DOI QR코드

DOI QR Code

Antioxidant action of soy isoflavones on oxidative stress and antioxidant enzyme activities in exercised rats

  • Yoon, Gun-Ae (Department of Food and Nutrition, College of Natural Science and Human Ecology, Dong-eui University) ;
  • Park, Sunmin (Department of Food and Nutrition, College of Natural Science, Hoseo University)
  • Received : 2014.03.20
  • Accepted : 2014.05.29
  • Published : 2014.12.01

Abstract

BACKGROUND/OBJECTIVES: Isoflavones are widely believed to be beneficial to human health, in relation to their antioxidant potentials. Exercise can cause an imbalance between reactive oxygen species (ROS) and antioxidants. This study was conducted in order to investigate the ability of isoflavones in amelioration of oxidative stress induced by exercise. MATERIALS/METHODS: Male Sprague-Dawley rats were assigned to one of four groups: isoflavone-free with no exercise (CON-sd), isoflavone-free with exercise (CON-ex), isoflavone-supplemented with no exercise (ISF-sd), and isoflavone-supplemented with exercise (ISF-ex). Animals exercised on the treadmill for 30 minutes per day, five days per week. TBARS as a marker of oxidative stress and antioxidant enzyme activity, including SOD, GSH-px, and catalase were determined in liver tissue. Serum lipid profile was also examined. RESULTS: A significant effect of isoflavone alone was observed on abdominal fat pad mass. ISF-ex had significantly less abdominal fat pad than CON-ex. Both exercise and isoflavone treatment had significant effects on lowering plasma triglyceride (TG), thus, the ISF-ex group had a significantly lower TG level than the CON-sd group, by 30.9%. However, no differences were observed in plasma cholesterol, HDL-C, and cholesterol/HDL-C ratio. Exercise, isoflavone, and exercise-isoflavone interaction effects were significant on thiobarbituric acid reactive substances (TBARS) (P = 0.001, 0.002, and 0.005, respectively). The CON-ex group showed a higher TBARS level than the other three groups. By contrast, in the ISF-ex group, TBARS was restored to the level of the ISF-sd or CON-sd group. Isoflavone had a significant effect on superoxide dismutase (SOD) (P = 0.022) and catalase activities (P = 0.049). Significantly higher SOD and catalase activities were observed in ISF-ex than CON-ex. SOD and catalase activities showed an inverse pattern of TBARS. Taken together, isoflavones increased the activities of SOD and catalase with concomitant decreases in TBARS, indicative of decreased oxidative stress. CONCLUSIONS: Isoflavone supplementation enhances antioxidant action with attenuation of exercise-induced oxidative stress, as measured by decreases in TBARS, and inhibits body fat accumulation and plasma TG increase. Antioxidative effects ascribed to isoflavones may be partially exerted via enhancement of antioxidant enzyme activities.

Keywords

References

  1. Radak Z, Kaneko T, Tahara S, Nakamoto H, Ohno H, Sasvari M, Nyakas C, Goto S. The effect of exercise training on oxidative damage of lipids, proteins, and DNA in rat skeletal muscle: evidence for beneficial outcomes. Free Radic Biol Med 1999;27:69-74. https://doi.org/10.1016/S0891-5849(99)00038-6
  2. Borek C. Antioxidant health effects of aged garlic extract. J Nutr 2001;131:1010S-1015S.
  3. Alessio HM, Hagerman AE, Romanello M, Carando S, Threlkeld MS, Rogers J, Dimitrova Y, Muhammed S, Wiley RL. Consumption of green tea protects rats from exercise-induced oxidative stress in kidney and liver. Nutr Res 2002;22:1177-88. https://doi.org/10.1016/S0271-5317(02)00421-9
  4. Yousef MI, Kamel KI, Esmail AM, Baghdadi HH. Antioxidant activities and lipid lowering effects of isoflavone in male rabbits. Food Chem Toxicol 2004;42:1497-503. https://doi.org/10.1016/j.fct.2004.04.012
  5. Erba D, Casiraghi MC, Martinez-Conesa C, Goi G, Massaccesi L. Isoflavone supplementation reduces DNA oxidative damage and increases O-${\beta}$-N-acetyl-D-glucosaminidase activity in healthy women. Nutr Res 2012;32:233-40. https://doi.org/10.1016/j.nutres.2012.03.007
  6. Schewe T, Steffen Y, Sies H. How do dietary flavanols improve vascular function? A position paper. Arch Biochem Biophys 2008;476:102-6. https://doi.org/10.1016/j.abb.2008.03.004
  7. Sawa T, Nakao M, Akaike T, Ono K, Maeda H. Alkylperoxyl radical-scavenging activity of various flavonoids and other phenolic compounds: implications for the anti-tumor-promoter effect of vegetables. J Agric Food Chem 1999;47:397-402. https://doi.org/10.1021/jf980765e
  8. Sierens J, Hartley JA, Campbell MJ, Leathem AJ, Woodside JV. In vitro isoflavone supplementation reduces hydrogen peroxide-induced DNA damage in sperm. Teratog Carcinog Mutagen 2002;22:227-34. https://doi.org/10.1002/tcm.10015
  9. Banz W, Hauck S, Gename B, Winters T, Bartke A. Soy isoflavones modify liver free radical scavenger systems and liver parameters in Sprague-Dawley rats. J Med Food 2004;7:477-81. https://doi.org/10.1089/jmf.2004.7.477
  10. Ibrahim WH, Habib HM, Chow CK, Bruckner GG. Isoflavone-rich soy isolate reduces lipid peroxidation in mouse liver. Int J Vitam Nutr Res 2008;78:217-22. https://doi.org/10.1024/0300-9831.78.45.217
  11. Urso ML, Clarkson PM. Oxidative stress, exercise, and antioxidant supplementation. Toxicology 2003;189:41-54. https://doi.org/10.1016/S0300-483X(03)00151-3
  12. Burneiko RC, Diniz YS, Galhardi CM, Rodrigues HG, Ebaid GM, Faine LA, Padovani CR, Cicogna AC, Novelli EL. Interaction of hypercaloric diet and physical exercise on lipid profile, oxidative stress and antioxidant defenses. Food Chem Toxicol 2006;44:1167-72. https://doi.org/10.1016/j.fct.2006.01.004
  13. Qiao D, Hou L, Liu X. Influence of intermittent anaerobic exercise on mouse physical endurance and antioxidant components. Br J Sports Med 2006;40:214-8. https://doi.org/10.1136/bjsm.2005.020099
  14. Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979;95:351-8. https://doi.org/10.1016/0003-2697(79)90738-3
  15. Flohe L, Gunzler WA. Assays of glutathione peroxidase. Methods Enzymol 1984;105:114-20. https://doi.org/10.1016/S0076-6879(84)05015-1
  16. Aebi H. Catalase. In: Bergmeyer HU, editor. Methods of enzymatic analysis. Weinheim: Academic Press; 1974. p.673-84.
  17. Fidanza F. Erythrocyte superoxide dismutase. In: Nutritional status assessment: a manual for population studies. New York (NY): Chapman & Hall; 1991. p.398-401.
  18. Seifried HE, Anderson DE, Fisher EI, Milner JA. A review of the interaction among dietary antioxidants and reactive oxygen species. J Nutr Biochem 2007;18:567-79. https://doi.org/10.1016/j.jnutbio.2006.10.007
  19. Chen CY, Bakhiet RM, Hart V, Holtzman G. Isoflavones improve plasma homocysteine status and antioxidant defense system in healthy young men at rest but do not ameliorate oxidative stress induced by 80% VO2pk exercise. Ann Nutr Metab 2005;49:33-41. https://doi.org/10.1159/000084175
  20. Cederroth CR, Nef S. Soy, phytoestrogens and metabolism: a review. Mol Cell Endocrinol 2009;304:30-42. https://doi.org/10.1016/j.mce.2009.02.027
  21. el-Demerdash FM, Yousef MI, Al-Salhen KS. Protective effects of isoflavone on some biochemical parameters affected by cypermethrin in male rabbits. J Environ Sci Health B 2003;38:365-78. https://doi.org/10.1081/PFC-120019902
  22. Weggemans RM, Trautwein EA. Relation between soy-associated isoflavones and LDL and HDL cholesterol concentrations in humans: a meta-analysis. Eur J Clin Nutr 2003;57:940-6. https://doi.org/10.1038/sj.ejcn.1601628
  23. Kawakami Y, Tsurugasaki W, Yoshida Y, Igarashi Y, Nakamura S, Osada K. Regulative actions of dietary soy isoflavone on biological antioxidative system and lipid metabolism in rats. J Agric Food Chem 2004;52:1764-8. https://doi.org/10.1021/jf0345898
  24. Demonty I, Lamarche B, Deshaies Y, Jacques H. Role of soy isoflavones in the hypotriglyceridemic effect of soy protein in the rat. J Nutr Biochem 2002;13:671-7. https://doi.org/10.1016/S0955-2863(02)00214-0
  25. Sohn E, Deyhim F, Devareddy L, Arjmandi BH. Soy isoflavones attenuate estrogen-deficient-induced increases in abdominal fat in the hamster. Nutr Res 2004;24:1023-9. https://doi.org/10.1016/j.nutres.2004.09.005
  26. Nelson SK, Bose SK, Grunwald GK, Myhill P, McCord JM. The induction of human superoxide dismutase and catalase in vivo: a fundamentally new approach to antioxidant therapy. Free Radic Biol Med 2006;40:341-7. https://doi.org/10.1016/j.freeradbiomed.2005.08.043
  27. Pszczola DE Katz F, Giese J. Research trends in healthful foods. Food Technol 2000;54:45-52.
  28. Castro L, Freeman BA. Reactive oxygen species in human health and disease. Nutrition 2001;17:161, 163-5.
  29. McCord JM. The evolution of free radicals and oxidative stress. Am J Med 2000;108:652-9. https://doi.org/10.1016/S0002-9343(00)00412-5
  30. Itoh M, Oh-Ishi S, Hatao H, Leeuwenburgh C, Selman C, Ohno H, Kizaki T, Nakamura H, Matsuoka T. Effects of dietary calcium restriction and acute exercise on the antioxidant enzyme system and oxidative stress in rat diaphragm. Am J Physiol Regul Integr Comp Physiol 2004;287:R33-8. https://doi.org/10.1152/ajpregu.00598.2003
  31. Oh HY, Lim S, Lee JM, Kim DY, Ann ES, Yoon S. A combination of soy isoflavone supplementation and exercise improves lipid profiles and protects antioxidant defense-systems against exercise-induced oxidative stress in ovariectomized rats. Biofactors 2007;29:175-85. https://doi.org/10.1002/biof.5520290402
  32. Hsu CS, Chiu WC, Yeh SL. Effects of soy isoflavone supplementation on plasma glucose, lipids, and antioxidant enzyme activities in streptozotocin-induced diabetic rats. Nutr Res 2003;23:67-75. https://doi.org/10.1016/S0271-5317(02)00386-X
  33. Valsecchi AE, Franchi S, Panerai AE, Rossi A, Sacerdote P, Colleoni M. The soy isoflavone genistein reverses oxidative and inflammatory state, neuropathic pain, neurotrophic and vasculature deficits in diabetes mouse model. Eur J Pharmacol 2011;650:694-702. https://doi.org/10.1016/j.ejphar.2010.10.060
  34. McCarty MF. Isoflavones made simple - genistein's agonist activity for the beta-type estrogen receptor mediates their health benefits. Med Hypotheses 2006;66:1093-114. https://doi.org/10.1016/j.mehy.2004.11.046
  35. Lee JS. Effects of soy protein and genistein on blood glucose, antioxidant enzyme activities, and lipid profile in streptozotocin-induced diabetic rats. Life Sci 2006;79:1578-84. https://doi.org/10.1016/j.lfs.2006.06.030
  36. Dixit AK, Bhatnagar D, Kumar V, Chawla D, Fakhruddin K, Bhatnagar D. Antioxidant potential and radioprotective effect of soy isoflavone against gamma irradiation induced oxidative stress. J Funct Foods 2012;4:197-206. https://doi.org/10.1016/j.jff.2011.10.005

Cited by

  1. Antidiabetic Potential of Kefir Combination from Goat Milk and Soy Milk in Rats Induced with Streptozotocin-Nicotinamide vol.35, pp.6, 2015, https://doi.org/10.5851/kosfa.2015.35.6.847
  2. Dietary soy isoflavones alleviate dextran sulfate sodium-induced inflammation and oxidative stress in mice vol.14, pp.1, 2017, https://doi.org/10.3892/etm.2017.4469
  3. Association between consumption of soy and risk of cardiovascular disease: A meta-analysis of observational studies vol.24, pp.7, 2017, https://doi.org/10.1177/2047487316686441
  4. TMF and glycitin act synergistically on keratinocytes and fibroblasts to promote wound healing and anti-scarring activity vol.49, pp.3, 2017, https://doi.org/10.1038/emm.2016.167
  5. Oxidative stress and inflammation: liver responses and adaptations to acute and regular exercise vol.51, pp.2, 2017, https://doi.org/10.1080/10715762.2017.1291942
  6. Antioxidant Effects of Biochanin A in Streptozotocin Induced Diabetic Rats vol.60, pp.0, 2017, https://doi.org/10.1590/1678-4324-2017160741
  7. Antioxidant and hypolipidemic effects of soymilk fermented via Lactococcus acidophilus MF204 pp.2042-650X, 2017, https://doi.org/10.1039/C7FO00701A
  8. Inflammaging and Skeletal Muscle: Can Protein Intake Make a Difference? vol.146, pp.10, 2016, https://doi.org/10.3945/jn.116.230912
  9. Rebelling against the (Insulin) Resistance: A Review of the Proposed Insulin-Sensitizing Actions of Soybeans, Chickpeas, and Their Bioactive Compounds vol.10, pp.4, 2018, https://doi.org/10.3390/nu10040434
  10. Molecular Action of Herbal Antioxidants in Regulation of Cancer Growth: Scope for Novel Anticancer Drugs pp.1532-7914, 2018, https://doi.org/10.1080/01635581.2018.1539187
  11. Physiological parameters and productive performance of rabbit does and their offsprings with dietary supplementation of soy lecithin vol.53, pp.9, 2018, https://doi.org/10.1590/s0100-204x2018000900012
  12. Isoflavones in gynecology vol.64, pp.6, 2018, https://doi.org/10.1590/1806-9282.64.06.560
  13. Role of Elicitors Foliar Application in Increasing Isoflavone Content of Two Soybean Cultivars vol.17, pp.2, 2018, https://doi.org/10.3923/ja.2018.106.111
  14. Role of Elicitors in Chlorophyll Content and Stomatal Density of Soybean Cultivars by Foliar Application vol.17, pp.2, 2018, https://doi.org/10.3923/ja.2018.112.117
  15. Soy isoflavones protect against oxidative stress and diminish apoptosis in ovary of middle-aged female rats pp.1473-0766, 2019, https://doi.org/10.1080/09513590.2018.1559287
  16. Dietary soy isoflavones during pregnancy suppressed the immune function in male offspring albino rats vol.5, pp.None, 2014, https://doi.org/10.1016/j.toxrep.2018.02.002
  17. The effects of coenzyme Q10 on oxidative stress and heat shock proteins in rats subjected to acute and chronic exercise vol.22, pp.3, 2014, https://doi.org/10.20463/jenb.2018.0019
  18. Development of Health Products from Natural Sources vol.26, pp.24, 2019, https://doi.org/10.2174/0929867325666180926152139
  19. Isoflavones vol.24, pp.6, 2019, https://doi.org/10.3390/molecules24061076
  20. Protective effect of daidzein against streptozotocin‐induced Alzheimer's disease via improving cognitive dysfunction and oxidative stress in rat model vol.33, pp.6, 2014, https://doi.org/10.1002/jbt.22319
  21. Soy Isoflavones Improve the Spermatogenic Defects in Diet-Induced Obesity Rats Through Nrf2/HO-1 Pathway vol.24, pp.16, 2014, https://doi.org/10.3390/molecules24162966
  22. Association of Untargeted Urinary Metabolomics and Lung Cancer Risk Among Never-Smoking Women in China vol.2, pp.9, 2014, https://doi.org/10.1001/jamanetworkopen.2019.11970
  23. Comparison of the Effects of Soy Protein and Whey Protein Supplementation during Exercise: a Systematic Review vol.21, pp.4, 2014, https://doi.org/10.17921/2447-8938.2019v21n4p397-403
  24. Multimodal α -Glucosidase and α -Amylase Inhibition and Antioxidant Effect of the Aqueous and Methanol Extracts from the Trunk Bark of Ceiba pentandra vol.2020, pp.None, 2014, https://doi.org/10.1155/2020/3063674
  25. Concise anti-oxidative stress defence effects of Duvalia corderoyi in the liver and kidney tissues of streptozotocin-induced diabetic rats vol.14, pp.1, 2014, https://doi.org/10.1080/16583655.2020.1751962
  26. Facile Synthesis of Novel Isoflavone/1,2,3-Triazole Hybrid Heterocycles as Potential Antimicrobial Agents vol.90, pp.5, 2020, https://doi.org/10.1134/s1070363220050266
  27. Protective effect of genistein in a rat model of ischemic acute kidney injury vol.753, pp.None, 2014, https://doi.org/10.1016/j.gene.2020.144789
  28. Pu-erh Tea Extract Treatment Could Be an Efficient Way to Enhance the Yield and Nutritional Value of Soybean Sprout vol.25, pp.17, 2020, https://doi.org/10.3390/molecules25173869
  29. Pengembangan Soyghurt (Yoghurt Susu Kacang Kedelai) Sebagai Minuman Probiotik Tinggi Isoflavon vol.4, pp.3, 2014, https://doi.org/10.20473/amnt.v4i3.2020.244-249
  30. Soy isoflavones ameliorate the cognitive dysfunction of Goto-Kakizaki rats by activating the Nrf2-HO-1 signalling pathway vol.12, pp.21, 2014, https://doi.org/10.18632/aging.103877
  31. Health Promotion Effects of Soy Isoflavones vol.66, pp.6, 2014, https://doi.org/10.3177/jnsv.66.502
  32. Alternatives to hormone therapy for management of climacteric syndrome vol.2021, pp.3, 2021, https://doi.org/10.21518/2079-701x-2021-3-136-143
  33. Soy intake is associated with lowering blood pressure in adults: A systematic review and meta-analysis of randomized double-blind placebo-controlled trials vol.59, pp.None, 2014, https://doi.org/10.1016/j.ctim.2021.102692
  34. Current Perspectives on the Beneficial Effects of Soybean Isoflavones and Their Metabolites for Humans vol.10, pp.7, 2021, https://doi.org/10.3390/antiox10071064
  35. Natural isoflavonoids in invasive cancer therapy: From bench to bedside vol.35, pp.8, 2021, https://doi.org/10.1002/ptr.7072
  36. From Menopause to Neurodegeneration-Molecular Basis and Potential Therapy vol.22, pp.16, 2021, https://doi.org/10.3390/ijms22168654
  37. Soy Isoflavones Intake and Obesity in Chinese Adults: A Cross-Sectional Study in Shanghai, China vol.13, pp.8, 2014, https://doi.org/10.3390/nu13082715
  38. Genistein and exercise treatment reduced NASH related HDAC3, IL-13 and MMP-12 expressions in ovariectomized rats fed with high fat high fructose diet vol.11, pp.6, 2021, https://doi.org/10.1016/j.jtcme.2021.04.004
  39. Production of Genistein in Amaranthus tricolor var. tristis and Spinacia oleracea by Expression of Glycine max Isoflavone Synthase vol.10, pp.11, 2014, https://doi.org/10.3390/plants10112311
  40. Potential therapeutic interventions of plant-derived isoflavones against acute lung injury vol.101, pp.no.pa, 2014, https://doi.org/10.1016/j.intimp.2021.108204