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Acute effects of cadmium on liver phase I and phase II enzymes and metallothionein accumulation on sea bream Sparus aurata

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Abstract

This research was designed to study Sparus aurata (sea bream) biotransformation and detoxification responses to acute exposure to cadmium (Cd). Sexually immature gilthead sea bream were treated by intraperitoneal injection of Cd chloride (200 μg kg−1) for 6, 12, 24 and 48 h. Cd accumulation was quantified in sea bream liver by graphite furnace atomic absorption spectroscopy after the various exposure periods. The following biological responses were measured: (1) ethoxyresorufin-O-deethylase (EROD) activity as phase I biotransformation parameter, (2) liver glutathione-S-transferase (GST) activity as a phase II conjugation enzyme and metallothionein (MT) content as specific response to Cd contamination. Cd bioaccumulation in the liver resulted in an increasing uptake up to 10.3 μg g−1 wet weight after 48 h of exposure. EROD showed a significant activation only after 6 h exposure and a return to control levels after 12 h. GST revealed significant activation starting from 12 h exposure. MT accumulation in liver showed the same behavior as GST activation.

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References

  • Amiard JC, Amiard-Triquet C, Barka S, Pellerin J, Rainbowd P-S (2006) Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquat Toxicol 76:160–202

    Article  PubMed  CAS  Google Scholar 

  • Amiard JC, Pineau A, Boiteau H-L, Metayer C, Amiard-Triquet C (1987) Application de la spectrométrie d’absorption atomique Zeeman aux dosages de huit éléments traces (Ag, Cd, Cr, Cu, Mn, Ni, Pb et Se) dans les matrices biologiques solides. Water Res 21:693–697

    Article  CAS  Google Scholar 

  • Arrigo AP (1999) Gene expression and the thiol redox state. Free Radic Biol Med 27:936–944

    Article  PubMed  CAS  Google Scholar 

  • Banni M, Dondero F, Jebali J, Guerbej H, Boussetta H, Viarengo, A (2007) Assessment of heavy metal contamination using real time PCR analysis of mussel metallothionein mt10 and mt20 expression: a validation along the Tunisian coasts. Biomarkers 12(4): 369–383

    Article  PubMed  CAS  Google Scholar 

  • Banni M, Jebali J, Daubeze M, Clerandau C, Guerbej H, Narbonne JF, Boussetta H (2005) Monitoring pollution in Tunisian coasts: application of a classification scale based on biochemical markers. Biomarkers 10(2–3):105–116

    Article  PubMed  CAS  Google Scholar 

  • Bebianno MJ, Company R, Serafima L, Camus L, Cosson RP, Fiala-Medoni A (2005) Antioxidant systems and lipid peroxidation in Bathymodiolus azoricus from Mid-Atlantic Ridge hydrothermal vent fields. Aquat Toxicol 75:354–373

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Burke MD, Mayer RT (1974) Ethoxyresorufin: direct fluorimetric assay of a microsomal O-deethylation which is preferentially inducible by 3-methylcholanthrene. Drugs Metab Dispos 2:583–588

    CAS  Google Scholar 

  • Casalino E, Sblano C, Landriscina C (1997) Enzyme activity alteration by cadmium administration to rats: the possibility of iron involvement in lipid peroxidation. Arch Biochem Biophys 346:171–179

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Cho MK, Kim SG (2000) Induction of class alpha glutathione S-transferases by 4-methylthiazole in the rat liver: role of oxidative stress. Toxicol Lett 115:107–115

    Article  PubMed  CAS  Google Scholar 

  • Cousinou M, Nilsen UB, Lopez-Barea J, Dorado G (2000) New methods to use fish cytochrome P4501A to assess marine organic pollutants. Sci Total Environ 247:213–225

    Article  PubMed  CAS  Google Scholar 

  • Cvec G (1990) Membrane electrostatics. Biochem Biophys Acta 1031–3:371–382

    Google Scholar 

  • Dalal R, Bhattacharya S (1994) Effect of cadmium, mercury, and zinc on the hepatic microsomal enzymes of Channa punctatus. Bull Environ Toxicol 58:893–897

    Google Scholar 

  • Dua R, Gill KD (2001) Aluminium phosphide exposure: implication on rat brain lipid peroxidation and antioxidant defence system. Pharmacol Toxicol 89:315–319

    Article  PubMed  CAS  Google Scholar 

  • Duquesne S, Richard A (1994) Isolation and characterization of naturally and artificially induced hepatic metallothioneins from two species of flatfish: Limanda limanda and Microstomus kitt. Mar Biol 119:461470

    Article  Google Scholar 

  • Giles MA (1988) Accumulation of cadmium by rainbow trout, Salmo gairdneri, during extended exposure. Can J Fish Aquat Sci 45:1045–1053

    Article  CAS  Google Scholar 

  • Goksoyr A, Forlin L (1992) The cytochrome P-450 system in fish, aquatic toxicology and environmental monitoring. Aquat Toxicol 22:287–313

    Article  Google Scholar 

  • Gravato C, Santos MA (2002) Juvenile sea bass liver P450, EROD induction and erythrocytic genotoxic responses to PAH and PAH-like compounds. Ecotoxicol Environ Saf 51:115–127

    Article  PubMed  CAS  Google Scholar 

  • Habig W, Pabst M, Jakoby W (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249(22):7130–7139

    PubMed  CAS  Google Scholar 

  • Hallenbeck WH (1984) Human health effects of exposure to cadmium. Experientia 40:136–142

    Article  PubMed  CAS  Google Scholar 

  • Jebali J, Banni M, De Alemeida E-A, Bannaoui A, Boussetta H (2006) Effects of malathion and cadmium on acetylcholinesterase activity and metallothionein levels in the fish Seriola dumerilli. Fish Physiol Biochem 32(1):93–98

    Google Scholar 

  • Kafel A, Bednarska K, Augustyniak M, Witas I, Szulinska E (2003) Activity of glutathione S-transferase in Spodoptera exigua larvae exposed to cadmium and zinc in two subsequent generations. Environ Int 28:683–686

    Article  PubMed  CAS  Google Scholar 

  • Kraemer LD, Campbell PGC, Hare L (2005) Dynamics of Cd, Cu and Zn accumulation in organs and sub-cellular fractions in field transplanted juvenile yellow perch (Perca flavescens). Envir Poll 138(2):324–337

    Article  CAS  Google Scholar 

  • Lamb JG, Franklin MR (2000) Early events in the induction of rat hepatic UDP-glucuronosyl-transferase, glutathione S-transferase and microsomal epoxide hydrolase by 1,7-phenanthroline: comparison with oltipraz, tert-butyl-4-hydroxyanisole, and tert-butylhydroquinone. Drug Metab Dispos 28:1018–1023

    PubMed  CAS  Google Scholar 

  • Lane TW, Morel FMM (2000) A biological function for cadmium in marine diatoms. Proc Natl Acad Sci USA 97:4627–4631

    Article  PubMed  CAS  Google Scholar 

  • Lange U, Danischewski D, Siebers D (1993) Regional variability and sexual differences in ethoxyresorufin O-deethylase activities and cytochrome P450 concentration in the liver of mature dab (Limanda limanda L.) in German Bight. In: Braumbeck T, Hunke W, Segner H (eds) Fish ecotoxicology and ecophysiology. VCH Verlag Chemie

  • Lemaire P, Förlin L, Livingstone DR (1996) Responses of hepatic biotransformation and antioxidant enzymes to CYP1A-inducers (3-methylcholanthrene, b-naphthoflavone) in sea bass (Dicentrarchus labrax), dab (Limanda limanda) and rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 36:141–160

    Article  CAS  Google Scholar 

  • Lemaire-Gony S, Lemaire P (1996) Interactive effects of cadmium and BaP on cellular structure and biotransformation enzymes of the liver of the European eel Anguila anguilla. Aquat Toxicol 22: 145–160

    Article  Google Scholar 

  • Lemaire P, Mathieu A, Giudicelli J, Lafaurie M (1992) Effect of BaP on hepatic biotransformation activities: time course of induction in aquaculture European sea bass (Dicentrarchus labrax). Polycyclic Arom Comp 2:263–273

    Article  CAS  Google Scholar 

  • Lemaire-Gony S, Lemaire P, Pulsford A (1995) Effects of cadmium and benzo(a)pyrene on the immune system, gill ATPase and EROD activity of European sea bass Dicentrarchus labrax. Aquat Toxicol 31:297–313

    Article  CAS  Google Scholar 

  • McGeer JC, Szebedinsky C, McDonald DG, Wood CM (2000) Effects of chronic sublethal exposure to waterborne Cu, Cd or Zn in rainbow trout: tissue specific metal accumulation. Aquat Toxicol 50:245–256

    Article  PubMed  CAS  Google Scholar 

  • Monod G, Vindimian E (1991) Effect of storage conditions and subcellular fractionation of fish and cytochrome P-450-dependent enzymatic activities used for the monitoring of water pollution. Water Res 25:173–177

    Article  CAS  Google Scholar 

  • Olsson PE (1993) Metallothionein gene expression and regulation in fish. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes, vol 2. Elsevier Science, pp 259–278

  • Pacheco M, Santos MA (1997) Induction of liver EROD activity and genotoxic effects by polycyclic aromatic hydrocarbons and resin acids on the juvenile eel (Anguilla anguilla L.). Ecotoxicol Environ Saf 38:252–259

    Article  PubMed  CAS  Google Scholar 

  • Rahaman Q, Abidi P, Afaq F, Schiffman D, Mossman BT, Kamp DW, Athar M (1999) Glutathione redox system in oxidative lung injury. Crit Rev Toxicol 29:543–568

    Article  Google Scholar 

  • Rodrıguez-Ariza A, Alhama J, Dıaz-Mendez FM, Lopez-Barea J (1999) Content of 8-oxodG in chromosomal DNA of Sparus aurata fish as biomarker of oxidative stress and environmental pollution. Mutat Res 438:97–107

    PubMed  Google Scholar 

  • Roméo M, Bennani M, 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 48:185–194

    Article  PubMed  Google Scholar 

  • Smaoui-Damak W, Hamza-Chaffaia A, Bebianno M-J, Amiard J-C (2006) Variation of metallothioneins in gills of the clam Ruditapes decussates from the Gulf of Gabe’s (Tunisia). Comp Biochem Phys C 139:181–188

    Google Scholar 

  • Stegeman JJ (1989) Cytochrome P-450 forms in fish: catalytic, immunological and sequences similarities. Xenobiotica 19:1093–l110

    Article  PubMed  CAS  Google Scholar 

  • Stegeman JJ, Hahn ME (1994) Biochemistry and molecular biology of monooxygenases: current perspectives on forms, functions and regulation of cytochrome P450 in aquatic species In: Malins DD, Ostrander GK (eds) Aquatic toxicology. Lewis, Boca Raton, pp 87–206

  • Tocanne JF, Teissie J (1990) Ionization of phospholipids and phospholipid-supported interfacial lateral diffusion of protons in membrane model systems. Biochim Biophys Acta 1031:111–142

    PubMed  CAS  Google Scholar 

  • Tully DB, Collins BJ, Overstreet JD, Smith CS, Mumtaz MM, Chapin RE (2000) Effects of arsenic, cadmium, chromium, and lead on gene expression regulated by a battery of 13 different promoters in recombinant HepG2 cells. Toxicol Appl Pharmacol 168:79–90

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Vallee BL, Ulmer DD (1972) Biochemical effects of mercury, cadmium and lead. Annu Rev Biochem 41:92–128

    Article  Google Scholar 

  • Viarengo A, Bettella E, Fabbri R, Burlando B, Lafaurie M (1997a) Heavy metal inhibition of EROD activity in liver microsomes from the bass Dicentrarchus labrax exposed to organic xenobiotics: role of GSH in the reduction of heavy metal effects. Mar Environ Res 43:1–11

    Article  Google Scholar 

  • Viarengo A, Ponzano E, Dondero F, Fabbri R (1997b) A simple spectrophotometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antarctic molluscs. Mar Env Res 44:69–84

    Article  CAS  Google Scholar 

  • Viarengo A, Burlando B, Cavaletto M, Marchi B, Ponzano E, Blasco J (1999) Role of metallothionein against oxidative stress in the mussel Mytilus galloprovincialis. Am J Physiol 277:1612–1619

    Google Scholar 

  • Viarengo A, Mancinelli G, Pertica M, Fabbri R, Orunesu M (1993) Effects of heavy metals on Ca2+-ATPase activity present in gill cell plasma-membrane of mussels (Mytilus galloprovincialis Lam.). Comp Biochem Physiol 106:655–660

    Article  CAS  Google Scholar 

  • Yousef MI (2004) Aluminium-induced changes in hematobiochemical parameters, lipid peroxidation and enzyme activities of male rabbits: protective role of ascorbic acid. Toxicology 199:47–57

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

A special thanks to the Ministry of Higher Education, Scientific Research and Technology of Tunisia “Unité de Recherche en Biochimie et Toxicologie Environnementale” who allowed this study to be conducted. This research was supported by “Cooperation Inter-Universitaire Franco-Tunisienne (CMCU)” within the framework of the project (04G0907).

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Correspondence to M. Banni or H. Boussetta.

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Bouraoui, Z., Banni, M., Ghedira, J. et al. Acute effects of cadmium on liver phase I and phase II enzymes and metallothionein accumulation on sea bream Sparus aurata . Fish Physiol Biochem 34, 201–207 (2008). https://doi.org/10.1007/s10695-007-9177-y

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