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Cadmium Accumulation and Antioxidant Responses in Sparus aurata Exposed to Waterborne Cadmium

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Abstract

Cadmium (Cd), a nonessential trace element, is rapidly accumulated by most living organisms and subsequently exerts its toxicity at different molecular levels. This study exposed gilthead sea bream (Sparus aurata) to waterborne 0.1 mg/l Cd for 11 days and investigated the Cd accumulation pattern, lipid oxidation, and response of antioxidant defences. At the end of the experiment, mean Cd concentrations in gills and liver, the organs most prone to metal accumulation, were 209.4 and 371.7 ng/g ww, respectively. Muscle did not show any Cd retention during the 11 days of exposure. In liver, the cytosolic fraction of the metal was chelated into the nontoxic form by metallothionein (MT), a specific Cd-inducible protein. Zn and Cu concentrations were not influenced by Cd exposure. Glutathione (GSH) concentrations and the antioxidant enzyme activities of GSH reductase and GSH peroxidase showed an overall decreasing trend. In addition, lipid and aqueous hydroperoxide levels did not show any significant variation. Oxidative stress indirectly generated by Cd seems to be compensated for by the different biochemical systems tailored to decrease cellular damage. In particular, the negative effects of Cd accumulation in tissues were probably counteracted by the induction of MT.

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References

  • Aït-Aïssa S, Ausseil O, Palluel O, Vindimian E, Garnier-Laplace J, Porcher JM (2003) Biomarker responses in juvenile rainbow trout (Oncorhynchus mykiss) after single and combined exposure to low doses of cadmium, zinc, PCB77 and 17beta-oestradiol. Biomarkers 8:491–508

    Article  Google Scholar 

  • Bagchi D, Bagchi M, Hassoun EA, Stohs SJ (1996) Cadmium-induced excretion of urinary lipid metabolites, DNA damage, glutathione depletion, and hepatic lipid peroxidation in Sprague-Dawley rats. Biol Trace Elem Res 52:143–154

    Article  CAS  Google Scholar 

  • Basha JS, Rani AV (2003) Cadmium-induced antioxidant defence mechanism in fresh water teleost Oreochromis mossambicus (Tilapia). Ecotoxicol Environ Saf 56:218–221

    Article  CAS  Google Scholar 

  • Belyaeva EA, Dymkowska D, Wieckowski MR, Wojtczak L (2008) Mitochondria as an important target in heavy metal toxicity in rat hepatoma AS-30D cells. Toxicol Appl Pharmacol 231:34–42

    Article  CAS  Google Scholar 

  • Carpenè E, Vašàk M (1989) Hepatic metallothioneins from goldfish (Carassius auratus L). Comp Biochem Physiol C Toxicol Pharmacol 92:463–468

    Google Scholar 

  • Carpené E, Serra R, Manera M, Isani G (1999) Seasonal changes of zinc, copper, and iron in gilthead sea bream (Sparus aurata) fed fortified diets. Biol Trace Elem Res 69:121–139

    Article  Google Scholar 

  • Carpenè E, Camatti A, Isani G, Cattani O, Cortesi P (1992) Cd-metallothionein in liver and kidney of goldfish (Carassius auratus): effects of temperature and salinity. Ital J Biochem 41:273–282

    Google Scholar 

  • Cattani O, Serra R, Isani G, Raggi G, Cortesi P, Carpenè E (1996) Correlation between metallothionein and energy metabolism in sea bass Dicentrarchus labrax exposed to cadmium. Comp Biochem Physiol C Toxicol Pharmacol 113:193–199

    Google Scholar 

  • Chowdhury MJ, Grosell M, McDonald DG, Wood CM (2003) Plasma clearance of cadmium and zinc in non-acclimated and metal-acclimated trout. Aquat Toxicol 64:259–275

    Article  CAS  Google Scholar 

  • Cretì P, Trinchella F, Scudiero R (2010) Heavy metal bioaccumulation and metallothionein content in tissues of the sea bream Sparus aurata from three different fish farming systems. Environ Monit Assess 165:321–329

    Article  Google Scholar 

  • Cuypers A, Plusquin M, Remans T, Jozefczak M, Keunen E, Gielen H et al (2010) Cadmium stress: An oxidative challenge. Biometals 23:927–940

    Article  CAS  Google Scholar 

  • Dalla Libera L, Carpenè E, Theibert J, Collins JH (1991) Fish myosin alkali light chains originate from two different genes. J Muscle Res Cell Motil 12:366–371

    Article  CAS  Google Scholar 

  • Dorta DJ, Leite S, De Marco KC, Prado IM, Rodrigues T, Mingatto FE et al (2003) A proposed sequence of events for cadmium-induced mitochondrial impairment. J Inorg Biochem 97:251–257

    Article  CAS  Google Scholar 

  • Eissa BL, Ossana NA, Ferrari L, Salibián A (2010) Quantitative behavioral parameters as toxicity biomarkers: Fish responses to waterborne cadmium. Arch Environ Contam Toxicol 58:1032–1039

    Article  CAS  Google Scholar 

  • Falfushynska HI, Stoliar OB (2009) Function of metallothioneins in carp Cyprinus carpio from two field sites in Western Ukraine. Ecotoxicol Environ Saf 72:1425–1432

    Article  CAS  Google Scholar 

  • Firat O, Cogun HY, Aslanyavrusu S, Kargin F (2009) Antioxidant responses and metal accumulation in tissues of Nile tilapia Oreochromis niloticus under Zn, Cd and Zn + Cd exposures. J Appl Toxicol 29:295–301

    Article  CAS  Google Scholar 

  • Food and Agriculture Organization of the United Nations (2008) Fisheries and Aquaculture Department. http://www.fao.org/fishery/sofia/en. Accessed 2 Apr 2008

  • Food and Agriculture Organization/World Health Organization (1972) Evaluation of certain food additives and the contaminants mercury, cadmium and lead. WHO Technical Report Series No. 505, Geneva, Switzerland

  • Gobe G, Crane D (2010) Mitochondria, reactive oxygen species and cadmium toxicity in the kidney. Toxicol Lett 198:49–55

    Article  CAS  Google Scholar 

  • Hollis L, Hogstrand C, Wood CM (2001) Tissue-specific cadmium accumulation, metallothionein induction, and tissue zinc and copper levels during chronic sublethal cadmium exposure in juvenile rainbow trout. Arch Environ Contam Toxicol 41:468–474

    Article  CAS  Google Scholar 

  • Isani G, Andreani G, Monari M, Carpenè E (2003) Metal concentrations (Cu, Zn and Cd) and metallothionein expression in Sparus aurata exposed to waterborne copper. J Trace Elem Med Biol 17:17–23

    CAS  Google Scholar 

  • Isani G, Andreani G, Cocchioni F, Fedeli D, Carpenè E, Falcioni G (2009) Cadmium accumulation and biochemical responses in Sparus aurata following sub-lethal cadmium exposure. Ecotoxicol Environ Saf 72:224–230

    Article  CAS  Google Scholar 

  • Kamunde C (2009) Early subcellular partitioning of cadmium in gill and liver of rainbow trout (Oncorhynchus mikiss) following low to near lethal waterborne cadmium exposure. Aquat Toxicol 91:291–301

    Article  CAS  Google Scholar 

  • Kamunde C, MacPhail R (2011) Metal-metal interactions of dietary cadmium, copper and zinc in rainbow trout, Oncorhynchus mykiss. Ecotoxicol Environ Saf (in press)

  • Knapen D, Bervoets L, Verheyen E, Blust R (2004) Resistance to water pollution in natural gudgeon (Gobio gobio) populations may be due to genetic adaptation. Aquat Toxicol 67:155–165

    Article  CAS  Google Scholar 

  • Kraal MH, Kraak MSH, De Graat CJ, Davids C (1995) Uptake and tissue distribution of dietary and aqueous cadmium by carp (Cyprinus carpio). Ecotoxicol Environ Saf 31:79–183

    Article  Google Scholar 

  • Lazo JS, Kondo Y, Dellapiazza D, Michalska AE, Choo KH, Pitt BR (1995) Enhanced sensitivity to oxidative stress in cultured embryonic cells from transgenic mice deficient in metallothionein I and II genes. J Biol Chem 270:5506–5510

    Article  CAS  Google Scholar 

  • Liu J, Qu W, Kadiiska MB (2009) Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicol Appl Pharmacol 238:209–214

    Article  CAS  Google Scholar 

  • Martyniuk CJ, Sanchez BC, Szabo NJ, Denslow ND, Sepúlveda MS (2009) Aquatic contaminants alter genes involved in neurotransmitter synthesis and gonadotropin release in largemouth bass. Aquat Toxicol 95:1–9

    Article  CAS  Google Scholar 

  • Messaoudi I, Barhoumi S, Saïd K, Kerken A (2009) Study on the sensitivity to cadmium of marine fish Salaria basilisca (Pisces: Blennidae). J Environ Sci 21:1620–1624

    Article  CAS  Google Scholar 

  • Minghetti M, Leaver MJ, Carpenè E, George SG (2008) Copper transporter 1, metallothionein and glutathione reductase genes are differentially expressed in tissues of sea bream (Sparus aurata) after exposure to dietary or waterborne copper. Comp Biochem Physiol C Toxicol Pharmacol 147:450–459

    Article  CAS  Google Scholar 

  • Mocchegiani E, Giacconi R, Cipriano C, Gasparini N, Orlando F, Stecconi R et al (2002) Metallothioneins (I + II) and thyroid-thymus axis efficiency in old mice: Role of corticosterone and zinc supply. Mech Ageing Dev 123:675–694

    Article  CAS  Google Scholar 

  • Nordberg GF, Jin T, Wu X, Lu J, Chen L, Lei L et al (2009) Prevalence of kidney dysfunction in humans: Relationship to cadmium dose, metallothionein, immunological and metabolic factors. Biochimie 91:1282–1295

    Article  CAS  Google Scholar 

  • Overnell J, McIntosh R, Fletcher TC (1987) The enhanced induction of metallothionein by zinc, its half-life in the marine fish Pleuronectes platessa, and the influence of stress factors on metallothionein levels. Experientia 43:178–181

    Article  CAS  Google Scholar 

  • Part P, Lock RA (1983) Diffusion of calcium, cadmium and mercury in a mucous solution from rainbow trout. Comp Biochem Physiol C Toxicol Pharmacol 76:259–263

    Article  CAS  Google Scholar 

  • Serra R, Isani G, Cattani O, Carpené E (1996) Trace elements variations in Sparus aurata during the growing season. Biol Trace Elem Res 51:107–116

    Article  CAS  Google Scholar 

  • Sheader DL, Williams TD, Lyons BP, Chipman JK (2006) Oxidative stress response of European flounder (Platichthys flesus) to cadmium determined by a custom cDNA microarray. Mar Environ Res 62:33–44

    Article  CAS  Google Scholar 

  • Suren E, Ylmaz S, Turkoglu M, Kaia S (2007) Concentrations of cadmium and lead heavy metals in Dardanelles seawater. Environ Monit Assess 125:91–98

    Article  Google Scholar 

  • Takaki A, Jimi S, Segawa M, Hisano S, Takebayashi S, Iwasaki H (2004) Long-term cadmium exposure accelerates age-related mitochondrial changes in renal epithelial cells. Toxicology 203:145–154

    Article  CAS  Google Scholar 

  • Urena R, Peri S, Del Ramo J, Torreblanca A (2007) Metal and metallothionein content in tissues from wild and farmed Anguilla anguilla at commercial size. Environ Int 33:532–539

    Article  CAS  Google Scholar 

  • Vaglio A, Landriscina C (1999) Changes in liver enzyme activity in the teleost Sparus aurata in response to cadmium intoxication. Ecotoxicol Environ Saf 43:111–116

    Article  CAS  Google Scholar 

  • Waalkes MP (2003) Cadmium carcinogenesis. Mutat Res 533:107–120

    Article  CAS  Google Scholar 

  • Wang Y, Fang J, Leonard SS, Rao KM (2004) Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radic Biol Med 36:1434–1443

    Article  CAS  Google Scholar 

  • Webb M (1987) Toxicological significance of metallothionein. In: Kägi JHR, Kojima Y (eds) Metallothionein II. Birkhauser Verlag, Basel, Germany

    Google Scholar 

  • Williams TD, Diab AM, George SG, Godfrey RE, Sabine V, Conesa A et al (2006) Development of the GENIPOL European flounder (Platichthys flesus) microarray and determination of temporal transcriptional responses to cadmium at low dose. Environ Sci Technol 40:6479–6488

    Article  CAS  Google Scholar 

  • Wright J, George SG, Martinez-Lara E, Carpenè E, Kindt M (2000) Levels of cellular glutathione and metallothionein affect the toxicity of oxidative stressors in an established carp cell line. Mar Environ Res 50:503–508

    Article  CAS  Google Scholar 

  • Wu SM, Shih MJ, Ho YC (2007) Toxicological stress response and cadmium distribution in hybrid tilapia (Oreochromis sp) upon cadmium exposure. Comp Biochem Physiol C Toxicol Pharmacol 145:218–226

    Article  Google Scholar 

  • Zhang L, Wang WX (2007) Gastrointestinal uptake of cadmium and zinc by a marine teleost Acanthopagrus schlegeli. Aquat Toxicol 85:143–153

    Article  CAS  Google Scholar 

  • Zirong X, Shijun B (2007) Effects of waterborne Cd exposure and glutathione metabolism in Nile tilapia (Oreochromis Niloticus) liver. Ecotoxicol Environ Saf 67:89–94

    Article  Google Scholar 

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Acknowledgment

This project was funded by a grant from MIUR (Grant No. 2005073277_001) to E. C.

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Authors and Affiliations

  1. Department of Food Science, “Federico II” University of Naples, Naples, Italy

    T. Cirillo, R. Amodio Cocchieri & E. Fasano

  2. Department of Pathology and Animal Health, “Federico II” University of Naples, Naples, Italy

    A. Lucisano, S. Tafuri & M. C. Ferrante

  3. Department of Medical Veterinary Sciences, Veterinary Medicine Faculty, University of Bologna, via Tolara di Sopra 50, Ozzano Emilia, 60024, Italy

    E. Carpenè, G. Andreani & G. Isani

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  1. T. Cirillo
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  2. R. Amodio Cocchieri
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Correspondence to G. Isani.

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Cirillo, T., Amodio Cocchieri, R., Fasano, E. et al. Cadmium Accumulation and Antioxidant Responses in Sparus aurata Exposed to Waterborne Cadmium. Arch Environ Contam Toxicol 62, 118–126 (2012). https://doi.org/10.1007/s00244-011-9676-9

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  • DOI: https://doi.org/10.1007/s00244-011-9676-9

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