exercise-induced muscle fibre injury. Sports Med. 12(3): 184-207.

7. Asami S, Hirano T, Yamaguchi R, Itoh H, Kasai H (1998). Reduction of 8-hydroxyguanine in human leukocyte DNA by physical exercise. Free Radic Res. 29(6): 581-584.

8. Asami S, Hirano T, Yamaguchi R, Tsurudome Y, Itoh H, Kasai H (1998). Effects of forced and spontaneous exercise on 8-hydroxydeoxyguanosine levels in rat organs. Biochem Biophys Res Commun. 243(3): 678-682.

9. Asayama K, Kato K (1990). Oxidative muscular injury and its relevance to hyperthyroidism. Free Radic Biol Med. 8(3): 293-303.

10. Aydin C, Ince E, Koparan S, Cangul I, Naziroglu M, Ak F (2005). Protective effects of long term dietary restriction on swimming exercise-induced oxidative stress in liver, heart and kidney of rat. Cell Biochem Funct. 25: 129-137.

11. Baba T, Shimizu T, Suzuki Y, Ogawara M, Isono K, Koseki H, Kurosawa H, Shirasawa T (2005). Estrogen, insulin, and dietary signals cooperatively regulate longevity signals to enhance resistance to oxidative stress in mice. J Biol Chem. 280(16): 16417-16426.

12. Bachur JA, Garcia SB, Vannucchi H, Jordao AA, Chiarello PG, Zucoloto S (2007). Anti-oxidative systems in rat skeletal muscle after acute physical exercise. Appl Physiol Nutr Metab. 32(2):190-196.

13. Bailey DM, Lawrenson L, McEneny J, Young IS, James PE, Jackson SK, Henry RR, Mathieu-Costello O, McCord JM, Richardson RS (2007). Electron paramagnetic spectroscopic evidence of exercise-induced free radical accumulation in human skeletal muscle. Free Radic Res. 41(2): 182-190.

14. Banerjee A, Mandal A, Chandra D, Chakraborti (2003). Oxidant, antioxidant and physical exercise. Molec Cell Biochem. 253(1-2): 307-312.

15. Beckman K, Ames B (1998). The free radical theory of aging matures. Physiol Rev. 78(2): 547-581.

16. Bejma J, Ji L (1999). Aging and acute exercise enhance free radical generation in rat skeletal muscle. J Appl Physiol. 87(1): 465-470.

17. Bejma J, Ramires P, Ji L (2000). Free radical generation and oxidative stress with ageing and exercise: differential effects in the myocardium and liver. Acta Physiol Scand. 169(4): 343-351.

18. Booth FW, Chakravarthy MV, Gordon SE, Spangenburg EE (2002). Waging war on physical inactivity: using modern molecular ammunition against an ancient enemy. J Appl Physiol. 93(1): 3-30.

19. Carreras MC, Poderoso JJ (2007). Mitochondrial nitric oxide in the signaling of cell integrated responses. Am J Physiol. 292(5): C1569-C1580.

20. Chevion S, Moran D, Heled Y, Shani Y, Regev G, Abbou B, Berenshtein E, Stadtman E, Epstein Y (2003). Plasma antioxidant status and cell injury after severe physical exercise. Proc Natl Acad Sci USA, 100(9): 5119-5123.

21. Child R, Brown S, Day S, Donnelly A, Roper H, Saxton J (1999). Changes in indices of antioxidant status, lipid peroxidation and inflammation in human skeletal muscle after eccentric muscle actions. Clin Scien. 96: 105-115.

22. Child R, Wilkinson D, Fallowfield J, Donnelly A (1998). Elevated serum antioxidant capacity and plasma malondialdehyde concentration in response to a simulated half-marathon run. Med Sci Sports Exerc. 30: 1603-1607.

23. Clarkson P, Hubal M (2002). Exercise-induced muscle damage in humans. Am J Phys Med Rehabil. 81: S52-S69.

24. Clarkson P, Thompson H (2000). Antioxidants: what role do they play in physical activity and health? Am J Clin Nutr. 72: 637S-646S.

25. Criswell D, Powers S, Dodd S, Lawler J, Edwards W (1993). High intensity training-induced changes in skeletal muscle antioxidant enzyme activity. Med Sci Sports Exerc. 25(10): 1135-1140.

26. Cui K, Luo X, Xu K, Ven Murthy MR (2004). Role of oxidative stress in neurodegeneration: recent developments in assay methods for oxidative stress and nutraceutical antioxidants. Prog Neuropsychopharmacol Biol Psychiatry. 28(5): 771-799.

27. Demirbag R, Yilmaz R, Guzel S, Celik H, Kocyigit A, Ozcan E (2006). Effects of treadmill exercise test on oxidative/antioxidative parameters and DNA damage. Anadolu Kardiyol Derg. 6(2):135-140.

28. Di Iorio A, Abate M, Di Renzo D, Russolillo A, Battaglini C, Ripari P, Saggini R, Paganelli R, Abate G (2006). Sarcopenia: age-related skeletal muscle changes from determinants to physical disability. Int J Immunopathol Pharmacol. 19(4): 703-719.

29. Dillard C, Litov R, Savin W, Dumelin E, Tappel A (1978). Effects of exercise, vitamin E, and ozone on pulmonary function and lipid peroxidation. J Appl Physiol. 45(6): 927-932.

30. DiMauro S (1999). Exercise intolerance and the mitochondrial respiratory chain. Ital J Neurol Sci. 20: 387-393.

31. Di Meo S, Venditti P (2001). Mitochondria in exercise-induced oxidative stress. Biol Signals Recept. 10(1-2): 125-140.

32. Dröge, W (2002). Free radicals in the physiological controlo of cell function. Physiol Rev. 82: 47-95.

33. Duarte J, Carvalho F, Bastos ML, Soares J, Appell HJ (1994). Do invading leucocytes contribute to the decrease in glutathione concentrations indicating oxidative stress in exercised muscle, or are they important for its recovery? Eur J Appl Physiol. 68(1): 48-53.

34. Duarte J, Appell HJ, Carvalho F, Bastos ML, Soares J (1993). Endothelium-derived oxidative stress may contribute to exercise-induced muscle damage. Int J Sports Med. 14(8): 440-443.

35. Duarte JA,  Carvalho F, Fernandes E, Remião F, Bastos ML, Magalhães J, Appell H (2004). D-Amphetamine-induced hydrogen peroxide production in skeletal muscle is modulated by Monoamine Oxidase inhibition. Int J Sports Med. 25: 446-449.

36. Duarte J, Leão A, Magalhães J, Ascensão A, Bastos M, Amado F, Vilarinho L, Quelhas D, Appell HJ, Carvalho F (2005). Strenuous exercise aggravates MDMA-induced skeletal muscle damage in mice. Toxicology. 206(3): 349-358.

37. Dudley RW, Danialou G, Govindaraju K, Lands L, Eidelman DE, Petrof BJ (2006). Sarcolemmal damage in dystrophin deficiency is modulated by synergistic interactions between mechanical and oxidative/nitrosative stresses. Am J Pathol. 168(4): 1276-1287.

38. Evans, W. (2000). Vitamin E, vitamin C, and exercise. Am J Clin Nutr. 72: 647S-657S.

39. Fehrenbach E, Niess AM, Veith R, Dickhuth HH, Northoff H (2001). Changes of HSP72-expression in leukocytes are associated with adaptation to exercise under conditions of high environmental temperature. J Leukoc Biol. 69(5): 747-754.

40. Fielding R, Manfredi T, Ding W, Fiatarone M, Evans W, Cannon J (1993). Acute phase response in exercise. III. Neutrophil and IL-1 beta accumulation in skeletal muscle. Am J Physiol. 265(1 Pt 2): R166-R172.

41. Finaud J, Lac G, Filaire E (2006). Oxidative stress: relationship with exercise and training. Sports Med. 36(4): 327-358.

42. Fornai F, Lenzi P, Frenzilli G, Gesi M, Ferruci M, Lazzeri G, Biagioni F, Nigro M, Falleni A, Giusiani M, Pellegrini A, Blandini F, Ruggieri S, Paparelli A (2004). DNA damage and ubiquitinated neuronal inclusions in the substantia nigra and striatium of mice following MDMA (ecstasy). Psychopharmacol. 173: 353-363.

43. Frei B (1999). Molecular and biological mechanisms of antioxidant action. FASEB J. 13(9): 963-964.

44. Fridrovich I (1995). Superoxide radical and superoxide dismutases. Ann Rev Biochem. 64: 97-112.

45. Gassen M, Lamensdorf I, Armony T, Finberg J, Youdim M (2003). Attenuation of methamphetamine induced dopaminergic neurotoxicity by flupirtine: microdialysis study on dopamine release and free radical generation. J Neural Transm. 110: 171-182.

46. Gastell P, Alejo J (2000). Métodos para medir el daño oxidativo. Rev Cub Med Militar. 29(3): 192-198.

47. Gissel H, Clausen T (2001). Excitation-induced Ca2+ influx and skeletal muscle cell damage. Acta Physiol Scand. 171: 327-334.

48. Goldfarb A (1999). Nutritional antioxidants as therapeutic and preventive modalities in exercise-induced muscle damage. Can J Appl Physiol. 24, 3: 249-266.

49. Gomez-Cabrera M, Borrás C, Pallard— F, Sastre J, Ji L, Viña J (2005). Decreasing xanthine oxidase-mediated oxidative stress prevents useful cellular adaptations to exercise in rats. J Physiol. 567(Pt 1): 113-120.

50. Guerrero N, Ruiz M, Barberena E, Dehesa A, Fainstein M (2003). Daño al ADN y niveles de radicales librés en fibroblastos de ratones jóvenes y viejos. Rev Cub Investig Biomed. 22(2): 109-116.

51. Halliwell B (1991). Reactive oxygen species in living systems: source, biochemistry, and role in human disease. Am J Med. 91(suppl 3C): 14S-22S.

52. Harman D (1991). The aging process: major risk factor for disease and death. Proc Natl Acad Sci USA. 88(12): 5360-5363.

53. Harman D (2003). The free radical theory of aging. Antioxid Redox Signal. 5(5): 557-561.

54. Hellesten Y (2000). The role of xantina oxidase in exercise. In: Sen C, Packer L, & Hanninen O (Eds.) Handbook of Oxidants and Antioxidants in Exercise. Basel: Elsevier Science. pp: 153-176.

55. Hellsten Y, Richter E, Kiens B, Bangsbo J (1999). AMP deamination and purine exchange in human skeletal muscle during and after intense exercise. J Physiol. 520 (3): 909-920.

56. Hii CS, Ferrante A (2007). Regulation of the NADPH oxidase activity and anti-microbial function of neutrophils by arachidonic acid. Arch Immunol Ther Exp. 55(2): 99-110.

57. Ho Y, Xiong Y, Ma W, Spector A, Ho D (2004). Mice lacking catalase develop normally but show differential sensitivity to oxidant tissue injury. J Biol Chem. 279(31): 32804-32812.

58. Ide T, Tsutsui H, Kinugawa S, Utsumi H, Kang D, Hattori N, Uchida K, Arimura K, Egashira K, Takeshita A (1999). Mitochondrial electron transport complex I is a potential source of oxygen free radicals in the failing myocardium. Circul Res. 15: 357-363.

59. Jackson M (1996). Oxygen radical production and muscle damage during running exercise. In: Marconnet P, Saltin B, Komi P, Poortmans (Eds.) Human Muscular Function During Dynamic Exercise. Bassel: Karger. pp: 121-133.

60. Jayanthi S, Ladenheim B, Andrews A, Cadet J (1999). Overexpression of human copper/zinc Superoxide Dismutase in transgenic mice attenuates oxidative stress caused by methylenedioxymethamphetamine (Ecstasy). Neuroscience. 91(4): 1379-1387.

61. Jenkins RR (1988). Free radical chemistry. Relationship to exercise. Sports Med. 5(3): 156-170.

62. Ji LL (1995). Exercise and oxidative stress: role of the cellular antioxidant systems. Exerc Sport Sci Rev. 23: 135-166.

63. Ji L (1999). Antioxidants and oxidative stress in exercise. Proc Soc Exp Biol Med. 222: 283-292.

64. Ji L (2000) Exercise-induced oxidative stress in the heart. In: Sen CK, Packer L, Hanninen O editors. Handbook of oxidants and antioxidants in exercise. Basel: Elsevier B.V. p. 689-712.

65. Ji LL (2002) Exercise-induced modulation of antioxidant defense. Ann N Y Acad Sci. 959: 82-92.

66. Ji LL, Gomez-Cabrera MC, Vina J (2006). Exercise and hormesis: activation of cellular antioxidant signaling pathway. Ann N Y Acad Sci. 1067: 425-435.

67. Karanth J, Jeevaratnam K (2005). Oxidative stress and antioxidant status in rat blood, liver and muscle: effect of dietary lipid, carnitine and exercise. Int J Vitam Nutr Res. 75(5): 333-339.

68. Kayatekin B, Gönenç S, Açikgöz O, Uysal N, Dayi A (2002). Effects of sprint exercise on oxidative stress in skeletal muscle and liver. Eur J Appl Physiol. 87(2): 141-144.

69. Kita T, Wagner G, Nakashima T (2003). Current research on methamphetamine-induced neurotoxicity: animals models of monoamine disruption. J Pharmacol Sci. 92: 178-195.

70. Lambertucci R, Leveda-Pires A, Rossoni L, Pithon-Curi T (2007) Effects of aerobic exercise training on antioxidant enzyme activities and mRNA levels in soleus muscle from young and aged rats. Mech Aging Develop. 128(3): 267-275.

71. Laughlin M, Simpson T, Sexton W, Brown O, Smith J, Korthuis R (1990). Skeletal muscle oxidative capacity, antioxidant enzymes, and exercise training. J Appl Physiol. 68(6): 2337-2343.

72. Lawler J, Powers S (1999). Oxidative stress, antioxidant status, and the contracting diaphragm. Can J Appl Physiol. 23(1): 23-55.

73. Leaf D, Kleinman M, Hamilton M, Barstow T (1997). The effect of exercise intensity on lipid peroxidation. Med Sci Sports Exerc. 29: 1036-1039.

74. Lee J, Koo N, Min DB (2004). Reactive oxygen species, aging, and antioxidative nutraceuticals. Compre Rev Food Sci Food Safety. 3: 21-33.

75. Lees SJ, Booth FW (2005). Physical inactivity is a disease. World Rev Nutr Diet. 95: 73-79.

76. Leeuwenburgh C, Heinecke J (2001). Oxidative stress and antioxidants in exercise. Curr Med Chem. 8(7): 829-838.

77. Leeuwenburgh C, Ji L (1996). Alteration of glutathione and antioxidant status with exercise in unfed and refed rats. J Nutr. 126(7): 1833-1843.

78. Lew H, Pyke S, Quintanilha A (1985). Changes in the glutathione status of plasma, liver and muscle following exhaustive exercise in rats. FEBS Lett. 185(2): 262-266.

79. Lieber R, Fridén J (2002). Mechanisms of muscle injury gleaned from animals models. Am J Phys Med Rehab. 81: S70-S79.

80. Liu J, Yeo HC, Overvik-Douki E, Hagen T, Doniger SJ, Chu DW, Brooks GA, Ames BN (2000). Chronically and acutely exercised rats: biomarkers of oxidative stress and endogenous antioxidants. J Appl Physiol. 89: 21-28.

81. Luhová L, Lebeda A, Hedererová D, Pe P (2003). Activities of amine oxidase, peroxidase and catalase in seedlings of Pisum Sativum L. under different light conditions. Plant Soil Environ.  49(4): 151-157.

82. McArdle A, Pattwell D, Vasilaki A, Griffiths R, Jackson J (2001). Contractile activity-induced oxidative stress: cellular origin and adaptive responses. Am J Physiol. 280: C621-C627.

83. McLoughlin T, Mylona E, Hornberger T, Esser K, Pizza F (2003) Inflammatory cells in rat skeletal muscle are elevated after electrically stimulated contractions. J Appl Physiol. 94(3): 876-882.

84. Metin G, Atukeren P, Alturfan A, Gülyasar T, Kaya M, Gümüstas M (2003). Lipid peroxidation, erythrocyte Superoxide-Dismutase activity and trace metals in young male footballers. Yonsei Med J. 44(6): 979-986.

85. Morel Y, Barouki R (1999). Repression of gene expression by oxidative stress. Biochem J. 342: 481-496.

86. Mota MP, Figueiredo P, Duarte JA (2004). Teorias biológicas do envelhecimento. Rev Port Ciênc Desp. 4(1): 81-110.

87. Muller F, Liu Y, Van Remmen H (2004). Complex III releases superoxide to both sides of the inner mitochondrial membrane. J Biol Chem. 279(47): 49064-49073.

88. Nakamura K, Yamagishi S, Yoshida T, Matsui T, Imaizumi T, Inoue H, Sata M (2007). Hydrogen peroxide stimulates pigment epithelium-derived factor gene and protein expression in the human hepatocyte cell line OUMS-29. J Int Med Res. 35(3): 427-432.

89. Niess A, Hartmann A, Grünert-Fuchs M, Poch B, Speit G (1996). DNA damage after exhaustive treadmill running in trained and untrained men. Int J Sports Med. 72(2): 549-554.

90. Nosaka K, Newton M (2002). Concentric or eccentric training effect on eccentric exercise-induced muscle damage. Med Sci Sports Exerc. 34(1): 63-69.

91. Obata T (2002). Dopamine efflux by MPTP and hydroxyl radical generation. J Neural Transm. 109: 1159-1180.

92. Ogonovszky H, Sasvári M, Dosek A, Berkes I, Kaneko T, Tahara S, Nakamoto H, Goto S, Radák Z (2005). The effects of moderate, strenuous, and overtraining on oxidative stress markers and DNA repair in rat liver. Can J Appl Physiol. 30(2): 186-195.

93. Ohkuwa T, Sato Y, Naoi M (1997). Glutathione status and reactive oxygen generation in tissues of young and old exercised rats. Acta Physiol Scand. 159: 237-244.

94. Oliveira A, Schneider C, Ribeiro J, Deresz L, Barp J, Belló-Klein A (2003). Oxidative stress after three different intensities of running. Med Sci Sports Exerc. 35: S367.

95. O'Neill C, Stebbins C, Bonigut S, Halliwell B, Longhurst J (1996). Production of hydroxyl radicals in contracting skeletal muscle of cats. J Appl Physiol. 81(3): 1197-1206.

96. Perez A, Cabral de Oliveira A, Estevez E, Molina A, Prieto J, Alvarez A (2003). Mitochondrial, sarcoplasmic membrane integrity and protein degradation in heart and skeletal muscle in exercised rats. Comp Biochem Physiol C Toxicol Pharmacol. 2: 199-206.

97. Petrova V, Rasheva T, Kujumdzieva A (2002). Catalase enzyme in mitochondria of Saccharomyces cerevisiae. Electron J Biotechnol. 5(1): 29-41.

98. Powers S, Criswell D, Lawler J, Ji L, Martin D, Herb R, Dudley G (1994). Influence of exercise and fiber type on antioxidant enzyme activity in rat skeletal muscle. Am J Physiol. 266: R375-R380.

99. Powers S, Howley E (2001). Exercise Physiology: Theory and Application to Fitness and Performance. Fourth Ed., McGraw Hill, New York.

100. Powers S, Leeuwenburgh C (1999). Exercise training-induced alterations in skeletal muscle antioxidant capacity: a brief review. Med Sci Sports Exerc. 31(7): 987-997.

101. Powers S, Lennon S (1999). Analysis of cellular responses to free radicals: focus on exercise and skeletal muscle. Proc Nutr Soc. 58(4): 1025-1033.

102. Pryor W (1986). Oxy-Radicals and Related Species: Their Formation, Lifetimes, and Reactions. Ann Rev Physiol. 48: 657-667.

103. Radi R (1993). Biological antioxidant systems. Toxicol Ind Health. 9: 53-62.

104. Räisänen S, Lehenkari P, Tasanen M, Rahkila P, Härkönen P, Väänänen (1999). Cronic anhydrase III protects cells from hydrogen peroxide-induced apoptosis. FASEB J. 13: 513-522.

105. Sankarapandi S, Zweier J (1999). Bicarbonate is required for the peroxidase function of Cu, Zn-superoxide dismutase at physiological pH. J Biol Chem. 274(3): 1226-1232.

106. Selamoglu S, Turgay F, Kayatekin B, Gönenc S, Yslegen C (2000). Aerobic and anaerobic training effects on the antioxidant enzymes of the blood. Acta Physiol Hung. 87(3): 267-273.

107. Sen CK (1995). Oxidants and antioxidants in exercise. J Appl Physiol. 79(3): 675-686.

108. Sen CK (2001). Antioxidants in Exercise Nutrition. Sports Med. 31(13): 891-908.

109. Shan XQ, Aw TY, Jones DP (1989). Glutathione-dependent protection against oxidative injury. Pharmacol Ther. 47(1): 61-71.

110. Sies H (1997). Physiological society symposium: impaired endothelial and smooth muscle cell function in oxidative stress. Oxidative stress: Oxidants and antioxidants. Exp Physiol. 82: 291-295.

111. Smolka M, Zoppi C, Alves A, Silveira L, Marangoni S, Pereira-Da-Silva L, Novello JC, Macedo DV (2000). HSP72 as a complementary protection against oxidative stress induced by exercise in the soleus muscle of rats. Am J Physiol. 279: R1539-R1545.

112. Stadtman E (1993). Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Ann Rev Biochem. 62: 797-821.

113. Symons JD, Theodossy SJ, Longhurst JC, Stebbins CL (1991). Intramuscular accumulation of prostaglandins during static contraction of the cat triceps surae. J Appl Physiol. 71(5): 1837-1842.

114. Tidball JG, Wehling-Henricks M (2007). The role of free radicals in the pathophysiology of muscular dystrophy. J Appl Physiol. 102(4): 1677-1686.

115. Tonkonogi M, Sahlin K (2002). Physical exercise and mitochondrial function in human skeletal muscle. Exerc Sport Sci Rev. 30(3): 129-137.

116. Vandenburgh HH, Hatfaludy S, Sohar I, Shansky J (1990). Stretch-induced prostaglandins and protein turnover in cultured skeletal muscle. Am J Physiol. 259(2 Pt 1): C232-C240.

117. Venditti P, Di Meo S (1997). Effect of training on antioxidant capacity, tissue damage, and endurance of adult male rats. Int J Sports Med. 18(7): 497-502.

118. Viitala P, Newhouse I, LaVoie N, Gottardo C (2004). The effects of antioxidant vitamin supplementation on resistance exercise induced lipid peroxidation in trained and untrained participants. Lipids Health Dis. 3(14): 1-9.

119. Vollaard N, Shearman J, Cooper C (2005). Exercise-induced oxidative stress: myths, realities and physiological relevance. Sports Med. 35(12): 1045-1062.

120. Wang W, Ballatori N (1998). Endogenous glutathione conjugates: occurrence and biological functions. Pharmacol Rev. 50(3): 335-356.

121. Watson T, MacDonald-Wicks L, Garg M (2005).Oxidative stress and antioxidants in athletes undertaking regular exercise training. Int J Sport Nutr Exerc Metab. 15(2): 131-146.

122. White C, Shelton J, Moellering D, Jo H, Patel R, Darley-Usmar V (2000). Exercise and xantine oxidase in the vasculature: superoxide and nitric oxide interactions. In: Sen C, Packer L & Hanninen, (Eds.) Handbook of Oxidants and Antioxidants in Exercise. Basel: Elsevier Science. pp: 69-86.

123. Yeldandi A, Rao M, Reddy J (2000). Hydrogen peroxide generation in peroxisome proliferator-induced oncogenesis. Mutat Res. 448(2): 159-177. 

124. Yildiz O (2007). Vascular smooth muscle and endothelial functions in aging. Ann N Y Acad Sci. 1100: 353-360.

125. Yu B (1994). Cellular defenses against damage from reactive oxygen species. Physiol Rev. 74(1): 139-162.

 

 

 

Correspondência

José Alberto Duarte

CIAFEL, FADEUP

R. Dr. Plácido Costa, 91

4200-450 Porto

Tel: 225074784; Fax: 225500689

e-mail: jarduarte@fade.up.pt