Exercise protects against doxorubicin-induced oxidative stress and proteolysis in skeletal muscle

Journal of Applied Physiology

Volumn 110, Issue 4, 2011, Pages 935-942

  Smuder, Ashley J ^a   Kavazis, Andreas N ^a,b   Min, Kisuk ^a   Powers, Scott K ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b MISSISSIPPI STATE UNIVERSITY   (United States)

Author keywords

Antioxidants; Myocytes; Reactive oxygen species

Indexed keywords

CASPASE 3; DOXORUBICIN; HEAT SHOCK PROTEIN 72; REACTIVE OXYGEN METABOLITE;

ANALYSIS OF VARIANCE; ANIMAL; ANIMAL EXPERIMENT; ARTICLE; DRUG EFFECT; MALE; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY; RAT; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; CASPASE 3; DOXORUBICIN; HSP72 HEAT-SHOCK PROTEINS; MALE; MUSCLE, SKELETAL; OXIDATIVE STRESS; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES;

EID: 79954602246     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00677.2010     Document Type: Article

References (49)

1. Ascensao A, Magalhaes J, Soares JM, Ferreira R, Neuparth MJ, Marques F, Oliveira PJ, Duarte JA. Moderate endurance training prevents doxorubicin-induced in vivo mitochondriopathy and reduces the development of cardiac apoptosis. Am J Physiol Heart Circ Physiol 289: H722-H731, 2005. (Pubitemid 41129389)
2. Cadenas E, Davies KJ. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29: 222-230, 2000.
3. Carter SK. Adriamycin-a review. J Natl Cancer Inst 55: 1265-1274, 1975.
4. Childs AC, Phaneuf SL, Dirks AJ, Phillips T, Leeuwenburgh C. Doxorubicin treatment in vivo causes cytochrome c release and cardiomyocyte apoptosis, as well as increased mitochondrial efficiency, superoxide dismutase activity, and Bcl-2:Bax ratio. Cancer Res 62: 4592-4598, 2002.
5. Criswell D, Powers S, Dodd S, Lawler J, Edwards W, Renshler K, Grinton S. High intensity training-induced changes in skeletal muscle antioxidant enzyme activity. Med Sci Sports Exerc 25: 1135-1140, 1993. (Pubitemid 23298826)
6. Doroshow JH, Tallent C, Schechter JE. Ultrastructural features of adriamycin-induced skeletal and cardiac muscle toxicity. Am J Pathol 118: 288-297, 1985. (Pubitemid 15127685)
7. Du J, Wang X, Miereles C, Bailey JL, Debigare R, Zheng B, Price SR, Mitch WE. Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J Clin Invest 113: 115-123, 2004. (Pubitemid 38541638)
8. Enns D, Karmazyn M, Mair J, Lercher A, Kountchev J, Belcastro A. Calpain, calpastatin activities and ratios during myocardial ischemiareperfusion. Mol Cell Biochem 241: 29-35, 2002. (Pubitemid 35385831)
9. Ertunc M, Sara Y, Korkusuz P, Onur R. Differential contractile impairment of fast- and slow-twitch skeletal muscles in a rat model of doxorubicin-induced congestive heart failure. Pharmacology 84: 240-248, 2009.
10. Febbraio MA, Steensberg A, Walsh R, Koukoulas I, van Hall G, Saltin B, Pedersen BK. Reduced glycogen availability is associated with an elevation in HSP72 in contracting human skeletal muscle. J Physiol 538: 911-917, 2002. (Pubitemid 35190081)
11. Ferrans VJ. Overview of cardiac pathology in relation to anthracycline cardiotoxicity. Cancer Treat Rep 62: 955-961, 1978. (Pubitemid 8377895)
12. Gilliam LA, Ferreira LF, Bruton JD, Moylan JS, Westerblad H, St Clair DK, Reid MB. Doxorubicin acts through tumor necrosis factor receptor subtype 1 to cause dysfunction of murine skeletal muscle. J Appl Physiol 107: 1935-1942, 2009.
13. Goll DE, Thompson VF, Li H, Wei W, Cong J. The calpain system. Physiol Rev 83: 731-801, 2003. (Pubitemid 36828925)
14. Jackson MJ. Redox regulation of skeletal muscle. IUBMB Life 60: 497-501, 2008.
15. Jang YM, Kendaiah S, Drew B, Phillips T, Selman C, Julian D, Leeuwenburgh C. Doxorubicin treatment in vivo activates caspase-12 mediated cardiac apoptosis in both male and female rats. FEBS Lett 577: 483-490, 2004. (Pubitemid 39539206)
16. Kang YJ, Chen Y, Yu A, Voss-McCowan M, Epstein PN. Overexpression of metallothionein in the heart of transgenic mice suppresses doxorubicin cardiotoxicity. J Clin Invest 100: 1501-1506, 1997. (Pubitemid 27425776)
17. Kourie JI. Interaction of reactive oxygen species with ion transport mechanisms. Am J Physiol Cell Physiol 275: C1-C24, 1998. (Pubitemid 28381298)
18. Kowaltowski AJ, Vercesi AE. Mitochondrial damage induced by conditions of oxidative stress. Free Radic Biol Med 26: 463-471, 1999. (Pubitemid 29013479)
19. Lawler JM, Powers SK, Hammeren J, Martin AD. Oxygen cost of treadmill running in 24-mo-old Fischer-344 rats. Med Sci Sports Exerc 25: 1259-1264, 1993. (Pubitemid 23326479)
20. Leeuwenburgh C. Role of apoptosis in sarcopenia. J Gerontol A Biol Sci Med Sci 58: 999-1001, 2003. (Pubitemid 37467296)
21. Leeuwenburgh C, Hollander J, Leichtweis S, Griffiths M, Gore M, Ji LL. Adaptations of glutathione antioxidant system to endurance training are tissue and muscle fiber specific. Am J Physiol Regul Integr Comp Physiol 272: R363-R369, 1997.
22. Li W, Moylan JS, Chambers MA, Smith J, Reid MB. Interleukin-1 stimulates catabolism in C2C12 myotubes. Am J Physiol Cell Physiol 297: C706-C714, 2009.
23. Lim CC, Zuppinger C, Guo X, Kuster GM, Helmes M, Eppenberger HM, Suter TM, Liao R, Sawyer DB. Anthracyclines induce calpaindependent titin proteolysis and necrosis in cardiomyocytes. J Biol Chem 279: 8290-8299, 2004. (Pubitemid 38294721)
24. McArdle A, Jackson MJ. Exercise, oxidative stress and ageing. J Anat 197: 539-541, 2000. (Pubitemid 32051533)
25. 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.
26. McClung JM, Whidden MA, Kavazis AN, Falk DJ, Deruisseau KC, Powers SK. Redox regulation of diaphragm proteolysis during mechanical ventilation. Am J Physiol Regul Integr Comp Physiol 294: R1608-R1617, 2008.
27. McLoon LK, Falkenberg JH, Dykstra D, Iaizzo PA. Doxorubicin chemomyectomy as a treatment for cervical dystonia: Histological assessment after direct injection into the sternocleidomastoid muscle. Muscle Nerve 21: 1457-1464, 1998. (Pubitemid 28453134)
28. Mukhopadhyay P, Rajesh M, Yoshihiro K, Hasko G, Pacher P. Simple quantitative detection of mitochondrial superoxide production in live cells. Biochem Biophys Res Commun 358: 203-208, 2007. (Pubitemid 46719103)
29. Naito H, Powers SK, Demirel HA, Aoki J. Exercise training increases heat shock protein in skeletal muscles of old rats. Med Sci Sports Exerc 33: 729-734, 2001. (Pubitemid 32336632)
30. Noble EG, Milne KJ, Melling CW. Heat shock proteins and exercise: A primer. Appl Physiol Nutr Metab 33: 1050-1065, 2008.
31. Poso AR, Eklund-Uusitalo S, Hyyppa S, Pirila E. Induction of heat shock protein 72 mRNA in skeletal muscle by exercise and training. Equine Vet J Suppl Sep: 214-218, 2002.
32. Powers SK, Criswell D, Lawler J, Ji LL, Martin D, Herb RA, Dudley G. Influence of exercise and fiber type on antioxidant enzyme activity in rat skeletal muscle. Am J Physiol Regul Integr Comp Physiol 266: R375-R380, 1994.
33. Powers SK, Criswell D, Lawler J, Martin D, Ji LL, Herb RA, Dudley G. Regional training-induced alterations in diaphragmatic oxidative and antioxidant enzymes. Respir Physiol 95: 227-237, 1994. (Pubitemid 24066433)
34. Powers SK, Jackson MJ. Exercise-induced oxidative stress: Cellular mechanisms and impact on muscle force production. Physiol Rev 88: 1243-1276, 2008.
35. 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. (Pubitemid 40129594)
36. Powers SK, Kavazis AN, McClung JM. Oxidative stress and disuse muscle atrophy. J Appl Physiol 102: 2389-2397, 2007. (Pubitemid 47080773)
37. Powers SK, MLA, Demirel HA. Exercise, heat shock proteins, and myocardial protection from I-R injury. Med Sci Sports Exerc 33: 386-392, 2001. (Pubitemid 32209657)
38. Primeau AJ, Adhihetty PJ, Hood DA. Apoptosis in heart and skeletal muscle. Can J Appl Physiol 27: 349-395, 2002.
39. Singal PK, Li T, Kumar D, Danelisen I, Iliskovic N. Adriamycininduced heart failure: Mechanism and modulation. Mol Cell Biochem 207: 77-86, 2000.
40. Smuder AJ, Kavazis AN, Hudson MB, Nelson WB, Powers SK. Oxidation enhances myofibrillar protein degradation via calpain and caspase-3. Free Radic Biol Med 49: 1152-1160.
41. Stone P, Hardy J, Broadley K, Tookman AJ, Kurowska A, A'Hern R. Fatigue in advanced cancer: A prospective controlled cross-sectional study. Br J Cancer 79: 1479-1486, 1999. (Pubitemid 29116808)
42. Takemura G, Fujiwara H. Doxorubicin-induced cardiomyopathy from the cardiotoxic mechanisms to management. Prog Cardiovasc Dis 49: 330-352, 2007. (Pubitemid 46295436)
43. van der Westhuyzen DR, Matsumoto K, Etlinger JD. Easily releasable myofilaments from skeletal and cardiac muscles maintained in vitro. Role in myofibrillar assembly and turnover. J Biol Chem 256: 11791-11797, 1981.
44. van Norren K, van Helvoort A, Argiles JM, van Tuijl S, Arts K, Gorselink M, Laviano A, Kegler D, Haagsman HP, van der Beek EM. Direct effects of doxorubicin on skeletal muscle contribute to fatigue. Br J Cancer 100: 311-314, 2009.
45. Wallace KB. Adriamycin-induced interference with cardiac mitochondrial calcium homeostasis. Cardiovasc Toxicol 7: 101-107, 2007. (Pubitemid 47339855)
46. Yamada P, Amorim F, Moseley P, Schneider S. Heat shock protein 72 response to exercise in humans. Sports Med 38: 715-733, 2008.
47. Yamamoto Y, Hoshino Y, Ito T, Nariai T, Mohri T, Obana M, Hayata N, Uozumi Y, Maeda M, Fujio Y, Azuma J. Atrogin-1 ubiquitin ligase is upregulated by doxorubicin via p38-MAP kinase in cardiac myocytes. Cardiovasc Res 79: 89-96, 2008. (Pubitemid 351881941)
48. Yen HC, Oberley TD, Vichitbandha S, Ho YS, St. Clair DK. The protective role of manganese superoxide dismutase against adriamycininduced acute cardiac toxicity in transgenic mice. J Clin Invest 98: 1253-1260, 1996. (Pubitemid 26299939)
49. Zergeroglu MA, McKenzie MJ, Shanely RA, Van Gammeren D, DeRuisseau KC, Powers SK. Mechanical ventilation-induced oxidative stress in the diaphragm. J Appl Physiol 95: 1116-1124, 2003. (Pubitemid 37034008)