Nutrition Research and Practice

The Korean Nutrition Society (한국영양학회)
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Lycopene supplementation suppresses oxidative stress induced by a high fat diet in gerbils

  • Received : 2012.09.17
  • Accepted : 2012.12.03
  • Published : 2013.02.01
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Abstract

The effect of lycopene supplementation on the antioxidant system was investigated by analyzing lipid peroxide levels, glutathione contents, and antioxidant enzyme activities in Mongolian gerbils fed a high fat diet. Gerbils were fed on each experimental diet for 6 weeks; normal diet (NC), normal diet with 0.05% lycopene (NL), high fat diet (HF), and a high fat diet with 0.05% lycopene (HFL). Dietary supplementation of lycopene increased hepatic lycopene level in gerbils fed a normal or high fat diet (P < 0.05). Liver and erythrocyte concentrations of lipid peroxide increased in gerbils fed a high fat diet, whereas lycopene supplementation decreased liver and erythrocyte concentrations of lipid peroxide (P < 0.05). Hepatic total glutathione content was higher in the NL group than that in the NC group (P < 0.05). Total antioxidant status in plasma increased following lycopene supplementation compared with that of the non-lycopene supplemented groups (P < 0.05). Hepatic catalase activity increased following dietary lycopene supplementation (P < 0.05). Superoxide dismutase activity in liver remained unchanged with lycopene supplementation, but erythrocyte superoxide dismutase activity increased in NL group compared with NC group (P < 0.05). Glutathione-S-transferase activity increased in the NL group compared to NC group (P < 0.05). Liver and erythrocyte glutathione peroxidase activity increased significantly in the NL group compared to that in the HF group (P < 0.05). Liver glutathione reductase activity was higher in the NL group than that in the NC group (P < 0.05). These results suggest that lycopene supplementation may be efficient for preventing chronic diseases induced by oxidative stress related to high fat diet.

Keywords

References

  1. Halliwell B. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 2006;141: 312-22. https://doi.org/10.1104/pp.106.077073
  2. 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
  3. Spector A. Review: oxidative stress and disease. J Ocul Pharmacol Ther 2000;16:193-201. https://doi.org/10.1089/jop.2000.16.193
  4. Rudich A, Kanety H, Bashan N. Adipose stress-sensing kinases: linking obesity to malfunction. Trends Endocrinol Metab 2007; 18:291-9. https://doi.org/10.1016/j.tem.2007.08.006
  5. Blokhina O, Virolainen E, Fagerstedt KV. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 2003;91 Spec No:179-94. https://doi.org/10.1093/aob/mcf118
  6. Martinez A, Rodriguez-Girones MA, Barbosa A, Costas M. Donator acceptor map for carotenoids, melatonin and vitamins. J Phys Chem A 2008;112:9037-42. https://doi.org/10.1021/jp803218e
  7. Lauretani F, Semba RD, Dayhoff-Brannigan M, Corsi AM, Di Iorio A, Buiatti E, Bandinelli S, Guralnik JM, Ferrucci L. Low total plasma carotenoids are independent predictors of mortality among older persons: the InCHIANTI study. Eur J Nutr 2008; 47:335-40. https://doi.org/10.1007/s00394-008-0732-9
  8. Omoni AO, Aluko RE. The anti-carcinogenic and anti-atherogenic effects of lycopene: a review. Trends Food Sci Technol 2005;16:344-50. https://doi.org/10.1016/j.tifs.2005.02.002
  9. Ellinger S, Ellinger J, Müller SC, Stehle P. Tomatoes and lycopene in prevention and therapy--is there an evidence for prostate diseases? Aktuelle Urol 2009;40:37-43. https://doi.org/10.1055/s-2008-1077031
  10. Amin AR, Kucuk O, Khuri FR, Shin DM. Perspectives for cancer prevention with natural compounds. J Clin Oncol 2009;27: 2712-25. https://doi.org/10.1200/JCO.2008.20.6235
  11. Gupta SK, Trivedi D, Srivastava S, Joshi S, Halder N, Verma SD. Lycopene attenuates oxidative stress induced experimental cataract development: an in vitro and in vivo study. Nutrition 2003;19:794-9. https://doi.org/10.1016/S0899-9007(03)00140-0
  12. 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
  13. Castenmiller JJ, West CE. Bioavailability and bioconversion of carotenoids. Annu Rev Nutr 1998;18:19-38. https://doi.org/10.1146/annurev.nutr.18.1.19
  14. Lee CM, Lederman JD, Hofmann NE, Erdman JW. The Mongolian gerbil (Meriones unguiculatus) is an appropriate animal model for evaluation of the conversion of $\beta$-carotene to vitamin A. J Nutr 1998;128:280-6. https://doi.org/10.1093/jn/128.2.280
  15. Huang CS, Chuang CH, Hu ML. Effects of lycopene supplementation on plasma and tissue lycopene levels in various rodent strains. Int J Vitam Nutr Res 2006;76:377-84. https://doi.org/10.1024/0300-9831.76.6.377
  16. Boileau TW, Clinton SK, Erdman JW Jr. Tissue lycopene concentrations and isomer patterns are affected by androgen status and dietary lycopene concentration in male F344 rats. J Nutr 2000;130:1613-8. https://doi.org/10.1093/jn/130.6.1613
  17. Jain CK, Agarwal S, Rao AV. The effect of dietary lycopene on bioavailability, tissue distribution, in vivo antioxidant properties and colonic preneoplasia in rats. Nutr Res 1999;19:1383-91. https://doi.org/10.1016/S0271-5317(99)00095-0
  18. Hogeboom GH. [3] Fractionation of cell components of animal tissues. Methods Enzymol 1955;1:16-9. https://doi.org/10.1016/0076-6879(55)01007-0
  19. Miller KW, Lorr NA, Yang CS. Simultaneous determination of plasma retinol, $\alpha$-tocopherol, lycopene, $\alpha$-carotene, and $\beta$-carotene by high-performance liquid chromatography. Anal Biochem 1984;138:340-5. https://doi.org/10.1016/0003-2697(84)90819-4
  20. 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
  21. Aebi H. Catalase. In: Bergmeyer HU, Gawehn K, editors. Methods of Enzymatic Analysis. 2nd ed. New York: Academic Press; 1974. p.673-89.
  22. 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
  23. Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967;70:158-69.
  24. 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
  25. Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 1974;249:7130-9.
  26. Rao AV. Lycopene, tomatoes, and the prevention of coronary heart disease. Exp Biol Med (Maywood) 2002;227:908-13. https://doi.org/10.1177/153537020222701011
  27. Agarwal S, Rao AV. Tomato lycopene and its role in human health and chronic diseases. CMAJ 2000;163:739-44.
  28. Mackinnon ES, Rao AV, Josse RG, Rao LG. Supplementation with the antioxidant lycopene significantly decreases oxidative stress parameters and the bone resorption marker N-telopeptide of type I collagen in postmenopausal women. Osteoporos Int 2011;22:1091-101. https://doi.org/10.1007/s00198-010-1308-0
  29. Agarwal S, Rao AV. Tomato lycopene and low density lipoprotein oxidation: a human dietary intervention study. Lipids 1998;33: 981-4. https://doi.org/10.1007/s11745-998-0295-6
  30. Kravchenko LV, Morozov SV, Beketova NA, Deryagina VP, Avren'eva LI, Tutel'yan VA. Antioxidant status of rats receiving lycopene in different doses. Bull Exp Biol Med 2003;135:353-7. https://doi.org/10.1023/A:1024608730471
  31. Gitenay D, Lyan B, Rambeau M, Mazur A, Rock E. Comparison of lycopene and tomato effects on biomarkers of oxidative stress in vitamin E deficient rats. Eur J Nutr 2007;46:468-75. https://doi.org/10.1007/s00394-007-0687-2
  32. Tso P, Lee T, DeMichele SJ. Randomized structured triglycerides increase lymphatic absorption of tocopherol and retinol compared with the equivalent physical mixture in a rat model of fat malabsorption. J Nutr 2001;131:2157-63. https://doi.org/10.1093/jn/131.8.2157
  33. Lee A, Thurnham DI, Chopra M. Consumption of tomato products with olive oil but not sunflower oil increases the antioxidant activity of plasma. Free Radic Biol Med 2000;29:1051-5. https://doi.org/10.1016/S0891-5849(00)00440-8
  34. Unlu NZ, Bohn T, Clinton SK, Schwartz SJ. Carotenoid absorption from salad and salsa by humans is enhanced by the addition of avocado or avocado oil. J Nutr 2005;135:431-6. https://doi.org/10.1093/jn/135.3.431
  35. Requena JR, Fu MX, Ahmed MU, Jenkins AJ, Lyons TJ, Thorpe SR. Lipoxidation products as biomarkers of oxidative damage to proteins during lipid peroxidation reactions. Nephrol Dial Transplant 1996;11 Suppl 5:48-53.
  36. Hegsted DM, Gallagher A. Dietary fat and cholesterol and serum cholesterol in the gerbil. J Lipid Res 1967;8:210-4.
  37. Bahcecioglu IH, Kuzu N, Metin K, Ozercan IH, Ustündag B, Sahin K, Kucuk O. Lycopene prevents development of steatohepatitis in experimental nonalcoholic steatohepatitis model induced by high-fat diet. Vet Med Int 2010;2010. pii: 262179.
  38. Ono H, Sakamoto A, Sakura N. Plasma total glutathione concentrations in healthy pediatric and adult subjects. Clin Chim Acta 2001;312:227-9. https://doi.org/10.1016/S0009-8981(01)00596-4
  39. Paolicchi A, Dominici S, Pieri L, Maellaro E, Pompella A. Glutathione catabolism as a signaling mechanism. Biochem Pharmacol 2002;64:1027-35. https://doi.org/10.1016/S0006-2952(02)01173-5
  40. Hsu CL, Yen GC. Effect of gallic acid on high fat diet-induced dyslipidaemia, hepatosteatosis and oxidative stress in rats. Br J Nutr 2007;98:727-35.
  41. Anderson EJ, Lustig ME, Boyle KE, Woodlief TL, Kane DA, Lin CT, Price JW 3rd, Kang L, Rabinovitch PS, Szeto HH, Houmard JA, Cortright RN, Wasserman DH, Neufer PD. Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest 2009;119:573-81. https://doi.org/10.1172/JCI37048
  42. Leal M, Shimada A, Ruiz F, Gonzalez de Mejia E. Effect of lycopene on lipid peroxidation and glutathione-dependent enzymes induced by T-2 toxin in vivo. Toxicol Lett 1999;109:1-10.
  43. Moreira EA, Fagundes RL, Filho DW, Neves D, Sell F, Bellisle F, Kupek E. Effects of diet energy level and tomato powder consumption on antioxidant status in rats. Clin Nutr 2005;24: 1038-46. https://doi.org/10.1016/j.clnu.2005.08.005
  44. Kumar P, Kumar A. Effect of lycopene and epigallocatechin- 3-gallate against 3-nitropropionic acid induced cognitive dysfunction and glutathione depletion in rat: a novel nitric oxide mechanism. Food Chem Toxicol 2009;47:2522-30. https://doi.org/10.1016/j.fct.2009.07.011
  45. Hsu CL, Wu CH, Huang SL, Yen GC. Phenolic compounds rutin and o-coumaric acid ameliorate obesity induced by high-fat diet in rats. J Agric Food Chem 2009;57:425-31. https://doi.org/10.1021/jf802715t
  46. 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
  47. Atessahin A, Yilmaz S, Karahan I, Ceribasi AO, Karaoglu A. Effects of lycopene against cisplatin-induced nephrotoxicity and oxidative stress in rats. Toxicology 2005;212:116-23. https://doi.org/10.1016/j.tox.2005.04.016

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