Abstract
Juvenile common carp were treated with Cd2+ at a sublethal concentration for Cyprinidae (6.4 mg/L). The expression of N-methyl-D-aspartate receptor subunit genes (NR2A, NR2B) and ATP-binding cassette subfamily C member 1 gene (ABCC1) was compared between treated and untreated fish. In addition, cadmium accumulation in the fish tissues was assessed. NR2A was 18.9-fold upregulated by Cd2+ in the eyes (choroid + retina), which accumulated Cd, and was not upregulated in brain, which didn’t accumulate Cd. This may have been caused by the blocking of calcium channels by Cd2+, which has a very similar ionic radius to that of Ca2+. ABCC1 was 2.6-fold upregulated in gills and was not upregulated in liver; both tissues accumulated high levels of Cd. This difference may have been caused by the accumulation of predominantly previously inactivated Cd in liver or by some difference in the mechanisms of self-detoxification from Cd2+ in fish gills and liver.
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References
An YJ, Kampbell DH (2003) Total, dissolved, and bioavailable metals at Lake Texoma marinas. Environ Pollut 122:253–259. https://doi.org/10.1016/s0269-7491(02)00291-9
Choong G, Liu Y, Templeton DM (2014) Interplay of calcium and cadmium in mediating cadmium toxicity. Chem Biol Interact 211:54–65. https://doi.org/10.1016/j.cbi.2014.01.007
Cobbina SJ, Mao G, Zhao T, Xu H, Zhang Z, Liu H, Zou Y, Wu X, Yang L (2017) Modulation of N-methyl-D-aspartate receptors (NMDAR), Bcl-2 and C-Fos gene expressions on exposure to individual and mixtures of low concentration metals in zebrafish (Danio rerio). Arch Environ Contam Toxicol 72:418–427. https://doi.org/10.1007/s00244-016-0352-y
Cull-Candy S, Brickley S, Farrant M (2001) NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 11:327–335. https://doi.org/10.1016/s0959-4388(00)00215-4
Eftekhari A, Dizaj SM, Chodari L, Sunar S, Hasanzadeh A, Ahmadian E, Hasanzadeh M (2018) The promising future of nano-antioxidant therapy against environmental pollutants induced-toxicities. Biomed Pharmacother 103:1018–1027. https://doi.org/10.1016/j.biopha.2018.04.126
Erickson RJ, Nichols JW, Cook PM, Ankley GT (2008) Bioavailability of chemical contaminants in aquatic systems. In: Di Giulio RT, Hinton DE (eds) The toxicology of fishes. CRC Press, Boca Raton, pp 9–54
Fard JK, Hamzeiy H, Sattari M, Eftekhari A, Ahmadian E, Eghbal MA (2016) Triazole rizatriptan Induces liver toxicity through lysosomal/mitochondrial dysfunction. Drug Res (Stuttg) 66:470–478. https://doi.org/10.1055/s-0042-110178
Hinkle PM, Kinsella PA, Osterhoudt KC (1987) Cadmium uptake and toxicity via voltage-sensitive calcium channels. J Biol Chem 262:16333–16337
Javed M, Usmani N (2019) An overview of the adverse effects of heavy metal contamination on fish health. Proc Natl Acad Sci India B 89:389–403. https://doi.org/10.1007/s40011-017-0875-7
Keppler D, Cui Y, König J, Leier I, Nies A (1999) Export pumps for anionic conjugates encoded by MRP genes. Adv Enzyme Regul 39:237–246. https://doi.org/10.1016/s0065-2571(98)00015-6
Li F, Tsien JZ (2009) Memory and the NMDA receptors. N Engl J Med 361:302–303. https://doi.org/10.1056/NEJMcibr0902052
Long Y, Li Q, Cui Z (2011) Molecular analysis and heavy metal detoxification of ABCC1/MRP1 in zebrafish. Mol Biol Rep 38:1703–1711. https://doi.org/10.1007/s11033-010-0283-z
Mandegary A, Saeedi A, Eftekhari A, Montazeri V, Sharif E (2013) Hepatoprotective effect of silyamarin in individuals chronically exposed to hydrogen sulfide; modulating influence of TNF-α cytokine genetic polymorphism. Daru 21:28. https://doi.org/10.1186/2008-2231-21-28
Mohammadi S, Gholamin M, Mohammadi M, Mansouri A, Mahmoodian R, Attari S, Kebriaei SM, Zibaei B, Roshanaei M, Daneshvar F, Khandehro M, Khodadadegan MA, Delshad A, Mohammadzadeh F, Peyvandi M, Ghayour-Mobarhan M, Tavallaie S, Boroumand-Noughabi S, Ferns G (2018) Down-regulation of CatSper 1 and CatSper 2 genes by lead and mercury. Environ Toxicol Pharmacol 59:82–86. https://doi.org/10.1016/j.etap.2018.03.007
OECD (2019) Test No. 203: fish, acute toxicity test, OECD guidelines for the testing of chemicals. OECD, Paris
Pekel M, Platt B, Büsselberg D (1993) Mercury (Hg2+) decreases voltage-gated calcium channel currents in rat DRG and Aplysia neurons. Brain Res 632:121–126. https://doi.org/10.1016/0006-8993(93)91146-j
Rios C, Méndez-Armenta M (2019) Cadmium neurotoxicity. In: Nriagu J (ed) Encyclopedia of environmental health. University of Michigan, School of Public Health, Ann Arbor, pp 485–491
Roesijadi G, Unger ME (1993) Cadmium uptake in gills of the mollusc Crassostrea virginica and inhibition by calcium channel blockers. Aquat Toxicol 24:195–206. https://doi.org/10.1016/0166-445X(93)90071-8
Sandbichler AM, Höckner M (2016) Cadmium protection strategies—a hidden trade-off? Int J Mol Sci 17:139. https://doi.org/10.3390/ijms17010139
Shannon RD (1976) Revised effective ionic radii and systematic studies of interatomic distances in halides and chalcogenides. Acta Crystallogr 32:751–767. https://doi.org/10.1107/S0567739476001551
Stohs SJ, Bagchi D, Hassoun E, Bagchi M (2000) Oxidative mechanisms in the toxicity of chromium and cadmium ions. J Environ Pathol Toxicol Oncol 19:201–213
Swandulla D, Armstrong CM (1989) Calcium channel block by cadmium in chicken sensory neurons. Proc Natl Acad Sci USA 86:1736–1740. https://doi.org/10.1073/pnas.86.5.1736
Taylor WR (1988) Permeation of barium and cadmium through slowly inactivating calcium channels in cat sensory neurones. J Physiol 407:433–452. https://doi.org/10.1113/jphysiol.1988.sp017424
Thomson EA, Luoma SN, Johansson CE, Cain DJ (1984) Comparison of sediments and organisms in identifying sources of biologically available trace metal contamination. Water Res 18:755–765. https://doi.org/10.1016/0043-1354(84)90172-6
Toyoda Y, Hagiya Y, Adachi T, Hoshijima K, Kuo MT, Ishikawa T (2008) MRP class of human ATP binding cassette (ABC) transporters: historical background and new research directions. Xenobiotica 38:833–862. https://doi.org/10.1080/00498250701883514
Traynelis SF, Burgess MF, Zheng F, Lyuboslavsky P, Powers JL (1998) Control of voltage-independent zinc inhibition of NMDA receptors by the NR1 subunit. J Neurosci 18:6163–6175. https://doi.org/10.1523/JNEUROSCI.18-16-06163.1998
Valko M, Morris H, Cronin MT (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208. https://doi.org/10.2174/0929867053764635
Vasina DA, Zhdanov DD, Orlova EV, Orlova VS, Pokrovskaya MV, Aleksandrova SS, Sokolov NN (2017) Apoptotic endonuclease EndoG inhibits telomerase activity and induces malignant transformation of human CD4+ T cells. Biochemistry 82:24–37. https://doi.org/10.1134/S0006297917010035
Yamamoto T, Arai Y, Seki T (2005) Measurement of heavy metals using ICP-MS for the RoHS/ELV Directives. Agilent ICP-MS Journal (23):2
Yin X, Sun JZ, Mei Y, Guo X, Chen SL, Wang ZL, Yang L (2008) Effect of Hg2+ on voltage-dependent calcium channels and intracellular free calcium in trigeminal ganglion neurons of rats. Zhonghua Lao Dong Wei Sheng Zhi Ye Bing Za Zhi 26:542–545
Zolotarev K, Belyaeva N (2010) Zebrafish as a test-system for modeling heavy metals toxic action at freshwaterfish. In: Proceedings of the Moscow international scientific and practical conference “Biotechnology: Ecology of Big Cities”. Expo-Biochem-Technologies, Moscow, pp 417–418
Zolotarev KV, Belyaeva NF, Mikhailova MV, Kashirtseva VN, Nakhod KV, Nakhod VI, Zgoda VG (2015) Searching for markers of Cd2+ and Cu2+ toxic action using proteomic profiling of Danio rerio liver and heart. In: Proceedings of the VIII Moscow international congress “Biotechnology: State of the Art and Prospects of Development”. Expo-Biochem-Technologies, Moscow, pp 57–58
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The work was done in the Framework of the Russian Federation Fundamental Research Program for the long-term period for 2021–2030.
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Zolotarev, K.V., Mikhailov, A.N., Mikhailova, M.V. et al. Tissue-Specific Expression of Genes Involved in Cellular Transportation in Common Carp (Cyprinus carpio) Exposed to Cadmium. Bull Environ Contam Toxicol 106, 978–982 (2021). https://doi.org/10.1007/s00128-021-03270-z
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DOI: https://doi.org/10.1007/s00128-021-03270-z