Age-dependent increase in oxidative stress in gastrocnemius muscle with unloading

Journal of Applied Physiology

Volumn 105, Issue 6, 2008, Pages 1695-1705

  Siu, Parco M ^a   Pistilli, Emidio E ^b   Alway, Stephen E ^b  

^a HONG KONG POLYTECHNIC UNIVERSITY   (Hong Kong)

^b WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Muscle disuse; Reactive oxygen species; Sarcopenia

Indexed keywords

3 NITROTYROSINE; 4 HYDROXYALKENAL; ALKENE DERIVATIVE; CATALASE; HYDROGEN PEROXIDE; MALONALDEHYDE; MANGANESE SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

AGE; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GASTROCNEMIUS MUSCLE; IMMOBILIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

AGING; ANIMALS; BLOTTING, WESTERN; CATALASE; FEMALE; HINDLIMB SUSPENSION; HYDROGEN PEROXIDE; MALE; MALONDIALDEHYDE; MUSCLE, SKELETAL; ORGAN SIZE; OXIDATIVE STRESS; RATS; RATS, INBRED BN; RATS, INBRED F344; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SUPEROXIDE DISMUTASE; TYROSINE;

EID: 57349109417     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.90800.2008     Document Type: Article

References (66)

1. Adams NR, Boice R. A longitudinal study of dominance in an outdoor colony of domestic rats. J Comp Psychol 97: 24-33, 1983.
2. Appell HJ, Duarte JA, Soares JM. Supplementation of vitamin E may attenuate skeletal muscle immobilization atrophy. Int J Sports Med 18: 157-160, 1997.
3. Arbogast S, Smith J, Matuszczak Y, Hardin BJ, Moylan JS, Smith JD, Ware J, Kennedy AR, Reid MB. Bowman-Birk inhibitor concentrate prevents atrophy, weakness, and oxidative stress in soleus muscle of hindlimb-unloaded mice. J Appl Physiol 102: 956-964, 2007.
4. Barreiro E, Coronell C, Lavina B, Ramirez-Sarmiento A, Orozco-Levi M, Gea J. Aging, sex differences, and oxidative stress in human respiratory and limb muscles. Free Radic Biol Med 41: 797-809, 2006.
5. Bejma J, Ji LL. Aging and acute exercise enhance free radical generation in rat skeletal muscle. J Appl Physiol 87: 465-470, 1999.
6. Bergamini CM, Gambetti S, Dondi A, Cervellati C. Oxygen, reactive oxygen species and tissue damage. Curr Pharm Des 10: 1611-1626, 2004.
7. Bonnefont-Rousselot D. Glucose and reactive oxygen species. Curr Opin Clin Nutr Metab Care 5: 561-568, 2002.
8. Brown M, Hasser EM. Complexity of age-related change in skeletal muscle. J Gerontol A Biol Sci Med Sci 51: B117-B123, 1996.
9. Cakatay U, Telci A, Kayali R, Tekeli F, Akcay T, Sivas A. Relation of aging with oxidative protein damage parameters in the rat skeletal muscle. Clin Biochem 36: 51-55, 2003.
10. Carmeli E, Coleman R, Reznick AZ. The biochemistry of aging muscle. Exp Gerontol 37: 477-489, 2002.
11. Ceconi C, Boraso A, Cargnoni A, Ferrari R. Oxidative stress in cardiovascular disease: myth or fact? Arch Biochem Biophys 420: 217-221, 2003.
12. Ceriello A, Motz E. Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler Thromb Vasc Biol 24: 816-823, 2004.
13. Chen CN, Brown-Borg HM, Rakoczy SG, Thompson LV. Muscle disuse: adaptation of antioxidant systems is age dependent. J Gerontol A Biol Sci Med Sci 63: 461-466, 2008.
14. Chen KD, Alway SE. A physiological level of clenbuterol does not prevent atrophy or loss of force in skeletal muscle of old rats. J Appl Physiol 89: 606-612, 2000.
15. Chen KD, Alway SE. Clenbuterol reduces soleus muscle fatigue during disuse in aged rats. Muscle Nerve 24: 211-222, 2001.
16. Droge W. Free radicals in the physiological control of cell function. Physiol Rev 82: 47-95, 2002.
17. Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 11: 81-128, 1991.
18. Ferrari R, Agnoletti L, Comini L, Gaia G, Bachetti T, Cargnoni A, Ceconi C, Curello S, Visioli O. Oxidative stress during myocardial ischaemia and heart failure. Eur Heart J 19, Suppl B: B2-B11, 1998.
19. Fulle S, Protasi F, Di Tano G, Pietrangelo T, Beltramin A, Boncompagni S, Vecchiet L, Fano G. The contribution of reactive oxygen species to sarcopenia and muscle ageing. Exp Gerontol 39: 17-24, 2004.
20. Gianni P, Jan KJ, Douglas MJ, Stuart PM, Tarnopolsky MA. Oxidative stress and the mitochondrial theory of aging in human skeletal muscle. Exp Gerontol 39: 1391-1400, 2004.
21. O2 max. J Gerontol A Biol Sci Med Sci 59: 1099-1110, 2004.
22. Hollander J, Bejma J, Ookawara T, Ohno H, Ji LL. Superoxide dismutase gene expression in skeletal muscle: fiber-specific effect of age. Mech Ageing Dev 116: 33-45, 2000.
23. Ikemoto M, Nikawa T, Kano M, Hirasaka K, Kitano T, Watanabe C, Tanaka R, Yamamoto T, Kamada M, Kishi K. Cysteine supplementation prevents unweighting-induced ubiquitination in association with redox regulation in rat skeletal muscle. Biol Chem 383: 715-721, 2002.
24. Ji LL. Antioxidant signaling in skeletal muscle: a brief review. Exp Gerontol 42: 582-593, 2007.
25. Ji LL, Dillon D, Wu E. Alteration of antioxidant enzymes with aging in rat skeletal muscle and liver. Am J Physiol Regul Integr Comp Physiol 258: R918-R923, 1990.
26. Ji LL, Leeuwenburgh C, Leichtweis S, Gore M, Fiebig R, Hollander J, Bejma J. Oxidative stress and aging. Role of exercise and its influences on antioxidant systems. Ann NY Acad Sci 854: 102-117, 1998.
27. Koesterer TJ, Dodd SL, Powers S. Increased antioxidant capacity does not attenuate muscle atrophy caused by unweighting. J Appl Physiol 93: 1959-1965, 2002.
28. Kondo H, Miura M, Itokawa Y. Oxidative stress in skeletal muscle atrophied by immobilization. Acta Physiol Scand 142: 527-528, 1991.
29. Kondo H, Miura M, Itokawa Y. Antioxidant enzyme systems in skeletal muscle atrophied by immobilization. Pflügers Arch 422: 404-406, 1993.
30. Kondo H, Miura M, Nakagaki I, Sasaki S, Itokawa Y. Trace element movement and oxidative stress in skeletal muscle atrophied by immobilization. Am J Physiol Endocrinol Metab 262: E583-E590, 1992.
31. Kondo H, Nakagaki I, Sasaki S, Hori S, Itokawa Y. Mechanism of oxidative stress in skeletal muscle atrophied by immobilization. Am J Physiol Endocrinol Metab 265: E839-E844, 1993.
32. Kondo H, Nishino K, Itokawa Y. Hydroxyl radical generation in skeletal muscle atrophied by immobilization. FEBS Lett 349: 169-172, 1994.
33. Lambertucci RH, Levada-Pires AC, Rossoni LV, Curi R, Pithon-Curi TC. Effects of aerobic exercise training on antioxidant enzyme activities and mRNA levels in soleus muscle from young and aged rats. Mech Ageing Dev 128: 267-275, 2007.
34. Lawler JM, Song W, Demaree SR. Hindlimb unloading increases oxidative stress and disrupts antioxidant capacity in skeletal muscle. Free Radic Biol Med 35: 9-16, 2003.
35. Leeuwenburgh C, Fiebig R, Chandwaney R, Ji LL. Aging and exercise training in skeletal muscle: responses of glutathione and antioxidant enzyme systems. Am J Physiol Regul Integr Comp Physiol 267: R439-R445, 1994.
36. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275, 1951.
37. Martindale JL, Holbrook NJ. Cellular response to oxidative stress: signaling for suicide and survival. J Cell Physiol 192: 1-15, 2002.
38. McArdle A, Pattwell D, Vasilaki A, Griffiths RD, Jackson MJ. Contractile activity-induced oxidative stress: cellular origin and adaptive responses. Am J Physiol Cell Physiol 280: C621-C627, 2001.
39. Millan-Crow LA, Cruthirds DL. Manganese superoxide dismutase in disease. Free Radic Res 34: 325-336, 2001.
40. 2 release from activated human leukocytes using a dihydroxyphenoxazine derivative. J Immunol Methods 202: 133-141, 1997.
41. Morey-Holton ER, Globus RK. Hindlimb unloading rodent model: technical aspects. J Appl Physiol 92: 1367-1377, 2002.
42. Murrant CL, Reid MB. Detection of reactive oxygen and reactive nitrogen species in skeletal muscle. Microsc Res Tech 55: 236-248, 2001.
43. Ohira Y, Yoshinaga T, Nomura T, Kawano F, Ishihara A, Nonaka I, Roy RR, Edgerton VR. Gravitational unloading effects on muscle fiber size, phenotype and myonuclear number. Adv Space Res 30: 777-781, 2002.
44. Pansarasa O, Bertorelli L, Vecchiet J, Felzani G, Marzatico F. Age-dependent changes of antioxidant activities and markers of free radical damage in human skeletal muscle. Free Radic Biol Med 27: 617-622, 1999.
45. Pansarasa O, Castagna L, Colombi B, Vecchiet J, Felzani G, Marzatico F. Age and sex differences in human skeletal muscle: role of reactive oxygen species. Free Radic Res 33: 287-293, 2000.
46. Pistilli EE, Siu PM, Alway SE. Interleukin-15 responses to aging and unloading-induced skeletal muscle atrophy. Am J Physiol Cell Physiol 292: C1298-C1304, 2007.
47. Poli G, Leonarduzzi G, Biasi F, Chiarpotto E. Oxidative stress and cell signalling. Curr Med Chem 11: 1163-1182, 2004.
48. Powers SK, Kavazis AN, DeRuisseau KC. Mechanisms of disuse muscle atrophy: role of oxidative stress. Am J Physiol Regul Integr Comp Physiol 288: R337-R344, 2005.
49. Powers SK, Kavazis AN, McClung JM. Oxidative stress and disuse muscle atrophy. J Appl Physiol 102: 2389-2397, 2007.
50. Radak Z, Takahashi R, Kumiyama A, Nakamoto H, Ohno H, Ookawara T, Goto S. Effect of aging and late onset dietary restriction on antioxidant enzymes and proteasome activities, and protein carbonylation of rat skeletal muscle and tendon. Exp Gerontol 37: 1423-1430, 2002.
51. Reid MB. Redox modulation of skeletal muscle contraction: what we know and what we don't. J Appl Physiol 90: 724-731, 2001.
52. Reid MB, 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.
53. Rothermel B, Vega RB, Yang J, Wu H, Bassel-Duby R, Williams RS. A protein encoded within the Down syndrome critical region is enriched in striated muscles and inhibits calcineurin signaling. J Biol Chem 275: 8719-8725, 2000.
54. Servais S, Letexier D, Favier R, Duchamp C, Desplanches D. Prevention of unloading-induced atrophy by vitamin E supplementation: links between oxidative stress and soleus muscle proteolysis? Free Radic Biol Med 42: 627-635, 2007.
55. Simon HU, Haj-Yehia A, Levi-Schaffer F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5: 415-418, 2000.
56. Siu PM, Alway SE. Id2 and p53 participate in apoptosis during unloading-induced muscle atrophy. Am J Physiol Cell Physiol 288: C1058-C1073, 2005.
57. Siu PM, Alway SE. Mitochondria-associated apoptotic signalling in denervated rat skeletal muscle. J Physiol 565: 309-323, 2005.
58. Siu PM, Alway SE. Subcellular responses of p53 and Id2 in fast and slow skeletal muscle in response to stretch-induced overload. J Appl Physiol 99: 1897-1904, 2005.
59. Siu PM, Bryner RW, Martyn JK, Alway SE. Apoptotic adaptations from exercise training in skeletal and cardiac muscles. FASEB J 18: 1150-1152, 2004.
60. Siu PM, Pistilli EE, Alway SE. Apoptotic responses to hindlimb suspension in gastrocnemius muscles from young adult and aged rats. Am J Physiol Regul Integr Comp Physiol 289: R1015-R1026, 2005.
61. Siu PM, Pistilli EE, Butler DC, Alway SE. Aging influences cellular and molecular responses of apoptosis to skeletal muscle unloading. Am J Physiol Cell Physiol 288: C338-C349, 2005.
62. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC. Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76-85, 1985.
63. Stevenson EJ, Giresi PG, Koncarevic A, Kandarian SC. Global analysis of gene expression patterns during disuse atrophy in rat skeletal muscle. J Physiol 551: 33-48, 2003.
64. Storz P. Reactive oxygen species in tumor progression. Front Biosci 10: 1881-1896, 2005.
65. Turturro A, Witt WW, Lewis S, Hass BS, Lipman RD, Hart RW. Growth curves and survival characteristics of the animals used in the Biomarkers of Aging Program. J Gerontol A Biol Sci Med Sci 54: B492-B501, 1999.
66. Zhou M, Diwu Z, Panchuk-Voloshina N, Haugland RP. A stable nonfluorescent derivative of resorufin for the fluorometric determination of trace hydrogen peroxide: applications in detecting the activity of phagocyte NADPH oxidase and other oxidases. Anal Biochem 253: 162-168, 1997.