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

  • T. Cirillo
  • R. Amodio Cocchieri
  • E. Fasano
  • A. Lucisano
  • S. Tafuri
  • M. C. Ferrante
  • E. Carpenè
  • G. Andreani
  • G. Isani
Article

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.

Keywords

GSSG Lipid Hydroperoxide Xylenol Orange Provisional Tolerable Weekly Intake Exposed Fish 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgment

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

References

  1. 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 8:491–508CrossRefGoogle Scholar
  2. 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 52:143–154CrossRefGoogle Scholar
  3. Basha JS, Rani AV (2003) Cadmium-induced antioxidant defence mechanism in fresh water teleost Oreochromis mossambicus (Tilapia). Ecotoxicol Environ Saf 56:218–221CrossRefGoogle Scholar
  4. 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 231:34–42CrossRefGoogle Scholar
  5. Carpenè E, Vašàk M (1989) Hepatic metallothioneins from goldfish (Carassius auratus L). Comp Biochem Physiol C Toxicol Pharmacol 92:463–468Google Scholar
  6. 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 69:121–139CrossRefGoogle Scholar
  7. 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 41:273–282Google Scholar
  8. 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 113:193–199Google Scholar
  9. Chowdhury MJ, Grosell M, McDonald DG, Wood CM (2003) Plasma clearance of cadmium and zinc in non-acclimated and metal-acclimated trout. Aquat Toxicol 64:259–275CrossRefGoogle Scholar
  10. 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 165:321–329CrossRefGoogle Scholar
  11. Cuypers A, Plusquin M, Remans T, Jozefczak M, Keunen E, Gielen H et al (2010) Cadmium stress: An oxidative challenge. Biometals 23:927–940CrossRefGoogle Scholar
  12. 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 12:366–371CrossRefGoogle Scholar
  13. 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 97:251–257CrossRefGoogle Scholar
  14. Eissa BL, Ossana NA, Ferrari L, Salibián A (2010) Quantitative behavioral parameters as toxicity biomarkers: Fish responses to waterborne cadmium. Arch Environ Contam Toxicol 58:1032–1039CrossRefGoogle Scholar
  15. Falfushynska HI, Stoliar OB (2009) Function of metallothioneins in carp Cyprinus carpio from two field sites in Western Ukraine. Ecotoxicol Environ Saf 72:1425–1432CrossRefGoogle Scholar
  16. 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 29:295–301CrossRefGoogle Scholar
  17. Food and Agriculture Organization of the United Nations (2008) Fisheries and Aquaculture Department. http://www.fao.org/fishery/sofia/en. Accessed 2 Apr 2008
  18. 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, SwitzerlandGoogle Scholar
  19. Gobe G, Crane D (2010) Mitochondria, reactive oxygen species and cadmium toxicity in the kidney. Toxicol Lett 198:49–55CrossRefGoogle Scholar
  20. 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 41:468–474CrossRefGoogle Scholar
  21. 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 17:17–23Google Scholar
  22. 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 72:224–230CrossRefGoogle Scholar
  23. 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 91:291–301CrossRefGoogle Scholar
  24. Kamunde C, MacPhail R (2011) Metal-metal interactions of dietary cadmium, copper and zinc in rainbow trout, Oncorhynchus mykiss. Ecotoxicol Environ Saf (in press)Google Scholar
  25. 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 67:155–165CrossRefGoogle Scholar
  26. 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 31:79–183CrossRefGoogle Scholar
  27. 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 270:5506–5510CrossRefGoogle Scholar
  28. Liu J, Qu W, Kadiiska MB (2009) Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicol Appl Pharmacol 238:209–214CrossRefGoogle Scholar
  29. 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 95:1–9CrossRefGoogle Scholar
  30. 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 21:1620–1624CrossRefGoogle Scholar
  31. 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 147:450–459CrossRefGoogle Scholar
  32. 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 123:675–694CrossRefGoogle Scholar
  33. 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 91:1282–1295CrossRefGoogle Scholar
  34. 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 43:178–181CrossRefGoogle Scholar
  35. Part P, Lock RA (1983) Diffusion of calcium, cadmium and mercury in a mucous solution from rainbow trout. Comp Biochem Physiol C Toxicol Pharmacol 76:259–263CrossRefGoogle Scholar
  36. Serra R, Isani G, Cattani O, Carpené E (1996) Trace elements variations in Sparus aurata during the growing season. Biol Trace Elem Res 51:107–116CrossRefGoogle Scholar
  37. 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 62:33–44CrossRefGoogle Scholar
  38. Suren E, Ylmaz S, Turkoglu M, Kaia S (2007) Concentrations of cadmium and lead heavy metals in Dardanelles seawater. Environ Monit Assess 125:91–98CrossRefGoogle Scholar
  39. 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 203:145–154CrossRefGoogle Scholar
  40. 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 33:532–539CrossRefGoogle Scholar
  41. Vaglio A, Landriscina C (1999) Changes in liver enzyme activity in the teleost Sparus aurata in response to cadmium intoxication. Ecotoxicol Environ Saf 43:111–116CrossRefGoogle Scholar
  42. Waalkes MP (2003) Cadmium carcinogenesis. Mutat Res 533:107–120CrossRefGoogle Scholar
  43. Wang Y, Fang J, Leonard SS, Rao KM (2004) Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radic Biol Med 36:1434–1443CrossRefGoogle Scholar
  44. Webb M (1987) Toxicological significance of metallothionein. In: Kägi JHR, Kojima Y (eds) Metallothionein II. Birkhauser Verlag, Basel, GermanyGoogle Scholar
  45. 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 40:6479–6488CrossRefGoogle Scholar
  46. 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 50:503–508CrossRefGoogle Scholar
  47. 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 145:218–226CrossRefGoogle Scholar
  48. Zhang L, Wang WX (2007) Gastrointestinal uptake of cadmium and zinc by a marine teleost Acanthopagrus schlegeli. Aquat Toxicol 85:143–153CrossRefGoogle Scholar
  49. Zirong X, Shijun B (2007) Effects of waterborne Cd exposure and glutathione metabolism in Nile tilapia (Oreochromis Niloticus) liver. Ecotoxicol Environ Saf 67:89–94CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • T. Cirillo
    • 1
  • R. Amodio Cocchieri
    • 1
  • E. Fasano
    • 1
  • A. Lucisano
    • 2
  • S. Tafuri
    • 2
  • M. C. Ferrante
    • 2
  • E. Carpenè
    • 3
  • G. Andreani
    • 3
  • G. Isani
    • 3
  1. 1.Department of Food Science“Federico II” University of NaplesNaplesItaly
  2. 2.Department of Pathology and Animal Health“Federico II” University of NaplesNaplesItaly
  3. 3.Department of Medical Veterinary Sciences, Veterinary Medicine FacultyUniversity of BolognaOzzano EmiliaItaly

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