Skip to main content

Advertisement

SpringerLink
Log in

Different effects of low- and high-dose waterborne zinc on Zn accumulation, ROS levels, oxidative damage and antioxidant responses in the liver of large yellow croaker Pseudosciaena crocea

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

The aim of the present study was to assess survival rate, Zn accumulation, reactive oxygen species (ROS) levels, oxidative damage and antioxidant responses after Zn exposure (2 and 8 mg L−1 Zn) at different exposure times (6, 12, 24, 48 and 96 h) in the liver of large yellow croaker. Survival rate was reduced at 96 h, and hepatic Zn content increased during 24–96 by 8 mg L−1 Zn. In the 2 mg L−1 Zn group, no fish died and the increase in Zn content merely occurred at 96 h. Exposure to 8 mg L−1 Zn induced accumulation of ROS, lipid peroxidation and protein carbonylation during the late stage of exposure. In contrast, exposure to 2 mg L−1 Zn did not result in oxidative damage, which may result from the up-regulation of antioxidant defenses. Although exposure to 8 mg L−1 Zn increased activities and mRNA levels of antioxidant enzymes during the early stage of exposure, including Cu/Zn–SOD, Mn–SOD, CAT, GPx and GR, the activities of these enzymes except Cu/Zn–SOD were inhibited at 96 h. Furthermore, a sharp increase in Nrf2 expression was observed in fish exposed to 8 mg L−1 at 6 and 12 h, and 2 mg L−1 at 12 h and 24 h, suggesting that Nrf2 was required for the protracted induction of these genes. The late increase in Keap1 expression may support its role in switching off the Nrf2 response. In conclusion, the present study demonstrated different effects of low- and high-dose waterborne Zn on antioxidant responses, which could contribute to the understanding of antioxidant and toxic roles of zinc on a molecular level.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adeyemi JA, Klerks PL (2013) Occurrence of copper acclimation in the least killifish Heterandria formosa, and associated biochemical and physiological mechanisms. Aquat Toxicol 130:51–57

    Article  PubMed  Google Scholar 

  • An KW, Shin HS, Choi CY (2008) Physiological responses and expression of metallothionein (MT) and superoxide dismutase (SOD) mRNAs in olive flounder, Paralichthys olivaceus exposed to benzo[a]pyrene.Comp. Biochem Physiol B Biochem Mol Biol 149:534–539

    Article  Google Scholar 

  • Atli G, Alptekin O, Tukel S, Canli M (2006) Response of catalase activity to Ag+, Cd2+, Cr6+, Cu2+ and Zn2+ in five tissues of freshwater fish Oreochromis niloticus. Comp Biochem Physiol C Pharmacol Toxicol 143:218–224

    Article  Google Scholar 

  • Baird L, Dinkova-Kostova AT (2011) The cytoprotective role of the Keap1–Nrf2 pathway. Arch Toxicol 85:241–272

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  Google Scholar 

  • Beutler E (1982) Catalase. Red cell metabolism, a manual of biochemical methods, pp 105–106

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

    Article  CAS  PubMed  Google Scholar 

  • Cho YS, Choi BN, Kim KH, Kim SK, Kim DS, Bang IC, Nam YK (2006) Differential expression of Cu/Zn superoxide dismutase mRNA during exposures to heavy metals in rockbream (Oplegnathus fasciatus). Aquaculture 253:667–679

    Article  CAS  Google Scholar 

  • Cho YS, Lee SY, Bang IC, Kim DS, Nam YK (2009) Genomic organization and mRNA expression of manganese superoxide dismutase (Mn–SOD) from Hemibarbus mylodon (Teleostei, Cypriniformes). Fish Shellfish Immunol 27:571–576

    Article  CAS  PubMed  Google Scholar 

  • Copple IM, Goldring CE, Kitteringham NR, Park BK (2008) The Nrf2–Keap1 defence pathway: role in protection against drug-induced toxicity. Toxicology 246:24–33

    Article  CAS  PubMed  Google Scholar 

  • Craig PM, Wood CM, McClelland GB (2007) Oxidative stress response and gene expression with acute copper exposure in zebrafish (Danio rerio). Am J Physiol Regul Integr Comp Physiol 293:R1882–R1892

    Article  CAS  PubMed  Google Scholar 

  • Dolci G, Vey L, Schuster A, Roversi K, Roversi K, Dias V, Pase C, Barcelos R, Antoniazzi C, Golombieski J (2014) Hypoxia acclimation protects against oxidative damage and changes in prolactin and somatolactin expression in silver catfish (Rhamdia quelen) exposed to manganese. Aquat Toxicol 157:175–185

    Article  CAS  PubMed  Google Scholar 

  • Drotar A, Phelps P, Fall R (1985) Evidence for glutathione peroxidase activities in cultured plant cells. Plant Sci 42:35–40

    Article  CAS  Google Scholar 

  • Eroglu A, Dogan Z, Kanak E, Atli G, Canli M (2014) Effects of heavy metals (Cd, Cu, Cr, Pb, Zn) on fish glutathione metabolism. Environ Sci Pollut R 22:3229–3237

    Article  Google Scholar 

  • Fu H, Steinebach OM, Van den Hamer CJA, Balm PHM, Lock RAC (1990) Involvement of cortisol and metallothionein-like proteins in the physiological responses of tilapia, Oreochromis mossambicus to sub-lethal cadmium stress. Aquat Toxicol 16:257–270

    Article  CAS  Google Scholar 

  • Gallego A, Martin-González A, Ortega R, Gutierrez JC (2007) Flow cytometry assessment of cytotoxicity and reactive oxygen species generation by single and binary mixtures of cadmium, zinc and copper on populations of the ciliated protozoan Tetrahymena thermophila. Chemosphere 68:647–661

    Article  CAS  PubMed  Google Scholar 

  • Giuliani ME, Regoli F (2014) Identification of the Nrf2–Keap1 pathway in the European eel Anguilla anguilla: role for a transcriptional regulation of antioxidant genes in aquatic organisms. Aquat Toxicol 150:117–123

    Article  CAS  PubMed  Google Scholar 

  • Halliwell B, Gutteridge JM (1999) Free radicals in biology and medicine. Oxford University Press, Oxford

    Google Scholar 

  • Hansen B, Romma S, Garmo Ø, Olsvik P, Andersen R (2006) Antioxidative stress proteins and their gene expression in brown trout (Salmo trutta) from three rivers with different heavy metal levels. Comp Biochem Physiol C Pharmacol Toxicol 143:263–274

    Article  CAS  Google Scholar 

  • Heath AG (1995) Water pollution and fish physiology. CRC Press, Boca Raton

    Google Scholar 

  • Huang C, Chen QL, Luo Z, Shi X, Pan YX, Song YF, Zhuo MQ, Wu K (2014) Time-dependent effects of waterborne copper exposure influencing hepatic lipid deposition and metabolism in javelin goby Synechogobius hasta and their mechanism. Aquat Toxicol 155:291–300

    Article  CAS  PubMed  Google Scholar 

  • Jiang WD, Liu Y, Hu K, Jiang J, Li SH, Feng L, Zhou XQ (2014) Copper exposure induces oxidative injury, disturbs the antioxidant system and changes the Nrf2/ARE (CuZnSOD) signaling in the fish brain: protective effects of myo-inositol. Aquat Toxicol 155:301–313

    Article  CAS  PubMed  Google Scholar 

  • Jiang WD, Liu Y, Jiang J, Wu P, Feng L, Zhou XQ (2015) Copper exposure induces toxicity to the antioxidant system via the destruction of Nrf2/ARE signaling and caspase-3-regulated DNA damage in fish muscle: amelioration by myo-inositol. Aquat Toxicol 159:245–255

    Article  CAS  PubMed  Google Scholar 

  • Kang SW, Rhee SG, Chang TS, Jeong W, Choi MH (2005) 2-Cys peroxiredoxin function in intracellular signal transduction: therapeutic implications. Trends Mol Med 11:571–578

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi M, Itoh K, Suzuki T, Osanai H, Nishikawa K, Katoh Y, Takagi Y, Yamamoto M (2002) Identification of the interactive interface and phylogenic conservation of the Nrf2–Keap1 system. Genes Cells 7:807–820

    Article  CAS  PubMed  Google Scholar 

  • LeBel CP, Ischiropoulos H, Bondy SC (1992) Evaluation of the probe 2′, 7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 5:227–231

    Article  CAS  PubMed  Google Scholar 

  • Lee OH, Jain AK, Papusha V, Jaiswal AK (2007) An auto-regulatory loop between stress sensors INrf2 and Nrf2 controls their cellular abundance. J Biol Chem 282:36412–36420

    Article  CAS  PubMed  Google Scholar 

  • Li J, Stein TD, Johnson JA (2004) Genetic dissection of systemic autoimmune disease in Nrf2-deficient mice. Physiol Genomics 18:261–272

    Article  CAS  PubMed  Google Scholar 

  • Liu P, Yu Y, Liu C (1991) Studies on the situation of pollution and countermeasures of control of the oceanic environment in Zhoushan fishing ground—the largest fishing ground in China. Mar Pollut Bull 23:281–288

    Article  Google Scholar 

  • Livingstone D, Martinez PG, Michel X, Narbonne J, Ohara S, Ribera D, Winston G, (1990) Oxyradical production as a pollution-mediated mechanism of toxicity in the common mussel, Mytilus edulis L., and other molluscs. Funct Ecol 4:415–424

    Article  Google Scholar 

  • Loro VL, Jorge MB, da Silva KR, Wood CM (2012) Oxidative stress parameters and antioxidant response to sublethal waterborne zinc in a euryhaline teleost Fundulus heteroclitus: protective effects of salinity. Aquat Toxicol 110:187–193

    Article  PubMed  Google Scholar 

  • Lushchak VI, Bagnyukova TV, Husak VV, Luzhna LI, Lushchak V, Storey KB (2005) Hyperoxia results in transient oxidative stress and an adaptive response by antioxidant enzymes in goldfish tissues. Int J Biochem Cell B 37:1670–1680

    Article  CAS  Google Scholar 

  • Martínez-Reyes I, Cuezva JM (2014) The H+-ATP synthase: a gate to ROS-mediated cell death or cell survival. BBA-Bioenergetics 1837:1099–1112

    Article  PubMed  Google Scholar 

  • McGeer JC, Nadella S, Alsop DH, Hollis L, Taylor LN, McDonald DG, Wood CM (2007) Influence of acclimation and cross-acclimation of metals on acute Cd toxicity and Cd uptake and distribution in rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 84:190–197

    Article  CAS  PubMed  Google Scholar 

  • Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417:1–13

    Article  CAS  PubMed  Google Scholar 

  • Nam YK, Cho YS, Choi BN, Kim KH, Kim SK, Kim DS (2005) Alteration of antioxidant enzymes at the mRNA level during short-term starvation of rockbream Oplegnathus fasciatus. Fish Sci 71:1385–1387

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pick E, Keisari Y (1981) Superoxide anion and hydrogen peroxide production by chemically elicited peritoneal macrophages—induction by multiple nonphagocytic stimuli. Cell Immunol 59:301–318

    Article  CAS  PubMed  Google Scholar 

  • Prasad AS (2014) Zinc: an antioxidant and anti-inflammatory agent: role of zinc in degenerative disorders of aging. J Trace Elem Med Biol 28:364–371

    Article  CAS  PubMed  Google Scholar 

  • Qu R, Feng M, Wang X, Qin L, Wang C, Wang Z, Wang L (2014) Metal accumulation and oxidative stress biomarkers in liver of freshwater fish Carassius auratus following in vivo exposure to waterborne zinc under different pH values. Aquat Toxicol 150:9–16

    Article  CAS  PubMed  Google Scholar 

  • Regoli F, Giuliani ME (2014) Oxidative pathways of chemical toxicity and oxidative stress biomarkers in marine organisms. Mar Environ Res 93:106–117

    Article  CAS  PubMed  Google Scholar 

  • Sampaio FG, de Lima Boijink C, Oba ET, dos Santos LRB, Kalinin AL, Rantin FT (2008) Antioxidant defenses and biochemical changes in pacu (Piaractus mesopotamicus) in response to single and combined copper and hypoxia exposure. Comp Biochem Physiol C Pharmacol Toxicol 147:43–51

    Article  Google Scholar 

  • Sarkar S, Mukherjee S, Chattopadhyay A, Bhattacharya S (2014) Low dose of arsenic trioxide triggers oxidative stress in zebrafish brain: expression of antioxidant genes. Ecotox Environ Safe 107:1–8

    Article  CAS  Google Scholar 

  • Shi X, Zhou B (2010) The role of Nrf2 and MAPK pathways in PFOS-induced oxidative stress in zebrafish embryos. Toxicol Sci 115:391–400

    Article  CAS  PubMed  Google Scholar 

  • Sun S, Ge X, Zhu J, Xuan F, Jiang X (2014) Identification and mRNA expression of antioxidant enzyme genes associated with the oxidative stress response in the Wuchang bream (Megalobrama amblycephala Yih) in response to acute nitrite exposure. Comp Biochem Physiol C Pharmacol Toxicol 159:69–77

    Article  CAS  Google Scholar 

  • Sun Z, Zhang S, Chan JY, Zhang DD (2007) Keap1 controls postinduction repression of the Nrf2-mediated antioxidant response by escorting nuclear export of Nrf2. Mol Cell Biol 27:6334–6349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka K, Sano T, Ishizuka K, Kitta K, Kawamura Y (1994) Comparison of properties of leaf and root glutathione reductases from spinach. Physiol Plant 91:353–358

    Article  CAS  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F, (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:research0034

  • Vieira MC, Torronteras R, Córdoba F, Canalejo A (2012) Acute toxicity of manganese in goldfish Carassius auratus is associated with oxidative stress and organ specific antioxidant responses. Ecotox Environ Safe 78:212–217

    Article  CAS  Google Scholar 

  • Wang L, Gallagher EP (2013) Role of Nrf2 antioxidant defense in mitigating cadmium-induced oxidative stress in the olfactory system of zebrafish. Toxicol Appl Pharm 266:177–186

    Article  CAS  Google Scholar 

  • Watanabe T, Kiron V (1994) Prospects in larval fish dietetics. Aquaculture 124:223–251

    Article  Google Scholar 

  • Wu C, Zhang D, Kan M, Lv Z, Zhu A, Su Y, Zhou D, Zhang J, Zhang Z, Xu M (2014a) The draft genome of the large yellow croaker reveals well-developed innate immunity. Nat Commun 5:5227

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu P, Jiang WD, Liu Y, Chen GF, Jiang J, Li SH, Feng L, Zhou XQ (2014b) Effect of choline on antioxidant defenses and gene expressions of Nrf2 signaling molecule in the spleen and head kidney of juvenile Jian carp (Cyprinus carpio var. Jian). Fish Shellfish Immunol 38:374–382

    Article  CAS  PubMed  Google Scholar 

  • Zhang XD, Zhu YF, Cai LS, Wu TX (2008) Effects of fasting on the meat quality and antioxidant defenses of market-size farmed large yellow croaker (Pseudosciaena crocea). Aquaculture 280:136–139

    Article  CAS  Google Scholar 

  • Zheng JL, Luo Z, Chen QL, Liu X, Liu CX, Zhao YH, Gong Y (2011) Effect of waterborne zinc exposure on metal accumulation, enzymatic activities and histology of Synechogobius hasta. Ecotox Environ Safe 74:1864–1873

    Article  CAS  Google Scholar 

  • Zheng JL, Zhu QL, Wu CW, Zhu AY, Shen B, Zeng L (2016) Zinc acclimation mitigated high zinc induced oxidative stress by enhancing antioxidant defenses in large yellow croaker Pseudosciaena crocea. Aquat Toxicol 172:21–29

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Public Science and Technology Research Funds Projects of Ocean (201505025), Natural Science Foundation of Zhejiang Province (LY15C190009) and Scientific Research Foundation of Zhejiang Ocean University (22115010215). The authors thank the Dahaiyang Fisheries Co. Ltd. for supporting large yellow croaker.

Author information

Author notes

    Authors and Affiliations

    1. National Engineering Research Center of Marine Facilities Aquaculture, Zhejiang Ocean University, Zhoushan, 316022, People’s Republic of China

      Jia-Lang Zheng, Lin Zeng, Mei-Ying Xu, Bin Shen & Chang-Wen Wu

    Authors
    1. Jia-Lang Zheng
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Lin Zeng
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Mei-Ying Xu
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Bin Shen
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Chang-Wen Wu
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Chang-Wen Wu.

    Additional information

    Jia-Lang Zheng and Lin Zeng have contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Zheng, JL., Zeng, L., Xu, MY. et al. Different effects of low- and high-dose waterborne zinc on Zn accumulation, ROS levels, oxidative damage and antioxidant responses in the liver of large yellow croaker Pseudosciaena crocea . Fish Physiol Biochem 43, 153–163 (2017). https://doi.org/10.1007/s10695-016-0275-6

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s10695-016-0275-6

    Keywords

    Search

    Navigation