DOI QR코드

DOI QR Code

Alteration of hepatic anti-oxidant systems by 4-nonylphenol, a metabolite of alkylphenol polyethoxylate detergents, in Far Eastern catfish Silurus asotus

  • Park, Kwan Ha (Department of Aquatic Life Medicine, College of Ocean Science and Technology, Kunsan National University)
  • Received : 2015.04.23
  • Accepted : 2015.05.28
  • Published : 2015.01.01

Abstract

Objectives This study aimed to estimate the effects of 4-nonylphenol (NP), a ubiquitously present surfactant in aquatic environments, on the anti-oxidant systems of the liver in the Far Eastern catfish Silurus asotus. Methods Changes in biochemical parameters involved in glutathione (GSH)-related and other anti-oxidant systems were analyzed following 4 weeks of 4-NP administration (0.1 and 1.0 mg/kg diet) via a formulated diet to catfish. Results 4-NP exposure induced an elevation in hepatic lipid peroxide levels and an accompanying decrease in reduced state GSH after 2 weeks, suggesting pro-oxidant effects of the chemical in catfish. This oxidative stress was associated with an inhibition of the GSH-utilizing enzyme glutathione peroxidase at the same time point. This inhibition was restored after 4 weeks. The activities of other anti-oxidant enzymes, i.e., glutathione reductase, superoxide dismutase and catalase were increased after 4 weeks. These enzyme increases occurred more strongly at the higher 4-NP concentration (1.0 mg/kg diet). Conclusions 4-NP given to catfish at 0.1 to 1.0 mg/kg diet, concentrations relevant to environmental levels, depletes the endogenous anti-oxidant molecule GSH and temporarily inhibits GSH-related anti-oxidant enzymes. Such declines in anti-oxidant capacity and elevated oxidative stress seem to be compensated eventually by subsequent activation of various anti-oxidant enzyme systems.

Keywords

References

  1. Soverchia L, Ruggeri B, Palermo F, Mosconi G, Cardinaletti G, Scortichini G, et al. Modulation of vitellogenin synthesis through estrogen receptor beta-1 in goldfish (Carassius auratus) juveniles exposed to 17-beta estradiol and nonylphenol. Toxicol Appl Pharmacol 2005;209(3):236-243. https://doi.org/10.1016/j.taap.2005.04.013
  2. Lacorte S, Raldua D, Martinez E, Navarro A, Diez S, Bayona JM, et al. Pilot survey of a broad range of priority pollutants in sediment and fish from the Ebro river basin (NE Spain). Environ Pollut 2006;140(3):471-482. https://doi.org/10.1016/j.envpol.2005.08.008
  3. European Chemicals Agency. Support document for identification of 4-nonylphenol, branched and linear, ethoxylated [cited 2015 May 29]. Available from: http://echa.europa.eu/documents/10162/14598345/support_document_4-nonylphenol+ethoxylates_20130612_en.pdf.
  4. Ahel M, McEvoy J, Giger W. Bioaccumulation of the lipophilic metabolites of nonionic surfactants in freshwater organisms. Environ Pollut 1993;79(3):243-248. https://doi.org/10.1016/0269-7491(93)90096-7
  5. Pomatto V, Palermo F, Mosconi G, Cottone E, Cocci P, Nabissi M, et al. Xenoestrogens elicit a modulation of endocannabinoid system and estrogen receptors in 4NP treated goldfish, Carassius auratus. Gen Comp Endocrinol 2011;174(1):30-35. https://doi.org/10.1016/j.ygcen.2011.08.001
  6. Jobling S, Sumpter JP. Detergent components in sewage effluent are weakly oestrogenic to fish: an in vitro study using rainbow trout (Oncorhynchus mykiss) hepatocytes. Aquat Toxicol 1993;27(3-4):361-372. https://doi.org/10.1016/0166-445X(93)90064-8
  7. White R, Jobling S, Hoare SA, Sumpter JP, Parker MG. Environmentally persistent alkylphenolic compounds are estrogenic. Endocrinology 1994;135(1):175-182. https://doi.org/10.1210/endo.135.1.8013351
  8. Xu H, Yang M, Qiu W, Pan C, Wu M. The impact of endocrinedisrupting chemicals on oxidative stress and innate immune response in zebrafish embryos. Environ Toxicol Chem 2013;32(8):1793-1799. https://doi.org/10.1002/etc.2245
  9. Jayakanthan M, Jubendradass R, D'Cruz SC, Mathur PP. A use of homology modeling and molecular docking methods: to explore binding mechanisms of nonylphenol and bisphenol A with antioxidant enzymes. Methods Mol Biol 2015;1268:273-289. https://doi.org/10.1007/978-1-4939-2285-7_12
  10. Chen BS, Yen JH. Effect of endocrine disruptor nonylphenol on physiologic features and proteome during growth in Arabidopsis thaliana. Chemosphere 2013;91(4):468-474. https://doi.org/10.1016/j.chemosphere.2012.11.072
  11. Aly HA, Domenech O, Banjar ZM. Effect of nonylphenol on male reproduction: analysis of rat epididymal biochemical markers and antioxidant defense enzymes. Toxicol Appl Pharmacol 2012;261(2):134-141. https://doi.org/10.1016/j.taap.2012.02.015
  12. Choi MS, Park HJ, Oh JH, Lee EH, Park SM, Yoon S. Nonylphenol-induced apoptotic cell death in mouse TM4 Sertoli cells via the generation of reactive oxygen species and activation of the ERK signaling pathway. J Appl Toxicol 2014;34(6):628-636. https://doi.org/10.1002/jat.2886
  13. Kim KD, Kim JD, Lim SG, Kang YJ, Son MH. Effects of dietary lipid sources on the growth and body composition of the far eastern catfish, Silurus asotus. Korean J Fish Aquat Sci 2010;43(5):445-450 (Korean). https://doi.org/10.5657/kfas.2010.43.5.445
  14. Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979;95(2):351-358. https://doi.org/10.1016/0003-2697(79)90738-3
  15. Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophys 1959;82(1):70-77. https://doi.org/10.1016/0003-9861(59)90090-6
  16. Goldberg DM, Sparner RJ. Glutathione reductase. In: Bergmeyer HU, Bergmeyer J, Grassl M, Moss DW, editors. Methods of enzymatic analysis. 3rd ed. Weinheim: Verlag Chemie; 1987, p. 258-265.
  17. Lawrence RA, Burk RF. Glutathione peroxidase activity in selenium-deficient rat liver. 1976. Biochem Biophys Res Commun 2012;425(3):503-509. https://doi.org/10.1016/j.bbrc.2012.08.016
  18. Kakkar P, Das B, Viswanathan PN. A modified spectrometric assay for superoxide dismutase. Indian J Biochem Biophys 1984;21(2):130-132.
  19. Sinha AK. Colorimetric assay of catalase. Anal Biochem 1972;47(2):389-394. https://doi.org/10.1016/0003-2697(72)90132-7
  20. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-254. https://doi.org/10.1016/0003-2697(76)90527-3
  21. Duncan DB. Multiple range and multiple F tests. Biometrics 1955;11(1):1-42. https://doi.org/10.2307/3001478
  22. Palermo FA, Mosconi G, Angeletti M, Polzonetti-Magni AM. Assessment of water pollution in the Tronto River (Italy) by applying useful biomarkers in the fish model Carassius auratus. Arch Environ Contam Toxicol 2008;55(2):295-304. https://doi.org/10.1007/s00244-007-9113-2
  23. Jaeschke H. Antioxidant defense mechanisms. In: McQueen CA, editor. Comprehensive toxicology. 2nd ed. Oxford: Elsevier; 2010, p. 319-337.
  24. Meng SL, Chen JZ, Hu GD, Song C, Fan LM, Qiu LP, et al. Effects of chronic exposure of methomyl on the antioxidant system in liver of Nile tilapia (Oreochromis niloticus). Ecotoxicol Environ Saf 2014;101:1-6. https://doi.org/10.1016/j.ecoenv.2013.10.020
  25. Hernandez JP, Chapman LM, Kretschmer XC, Baldwin WS. Gender-specific induction of cytochrome P450s in nonylphenol-treated FVB/NJ mice. Toxicol Appl Pharmacol 2006;216(2):186-196. https://doi.org/10.1016/j.taap.2006.05.014
  26. Kazeto Y, Place AR, Trant JM. Effects of endocrine disrupting chemicals on the expression of CYP19 genes in zebrafish (Danio rerio) juveniles. Aquat Toxicol 2004;69(1):25-34. https://doi.org/10.1016/j.aquatox.2004.04.008
  27. Cocci P, Mosconi G, Palermo FA. Effects of 4-nonylphenol on hepatic gene expression of peroxisome proliferator-activated receptors and cytochrome P450 isoforms (CYP1A1 and CYP3A4) in juvenile sole (Solea solea). Chemosphere 2013;93(6):1176-1181. https://doi.org/10.1016/j.chemosphere.2013.06.058
  28. Meucci V, Arukwe A. The xenoestrogen 4-nonylphenol modulates hepatic gene expression of pregnane X receptor, aryl hydrocarbon receptor, CYP3A and CYP1A1 in juvenile Atlantic salmon (Salmo salar). Comp Biochem Physiol C Toxicol Pharmacol 2006;142(1-2):142-150. https://doi.org/10.1016/j.cbpc.2005.11.011
  29. Ying GG, Kookana RS, Dillon P. Sorption and degradation of selected five endocrine disrupting chemicals in aquifer material. Water Res 2003;37(15):3785-3791. https://doi.org/10.1016/S0043-1354(03)00261-6
  30. Van Leeuwen S, De Boer J; Netherlands Institute for Fisheries Research. Detecting organic contaminants in food: the case of fish and shellfish. In: Watson DH, editor. Pesticide, veterinary and other residues in food. Cambridge: Woodhead Pub.; 2004, p. 536-576.

Cited by

  1. Effects of perinatal exposure to nonylphenol on delivery outcomes of pregnant rats and inflammatory hepatic injury in newborn rats vol.49, pp.12, 2015, https://doi.org/10.1590/1414-431x20165647
  2. Endocrine disruption, oxidative stress, and testicular damage induced by 4-nonylphenol in Clarias gariepinus: the protective role of Cydonia oblonga vol.43, pp.4, 2015, https://doi.org/10.1007/s10695-017-0355-2
  3. Hepatotoxic responses of 4-nonylphenol on African catfish (Clarias gariepinus): antixoidant and histochemical biomarkers vol.44, pp.3, 2015, https://doi.org/10.1007/s10695-018-0485-1
  4. Antioxidant responses and DNA damage in primary hepatocytes of Van fish (Alburnus tarichi, Güldenstadt 1814) exposed to nonylphenol or octylphenol vol.41, pp.4, 2015, https://doi.org/10.1080/01480545.2018.1461899
  5. Hsp27, a potential EcR target, protects nonylphenol-induced cellular and organismal toxicity in Drosophila melanogaster vol.293, pp.None, 2022, https://doi.org/10.1016/j.envpol.2021.118484