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Toxicity and accumulation of zinc pyrithione in the liver and kidneys of Carassius auratus gibelio: association with P-glycoprotein expression

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Abstract

Zinc pyrithione (ZPT) is a broad-spectrum antibacterial and antifungal agent; therefore, it is widely used in industry and civilian life. It is discharged into the aquatic environment with industrial and civilian waste water. Carassius sp. is one of the most widely distributed and farmed fish in China. The effects of aquatic ZPT on Carassius sp. remain unknown. In this study, we determined the acute toxicity of ZPT on Carassius sp. The results showed that the median lethal concentration (LC50 96 h) of ZPT on Carassius sp. cultivated in freshwater or water with 1.5 or 3 ‰ salinity was 0.163, 0.126, and 0.113 mg/L, respectively. ZPT has a higher affinity to the liver than the kidney, with a prolonged tissue residual time. P-glycoprotein (P-gp), an ATP-binding cassette transporter, was found to be induced in the liver and kidney tissues of these Carassius spp. after ZPT treatment, based on the determination of its mRNA and protein levels by quantitative real-time reverse transcription polymerase chain reaction and immunohistochemistry, respectively. The ZPT accumulation and magnitude of P-gp induction were also affected by the salinity of the cultivation water. These results suggest that aquatic ZPT is potentially toxic to Carassius sp. We speculate that P-gp induction may play a protective role for Carassius sp. Our findings provide a basis for assessing the potential risk of ZPT to aquatic animals including Carassius sp.

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References

  • Agarwal S, Arya V, Zhang L (2013) Review of P-gp inhibition data in recently approved new drug applications: utility of the proposed [I(1)]/IC(50) and [I(2)]/IC(50) criteria in the P-gp decision tree. J Clin Pharmacol 53(2):228–233

    Article  CAS  PubMed  Google Scholar 

  • Bao VW, Lui GC, Leung KM (2014) Acute and chronic toxicities of zinc pyrithione alone and in combination with copper to the marine copepod Tigriopus japonicus. Aquat Toxicol 157:81–93

    Article  CAS  PubMed  Google Scholar 

  • Bard SM (2000) Multixenobiotic resistance as a cellular defense mechanism in aquatic organisms. Aquat Toxicol 48(4):357–389

    Article  CAS  PubMed  Google Scholar 

  • Bard SM, Gadbois S (2007) Assessing neuroprotective P-glycoprotein activity at the blood-brain barrier in killifish (Fundulus heteroclitus) using behavioural profiles. Mar Environ Res 64(5):679–682

    Article  CAS  PubMed  Google Scholar 

  • Bard SM, Woodin BR, Stegeman JJ (2002) Expression of P-glycoprotein and cytochrome p450 1A in intertidal fish (Anoplarchus purpurescens) exposed to environmental contaminants. Aquat Toxicol 60(1–2):17–32

    Article  CAS  PubMed  Google Scholar 

  • Bones J, Thomas KV, Paull B (2006) Improved method for the determination of zinc pyrithione in environmental water samples incorporating on-line extraction and preconcentration coupled with liquid chromatography atmospheric pressure chemical ionisation mass spectrometry. J Chromatogr A 1132(1–2):157–164

    Article  CAS  PubMed  Google Scholar 

  • Brayfield A (2011) Pyrithione zinc. Martindale: the complete drug reference. Pharmaceutical Press, London

    Google Scholar 

  • Caminada D, Zaja R, Smital T, Fent K (2008) Human pharmaceuticals modulate P-gp1 (ABCB1) transport activity in the fish cell line PLHC-1. Aquat Toxicol 90(3):214–222

    Article  CAS  PubMed  Google Scholar 

  • Daborn K, Cozzi RR, Marshall WS (2001) Dynamics of pavement cell-chloride cell interactions during abrupt salinity change in Fundulus heteroclitus. J Exp Biol 204(Pt 11):1889–1899

    CAS  PubMed  Google Scholar 

  • Dawson TL, DeAngelis Y, Kaczsvinsky J, Schwartz J (2004) Broad-spectrum anti-fungal activity of pyrithione zinc and its effect on the causes of dandruff and associated itch. J Am Acad Dermatol 3(50):36

    Article  Google Scholar 

  • Doose CA, Ranke J, Stock F, Bottin-Weber U, Jastorff B (2004) Structure–activity relationships of pyrithiones—IPC-81 toxicity tests with the antifouling biocide zinc pyrithione and structural analogs. Green Chem 6:259–266

    Article  CAS  Google Scholar 

  • Faergemann J (2000) Management of seborrheic dermatitis and pityriasis versicolor. Am J Clin Dermatol 1(2):75–80

    Article  CAS  PubMed  Google Scholar 

  • Gui J, Zhou L (2010) Genetic basis and breeding application of clonal diversity and dual reproduction modes in polyploid Carassius auratus gibelio. Sci China Life Sci 53(4):409–415

    Article  PubMed  Google Scholar 

  • Guthery E, Seal LA, Anderson EL (2005) Zinc pyrithione in alcohol-based products for skin antisepsis: persistence of antimicrobial effects. Am J Infect Control 33(1):15–22

    Article  PubMed  Google Scholar 

  • He Q, Liu K, Wang S, Hou H, Yuan Y, Wang X (2012) Toxicity induced by emodin on zebrafish embryos. Drug Chem Toxicol 35(2):149–154

    Article  CAS  PubMed  Google Scholar 

  • Hu Q, Zhong JQ, Zheng R, Ji MS, Wang K (2012) Determination of zinc pyrithione and impurities test in cosmetic material by HPLC. Chin J Health Lab Technol 22(9):2037–2040

    CAS  Google Scholar 

  • Hu K, Li HR, Ou RJ, Li CZ, Yang XL (2014) Tissue accumulation and toxicity of isothiazolinone in Ctenopharyngodon idellus (grass carp): association with P-glycoprotein expression and location within tissues. Environ Toxicol Pharmacol 37(2):529–535

    Article  CAS  PubMed  Google Scholar 

  • Kalous L, Memis D, Bohlen J (2004) Finding of triploid Carassius gibelio (Bloch, 1780) (Cypriniformes, Cyprinidae) in Turkey. Cybium 28(1):77–79

    Google Scholar 

  • Kleinow KM, Doi AM, Smith AA (2000) Distribution and inducibility of P-glycoprotein in the catfish: immunohistochemical detection using the mammalian C-219 monoclonal. Mar Environ Res 50(1–5):313–317

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi N, Okamura H (2002) Effects of new antifouling compounds on the development of sea urchin. Mar Pollut Bull 44(8):748–751

    Article  CAS  PubMed  Google Scholar 

  • Konstantinou IK, Albanis TA (2004) Worldwide occurrence and effects of antifouling paint booster biocides in the aquatic environment: a review. Environ Int 30(2):235–248

    Article  CAS  PubMed  Google Scholar 

  • Lu L, Song F (2002) Fish acute toxicity experiment. Bull Biol 37(7):50–52

    Google Scholar 

  • Lv F, Hu Y, Huang JT, Wang AM (2007) Effects of salinity on hemoglobin and protein of muscle of allogynogemetic Crucian carp. Freshw Fish 37(5):56–59

    Google Scholar 

  • Madsen T, Samsøe-Petersen L, Gustavson K, Rasmussen D (2000) Ecotoxicological assessment of antifouling biocides and nonbiocidal antifouling paints. Environmental Project Report 531. Danish Environmental Protection Agency, Copenhagen, Denmark

  • Martinez-Alvarez RM, Sanz A, Garcia-Gallego M, Domezain A, Domezain J, Carmona R, del Valle Ostos-Garrido M, Morales AE (2005) Adaptive branchial mechanisms in the sturgeon Acipenser naccarii during acclimation to saltwater. Comp Biochem Physiol A Mol Integr Physiol 141(2):183–190

    Article  PubMed  Google Scholar 

  • Nolen GA, Dierckman TA (1979) Reproduction and teratology studies of zinc pyrithione administered orally or topically to rats and rabbits. Food Cosmet Toxicol 17(6):639–649

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanchez-Bayo F, Goka K (2006) Influence of light in acute toxicity bioassays of imidacloprid and zinc pyrithione to zooplankton crustaceans. Aquat Toxicol 78(3):262–271

    Article  CAS  PubMed  Google Scholar 

  • Tan X, Yim SY, Uppu P, Kleinow KM (2010) Enhanced bioaccumulation of dietary contaminants in catfish with exposure to the waterborne surfactant linear alkylbenzene sulfonate. Aquat Toxicol 99(2):300–308

    Article  CAS  PubMed  Google Scholar 

  • Thomas KV (1999) Determination of the antifouling agent zinc pyrithione in water samples by copper chelate formation and high-performance liquid chromatography-atmospheric pressure chemical ionisation mass spectrometry. J Chromatogr A 833(1):105–109

    Article  CAS  PubMed  Google Scholar 

  • Voulvoulis N, Scrimshaw MD, Lester JN (2002) Comparative environmental assessment of biocides used in antifouling paints. Chemosphere 47(7):789–795

    Article  CAS  PubMed  Google Scholar 

  • Wallströma E, Jespersenb HT, Schaumburg K (2011) A new concept for anti-fouling paint for Yachts. Prog Org Coat 72:109–114

    Article  Google Scholar 

  • Wang LH (2000) Determination of zinc pyrithione in hair care products on metal oxides modified carbon electrodes. Electroanalysis 12(3):227–232

    Article  CAS  Google Scholar 

  • Wu T, Ding Z, Ren M, An L, Xiao Z, Liu P, Gu W, Meng Q, Wang W (2013) The histo- and ultra-pathological studies on a fatal disease of Prussian carp (Carassius gibelio) in mainland China associated with cyprinid herpesvirus 2 (CyHV-2). Aquaculture 412–413:8–13

    Article  Google Scholar 

  • Xu X, Fu J, Wang H, Zhang B, Wang X, Wang Y (2011) Influence of P-glycoprotein on embryotoxicity of the antifouling biocides to sea urchin (Strongylocentrotus intermedius). Ecotoxicology 20(2):419–428

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by the Special Fund for Agro-scientific Research in the Public Interest (Grant 201203085), the 863 Program (Grant 2011AA10A216), the National Science and Technology Resources Platform, Key Laboratory of Genetic Resources for Freshwater Aquaculture and Fisheries and the Shanghai University Knowledge Service Platform.

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    Authors and Affiliations

    1. National Pathogen Collection Center for Aquatic Animals, Shanghai Ocean University, 999 Hucheng Huan Road, Lingang New City, Shanghai, 201306, People’s Republic of China

      Tao Ren, Teng-Fei Liu, Kun Hu, Hao-Ran Li & Xian-Le Yang

    2. East China Sea Fisheries Research Institute Chinese Academy of Fishery Sciences, Shanghai, 201306, People’s Republic of China

      Gui-Hong Fu & Wen-Hong Fang

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    1. Tao Ren
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    2. Gui-Hong Fu
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    3. Teng-Fei Liu
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    4. Kun Hu
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    Correspondence to Kun Hu.

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    Tao Ren and Gui-Hong Fu have contributed equally to this study.

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    Ren, T., Fu, GH., Liu, TF. et al. Toxicity and accumulation of zinc pyrithione in the liver and kidneys of Carassius auratus gibelio: association with P-glycoprotein expression. Fish Physiol Biochem 43, 1–9 (2017). https://doi.org/10.1007/s10695-016-0262-y

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