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Effects of tributyltin (TBT) on enzyme activity and oxidative stress in hepatopancreas and hemolymph of small abalone, Haliotis diversicolor supertexta

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Abstract

We investigated the effect of tributyltin (TBT) exposure on the concentration of malondialdehyde (MDA) and the activity levels of the superoxide dismutase (SOD), catalase (CAT), and acid and alkaline phosphatase (ACP and AKP) enzymes in the small abalone, Haliotis diversicolor supertexta. We collected samples of the hepatopancreas and hemolymph 2, 6, 24, 48, 96, and 192 h after exposure to 0.35 µg (Sn)/L TBT. In the hepatopancreas, ACP activity was significantly higher in animals exposed to TBT 2, 24, and 96 h post-exposure compared with the control animals. AKP activity was also higher after 2 h, but SOD and CAT activity was unchanged. The concentration of MDA in the hemolymph was significantly higher than the control animals 2 and 6 h post-exposure. In the hemolymph of animals exposed to TBT, ACP activity was significantly lower than in the control animals 192 h post-exposure, whereas AKP activity was significantly lower 2 and 192 h post-exposure. Hemolymph SOD activity and levels of MDA were significantly lower than in the control animals 24 h after exposure but significantly higher after 96 h. Our results demonstrate that exposure to TBT cause rapid changes in ACP and AKP activity as well as altering the concentration of MDA in the hepatopancreas and hemolymph. SOD and CAT do not appear to be involved in the detoxification of TBT in the hepatopancreas of small abalone.

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References

  • Aebi H. 1984. Catalase in vitro. Meth. Enzymol., 105: 121–126.

    Article  Google Scholar 

  • Axiak V, Vella A J, Agius D, Bonnici P, Cassar G, Cassone R, Chircop P, Micallef D, Mintoff B, Sammut M. 2000. Evaluation of environmental levels and biological impact of TBT in Malta (central Mediterranean). Sci. Total Environ., 258: 89–97.

    Article  Google Scholar 

  • Barrett A J. 1972. Lysosomal enzymes. In: Dingle JT (Ed.), Lysosomes: A Laboratory Handbook. North-Holland, Amsterdam. p. 46–135.

    Google Scholar 

  • Bekri K, Saint-Louis R, Pelletier E. 2006. Determination of tributyltin and 4-hydroxybutyldibutyltin chlorides in seawater by liquid chromatography with atmospheric pressure chemical ionization-mass spectrometry. Anal. Chim. Acta, 578: 203–212.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Buggy C J, Tobin J M. 2006. Seasonal and spatial distributions of tributyltin in surface sediment of the Tolka Estuary, Dublin, Ireland. Environ. Pollut., 143: 294–303.

    Article  Google Scholar 

  • Cajaraville M P, Bebianno M J, Blasco J, Porte C, Sarasquete C, Viarengo A. 2000. The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a practical approach. Sci. Total Environ., 247: 295–311.

    Article  Google Scholar 

  • Celik I. 2007. Determination of toxicity of trichloroacetic acid in rats: 50 days drinking water study. Pestic. Biochem. Physiol., 89: 39–45.

    Article  Google Scholar 

  • Champ M A. 2000. A review of organotin regulatory strategies, pending actions, related costs and benefits. Sci. Total Environ., 258: 21–71.

    Article  Google Scholar 

  • Enan E E, Enan O H, El-Sebae A E. 1982. Biochemical target affected by sub-lethal doses of organophosphorus insecticides. Int. Pest Control., 24: 120–122.

    Google Scholar 

  • Esterbauer H, Cheeseman K H. 1990. Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal. Meth. Enzymol., 186: 407–421.

    Article  Google Scholar 

  • Feng S Y. 1988. Cellular defense mechanisms of oysters and mussels. Am. Fish. Soc. Spec. Publ., 18: 153–168.

    Google Scholar 

  • Funes V, Alhama J, Navas J I, Lopez-Barea J, Peinado J. 2006 Ecotoxicological effects of metal pollution in two mollusc species from the Spanish South Atlantic littoral. Environ Pollut., 139: 214–223.

    Article  Google Scholar 

  • Geiger D L. 1999. Distribution and biogeography of the recent Haliotidae (Gastropoda: Vetigastropod) world-wide. Boll. Malacol., 35: 57–120.

    Google Scholar 

  • Georgiades E T, Holdway D A, Brennan S E, Butty J S, Temara A. 2003. The impact of oil-derived products on the behaviour and biochemistry of the eleven-armed asteroid Coscinasterias muricata (Echinodermata). Mar. Environ. Res., 55: 257–276.

    Article  Google Scholar 

  • Geret F, Serafim A, Barreira L, Maria J B. 2002. Response of antioxidant systems to copper in the gills of the clam Ruditapes decussatus. Mar. Environ. Res., 54: 413–417.

    Article  Google Scholar 

  • Gronczewska J, Biegniewska A, Zietara M S, Skorkowski E F. 2004. Inhibition by tributyltin of herring skeletal muscle lactate dehydrogenase activity. Comp. Biochem. Physiol. C, Comp. Pharmacol. Toxicol., 137: 307–311.

    Article  Google Scholar 

  • Grzyb K, Rychlowski M, Biegniewska A, Skorkowski E F. 2003. Quantitative determination of creatine kinase release from herring (Clupea harengus) spermatozoa induced by tributyltin. Comp. Biochem. Physiol. C, Comp. Pharmacol. Toxicol., 135: 207–213.

    Article  Google Scholar 

  • Hønsi T G, Stenersen J. 2000. Activity and localisation of the lysosomal marker enzymes acid phosphatase, N-acetyl-β-D-glucosaminidase, and β-galactosidase in the earthworms Eisenia fetida and E. veneta. Comp. Biochem. Physiol. B, Biochem. Mol. Biol., 125: 429–437.

    Article  Google Scholar 

  • Horiguchi T, Kojima M, Kaya M, Matsuo T, Shiraishi H, Morita M, Adachi Y. 2002. Tributyltin and triphenyltin induce spermatogenesis in ovary of female abalone, Haliotis gigantea. Mar. Environ. Res., 54: 679–684.

    Article  Google Scholar 

  • Horiguchi T, Kojima M, Takiguchi N, Kaya M, Shiraishi H, Morita M. 2005. Continuing observation of disturbed reproductive cycle and ovarian spermatogenesis in the giant abalone, Haliotis madaka from an organotin-contaminated site of Japan. Mar. Pollut. Bull., 51: 817–822.

    Article  Google Scholar 

  • Horiguchi T, Takiguchi N, Cho H S, Kojima M, Kaya M, Shiraishi H, Morita M, Hirose H, Shimizu M. 2000. Ovo-testis and disturbed reproductive cycle in the giant abalone, Haliotis madaka: possible linkage with organotin contamination in a site of population decline. Mar. Environ. Res., 50: 223–229.

    Article  Google Scholar 

  • Hunt J W, Anderson B S. 1989. Sublethal effects of zinc and municipal effluents on larvae of the red abalone Haliotis rufescens. Mar. Biol., 101: 545–552.

    Article  Google Scholar 

  • Inoue S, Oshima Y, Usuki H, Hamaguchi M, Hanamura Y, Kai N, Shimasaki Y, Honjo T. 2006. Effects of tributyltin maternal and/or waterborne exposure on the embryonic development of the Manila clam, Ruditapes philippinarum. Chemosphere, 63: 881–888.

    Article  Google Scholar 

  • Inoue S, Oshima Y, Usuki H, Hamaguchi M, Hanamura Y, Kai N, Shimasaki Y, Honjo T. 2007. Effect of tributyltin on veliger larvae of the Manila clam, Ruditapes philippinarum. Chemosphere, 66: 1 353–1 357.

    Google Scholar 

  • Jiang G B, Zhou Q F, Liu J Y, Wu D J. 2001. Occurrence of butyltin compounds in the waters of selected lakes, rivers and coastal environments from China. Environ. Pollut., 115: 81–87.

    Article  Google Scholar 

  • Liao C M, Ling M P. 2004. Probabilistic risk assessment of abalone Haliotis diversicolor supertexta exposed to waterborne zinc. Environ. Pollut., 127: 217–227.

    Article  Google Scholar 

  • Liu H G, Wang Y, Lian L, Xu L H. 2006. Tributyltin induces DNA damage as well as oxidative damage in rats. Environ Toxicol., 21: 166–171.

    Article  Google Scholar 

  • Livingstone D R. 2001. Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar. Pollut. Bull., 42: 656–666.

    Article  Google Scholar 

  • Matozzo V, Ballarin L, Marin M G. 2004. Exposure of the clam Tapes philippinarum to 4-nonylphenol: changes in anti-oxidant enzyme activities and re-burrowing capability. Mar. Pollut. Bull., 48: 563–571.

    Article  Google Scholar 

  • Mazorra M T, Rubio J A, Blasco J. 2002. Acid and alkaline phosphatase activities in the clam Scrobicularia plana: kinetic characteristics and effects of heavy metals. Comp. Biochem. Physiol. B, Biochem. Mol. Biol., 131: 241–249.

    Article  Google Scholar 

  • McClellan-Green P, Robbins J. 2000. Effects of TBT and 3-MC co-exposure on cytochrome P450 expression and activity in marine organisms. Mar. Environ. Res., 50: 243.

    Article  Google Scholar 

  • McCord J M, Fridovich J. 1969. Superoxide dismutase: an enzymatic function for erythrocuprein (hemocuprein). J. Biol. Chem., 244: 6 049–6 055.

    Google Scholar 

  • Meng P J, Wang J T, Liu L L, Chen M H, Hung T C. 2005. Toxicity and bioaccumulation of tributyltin and triphenyltin on oysters and rock shells collected from Taiwan mariculture area. Sci. Total Environ., 349: 140–149.

    Article  Google Scholar 

  • Oruç E Ö, Usta D. 2007. Evaluation of oxidative stress responses and neurotoxicity potential of diazinon in different tissues of Cyprinus carpio. Environ. Toxicol. Pharmacol., 23: 48–55.

    Article  Google Scholar 

  • Pampanin D M, Camus L, Gomiero A, Marangon I, Volpato E, Nasci C. 2005. Susceptibility to oxidative stress of mussels (Mytilus galloprovincialis) in the Venice Lagoon (Italy). Mar. Pollut. Bull., 50: 1 548–1 557.

    Google Scholar 

  • Peakall D W. 1994. Biomarkers: the way forward in environmental assessment. Toxicol. Ecotoxicol. News, 1: 55–60.

    Google Scholar 

  • Prieto A I, Jos A, Pichardo S, Moreno I, Camean A M. 2006. Differential oxidative stress responses to microcystins LR and RR in intraperitoneally exposed tilapia fish (Oreochromis sp.). Aquat. Toxicol., 77: 314–321.

    Article  Google Scholar 

  • Rahman M F, Siddiqui M K. 2004. Biochemical effects of vepacide (from Azadirachta indica) on Wistar rats during subchronic exposure. Ecotoxicol. Environ. Saf., 59: 332–339.

    Article  Google Scholar 

  • Rajalakshmi S, Mohandas A. 2005. Copper-induced changes in tissue enzyme activity in a freshwater mussel. Ecotoxicol. Environ. Saf., 62: 140–143.

    Article  Google Scholar 

  • Rao J V. 2006. Toxic effects of novel organophosphorus insecticide (RPR-V) on certain biochemical parameters of euryhaline fish, Oreochromis mossambicus. Pestic Biochem. Physiol., 86: 78–84.

    Article  Google Scholar 

  • Ron v, Jonny B, Nico P E V. 2003. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ. Toxicol. Pharmacol., 13: 57–149.

    Article  Google Scholar 

  • Rurangwa E, Biegniewska A, Slominska E, Skorkowski E F, Ollevier F. 2002. Effect of tributyltin on adenylate content and enzyme activities of teleost sperm: a biochemical approach to study the mechanisms of toxicant reduced spermatozoa motility. Comp. Biochem. Physiol. C, Comp. Pharmacol. Toxicol., 131: 335–344.

    Article  Google Scholar 

  • Samman S, Soto C, Cooke L, Ahmad Z, Farmakalidis E. 1996. Is erythrocyte alkaline phosphatase activity a marker of zinc status in humans? Biol. Trace Elem. Res., 51: 285–291.

    Article  Google Scholar 

  • Santos M M, Micael J, Carvalho A P, Morabito R, Booy P, Massanisso P, Lamoree M, Reis-Henriques M A. 2006. Estrogens counteract the masculinizing effect of tributyltin in zebrafish. Comp. Biochem. Physiol. C, Comp. Pharmacol. Toxicol., 142: 151–155.

    Article  Google Scholar 

  • Shim W J, Hong S H, Kim N S, Yim U H, Li D, Oh J R. 2005. Assessment of butyl- and phenyltin pollution in the coastal environment of Korea using mussels and oysters. Mar. Pollut. Bull., 4th International Conference on Marine Pollution and Ecotoxicology, 51: 922–931.

    Google Scholar 

  • Shimasaki Y, Oshima Y, Inoue S, Inoue Y, Kang I J, Nakayama K, Imoto H, Honjo T. 2006. Effect of tributyltin on reproduction in Japanese whiting, Sillago japonica. Mar. Environ. Res., Pollutant Responses in Marine Organisms (PRIMO 13). 62: S245–S248.

    Google Scholar 

  • Siah A, Pellerin J, Amiard J C, Pelletier E, Viglino L. 2003. Delayed gametogenesis and progesterone levels in soft-shell clams (Mya arenaria) in relation to in situ contamination to organotins and heavy metals in the St. Lawrence River (Canada). Comp. Biochem. Physiol. C, Comp. Pharmacol. Toxicol., 135: 145–156.

    Article  Google Scholar 

  • Svavarsson J. 2000. Imposex in the Dogwhelk (Nucella lapillus) due to TBT Contamination: Improvement at High Latitudes. Mar. Pollut. Bull., 40: 893–897.

    Article  Google Scholar 

  • Topcu I, Vatansever S, Var A, Cavus Z, Cilaker S, Sakarya M. 2007. The effect of Misoprostol, a prostaglandin E1 analog, on apoptosis in ischemia-reperfusion-induced intestinal injury. Acta Histochem., 109: 322–329.

    Article  Google Scholar 

  • Vega-López A, Galar-Martínez M, Jiménez-Orozco F A, García-Latorre E, Domínguez-López M L. 2007. Gender related differences in the oxidative stress response to PCB exposure in an endangered goodeid fish (Girardinichthys viviparus). Comp. Biochem. Physiol., Part A Mol. Integr. Physiol.; Second Special Issue of CBP dedicated to “The Face of Latin American Comparative Biochemistry and Physiology” organized by Marcelo Hermes-Lima Brazil) and co-edited by Carlos Navas (Brazil), Rene Beleboni (Brazil), Tania Zenteno-Savin (Mexico) and the Editors of CBP — This issue is in honour of Cicero Lima and the late Peter W Hochachka, teacher, friend and devoted supporter of Latin American science. 146: 672–678.

  • Wang C G, Chen Y X, Li Y, Wei W, Yu Q. 2005. Effects of low dose tributyltin on activities of hepatic antioxidant and phase II enzymes in Sebastiscus marmoratus. Bull. Environ. Contam. Toxicol., 74: 114–119.

    Article  Google Scholar 

  • Wang S H, Wang Y L, Zhang Z X. 2004. Different response of innate immune factors in abalone Haliotis diversicolor supertexta to E. coli or Vibrio parahaemolyticus infection. J. Shellfish Res., 23: 1 173–1 177.

    Google Scholar 

  • Wang X H, Hong H S, Zhao D M, Hong L Y. 2008. Environmental behavior of organotin compounds in the coastal environment of Xiamen, China. Mar. Pollut. Bull., 57: 419–424.

    Article  Google Scholar 

  • Yang R Q, Zhou Q F, Liu J Y, Jiang G B. 2006. Butyltins compounds in molluscs from Chinese Bohai coastal waters. Food Chem., 97: 637–643.

    Article  Google Scholar 

  • Zhang M, Wang L, Guo Z Y, Wang B J. 2004. Effect of lipopolysaccharide and Vibrio anguillarum on the activities of phosphatase, superoxide dismutase and the content of hemocyanin in the serum of Fenneropenaeus chinensis. Mar Sci., 28: 22–25. (in Chinese)

    Google Scholar 

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Authors and Affiliations

  1. State Key Laboratory of Marine Environmental Science, Ministry of Education, Environmental Science Research Center, Xiamen University, Xiamen, 361005, China

    Xiwei Jia  (贾锡伟) & Bangqin Huang  (黄邦钦)

  2. The Key Laboratory of Science and Technology for Aquaculture and Food Safety, Fisheries College, Jimei University, Xiamen, 361021, China

    Xiwei Jia  (贾锡伟), Ziping Zhang  (张子平), Shuhong Wang  (王淑红), Peng Lin  (林鹏), Zhihua Zou  (邹志华) & Yilei Wang  (王艺磊)

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  1. Xiwei Jia  (贾锡伟)
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Correspondence to Yilei Wang  (王艺磊).

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Supported by the Committee of Xiamen Science and Technology, Xiamen, China (No. 502Z20055024), the National Natural Science Foundation of China (No. 20877034), and the Innovation Team Foundation of Jimei University (No. 2008A001)

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Jia, X., Zhang, Z., Wang, S. et al. Effects of tributyltin (TBT) on enzyme activity and oxidative stress in hepatopancreas and hemolymph of small abalone, Haliotis diversicolor supertexta . Chin. J. Ocean. Limnol. 27, 816–824 (2009). https://doi.org/10.1007/s00343-009-9222-z

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