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Effects of 4-tert-octylphenol on glutathione-related antioxidant status in olive flounder Paralichthys olivaceus

  • Jee, Jung-Hoon (Ministry of Oceans and Fisheries) ;
  • Keum, Yoo-Hwa (Ministry of Oceans and Fisheries) ;
  • Bae, Jun Sung (Department of Aquatic Life Medicine, Kunsan National University) ;
  • Lee, Chae Won (Department of Aquatic Life Medicine, Kunsan National University) ;
  • Yang, Chan Yeong (Department of Aquatic Life Medicine, Kunsan National University) ;
  • Choi, Sang-Hoon (Department of Aquatic Life Medicine, Kunsan National University) ;
  • Kang, Ju-Chan (Department of Aquatic Life Medicine, Pukyong National University) ;
  • Park, Kwan Ha (Department of Aquatic Life Medicine, Kunsan National University)
  • Received : 2019.11.19
  • Accepted : 2019.12.03
  • Published : 2019.12.31

Abstract

Effects on glutathione-related antioxidant parameters were examined after a chronic exposure of olive flounder, Paralichthys olivaceus to dietary 4-tert-octylphenol (4-tert-OP). Fish were fed diets containing 4-tert-OP at 0, 1, 5 and 10 mg/kg diet for 6 weeks. Antioxidant parameters examined were reduced glutathione (GSH) contents and enzyme activities of glutathione reductase (GR), glutathione S-transferase (GST) and glutathione peroxidase (GPx) in tissue homogenates of the liver, kidney and gill. It was observed that all parameters examined increased although there were some differences in dose responses and temporal patterns in the increase. GSH contents increased after exposure to 4-tert-OP in the three organs examined. However, the GSH increase was evident only after 4 weeks in the liver whereas it was elevated after 2 weeks in the kidney and gill. GR activity exhibited a significant increase in response to 4-tert-OP at 1 mg/kg in all three organs, however, its activity returned to control levels when exposed to 5 and 10 mg/kg. Hepatic GST activity showed an earlier increase at week 2 in contrast to the kidney and gill where they increased after 4 weeks of 4-tert-OP exposure. Temporal patterns in GPx activity changes to 4-tert-OP exposure were dissimilar among the organs: hepatic activity increased from week 2 through week 6; renal activity increased transiently at week 2; gill levels were higher through weeks 4 - 6. The results suggest that elevation of several GSH-related antioxidant parameters can be considered as evaluation criteria for 4-tert-OP-induced oxidative stress in a fish.

Keywords

References

  1. Aydogan, M., Korkmaz, A., Barlas, N. and Kolankaya, D.: The effect of vitamin C on bisphenol A, nonylphenol and octylphenol induced brain damages of male rats. Toxicology 249: 35-39, 2008. https://doi.org/10.1016/j.tox.2008.04.002
  2. Behne, D. and Wolters, W.: Distribution of selenium and glutathione peroxidase in the rat. J. Nutr. 113: 456-461, 1983. https://doi.org/10.1093/jn/113.2.456
  3. Beresford, N., Routledge, E. J., Harris, C. A. and Sumpter, J. P.: Issues arising when interpreting results from an in vitro assay for estrogenic activity. Toxicol. Appl. Pharmacol. 162:22-33, 2000. https://doi.org/10.1006/taap.1999.8817
  4. Beutler, E.: Red cell metabolism. In: A Manual of Biochemical Methods, 3rd eds. Grune and Stratton, Orlando, FL, USA. p. 133, 1984.
  5. Bradford, M. M.: A rapid sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254, 1976. https://doi.org/10.1006/abio.1976.9999
  6. Chen, G., Xu, Y., Xu, L., Zheng, Y., Schramm, K. W. and Kettrup, A.: Influence of dioxin and metal-contaminated sediment on phase I and II biotransformation enzymes in silver crucian carp. Ecotoxicol. Environ. Saf. 40:234-238, 1998. https://doi.org/10.1006/eesa.1997.1611
  7. Davies, P. E.: The toxicology and metabolism of chlorothalonil in fish III: metabolism, enzymatics and detoxication in Salmo spp. and Galaxias spp. Aquat. Toxicol. 7: 277-299, 1985. https://doi.org/10.1016/0166-445x(85)90045-1
  8. Di Giulio, R. T., Habig, C. and Gallagher, E. P.: Effects of Black Rock Harbor sediments on indices of biotransformation, oxidative stress, and DNA integrity in channel catfish. Aquat. Toxicol. 26:1-22, 1993. https://doi.org/10.1016/0166-445X(93)90002-I
  9. Dierickx, P. J.: Glutathione S-transferase in aquatic macro-invertebrates and its interaction with different organic micropollutants. Sci. Total Environ. 40:93-102, 1984. https://doi.org/10.1016/0048-9697(84)90344-9
  10. Duncan, D. B.: Multiple-range and multiple F tests. Biometrics 11:1-42, 1955. https://doi.org/10.2307/3001478
  11. Fair, P. H.: Interaction of benzo(a)pyrene and cadmium on glutathione S-transferase and benzo(a)pyrene hydroxylase in the black sea bass Centropristis striata. Arch. Environ. Contam. Toxicol. 12:195-201, 1986. https://doi.org/10.1007/BF01059581
  12. Ferguson, P. L., Iden, C. R. and Brownawell, B. J.: Analysis of alkylphenol ethoxylate metabolites in the aquatic environment using liquid chromatographyelectrospray mass spectrometry. Anal. Chem. 72:4322-4330, 2000. https://doi.org/10.1021/ac000342n
  13. Filho, D. W.: Fish antioxidant defenses and comparative approach. Braz. J. Med. Biol. Res. 29:1735-1742, 1996.
  14. Folmar, L. C., Gardner, G. R., Schreibman, M. P., Magliulo-Cepriano, L., Mills, L. J., Zaroogian, G., Gutijahr-Gobell, R., Haebler, R., Horowitz, D.B. and Denslow, N. D.: Vitellogenin-induced pathology in male summer flounder (Paralichthys dentatus). Aquat. Toxicol. 51:431-441, 2001. https://doi.org/10.1016/S0166-445X(00)00121-1
  15. Forman, H.J., Zhang, H. and Rinna, A.: Glutathione: overview of its protective roles, measurements, and biosynthesis. Mol. Aspects Med. 30:1-12, 2009. https://doi.org/10.1016/j.mam.2008.08.006
  16. Gadagbui, B. K. M. and Goksoyr, A.: CYP1A and other biomarker responses to effluents from a textile mill in the Volta River (Ghana) using caged tilapia (Oreochromis niloticus) and sediment-exposed mudfish (Clarias anguillaris). Biomarkers 1:252-261, 1996. https://doi.org/10.3109/13547509609079365
  17. Gallagher, E. P., Canada, A. T. and Di Giulio, R. T.: The protective role of glutathione in chlorothalonilinduced toxicity to channel catfish. Aquat. Toxicol. 23:155-168, 1992. https://doi.org/10.1016/0166-445X(92)90049-S
  18. Goldberg, D. M. and Sparner, R. J.: Glutathione reductase. In: Bergmeyer, H.U. (eds.), Methods of Enzymatic Analysis, vol. 3. Verlag-Chemie, Weinheim, Germany, pp. 258-265, 1987.
  19. Gray, M. A., Teather, K. L. and Metcalfe, C. D.: Reproductive success and behavior of Japanese medaka (Oryzias latipes) exposed to 4-tert-octylphenol. Environ. Toxicol. Chem. 18:2587-2594, 1999. https://doi.org/10.1897/1551-5028(1999)018<2587:RSABOJ>2.3.CO;2
  20. Habig, W. H., Pabst, M. J. and Jakoby, W. B.: Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249:7130-7139, 1974. https://doi.org/10.1016/S0021-9258(19)42083-8
  21. Halliwell, B. and Gutteridge, J. M. C. Free Radicals in Biology and Medicine. 3rd ed. Oxford University Press, New York, USA, 1999.
  22. Jobling, S., Sheahan, D., Osborne, J. A., Matthiessen, P. and Sumpter, J.: Inhibition of testicular growth in rainbow trout (Oncorhynchus mykiss) exposed to estrogenic alkylphenolic chemicals. Environ. Toxicol. Chem. 15:194-202, 1996. https://doi.org/10.1002/etc.5620150218
  23. Kim, K. B., Seo, K. W., Kim, Y. J., Park, M., Park and C. W., Kim, P. Y.: Estrogenic effects of phenolic compounds on glucose-6-phosphate dehydrogenase in MCF-7 cells and uterine glutathione peroxidase in rats. Chemosphere 50:1167-1173, 2003 https://doi.org/10.1016/S0045-6535(02)00628-8
  24. Lackner, R.: "Oxidative Stress" in fish by environmental pollutants. In: T. Braunbeck, D.E. Hinton,, B. Streit (eds.), Fish Ecotoxicology, Birkhauser Verlag, Basel, Switzerland, pp. 203-224, 1998.
  25. Livingstone, D. R.: Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar. Poll. Bull. 42:656-666, 2001. https://doi.org/10.1016/S0025-326X(01)00060-1
  26. Masden L., Korsgaard B. and Bjerregaard P.: Estrogenic effects in flounder Platichthys flesus orally exposed to 4-tert-octylphenol. Aquat. Toxicol. 64:393-405, 2003. https://doi.org/10.1016/S0166-445X(03)00106-1
  27. Meesters, R. J. and Schroder, H. F.: Simultaneous determination of 4-nonylphenol and bisphenol A in sewage sludge. Anal. Chem. 74:3566-3574, 2002. https://doi.org/10.1021/ac011258q
  28. Naylor, C. G., Mieure, J. P., Adams, W. J., Weeks, J. A., Castaldi, F. J., Ogle, L. D. and Romano, R. R.: Alkylphenol ethoxylates in the environment. J. Am. Oil Chem. Soc. 69:695-705, 1992. https://doi.org/10.1007/BF02635812
  29. Otto, D. M. and Moon, T. W.: 3,3',4,4'-tetrachlorobiphenyl effects on antioxidant enzymes and glutathione status in different tissues of rainbow trout. Pharmacol. Toxicol. 77:281-287, 1995. https://doi.org/10.1111/j.1600-0773.1995.tb01028.x
  30. Ou, P., Nourooz-Zadeh, J., Tritschler, H. J. and Wolff, S.: Activation of aldose reductase in rat lens and metal-ion chelation by aldose reductase inhibitors and lipoic acid. Free Rad. Res. 25: 337-346, 1996. https://doi.org/10.3109/10715769609149056
  31. Pesonen, M., Andersson, T. B., Sorri, V. and Korkalainen, M.: Biochemical and ultrastructural changes in the liver of Baltic salmon sac fry suffering from high mortality (M74). Environ. Toxicol. Chem. 18: 1007-1013, 1999. https://doi.org/10.1897/1551-5028(1999)018<1007:BAUCIT>2.3.CO;2
  32. Petrovic, M., Lacorte, S., Viana, P. and Barcelo, D. : Pressurized liquid extraction followed by liquid chromatography-mass spectrometry for the determination of alkylphenolic compounds in river sediment. J. Chromatogr. A 959:15-23, 2002.
  33. Ross, D., Thor, H., Threadgill, M., Sandy, M., Smith, M., Moldeus P. and Orrenius, S.: The role of oxidative processes in the cytotoxicity of substituted 1,4-naphthoquinones in isolated hepatocytes. Arch. Biochem. Biophys. 248:460-466, 1986. https://doi.org/10.1016/0003-9861(86)90499-6
  34. Roy, S., Lindstrom-Seppa, P., Huuskonen, S. and Hanninen, O.: Responses on biotransformation and antioxidant enzymes in Lemna minor and Oncorhynchus mykiss simultaneously to hexaclorobenzene. Chemosphere 30:1489-1498. https://doi.org/10.1016/0045-6535(95)00043-8
  35. Rudneva-Titova, I. I. and Zherko, N. V.: Effects of polychlorinated biphenyls on the activity of anti-oxidant enzymes and lipid peroxidation in muscle and liver of two Black Sea fish species. Biochemistry 59:25-31, 1994.
  36. Staniszewska, M., Falkowska, L., Grabowski, P., Kwaśniak, J, Mudrak-Cegiolka, S., Reindl, A.R., Sokolowski, A., Szumilo, E. and Zgrundo, A.: Bisphenol A, 4-tert-octylphenol, and 4-nonylphenol in the Gulf of Gdańsk (Southern Baltic). Arch. Environ. Contam. Toxicol. 67:335-347, 2014. https://doi.org/10.1007/s00244-014-0023-9
  37. Stein, J, E., Collier, T. K., Reichert, W. L., Casillas, E., Hom, T. and Varanasi, U.: Bioindicators of contaminant exposure and sublethal effects: studies with benthic fish in Puget Sound, Washington. Environ. Toxicol. Chem. 11:701-714, 1992. https://doi.org/10.1897/1552-8618(1992)11[701:BOCEAS]2.0.CO;2
  38. Stenersen, J., Kobro, S., Bjerke, M. and Arend, U.: Glutathione transferases in aquatic and terrestrial animals from nine phyla. Comp. Biochem. Physiol. C 86: 73-82, 1987.
  39. Stephensen, E., Svavarsson, J., Sturve, J., Ericson, G., Adolfsson-Erici, M. and Forlin, L.: Biochemical indicators of pollution exposure in shorthorn sculpin (Myoxocephalus scorpius), caught in four harbours on the southwest coast of Iceland. Aquat. Toxicol. 48:431-442, 2000. https://doi.org/10.1016/S0166-445X(99)00062-4
  40. Talmage, S.: Environmental and human safety of major surfactants: alcohol ethoxylates and alkylphenol ethoxylates. Lewis Publishers, Boca Raton, FL, USA, 1994.
  41. Tjarnlund, U., Ericson, G., Lindesjoo, E., Petterson, I., Åkerman, G. and Balk, L.: Further studies of the effects of exhaust from two-stroke outboard motors on fish. Mar. Environ. Res. 42:267-271, 1996. https://doi.org/10.1016/0141-1136(95)00053-4
  42. Toomey, B. H., Monteverdi, G. H. and Di Giulio, R. T.: Octylphenol induces vitellogenin production and cell death in fish hepatocytes. Environ. Toxicol. Chem. 18:734-739, 1999. https://doi.org/10.1897/1551-5028(1999)018<0734:OIVPAC>2.3.CO;2
  43. Yu, I. T., Rhee, J. S., Raisuddin, S. and Lee, J. S.: Characterization of the glutathione S-transferase-Mu (GSTM) gene sequence and its expression in the hemaphroditic fish, Krytolebias marmoratus as a function of development, gender type and chemical exposure. Chem. Biol. Interact. 174:118-125, 2008. https://doi.org/10.1016/j.cbi.2008.05.011
  44. Vandeputte, C., Guizon, I., Genestie-Denis, I., Vannier, B. and Lorenzon, G.: A microtiter plate assay for total glutathione and glutathione disulfide contents in cultured/isolated cells: performance study of a new miniaturized protocol. Cell Biol. Toxicol. 10:415-421, 1994. https://doi.org/10.1007/BF00755791
  45. White, R., Jobling, S., Hoare, S. A., Sumpter, J. P. and Parker, M. G.: Environmentally persistent alkylphenolic compounds are estrogenic. Endocrinology 135:175-182, 1994. https://doi.org/10.1210/en.135.1.175
  46. Winston, G.W.: Oxidants and antioxidants in aquatic animals. Comp. Biochem. Physiol. C 100:173-176, 1991. https://doi.org/10.1016/0742-8413(91)90148-M
  47. Winston, G. W. and Di Giulio, R. T.: Prooxidant and antioxidant mechanisms in aquatic organisms. Aquat. Toxicol. 19:137-161, 1991. https://doi.org/10.1016/0166-445X(91)90033-6
  48. Yoshida, M., Katsuda, S., Takenaka, A., Watanabe, G., Taya, K. and Maekawa, A.: Effects of neonatal exposure to a high-dose p-tert-octylphenol on the male reproductive tract in rats. Toxicol. Lett. 121:21-33, 2001. https://doi.org/10.1016/s0378-4274(01)00311-3