Swimming Training Induces Liver Mitochondrial Adaptations to Oxidative Stress in Rats Submitted to Repeated Exhaustive Swimming Bouts

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Lima, Frederico D ^a   Stamm, Daniel N ^a   Della Pace, Iuri D ^a   Dobrachinski, Fernando ^a   de Carvalho, Nélson R ^a   Royes, Luiz Fernando F ^a   Soares, Félix A ^a   Rocha, João B ^a   González Gallego, Javier ^b   Bresciani, Guilherme ^a  

^a FEDERAL UNIVERSITY OF SANTA MARIA   (Brazil)

^b UNIVERSITY OF LEÓN   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE; MANGANESE SUPEROXIDE DISMUTASE; REACTIVE OXYGEN METABOLITE; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

AEROBIC EXERCISE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENZYME ACTIVITY; LIPID PEROXIDATION; LIVER MITOCHONDRION; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OXIDATIVE STRESS; PHYSICAL ACTIVITY; PHYSICAL STRESS; RAT;

EID: 84925746661     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055668     Document Type: Article

References (71)

1. Mastorakos G, Pavlatou M, (2005) Exercise as a stress model and the interplay between the hypothalamus-pituitary-adrenal and the hypothalamus-pituitary-thyroid axes. Horm Metab Res 37: 577-584.
2. Hoene M, Franken H, Fritsche L, Lehmann R, Pohl AK, et al. (2010) Activation of the mitogen-activated protein kinase (MAPK) signalling pathway in the liver of mice is related to plasma glucose levels after acute exercise. Diabetologia 53: 1131-1141.
3. Malaguti M, Angeloni C, Garatachea N, Baldini M, Leoncini E, et al. (2009) Sulforaphane treatment protects skeletal muscle against damage induced by exhaustive exercise in rats. J Appl Physiol 107: 1028-1036.
4. Gobatto CA, de Mello MA, Sibuya CY, de AzevedoJR, dos Santos LA, et al. (2001) Maximal lactate steady state in rats submitted to swimming exercise. Comp Biochem. Physiol A Mol Integr Physiol 130: 21-27.
5. Davies KJ, Quintanilha AT, Brooks GA, Packer L, (1982) Free radicals and tissue damage produced by exercise. Biochem Biophys Res Commun 107: 1198-1205.
6. Gómez-Cabrera MC, Viña J, Ji LL, (2009) Interplay of oxidants and antioxidants during exercise: implications for muscle health. Phys Sportsmed 37: 116-123.
7. Alessio HM, Hagerman AE, Fulkerson BK, Ambrose J, Rice RE, et al. (2000) Generation of reactive oxygen species after exhaustive aerobic and isometric exercise. Med Sci Sports Exerc 32: 1576-1581.
8. Fogarty MC, Hughes CM, Burke G, Brown JC, Trinick TR, et al. (2011) Exercise-induced lipid peroxidation: Implications for deoxyribonucleic acid damage and systemic free radical generation. Environ Mol Mutagen 52: 35-42.
9. Sies H (1985) Oxidative stress: introductory remarks. In Sies H, editor. Oxidative Stress. Academic Press: London, 1-8.
10. Cakir B, Kasimay O, Ersoy Y, Ercan F, Yegen BC, (2010) Stress-idnuced multiple organ damage in rats is ameliorated by the antioxidant and anxiolitic effects of regular exercise. Cell Biochem Funct 28: 469-479.
11. Veneroso C, Tuñon MJ, Gonzalez-Gallego J, Collado PS, (2009) Melatonin reduces cardiac inflammatory injury induced by acute exercise. J. Pin. Res. 47: 184-191.
12. Hoene M, Weigert C, (2010) The stress response of the liver to physical exercise. Exerc Immunol Rev 16: 163-183.
13. Gul M, Laaksonen DE, Atalay M, Vider L, Hänninen O, (2002) Effects of endurance training on tissue glutathione homeostasis and lipid peroxidation in streptozotocin-induced diabetic rats. Scand J Med Sci Sports 12: 163-170.
14. Huang CC, Tsai SC, Lin WT, (2008) Potential ergogenic effects of L-arginine against oxidative and inflammatory stress induced by acute exercise in aging rats. Exp Gerontol 43: 571-577.
15. Villa JG, Almar MM, Collado PS, Llamazares E, Gonzalez-Gallego J, (1993) Impairment of bile secretion induced by exhaustive exercise in the rat. Protective effects of S-adenosyl-L-methionine. Int J Sports Med 14: 179-184.
16. Korivi M, Hou CW, Huang CY, Lee SD, Hsu MF, et al. (2012) Ginsenoside-Rg1 Protects the Liver against Exhaustive Exercise-Induced Oxidative Stress in Rats. Evid Based Complement Alternat Med doi:10.1155/2012/932165; 2012.
17. Liu J, Yeo HC, Overvik-Douki E, Hagen T, Doniger SJ, et al. (2000) Chronically and acutely exercised rats: biomarkers of oxidative stress and endogenous antioxidants. J Appl Physiol 89: 21-28.
18. Leeuwenburgh C, Ji LL, (1995) Glutathione depletion in rested and exercised mice: biochemical consequence and adaptation. Arch Biochem Biophys 316: 941-949.
19. Lew H, Pyke S, Quintanilha A, (1985) Changes in the glutathione status of plasma, liver and muscle following exhaustive exercise in rats. FEBS Lett 185: 262-266.
20. Boveris A, Chance B, (1973) The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J 134: 707-716.
21. 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.
22. Rasmussen UF, Krustrup P, Bangsbo J, Rasmussen HN, (2001) The effect of high intensity exhaustive exercise studied in isolated mitochondria from human skeletal muscle. Pflugers Arch 443: 180-187.
23. Radak Z, Chung HY, Naito H, Takahashi R, Jung KJ, et al. (2004) Age-associated increase in oxidative stress and nuclear factor kappaB activation are attenuated in rat liver by regular exercise. FASEB J 18: 749-750.
24. Willis WT, Jackman MR, (1994) Mitochondrial function during heavy exercise. Med Sci Sports Exerc 26: 1347-1353.
25. Powers SK, Duarte J, Kavazis AN, (2010) Talbert, E.E. Reactive oxygen species are signalling molecules for muscle adaptation. Exp Physiol 95: 1-9.
26. Hollander J, Fiebig R, Gore M, Bejma J, Ookawara T, et al. (1999) Superoxide dismutase gene expression: fiber-specificadaptation to endurance training. Am. J. Physiol. 277: R856-R862.
27. Radak Z, Sasvari M, Nyakas C, Taylor AW, Ohno H, et al. (2000) Regular training modulates the accumulation of reactive carbonyl derivatives in mitochondrial and cytosolic fractions of rat skeletal muscle. Arch Biochem Biophys 383: 114-118.
28. Botezelli JD, Cambri LT, Ghezzi AC, Dalia RA, Scariot PP, et al. (2011) Different exercise protocols improve metabolic syndrome markers, tissue triglycerides content and antioxidant status in rats. Diabetol Metab Syndr doi: 10.1186/1758-5996-3-35.
29. Wilson DO, Johnson P, (2000) Exercise modulates antioxidant enzyme gene expression in rat myocardium and liver. J Appl Physiol 88: 1791-1796.
30. Kakarla P, Vadluri G, Reddy Kesireddy S, (2005) Response of hepatic antioxidant system to exercise training in aging female rat. J Exp Zool A Comp Exp Biol 303: 203-208.
31. Cobley JN, McGlory C, Morton JP, Close GL, (2011) N-Acetylcysteine's attenuation of fatigue after repeated bouts of intermittent exercise: practical implications for tournament situations. Int J Sport Nutr Exerc Metab 21: 451-461.
32. Arida RM, Scorza FA, dos Santos NF, Peres CA, Cavalheiro EA, (1999) Effect of physical exercise on seizure occurrence in a model of temporal lobe epilepsy in rats. Epilepsy Res 37: 45-52.
33. da Luz G, Frederico MJ, da Silva S, Vitto MF, Cesconetto PA, et al. (2011) Endurance exercise training ameliorates insulin resistance and reticulum stress in adipose and hepatic tissue in obese rats. Eur J Appl Physiol 111: 2015-2023.
34. Lee FT, Kuo TY, Liou SY, Chien CT, (2009) Chronic Rhodiola rosea extract supplementation enforces exhaustive swimming tolerance. Am J Chin Med 37: 557-572.
35. Marquezi ML, Roschel HA, dos Santa Costa A, Sawada LA, Lancha AH Jr, (2003) Effect of aspartate and asparagine supplementation on fatigue determinants in intense exercise. Int J Sport Nutr Exerc Metab 13: 65-75.
36. de Araujo GG, Papoti M, Manchado F de B, de Mello MA, Gobatto CA, (2007) Protocols for hyperlactatemia induction in the lactate minimum test adapted to swimming rats. Comp Biochem Physiol A Mol Integr Physiol 148: 888-892.
37. Bhattacharya SK, Thakar JH, Johnson PL, Shanklin DR, (1991) Isolation of skeletal-muscle mitochondria from hamsters using an ionic medium containing ethylenediaminetetraacetic acid and nagarse. Anal Biochem 192: 344-349.
38. Hissin PJ, Hilf R, (1976) Fluorometric Method for Determination of Oxidized and Reduced Glutathione in Tissues. Anal Biochem 74: 214-226.
39. Misra HP, Fridovich I, (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247: 3170-3175.
40. Ohkawa H, Ohishi N, Yagi K, (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95: 351-358.
41. Pastor A, Collado PS, Almar M, González-Gallego J, (1996) Microsomal function in biliary obstructed rats: Effects of S-adenosylmethionine. J Hepatol 24: 353-359.
42. Levine RL, Garland D, Oliver CN, Amici A, Climent I, et al. (1990) Determination of Carbonyl Content in Oxidatively Modified Proteins. Method Enzymol 186: 464-478.
43. Cohen G, Farooqui R, Kesler N, (1997) Parkinson disease: a new link between monoamine oxidase and mitochondrial electron fl{ligature}ow. Proc Natl Acad Sci USA 94: 4890-4894.
44. Berridge MV, Tan AS, (1993) Characterization of the cellular reduction of 3-(4,5-dimethylthiazol-2 yl)-2,5-diphenyltetrazolium bromide (MTT): subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction. Arch Biochem Biophys 303: 474-482.
45. Akerman KEO, Wikstron KF, (1976) Safranine as a probe of the mitochondrial membrane potential. FEBS Lett 68: 191-197.
46. Ali SF, LeBel CP, Bondy SC, (1992) Reactive oxygen species formation as a biomarker of methylmercury and trimethyltin neurotoxicity. Neurotoxicology 13: 637-48.
47. Dionisio N, Garcia-Mediavilla MV, Sanchez-Campos S, Majano PL, Benedicto I, et al. (2009) Hepatitis C virus NS5A and core proteins induce oxidative stress-mediated calcium signalling alterations in hepatocytes. Journal of Hepatol 50: 872-82.
48. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
49. Lima FD, Oliveira MS, Furian AF, Souza MA, Rambo LM, et al. (2009) Adaptation to oxidative challenge induced by chronic physical exercise prevents Na+,K+-ATPase activity inhibition after traumatic brain injury. Brain Res 1279: 147-155.
50. Rambo LM, Ribeiro LR, Oliveira MS, Furian AF, Lima FD, et al. (2009) Additive anticonvulsant effects of creatine supplementation and physical exercise against pentylenetetrazol-induced seizures. Neurochem Int 55: 333-340.
51. Souza MA, Oliveira MS, Furian AF, Rambo LM, Ribeiro LR, et al. (2009) Swimming training prevents pentylenetetrazol-induced inhibition of Na+, K+-ATPase activity, seizures, and oxidative stress. Epilepsia 50: 811-823.
52. Ravi Kiran T, Subramanyam MV, Prathima S, Asha Devi S, (2006) Blood lipid profile and myocardial superoxide dismutase in swim-trained young and middle-aged rats: comparison between left and right ventricular adaptations to oxidative stress. J Comp Physiol B 176: 749-762.
53. Clavel S, Farout L, Briand M, Briand Y, Jouanel P, (2002) Effect of endurance training and/or fish oil supplemented diet on cytoplasmic fatty acid binding protein in rat skeletal muscles and heart. Eur J Appl Physiol 87: 193-201.
54. Yoshioka M, Doucet E, St-Pierre S, Almeras N, Richard D, et al. (2001) Impact of high-intensity exercise on energy expenditure, lipid oxidation and body fatness. Int J Obes Relat Metab Disord 25: 332-339.
55. Kiens B, Richter EA, (1998) Utilization of skeletal muscle triacylglycerol during postexercise recovery in humans. Am J Physiol 275: E332-E337.
56. Belardinelli P, Ciancetta L, Staudt M, Pizzella V, Londei A, et al. (2007) Cerebro-muscular and cerebro-cerebral coherence in patients with pre- and perinatally acquired unilateral brain lesions. Neuroimage 37: 1301-1314.
57. Kiraly MA, Kiraly SJ, (2005) The effect of exercise on hippocampal integrity: review of recent research. Int J Psychiatry Med 35: 75-89.
58. Lazarevic G, Antic S, Cvetkovic T, Vlahovic P, Tasic I, et al. (2006) A physical activity programme and its effects on insulin resistance and oxidative defense in obese male patients with type 2 diabetes mellitus. Diabetes Metab 32: 583-590.
59. Packer L, Cadenas E, (2007) Oxidants and antioxidants revisited. New concepts of oxidative stress. Free Radic Res 41: 951-952.
60. Sachdev S, Davies KJ, (2008) Production, detection, and adaptive responses to free radicals in exercise. Free Radic Biol Med 44: 215-223.
61. Sun L, Shen W, Liu Z, Guan S, Liu J, et al. (2010) Endurance exercise causes mitochondrial and oxidative stress in rat liver: effects of a combination of mitochondrial targeting nutrients. Life Sci 86: 39-44.
62. Nikolaidis MG, Jamurtas AZ, Paschalis V, Fatouros IG, Koutedakis Y, et al. (2008) The effect of muscle-damaging exercise on blood and skeletal muscle oxidative stress: magnitude and time-course considerations. Sports Med. 38: 579-606.
63. Mrtensson J, Meister A, (1991) Glutathione deficiency decreases tissue ascorbate levels in newborn rats: ascorbate spares glutathione and protects. Proc Natl Acad Sci USA 88: 4656-4660.
64. Navarro A, Gomez C, López-Cepero JM, Boveris A, (2004) Beneficial effects of moderate exercise on mice aging: survival, behavior, oxidative stress, and mitochondrial electron transfer. Am J Physiol Regul Integr Comp Physiol 286: R505-511.
65. De Minicis S, Bataller R, Brenner DA, (2006) NADPH oxidase in the liver: defensive, offensive, or fibrogenic? Gastroenterology 131: 272-275.
66. Levine RL, Stadtman ER, (2001) Oxidative modification of proteins during aging. Exp Gerontol 36: 1495-1502.
67. Linton S, Davies MJ, Dean RT, (2001) Protein oxidation and ageing. Exp. Gerontol 36: 1503-1518.
68. Echtay KS, (2007) Mitochondrial uncoupling proteins- what is their physiological role? Free Radic Biol Med 43: 1351-1371.
69. Berna T, Dobrucki J, (2002) Mitochondrial and nonmitochondrial reduction of MTT: interaction of MTT with TMRE, JC-1, and NAO mitochondrial fl{ligature}uorescent probes. Citometry 47: 236-242.
70. Grassi B, Porcelli S, Salvadego D, Zoladz JA, (2011) Slow VO2 kinetics during moderate-intensity exercise as markers of lower metabolic stability and lower exercise tolerance. Eur J Appl Physiol 111: 345-355.
71. Remedio RN, Castellar A, Barbosa RA, Gomes RJ, Caetano FH, (2011) Morphology and protein content of hepatocytes in type I diabetic rats submitted to physical exercises. Micron 42: 484-491.