DOI QR코드

DOI QR Code

Dual effects of a mixture of grape pomace (Campbell Early) and Omija fruit ethanol extracts on lipid metabolism and the antioxidant defense system in diet-induced obese mice

  • Han, Hye Jin (Department of Food Science and Nutrition, Kyungpook National University) ;
  • Jung, Un Ju (Department of Food Science and Nutrition, Kyungpook National University) ;
  • Kim, Hye-Jin (Food R&D, CJ Cheiljedang Corp.) ;
  • Moon, Byoung Seok (Food R&D, CJ Cheiljedang Corp.) ;
  • Cho, Su-Jung (Department of Food Science and Nutrition, Kyungpook National University) ;
  • Park, Yong Bok (School of Life Science & Biotechnology, Kyungpook National University) ;
  • Lee, Dong Gun (School of Life Science & Biotechnology, Kyungpook National University) ;
  • Choi, Myung-Sook (Department of Food Science and Nutrition, Kyungpook National University)
  • Received : 2014.09.18
  • Accepted : 2015.02.05
  • Published : 2015.06.01

Abstract

BACKGROUND/OBJECTIVES: We investigated the effects of a combination of grape pomace (Vitis labrusca, Campbell Early) and Omija fruit (Schizandra chinensis, Baillon) ethanol extracts on lipid metabolism and antioxidant defense system in diet-induced obese mice. MATERIALS/METHODS: Forty male C57BL/6J mice were divided into four groups and fed high-fat diet (control group, CON) or high-fat diet added 0.5% grape pomace extract (GPE), 0.05% Omija fruit extract (OFE) or 0.5% GPE plus 0.05% OFE (GPE+OFE) for 12 weeks. RESULTS: In contrast to the GPE- or OFE-supplemented groups, the GPE+OFE group showed significantly lower body weight and white adipose tissue weights than the CON group. Moreover, GPE+OFE supplementation significantly decreased plasma total cholesterol and increased the plasma HDL-cholesterol/total-cholesterol ratio (HTR) compared to the control diet. The hepatic triglyceride level was significantly lower in the GPE+OFE and GPE groups by increasing ${\beta}$-oxidation and decreasing lipogenic enzyme compared to the CON group. Furthermore, GPE+OFE supplementation significantly increased antioxidant enzyme activities with a simultaneous decrease in liver $H_2O_2$ content compared to the control diet. CONCLUSIONS: Together our results suggest that supplementation with the GPE+OFE mixture may be more effective in improving adiposity, lipid metabolism and oxidative stress in high-fat diet-fed mice than those with GPE and OFE alone.

Keywords

References

  1. Kopelman PG. Obesity as a medical problem. Nature 2000;404: 635-43. https://doi.org/10.1038/35007508
  2. Fabbrini E, Sullivan S, Klein S. Obesity and nonalcoholic fatty liver disease: biochemical, metabolic, and clinical implications. Hepatology 2010;51:679-89. https://doi.org/10.1002/hep.23280
  3. Bray GA, Tartaglia LA. Medicinal strategies in the treatment of obesity. Nature 2000;404:672-7. https://doi.org/10.1038/35007544
  4. Yun JW. Possible anti-obesity therapeutics from nature--a review. Phytochemistry 2010;71:1625-41. https://doi.org/10.1016/j.phytochem.2010.07.011
  5. Liu RH. Health benefits of fruit and vegetables are from additive and synergistic combinations of phytochemicals. Am J Clin Nutr 2003;78:517S-520S. https://doi.org/10.1093/ajcn/78.3.517S
  6. Kota SK, Jammula S, Kota SK, Satya Krishna SV, Meher LK, Rao ES, Modi KD. Nutraceuticals in pathogenic obesity; striking the right balance between energy imbalance and inflammation. J Med Nutr Nutraceuticals 2012;1:63-76. https://doi.org/10.4103/2278-019X.101288
  7. Gehm BD, McAndrews JM, Chien PY, Jameson JL. Resveratrol, a polyphenolic compound found in grapes and wine, is an agonist for the estrogen receptor. Proc Natl Acad Sci USA 1997;94: 14138-43. https://doi.org/10.1073/pnas.94.25.14138
  8. Pastrana-Bonilla E, Akoh CC, Sellappan S, Krewer G. Phenolic content and antioxidant capacity of muscadine grapes. J Agric Food Chem 2003;51:5497-503. https://doi.org/10.1021/jf030113c
  9. Makris DP, Boskou G, Andrikopoulos NK, Kefalas P. Characterisation of certain major polyphenolic antioxidants in grape (Vitis vinifera cv. Roditis) stems by liquid chromatography-mass spectrometry. Eur Food Res Technol 2008;226:1075-9. https://doi.org/10.1007/s00217-007-0633-9
  10. Hogan S, Canning C, Sun S, Sun X, Zhou K. Effects of grape pomace antioxidant extract on oxidative stress and inflammation in diet induced obese mice. J Agric Food Chem 2010;58:11250-6. https://doi.org/10.1021/jf102759e
  11. Saunders RM. Monograph of Kadsura (Schisandraceae). Syst Bot Monogr 1998;54:1-106. https://doi.org/10.2307/25096646
  12. Lin Q, Duan L, Yao B. Notes on three species of the genus Kadsura Juss. (Schisandraceae). Acta Phytotaxonomica Sinica 2005;43:567-70. https://doi.org/10.1360/aps030102
  13. Zhang CL, He XL. Advances in research on Schisandra chinesis (Turcz.) Baill. J Baoding Teach Coll 2005;17:36-9.
  14. Kim SH, Joo MH, Yoo SH. Structural identification and antioxidant properties of major anthocyanin extracted from Omija (Schizandra chinensis) fruit. J Food Sci 2009;74:C134-40. https://doi.org/10.1111/j.1750-3841.2009.01049.x
  15. Guo LY, Hung TM, Bae KH, Shin EM, Zhou HY, Hong YN, Kang SS, Kim HP, Kim YS. Anti-inflammatory effects of schisandrin isolated from the fruit of Schisandra chinensis Baill. Eur J Pharmacol 2008;591:293-9. https://doi.org/10.1016/j.ejphar.2008.06.074
  16. Park HJ, Cho JY, Kim MK, Koh PO, Cho KW, Kim CH, Lee KS, Chung BY, Kim GS, Cho JH. Anti-obesity effect of Schisandra chinensis in 3T3-L1 cells and high fat diet-induced obese rats. Food Chem 2012;134:227-34. https://doi.org/10.1016/j.foodchem.2012.02.101
  17. Choi SY, Lee Y, Lee P, Kim KT. Comparison of the antioxidative effects and content of anthocyanin and phenolic compounds in different varieties of Vitis vinifera ethanol extract. J Food Sci Nutr 2011;16:24-8. https://doi.org/10.3746/jfn.2011.16.1.024
  18. Cho SJ, Jung UJ, Park HJ, Kim HJ, Park YB, Kim SR, Choi MS. Combined ethanol extract of grape pomace and omija fruit ameliorates adipogenesis, hepatic steatosis, and inflammation in dietinduced obese mice. Evid Based Complement Alternat Med 2013; 2013:212139.
  19. Cho SJ, Jung UJ, Choi MS. Differential effects of low-dose resveratrol on adiposity and hepatic steatosis in diet-induced obese mice. Br J Nutr 2012;108:2166-75. https://doi.org/10.1017/S0007114512000347
  20. Hulcher FH, Oleson WH. Simplified spectrophotometric assay for microsomal 3-hydroxy-3-methylglutaryl CoA reductase by measurement of coenzyme A. J Lipid Res 1973;14:625-31.
  21. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957;226:497-509.
  22. Ochoa S. Malic enzyme: malic enzymes from pigeon and wheat germ. Methods Enzymol 1995;1:323-6.
  23. Pitkanen E, Pitkanen O, Uotila L. Enzymatic determination of unbound D-mannose in serum. Eur J Clin Chem Clin Biochem 1997;35:761-6.
  24. Nepokroeff CM, Lakshmanan MR, Porter JW. Fatty-acid synthase from rat liver. Methods Enzymol 1975;35:37-44. https://doi.org/10.1016/0076-6879(75)35136-7
  25. Walton PA, Possmayer F. Mg2-dependent phosphatidate phosphohydrolase of rat lung: development of an assay employing a defined chemical substrate which reflects the phosphohydrolase activity measured using membrane-bound substrate. Anal Biochem 1985; 151:479-86. https://doi.org/10.1016/0003-2697(85)90208-8
  26. Lazarow PB. Assay of peroxisomal ${\beta}$-oxidation of fatty acids. Methods Enzymol 1981;72:315-9. https://doi.org/10.1016/S0076-6879(81)72021-4
  27. 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
  28. Aebi H. Catalase. In: Bergmeyer HU, Gawehn K, editors. Methods of Enzymatic Analysis. 2nd ed. Weinheim: Academic Press; 1974. p.673-84.
  29. Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967;70:158-69.
  30. Pinto RE, Bartley W. The effect of age and sex on glutathione reductase and glutathione peroxidase activities and on aerobic glutathione oxidation in rat liver homogenates. Biochem J 1969;112: 109-15. https://doi.org/10.1042/bj1120109
  31. Wolff SP. Ferrous ion oxidation in presence of ferric ion indicator xylenol orange for measurement of hydroperoxides. Methods Enzymol 1994;233:182-9. https://doi.org/10.1016/S0076-6879(94)33021-2
  32. Yunoki K, Sasaki G, Tokuji Y, Kinoshita M, Naito A, Aida K, Ohnishi M. Effect of dietary wine pomace extract and oleanolic acid on plasma lipids in rats fed high-fat diet and its DNA microarray analysis. J Agric Food Chem 2008;56:12052-8. https://doi.org/10.1021/jf8026217
  33. Khanal RC, Howard LR, Rogers TJ, Wilkes SE, Dhakal IB, Prior RL. Effect of feeding grape pomace on selected metabolic parameters associated with high fructose feeding in growing Sprague-Dawley rats. J Med Food 2011;14:1562-9. https://doi.org/10.1089/jmf.2010.0281
  34. Samra JS. Sir David Cuthbertson Medal Lecture. Regulation of lipid metabolism in adipose tissue. Proc Nutr Soc 2000;59:441-6. https://doi.org/10.1017/S0029665100000604
  35. Wanless IR, Lentz JS. Fatty liver hepatitis (steatohepatitis) and obesity: an autopsy study with analysis of risk factors. Hepatology 1990;12: 1106-10. https://doi.org/10.1002/hep.1840120505
  36. Brown CD, Higgins M, Donato KA, Rohde FC, Garrison R, Obarzanek E, Ernst ND, Horan M. Body mass index and the prevalence of hypertension and dyslipidemia. Obes Res 2000;8:605-19. https://doi.org/10.1038/oby.2000.79
  37. Lu W, Resnick HE, Jablonski KA, Jones KL, Jain AK, Howard WJ, Robbins DC, Howard BV. Non-HDL cholesterol as a predictor of cardiovascular disease in type 2 diabetes: the strong heart study. Diabetes Care 2003;26:16-23. https://doi.org/10.2337/diacare.26.1.16
  38. Loftus TM, Jaworsky DE, Frehywot GL, Townsend CA, Ronnett GV, Lane MD, Kuhajda FP. Reduced food intake and body weight in mice treated with fatty acid synthase inhibitors. Science 2000;288: 2379-81. https://doi.org/10.1126/science.288.5475.2379
  39. Park J, Rho HK, Kim KH, Choe SS, Lee YS, Kim JB. Overexpression of glucose-6-phosphate dehydrogenase is associated with lipid dysregulation and insulin resistance in obesity. Mol Cell Biol 2005; 25:5146-57. https://doi.org/10.1128/MCB.25.12.5146-5157.2005
  40. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, Nakayama O, Makishima M, Matsuda M, Shimomura I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 2004;114:1752-61. https://doi.org/10.1172/JCI21625
  41. Betteridge DJ. What is oxidative stress? Metabolism 2000;49:3-8.
  42. 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
  43. Kim JS, Choi SY. Physicochemical properties and antioxidative activities of omija (Schizandra chinensis Bailon). Korean J Food Nutr 2008;21:35-42.
  44. Tsuda T. Regulation of adipocyte function by anthocyanins; possibility of preventing the metabolic syndrome. J Agric Food Chem 2008;56:642-6. https://doi.org/10.1021/jf073113b
  45. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, Messadeq N, Milne J, Lambert P, Elliott P, Geny B, Laakso M, Puigserver P, Auwerx J. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-$1{\alpha}$. Cell 2006;127:1109-22. https://doi.org/10.1016/j.cell.2006.11.013
  46. Kim S, Jin Y, Choi Y, Park T. Resveratrol exerts anti-obesity effects via mechanisms involving down-regulation of adipogenic and inflammatory processes in mice. Biochem Pharmacol 2011;81: 1343-51. https://doi.org/10.1016/j.bcp.2011.03.012
  47. Cho SJ, Park HJ, Jung UJ, Kim HJ, Moon BS, Choi MS. The beneficial effects of combined grape pomace and omija fruit extracts on hyperglycemia, adiposity and hepatic steatosis in db/db mice: a comparison with major index compounds. Int J Mol Sci 2014;15: 17778-89. https://doi.org/10.3390/ijms151017778
  48. Drotman RB, Lawhorn GT. Serum enzymes as indicators of chemically induced liver damage. Drug Chem Toxicol 1978;1:163-71. https://doi.org/10.3109/01480547809034433

Cited by

  1. Anti-melanogenic effect of gomisin N from Schisandra chinensis (Turcz.) Baillon (Schisandraceae) in melanoma cells vol.40, pp.7, 2017, https://doi.org/10.1007/s12272-017-0903-4
  2. Assessment of the effect of grape seed cake inclusion in the diet of healthy fattening-finishing pigs pp.09312439, 2017, https://doi.org/10.1111/jpn.12697
  3. Dermal Papilla Cells Proliferation Constituent of Schisandra chinensis Fruits and Optimization Using Response Surface Methodology vol.46, pp.4, 2020, https://doi.org/10.15230/scsk.2020.46.4.415
  4. Dynamics of Body Composition Indices and Biochemical Parameters in Participants of Countermeasure-Free 21-Day “Dry” Immersion vol.47, pp.3, 2015, https://doi.org/10.1134/s0362119721030178
  5. Targeting interleukin‐β by plant‐derived natural products: Implications for the treatment of atherosclerotic cardiovascular disease vol.35, pp.10, 2015, https://doi.org/10.1002/ptr.7194
  6. New dibenzocyclooctadiene lignan from Schisandra chinensis (Turcz.) Baill. fruits vol.64, pp.1, 2015, https://doi.org/10.1186/s13765-021-00618-1