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Suppression of oxidative stress by grape seed supplementation in rats

  • Received : 2011.09.07
  • Accepted : 2012.01.29
  • Published : 2012.02.29

Abstract

Polyphenol-rich grape seeds have a beneficial effect on human health. The present study was performed to investigate the effects of grape seeds on antioxidant activities in rats. Male Sprague-Dawley rats were randomly divided into a control diet group (C), a high-fat diet group (HF), a 5% grape seed-supplemented control diet group (G), and a 5% grape seed-supplemented high-fat diet group (HG). Dietary supplementation with grape seeds reduced serum concentrations of lipid peroxides compared with those in the C and HF groups. The hepatic level of lipid peroxides decreased significantly in the grape seed groups compared with that in the C and HF groups. Superoxide dismutase activity in the G group increased significantly compared with that in the C group. Catalase activity tended to be higher by feeding grape seeds. The grape seed diet increased glutathione peroxidase activity in the C group. Glutathione-S-transferase activity increased significantly in the G group compared with that in the C group. Hepatic content of total glutathione increased significantly in the HG group but decreased significantly in the HF group. The ratio of reduced glutathione and oxidized glutathione increased by feeding the grape seed diet. Total vitamin A concentration was significantly higher in HG group than in other groups. Liver tocopherol content of the G and HG groups was significantly higher than that of the control groups. These results suggest that dietary supplementation with grape seeds is beneficial for suppressing lipid peroxidation in high fat-fed rats.

Keywords

References

  1. Bray GA, Paeratakul S, Popkin BM. Dietary fat and obesity: a review of animal, clinical and epidemiological studies. Physiol Behav 2004;83:549-55. https://doi.org/10.1016/j.physbeh.2004.08.039
  2. Ozata M, Mergen M, Oktenli C, Aydin A, Sanisoglu SY, Bolu E, Yilmaz MI, Sayal A, Isimer A, Ozdemir IC. Increased oxidative stress and hypozincemia in male obesity. Clin Biochem 2002;35: 627-31. https://doi.org/10.1016/S0009-9120(02)00363-6
  3. Slattery ML, Curtin KP, Edwards SL, Schaffer DM. Plant foods, fiber, and rectal cancer. Am J Clin Nutr 2004;79:274-81. https://doi.org/10.1093/ajcn/79.2.274
  4. Smith-Warner SA, Spiegelman D, Yaun SS, Albanes D, Beeson WL, van den Brandt PA, Feskanich D, Folsom AR, Fraser GE, Freudenheim JL, Giovannucci E, Goldbohm RA, Graham S, Kushi LH, Miller AB, Pietinen P, Rohan TE, Speizer FE, Willett WC, Hunter DJ. Fruits, vegetables and lung cancer: a pooled analysis of cohort studies. Int J Cancer 2003;107:1001-11. https://doi.org/10.1002/ijc.11490
  5. Cui J, Juhasz B, Tosaki A, Maulik N, Das DK. Cardioprotection with grapes. J Cardiovasc Pharmacol 2002;40:762-9. https://doi.org/10.1097/00005344-200211000-00014
  6. Leifert WR, Abeywardena MY. Cardioprotective actions of grape polyphenols. Nutr Res 2008;28:729-37. https://doi.org/10.1016/j.nutres.2008.08.007
  7. Torres JL, Varela B, Garcia MT, Carilla J, Matito C, Centelles JJ, Cascante M, Sort X, Bobet R. Valorization of grape (Vitis vinifera) byproducts. Antioxidant and biological properties of polyphenolic fractions differing in procyanidin composition and flavonol content. J Agric Food Chem 2002;50:7548-55. https://doi.org/10.1021/jf025868i
  8. Shi J, Yu J, Pohorly JE, Kakuda Y. Polyphenolics in grape seeds-biochemistry and functionality. J Med Food 2003;6:291-9. https://doi.org/10.1089/109662003772519831
  9. Nandakumar V, Singh T, Katiyar SK. Multi-targeted prevention and therapy of cancer by proanthocyanidins. Cancer Lett 2008; 269:378-87. https://doi.org/10.1016/j.canlet.2008.03.049
  10. Mittal A, Elmets CA, Katiyar SK. Dietary feeding of proanthocyanidins from grape seeds prevents photocarcinogenesis in SKH-1 hairless mice: relationship to decreased fat and lipid peroxidation. Carcinogenesis 2003;24:1379-88. https://doi.org/10.1093/carcin/bgg095
  11. Beveridge TH, Girard B, Kopp T, Drover JC. Yield and composition of grape seed oils extracted by supercritical carbon dioxide and petroleum ether: varietal effects. J Agric Food Chem 2005;53:1799-804. https://doi.org/10.1021/jf040295q
  12. Ahn HS, Jeon TI, Lee JY, Hwang SG, Lim Y, Park DK. Antioxidative activity of persimmon and grape seed extract: in vitro and in vivo. Nutr Res 2002;22:1265-73. https://doi.org/10.1016/S0271-5317(02)00429-3
  13. Spranger I, Sun B, Mateus AM, de Freitas V, Ricardo-da-Silva JM. Chemical characterization and antioxidant activities of oligomeric and polymeric procyanidin fractions from grape seeds. Food Chem 2008;108:519-32. https://doi.org/10.1016/j.foodchem.2007.11.004
  14. Sato M, Maulik G, Ray PS, Bagchi D, Das DK. Cardioprotective effects of grape seed proanthocyanidin against ischemic reperfusion injury. J Mol Cell Cardiol 1999;31:1289-97. https://doi.org/10.1006/jmcc.1999.0961
  15. Sato M, Bagchi D, Tosaki A, Das DK. Grape seed proanthocyanidin reduces cardiomyocyte apoptosis by inhibiting ischemia/reperfusion-induced activation of JNK-1 and C-JUN. Free Radic Biol Med 2001;31:729-37. https://doi.org/10.1016/S0891-5849(01)00626-8
  16. Hogeboom GH. [3] Fractionation of cell components of animal tissues. Methods Enzymol 1955;1:16-9.
  17. Yagi K. A simple fluorometric assay for lipoperoxide in blood plasma. Biochem Med 1976;15:212-6. https://doi.org/10.1016/0006-2944(76)90049-1
  18. 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
  19. Aebi H. Catalase. In: Bergmeyer HU, editor. Methods of Enzymatic Analysis, Vol. 11. New York: Academic Press; 1974. p.673-84.
  20. Marklund S, Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 1974;47:469-74. https://doi.org/10.1111/j.1432-1033.1974.tb03714.x
  21. Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967;70:158-69.
  22. Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 1974;249:7130-9.
  23. Anderson ME. Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol 1985;113: 548-55.
  24. Furr HC, Amedee-Manesme O, Olson JA. Gradient reversedphase high-performance liquid chromatographic separation of naturally occurring retinoids. J Chromatogr 1984;309:299-307. https://doi.org/10.1016/0378-4347(84)80037-7
  25. Scandalios JG. Oxidative stress responses--what have genomescale studies taught us? Genome Biol 2002;3:REVIEWS1019.
  26. Milagro FI, Campion J, Martinez JA. Weight gain induced by high-fat feeding involves increased liver oxidative stress. Obesity (Silver Spring) 2006;14:1118-23. https://doi.org/10.1038/oby.2006.128
  27. Hirao K, Maruyama T, Ohno Y, Hirose H, Shimada A, Takei I, Murata M, Morii T, Eguchi T, Hayashi M, Saruta T, Itoh H. Association of increased reactive oxygen species production with abdominal obesity in type 2 diabetes. Obes Res Clin Pract 2010; 4:e83-90. https://doi.org/10.1016/j.orcp.2009.09.004
  28. Folmer V, Soares JC, Gabriel D, Rocha JB. A high fat diet inhibits delta-aminolevulinate dehydratase and increases lipid peroxidation in mice (Mus musculus). J Nutr 2003;133:2165-70. https://doi.org/10.1093/jn/133.7.2165
  29. Lee SJ, Choi SK, Seo JS. Grape skin improves antioxidant capacity in rats fed a high fat diet. Nutr Res Pract 2009;3:279-85. https://doi.org/10.4162/nrp.2009.3.4.279
  30. Niki E. Lipid peroxidation products as oxidative stress biomarkers. Biofactors 2008;34:171-80. https://doi.org/10.1002/biof.5520340208
  31. Choi CS, Chung HK, Choi MK, Kang MH. Effects of grape pomace on the antioxidant defense system in diet-induced hypercholesterolemic rabbits. Nutr Res Pract 2010;4:114-20. https://doi.org/10.4162/nrp.2010.4.2.114
  32. Clementi E, Brown GC, Feelisch M, Moncada S. Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc Natl Acad Sci U S A 1998;95:7631-6. https://doi.org/10.1073/pnas.95.13.7631
  33. Sen CK. Cellular thiols and redox-regulated signal transduction. Curr Top Cell Regul 2000;36:1-30.
  34. Sehirli O, Ozel Y, Dulundu E, Topaloglu U, Ercan F, Sener G. Grape seed extract treatment reduces hepatic ischemia-reperfusion injury in rats. Phytother Res 2008;22:43-8. https://doi.org/10.1002/ptr.2256
  35. Alia M, Horcajo C, Bravo L, Goya L. Effect of grape antioxidant dietary fiber on the total antioxidant capacity and the activity of liver antioxidant enzymes in rats. Nutr Res 2003;23:1251-67. https://doi.org/10.1016/S0271-5317(03)00131-3
  36. Bozan B, Tosun G, Ozcan D. Study of polyphenol content in the seeds of red grape (Vitis vinifera L.) varieties cultivated in Turkey and their antiradical activity. Food Chem 2008;109: 426-30. https://doi.org/10.1016/j.foodchem.2007.12.056
  37. Ramchandani AG, Chettiyar RS, Pakhale SS. Evaluation of antioxidant and anti-initiating activities of crude polyphenolic extracts from seedless and seeded Indian grapes. Food Chem 2010;119:298-305. https://doi.org/10.1016/j.foodchem.2009.06.032
  38. Quettier-Deleu C, Voiselle G, Fruchart JC, Duriez P, Teissier E, Bailleul F, Vasseur J, Trotin F. Hawthorn extracts inhibit LDL oxidation. Pharmazie 2003;58:577-81.
  39. Schreckinger ME, Wang J, Yousef G, Lila MA, de Mejia EG. Antioxidant capacity and in vitro inhibition of adipogenesis and inflammation by phenolic extracts of Vaccinium floribundum and Aristotelia chilensis. J Agric Food Chem 2010;58:8966-76. https://doi.org/10.1021/jf100975m
  40. Zern TL, Fernandez ML. Cardioprotective effects of dietary polyphenols. J Nutr 2005;135:2291-4. https://doi.org/10.1093/jn/135.10.2291
  41. Goni I, Martín N, Saura-Calixto F. In vitro digestibility and intestinal fermentation of grape seed and peel. Food Chem 2005; 90:281-6. https://doi.org/10.1016/j.foodchem.2004.03.057
  42. Chandalia M, Garg A, Lutjohann D, von Bergmann K, Grundy SM, Brinkley LJ. Beneficial effects of high dietary fiber intake in patients with type 2 diabetes mellitus. N Engl J Med 2000;342:1392-8. https://doi.org/10.1056/NEJM200005113421903
  43. Rodriguez-Cabezas ME, Galvez J, Lorente MD, Concha A, Camuesco D, Azzouz S, Osuna A, Redondo L, Zarzuelo A. Dietary fiber down-regulates colonic tumor necrosis factor alpha and nitric oxide production in trinitrobenzenesulfonic acid-induced colitic rats. J Nutr 2002;132:3263-71. https://doi.org/10.1093/jn/132.11.3263
  44. Ciaccio M, Valenza M, Tesoriere L, Bongiorno A, Albiero R, Livrea MA. Vitamin A inhibits doxorubicin-induced membrane lipid peroxidation in rat tissues in vivo. Arch Biochem Biophys 1993;302:103-8. https://doi.org/10.1006/abbi.1993.1186
  45. van Dam B, van Hinsbergh VW, Stehouwer CD, Versteilen A, Dekker H, Buytenhek R, Princen HM, Schalkwijk CG. Vitamin E inhibits lipid peroxidation-induced adhesion molecule expression in endothelial cells and decreases soluble cell adhesion molecules in healthy subjects. Cardiovasc Res 2003;57:563-71. https://doi.org/10.1016/S0008-6363(02)00699-5
  46. Frank J, Budek A, Lundh T, Parker RS, Swanson JE, Lourenco CF, Gago B, Laranjinha J, Vessby B, Kamal-Eldin A. Dietary flavonoids with a catechol structure increase alpha-tocopherol in rats and protect the vitamin from oxidation in vitro. J Lipid Res 2006;47:2718-25. https://doi.org/10.1194/jlr.M600291-JLR200
  47. Wie M, Sung J, Choi Y, Kim Y, Jeong HS, Lee J. Tocopherols and tocotrienols in grape seeds from 14 cultivars grown in Korea. Eur J Lipid Sci Technol 2009;111:1255-8. https://doi.org/10.1002/ejlt.200900058
  48. Sies H, Stahl W. Vitamins E and C, beta-carotene, and other carotenoids as antioxidants. Am J Clin Nutr 1995;62:1315S- 1321S. https://doi.org/10.1093/ajcn/62.6.1315S

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