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Perturbations in ROS-related processes of the fish Gambusia holbrooki after acute and chronic exposures to the metals copper and cadmium

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Abstract

Metallic contamination is a widespread phenomena, particularly in areas impacted by human activities, and has become a relevant environmental concern. However, the toxicity of metals on fish requires full characterization in terms of short- and long-term effects. Thus, the purpose of this study was to determine the acute and chronic oxidative stress response in liver and gills of Gambusia holbrooki exposed to copper and cadmium. To assess the effects of these two metals, we adopted a strategy of analyzing the pollution effects caused by salts of the two metallic elements, and we quantified the oxidative stress biomarkers catalase, glutathione reductase, glutathione-S-transferases, and lipid peroxidation after exposure (4 and 28 days) to ecologically relevant concentrations, thus simulating actual conditions of exposure in the wild. Our results showed that copper elicited strong effects in all tested biomarkers for both acute and chronic challenges. Cadmium caused a similar response and was shown to cause significant changes particularly in catalase and glutathione-S-transferases activities. These findings evidence that ecologically relevant concentrations of common anthropogenic contaminants are causative agents of serious imbalances (namely oxidative stress) that are likely to trigger life-threatening events.

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References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 6:105–121

    Google Scholar 

  • Ahmad I, Oliveira M, Pacheco M, Santos MA (2005) Anguilla anguilla L. oxidative stress biomarkers responses to copper exposure with or without b-naphthoflavone pre-exposure. Chemosphere 61:267–275

  • Almeida JA, Diniz YS, Marques SFG, Faine LA, Ribas BO, Burneiko RC, Novelli ELB (2002) The use of the oxidative stress responses as biomarkers in Nile tilapia (Oreochromis niloticus) exposed to in vivo cadmium contamination. Environ Int 27:673–679

    Article  CAS  Google Scholar 

  • Banni M, Chouchene L, Said K, Kerkeni A, Messaoudi I (2011) Mechanisms underlying the protective effect of zinc and selenium against cadmium-induced oxidative stress in zebrafish Danio rerio. Biometals 24(6):981–992

    Article  CAS  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310

    Article  CAS  Google Scholar 

  • Carlberg I, Mannervik B (1985) Glutathione reductase. Methods Enzymol 113:484–490

    Article  CAS  Google Scholar 

  • Espinoza HM, Williams CR, Gallagher EP (2012) Effect of cadmium on glutathione S-transferase and metallothionein gene expression in coho salmon liver, gill and olfactory tissues. Aquat Toxicol 110–111:37–44

    Article  Google Scholar 

  • Eyckmans M, Celis N, Horemans N, Blust R, De Boeck G (2011) Exposure to waterborne copper reveals differences in oxidative stress response in three freshwater fish species. Aquat Toxicol 103:112–120

    Article  CAS  Google Scholar 

  • Fernandes C, Fontaínhas-Fernandes A, Cabral D, Salgado MA (2008). Heavy metals in water, sediment and tissues of Liza saliens from Esmoriz–Paramos lagoon, Portugal. Environ Monit Assess 136:267–275

  • Ferreira, J.G., Simas, T., Nobre, A., Silva, M.C., Shifferegger, K., Lencart-Silva, J. (2003). Identification of Sensitive Areas and Vulnerable Zones in Transitional and Coastal Portuguese Systems – Application of the United States National Estuarine Eutrophication Assessment to the Minho, Lima, Douro, Ria de Aveiro, Mondego, Tagus, Sado, Mira, Ria Formosa and Guadiana Systems. Edited by Instituto da Água and Institute of Marine Research, Portugal

  • Firat O, Kargin F (2010) Effects of zinc and cadmium on erythrocyte antioxidant systems of a freshwater fish Oreochromis niloticus. J Biochem Mol Toxicol 24(4):223–229

    Article  CAS  Google Scholar 

  • García-Fernández AJ, Bayoumi AE, Pérez-Pertejo Y, Motas M, Reguera RM, Ordóñez C, Balaña-Fouce R, Ordóñez D (2002) Alterations of the glutathione–redox balance induced by metals in CHO-K1 cells. Comp Biochem Physiol C Toxicol Pharmacol 132(3):365–373

    Article  Google Scholar 

  • Gravato C, Teles M, Oliveira M, Santos MA (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(10):1821–1830

    Article  CAS  Google Scholar 

  • Greco L, Serrano R, Blanes MA, Serrano E, Capri E (2010) Bioaccumulation markers and biochemical responses in European sea bass (Dicentrarchus labrax) raised under different environmental conditions. Ecotoxicol Environ Saf 73:38–45

    Article  CAS  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7137

    CAS  Google Scholar 

  • 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 Physiol Biochem 37(1):97–103

    Article  CAS  Google Scholar 

  • Jiang W-D, Wua P, Kuang S-Y, Liu Y, Jiang J, Hu K, Li S-H, Tang L, Feng L, Zhou X-Q (2011) Myo-inositol prevents copper-induced oxidative damage and changes in antioxidant capacity in various organs and the enterocytes of juvenile Jian carp (Cyprinus carpio var. Jian). Aquat Toxicol 105:543–551

    Article  CAS  Google Scholar 

  • Jin Y, Zhang X, Shu L, Chen L, Sun L, Qian H, Liu W, Fu Z (2010) Oxidative stress response and gene expression with atrazine exposure in adult female zebrafish (Danio rerio). Chemosphere 78:846–852

    Article  CAS  Google Scholar 

  • Johnston BD, Scown TM, Moger J, Cumberland SA, Baalousha M, Linge K, van Aerle R, Jarvis K, Lead JR, Tyler CR (2010) Bioavailability of nanoscale metal oxides TiO2, CeO2, and ZnO to fish. Environ Sci Technol 44:1144–1151

    Article  CAS  Google Scholar 

  • Jomova K, Valko M (2011) Advances in metal-induced oxidative stress and human disease. Toxicology 283:65–87

    Article  CAS  Google Scholar 

  • Lapointe D, Pierron F, Couture P (2011) Individual and combined effects of heat stress and aqueous or dietary copper exposure in fathead minnows (Pimephales promelas). Aquat Toxicol 104:80–85

    Article  CAS  Google Scholar 

  • Liu X-D, Thiele DJ (1997) Yeast metallothionein gene expression in response to metals and oxidative stress. Methods 11(3):289–299

    Article  CAS  Google Scholar 

  • López-Galindo C, Vargas-Chacoff L, Nebot E, Casanueva JF, Rubio D, Solé M, Mancera JM (2010) Biomarker responses in Solea senegalensis exposed to sodium hypochlorite used as antifouling. Chemosphere 78:885–893

    Article  Google Scholar 

  • Lushchak VI (2011a) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30

    Article  CAS  Google Scholar 

  • Lushchak VI (2011b) Adaptive response to oxidative stress: bacteria, fungi, plants and animals. Comp Biochem Physiol C 153:175–190

    Google Scholar 

  • Modesto KA, Martinez CBR (2010) Roundup (R) causes oxidative stress in liver and inhibits acetylcholinesterase in muscle and brain of the fish Prochilodus lineatus. Chemosphere 78:294–299

    Article  CAS  Google Scholar 

  • Mucha AP, Vasconcelos MT, Bordalo AA (2003) Macrobenthic community in the Douro estuary: relations with trace metals and natural sediment characteristics. Environ Pollut 121(2):169–180

    Article  CAS  Google Scholar 

  • Ninh Pham A, Xing G, Miller CJ, Waite TD (2013) Fenton-like copper redox chemistry revisited: hydrogen peroxide and superoxide mediation of copper-catalyzed oxidant production. J Catal 301:54–64

    Article  Google Scholar 

  • Nunes B, Carvalho F, Guilhermino L (2004) Acute and chronic effects of clofibrate and clofibric acid on the enzymes acetylcholinesterase, lactate dehydrogenase and catalase of the mosquitofish, Gambusia holbrooki. Chemosphere 57:1581–1589

    Article  CAS  Google Scholar 

  • Nunes B, Gaio R, Carvalho F, Guilhermino L (2008) Behaviour and biomarkers of oxidative stress in Gambusia holbrooki after acute exposure to widely used pharmaceuticals and a detergent. Ecotoxicol Environ Saf 71:341–354

    Article  CAS  Google Scholar 

  • OECD (1992) Test no. 203: fish, acute toxicity test. OECD Guidel Test Chem 1(2):1–9

    Google Scholar 

  • OECD (2000) Test no. 215: fish, juvenile growth test. OECD Guidel Test Chem 1(2):1–16

    Google Scholar 

  • OECD (2002) Guidance document on aquatic ecotoxicology in the context of the Directive 91/414/EEC. European Commission Health & Consumer Protection Directorate-General, Directorate E-Food Safety: plant health, animal health and welfare, international questions, E1-Plant health: 1–61

  • Ognjanovic BI, Dorordevic NZ, Perendndija BR, Despotootovic SG, Žikic RV, Štajn AS, Saicic ZS (2008) Concentration of antioxidant compounds and lipid peroxidation in the liver and white muscle of hake (Merluccius merluccius L.) in the Adriatic Sea. Arch Biol Sci 60:601–607

    Article  Google Scholar 

  • Olivari FA, Hernández PP, Allende ML (2008) Acute copper exposure induces oxidative stress and cell death in lateral line hair cells of zebrafish larvae. Brain Res 1244:1–12

    Article  CAS  Google Scholar 

  • Pretto A, Loro VL, Baldisserotto B, Pavanato MA, Moraes BS, Menezes C, Cattaneo R, Clasen B, Finamor IA, Dressler V (2011) Effects of water cadmium concentrations on bioaccumulation and various oxidative stress parameters in Rhamdia quelen. Arch Environ Contam Toxicol 60(2):309–318

    Article  CAS  Google Scholar 

  • Pytharopoulou S, Grintzalis K, Sazakli E, Leotsinidis M, Georgiou CD, Kalpaxis DL (2011) Translational responses and oxidative stress of mussels experimentally exposed to Hg, Cu and Cd: one pattern does not fit at all. Aquat Toxicol 105:157–165

    Article  CAS  Google Scholar 

  • Rensing C, Rosen BP (2009) Heavy metals cycle (arsenic, mercury, selenium, others). Encyclopedia of microbiology, 3rd edn. Academic, p 205–219

  • Sáez MI, Casas JJ, Guil-Gerrero JL, Gil MD, Cañero R, Suárez MD (2013a) Effects of organic matter, alkalinity and pH on acute copper toxicity to mosquitofish, Gambusia holbrooki: Implications for a multipurpose management of irrigation ponds. Int Rev Hydrobiol 98:1–9

    Article  Google Scholar 

  • Sáez MI, García-Mesa S, Casas JJ, Guil-Guerrero LJ, Venegas-Venegas CE, Morales AE, Suárez MD (2013b) Effect of sublethal concentrations of waterborne copper on lipid peroxidation and enzymatic antioxidant response in Gambusia holbrooki. Environ Toxicol Pharmacol 36:125–134

    Article  Google Scholar 

  • Saini N, Oelhafen S, Hua H, Georgiev O, Schaffner W, Büeler H (2010) Extended lifespan of Drosophila parkin mutants through sequestration of redox-active metals and enhancement of anti-oxidative pathways. Neurobiol Dis 40(1):82–92

    Article  CAS  Google Scholar 

  • Sanchez A, Palluel O, Meunier L, Coquery M, Porcher J-M, Aït-Aïssaa S (2005) Copper-induced oxidative stress in three-spined stickleback: relationship with hepatic metal levels. Environ Toxicol Pharmacol 19:177–183

    Article  CAS  Google Scholar 

  • Serafim A, Company R, Lopes B, Rosa J, Cavaco A, Castela G, Castela E, Olea N, Bebianno MJ (2012) Assessment of essential and nonessential metals and different metal exposure biomarkers in the human placenta in a population from the south of Portugal. J Toxicol Environ Health A 75(13–15):867–877

    Article  CAS  Google Scholar 

  • Shaikh ZA, Vu TT, Zaman K (1999) Oxidative stress as a mechanism of chronic cadmium-induced hepatotoxicity and renal toxicity and protection by antioxidants. Toxicol Appl Pharmacol 154:256–263

    Article  CAS  Google Scholar 

  • Soares SS, Martins H, Gutiérrez-Merino C, Aureliano M (2008) Vanadium and cadmium in vivo effects in teleost cardiac muscle: metal accumulation and oxidative stress markers. Comp Biochem Physiol C 147:168–178

    CAS  Google Scholar 

  • Vergauwen L, Hagenaars A, Blusta R, Knapen D (2013) Temperature dependence of long-term cadmium toxicity in the zebrafish is not explained by liver oxidative stress: evidence from transcript expression to physiology. Aquat Toxicol 126:52–62

    Article  CAS  Google Scholar 

  • Vieira LR, Gravato C, Soares AMVM, Morgado F, Guilhermino L (2009) Acute effects of copper and mercury on the estuarine fish Pomatoschistus microps: linking biomarkers to behaviour. Chemosphere 76:1416–1427

    Article  CAS  Google Scholar 

  • Wang X, Fang H, Huang Z, Shang W, Hou T, Cheng A, Cheng H (2013) Imaging ROS signaling in cells and animals. J Mol Med 91(8):917–927

    Article  CAS  Google Scholar 

  • Won E-J, Rhee J-S, Kim R-O, Ra K, Kim K-T, Shin K-H, Lee J-S (2012) Susceptibility to oxidative stress and modulated expression of antioxidant genes in the copper-exposed polychaete Periunereis nuntia. Comp Biochem Physiol C 155:344–351

    CAS  Google Scholar 

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Acknowledgments

Joana L. Pereira is recipient of an individual scholarship by the Portuguese Foundation for Science and Technology (SFRH/BPD/44733/2008). This study was supported by FEDER funds through the program COMPETE and by national funds through FCT under the scope of the project BiOtoMetal (PTDC/AMB/70431/2006).

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Authors and Affiliations

  1. Departamento de Biologia, Centro de Estudos do Ambiente e do Mar (CESAM), Universidade de Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal

    Bruno Nunes, Carina Caldeira, Joana Luísa Pereira & Fernando Gonçalves

  2. Faculdade de Ciências da Saúde, Universidade Fernando Pessoa, Rua Carlos da Maia 296, 4200-150, Porto, Portugal

    Alberto Teodorico Correia

  3. Centro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR–CIMAR), Rua dos Bragas 289, 450-123, Porto, Portugal

    Alberto Teodorico Correia

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  1. Bruno Nunes
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  2. Carina Caldeira
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  3. Joana Luísa Pereira
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  4. Fernando Gonçalves
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  5. Alberto Teodorico Correia
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Correspondence to Bruno Nunes.

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Responsible editor: Philippe Garrigues

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Nunes, B., Caldeira, C., Pereira, J.L. et al. Perturbations in ROS-related processes of the fish Gambusia holbrooki after acute and chronic exposures to the metals copper and cadmium. Environ Sci Pollut Res 22, 3756–3765 (2015). https://doi.org/10.1007/s11356-014-3580-6

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  • DOI: https://doi.org/10.1007/s11356-014-3580-6

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