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Biological Trace Element Research

, Volume 165, Issue 1, pp 103–109 | Cite as

Methylmercury-Induced Oxidative Stress in Rainbow Trout (Oncorhynchus mykiss) Liver: Ameliorating Effect of Vitamin C

  • Z. Mozhdeganloo
  • A. Moghadam Jafari
  • M. K. Koohi
  • M. HeidarpourEmail author
Article

Abstract

The present study was undertaken to evaluate methylmercury-induced alterations in hepatic enzymes and oxidative stress markers in liver tissue of rainbow trout (Oncorhynchus mykiss) by using a perfusion method, and to explore possible protective effect of vitamin C against these alterations. Forty-eight fish were divided into six groups containing control, test, and amelioration groups. The liver of fish in the test groups were exposed to different doses of methylmercury, i.e., 0.6, 1.2, and 2.4 μg L−1, respectively, for 120 min. In the amelioration group, liver was treated with vitamin C (17.2 μg L−1) along with high dose (2.4 μg L−1) of methylmercury. The results of the present study showed that exposure with 0.6, 1.2, and 2.4 μg L−1 of methylmercury significantly increased (p < 0.05) hepatic enzyme activities (alanine transaminase (ALT), aspartate transaminase (AST), and Lactate dehydrogenase (LDH)) and malondialdehyde (MDA) level, as a marker of lipid peroxidation. On the other hand, the concentration of reduced glutathione (GSH) and total antioxidant capacity of the liver decreased (p < 0.05) in the methylmercury-exposed groups when compared to the control group. Pearson’s correlation analysis revealed a positive correlation between MDA concentration and ALT, AST, and LDH activities in the methylmercury groups, suggesting that the enhanced lipid peroxidation may be linked to hepatic damage caused by methylmercury. Treatment with vitamin C in methylmercury-exposed group led to a significant decrease (p < 0.05) in MDA concentration and hepatic enzyme activities and significant increase (p < 0.05) in levels of GSH and total antioxidant capacity. The values of measured parameters in the methylmercury + vitamin C group were comparable to those of the control group. The results of the present study demonstrated that methylmercury exposure induces oxidative stress in the liver of rainbow trout and treatment with vitamin C can protect fish liver against this oxidative insult.

Keywords

Methylmercury Vitamin C Oxidative stress Liver Rainbow trout 

Notes

Acknowledgments

This study was supported by research fund of Ferdowsi University of Mashhad (project no. 2/26807). The authors wish to thank technicians who kindly helped us for sample collection of this study.

Conflict of Interest

The authors declare that there is no conflict of interests.

References

  1. 1.
    Atli G, Canli M (2010) Response of antioxidant system of fresh water fish Oreochromis niloticus to acute and chronic metal (Cd, Cu, Cr, Zn, Fe) exposures. Ecotoxicol Environ Saf 73:1884–1889CrossRefPubMedGoogle Scholar
  2. 2.
    Farombi EO, Adelowo OA, Ajimoko YR (2007) Biomarkers of oxidative stress and heavy metal levels as indicators of environmental pollution in African cat fish (Clarias gariepinus) from nigeria ogun river. Int J Environ Res Public Health 4:158–165CrossRefPubMedCentralPubMedGoogle Scholar
  3. 3.
    Yadetie F, Karlsen OA, Lanzén A, Berg K, Olsvik P, Hogstrand C, Goksøyr A (2013) Global transcriptome analysis of Atlantic cod (Gadus morhua) liver after in vivo methylmercury exposure suggests effects on energy metabolism pathways. Aquat Toxicol 126:314–325CrossRefPubMedGoogle Scholar
  4. 4.
    Bleau H, Daniel C, Chevalier G, van Tra H, Hontela A (1996) Effects of acute exposure to mercury chloride and methylmercury on plasma cortisol, T3, T4, glucose and liver glycogen in rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 34:221–235CrossRefGoogle Scholar
  5. 5.
    Jensen S, Jernelov A (1969) Biological methylation of mercury in aquatic organisms. Nature 223:753CrossRefPubMedGoogle Scholar
  6. 6.
    Lock RAC, van Overbeeke AP (1981) Effects of mercuric chloride and methylmercuric chloride on mucus secretion in rainbow trout, Salmo gairdneri Richardson. Comp Biochem Physiol 69:67–73Google Scholar
  7. 7.
    Klaper R, Carter BJ, Richter CA, Drevnick PE, Sandheinrich MB, Tillitt DE (2008) Use of a 15 k gene microarray to determine gene expression changes in response to acute and chronic methylmercury exposure in the fathead minnow Pimephales promelas Rafinesque. J Fish Biol 72:2207–2280CrossRefGoogle Scholar
  8. 8.
    Bourdineaud JP, Cambier S, Benard G, Mesmer-Dudons N, Gonzalez P, Rossignol R, Brethes D (2009) At environmental doses, dietary methylmercury inhibits mitochondrial energy metabolism in skeletal muscles of the zebra fish (Danio rerio). Int J Biochem Cell B 41:791–799CrossRefGoogle Scholar
  9. 9.
    Berg K, Puntervoll P, Valdersnes S, Goksoyr A (2010) Responses in the brain proteome of Atlantic cod (Gadus morhua) exposed to methylmercury. Aquat Toxicol 100:51–65CrossRefPubMedGoogle Scholar
  10. 10.
    Nostbakken OJ, Martin SAM, Cash P, Torstensen BE, Amlund H, Olsvik PA (2012) Dietary methylmercury alters the proteome in Atlantic salmon (Salmo salar) kidney. Aquat Toxicol 108:70–77CrossRefPubMedGoogle Scholar
  11. 11.
    Sevcikova M, Modra H, Slaninova A, Svobodova Z (2011) Metals as a cause of oxidative stress in fish: a review. Vet Med (Praha) 56:537–546Google Scholar
  12. 12.
    Zhang X, Xie P, Li D, Tang R, Lei H, Zhao Y (2009) Time-dependent oxidative stress responses of crucian carp (Carassius auratus) to intraperitoneal injection of extracted microcystins. Bull Environ Contam Toxicol 82:574–578CrossRefPubMedGoogle Scholar
  13. 13.
    Almeida JA, Barreto RE, Novelli ELB, Castro FJ, Moron SE (2009) Oxidative stress biomarkers and aggressive behavior in fish exposed to aquatic cadmium contamination. Neotrop Ichthyol 7:103–108CrossRefGoogle Scholar
  14. 14.
    Romeo M, Bennani N, Gnassia-Barelli M, Lafaurie M, Girard JP (2000) Cadmium and copper display different responses towards oxidative stress in the kidney of the sea bass Dicentrarchus labrax. Aquat Toxicol 48:185–194CrossRefPubMedGoogle Scholar
  15. 15.
    Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30CrossRefPubMedGoogle Scholar
  16. 16.
    Ralston NV, Ralston CR, Blackwell JL, Raymond LJ (2008) Dietary and tissue selenium in relation to methylmercury toxicity. Neurotoxicology 29:802–811CrossRefPubMedGoogle Scholar
  17. 17.
    Larose C, Canuel R, Luccote M, Di Giulio R (2008) Toxicological effects of methylmercury on walleye (Sander vitreus) and perch (Perca flavescens) from lakes of the boreal forest. Comp Biochem Physiol C 147:139–149Google Scholar
  18. 18.
    Mieiro CL, Ahmad I, Pereira ME, Duarte AC, Pacheco M (2010) Antioxidant system breakdown in brain of feral gulden grey mullet (Liza aurata) as an effect of mercury exposure. Ecotoxicology 19:1034–1045CrossRefPubMedGoogle Scholar
  19. 19.
    Raldua D, Diez S, Bayona JM, Barcelo D (2007) Mercury levels and liver pathology in feral fish living in the vicinity of a mercury cell chlor-alkali factory. Chemosphere 66:1217–1225CrossRefPubMedGoogle Scholar
  20. 20.
    Navarro A, Quiros L, Casado M, Faria M, Carrasco L, Benejam L, Benito J, Diez S, Raldua D, Barata C, Bayona JM, Pina B (2009) Physiological responses to mercury in feral carp populations inhabiting the low Ebro River (NE Spain), a historically contaminated site. Aquat Toxicol 93:150–157CrossRefPubMedGoogle Scholar
  21. 21.
    Badgujar PC, Pawar NN, Chandratre GA, Telang AG, Sharma AK (2014) Fipronil induced oxidative stress in kidney and brain of mice: protective effect of vitamin E and vitamin C. Pestic Biochem Physiol. doi: 10.1016/j.pestbp.2014.10.013 PubMedGoogle Scholar
  22. 22.
    Garcia F, Pilarski F, Onaka EM, Moraes FR (2007) Martins ML (2007) Hematology of Piaractus mesopotamicus fed diets supplemented with vitamins C and E, challenged by Aeromonas hydrophila. Aquaculture 271:39–46CrossRefGoogle Scholar
  23. 23.
    Harabawy ASA, Mosleh YYI (2014) The role of vitamins A, C, E and selenium as antioxidants against genotoxicity and cytotoxicity of cadmium, copper, lead and zinc on erythrocytes of Nile tilapia, Oreochromis niloticus. Ecotoxicol Environ Saf 104:28–35CrossRefPubMedGoogle Scholar
  24. 24.
    Vijayavel K, Gopalakrishnan S, Thilagam H, Balasubramanian MP (2006) Dietary ascorbic acid and α-tocopherol mitigates oxidative stress induced by copper in the thorn fish Terapon jarbua. Sci Total Environ 372:157–163CrossRefPubMedGoogle Scholar
  25. 25.
    Nichols JW, Hoffman AD, Fitzsimmons PN (2009) Optimization of an isolated perfused rainbow trout liver model: clearance studies with 7-ethoxycoumarin. Aquat Toxicol 95:182–194CrossRefPubMedGoogle Scholar
  26. 26.
    Datta M, Kaviraj A (2003) Ascorbic acid supplementation of diet for reduction of deltamethrin induced stress in freshwater catfish Clarias gariepinus. Chemosphere 53:883–888CrossRefPubMedGoogle Scholar
  27. 27.
    Brett SE, Leary SC, Welsh DG, Leatherland JF (1998) The application of an in vitro perfused liver preparation to examine the effects of epinephrine and bovine thyroid-stimulating hormone on triiodo-l-thyronine release from the liver of rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 109:212–222CrossRefPubMedGoogle Scholar
  28. 28.
    Placer ZA, Cushman L, Johnson B (1966) Estimation of product of lipid peroxidation (malonyldialdehyde) in biochemical system. Anal Biochem 16:359–364CrossRefPubMedGoogle Scholar
  29. 29.
    Benzie IFF, Strain JJ (1996) Ferric reducing ability of plasma (FRAP) as a measure of antioxidant power: The FRAP assay. Anal Biochem 239:70–76CrossRefPubMedGoogle Scholar
  30. 30.
    Hayes JD, Flanagan JU, Jowsey IR (2005) Glutathione transferases. Annu Rev Pharmacol Toxicol 45:51–88CrossRefPubMedGoogle Scholar
  31. 31.
    Elia AC, Galarini R, Taticchi MI, Dorr AJM, Mantilacci L (2003) Antioxidant responses and bioaccumulation in Ictalurus melas under mercury exposure. Ecotoxicol Environ Saf 55:162–167CrossRefPubMedGoogle Scholar
  32. 32.
    Richter CA, Garcia-Reyero N, Martyniuk C, Knoebl I, Pope M, Wright-Osment MK, Denslow ND, Tillitt DE (2011) Gene expression changes in female zebrafish (Danio rerio) brain in response to acute exposure to methylmercury. Environ Toxicol Chem 30:301–308CrossRefPubMedCentralPubMedGoogle Scholar
  33. 33.
    Monteiro DA, Rantin FT, Kalinin AL (2010) Inorganic mercury exposure: toxicological effects, oxidative stress biomarkers and bioaccumulation in the tropical freshwater fish matrinxa, Brycon amazonicus (Spix and Agassiz, 1829). Ecotoxicology 19:105–123CrossRefPubMedGoogle Scholar
  34. 34.
    Rana SVS, Singh R, Verma S (1995) Mercury-induced lipid peroxidation in the liver, kidney, brain and gills of a fresh water fish Channa punctatus. Japanese J Ichthyol 42:255–259Google Scholar
  35. 35.
    Elia AC, Dorr AJM, Mantilacci L, Taticchi MI, Galarini R (2000) Effects of mercury on glutathione and glutathione-dependent enzymes in catfish (Ictalurus melas R.). In: Markert B, Friese K (eds) Trace elements—their distribution and effects in the environment: trace metals in the environment. Elsevier Science, Amsterdam, pp 411–421CrossRefGoogle Scholar
  36. 36.
    Berntssen MHG, Aatland A, Handy RD (2003) Chronic dietary mercury exposure causes oxidative stress, brain lesions, and altered behaviour in Atlantic salmon (Salmo salar) parr. Aquat Toxicol 65:55–72CrossRefPubMedGoogle Scholar
  37. 37.
    Uner N, Oruç EO, Canli M, Sevgiler Y (2001) Effects of cypermethrin on antioxidant enzyme activities and lipid peroxidation in liver and kidney of the freshwater fish. Oreochromis niloticus and Cyprinus carpio (L.). Bull Environ Contam Toxicol 67:657–664CrossRefPubMedGoogle Scholar
  38. 38.
    Drevnick PE, Roberts AP, Otter RR, Hammerschmidt CR, Klaper R, Oris JT (2008) Mercury toxicity in livers of northern pike (Esox lucius) from Isle Royale, USA. Comp Biochem Physiol C 147:331–338Google Scholar
  39. 39.
    Meinelt T, Krüger R, Pietrock M, Osten R, Steinberg C (1997) Mercury pollution and macrophage centres in pike (Esox lucius) tissues. Environ Sci Pollut Res 4:32–36CrossRefGoogle Scholar
  40. 40.
    de Oliveira Ribeiro CA, Belger L, Pelletier É, Rouleau C (2002) Histopathological evidence of inorganic mercury and methylmercury toxicity in the arctic charr (Salvelinus alpinus). Environ Res 90:217–225CrossRefPubMedGoogle Scholar
  41. 41.
    Ramanathan K, Balakumar BS, Panneerselvam C (2002) Effects of ascorbic acid and α-tocopherol on arsenic-induced oxidative stress. Hum Exp Toxicol 21:675–680CrossRefPubMedGoogle Scholar
  42. 42.
    Ramanathan K, Anusuyadevi M, Shila S, Panneerselvam C (2005) Ascorbic acid and α-tocopherol as potent modulators of apoptosis on arsenic induced toxicity in rats. Toxicol Lett 156:297–306CrossRefPubMedGoogle Scholar
  43. 43.
    Hounkpatin ASY, Johnson RC, Guédénon P, Domingo E, Alimba CG, Boko M, Edorh PA (2012) Protective effects of vitamin c on haematological parameters in intoxicated Wistar rats with cadmium, mercury and combined cadmium and mercury. Int Res J Biol Sci 1:76–81Google Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Z. Mozhdeganloo
    • 1
  • A. Moghadam Jafari
    • 2
  • M. K. Koohi
    • 3
  • M. Heidarpour
    • 1
    • 4
    Email author
  1. 1.Department of Clinical Sciences, School of Veterinary MedicineFerdowsi University of MashhadMashhadIran
  2. 2.Department of Basic Sciences, School of Veterinary MedicineFerdowsi University of MashhadMashhadIran
  3. 3.Department of Basic Sciences, School of Veterinary MedicineUniversity of TehranTehranIran
  4. 4.MashhadIran

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