Role of mitochondrial superoxide dismutase in contraction-induced generation of reactive oxygen species in skeletal muscle extracellular space

American Journal of Physiology - Cell Physiology

Volumn 286, Issue 5 55-5, 2004, Pages

  McArdle, A ^a   Van Der Meulen, J ^b   Close, G L ^a   Pattwell, D ^a   Van Remmen, H ^c   Huang, T T ^d   Richardson, A G ^c   Epstein, C J ^d   Faulkner, J A ^b   Jackson, M J ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Hydroxyl radicals; Microdialysis

Indexed keywords

2,3 DIHYDROXYBENZOIC ACID; CATALASE; CYTOCHROME C; GLUTATHIONE; HYDROXYL RADICAL; MALONALDEHYDE; REACTIVE OXYGEN METABOLITE; SALICYLIC ACID; SUPEROXIDE; SUPEROXIDE DISMUTASE;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRACELLULAR SPACE; GASTROCNEMIUS MUSCLE; KNOCKOUT MOUSE; MALE; MICRODIALYSIS; MITOCHONDRION; MOUSE; MUSCLE CONTRACTION; MUSCLE ISOMETRIC CONTRACTION; NONHUMAN; PRIORITY JOURNAL; SKELETAL MUSCLE;

ANIMALS; CYTOCHROMES C; EXTRACELLULAR SPACE; HETEROZYGOTE; HYDROXYBENZOIC ACIDS; ISOMETRIC CONTRACTION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

ANIMALIA;

EID: 11144356719     PISSN: 03636143     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpcell.00322.2003     Document Type: Article

References (47)

1. Anderson ME. Measurement of antioxidants: glutathione. In: Free Radicals: a Practical Approach, edited by Punchard NA and Kelly FJ. Oxford, UK: IRL, 1996, p. 213-226.
2. Balon TW and Nadler JL. Nitric oxide release is present from incubated skeletal muscle preparations. J Appl Physiol 77: 2519-2521, 1994.
3. Brooks SV and Faulkner JA. Contractile properties of skeletal muscles from young, adult and aged mice. J Physiol 404: 71-82, 1988.
4. Chirico S. High-performance liquid chromatography-based thiobarbituric acid tests. Methods Enzymol 233: 314-318, 1990.
5. Claiborne A. Catalase activity. In: CRC Handbook of Methods for Oxygen Radical Research, edited by Greenwald RA. Boca Raton, FL: CRC, 1985, p. 283-284.
6. Crapo JD, McCord JM, and Fridovich I. Preparation and assay of superoxide dismutases. Methods Enzymol 105: 382-393, 1984.
7. Davies KJA, Quintanilla AT, Brooks GA, and Packer L. Free radicals and tissue damage produced by exercise. Biochem Biophys Res Commun 107: 1198-1205, 1982.
8. De Grey AD. The reductive hotspot hypothesis: an update. Arch Biochem Biophys 373: 295-301, 2000.
9. Denicola A, Souza JM, Gatti RM, Augusto O, and Raddi R. Desferrioxamine inhibition of the hydroxyl radical-like reactivity of peroxynitrite: role of the hydroxamic groups. Free Radic Biol Med 19: 11-19, 1995.
10. 2+ homeostasis. Arch Biochem Biophys 235: 343-350, 1984.
11. Ferger B, Rose S, Jenner A, Halliwell B, and Jenner P. 6-Hydroxydopamine increases hydroxyl radical production and DNA damage in rat striatum. Neuroreport 12: 1155-1159, 2001.
12. Forman HJ and Azzi A. On the virtual existence of superoxide anions in mitochondria: thoughts regarding its role in pathophysiology. FASEB J 11: 374-375, 1997.
13. Grootveld M and Halliwell B. Aromatic hydroxylation as a potential measure of hydroxyl-radical formation in vivo. Identification of hydroxylated derivatives of salicylate in human body fluids. Biochem J 237: 499-504, 1986.
14. Gus'kova RA, Ivanov II, Kol'tover VK, Akhobadze VV, and Rubin AB. Permeability of bilayer lipid membranes for superoxide radicals. Biochim Biophys Acta 778: 579-585, 1984.
15. Halliwell B and Gutteridge JMC. Free Radical Biology and Medicine. Oxford: Oxford Univ. Press, 1989.
16. Halliwell B and Kaur H. Hydroxylation of salicylate and phenylalanine as assays for hydroxyl radicals: a cautionary note visited for the third time. Free Radic Res 27: 239-244, 1997.
17. Han D, Antunes F, Canali R, Rettori D, and Cadenas E. Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol. J Biol Chem 278: 5557-5563, 2003.
18. Hirschfield W, Moody MR, O'Brien W, Gregg AR, Bryan RM Jr, and Reid MB. Nitric oxide release and contractile properties of skeletal muscles from mice deficient in type III NOS. Am J Physiol Regul Integr Comp Physiol 278: R95-R100, 2000.
19. Huang TT, Carlson EJ, Gillespie AM, and Epstein CJ. Genetic modification of the dilated cardiomyopathy and neonatal lethality phenotype of mice lacking manganese superoxide dismutase. Age Ageing 21: 83-84, 1998.
20. Jackson MJ. Free radical mechanisms in exercise-related muscle damage. In: Oxidative Stress in Skeletal Muscle, edited by Reznick AZ, Packer L, Sen CK, Holloszy JO, and Jackson MJ. Basel: Birkhauser, 1998, p. 75-86.
21. Jackson MJ, Edwards RHT, and Symons MCR. Electron spin resonance studies of intact mammalian skeletal muscle. Biochim Biophys Acta 847: 185-190, 1985.
22. Kaur H, Whiteman M, and Halliwell B. Peroxynitrite-dependent aromatic hydroxylation and nitration of salicylate and phenylalanine. Is hydroxyl radical involved? Free Radic Res 26: 71-82, 1997.
23. Lawler JM and Hu Z. Interaction of nitric oxide and reactive oxygen species on rat diaphragm contractility. Acta Physiol Scand 169: 229-236, 2000.
24. Lebovitz RM, Zhang H, Vogel H, Cartright J, Dionne L, Lu N, Huang S, and Matzuk MM. Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc Natl Acad Sci USA 93: 9782-9787, 1996.
25. Loschen G, Azzi A, Richter C, and Flohe L. Superoxide radicals as precursors of mitochondrial hydrogen peroxide. FEBS Lett 42: 68-72, 1974.
26. Lymar SV, Khairutdiov RF, and Hurst JK. Hydroxyl radical formation by O-O bond hydrolysis in peroxynitrous acid. Inorg Chem 42: 5259-5266, 2003.
27. McArdle A, Pattwell D, Vasilaki A, Griffiths RD, and Jackson MJ. Contractile activity-induced oxidative stress: cellular origin and adaptive responses. Am J Physiol Cell Physiol 280: C621-C627, 2001.
28. Morré DM, Lenaz G, and Morré DJ. Surface oxidase and oxidative stress propagation in aging. J Exp Biol 203: 1513-1521, 2000.
29. Murrant CL and Reid MB. Detection of reactive oxygen and reactive nitrogen species in skeletal muscle. Microsc Res Tech 55: 236-248, 2001.
30. Narayan M, Berliner LJ, Merola AJ, Diaz PT, and Clanton TL. Biological reactions of peroxynitrite: evidence of alternative pathways of salicylate hydroxylation. Free Radic Res 27: 63-72, 1997.
31. Obata T. Use of microdialysis for in vivo monitoring of hydroxyl radical generation in the rat. J Pharm Pharmacol 49: 724-730, 1997.
32. O'Neill CA, Stebbins CL, Bonigut S, Halliwell B, and Longhurst JC. Production of hydroxyl radicals in contracting skeletal muscle of cats. J Appl Physiol 81: 1197-1206, 1996.
33. Paky A, Michael JR, Burke-Wolin TM, Wolin MS, and Gurtner GH. Endogenous production of superoxide by rabbit lungs: effects of hypoxia or metabolic inhibitors. J Appl Physiol 74: 2868-2874, 1993.
34. Pattwell D, McArdle A, Griffiths RD, and Jackson MJ. Measurement of free radical production by in vivo microdialysis during ischemia/reperfusion injury to skeletal muscle. Free Radic Biol Med 30: 979-985, 2001.
35. Reid MB. Reactive oxygen and nitric oxide in skeletal muscle. News Physiol Sci 11: 114-119, 1996.
36. Reid MB and Durham WJ. Generation of reactive oxygen and nitrogen species in contracting skeletal muscle: potential impact on aging. Ann NY Acad Sci 959: 108-116, 2002.
37. Reid MB, Shoji T, Moody MR, and Entman ML. Reactive oxygen in skeletal muscle. II. Extracellular release of free radicals. J Appl Physiol 75: 1805-1809, 1992.
38. Reznick AZ, Packer L, Sen CK, Holloszy JO, and Jackson MJ. Oxidative Stress in Skeletal Muscle. Basel: Birkhauser, 1998.
39. Sen CK and Goldfarb AH. Antioxidants and physical exercise. In: Handbook of Oxidants and Antioxidants in Exercise, edited by Sen CK, Packer L, and Hanninen O. Amsterdam: Elsevier, 2000, p. 297-320.
40. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, and Klenk DC Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76-85, 1985.
41. Sun JZ, Kaur H, Halliwell B, Li XY, and Bolli R. Use of aromatic hydroxylation of phenylalanine to measure production of hydroxyl radicals after myocardial ischemia in vivo. Direct evidence for a pathogenic role of the hydroxyl radical in myocardial stunning. Circ Res 73: 534-549.
42. Thompson L, Trujillo M, Telleri R, Radi R. Kinetics of cytochrome c oxidation by peroxynitrite: implications for superoxide measurements in nitric oxide-producing biological systems. Arch Biochem Biophys 319: 153-154, 1995.
43. Van den Hoek TL, Becker LB, Shao Z, Li C, and Schumacker PT. Reactive oxygen species released from mitochondria during brief hypoxia induce preconditioning in cardiomyocytes. J Biol Chem 273: 18092-18098, 1998.
44. Van der Meulen JH, McArdle A, Jackson MJ, and Faulkner JA. Contraction-induced injury to the extensor digitorum longus muscles of rats: the role of vitamin E. J Appl Physiol 83: 817-823, 1997.
45. Van Remmen H, Salador C, Yang H, Huang TT, Epstein CJ, and Richardson A. Characterisation of the antioxidant status of the heterozygous manganese superoxide dismutase knockout mouse. Arch Biochem Biophys 363: 91-97, 1999.
46. Van Remmen H, Williams MD, Guo Z, Estlack L, Yang H, Carlson EJ, Epstein CJ, Huang TT, and Richardson A. Knockout mice heterozygous for Sod2 show alterations in cardiac mitochondrial function and apoptosis. Am J Physiol Heart Circ Physiol 281: H1422-H1432, 2001.
47. Williams MD, Van Remmen H, Conrad CC, Huang TT, Epstein CJ, and Richardson A. Increased oxidative damage is correlated to altered mitochondrial function in heterozygous manganese superoxide dismutase knockout mice. J Biol Chem 273: 28510-28515, 1998