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Effects of Exposure to a Mixture of Cadmium and Chromium on Detoxification Enzyme (GST, P450-MO) Activities in the Frog Rana ridibunda

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Abstract

The effect of two heavy metals, namely chromium and cadmium, on GST and P450-MO activities in the liver, kidney and gut of the frog Rana ridibunda, and the use of these detoxification enzyme systems as possible markers of heavy metal contamination of rivers in Northern Greece was investigated. In control animals, the highest P450-MO activity was observed in the liver and the lowest activity in the gut. As regards GST, the liver and kidneys showed the highest activity. Exposure of Rana to either Cr or a mixture of Cr and Cd caused a decrease in liver GST and P450-MO and renal GST activities. An important finding was that both GST and P450-MO activities were negatively correlated with concentrations of both metals in the liver of mixture-exposed animals. The results suggest that the determination of GST and P450-MO activities, in combination, could serve to indicate heavy metal contamination in rivers of Northern Greece.

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Abbreviations

Cd:

cadmium

CDNB:

1-chloro-2,4-dinitrobenzene

Cr:

chromium

GSH:

reduced glutathione

GST(s):

glutathione S-transferase(s)

pNA:

p-nitroanisole

P450-MO:

cytochrome P450-dependent monooxygenases

References

  • B.J. Alloway (1990) Cadmium B.J. Alloway (Eds) Heavy metals in Soils John Wiley & Sons London 100–24

    Google Scholar 

  • M.M. Almar P.J. Dierickx (1990) ArticleTitleIn vitro interaction of mercury, copper (II) and cadmium with human glutathione transferase π Res. Commun. Chem. Pathol. Pharmacol. 69 99–102

    Google Scholar 

  • K.F. Armstrong D.M. Suckling (1990) ArticleTitleCorrelation of azinphosmethyl resistance with detoxication enzyme activity in the light brown apple moth Epiphyas postvittana (Lepidoptera: Tortricidae) Pestic. Biochem. Physiol. 36 281–9

    Google Scholar 

  • D.H. Barch L.M. Rundhaugen N.S. Pillay (1995) ArticleTitleEllagic acid induces transcription of the rat glutathione S-transferase-Ya gene Carcinogenesis 16 665–8

    Google Scholar 

  • G. Batist A. Tulpule B.K. Sinha A.G. Katki C.E. Myers K.H. Cowan (1986) ArticleTitleOverexpression of a novel anionic glutathione transferase in multi-drug resistant human breast cancer cells J. Biol. Chem. 261 15544–9

    Google Scholar 

  • J. Beyer M. Sandvik J.U. Skaare E. Egaas K. Hylland R. Waagbo A. Goksoyr (1997) ArticleTitleTime- and dose-dependent biomarker responses in flounder (Platichthys flesus L.) exposed to benzo[a]pyrene, 2,3,3,4,4,5-hexachlorobiphenyl (PCB-156) and cadmium Biomarkers 2 35–44

    Google Scholar 

  • M.M. Bradford (1976) ArticleTitleA rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 248–54

    Google Scholar 

  • T. Burgeot G. Bocquene C. Porte J. Dimeet R.M. Santella L.M. Garcia de la Parra A. Pfhol-Leszkowicz C. Raoux F. Galgani (1996) ArticleTitleBioindicators of pollutant exposure in the northwestern Mediterranean Sea Mar. Ecol. Prog. Ser. 131 125–41

    Google Scholar 

  • W. Chen J. Nichols Y. Zhou K.-T. Chung R.W. Hart M.W. Chou (1995) ArticleTitleEffect of dietary restriction on glutathione S-transferase activity specific toward aflatoxin B1-8,9-epoxide Toxicol. Lett. 78 235–43

    Google Scholar 

  • A.G. Clark (1989) ArticleTitleThe comparative enzymology of the glutathione S-transferases from non-vertebrate organisms Comp. Biochem. Physiol. 92B 419–46

    Google Scholar 

  • G. DelBoccio C. Di Ilio M. Miranda A. Manilla O. Zarivi A. Bonfigli G. Federici (1987) ArticleTitleGlutathione transferase activity during Bufo bufo development Comp. Biochem. Physiol. 86B 749–53

    Google Scholar 

  • E. Egaas A. Christiansen O.M. Eklo O. Lode T. Kallqvist (2001) ArticleTitleEffects of a fungicide on glutathione transferase in gill of brown trout (Salmo trutta) Chem.-Biol. Interactions 133 328–30

    Google Scholar 

  • E. Egaas E.G. Jensen J.U. Skaare (1988) ArticleTitleActivities of some microsomal enzymes of the yellow mealworm, Tenebrio molitor (Linné): I. Basal levels and inducibility Pestic. Biochem. Physiol. 30 35–9

    Google Scholar 

  • M. Ehrich C. Larsen (1983) ArticleTitleDrug metabolism in adult white leghorn hens – response to enzyme inducers Comp. Biochem. Physiol. 74C 383–6

    Google Scholar 

  • E. Ernst (1990) ArticleTitleTesticular toxicity following short-term exposure to tri-and hexavalent chromium: an experimental study in the rat Toxicol. Lett. 51 269–75

    Google Scholar 

  • B.K.-M. Gadagbui M. Addy A. Goksoyr (1996) ArticleTitleSpecies characteristics of hepatic biotransformation enzymes in two tropical freshwater teleosts, Tilapia (Oreochromis niloticus) and Mudfish (Clarias anguillaris) Comp. Biochem. Physiol. 114C 201–11

    Google Scholar 

  • E.P. Gallagher R.T. di Giulio (1992) ArticleTitleA comparison of glutathione-dependent enzymes in liver, gills and posterior kidney of channel catfish (Ictalurus punctatus) Comp. Biochem. Physiol. 102C 543–7

    Google Scholar 

  • S. George P. Young M. Leaver D. Clarke (1990) ArticleTitleActivities of pollutant metabolising and detoxication systems in the liver of the plaice, Pleuronectes platessa: sex and seasonal variations in non-induced fish Comp. Biochem. Physiol. 96C 185–92

    Google Scholar 

  • Gerhardsson, L. and Skerfving, S. (1996). Concepts on biological markers and biomonitoring for metal toxicity. In L. Chang (eds). London: Lewis Publishers.

  • E.C. Grose J.H. Richards R.H. Jaskot M.G. Menache J.A. Graham W.C. Dauterman (1987) ArticleTitleGlutathione peroxidase and glutathione transferase activity in rat lung and liver following cadmium inhalation Toxicology 44 171–9

    Google Scholar 

  • W.H. Habig M.J. Pabst W.B. Jakoby (1974) ArticleTitleGlutathione S-transferases: the first enzymatic step in mercapturic acid formation J. Biol. Chem. 249 7130–9

    Google Scholar 

  • V.S. Haritos J.R.J. French J.T. Ahokas (1994) ArticleTitleCytochrome P450 monooxygenase and glutathione S-transferase activity of two Australian termites: Mastotermes darwiniensis and Coptotermes acinaciformis Insect Biochem. Mol. Biol. 24 929–35

    Google Scholar 

  • E. Hodgson (1983) ArticleTitleThe significance of cytochrome P-450 in insects Insect Biochem. 13 237–46

    Google Scholar 

  • A.A. Hunaiti M. Soud (2000) ArticleTitleEffect of lead concentration on the level of glutathione, glutathione S-transferase reductase and peroxidase in human blood Sci. Total Environ. 248 45–50

    Google Scholar 

  • M. Iscan T. Coban B.C. Eke (1994) ArticleTitleDifferential combined effect of cadmium and nickel on hepatic and renal glutathione S-transferases of the guinea pig Environ. Health Perspect. 102 69–72

    Google Scholar 

  • M. Iscan T. Coban B.C. Eke M. Iscan (1993b) ArticleTitleThe responses of hepatic monooxygenases of guinea-pig to cadmium and nickel Biol. Trace Elem. Res. 38 129–37

    Google Scholar 

  • M. Iscan T. Coban B.C. Eke M. Iscan (1995) ArticleTitleDifferential responses of hepatic monooxygenases and glutathione S-transferases of mice to a combination of cadmium and nickel Comp. Biochem. Physiol. 111C 61–8

    Google Scholar 

  • M. Iscan B.C. Eke T. Coban (1993a) ArticleTitleCombined effects of cadmium and nickel on hepatic glutathione S-transferases in rats Comp. Biochem. Physiol. 104C 453–6

    Google Scholar 

  • T. Ishikawa Z.-S. Li Y.-P. Lu P.A. Rea (1997) ArticleTitleThe GS-X pump in plant, yeast, and animal cells: structure, function, and gene expression Bioscience Rep. 17 189–207

    Google Scholar 

  • H. Jensson C. Guthenberg P. Alin B. Mannervik (1986) ArticleTitleRat glutathione transferase 8-8, an enzyme efficiently detoxifying 4-hydroxyalk-2-enals FEBS Lett. 203 207–9

    Google Scholar 

  • R. Karmakar S. Banik S. Bandyopadhyay M. Chatterjee (1998) ArticleTitleCadmium-induced alterations of hepatic lipid peroxidation, glutathione S-transferase activity and reduced glutathione level and their possible correlation with chromosomal aberration in mice: a time course study Mutat. Res. 397 183–90

    Google Scholar 

  • E.D. Karoly R.L. Rose D.M. Thompson E. Hodgson G.C. Rock R.M. Roe (1996) ArticleTitleMonooxygenase, esterase, and glutathione transferase activity associated with azinphosmethyl resistance in the tufted apple bud moth, Platynota idaeusalis Pestic. Biochem. Physiol. 55 109–21

    Google Scholar 

  • I. Kostaropoulos A.I. Papadopoulos (1998) ArticleTitleGlutathione S-transferase isoenzymes expressed in the three developmental stages of the insect Tenebrio molitor Insect Biochem. Mol. Biol. 28 901–9

    Google Scholar 

  • P. Lemaire A. Mathieu J. Giudicelli M. Lafaurie (1992) ArticleTitleEffect of diet on the responses of hepatic biotransformation enzymes to benzo(a)pyrene in the European sea bass (Dicentrarchus labrax) Comp. Biochem. Physiol. 102C 413–20

    Google Scholar 

  • V. Lenartova K. Holovska E. Martinez-Lara J. Lopez-Barea J.A. Barcena I. Rosival (1996) ArticleTitleChanges in GST-isoenzyme pattern of some organs of sheep exposed to different levels of pollution Comp. Biochem. Physiol. 114C 153–8

    Google Scholar 

  • B.A.S. Looise D.A. Holwerda E.M. Foekema (1996) ArticleTitleInduction of glutathione S-transferase in the freshwater bivalve Sphaerium corneum as a biomarker for short-term toxicity tests? Comp. Biochem. Physiol. 113C 103–7

    Google Scholar 

  • N.S. Loumbourdis D. Wray (1998) ArticleTitleHeavy metal concentration in the frog Rana ridibunda from a small river of Macedonia, Northern Greece Environ. Int. 24 427–31

    Google Scholar 

  • R.A. Lubet F.P. Guengerich R.W. Nims (1990) ArticleTitleThe induction of alkoxyresorufin metabolism: a potential indicator of environmental contamination Arch. Environ. Contam. Toxicol. 19 157–63

    Google Scholar 

  • B. Mannervik (1985) ArticleTitleIsoenzymes of glutathione transferase Adv. Enzymol. Mol. Biol. 57 357–417

    Google Scholar 

  • K.A. Marrs (1996) ArticleTitleThe functions and regulation of glutathione S-transferases in plants Annu. Rev. Plant Physiol. Plant Mol. Biol. 47 127–58

    Google Scholar 

  • E. Martinez-Lara F. Toribio J. Lopez-Barea J.A. Barcena (1996) ArticleTitleGlutathione-S-transferase isoenzyme patterns in the gilthead seabream (Sparus aurata) exposed to environmental contaminants Comp. Biochem. Physiol. 113C 215–20

    Google Scholar 

  • S. McGuire D.A. Daggett E. Bostad S. Nelson L.S. Wright F.L. Siegel S. Kornguth (1997) ArticleTitleIncreased levels of glutathione S-transferases and appearance of novel alpha class isoenzymes in kidneys of mice exposed to mercuric chloride: I. Biochemical, immunohistochemical studies Nephron 77 452–60

    Google Scholar 

  • K. Mitsumori M. Shibutani S. Sato H. Onodera J. Nakagawa Y. Hayashi Y. Ando (1998) ArticleTitleRelationship between the development of hepato-renal toxicity and cadmium accumulation in rats given minimum to large amounts of cadmium chloride in the long-term: preliminary study Arch. Toxicol. 72 545–52

    Google Scholar 

  • P.W. Mueller R.G. Price W.F. Finn (1998) ArticleTitleNew approaches for detection thresholds of human nephrotoxicity using cadmium as an example Environ. Health Persp. 106 227–30

    Google Scholar 

  • Peterson, L.A. and Guengerich, F.P. (1988). Comparison of and relationships between glutathione S-transferase and cytochrome P-450 systems. In H. Sies and B. Ketterer (eds). London: Academic Press. 254–9.

  • F.W. Plapp SuffixJr. (1984) ArticleTitleThe genetic basis of insecticide resistance in the house fly: evidence that a single locus plays a major role in metabolic resistance to insecticides Pestic. Biochem. Physiol. 22 194–201

    Google Scholar 

  • P. Puccini S. Menicagli V. Longo A. Santucci P.G. Gervasi (1992) ArticleTitlePurification and characterization of an acetone-inducible cytochrome P-450 from hamster liver microsomes Biochem. J. 287 863–70

    Google Scholar 

  • H. Ranson L. Prapanthadara J. Hemingway (1997) ArticleTitleCloning and characterization of two glutathione S-transferases from a DDT-resistant strain of Anopheles gambiae Biochem. J. 324 97–102

    Google Scholar 

  • M. Sidhu R. Prasad K.D. Gill R. Nath (1997) ArticleTitleAlterations in isoforms of glutathione S-transferase in liver and kidney of cadmium exposed rhesus monkeys: purification and kinetic characterization Mol. Cell. Biochem. 166 55–63

    Google Scholar 

  • C.-P. Siegers M. Schenke M. Younes (1987) ArticleTitleInfluence of cadmium chloride, mercuric chloride, and sodium vanadate on the glutathione-conjugating enzyme system in liver, kidney, and brain of mice J. Toxicol. Environ. Health 22 141–8

    Google Scholar 

  • I.G. Sipes A.J. Gandolfi (1991) Biotransformation of toxicants M.O. Amdur J. Doull C.D. Klaassen (Eds) Casarett and Doull’s toxicology: the basic science of Poisons EditionNumber4 Pergamon Press New York 88–126

    Google Scholar 

  • D. Stone P. Jepson R. Laskowski (2002) ArticleTitleTrends in detoxification enzymes and heavy metal accumulation in ground beetles (Coleoptera: Carabidae) inhabiting a gradient of pollution Comp. Biochem. Physiol. 132C 105–12

    Google Scholar 

  • K.H. Tan D.J. Meyer N. Gillies B. Ketterer (1988) ArticleTitleDetoxification of DNA hydroperoxide by glutathione transferases and the purification and characterization of glutathione transferases of the rat liver nucleus Biochem. J. 254 841–5

    Google Scholar 

  • S.-S. Tang C.-C. Lin G.-G. Chang (1996) ArticleTitleMetal-catalyzed oxidation and cleavage of Octopus glutathione transferase by the Cu(II)-ascorbate system Free Radical Biol. Med. 7 955–64

    Google Scholar 

  • A.K. Vogiatzis N.S. Loumbourdis (1998) ArticleTitleCadmium accumulation in liver and kidneys and hepatic metallothionein and glutathione levels in Rana ridibunda after exposure to CdCI2 Arch. Environ. Contam. Toxicol. 34 64–8

    Google Scholar 

  • A.K. Vogiatzis N.S. Loumbourdis (1999) ArticleTitleA study of glycogen, lactate, total fats, protein and glucose concentration in the liver of the frog Rana ridibunda after exposure to cadmium for 30 days Environ. Pollut. 104 335–40

    Google Scholar 

  • M. Watanabe K. Henmi K. Ogawa T. Suzuki (2003) ArticleTitleCadmium-dependent generation of reactive oxygen species and mitochondrial DNA breaks in photosynthetic and non-photosynthetic strains of Euglena gracilis Comp. Biochem. Physiol. 134C 227–34

    Google Scholar 

  • WHO (World Health Organization) (1988). Chromium. In Environmental Health Criteria, 61, 1–197, Geneva

  • L.S. Wright S.E. Kornguth T.D. Oberley F.L. Siegel (1998) ArticleTitleEffects of lead on glutathione S-transferase expression in rat kidney: a dose-response study Toxicol. Sci. 46 254–9

    Google Scholar 

  • K. Zaman R.S. MacGill J.E. Johnson S. Ahmad R.S. Pardini (1994) ArticleTitleAn insect model for assessing mercury toxicity: effect of mercury on antioxidant enzyme activities of the housefly (Musca domestica) and the cabbage looper moth (Ttrichoplusia ni) Arch. Environ. Contam. Toxicol. 26 114–8

    Google Scholar 

  • G. Zhao R.L. Rose E. Hodgson R.M. Roe (1996) ArticleTitleBiochemical mechanisms and diagnostic microassays for pyrethroid, carbamate, and organophosphate insecticide resistance/cross-resistance in the tobacco budworm, Heliothis virescens Pestic. Biochem. Physiol. 56 183–95

    Google Scholar 

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Correspondence to Nikolaos S. Loumbourdis.

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Kostaropoulos, I., Kalmanti, D., Theodoropoulou, B. et al. Effects of Exposure to a Mixture of Cadmium and Chromium on Detoxification Enzyme (GST, P450-MO) Activities in the Frog Rana ridibunda. Ecotoxicology 14, 439–447 (2005). https://doi.org/10.1007/s10646-004-1349-2

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  • DOI: https://doi.org/10.1007/s10646-004-1349-2

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