Elevated mitochondrial oxidative stress impairs metabolic adaptations to exercise in skeletal muscle

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Crane, Justin D ^a   Abadi, Arkan ^a   Hettinga, Bart P ^a   Ogborn, Daniel I ^a   Macneil, Lauren G ^a   Steinberg, Gregory R ^a   Tarnopolsky, Mark A ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; ADENINE NUCLEOTIDE TRANSLOCASE 1; CYTOCHROME C OXIDASE; MITOCHONDRIAL DNA; MITOCHONDRIAL ENZYME; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL TRANSCRIPTION FACTOR A; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 3;

ANIMAL EXPERIMENT; ARTICLE; CELL FUNCTION; ELECTRON TRANSPORT; ENZYME ACTIVITY; EXERCISE; FEMALE; GENOTYPE; MALE; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHYSICAL CAPACITY; PROTEIN ASSEMBLY; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RUNNING; SKELETAL MUSCLE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; DNA, MITOCHONDRIAL; DNA-BINDING PROTEINS; ELECTRON TRANSPORT; HIGH MOBILITY GROUP PROTEINS; MICE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MUSCLE, SKELETAL; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHYSICAL CONDITIONING, ANIMAL; PROTEIN FOLDING; SUPEROXIDE DISMUTASE; TRANSCRIPTION, GENETIC;

EID: 84891937761     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081879     Document Type: Article

References (51)

1. Barja G (1999) Mitochondrial oxygen radical generation and leak: sites of production in states 4 and 3, organ specificity, and relation to aging and longevity. J Bioenerg Biomembr 31:347-366. doi:10.1023/A: 1005427919188. PubMed: 10665525. (Pubitemid 30058570)
2. Muller FL, Liu Y, Van Remmen H (2004) Complex III releases superoxide to both sides of the inner mitochondrial membrane. J Biol Chem 279:49064-49073. doi:10.1074/jbc. M407715200. PubMed: 15317809. (Pubitemid 39625788)
3. Quinlan CL, Orr AL, Perevoshchikova IV, Treberg JR, Ackrell BA et al. (2012) Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions. J Biol Chem, 287:27255-64. PubMed: 22689576.
4. Houstis N, Rosen ED, Lander ES (2006) Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440:944-948. doi:10.1038/nature04634. PubMed: 16612386.
5. Lin MT, Beal MF (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443:787-795. doi:10.1038/nature05292. PubMed: 17051205. (Pubitemid 44622683)
6. Wanagat J, Cao Z, Pathare P, Aiken JM (2001) Mitochondrial DNA deletion mutations colocalize with segmental electron transport system abnormalities, muscle fiber atrophy, fiber splitting, and oxidative damage in sarcopenia. FASEB J 15:322-332. doi:10.1096/fj. 00-0320com. PubMed: 11156948. (Pubitemid 32141424)
7. Gomez-Cabrera MC, Domenech E, Viña J (2008) Moderate exercise is an antioxidant: upregulation of antioxidant genes by training. Free Radic Biol Med 44:126-131. doi:10.1016/j.freeradbiomed.2007.02.001. PubMed: 18191748.
8. Powers SK, Jackson MJ (2008) Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 88:1243-1276. doi:10.1152/physrev. 00031.2007. PubMed: 18923182.
9. St-Pierre J, Buckingham JA, Roebuck SJ, Brand MD (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem 277:44784-44790. doi:10.1074/jbc. M207217200. PubMed: 12237311. (Pubitemid 36159072)
10. Barreiro E, Rabinovich R, Marin-Corral J, Barberà JA, Gea J et al. (2009) Chronic endurance exercise induces quadriceps nitrosative stress in patients with severe COPD. Thorax 64:13-19. PubMed: 18835959.
11. Puente-Maestu L, Tejedor A, Lázaro A, de Miguel J, Alvarez-Sala L et al. (2012) Site of mitochondrial reactive oxygen species production in skeletal muscle of chronic obstructive pulmonary disease and its relationship with exercise oxidative stress. Am J Respir Cell Mol Biol 47:358-362. doi:10.1165/rcmb.2011-0382OC. PubMed: 22493009.
12. Gomez-Cabrera MC, Domenech E, Romagnoli M, Arduini A, Borras C et al. (2008) Oral administration of vitamin C decreases muscle mitochondrial biogenesis and hampers training-induced adaptations in endurance performance. Am J Clin Nutr 87:142-149. PubMed: 18175748.
13. Ristow M, Zarse K, Oberbach A, Klöting N, Birringer M et al. (2009) Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci U S A 106:8665-8670. doi:10.1073/pnas. 0903485106. PubMed: 19433800.
14. Higashida K, Kim SH, Higuchi M, Holloszy JO, Han DH (2011) Normal adaptations to exercise despite protection against oxidative stress. Am J Physiol Endocrinol Metab 301:E779-E784. doi:10.1152/ajpendo. 00655.2010. PubMed: 21750271.
15. Gutteridge JM, Halliwell B (2010) Antioxidants: Molecules, medicines, and myths. Biochem Biophys Res Commun 393:561-564. doi:10.1016/j.bbrc.2010.02.071. PubMed: 20171167.
16. Miller ER, Pastor-Barriuso R, Dalal D, Riemersma RA, Appel LJ, Guallar E (2005) Meta-analysis: high-dosage vitamin E supplementation may increase all-cause mortality. Ann Intern Med 142:37-46. doi:10.7326/0003-4819-142-1- 200501040-00110. PubMed: 15537682.
17. Van Remmen H, Ikeno Y, Hamilton M, Pahlavani M, Wolf N et al. (2003) Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging. Physiol Genomics 16:29-37. doi:10.1152/physiolgenomics. 00122.2003. PubMed: 14679299. (Pubitemid 38420018)
18. Safdar A, Hamadeh MJ, Kaczor JJ, Raha S, Debeer J et al. (2010) Aberrant mitochondrial homeostasis in the skeletal muscle of sedentary older adults. PLOS ONE 5:e10778. doi:10.1371/journal.pone.0010778. PubMed: 20520725.
19. Boyle KE, Newsom SA, Janssen RC, Lappas M, Friedman JE (2013) Skeletal muscle MnSOD, mitochondrial complex II, and SIRT3 enzyme activities are decreased in maternal obesity during human pregnancy and gestational diabetes mellitus. J Clin Endocrinol Metab, 98:E1601-9. PubMed: 23956348.
20. Larsen S, Stride N, Hey-Mogensen M, Hansen CN, Andersen JL et al. (2011) Increased mitochondrial substrate sensitivity in skeletal muscle of patients with type 2 diabetes. Diabetologia 54:1427-1436. doi: 10.1007/s00125-011-2098-4. PubMed: 21424396.
21. Lebovitz RM, Zhang H, Vogel H, Cartwright J, Dionne L et al. (1996) Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc Natl Acad Sci U S A 93:9782-9787. doi:10.1073/pnas.93.18.9782. PubMed: 8790408. (Pubitemid 26296686)
22. Li Y, Huang TT, Carlson EJ, Melov S, Ursell PC et al. (1995) Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet 11:376-381. doi: 10.1038/ng1295-376. PubMed: 7493016.
23. Ho YS, Gargano M, Cao J, Bronson RT, Heimler I et al. (1998) Reduced fertility in female mice lacking copper-zinc superoxide dismutase. J Biol Chem 273:7765-7769. doi:10.1074/jbc.273.13.7765. PubMed: 9516486. (Pubitemid 28152809)
24. Ran Q, Liang H, Ikeno Y, Qi W, Prolla TA et al. (2007) Reduction in glutathione peroxidase 4 increases life span through increased sensitivity to apoptosis. J Gerontol A Biol Sci Med Sci 62:932-942. doi: 10.1093/gerona/62.9. 932. PubMed: 17895430. (Pubitemid 47531208)
25. Zhang Y, Ikeno Y, Qi W, Chaudhuri A, Li Y et al. (2009) Mice deficient in both Mn superoxide dismutase and glutathione peroxidase-1 have increased oxidative damage and a greater incidence of pathology but no reduction in longevity. J Gerontol A Biol Sci Med Sci 64:1212-1220. PubMed: 19776219.
26. Parise G, Brose AN, Tarnopolsky MA (2005) Resistance exercise training decreases oxidative damage to DNA and increases cytochrome oxidase activity in older adults. Exp Gerontol 40:173-180. doi:10.1016/j.exger.2004.09.002. PubMed: 15763394. (Pubitemid 40343008)
27. McKenzie S, Phillips SM, Carter SL, Lowther S, Gibala MJ et al. (2000) Endurance exercise training attenuates leucine oxidation and BCOAD activation during exercise in humans. Am J Physiol Endocrinol Metab 278:E580-E587. PubMed: 10751189. (Pubitemid 30215166)
28. Walker RB, Everette JD (2009) Comparative reaction rates of various antioxidants with ABTS radical cation. J Agric Food Chem 57:1156-1161. doi:10.1021/jf8026765. PubMed: 19199590.
29. Ogborn DI, Smith KJ, Crane JD, Safdar A, Hettinga BP et al. (2012) Effects of creatine and exercise on skeletal muscle of FRG1-transgenic mice. Can J Neurol Sci 39:225-231. PubMed: 22343158.
30. Quinlivan EP, Gregory JF (2008) DNA digestion to deoxyribonucleoside: a simplified one-step procedure. Anal Biochem 373:383-385. doi:10.1016/j.ab.2007. 09.031. PubMed: 18028864.
31. Boushel R, Gnaiger E, Schjerling P, Skovbro M, Kraunsøe R et al. (2007) Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle. Diabetologia 50:790-796. doi:10.1007/s00125-007-0594-3. PubMed: 17334651. (Pubitemid 46355830)
32. Schägger H, von Jagow G (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 199:223-231. doi:10.1016/0003-2697 (91) 90094-A. PubMed: 1812789.
33. Lee HC, Wei YH (2005) Mitochondrial biogenesis and mitochondrial DNA maintenance of mammalian cells under oxidative stress. Int J Biochem Cell Biol 37:822-834. doi:10.1016/j.biocel.2004.09.010. PubMed: 15694841.
34. Boss O, Samec S, Paoloni-Giacobino A, Rossier C, Dulloo A et al. (1997) Uncoupling protein-3: a new member of the mitochondrial carrier family with tissue-specific expression. FEBS Lett 408:39-42. doi: 10.1016/S0014-5793 (97) 00384-0. PubMed: 9180264. (Pubitemid 27216458)
35. Brand MD, Pakay JL, Ocloo A, Kokoszka J, Wallace DC et al. (2005) The basal proton conductance of mitochondria depends on adenine nucleotide translocase content. Biochem J 392:353-362. doi:10.1042/BJ20050890. PubMed: 16076285. (Pubitemid 41796524)
36. Ji LL (2008) Modulation of skeletal muscle antioxidant defense by exercise: Role of redox signaling. Free Radic Biol Med 44:142-152. doi:10.1016/j.freeradbiomed.2007.02.031. PubMed: 18191750.
37. Radak Z, Chung HY, Goto S (2008) Systemic adaptation to oxidative challenge induced by regular exercise. Free Radic Biol Med 44:153-159. doi:10.1016/j.freeradbiomed.2007.01.029. PubMed: 18191751.
38. Van Remmen H, Salvador C, Yang H, Huang TT, Epstein CJ et al. (1999) Characterization of the antioxidant status of the heterozygous manganese superoxide dismutase knockout mouse. Arch Biochem Biophys 363:91-97. doi:10.1006/abbi.1998.1060. PubMed: 10049502. (Pubitemid 29394334)
39. Williams MD, Van Remmen H, Conrad CC, Huang TT et al. (1998) Increased oxidative damage is correlated to altered mitochondrial function in heterozygous manganese superoxide dismutase knockout mice. J Biol Chem 273:28510-28515. doi:10.1074/jbc.273.43.28510. PubMed: 9774481. (Pubitemid 28496158)
40. Bota DA, Van Remmen H, Davies KJ (2002) Modulation of Lon protease activity and aconitase turnover during aging and oxidative stress. FEBS Lett 532:103-106. doi:10.1016/S0014-5793 (02) 03638-4. PubMed: 12459471. (Pubitemid 35375875)
41. Kwong LK, Sohal RS (2000) Age-related changes in activities of mitochondrial electron transport complexes in various tissues of the mouse. Arch Biochem Biophys 373:16-22. doi:10.1006/abbi. 1999.1495. PubMed: 10620319. (Pubitemid 30046485)
42. Parise G, Phillips SM, Kaczor JJ, Tarnopolsky MA (2005) Antioxidant enzyme activity is up-regulated after unilateral resistance exercise training in older adults. Free Radic Biol Med 39:289-295. doi:10.1016/j.freeradbiomed.2005. 03.024. PubMed: 15964520. (Pubitemid 40814554)
43. Kang D, Hamasaki N (2005) Mitochondrial transcription factor A in the maintenance of mitochondrial DNA: overview of its multiple roles. Ann N Y Acad Sci 1042:101-108. doi:10.1196/annals.1338.010. PubMed: 15965051. (Pubitemid 40967627)
44. Yoshida Y, Izumi H, Ise T, Uramoto H, Torigoe T et al. (2002) Human mitochondrial transcription factor A binds preferentially to oxidatively damaged. DNA - Biochem Biophys Res Commun 295:945-951. doi: 10.1016/S0006-291X (02) 00757-X.
45. Canugovi C, Maynard S, Bayne AC, Sykora P, Tian J et al. (2010) The mitochondrial transcription factor A functions in mitochondrial base excision repair. DNA Repair (Amst) 9:1080-1089. doi:10.1016/j.dnarep. 2010.07.009. PubMed: 20739229.
46. Coskun PE, Beal MF, Wallace DC (2004) Alzheimer's brains harbor somatic mtDNA control-region mutations that suppress mitochondrial transcription and replication. Proc Natl Acad Sci U S A 101:10726-10731. doi:10.1073/pnas. 0403649101. PubMed: 15247418. (Pubitemid 38955810)
47. Puente-Maestu L, Lázaro A, Tejedor A, Camaño S, Fuentes M et al. (2011) Effects of exercise on mitochondrial DNA content in skeletal muscle of patients with COPD. Thorax 66:121-127. doi:10.1136/thoraxjnl-2011-201054c. 134. PubMed: 21097816.
48. Distelmaier F, Koopman W J H, Van Den Heuvel LP, Rodenburg RJ, Mayatepek E et al. (2009) Mitochondrial complex I deficiency: from organelle dysfunction to clinical disease. Brain 132:833-842. PubMed: 19336460.
49. Fukui H, Moraes CT (2008) The mitochondrial impairment, oxidative stress and neurodegeneration connection: reality or just an attractive hypothesis? Trends Neurosci 31:251-256. doi:10.1016/j.tins. 2008.02.008. PubMed: 18403030.
50. Lee S, Van Remmen H, Csete M (2009) Sod2 overexpression preserves myoblast mitochondrial mass and function, but not muscle mass with aging. Aging Cell 8:296-310. doi:10.1111/j. 1474-9726.2009.00477.x. PubMed: 19627269.
51. Pérez VI, Van Remmen H, Bokov A, Epstein CJ, Vijg J et al. (2009) The overexpression of major antioxidant enzymes does not extend the lifespan of mice. Aging Cell 8:73-75. doi:10.1111/j. 1474-9726.2008.00449.x. PubMed: 19077044.