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Protective Effect of Selenium on the Oxidative Damage of Kidney Cells Induced by Sodium Nitrite in Grass Carp (Ctenopharyngodon idellus)

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Abstract

The present study was conducted to investigate the protective effects of selenium on the oxidative damage of kidney cells (CIK) caused by nitrite exposure in grass carp (Ctenopharyngodon idella). Cells were pre-incubated by Na2SeO3 (10 μmol/L) for 12 h and then exposed to NaNO2 (25 mg/L) for 24 h, the cell viability, apoptosis, gene expression, and antioxidant enzyme activity were assayed. The results show that nitrite reduced cell viability and induced apoptosis, and the activities of superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx) as well as the sod, cat, and gpx genes reduced (p < 0.05), while the intracellular calcium ion concentration increased (p < 0.05). Interestingly, selenium treatment significantly alleviated the nitrite induced changes in cell growth, apoptosis, and calcium influx. The cell viability after low-concentration selenium treatment is higher than that of normal cells (p < 0.05). CIK cells were pre-incubated with Na2SeO3 and then exposed to NaNO2, the antioxidant indicators could be maintained at normal levels. And compared with nitrite exposure, intracellular calcium ion concentration and apoptotic rate of selenium-incubated still decreased. The expressions of Nrf2 and Keap1 genes increased significantly in CIK cells treated with sodium selenite for 12 h, and the same trend as the enzyme activities of this group. The results show that the supplement of selenium can enhance the cell’s resistance to sodium nitrite exposure to a certain extent, by alleviating the antioxidant imbalance, high apoptosis rate, and intracellular calcium ion disturbance caused by nitrite exposure. And the Nrf2-Keap1 pathway may play an important role in the process.

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Data and material are available from the corresponding author on reasonable request.

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References

  1. Larsen EH, Willumsen NJ, Christoffersen BC (1992) Role of proton pump of mitochondria-rich cells for active transport of chloride ions in toad skin epithelium. J Physiol 450(1):203–216

    Article  CAS  Google Scholar 

  2. Jensen L, Willumsen N, Larsen E (2002) Proton pump activity is required for active uptake of chloride in isolated amphibian skin exposed to freshwater. J Comp Physiol 172(6):503–511

    Article  CAS  Google Scholar 

  3. Lin Y, Miao LH, Pan WJ, Huang X, Deng JM, Zhang WX, Ge XP, Liu B, Ren MC, Zhou QL, Xie J, Pan LK, Xi BW (2018) Effect of nitrite exposure on the antioxidant enzymes and glutathione system in the liver of bighead carp, Aristichthys nobilis. Fish Shellfish Immunol 76:126–132

    Article  CAS  Google Scholar 

  4. Zhang WY, Li JJ, Chen Y, Si Q, Tian J, Jiang Q, Yang J (2019) Exposure time relevance of response to nitrite exposure: Insight from transcriptional responses of immune and antioxidant defense in the crayfish, Procambarus clarkii. Aquat Toxicol 10:52–62

    Google Scholar 

  5. Jia R, Han C, Lei JL, Jia R, Liu BL, Huang B, Huo HH, Yin ST (2015) Effects of nitrite exposure on haematological parameters, oxidative stress and apoptosis in juvenile turbot (Scophthalmus maximus). Aquat Toxicol 169:1–9

    Article  CAS  Google Scholar 

  6. Elsherbiny NM, Maysarah NM, El-Sherbiny M, Al-Gayyar MM (2017) Renal protective effects of thymoquinone against sodium nitrite-induced chronic toxicity in rats: Impact on inflammation and apoptosis. Life Sci 180:1–8

    Article  CAS  Google Scholar 

  7. Zeng H, Cao JJ, Combs GF Jr (2013) Selenium in bone health: roles in antioxidant protection and cell proliferation. Nutrients 5(1):97–110

    Article  CAS  Google Scholar 

  8. Zheng L, Jiang W-D, Feng L, Wu P, Tang L, Kuang S-Y, Zeng YY, Zhou XQ, Liu Y (2018) Selenium deficiency impaired structural integrity of the head kidney, spleen and skin in young grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 82:408–420

    Article  CAS  Google Scholar 

  9. Fontagné-Dicharry S, Godin S, Liu H, Antony Jesu Prabhu P, Bouyssière B, Bueno M, Tacon P, Médale F, Kaushik SJ (2015) Influence of the forms and levels of dietary selenium on antioxidant status and oxidative stress-related parameters in rainbow trout (Oncorhynchus mykiss) fry. Br J Nutr 113(12):1876–1887

    Article  Google Scholar 

  10. Jin X, Xu Z, Zhao X, Chen M, Xu S (2017) The antagonistic effect of selenium on lead-induced apoptosis via mitochondrial dynamics pathway in the chicken kidney. Chemosphere 180:259–266

    Article  CAS  Google Scholar 

  11. Chen M, Li X, Fan R, Cao C, Yao H, Xu S (2017) Selenium antagonizes cadmium-induced apoptosis in chicken spleen but not involving Nrf2-regulated antioxidant response. Ecotoxicol Environ Saf 145:503–510

    Article  CAS  Google Scholar 

  12. Zhao CY, Wang XL, Peng YK (2015) Role of Nrf2 in neurodegenerative diseases and recent progress of its activators. Acta Pharm Sin 50:375–384

    CAS  Google Scholar 

  13. Bell JG, Pirie BJ, Adron JW, Cowey CB (1986) Some effects of selenium deficiency on glutathione peroxidase (EC 1.11. 1.9) activity and tissue pathology in rainbow trout (Salmo gairdneri). Br J Nutr 55:305–311

    Article  CAS  Google Scholar 

  14. Stępkowski TM, Kruszewski MK (2011) Molecular cross-talk between the NRF2/KEAP1 signaling pathway, autophagy, and apoptosis. Free Radical Biol Med 50(9):1186–1195

    Article  Google Scholar 

  15. Kaspar JW, Niture SK, Jaiswal AK (2009) Nrf 2:INrf2 (Keap1) signaling in oxidative stress. Free Radical Biol Med 47:1304–1309

    Article  CAS  Google Scholar 

  16. Xie LX, Chen SQ, Yao CR, Li DP, Li L, Tang R (2019) Nitrite induces endoplasmic reticulum stress and associates apoptosis of liver cells in grass carp (Ctenopharyngodon idella ). Aquaculture 2019:507

    Google Scholar 

  17. Abdallah TM, Ashraf AG, Eglal AO, Hala SK, Maria AE (2017) Dietary supplementation of organic selenium improves growth, survival, antioxidant and immune status of meagre, argyrosomus regius, juveniles. Fish Shellfish Immunol 68:516–524

    Article  Google Scholar 

  18. Seunghan L, Rebecca WN, Seonghun W, Kumar K, Sungchul CB (2016) Dietary selenium requirement and toxicity levels in juvenile Nile tilapia, Oreochromis niloticus. Aquaculture 464:153–158

    Article  Google Scholar 

  19. Liu GX, Jiang GZ, Lu KL, Li XF, Zhou M, Zhang DD, Liu WB (2017) Effects of dietary selenium on the growth, selenium status, antioxidant activities, muscle composition and meat quality of blunt snout bream, Megalobrama amblycephala. Aquac Nutr 23(4):777–787

    Article  CAS  Google Scholar 

  20. Liu WX, Shang SH, Feng X, Zhang GP, Wu FB (2015) Modulation of exogenous selenium in cadmium-induced changes in antioxidative metabolism, cadmium uptake, and photosynthetic performance in the 2 tobacco genotypes differing in cadmium tolerance. Environ Toxicol Chem 34:92–99

    Article  Google Scholar 

  21. Steinbrenner H, Sies H (2009) Protection against reactive oxygen species by selenoproteins. Biochem Biophys Acta 1790(11):1478–1485

    Article  CAS  Google Scholar 

  22. Hatfifield DL, Tsuji PA, Carlson BA, Gladyshev VN (2014) Selenium and selenocysteine: roles in cancer, health, and development. Trends Biochem Sci 39:112–120

    Article  Google Scholar 

  23. Tanekhy M (2015) Lead poisoning in Nile tilapia (Oreochromis niloticus): oxidant and antioxidant relationship. Environ Monit Assess Environ 187(4):154

    Article  Google Scholar 

  24. Su CF, Luo L, Li Q, Wen H, Wang F-B (2008) Effects of dietary selenium on the anti-oxidation capability and histological structure of grass carp, Cenopharyngodon idellus. J Southwest China Normal Univ (Nat Sci Ed) 33(5):69–75

    CAS  Google Scholar 

  25. Saffari S, Keyvanshokooh S, Zakeri M, Johari SA, Pasha-Zanoosi H, Mozanzadeh MT (2018) Effects of dietary organic, inorganic, and nanoparticulate selenium sources on growth, hemato-immunological, and serum biochemical parameters of common carp(Cyprinus carpio). Fish Physiol Biochem 44(4):1087–1097

    Article  CAS  Google Scholar 

  26. Zheng J, Mao Y, Su Y, Wang J (2016) Effects of nitrite stress on mRNA expression of antioxidant enzymes, immune-related genes and apoptosis-related proteins in Marsupenaeus japonicus. Fish Shellfish Immunol 58:239–252

    Article  CAS  Google Scholar 

  27. Gao XQ, Fei F, Huo HH, Huang B, Meng XS, Zhang T, Liu BL (2020) Effect of acute exposure to nitrite on physiological parameters, oxidative stress, and apoptosis in Takifugu rubripes. Ecotoxicol Environ Saf. 188:109878

    Article  CAS  Google Scholar 

  28. Zheng X, Feng L, Jiang WD, Wu P, Liu Y, Jiang J, Kuang SY, Tang L, Tang WN, Zhang YA, Zhou XQ (2017) Dietary pyridoxine deficiency reduced growth performance and impaired intestinal immune function associated with TOR and NF-κB signalling of young grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 70:682–700

    Article  CAS  Google Scholar 

  29. Wu C, Ye J, Gao J, Chen L, Lu Z (2016) The effects of dietary carbohydrate on the growth, antioxidant capacities, innate immune responses and pathogen resistance of juvenile Black carp Mylopharyngodon piceus. Fish Shellfish Immunol 49:132–142

    Article  CAS  Google Scholar 

  30. Song ZX, Jiang WD, Liu Y, Wu P, Jiang J, Zhou XQ, Kuang SY, Tang L, Tang WN, Zhang YA, Feng L (2017) Dietary zinc deficiency reduced growth performance, intestinal immune and physical barrier functions related to NF-κB, TOR, Nrf2, JNK and MLCK signaling pathway of young grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 66:497–523

    Article  CAS  Google Scholar 

  31. Krebs J, Agellon LB, Michalak M (2015) Ca2+ homeostasis and endoplasmic reticulum (ER) stress: an integrated view of calcium signaling. Biochem Biophys Res Commun 460(1):114–121

    Article  CAS  Google Scholar 

  32. Song SL, Tan J, Miao YY, Li MM, Zhang Q (2017) Crosstalk of autophagy and apoptosis: involvement of the dual role of autophagy under ER stress. J Cell Physiol 232(11):2977–2984

    Article  CAS  Google Scholar 

  33. Song YF, Huang C, Shi X, Pan YX, Liu X, Luo Z (2016) Endoplasmic reticulum stress and dysregulation of calcium homeostasis mediate Cu-induced alteration in hepatic lipid metabolism of javelin goby Synechogobius hasta. Aquat Toxicol 175:20–29

    Article  CAS  Google Scholar 

  34. Xu C, Bailly-Maitre B, Reed JC (2005) Endoplasmic reticulum stress: cell life and death decisions. J Clin Investig 115(10):2656–2664

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors extend their sincere thanks to the members of the Fish Environmental Physiology and Freshwater Healthy Aquaculture Laboratory at the College of Fisheries in Huazhong Agricultural University.

Funding

This research was supported by the National Key R&D Program of China (No. 2019YFD0900301), China Agriculture Research System of MOF and MARA (CARS-45–24), and the National Natural Science Foundation (No.31502140).

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Authors and Affiliations

  1. College of Fisheries, Huazhong Agricultural University, Wuhan, 430070, China

    Tingting Zhang, Chaorui Yao, Zhenyi Hu, Dapeng Li & Rong Tang

  2. Engineering Research Center of Green Development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, Wuhan, 430070, China

    Dapeng Li & Rong Tang

  3. Hubei Provincial Engineering Laboratory for Pond Aquaculture, Wuhan, 430070, China

    Dapeng Li & Rong Tang

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  1. Tingting Zhang
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  2. Chaorui Yao
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Contributions

Tingting Zhang: formal analysis, writing (original draft). Chaorui Yao: draft layout, visualization. Zhenyi Hu: investigation. Dapeng Li: resources, supervision. Rong Tang: conceptualization, resources, supervision.

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Correspondence to Rong Tang.

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Zhang, T., Yao, C., Hu, Z. et al. Protective Effect of Selenium on the Oxidative Damage of Kidney Cells Induced by Sodium Nitrite in Grass Carp (Ctenopharyngodon idellus). Biol Trace Elem Res 200, 3876–3884 (2022). https://doi.org/10.1007/s12011-021-02982-x

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