Effects of Gender, Endurance Training and Acute Exhaustive Exercise on Oxidative Stress in the Heart and Skeletal Muscle of the Rat

10.4077/CJP.2012.BAA021

Sükrü Serdar Balcı；Hamdi Pepe；Sevin Güney；Çi ˘gdem Özer；Serkan Revan

gender differences ； endurance training ； exhaustive exercise ； oxidative stress ； heart ； skeletal

The Chinese Journal of Physiology

55卷4期（2012 / 08 / 01）

236 - 244

英文

Effects of gender differences and endurance training on exhaustive exercise induced-oxidative stress have been a question that has not been clarified in the literature. The aim of this study was to determine the effects of sex, acute exhaustive exercise and chronic aerobic exercise training on oxidative stress in the heart and the skeletal muscle. The study was carried out with 12 week-old male (n=24) and female (n=24) young adult Wistar rats. They were randomly divided into four groups: untrained, trained, untrained exhausted and trained exhausted. The rats in the trained group swam for 60 min/day, five days per week for eight weeks. Thereafter, one-half of the trained and one-half of the untrained rats were randomly selected into the trained and untrained exhaustive exercise groups, respectively. They were killed immediately after one last exhaustive swimming exercise. In the heart, endurance training decreased malondialdehyde (MDA) levels in the female rats at rest, but did not change in the male rats in the heart; MDA levels were also increased in female rats at rest in the gastrocnemius tissues. In the trained female rats, exhaustive exercise decreased MDA levels in the heart and gastrocnemius tissues. The nitric oxide (NO) levels in the heart in the untrained female rats were higher than in the male rats after exhaustive exercise. Training decreased the NO levels in both sexes in the gastrocnemius tissue at rest. In the heart, the untrained female rats had higher total glutathione (GSH) levels than in the male rats at rest. Also, exhaustive exercise decreased the GSH levels in the trained female rats. In the gastrocnemius, untrained female rats showed higher GSH levels than in the male after exhaustive exercise. The superoxide dismutase activities in the gastrocnemius were similar between the female and male rats. The results suggested that gender was a major determinant of changes in MDA, NO and GSH levels in the heart and gastrocnemius tissues after the exhaustive exercise or endurance training. Also, the responses to oxidative stress induced by acute exercise or training in the heart and gastrocnemius muscle tissues are different.

1. Ali, S.S.,Xiong, C.,Lucero, J.,Behrens, M.M.,Dugan, L.L.,Quick, K.L.(2006).Gender differences in free radical homeostasis during aging: shorter-lived female C57BL6 mice have increased oxidative stress.Aging Cell,5(6),565-574.
2. Aydin, C.,Ince, E.,Koparan, S.,Cangul, I.T.,Naziroglu, M.,Ak, F.(2007).Protective effects of long term dietary restriction on swimming exercise-induced oxidative stress in the liver, heart and kidney of rat.Cell Biochem. Funct.,25,129-137.
3. Aykaç, G.,Uysal, M.,Yalçin, A.S.,Koçak-Toker, N.,Sivas, A.,Oz, H.(1985).The effect of chronic ethanol ingestion on hepatic lipid peroxide, glutathione, glutathione peroxidase and glutathione transferase in rats.Toxicology,36,71-76.
4. Barp, J.,Araújo, A.S.,Fernandes, T.R.,Rigatto, K.V.,Llesuy, S.,Belló-Klein, A.,Singal, P.(2002).Myocardial antioxidant and oxidative stress changes due to sex hormones.Braz. J. Med. Biol. Res.,35,1075-1081.
5. Bloomer, R.J.,Davis, P.G.,Consitt, L.A.,Wideman, L.(2007).Plasma protein carbonyl response to increasing exercise duration in aerobically trained men and women.Int. J. Sports Med.,28,21-25.
6. Bloomer, R.J.,Fisher-Wellman, K.H.(2008).Blood oxidative stress biomarkers: influence of sex, exercise training status, and dietary intake.Gend. Med.,5(3),218-228.
7. Bloomer, R.J.,Goldfarb, A.H.,Wideman, L.,McKenzie, M.J.,Consitt, L.A.(2005).Effects of acute aerobic and anaerobic exercise on blood markers of oxidative stress.J. Strength Cond. Res.,19,276-285.
8. Borrás, C.,Gambini, J.,Gómez-Cabrera, M.C.,Sastre, J.,Pallardó, F.V.,Mann, G.E.,Viña, J.(2005).17β-oestradiol up-regulates longevity-related, antioxidant enzyme expression via the ERK1 and ERK2MAPK/NFκB cascade.Aging Cell.,4(3),113-118.
9. Borrás, C.,Sastre, J.,García-Sala, D.,Lloret, A.,Pallardó, F.V.,Viña, J.(2003).Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males.Free Radic. Biol. Med.,34,546-552.
10. Cao, G.,Giovanoni, M.,Prior, R.L.(1996).Antioxidant capacity in different tissues of young and old rats.Proc. Soc. Exp. Biol. Med.,211,359-365.
11. Casini, A.F.,Ferrali, M.,Pompella, A.,Maellaro, E.,Comporti, M.(1986).Lipid peroxidation and cellular damage in extrahepatic tissues of bromobenzene-intoxicated mice.Am. J. Pathol.,123,520-531.
12. da Rocha, R.F.,de Oliveira, M.R.,Pasquali, M.A.,Andrades, M.E.,Oliveira, M.W.S.,Behr, G.A.,Moreira, J.C.F.(2010).Vascular redox imbalance in rats submitted to chronic exercise.Cell Biochem. Funct.,28,190-196.
13. Ginsburg, G.S.,O''Toole, M.,Rimm, E.,Douglas, P.S.,Rifai, N.(2001).Gender differences in exercise-induced changes in sex hormone levels and lipid peroxidation in athletes participating in the Hawaii Ironman triathlon. Ginsburg-gender and exercise-induced lipid peroxidation.Clin. Chim. Acta,305,131-139.
14. Goldfarb, A.H.,McKenzie, M.J.,Bloomer, R.J.(2007).Gender comparisons of exercise-induced oxidative stress: influence of antioxidant supplementation.Appl. Physiol. Nutr. Metab.,32,1124-1131.
15. Gomez-Cabrera, M.C.,Viña, J.,Ji, L.L.(2009).Interplay of oxidants and antioxidants during exercise: implications for muscle health.Phys. Sportsmed.,37,116-123.
16. Gopal, I.(1997).The Faculty of the Graduate School at the University of North Carolina.
17. Gul, M.,Demircan, B.,Taysi, S.,Oztasan, N.,Gumustekin, K.,Siktar, E.,Polat, M.F.,Akar, S.,Akcay, F,Dane, S.(2006).Effects of endurance training and acute exhaustive exercise on antioxidant defense mechanisms in rat heart.Comp. Biochem. Physiol. A Mol. Integr. Physiol.,143,239-245.
18. Huh, K.,Shin, U.S.,Choi, J.W.,Lee, S.I.(1994).Effect of sex hormones on lipid peroxidation in rat liver.Arch. Pharm. Res.,17,109-114.
19. Ilhan, N.,Kamanli, A.,Ozmerdivenli, R.,Ilhan, N.(2004).Variable effects of exercise intensity on reduced glutathione, thiobarbituric acid reactive substance levels, and glucose concentration.Arch. Med. Res.,35,294-300.
20. Ji, L.L.(2002).Exercise-induced modulation of antioxidant defense.Ann. N. Y. Acad. Sci.,959,82-92.
21. Kaikkonen, J.,Porkkala-Sarataho, E.,Tuomainen, T.P.,Nyyssonen, K.,Kosonen, L.,Ristonmaa, U.,Lakka, H.M.,Salonen, R.,Korpela, H.,Salonen, J.T.(2002).Exhaustive exercise increases plasma/serum total oxidation resistance in moderately trained men and women, whereas their VLDL + LDL lipoprotein fraction is more susceptible to oxidation.Scand. J. Clin. Lab. Invest.,62,599-607.
22. Kakarla, P.,Vadluri, G.,Reddy, K.S.,Leeuwenburgh, C.(2005).Vulnerability of the mid aged rat myocardium to the age-induced oxidative stress: influence of exercise training on antioxidant defense system.Free Radic. Res.,39,1211-1217.
23. Katalinic, V.,Modun, D.,Music, I.,Boban, M.(2005).Gender differences in antioxidant capacity of rat tissues determined by 2,2'-azinobis (3-ethylbenzothiazoline 6-sulfonate; ABTS) and ferric reducing antioxidant power (FRAP) assays.Comp. Biochem. Physiol. C-Toxicol. Pharmacol.,140,47-52.
24. Knight, J.A.,Smith, S.E.,Kinder, V.E.,Anstall, H.B.(1987).Reference intervals for plasma lipoperoxides: age-, sex-, and specimen-related variations.Clin. Chem.,33,2289-2291.
25. Leeuwenburgh, C.,Ji, L.L.(1995).Glutathione depletion in rested and exercised mice: biochemical consequence and adaptation.Arch. Biochem. Biophys.,316,941-949.
26. Leeuwenburgh, C.,Leichtweis, S.,Hollander, J.,Fiebig, R.,Gore, M.,Ji, L.L.(1996).Effect of acute exercise on glutathione deficient heart.Mol. Cell. Biochem.,156,17-24.
27. 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.
28. Lew, H.,Quintanilha, A.(1991).Effects of endurance training and exercise on tissue antioxidative capacity and acetaminophen detoxification.Eur. J. Drug Metab. Pharmacokinet.,16,59-68.
29. Liu, J.,Yeo, H.C.,Overvik-Douki, E.,Hagen, T.,Doniger, S.J.,Chyu, D.W.,Brooks, G.A.,Ames, B.N.(2000).Chronically and acutely exercised rats: biomarkers of oxidative stress and endogenous antioxidants.J. Appl. Physiol.,89,21-28.
30. Lovlin, R.,Cottle, W.,Pyke, I.,Kavanagh, M.,Belcastro, A.N.(1987).Are indices of radical damage related to exercise intensity?.Eur. J. Appl. Physiol.,56,313-316.
31. Mastaloudis, A.,Yu, T.W.,O''Donnell, R.P.,Frei, B.,Dashwood, R.H.,Traber, M.G.(2004).Endurance exercise results in DNA damage as detected by the comet assay.Free Radic. Biol. Med.,36,966-975.
32. Miranda, K.M.,Espey, M.G.,Wink, D.A.(2001).A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite.Nitric Oxide,5(1),62-71.
33. Miyazaki, H.,Oh-ishi, S.,Ookawara, T.,Kizaki, T.,Toshinai, K.,Ha, S.,Haga, S.,Ji, L.L.,Ohno, H.(2001).Strenuous endurance training in humans reduces oxidative stress following exhausting exercise.Eur. J. Appl. Physiol.,84,1-6.
34. Ozbay, B.,Dülger, H.(2002).Lipid peroxidation and antioxidant enzymes in Turkish population: Relation to age, gender, exercise, and smoking.Tohoku J. Exp. Med.,197,119-124.
35. Oztasan, N.,Taysi, S.,Gumustekin, K.,Altinkaynak, K.,Aktas, O.,Timur, H.,Siktar, E.,Keles, S.,Akar, S., Akcay, F.,Dane, S.,Gul, M.(2004).Endurance training attenuates exercise-induced oxidative stress in erythrocytes in rat.Eur. J. Appl. Physiol.,91,622-627.
36. Pepe, H.,Balcı, S.S.,Revan, S.,Akalin, P.P.,Kurtoǧlu, F.(2009).Comparison of oxidative stress and antioxidant capacity before and after running exercises in both sexes.Gend. Med.,6(4),587-595.
37. Radak, Z.,Chung, H.Y.,Goto, S.(2008).Systemic adaptation to oxidative challenge induced by regular exercise.Free Radic. Biol. Med.,44,153-159.
38. Radak, Z.,Toldy, A.,Szabo, Z.,Siamilis, S.,Nyakas, C.,Silye, G.,Jakus, J.,Goto, S.(2006).The effects of training and detraining on memory, neurotrophins and oxidative stress markers in rat brain.Neurochem. Int.,49,387-392.
39. Sanz, A.,Hiona, A.,Kujoth, G.C.,Seo, A.Y.,Hofer, T.,Kouwenhoven, E.,Kalani, R.,Prolla, T.A.,Barja, G.,Leeuwenburgh, C.(2007).Evaluation of sex differences on mitochondrial bioenergetics and apoptosis in mice.Exp. Gerontol.,42,173-182.
40. Schmitz, K.H.,Warren, M.,Rundle, A.G.,Williams, N.I.,Gross, M.D.,Kurzer, M.S.(2008).Exercise effect on oxidative stress is independent of change in estrogen metabolism.Cancer Epidemiol. Biomarkers Prev.,17,220-223.
41. Seifi-Skishahr, F.,Siahkohian, M.,Nakhostin-Roohi, B.(2008).Influence of aerobic exercise at high and moderate intensities on lipid peroxidation in untrained men.J. Sports Med. Phys. Fit.,48,515-521.
42. Sen, C.K.,Packer, L.(2000).Thiol homeostasis and supplements in physical exercise.Am. J. Clin. Nutr.,72,653S-669S.
43. Sureda, A.,Tauler, P.,Aguiló, A.,Cases, N.,Fuentespina, E.,Córdova, A.,Tur, J.A.,Pons, A.(2005).Relation between oxidative stress markers and antioxidant endogenous defences during exhaustive exercise.Free Radic. Res.,39,1317-1324.
44. Taskiran, D.,Kutay, F.Z.,Sozmen, E.,Pogun, S.(1997).Sex differences in nitrite/nitrate levels and antioxidant defense in rat brain.Neuroreport,8(4),881-884.
45. Venditti, P.,Di Meo, S.(1997).Effect of training on antioxidant capacity, tissue damage, and endurance of adult male rats.Int. J. Sports Med.,18,497-502.
46. Viña, J.,Borrás, C.,Gambini, J.,Sastre, J.,Pallardó, F.V.(2005).Why females live longer than males? Importance of the upregulation of longevity-associated genes by oestrogenic compounds.FEBS Lett.,579,2541-2545.
47. Viña, J.,Sastre, J.,Pallardó, F.,Borrás, C.(2003).Mitochondrial theory of aging: importance to explain why females live longer than males.Antioxid. Redox. Signal.,5(5),549-556.
48. Wang, F.,He, Q.,Sun, Y.,Dai, X.,Yang, X.P.(2010).Female adult mouse cardiomyocytes are protected against oxidative stress.Hypertension,55,1172-1178.
49. Yamamoto, T.,Ohkuwa, T.,Itoh, H.,Sato, Y.,Naoi, M.(2002).Effect of gender differences and voluntary exercise on antioxidant capacity in rats.Comp. Biochem. Physiol. C-Toxicol. Pharmacol.,132,437-444.

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