Abstract
The study was conducted to evaluate the effect of zinc adaptation on histological morphology and antioxidant and immune responses of grass carp(Ctenopharyngodon idella). A total of 180 young grass carp (20.0 ± 2.0 g) was equally distributed into 9 groups, and triplicate groups were subjected to 0 μg/L Zn2+ (control group), 200 μg/L Zn2+, and 300 μg/L Zn2+ solution for 42 days, respectively. The results indicated that the liver and gill have obvious pathological changes after long-term adaptation to zinc except the intestine; the zinc adaptation can positively influence intestinal morphology. The activities of GPX (glutathione peroxidase activity), SOD (superoxide dismutase), and CAT (Catalase) were significantly increased in zinc treatment groups (P < 0.05). The genes expression levels of CuZnSOD (copper zinc superoxide dismutase), CAT, Hsp70 (heat shock protein-70), IL-1b (interleukin-1-b), and TGF-β1 (transforming growth factor-β1) were upregulated in the gill and intestine of grass carp following waterborne adaptation to zinc solution for 42 days (P < 0.05). In conclusion, zinc adaptation has different effects on organs of grass carp and may reduce the inflammatory response of the body’s gills and intestines by improving the body’s antioxidant and anti-stress defense capabilities.
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The data that support the findings of this study are available from the corresponding author Hongtao Ren upon reasonable request at Animal Science and Technology College, Henan University of Science and Technology, People’s Republic of China.
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References
Pei C, Gao Y, Sun X, Li L, Kong X (2019) A developed subunit vaccine based on fiber protein VP56 of grass carp reovirus providing immune protection against grass carp hemorrhagic disease. Fish Shellfish Immunol 90:12–19
Wang Y, Zhao H, Liu Y, Nie X, Xing M (2020) Zinc exerts its renal protection effect on arsenic-exposed common carp: a signaling network comprising Nrf2, NF-kappaB and MAPK pathways. Fish Shellfish Immunol 104:383–390
Vallee BL, Auld DS (1990). Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry 29 (24):5647e59.
Zhao H, Wang Y, Liu J, Guo M, Fei D, Yu H, Xing M (2019) The cardiotoxicity of the common carp (Cyprinus carpio) exposed to environmentally relevant concentrations of arsenic and subsequently relieved by zinc supplementation. Environ Pollut 253:741–748
Sahin N, Tuzcu M, Ozercan I, Sahin K, Prasad AS, Kucuk O (2009). Zinc picolinate in the prevention of leiomyoma in Japanese quail. J Med Food 12(6):1368e74.
Li TT, He E, Liao X, Lin X, Zhang L, Lu L, Guo Y, Liu Z, Luo X (2021) Zinc alleviates the heat stress of primary cultured hepatocytes of broiler embryos via enhancing the antioxidant ability and attenuating the heat shock responses. Animal Nutrition 7:621–630
Marreiro DDN, Cruz KJC, Morais JBS, Beserra JB, Severo JS, De Oliveira ARS (2017) Zinc and oxidative stress: current mechanisms. Antioxidants 6:24
Beloucif A, Kechrid Z, and Bekada AMA (2021). Effect of zinc deficiency on blood glucose, lipid profile, and antioxidant status in streptozotocin diabetic rats and the potential role of sesame oil. Biological Trace Element Research. https://doi.org/10.1007/s12011-021-02934-5.
Guo M, Wang Y, Zhao H, Wang D, Yin K, Liu Y, Li B, Xing M (2021) Zinc antagonizes common carp (Cyprinus carpio) intestinal arsenic poisoning through PI3K/AKT/mTOR signaling cascade and MAPK pathway. Aquatic Toxicology 240:105986
Ogino C, Yang GY (1978) Requirement of rainbow trout for dietary zinc. Nippon Suisan Gakkaishi 44(9):1015–1018
Huang F, Jiang M, Wen H, Wu F, Liu W, Tian J, Yang CH (2015) Dietary zinc requirement of adult Nile tilapia (Oreochromis niloticus) fed semi-purified diets, and effects on tissue mineral composition and antioxidant responses. Aquaculture 439:53–59
Powell SR (2000) The Antioxidant Properties of Zinc. J Nutr 130:1447–1454
Senger MR, Rosemberg DB, Rico EP, de Bem AM, Dias RD, Bogo MR, Bonan CD (2006) In vitro effect of zinc and cadmium on acetylcholinesterase and ectonucleotidase activities in zebrafish (Danio rerio) brain. Toxicol In Vitro 20(6):954–958
Shang X, Pe Yu, Yin YW, Zhang Y, Lua YT, Mao QH, Li YH (2021) Effect of selenium-rich Bacillus subtilis against mercury-induced intestinal damage repair and oxidative stress in common carp, Comparative Biochemistry and Physiology. Part C 239:108851
Li Z, Liu X, Cheng J, He Y, Wang X, Wang Z et al (2018) Transcriptome profiling provides gene resources for understanding gill immune responses in Japanese flounder (Paralichthys olivaceus) challenged with Edwardsiella tarda. Fish Shellfish Immunol 72:593–603
Jiao W, Han Q, Xu Y, Jiang H, Xing H, Teng X (2019) Impaired immune function and structural integrity in the gills of common carp (Cyprinus carpio L.) caused by chlorpyrifos exposure: Through oxidative stress and apoptosis. Fish Shellfish Immunol 86:239–245
Braz-Mota S, Campos DF, MacCormack TJ, Duarte RM, Val AL, Almeida-Val VMF (2018) Mechanisms of toxic action of copper and copper nanoparticles in two Amazon fish species: dwarf cichlid (Apistogramma agassizii) and cardinal tetra (Paracheirodon axelrodi). Sci Total Environ 630:1168–1180
Fonseca AR, Sanches Fernandes LF, Fontainhas-Fernandes A, Monteiro SM, Pacheco FAL (2017) The impact of freshwater metal concentrations on the severity of histopathological changes in fish gills: a statistical perspective. Sci Total Environ 599–600:217–226
Wong CKC, Wong MH (2000) Morphological and biochemical changes in the gills of Tilapia (Oreochromis mossambicus) toambient cadmium exposure. Aquat Toxicol 48(4):517–527
Cengiz EI, Unlu E (2006) Sublethal effects of commercial deltamethrin on the structure of the gill, liver and gut tissues of mosquitofish, Gambusia affinis: A microscopic study. Environ Toxicol Pharmacol 21(3):246–253
Lee S, Katya K, Park Y, Won S, Seong M, hamidoghli A, Bai SC (2017). Comparative evaluation of dietary probiotics Bacillus subtilis WB60 and Lactobacillus plantarum KCTC3928 on the growth performance, immunological parameters, gut morphology and disease resistance in Japanese eel, Anguilla japonica. Fish Shellfish Immunology 61, 201-210.
Pirarat N, Pinpimai K, Endo M, Katagiri T, Ponpornpisit A, Chansue N, Maita M (2011) Modulation of intestinal morphology and immunity in nile tilapia (Oreochromis niloticus) by Lactobacillus rhamnosus GG. Res Vet Sci 91:92–97
Ramos MA, Goncalves JFM, Costas B, Batista S, Lochmann R, Pires MA, Rema P, Ozorio ROA (2017) Commercial Bacillus probiotic supplementation of rainbow trout (Oncorhynchys mykiss) and brown trout (Salmo trutta): growth, immune responses and intestinal morphology. Aquac Res 48:2538–2549
Begam M, Sengupta M (2015) Immunomodulation of intestinal macrophages by mercury involves oxidative damage and rise of pro-inflammatory cytokine release in the fresh water fish Channa punctatus Bloch. Fish Shellfish Immunology 45(2):378–385
Adil AD, Kandhare AD, Ghosh SL, Bodhankar, (2016) Sodium arsenite-induced myocardial bruise in rats: Ameliorative effect of naringin via TGF-beta/Smad and Nrf/HO pathways. Chem Biol Interact 253:66–77
Saha S, Sadhukhan P, Mahalanobish S (2018) Ameliorative role of genistein against age-dependent chronic arsenic toxicity in murine brains via the regulation of oxidative stress and inflammatory signaling cascades. J Nutr Biochem 55:26–40
Tako E, Ferket PR, Uni Z (2004) Zinc-methionine enhances the intestine development and functionality in the late term embryos and broiler chickens. Poult Sci 83(Suppl):267
Ling SC, Luo Z, Chen GH, Zhang DG, Liu X (2017) Waterborne Zn influenced Zn uptake and lipid metabolism in two intestinal regions of juvenile goby Synechogobius hasta. Ecotoxicol Environ Saf 148:578–584
Altoé LS, Reis IB, Gomes M, Dolder H, Pirovani JM (2016) Could vitamin C and zinc chloride protect the germ cells against sodium arsenite? Hum Exp Toxicol 36:1800902110
Roy S, Bhattacharya S (2006) Arsenic-induced histopathology and synthesis of stress proteins in liver and kidney of Channa punctatus. Ecotoxicol Environ Saf 65(2):218–229
Zahedi S, Mirvaghefi A, Rafiee G, Mojazi Amiri B, Hedayati M, Makhdoomi C, Zarei Dagesaraki M (2014) The effect of a sub-lethal exposure to copper and the time course of recovery in clean water on biochemical changes in juvenile fish (Acipenser persicus). Mar Freshwat Physiol Behav 47:253–264
Zhang W, Xia S, Zhu J, Miao L, Ren M, Lin Y, Ge X, Sun S (2019) Growth performance, physiological response and histology changes of juvenile blunt snout bream, Megalobrama amblycephala exposed to chronic ammonia. Aquaculture 506:424–436
Salgueiro MJ, Zubillaga M, Lysionek A, Sarabia MI, Caro R, Paoli TD et al (2000) Zinc as an essential micronutrient: a review. Nutr Res 20:737–755
Dani V, Malhotra A, Dhawan D (2007) 131I induced hematological alterations in rat blood: protection by zinc. Biol Trace Elem Res 120:219–226
Banni M, Chouchene L, Said K, Kerkeni A, Messaoudi I (2011) Mechanisms underlying the protective effect of zinc and selenium against cadmium-induced oxidative stress in zebrafish Danio rerio. Biometals 24:981–992
Sevcikova M, Modra H, Slaninova A, Svobodova Z (2010) Metals as a cause of oxidative stress in fish: a review. Vet. Med. (Praha) 56:537–546
Daugaard M, Rohde M, Jäättelä M (2007) The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Lett 581:3702–3710
Feder M, Hofmann G (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282
Liu X, Ying X, Li Y, Yang H, Hao W, Yu M (2018) Identification differential behavior of. Spectrochim Acta 203:383–396
Wu T, Ge Y, Li Y, Xiang Y, Jiang Y, Hu Y (2018) Quality enhancement of large yellow croaker treated with edible coatings based on chitosan and lysozyme. Int J Biol Macromol 120:1072–1079
Acknowledgements
We would like to thank the postgraduate students of Animal Science and Technology College, Henan University of Science and Technology, People’s Republic of China, for their help throughout the research period.
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This work was supported by the Henan Natural Science Foundation (182300410032).
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Hongtao Ren designed the project, analyzed the data, and wrote the manuscript. Hui ying An, Ming xing Du, and Jian Zhou performed the experiments and collected the data.
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All experimental protocols were approved by the Bioethical Committee of Henan University of Science and Technology.
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Ren, H.t., An, H.y., Du, M.x. et al. Effects of Zinc Adaptation on Histological Morphology, Antioxidant Responses, and Expression of Immune-Related Genes of Grass Carp (Ctenopharyngodon idella). Biol Trace Elem Res 200, 5251–5259 (2022). https://doi.org/10.1007/s12011-022-03112-x
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DOI: https://doi.org/10.1007/s12011-022-03112-x