Antioxidants and skeletal muscle performance: "Common knowledge" vs. experimental evidence

Frontiers in Physiology

Volumn 3 MAR, Issue , 2012, Pages

  Hernández, Andrés ^a   Cheng, Arthur ^a   Westerblad, Håkan ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Antioxidants; Exercise; Fatigue; Muscle; Performance; Reactive nitrogen species; Reactive oxygen species; Recovery

Indexed keywords

EID: 84866282500     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00046     Document Type: Short Survey

References (68)

1. Allen, D. G., Lamb, G. D., and Westerblad, H. (2008). Skeletal muscle fatigue: cellular mechanisms. Phys-iol. Rev. 88, 287-332.
2. Allman, B. L., and Rice, C. L. (2001). Incomplete recovery of voluntary isometric force after fatigue is not affected by old age. Muscle Nerve 24, 1156-1167.
3. Andrade, F. H., Reid, M. B., Allen, D. G., and Westerblad, H. (1998a). Effect of hydrogen peroxide and dithio-threitol on contractile function of single skeletal muscle fibres from the mouse. J. Physiol. (Lond.) 509, 565-575.
4. Andrade, F. H., Reid, M. B., Allen, D. G., and Westerblad, H. (1998b). Effect of nitric oxide on single skeletal muscle fibres from the mouse. J. Physiol. (Lond.) 509, 577-586.
5. Andrade, F. H., Reid, M. B., and Westerblad, H. (2001). Contractile response of skeletal muscle to low peroxide concentrations: myofibrillar calcium sensitivity as a likely target for redox-modulation. FASEB J. 15, 309-311.
6. Aruoma, O. I., Halliwell, B., Hoey, B. M., and Butler, J. (1989). The antioxidant action of N-acetylcysteine: its reaction with hydrogen peroxide, hydroxyl radical, superoxide, and hypochlorous acid. Free Raic. Biol. Med. 6, 593-597.
7. Ashton, T., Young, I. S., Peters, J. R., Jones, E., Jackson, S. K., Davies, B., and Rowlands, C. C. (1999). Electron spin resonance spectroscopy, exercise, and oxidative stress: an ascorbic acid intervention study. J. Appl. Physiol. 87, 2032-2036.
8. Baker, A. J., Kostov, K. G., Miller, R. G., andWeiner,M.W. (1993). Slow force recovery after long-duration exercise: metabolic and activation factors in muscle fatigue. J. Appl. Physiol. 74, 2294-2300.
9. Bonetti, A., Solito, F., Carmosino, G., Bargossi, A. M., and Fiorella, P. L. (2000). Effect of ubidecarenone oral treatment on aerobic power in middle-aged trained subjects. J. Sports Med. Phys. Fitness 40, 51-57.
10. Booth, J., Mckenna, M. J., Ruell, P. A., Gwinn,T.H.,Davies,G.M.,Thomp-son, M. W., Harmer,A. R., Hunter, S. K.,and Sutton,J.R. (1997). Impaired calcium pump function does not slow relaxation in human skeletal muscle after prolonged exercise. J. Appl. Physiol. 83, 511-521.
11. Braun, B., Clarkson, P. M., Freed-son, P. S., and Kohl, R. L. (1991). Effects of coenzyme Q10 supplementation on exercise performance, VO2max, and lipid peroxidation in trained cyclists. Int. J. Sport Nutr. 1, 353-365.
12. Bruton, J. D., Place, N.,Yamada, T., Silva, J. P., Andrade, F. H., Dahlstedt, A. J., Zhang, S. J., Katz, A., Larsson, N. G., and Westerblad, H. (2008). Reactive oxygen species and fatigue-induced prolonged low-frequency force depression in skeletal muscle fibres of rats, mice and SOD2 over-expressing mice. J. Physiol. (Lond.) 586, 175-184.
13. Bryant, R. J., Ryder, J., Martino, P., Kim, J., and Craig, B. W. (2003). Effects of vitamin E and C supplementation either alone or in combination on exercise-induced lipid peroxidation in trained cyclists. J. Strength Cond. Res. 17, 792-800.
14. Clarkson, P. M. (1995). Antioxidants and physical performance. Crit. Rev. Food Sci. Nutr. 35, 131-141.
15. Commoner, B., Townsend, J., and Pake, G. E. (1954). Free radicals in biological materials. Nature 174, 689-691.
16. Corn, S. D., and Barstow, T. J. (2011). Effects of oral N-acetylcysteine on fatigue, critical power, and W' in exercising humans. Respir. Physiol. Neurobiol. 178, 261-268.
17. Davies, K. J., Quintanilha, A. T., Brooks, G. A., and Packer, L. (1982). Free radicals and tissue damage produced by exercise. Biochem. Biophys. Res. Commun. 107, 1198-1205.
18. Dekhuijzen, P. N. (2004). Antioxidant properties of N-acetylcysteine: their relevance in relation to chronic obstructive pulmonary disease. Eur. Respir. J. 23, 629-636.
19. Diaz, P. T., Brownstein, E., and Clanton, T. L. (1994). Effects of N-acetylcysteine on in vitro diaphragm function are temperature dependent. J. Appl. Physiol. 77, 2434-2439.
20. Diaz, P. T., Costanza, M. J., Wright, V. P., Julian, M. W., Diaz, J. A., and Clanton, T. L. (1998). Dithiothre-itol improves recovery from in vitro diaphragm fatigue. Med. Sci. Sports Exerc. 30, 421-426.
21. Dröge, W. (2002). Free radicals in the physiological control of cell function. Physiol. Rev. 82, 47-95.
22. Duhamel, T. A., Stewart, R. D., Tupling, A. R., Ouyang, J., and Green, H. J. (2007). Muscle sarcoplasmic reticu-lum calcium regulation in humans during consecutive days of exercise and recovery. J. Appl. Physiol. 103, 1212-1220.
23. Edwards, R. H., Hill, D. K., Jones, D. A., and Merton, P. A. (1977). Fatigue of long duration in human skeletal muscle after exercise. J. Physiol. (Lond.) 272, 769-778.
24. Ferreira, L. F., and Reid, M. B. (2008). Muscle-derived ROS and thiol regulation in muscle fatigue. J. Appl. Physiol. 104, 853-860.
25. Gaeini, A. A., Rahnama, N., and Hamedinia, M. R. (2006). Effects of vitamin E supplementation on oxida-tive stress at rest and after exercise to exhaustion in athletic students. J. Sports Med. Phys. Fitness 46, 458-461.
26. Glover, E. I., Martin, J., Maher, A., Thornhill, R. E., Moran, G. R., and Tarnopolsky, M. A. (2010). A randomized trial of coenzyme Q10 in mitochondrial disorders. Muscle Nerve 42, 739-748.
27. Hill, C. A., Thompson, M. W., Ruell, P. A., Thom, J. M., and White, M. J. (2001). Sarcoplasmic reticulum function and muscle contractile character following fatiguing exercise in humans. J. Physiol. (Lond.) 531, 871-878.
28. Karlsson, J., Lin, L. Sylven, C., and Jansson, E. (1996). Muscle ubiquinone in healthy physically active males. Mol. Cell. Biochem. 156, 169-172.
29. Kelly, M. K., Wicker, R. J., Barstow, T. J., and Harms, C. A. (2009). Effects of N-acetylcysteine on respiratory muscle fatigue during heavy exercise. Respir. Physiol. Neurobiol. 165, 67-72.
30. Khawli, F. A., and Reid, M. B. (1994). N-acetylcysteine depresses contractile function and inhibits fatigue of diaphragm in vitro. J. Appl. Physiol. 77, 317-324.
31. Laaksonen, R., Fogelholm, M., Himberg, J. J., Laakso, J., and Salorinne, Y. (1995). Ubiquinone supplementation and exercise capacity in trained young and older men. Eur. J. Appl. Physiol. Occup. Physiol. 72, 95-100.
32. Lamb, G. D., and Westerblad, H. (2011). Acute effects of reactive oxygen and nitrogen species on the contractile function of skeletal muscle. J. Physiol. (Lond.) 589, 2119-2127.
33. Lawrence, J. D., Bower, R. C., Riehl, W. P., and Smith, J. L. (1975). Effects of alpha-tocopherol acetate on the swimming endurance of trained swimmers. Am. J. Clin. Nutr. 28, 205-208.
34. Malm, C., Svensson, M., Ekblom, B., and Sjodin, B. (1997). Effects of ubiquinone-10 supplementation and high intensity training on physical performance in humans. Acta Physiol. Scand. 161, 379-384.
35. Matuszczak,Y., Farid, M.,Jones, J., Lans-downe, S., Smith, M. A., Taylor, A. A., and Reid, M. B. (2005). Effects of N-acetylcysteine on glutathione oxidation and fatigue during handgrip exercise. Muscle Nerve 32, 633-638.
36. +-pump activity and delays fatigue during prolonged exercise in humans. J. Physiol. (Lond.) 576, 279-288.
37. Medved, I., Brown, M. J., Bjorksten, A. R., Leppik, J. A., Sostaric, S., and McKenna, M. J. (2003). N-acetylcysteine infusion alters blood redox status but not time to fatigue during intense exercise in humans. J. Appl. Physiol. 94, 1572-1582.
38. Medved, I., Brown, M. J., Bjork-sten, A. R., and McKenna, M. J. (2004a). Effects of intravenous N-acetylcysteine infusion on time to fatigue and potassium regulation during prolonged cycling exercise. J. Appl. Physiol. 96, 211-217.
39. Medved, I., Brown, M. J., Bjorksten, A. R., Murphy, K. T., Petersen, A. C., Sostaric, S., Gong, X., and McKenna, M. J. (2004b). N-acetylcysteine enhances muscle cysteine and glu-tathione availability and attenuates fatigue during prolonged exercise in endurance-trained individuals. J. Appl. Physiol. 97, 1477-1485.
40. Mishima, T., Yamada, T., Matsunaga, S., and Wada, M. (2005). N-acetylcysteine fails to modulate the in vitro function of sarcoplasmic reticulum of diaphragm in the final phase of fatigue. Acta Physiol. Scand. 184, 195-202.
41. Mizuno, K., Tanaka, M., Nozaki, S., Mizuma, H., Ataka, S., Tahara, T., Sugino, T., Shirai, T., Kajimoto, Y., Kuratsune, H., Kajimoto, O., and Watanabe, Y. (2008). Antifatigue effects of coenzyme Q10 during physical fatigue. Nutrition 24, 293-299.
42. Mizuno, M., Quistorff, B., Theorell, H., Theorell, M., and Chance, B. (1997). Effects of oral supplementation of coenzyme Q10 on 31P-NMR detected skeletal muscle energy metabolism in middle-aged post-polio subjects and normal volunteers. Mol. Aspects Med. 18(Suppl.), S291-S298.
43. 2+ sensitivity in fatiguing mouse skeletal muscle at 37 degrees C. J. Physiol. (Lond.) 564, 189-199.
44. 2+ sensitivity in mouse skeletal muscle is reversed by dithiothreitol. J. Physiol. (Lond.) 571, 191-200.
45. Murphy, R. M., Dutka, T. L., and Lamb, G. D. (2008). Hydroxyl radical and glutathione interactions alter calcium sensitivity and maximum force of the contractile apparatus in rat skeletal muscle fibres. J. Physiol. (Lond.) 586, 2203-2216.
46. Nielsen, A. N., Mizuno, M., Ratkevicius, A., Mohr, T., Rohde, M., Mortensen, S. A., and Quistorff, B. (1999). No effect of antioxidant supplementation in triathletes on maximal oxygen uptake, 31P-NMRS detected muscle energy metabolism and muscle fatigue. Int. J. Sports Med. 20, 154-158.
47. 2+ content after fatigue. J. Appl. Physiol. 93, 1999-2008.
48. Petersen,A. C., McKenna,M. J., Medved, I., Murphy, K. T., Brown, M. J., Della Gatta, P., and Cameron-Smith, D. (2011). Infusion with the antioxidant N-acetylcysteine attenuates early adaptive responses to exercise in human skeletal muscle. Acta Physiol. (Oxf.) 204, 382-392.
49. Place, N., Yamada, T., Zhang, S. J., Westerblad, H., and Bruton, J. D. (2009). High temperature does not alter fatigability in intact mouse skeletal muscle fibres. J. Physiol. (Lond.) 587, 4717-4724.
50. Powers, S. K., DeRuisseau, K. C., Quindry, J., and Hamilton, K. L. (2004). Dietary antioxidants and exercise. J. Sports Sci. 22, 81-94.
51. Powers, S. K., and Jackson, M. J. (2008). Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol. Rev. 88, 1243-1276.
52. Pye, D., Palomero, J., Kabayo, T., and Jackson, M. J. (2007). Real-time measurement of nitric oxide in single mature mouse skeletal muscle fibres during contractions. J. Physiol. (Lond.) 581, 309-318.
53. Reid, M. B., Stokic, D. S., Koch, S. M., Khawli, F. A., and Leis, A. A. (1994). N-acetylcysteine inhibits muscle fatigue in humans. J. Clin. Invest. 94, 2468-2474.
54. Ristow, M., Zarse, K., Oberbach, A., Klöting, N., Birringer, M., Kiehn-topf, M., Stumvoll, M., Kahn, C. R., and Blüher, M. (2009). Antioxidants prevent health-promoting effects of physical exercise in humans. Proc. Natl. Acad. Sci. U.S.A. 106, 8665-8670.
55. Rokitzki, L., Logemann, E., Huber, G., Keck, E., and Keul, J. (1994a). Alphatocopherol supplementation in racing cyclists during extreme endurance training. Int. J. Sport Nutr. 4, 253-264.
56. Rokitzki, L., Logemann, E., Sagredos, A. N., Murphy, M., Wetzel-Roth, W., and Keul, J. (1994b). Lipid peroxidation and antioxidative vitamins under extreme endurance stress. Acta Physiol. Scand. 151, 149-158.
57. Sandström, M. E., Zhang, S. J., Bru-ton, J., Silva, J. P., Reid, M. B., Westerblad, H., and Katz, A. (2006). Role of reactive oxygen species in contraction-mediated glucose transport in mouse skeletal muscle. J. Physiol. (Lond.) 575, 251-262.
58. 2+-ATPase. Arch. Biochem. Biophys. 246, 589-601.
59. Shephard, R. J., Campbell, R., Pimm, P., Stuart, D., and Wright, G. R. (1974). Vitamin E, exercise, and the recovery from physical activity. Eur. J. Appl. Physiol. Occup. Physiol. 33, 119-126.
60. Shindoh, C., DiMarco, A., Thomas, A., Manubay, P., and Supinski, G. (1990). Effect of N-acetylcysteine on diaphragm fatigue. J. Appl. Physiol. 68, 2107-2113.
61. Strobel, N. A., Peake, J. M., Matsumoto, A., Marsh, S. A., Coombes, J. S., and Wadley, G. D. (2011). Antioxidant supplementation reduces skeletal muscle mitochondrial biogenesis. Med. Sci. Sports Exerc. 43, 1017-1024.
62. Sumida, S., Tanaka, K., Kitao, H., and Nakadomo, F. (1989). Exercise-induced lipid peroxidation and leakage of enzymes before and after vitamin E supplementation. Int. J. Biochem. 21, 835-838.
63. Supinski, G. S., Stofan, D., Ciufo, R., and DiMarco, A. (1997). N-acetylcysteine administration alters the response to inspiratory loading in oxygen-supplemented rats. J. Appl. Physiol. 82, 1119-1125.
64. Travaline, J. M., Sudarshan, S., Roy, B. G., Cordova, F., Leyenson, V., and Criner, G. J. (1997). Effect of N-acetylcysteine on human diaphragm strength and fatigability. Am. J. Resp. Crit. Care Med. 156, 1567-1571.
65. Westerblad, H., and Allen, D. G. (1991). Changes in myoplasmic calcium concentration during fatigue in single mouse muscle fibers. J. Gen. Physiol. 98, 615-635.
66. 2+]i to the slowing of relaxation in fatigued single fibres from mouse skeletal muscle. J. Physiol. (Lond.) 468, 729-740.
67. Westerblad, H., and Allen, D. G. (2011). Emerging roles of ROS/RNS in muscle function and fatigue. Antioxid. Redox Signal. 15, 2487-2499.
68. Weston, S. B., Zhou, S., Weatherby, R. P., and Robson, S. J. (1997). Does exogenous coenzyme Q10 affect aerobic capacity in endurance athletes? Int. J. Sport Nutr. 7, 197-206