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Antioxidative effects of fermented sesame sauce against hydrogen peroxide-induced oxidative damage in LLC-PK1 porcine renal tubule cells

  • Received : 2013.07.26
  • Accepted : 2013.12.17
  • Published : 2014.04.01

Abstract

BACKGROUND/OBJECTIVES: This study was performed to investigate the in vitro antioxidant and cytoprotective effects of fermented sesame sauce (FSeS) against hydrogen peroxide ($H_2O_2$)-induced oxidative damage in renal proximal tubule LLC-PK1 cells. MATERIALS/METHODS: 1,1-diphenyl-2-picrylhydrazyl (DPPH), hydroxyl radical ($^{\bullet}OH$), and $H_2O_2$ scavenging assay was used to evaluate the in vitro antioxidant activity of FSeS. To investigate the cytoprotective effect of FSeS against $H_2O_2$-induced oxidative damage in LLC-PK1 cells, the cellular levels of reactive oxygen species (ROS), lipid peroxidation, and endogenous antioxidant enzymes including catalase (CAT), superoxide dismutase (SOD), and glutathione peroxidase (GSH-px) were measured. RESULTS: The ability of FSeS to scavenge DPPH, $^{\bullet}OH$ and $H_2O_2$ was greater than that of FSS and AHSS. FSeS also significantly inhibited $H_2O_2$-induced ($500{\mu}M$) oxidative damage in the LLC-PK1 cells compared to FSS and AHSS (P < 0.05). Following treatment with $100{\mu}g/mL$ of FSeS and FSS to prevent $H_2O_2$-induced oxidation, cell viability increased from 56.7% (control) to 83.7% and 75.6%, respectively. However, AHSS was not able to reduce $H_2O_2$-induced cell damage (viability of the AHSS-treated cells was 54.6%). FSeS more effectively suppressed $H_2O_2$-induced ROS generation and lipid peroxidation compared to FSS and AHSS (P < 0.05). Compared to the other sauces, FSeS also significantly increased cellular CAT, SOD, and GSH-px activities and mRNA expression (P < 0.05). CONCULUSIONS: These results from the present study suggest that FSeS is an effective radical scavenger and protects against $H_2O_2$-induced oxidative damage in LLC-PK1 cells by reducing ROS levels, inhibiting lipid peroxidation, and stimulating antioxidant enzyme activity.

References

  1. Long LH, Kwee DC, Halliwell B. The antioxidant activities of seasonings used in Asian cooking. Powerful antioxidant activity of dark soy sauce revealed using the ABTS assay. Free Radic Res 2000;32:181-6. https://doi.org/10.1080/10715760000300181
  2. Wang H, Jenner AM, Lee CY, Shui G, Tang SY, Whiteman M, Wenk MR, Halliwell B. The identification of antioxidants in dark soy sauce. Free Radic Res 2007;41:479-88. https://doi.org/10.1080/10715760601110871
  3. Yang B, Yang H, Li J, Li Z, Jiang Y. Amino acid composition, molecular weight distribution and antioxidant activity of protein hydrolysates of soy sauce lees. Food Chem 2011;124:551-5. https://doi.org/10.1016/j.foodchem.2010.06.069
  4. Benjamin H, Storkson J, Nagahara A, Pariza MW. Inhibition of benzo(a)pyrene-induced mouse forestomach neoplasia by dietary soy sauce. Cancer Res 1991;51:2940-2.
  5. Ito A, Watanabe H, Basaran N. Effects of soy products in reducing risk of spontaneous and neutron-induced liver-tumors in mice. Int J Oncol 1993;2:773-6.
  6. Nagahara A, Benjamin H, Storkson J, Krewson J, Sheng K, Liu W, Pariza MW. Inhibition of benzo[a]pyrene-induced mouse forestomach neoplasia by a principal flavor component of Japanese-style fermented soy sauce. Cancer Res 1992;52:1754-6.
  7. Kataoka S, Liu W, Albright K, Storkson J, Pariza M. Inhibition of benzo[a]pyrene-induced mouse forestomach neoplasia and reduction of H2O2 concentration in human polymorphonuclear leucocytes by flavour components of Japanese-style fermented soy sauce. Food Chem Toxicol 1997;35:449-57. https://doi.org/10.1016/S0278-6915(97)00009-4
  8. Ham SS, Kim SH, Yoo SJ, Oh HT, Choi HJ, Chung MJ. Biological acivities of soybean sauce (Kangjang) supplemented with deep sea water and sea tangle. Korean J Food Preserv 2008;15:274-9.
  9. Yoon KD, Kwon DJ, Hong SS, Kim SI, Chung KS. Inhibitory effect of soybean and fermented soybean products on the chemically induced mutagenesis. Korean J Appl Microbiol Bioeng 1996;24: 525-8.
  10. Namiki M. Nutraceutical functions of sesame: a review. Crit Rev Food Sci Nutr 2007;47:651-73. https://doi.org/10.1080/10408390600919114
  11. Habermeyer M, Guth S, Eisenbrand G. Identification of gaps in knowledge concerning toxicology of 3-MCPD and glycidol esters. Eur J Lipid Sci Technol 2011;113:314-8. https://doi.org/10.1002/ejlt.201000314
  12. Lynch BS, Bryant DW, Hook GJ, Nestmann ER, Munro IC. Carcinogenicity of monochloro-1,2-propanediol ($\alpha$-chlorohydrin, 3-MCPD). Int J Toxicol 1998;17:47-76. https://doi.org/10.1177/109158189801700307
  13. Salahudeen AK, Clark EC, Nath KA. Hydrogen peroxide-induced renal injury. A protective role for pyruvate in vitro and in vivo. J Clin Invest 1991;88:1886-93. https://doi.org/10.1172/JCI115511
  14. Small DM, Coombes JS, Bennett N, Johnson DW, Gobe GC. Oxidative stress, anti-oxidant therapies and chronic kidney disease. Nephrology (Carlton) 2012;17:311-21. https://doi.org/10.1111/j.1440-1797.2012.01572.x
  15. Salahudeen AK. Role of lipid peroxidation in H2O2-induced renal epithelial (LLC-PK1) cell injury. Am J Physiol 1995;268:F30-8. https://doi.org/10.1152/ajpcell.1995.268.1.C30
  16. Nath KA, Salahudeen AK. Autoxidation of cysteine generates hydrogen peroxide: cytotoxicity and attenuation by pyruvate. Am J Physiol 1993;264:F306-14.
  17. Perantoni A, Berman JJ. Properties of Wilms' tumor line (TuWi) and pig kidney line (LLC-PK1) typical of normal kidney tubular epithelium. In Vitro 1979;15:446-54. https://doi.org/10.1007/BF02618414
  18. Lobo V, Patil A, Phatak A, Chandra N. Free radicals, antioxidants and functional foods: Impact on human health. Pharmacogn Rev 2010;4:118-26. https://doi.org/10.4103/0973-7847.70902
  19. Singh D, Kaur R, Chander V, Chopra K. Antioxidants in the prevention of renal disease. J Med Food 2006;9:443-50. https://doi.org/10.1089/jmf.2006.9.443
  20. Hatano T, Kagawa H, Yasuhara T, Okuda T. Two new flavonoids and other constituents in licorice root: their relative astringency and radical scavenging effects. Chem Pharm Bull (Tokyo) 1988;36: 2090-7. https://doi.org/10.1248/cpb.36.2090
  21. Halliwell B, Gutteridge JM, Aruoma OI. The deoxyribose method: a simple "test-tube" assay for determination of rate constants for reactions of hydroxyl radicals. Anal Biochem 1987;165:215-9. https://doi.org/10.1016/0003-2697(87)90222-3
  22. Rosen GM, Rauckman EJ. Spin trapping of superoxide and hydroxyl radicals. Methods Enzymol 1984;105:198-209. https://doi.org/10.1016/S0076-6879(84)05026-6
  23. Fraga CG, Leibovitz BE, Tappel AL. Lipid peroxidation measured as thiobarbituric acid-reactive substances in tissue slices: characterization and comparison with homogenates and microsomes. Free Radic Biol Med 1988;4:155-61. https://doi.org/10.1016/0891-5849(88)90023-8
  24. Nelson DP, Kiesow LA. Enthalpy of decomposition of hydrogen peroxide by catalase at 25 degrees C (with molar extinction coefficients of H2O2 solutions in the UV). Anal Biochem 1972;49:474-8. https://doi.org/10.1016/0003-2697(72)90451-4
  25. 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
  26. Hafeman DG, Sunde RA, Hoekstra WG. Effect of dietary selenium on erythrocyte and liver glutathione peroxidase in the rat. J Nutr 1974;104:580-7. https://doi.org/10.1093/jn/104.5.580
  27. Esaki H, Onozaki H, Osawa T. Antioxidative activity of fermented soybean products. In: Huang MT, Osawa T, Ho CT, Rosen RT, editors. Food Phytochemicals for Cancer Prevention I. ACS Symposium Series. Vol. 546. Washington, D.C.: American Chemical Society; 1994. p.353-60.
  28. Chang TS, Ding HY, Tai SS, Wu CY. Metabolism of the soy isoflavones daidzein and genistein by fungi used in the preparation of various fermented soybean foods. Biosci Biotechnol Biochem 2007;71: 1330-3. https://doi.org/10.1271/bbb.60573
  29. Lee IH, Chou CC. Distribution profiles of isoflavone isomers in black bean kojis prepared with various filamentous fungi. J Agric Food Chem 2006;54:1309-14. https://doi.org/10.1021/jf058139m
  30. Katsuzaki H, Kawakishi S, Osawa T. Sesaminol glucosides in sesame seeds. Phytochemistry 1994;35:773-6. https://doi.org/10.1016/S0031-9422(00)90603-4
  31. Moazzami AA, Andersson RE, Kamal-Eldin A. HPLC analysis of sesaminol glucosides in sesame seeds. J Agric Food Chem 2006;54: 633-8. https://doi.org/10.1021/jf051541g
  32. Miyake Y, Fukumoto S, Okada M, Sakaida K, Nakamura Y, Osawa T. Antioxidative catechol lignans converted from sesamin and sesaminol triglucoside by culturing with Aspergillus. J Agric Food Chem 2005;53:22-7. https://doi.org/10.1021/jf048743h
  33. Song JL. Anticancer effects of fermented sesame sauce [doctor's thesis]. Busan: Pusan National University; 2012.
  34. Liu K. Soybeans as Functional Foods and Ingredients. Champaign (IL): AOCS Press; 2004.
  35. Dong J, Ramachandiran S, Tikoo K, Jia Z, Lau SS, Monks TJ. EGFR-independent activation of p38 MAPK and EGFR-dependent activation of ERK1/2 are required for ROS-induced renal cell death. Am J Physiol Renal Physiol 2004;287:F1049-58. https://doi.org/10.1152/ajprenal.00132.2004
  36. Khan SR. Hyperoxaluria-induced oxidative stress and antioxidants for renal protection. Urol Res 2005;33:349-57. https://doi.org/10.1007/s00240-005-0492-4
  37. Halliwell B. Antioxidants in human health and disease. Annu Rev Nutr 1996;16:33-50. https://doi.org/10.1146/annurev.nu.16.070196.000341
  38. Braughler JM, Pregenzer JF. The 21-aminosteroid inhibitors of lipid peroxidation: reactions with lipid peroxyl and phenoxy radicals. Free Radic Biol Med 1989;7:125-30. https://doi.org/10.1016/0891-5849(89)90003-8
  39. Sheridan AM, Fitzpatrick S, Wang C, Wheeler DC, Lieberthal W. Lipid peroxidation contributes to hydrogen peroxide induced cytotoxicity in renal epithelial cells. Kidney Int 1996;49:88-93. https://doi.org/10.1038/ki.1996.12
  40. Incani A, Deiana M, Corona G, Vafeiadou K, Vauzour D, Dessì MA, Spencer JP. Involvement of ERK, Akt and JNK signalling in H2O2-induced cell injury and protection by hydroxytyrosol and its metabolite homovanillic alcohol. Mol Nutr Food Res 2010;54:788-96.
  41. Hou RC, Huang HM, Tzen JT, Jeng KC. Protective effects of sesamin and sesamolin on hypoxic neuronal and PC12 cells. J Neurosci Res 2003;74:123-33. https://doi.org/10.1002/jnr.10749
  42. Kang MH, Naito M, Tsujihara N, Osawa T. Sesamolin inhibits lipid peroxidation in rat liver and kidney. J Nutr 1998;128:1018-22. https://doi.org/10.1093/jn/128.6.1018
  43. Sirato-Yasumoto S, Katsuta M, Okuyama Y, Takahashi Y, Ide T. Effect of sesame seeds rich in sesamin and sesamolin on fatty acid oxidation in rat liver. J Agric Food Chem 2001;49:2647-51. https://doi.org/10.1021/jf001362t
  44. Thamilselvan S, Byer KJ, Hackett RL, Khan SR. Free radical scavengers, catalase and superoxide dismutase provide protection from oxalate-associated injury to LLC-PK1 and MDCK cells. J Urol 2000; 164:224-9. https://doi.org/10.1016/S0022-5347(05)67499-X
  45. Abdollahi M, Ranjbar A, Shadnia S, Nikfar S, Rezaie A. Pesticides and oxidative stress: a review. Med Sci Monit 2004;10:RA141-7.
  46. Comporti M. Glutathione depleting agents and lipid peroxidation. Chem Phys Lipids 1987;45:143-69. https://doi.org/10.1016/0009-3084(87)90064-8
  47. Nabavi SM, Nabavi SF, Eslami S, Moghaddam AH. In vivo protective effects of quercetin against sodium fluoride-induced oxidative stress in the hepatic tissue. Food Chem 2012;132:931-5. https://doi.org/10.1016/j.foodchem.2011.11.070
  48. Sharma R, Yang Y, Sharma A, Awasthi S, Awasthi YC. Antioxidant role of glutathione S-transferases: protection against oxidant toxicity and regulation of stress-mediated apoptosis. Antioxid Redox Signal 2004;6:289-300. https://doi.org/10.1089/152308604322899350
  49. Yu MU, Yoo JM, Lee YS, Lee YM, Hong JT, Oh KW, Song S, Yun YP, Yoo HS, Oh S. Altered de novo sphingolipid biosynthesis is involved in the serum deprivation-induced cell death in LLC-PK1 cells. J Toxicol Environ Health A 2004;67:2085-94. https://doi.org/10.1080/15287390490515065

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