Metal Induced Oxidative Stress in Fishes: A Review

Main Article Content

Jugendra Nath Das
Satabdi Saikia

Abstract

Fishes when exposed to various contaminants, particularly metals in their habitat can induce oxidative stress. In fishes, metals contamination results in oxidative stress by promoting reactive oxygen species (ROS) formation through redox cycling and impairing antioxidant defenses. ROS are harmful to all forms of aquatic life and can damage tissues and cellular components.Higher amount ofROS lead to varying degree of oxidative damage to the fish tissues including lipid peroxidation, protein and DNA oxidation as well as enzyme inactivation through different mechanisms as observed in different fish species. The present comprehension of how metals contribute to the onset of oxidative stress in fish is summed up in this review.


 

Downloads

Download data is not yet available.

Article Details

How to Cite
Jugendra Nath Das, & Satabdi Saikia. (2024). Metal Induced Oxidative Stress in Fishes: A Review . Journal of Advanced Zoology, 45(1), 434–449. https://doi.org/10.53555/jaz.v45i1.3582
Section
Articles
Author Biographies

Jugendra Nath Das

Department of Zoology, Sibsagar College, Joysagar (Autonomous), Assam-785665

Satabdi Saikia

Department of Zoology, Sibsagar College, Joysagar (Autonomous), Assam-785665

 

References

Chowdhury, S., & Saikia, S. K. (2020). Oxidative Stress in Fish: A Review. Journal of Scientific Research, 12(1), 145–160. https://doi.org/10.3329/jsr.v12i1.41716

Livingstone, D.R. (2003). Oxidative stress in aquatic organism in relation to pollution and agriculture. Revue de Medical Veterinary, 154, 427–430.

Forster, U., Whittmann, G.T.W. (1983). Metal Pollution in the Aquatic Environment. Springer-Verlag. Berlin.

Luoma, S.N., Rainbow P.S. (2008). Metal Contamination in Aquatic Environments. Cambridge University Press, Cambridge. 47-66.

Mahboob, S. (2013). Environmental pollution of heavy metals as a cause of oxidative stress in fish: a review. Life Sciences Journal, 10(10s): 336-347 (ISSN: 1097-8135). http://www.lifesciencesite.com.

Sies, H. (1986). Biochemistry of Oxidative Stress. Angewandte Chemie International Edition in English. https://doi.org/10.1002/anie.198610581

Lushchak, V.I. (2011). Environmentally induced oxidative stress in aquatic animals. Aquatic toxicology, 101 1, 13-30.

Scandalios, J.G. (2005). Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Brazilian journal of medical and biological research, Revistabrasileira de pesquisasmedicas e biologicas, 38(7), 995–1014. https://doi.org/10.1590/s0100-879x2005000700003

Ott, M., Gogvadze, V., Orrenius, S., & Zhivotovsky, B. (2007). Mitochondria, oxidative stress and cell death. Apoptosis: an international journal on programmed cell death, 12(5), 913–922. https://doi.org/10.1007/s10495-007-0756-2

Skulachev, V.P. (2012). Mitochondria-targeted antioxidants as promising drugs for treatment of age-related brain diseases. Journal of Alzheimers Disease, 28, 283–289.

Halliwell, B. and Gutteridge, J.M.C. (1999). Free Radicals in Biology and Medicine. Oxford University Press, Oxford, 1-25.

Yeldandi, A. V., Rao, M. S. & Reddy, J. K. (2000). Hydrogen peroxide generation in peroxisome proliferator-induced oncogenesis. Mutation research, 448(2), 159–177. https://doi.org/10.1016/s0027-5107(99)00234-1

Bartosz, G. (2009). Reactive oxygen species: destroyers or messengers?. Biochemical pharmacology, 77(8), 1303–1315. https://doi.org/10.1016/j.bcp.2008.11.009

Miller, J.W., Selhub, J., Joseph, J.A. (1996). Oxidative damage caused by free radicals produced during catecholamine autoxidation: protective effects of O-methylation and melatonin. Free Radical Biology Medicine, 21, 241–249.

Saller, S., Merz-Lange, J., Raffael, S., Hecht, S., Pavlik, R., Thaler, C., Berg, D., Berg, U., Kunz, L., Mayerhofer, A. (2012). Norepinephrine, active norepinephrine transporter, and norepinephrine-metabolism are involved in the generation of reactive oxygen species in human ovarian granulosa cells. Endocrinology, 153(3), 1472–1483.

Michail, K., Baghdasarian, A., Narwaley, M., Aljuhani, N., Siraki, A.G. (2013). Scavenging of free-radical metabolites of aniline xenobiotics and drugs by amino acid derivatives: toxicological implications of radical-transfer reactions. Chemical Research Toxicology, 26, 1872–1883. 2013.

Lushchak V.I. (2007). Free radical oxidation of proteins and its relationship with functional state of organisms. Biochemistry (Mosc), 72, 809–827.

Olcott, H.S., Mattill, H.A. (1931a). The unsaponifiable lipids of lettuce. II Fractionation. Journal of Biological Chemistry, 93, 59-64.

Olcott, H.S., Mattill, H.A. (1931b). The unsaponifiable lipids of lettuce. III Antioxidant. Journal of Biological Chemistry, 93, 65-70.

Monaghan, B.R., Schmitt, F.O. (1932). The effects of carotene and of vitamin A on the oxidation of linoleic acid. Journal of Biological Chemistry, 96, 387-395.

Fritsche, K.L., Johnston, P.V. (1988). Rapid autoxidation of fish oil in diets without added antioxidants. Journal of Nutrition, 118(4), 425-426.

Gonzalez, M.J., Gray, J.I., Schemmel, R.A., Dugan, L., Jr. Welsch, C.W. (1992). Lipid peroxidation products are elevated in fish oil diets even in the presence of added antioxidants. Journal of Nutrition, 122(11), 2190-2195.

Niki, E. (2000). Free radicals in the 1900's: from in vitro to in vivo. Free Radical Research, 33(6), 693-704.

Hermes-Lima, M. Willmore, W.G. Storey, K.B. (1995). Quantification of lipid peroxidation in tissue extracts based on Fe (III) xylenol orange complex formation. Free Radical Biology and Medicine, 19, 271–280.

Storey, K.B. (1996). Oxidative stress: animal adaptations in nature. Brazilian Journal of Medical and Biological Research, 29, 1715–1733.

Lushchak,V.I. (2011a). Adaptive response to oxidative stress: Bacteria, fungi, plants and animals. Comparative Biochemistry and Physiology, 153, 175–190.

Lushchak, V.I. (2011b). Environmentally induced oxidative stress in aquatic animals. Aquatic Toxicology, 101,13–30.

Lushchak, V.I. (2012). Glutathione homeostasis and functions: potential targets for medical interventions. Journal of Amino Acids, doi:10.1155/2012/736837

Talas, Z.S., Orun, I., Ozdemir, I., Erdogan, K., Alkan, A., Yilmaz, I. (2008). Antioxidative role of selenium against the toxic effect of heavy metals (Cd+2, Cr+3) on liver of rainbow trout (Oncorhynchus mykiss Walbaum 1792). Fish Physiology and Biochemistry, 34, 217–222.

Zhang, X., Yang, F., Zhang, X., Xu, Y., Liao, T., Song, S., Wang, J. (2008). Induction of hepatic enzymes and oxidative stress in Chinese rare minnow (Gobiocypris rarus) exposed to waterborne hexabromocyclododecane (HBCDD). Aquatic Toxicology. 86, 4–11.

Falfushynska, H.I. Stolyar, O.B. (2009). Responses of biochemical markers in carp Cyprinus carpio from two field sites in Western Ukraine. Ecotoxicology and Environmental Safety. 72, 729–736.

Hermes-Lima, M., Willmore, W.G., Storey, K.B. (1995). Quantification of lipid peroxidation in tissue extracts based on Fe (III) xylenol orange complex formation. Free Radical Biology and Medicine. 19, 271–280.

Lushchak, O.V., Bahniukova, T.V., Lushchak, V.I. (2003). Effect of aminotriazole on the activity of catalase and glucose-6-phosphate dehydrogenase in tissues of two frog species – Rana ridibunda and Rana esculenta. Ukrainskogo biokhimicheskogo zhurnal. 75(4), 45-50.

Lushchak, O.V. Kubrak, O.I. Torous, I.M. Nazarchuk, T.Y. Storey, K.B. Lushchak, V.I. (2009a). Trivalent chromium induces oxidative stress in goldfish brain. Chemosphere .75, 56–62.

Lushchak, O.V., Kubrak, O.I., Lozinsky, O.V., Storey, J.M., Storey, K.B., Lushchak, V.I. (2009b). Chromium (III) induces oxidative stress in goldfish liver and kidney. Aquatic Toxicology. 93, 45–52.

Lushchak, V. I. (2016). Contaminant-induced oxidative stress in fish: a mechanistic approach. Fish physiology and biochemistry, 42(2), 711–747. https://doi.org/10.1007/s10695-015-0171-5

Ohno, M., Oka, S., Nakabeppu, Y. (2009). Quantitative analysis of oxidized Guanine, 8-oxoguanine, in mitochondrial DNA by immunofluorescence method. Methods in Molecular Biology, 554, 199–212.

Olinski, R., Rozalski, R., Gackowski, D., Foksinski, M., Siomek, A., Cooke, M.S. (2006). Urinary measurement of 8-OxodG, 8-OxoGua, and 5HMUra: a noninvasive assessment of oxidative damage to DNA. Antioxidants and Redox Signaling, 8,1011–1019.

Malek, R.L., Sajadi, H., Abraham, J., Grundy, M.A., Gerhard, G.S. (2004). The effects of temperature reduction on gene expression and oxidative stress in skeletal muscle from adult zebrafish. Comparative Biochemistry & Physiology, 138, 363–373.

Grygoryev, D., Moskalenko, O., Zimbrick, J.D. (2008). Non-linear effects in the formation of DNA damage in medaka fish fibroblast cells caused by combined action of cadmium and ionizing radiation. Dose Response, 6, 283–298.

Jha, A.N. Ecotoxicological applications and significance of the comet assay. Mutagenesis, 23:207–221. 2008.

Vevers, W.F., Jha, A.N. (2008). Genotoxic and cytotoxic potential of titanium dioxide (TiO2) nanoparticles on fish cells in vitro. Ecotoxicology 17:410–420.

Schreck, C.B., Contreras-Sanchez, W., Fitzpatrick, M.S. (2001). Effects of stress on fish reproduction, gamete quality, and progeny. Aquaculture. 197:3–24.doi: 10.1016/B978-0-444-50913-0.50005-9.

Lushchak, V.I. (2011). Environmentally induced oxidative stress in aquatic animals. Aquatic Toxicology, 101(1), 13-30. doi:10.1016/j.aquatox.2010.10.006

Marí, M. Morales, A. Colell, A. García-Ruiz, C. Fernández-Checa, J.C. (2009). Mitochondrial glutathione, a key survival antioxidant. Antioxidants and Redox Signaling, 11(11), 2685-2700.

Lushchak, V.I. (2012). Glutathione homeostasis and functions: potential targets for medical interventions. Journal of Amino Acids. doi:10.1155/2012/736837

Jezierska, B., Witeska, M. (2001). Metal Toxicity to Fish. Wydawnictvo Akademii Podlaskej, Siedlce, 214–243.

Tao, S., Wen, Y., Long, A., Dawson, R., Cao, J. and Xu, F. (2001). Simulation of acid- base condition and copper speciation in fish gill microenvironment. Computers and Chemistry, 25, 215–222.

Kamunde, C., Clayton, C., Wood, C.M. (2002). Waterborne vs. dietary copper uptake in rainbow trout and the effects of previous waterborne copper exposure. American Journal Physiology Regulatory Integrated Comparative Physiology, 283, R69–R78.

Sevcikova, Marie & Modrá, Helena & Slaninova, Andrea & Svobodova, Z. (2011). Metals as a cause of oxidative stress in fish: A review. Veterinarni Medicina, 56, 537-546. 10.17221/4272-VETMED.

Stohs, S.J., Bagchi, D. (1995). Oxidative mechanisms in the toxicity of metals ions. Free Radical Biological Medicine, 2, 321–336.

Valko, M., Morris, H., Cronin, M.T. (2005). Metals, toxicity and oxidative stress. Current Medical Chemistry, 12, 1161–1208.

Lushchak, V.I. (2011). Environmentally induced oxidative stress in aquatic animals. Aquatic Toxicology. 1, 13–30.

Bury, N.R., Walker, P.A., Glover, C.N. (2003). Nutritive metal uptake in teleost fish. Journal of Experimental Biology, 206, 11–23.2003.

Walker, R.L., Fromm, P.O. (1976). Metabolism of iron by normal and iron deficient rainbow trout. Comparative Biochemistry and Physiology, 55, 311–318.

Carriquiriborde, P., Handy, R.D., Davies, S.J. (2004). Physiological modulation of iron metabolism in rainbow trout (Oncorhynchus mykiss) fed low and high iron diets. Journal of Experimental Biology. 207: 75–86.

Baker, R.T.M., Martin, P., Davies, S.J. (1997). Ingestion of sublethal levels of iron sulphate by African catfish affects growth and tissue lipid peroxidation. Aquatic Toxicology, 140, 51–61.

Bagnyukova, T.V., Chahrak, O.I., Lushchak, V.I. (2006). Coordinated response of gold fish antioxidant defenses to environmental stress. Aquatic Toxicology, 78, 325–331.

Lushchak, V.I. (2014a). Free radicals, reactive oxygen species, oxidative stress and its classification. Chemico-Biological Interactions, 224, 164–175.

Lushchak, V.I. (2014b). Classification of oxidative stress based on its intensity, EXCLI Journal, 13, 922-937.

Li, H.C., Zhou, Q., Wu, Y., Fu, J., Wang, T., Jiang, G. (2009). Effects of waterborne nano-iron on medaka (Oryzia slatipes): Antioxidant enzymatic activity, lipid peroxidation and histopathology. Ecotoxicology Environmental Safety, 72, 3684–3692.

Di Giulio, R.T., Benson, W.H., Sanderrs, B.M., Van Veld, P.A. (1995). Fundamentals of aquatic toxicology: Effects, environmental fate and risk assessment. Taylor & Francis, Washington, D.C. 523- 561.

Gravato, C., Teles, M., Oliveria, M., Santos, M.A. (2006). Oxidative stress, liver biotransformation and genotoxic effects induced by copper in Anguilla anguilla L. – the influence of pre-exposure to β- naphthoflavone. Chemosphere. 65: 1821–1830.

Sanchez, W., Palluel, O., Meunier, L., Coquery, M., Porcher, J.M., Ait-Aissa, S. (2005). Copper-induced oxidative stress in three-spined stickleback: relationship with hepatic metal levels. Environmental Toxicology Pharmacy, 19,177–183.

Machado, A.A. Hoff, M.L. Klein, R.D. Cardozo, J.G. Giacomin, M.M. Pinho, G.L. Bianchini, A. (2013). Biomarkers of waterborne copper exposure in the guppy Poecilia vivipara acclimated to salt water. Aquatic Toxicology,138–139, 60–69.

Bopp, S.K., Abicht, H.K., Knauer, K. (2008). Copper-induced oxidative stress in rainbow trout gill cells. Aquatic Toxicolog, 86, 197–204.

Craig, P.M., Wood, C.M., McClelland, G.B. (2007). Oxidative stress response and gene expression with acute copper exposure in zebrafish (Danio rerio). American Journal Physiology, 293, R1882–R1892.

Parvez, S., Sayeed, I., Pandey, S., Ahmad, A., Bin-Hafeez, B., Haque, R., Ahmad, I., Raisuddin, S. (2003). Modulatory effect of copper on non-enzymatic antioxidants in freshwater fish Channa punctatus (Bloch.). Biological Trace Element Research, 93, 237– 248.

Gutteridge, J.M. (1985). Inhibition of the Fenton reaction by the protein ceruloplasmin and other copper complexes. Assessment of ferrioxidase and radical scavenging activities. Chemico-Biology Interaction, 56, 113–120.

Luza, S.C., Speisky, H.C. (1996). Liver copper storage and transport during development: Implications for cytotoxicity. American Journal Clinical Nutrition. 63: 812–820.

Rosesijadi, G. (1996). Metallothionein and its role in toxic metal regulation. Comparative Biochemistry Physiology C, 113, 117–123.

Ahmad, I., Hamid, T., Fatima, M., Chand, H.S., Jain, S.K., Athar, M., Raisuddin, S. (2000). Induction of hepatic antioxidants in freshwater catfish (Channa punctatus, Bloch) is a biomarker of papermill effluent exposure. Biochimica et Biophysica Acta, 1523, 37–48.

Perdajas, J.R., Peindado, J., Lopez-Barea, J. (1995). Oxidative stress in fish exposed to model xenobiotics. Oxidatively modified forms of Cu, Zn-superoxide dismutase as potential biomarkers. Chemical - Biological Interaction, 98, 267–282.

Ransberry, V.E., Morash, A.J., Blewett, T.A., Wood, C.M., McClelland, G.B. (2015). Oxidative stress and metabolic responses to copper in freshwater- and seawater-acclimated killifish, Fundulus heteroclitus. Aquatic Toxicology, 161, 242–252.

Falfushynska, H.I., Gnatyshyna, L.L., Stoliar, O.B. (2012). Population-related molecular responses on the effect of pesticides in Carassius auratus gibelio. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 155(2), 396-406.

Halliwell, B., Gutteridge, J.M.C. (1989). Free Radicals in Biology and Medicine. Clarendon Press, Oxford.

Shi, X., Dalal, N.S. (1990). On the hydroxyl radical formation in the reaction between hydrogen peroxide and biologically generated chromium (V) species. Archives of Biochemistry and Biophysics, 277, 342–350.

Lushchak, V.I. (2008). Oxidative stress as a component of transition metal toxicity in fish. Aquatic Toxicology Research Focus. Nova Science Publishers Inc, Hauppaug, NY, USA, 1–29.

Pacheco, M., Santos, M.A., Pereira, P., Martínez, J.I., Alonso, P.J., Soares, M.J., Lopes, J.C. (2013). EPR detection of paramagnetic chromium in liver of fish (Anguilla anguilla) treated with dichromate (VI) and associated oxidative stress responses-contribution to elucidation of toxicity mechanisms. Comparative Biochemistry and Physiology C Toxicology Pharmacology, 157, 132–140.

Li, Z.H., Li, P., Randak, T. (2011). Evaluating the toxicity of environmental concentrations of waterborne chromium (VI) to a model teleost, Oncorhynchus mykiss: a comparative study of in vivo and in vitro. Comparative Biochemistry and Physiology C Toxicology Pharmacology, 153, 402–407.

Kubrak, O.I., Lushchak, O.V., Lushchak, J.V., Torous, I.M., Storey, J.M., Storey, K.B., Lushchak, V.I. (2010). Chromium effects on free radical processes in goldfish tissues: comparison of Cr (III) and Cr (VI) exposures on oxidative stress markers, glutathione status and antioxidant enzymes. Comparative Biochemistry and Physiology C Toxicology Pharmacology, 152, 360–370.

Ahmad, I., Maria, V.L., Oliveira, M., Pacheco, M., Santos, M.A. (2006). Oxidative stress and genotoxic effects in gill and kidney of Anguilla anguilla L. exposed to chromium with or without pre-exposure to β-naphthoflavone. Mutation Research, 608, 16–28.

Kuykendall, J.R., Miller, K.L., Mellinger, K.N., Cain, A.V. (2006). Waterborne and dietary hexavalent chromium exposure causes DNA-protein crosslink (DPX) formation in erythrocytes of largemouth bass (Micropterus salmoides). Aquatic Toxicology, 78, 27–31. 2006.

Sevikova, M., Modra, H., Slaninova, Z., Svobodova, S. (2011). Metals as a cause of oxidative stress in fish. Veterinary Medicine, 56, 537–546.

Kumar, P., Kumar, R., Nagpure, N.S., Nautiyal, P., Kushwaha, B., Dabas, A. (2013). Genotoxicity and antioxidant enzyme activity induced by hexavalent chromium in Cyprinus carpio after in vivo exposure. Drug and Chemical Toxicology, 36, 451–460.

Velma, V., Tchounwou, P.B. (2013). Oxidative stress and DNA damage induced by chromium in liver and kidney of goldfish, Carassius auratus. Biomark Insights, 8, 43–51.

Farag, A.M., May, T., Marty, G.D., Easton, M., Harper, D.D., Little, E.E., Cleveland, L. (2006). The effect of chronic chromium exposure on the health of Chinook salmon (Oncorhynchus tshawytscha). Aquatic Toxicology, 76, 246–257.

Li, M., Zheng, Y., Liang, H., Zou, L., Sun, J., Zhang, Y., Qin, F., Liu, S., Wang, Z. (2013a). Molecular cloning and characterization of cat, gpx1 and Cu/Zn-sod genes in pengze crucian carp (Carassius auratus var. Pengze) and antioxidant enzyme modulation induced by hexavalent chromium in juveniles. Comparative Biochemistry and Physiology C Toxicology Pharmacology, 157, 310–321.

Karaytug, S., Sevgiler, Y., Karayakar, F. (2014). Comparison of the protective effects of antioxidant compounds in the liver and kidney of Cd- and Cr-exposed common carp. Environmental Toxicology, 29, 129–137.

Lushchak, V.I. (2014a). Free radicals, reactive oxygen species, oxidative stress and its classification. Chemico-Biological Interactions, 224, 164–175.

Lushchak, V.I. (2014b). Classification of oxidative stress based on its intensity. EXCLI Journal, 13, 922-937.

Valko, M., Leibfritz, D., Moncol, J., Cronin, M.T., Mazur, M., Telser, J. (2007). Free radicals and antioxidants in normal physiological functions and human disease. International Journal of Biochemistry and Cell Biology, 39, 44–84.

Salonen, J.T. Seppanen, K. Nyyssonen, K. Koepela, H. Kauhanen, J. Kantola, M. Tuomilehto, J. Esterbauer, H. Tatzber, F. Salonen, R. (1995). Intake of mercury from fish, lipid peroxidation and the risk of myocardial infarction and coronary, cardiovascular, and any death in eastern Finnish men. Circulation, 91, 645– 655.

Gullar, E., Sanz-Gallarado, M.I., Van’t Veer, P., Bode, P., Aro, A., Gomez-Aracen, J., Kark, J.D., Riemersma, R.A., Marin-Moreno, J.M., Kok, F.J. (2002). Mercury, fish oils, and the risk of myocardial infarction. New England Journal of Medicine, 347, 1747–1754.

Hoserova, P., Kuban, V., Spurny, P., Habrata, P. (2006). Determination of total mercury and mercury species in fish and aquatic ecosystems of Moravian rivers. Veterinary Medicine, 51, 101–110.

Stohs, S.J., Bagchi, D. (1995). Oxidative mechanisms in the toxicity of metals ions. Free Radical Bioogical Medicine, 2, 321–336.

Sevikova, M., Modra, H., Slaninova, Z., Svobodova, S. (2011). Metals as a cause of oxidative stress in fish. Veterinary Medicine, 56, 537–546.

Baatrup, E. (1991). Structural and functional effects of heavy metals on the nervous system, including sense organs of fish. Comparative Biochemistry and Physiology, 100, 253–257.

Berntssen, M.H.G., Aatland, A., Handy, R.D. (2003). Chronic dietary mercury exposure causes oxidative stress, brain lesions, and altered behaviour in Atlantic salmon (Salmo salar) parr. Aquatic Toxicology, 65, 55–72.

Ho, N.Y., Yang, L., Legradi, J., Armant, O., Takamiya, M., Rastegar, S., Strähle, U. (2013). Gene responses in the central nervous system of zebrafish embryos exposed to the neurotoxicant methyl mercury. Environmental Science and Technology, 47, 3316–3325.

Wang, M., Wang, Y., Zhang, L., Wang, J., Hong, H., Wang, D. (2013). Quantitative proteomic analysis reveals the mode-of-action for chronic mercury hepatotoxicity to marine medaka (Oryzias melastigma). Aquatic Toxicology, 130–131, 123–131.

Elseady, Y. Zahran, E. (2013). Ameliorating effect of β-carotene on antioxidant response and hematological parameters of mercuric chloride toxicity in Nile tilapia (Oreochromis niloticus). Fish Physiology and Biochemistry, 39, 1031–1041.

Navarro, A., Quiros, L., Casado, M., Faria, M., Carrasco, L., Benejam, L., Benito, J., Diez, S., Raldua, D., Barata, C., Bayona, J.M., Pina, B. (2009). Physiological responses to mercury in feral carp populations inhabiting the low Ebro River (NE Spain), a historically contaminated site. Aquatic Toxicology, 93, 150–157.

Stohs, S.J. Bagchi, D. (1995). Oxidative mechanisms in the toxicity of metals ions. Free Radical Biological Medicine, 2, 321–336.

Sarkar, B. (2002). Heavy Metals in the Environment. Marcel Dekker, Inc. 231-270.

Gomes, J. M., Donnici, C. L., Júnior, J. D. C., da Silva, J. B. B. (2016). Validation of Methods Employing Fast Alkaline Solubilization to Determine Cadmium in Fish Liver, Spleen, Gills and Muscle by Graphite Furnace Atomic Absorption Spectrometry. Microchemical Journal, 124, 629-636. doi:10.1016/j.microc.2015.10.006

Olsvik, P. A., Søfteland, L., Hevrøy, E. M., Rasinger, J. D., Waagbø, R. (2016). Fish pre-acclimation temperature only modestly affects cadmium toxicity in Atlantic salmon hepatocytes. Journal of thermal biology, 57, 21-34. doi:10.1016/j.jtherbio.2016.02.003

Buchwalter, D. B. (2001). Metals. In: Molecular and Biochemical Toxicology. Smart, R. C. Hodgson, E. Wiley, 413-439.

Ercal, N., Gurer-Orhan, H., Aykin-Burns, N. (2001). Toxic metals and oxidative stress part I: Mechanisms involved in metal induced oxidative damage. Current Topics in Medicinal Chemistry, 1, 529–539.

Romeo, M., Bennani, M., Gnassia-Barelli, M., Lafaurie, M., Girard, J.P. (2000). Cadmium and copper display different response towards oxidative stress in the kidney of the sea bass Dicentrarchus labrax. Aquatic Toxicology, 48, 185–194.

De Smet, H., De Wachter, B., Lobinski, R., Blust, B. (2001). Dynamics of (Cd, Zn)-metallothioneins in gills, liver and kidney of common carp Cyprinus carpio during cadmium exposure. Aquatic Toxicology, 52, 269–281.

Jebali, J., Banni, M., Guerbej, H., Almeida, E.A., Bannaoui, A., Boussetta, H. (2006). Effects of malathion and cadmium on acetylcholine esterase activity and metallothionein levels in the fish Seriola dumerilli. Fish Physiology and Biochemistry, 32, 93–98.

Ghedira, J., Jebali, J., Bouraoui, Z., Banni, M., Guerbej, H., Bousetta, H. (2010). Metallothionein and metal levels in liver, gills and kidney of Sparus aurata exposed to sublethal doses of cadmium and copper. Fish Physiology and Biochemistry, 36, 101–107.

Kovarova, J., Celechovska, O., Kizek, R., Adam, V., Harustiakova, D., Svobodova, Z. (2009). Effect of metals, with special attention of Cd, content of the Svitava and Svratka rivers on levels of thiol compounds in fish liver and their use as biochemical markers. Neuroendocrinology Letters, 30, 167–169.

Cao, L., Huang, W., Liu, J., Yin, X., Dou, S. (2010). Accumulation and oxidative stress biomarkers in Japanese flounder larvae and juveniles under chronic cadmium exposure. Comparative Biochemistry and Physiology C, 151, 386–392.

Jia, X., Zhang, H., Liu, X. (2011). Low levels of cadmium exposure induce DNA damage and oxidative stress in the liver of Oujiang colored common carp Cyprinus carpio var. color. Fish Physiology and Biochemistry, 37, 97–103.

Madden, E. F., Sexton, M. J., Smith, D. R., Fowler, B. A. (2002). Lead. In: Heavy Metals in the Environment. Sarkar, B. Marcel Dekker, Inc. 409-456.

Musilova, J., Arvay, J., Vollmannova, A., Toth, T., Tomas, J. (2016). Environmental contamination by heavy metals in region with previous mining activity. Bulletin of environmental contamination and toxicology, 97(4), 569-575.doi:10.1007/s00128-016-1907-3

Buchwalter, D. B. (2001). Metals. In: Molecular and Biochemical Toxicology. Smart, R. C., Hodgson, E., Wiley, 413-439.

Mariussen, E., Heier, L. S., Teien, H. C., Pettersen, M. N., Holth, T. F., Salbu, B., Rosseland, B. O. (2017). Accumulation of lead (Pb) in brown trout (Salmo trutta) from a lake downstream a former shooting range. Ecotoxicology and Environmental Safety, 135, 327-336.doi:10.1016/j.ecoenv.2016.10.008

Has-Schön, E., Bogut, I., Vuković, R., Galović, D., Bogut, A., Horvatić, J. (2015). Distribution and age-related bioaccumulation of lead (Pb), mercury (Hg), cadmium (Cd), and arsenic (As) in tissues of common carp (Cyprinus carpio) and European catfish (Sylurus glanis) from the BuškoBlato reservoir (Bosnia and Herzegovina). Chemosphere, 135, 289-296. doi:10.1016/j.chemosphere.2015.04.015

Shah, S. L. (2006). Hematological parameters in tench Tinca tinca after short term exposure to lead. Journal of applied toxicology. 26(3). 223-228. doi:10.1002/jat.1129

Campana, O., Sarrasquete, C., Blasco, J. (2003). Effect of lead on ALA-D activity, metallothionein levels, and lipid peroxidation in blood, kidney, and liver of the toadfish Halobatrachus didactylus. Ecotoxicology and Environmental Safety, 55, 116–125.

Maiti, A.K., Saha, N.K., Paul, G. (2010). Effect of lead on oxidative stress, Na+ K+ ATPase activity and mitochondrial electron transport chain activity of the brain of Clarias batrachus L. Bulletin Environmental Contamination Toxicology, 84, 672–676.

Kovacik, Anton. (2017). Oxidative Stress in Fish induced by Environmental Pollutants. Scientific Papers Animal Science and Biotechnologies, 50, 121-125.

Costa, C. A., Trivelato, G. C., Pinto, A. M. & Bechara, E. J. (1997). Correlation between plasma 5-aminolevulinic acid concentrations and indicators of oxidative stress in lead-exposed workers. Clinical chemistry, 43(7), 1196-1202.

Bhattacharya, A., Bhattacharya, S. (2007). Induction of oxidative stress by arsenic in Clarias batrachus: Involvement of peroxisomes. Ecotoxicology and Environmental Safety, 66, 178–187.

Wang, Y.C., Chaung, R. H., Tung, C. (2004). Comparison of the cytotoxicity induced by different exposure to sodium arsenite in two fish cell lines. Aquatic Toxicology, 69, 67–79.

Ciardullo, S., Aureli, F., Raggi, A., Cubadda, F. (2010). Arsenic speciation in freshwater fish: Focus on extraction and mass balance. Talanta, 81, 213–221.

Allen, T., Singhal, R., Rana, S.V. (2004). Resistance to oxidative stress in a freshwater fish Channa punctatus after exposure to inorganic arsenic. Biological Trace Element Research, 98, 63–72.

Schlenk, D., Wolford, L., Chelius, M., Steevens, J., Chan, K. M. (1997). Effect of arsenite, arsenate, and the herbicide monosodium methyl arsonate (MSMA) on hepatic metallothionein expression and lipid peroxidation in channel catfish. Comparative Biochemistry and Physiology, 118, 177–1831997.

Seok, S.H., Baek, M.W., Lee, H.Y., Kim, D.J., Na, Y.R., Noh, K.J., Park, S.H., Lee, H.K., Lee, B.H., Ryu, D.Y., Park, J.H. (2007). Arsenite-induced apoptosis is prevented by antioxidants in zebrafish liver cell line. Toxicology In Vitro, 21, 870–877.

Sarkar, S., Mukherjee, S., Chattopadhyay, A., Bhattacharya, S. (2014). Low dose of arsenic trioxide triggers oxidative stress in zebrafish brain: expression of antioxidant genes. Ecotoxicology and Environmetal Safety, 107, 1–8.

Kubrak, O.I., Husak, V.V., Rovenko, B.M., Poigner, H., Kriews, M., Abele, D., Lushchak,V.I. (2013a). Antioxidant system efficiently protects goldfish gills from Ni2+-induced oxidative stress. Chemosphere, 90, 971–976.

Kubrak, O.I., Poigner, H., Husak, V.V., Rovenko, B.M., Meyer, S., Abele, D., Lushchak, V.I. (2014). Goldfish brain and heart are well protected from Ni²⁺-induced oxidative stress. Comparative Biochemistry and Physiology C Toxicology Pharmacology, 162, 43–50.

Kubrak, O.I., Husak, V.V., Rovenko, B.M., Poigner, H., Mazepa, M.A., Kriews, M., Abele, D., Lushchak, V.I. (2012c). Tissue specificity in nickel uptake and induction of oxidative stress in kidney and spleen of goldfish Carassius auratus, exposed to water borne nickel. Aquatic Toxicology, 118–119, 88–96.

Zheng, G.H., Liu, C.M., Sun, J.M., Feng, Z.J., Cheng, C. (2014). Nickel-induced oxidative stress and apoptosis in Carassius auratus liver by JNK pathway. Aquatic Toxicology, 147, 105–111.

Palermo, F.F., Risso, W.E., Simonato, J.D., Martinez, C.B. (2015). Bioaccumulation of nickel and its biochemical and genotoxic effects on juveniles of the neotropical fish Prochilodus lineatus. Ecotoxicology and Environmental Safety, 116,19–28.

Topal, A., Atamanalp, M., Oruç, E., Halıcı, M.B., Şişecioğlu, M., Erol, H.S., Gergit, A., Yılmaz, B. (2015). Neurotoxic effects of nickel chloride in the rainbow trout brain: Assessment of c-Fos activity, antioxidant responses, acetylcholinesterase activity, and histopathological changes. Fish Physiology and Biochemistry, 41, 625–634.

Ates, B., Orun, I., Talas, Z.S., Durmaz, G., Yilmaz, I. (2008). Effects of sodium selenite on some biochemical and hematological parameters of rainbow trout (Oncorhynchus mykiss Walbaum, 1792) exposed to Pb2+ and Cu2+. Fish Physiology and Biochemistry, 34, 53–59.

Orun, I., Talas, Z.S., Ozdemir, I., Alkan, A., Erdogan, K. (2008). Antioxidative role of selenium on some tissues of (Cd2+, Cr3+)-induced rainbow trout. Ecotoxicology and Environmental Safety, 71, 71–75.

Miller, L.L., Wang, F., Palace, W.P., Hontela, A. (2007). Effects of acute and subchronic exposures to waterborne selenite on the physiological stress response and oxidative stress indicators in juvenile rainbow trout. Aquatic Toxicology, 83, 263–271.

Kandemir, S., Dogru, M.I., Orun, I., Dogru, A., Altas, L., Erdogan, K., Orun, G. (2010). Polat. Determination of heavy metal levels, oxidative status, biochemical and hematological parameters in Cyprinus carpio L., 1785 from Bafra (Samsun) fish lakes. Journal of Animal and Veterinary Advances, 9, 617–622.