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Thiabendazole-induced cardiac toxicity in early developmental stages of zebrafish |
GUAN Sheng, HU Bin, ZHU Zhe-ning, WANG Bin-jie, WANG Ji-ye, ZHENG Ruo-nan |
Key Laboratory of Drug Prevention and Control Technology Research in Zhejiang Province, Department of Criminal Science and Technology, Zhejiang Police College, Hangzhou 310053, China |
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Abstract The development of the heart in zebrafish embryos was examined after exposure to different concentrations of thiabendazole (TBZ) solution (0.06, 0.6, and 6mg/L). The levels of catalase (CAT), superoxide dismutase (SOD), reactive oxygen species (ROS), and the expression of genes related to cardiac development were assessed. The results indicated that exposure to the high concentration of TBZ (6mg/L) caused severe cardiotoxicity, including pericardial edema and a reduced heart rate in zebrafish embryos. This concentration also induced significant oxidative stress in the heart, leading to a large number of apoptotic cells and marked changes in the expression of cardiac development-related genes (gate4, nppa, sox9b, vmhc), as well as apoptosis-related genes (bcl2, bax, puma, p53). These findings suggested that TBZ induced cardiotoxicity by disrupting the normal expression of genes involved in cardiac development, generating oxidative stress, and triggering apoptosis.
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Received: 16 July 2024
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[1] Gikas G D, Parlakidis P, Mavropoulos T, et al. Particularities of fungicides and factors affecting their fate and removal efficacy: A Review [J]. Sustainability, 2022,14(7):4056. [2] Choi T Y, Choi T I, Lee Y R, et al. Zebrafish as an animal model for biomedical research [J]. Experimental & Molecular Medicine, 2021,53(3):310-317. [3] Basha N J. Therapeutic efficacy of benzimidazole and its analogs: An update [J]. Polycyclic Aromatic Compounds, 2022,43(7):6549-6569. [4] Shahzad F, Vashisth T, Ritenour M A, et al. Quest for desirable quality of Tango Mandarin in the citrus greening era: The promise of integrated approaches [J]. Food Science and Technology, 2022,161:113321. [5] Li D, Gu Y, Feng Y, et al. Synthesis of silver nanoplates on electrospun fibers via tollens reaction for SERS sensing of pesticide residues [J]. Microchimica Acta, 2020,187(10):560. [6] Valdovinos F C, Alcantar R V, Gaspar R O, et al. Agricultural pesticide residues in honey and wax combs from Southeastern, Central and Northeastern Mexico [J]. Journal of Apicultural Research, 2017,56(5):667-679. [7] Séïde M, Marion M, Mateescu M A, et al. The fungicide thiabendazole causes apoptosis in rat hepatocytes [J]. Toxicology in Vitro, 2016,32: 232-239. [8] Ongono J S, Béranger R, Baghdadli A, et al. Pesticides used in Europe and autism spectrum disorder risk: Can novel exposure hypotheses be formulated beyond organophosphates, organochlorines, pyrethroids and carbamates? -A systematic review [J]. Environmental Research, 2020,187:109646. [9] Islam J Y, Hoppin J, Mora A M, et al. Respiratory and allergic outcomes among 5-year-old children exposed to pesticides [J]. Thorax, 2023,78(1):41-49. [10] Jang Y, Lee A Y, Kim J E, et al. Benomyl-induced effects of ORMDL3 overexpression via oxidative stress in human bronchial epithelial cells [J]. Food and Chemical Toxicology, 2016,98:100-106. [11] Han P, Rios M A, Tang X, et al. Benzimidazole fungicide biotransformation by comammox nitrospira bacteria: Transformation pathways and associated proteomic responses [J]. Journal of Hazardous Materials, 2023,445:130558. [12] Al-Mashaqbeh O, Alsafadi D, Dalahmeh S, et al. Removal of selected pharmaceuticals and personal care products in wastewater treatment plant in Jordan [J]. Water, 2019,11(10):2004. [13] El B K, Mekhzoum M E, Qaiss A E, et al. Recent advances in the synthesis and applications of thiabendazole derivatives: A short review [J]. Current Organic Chemistry, 2020,24(20):2367-2377. [14] Solel Z, Sandler D. Dioor A. Mobility and persistence of carbendazim and thiabendazole applied to soil via drip irrigation [J]. Phytopathology, 1979,69:1273-1277. [15] Bijlsma L, Pitarch E, Hernández F, et al. Ecological risk assessment of pesticides in the Mijares River (eastern Spain) impacted by citrus production using wide-scope screening and target quantitative analysis [J]. Journal of Hazardous Materials, 2021,412:125277. [16] Romero C R, Kassuha D, Peris V J, et al. Analysis of thiabendazole, 4-tert-octylphenol and chlorpyrifos in waste and sewage water by direct injection-micellar liquid chromatography [J]. Analyst, 2015, 140(5):1739-1746. [17] Barnhoorn I, van Dyk C. The first report of selected herbicides and fungicides in water and fish from a highly utilized and polluted freshwater urban impoundment [J]. Environmental Science and Pollution Research, 2020,27(26):33393-33398. [18] Chinescu C L, Nicolau A I. Preliminary survey of pharmaceutical residues in some important Romanian rivers [J]. Toxicological & Environmental Chemistry, 2015,96(9):1333-1345. [19] Tokatlı C, Köse E, Çiçek A, et al. Pesticide accumulation in Turkey’s Meriç River Basinwater and Sediment [J]. Polish Journal of Environmental Studies, 2019,29(1):1003-1008. [20] Sarmah S, Marrs J. Zebrafish as a vertebrate model system to evaluate effects of environmental toxicants on cardiac development and function [J]. International Journal of Molecular Sciences, 2016,17(12):2123. [21] Zhang X, Zhang P, Perez R V, et al. Assessing the toxicity of the benzamide fungicide zoxamide in zebrafish (danio rerio): Towards an adverse outcome pathway for beta-tubulin inhibitors [J]. Environmental Toxicology and Pharmacology, 2020,78:103405. [22] Westhoff J H, Steenbergen P J, Thomas L S V, et al. In vivo high-content screening in zebrafish for developmental nephrotoxicity of approved drugs [J]. Frontiers in Cell and Developmental Biology, 2020,8:583. [23] Sasagawa S, Nishimura Y, Kon T, et al. DNA damage response is involved in the developmental toxicity of mebendazole in zebrafish retina [J]. Frontiers in Pharmacology, 2016,7:57. [24] Andrade T S, Henriques J F, Almeida A R, et al. Carbendazim exposure induces developmental, biochemical and behavioural disturbance in zebrafish embryos [J]. Aquatic Toxicology, 2016,170:390-399. [25] Delescluse C, Ledirac N, Li R, et al. Induction of cytochrome P450 1A1gene expression, oxidative stress, and genotoxicity by carbaryl and thiabendazole in transfected human HepG2 and lymphoblastoid cells [J]. Biochemical Pharmacology, 2001,61(4):399-407. [26] Ogata A, Ando H, Kubo Y, et al. Teratogenicity of thiabendazole in ICR mice [J]. Food and Chemical Toxicology, 1984,22(7):509-520. [27] Tada Y, Yoneyama M, Kabashima J, et al. Effects of thiabendazole on the kidneys of ICR mice [J]. Food and Chemical Toxicology, 1989,27(5):307-315. [28] Park J, An G, Park H, et al. Developmental defects induced by thiabendazole are mediated via apoptosis, oxidative stress and alteration in PI3K/Akt and MAPK pathways in zebrafish [J]. Environment International, 2023,176:107973. [29] Holtzinger A, Evans T. Gata4regulates the formation of multiple organs [J]. Development, 2005,132(17):4005-4014. [30] Zeisberg E M, Ma Q, Juraszek A L, et al. Morphogenesis of the right ventricle requires myocardial expression of Gata4 [J]. Journal of Clinical Investigation, 2005,115(6):1522-1531. [31] England J, Loughna S. Heavy and light roles: Myosin in the morphogenesis of the heart [J]. Cellular and Molecular Life Sciences, 2012,70(7):1221-1239. [32] Jin D, Ni T T, Hou J, et al. Promoter analysis of ventricular myosin heavy chain (vmhc) in zebrafish embryos [J]. Developmental Dynamics, 2009,238(7):1760-1767. [33] Yelon D, Stainier D Y R. Patterning during organogenesis: Genetic analysis of cardiac chamber formation [J]. Seminars in Cell & Developmental Biology, 1999,10(1):93-98. [34] 刘 恋,张冉冉,杨 倩,等.利用CRISPR/Cas9技术构建tnnt2a基因突变斑马鱼及表型分析 [J]. 生理学报, 2017,69(3):267-275.Liu Lian, Zhang R, Yang Q, et al. Generation of tnnt2a knock-out zebrafish via CRISPR/Cas9 and phenotypic analysis. [J]. Acta Physiologica Sinica, 2017,69(3):267-275. [35] Grassini D R, Lagendijk A K, De Angelis J E, et al. Nppa and Nppb act redundantly during zebrafish cardiac development to confine AVC marker expression and reduce cardiac jelly volume [J]. Development, 2018,145(12):160739. [36] Forte M, Marchitti S, Di N F, et al. NPPA/atrial natriuretic peptide is an extracellular modulator of autophagy in the heart [J]. Autophagy, 2022,19(4):1087-1099. [37] Anilkumar U, Prehn J H M. Anti-apoptotic BCL-2family proteins in acute neural injury [J]. Frontiers in Cellular Neuroscience, 2014,8:281. [38] Kang P M, Izumo S. Apoptosis in heart: basic mechanisms and implications in cardiovascular diseases [J]. Trends in Molecular Medicine, 2003,9(4):177-182. [39] Cartron P F, Bellot G, Oliver L, et al. Bax inserts into the mitochondrial outer membrane by different mechanisms [J]. FEBS Letters, 2008,582(20):3045-3051. [40] Shen J, Liu P, Sun Y, et al. Embryonic exposure to prothioconazole induces oxidative stress and apoptosis in zebrafish (Danio rerio) early life stage [J]. Science of the Total Environment, 2021,756:143859. [41] Langheinrich U, Hennen E, Stott G, et al. Zebrafish as a model organism for the identification and characterization of drugs and genes affecting p53signaling [J]. Current Biology, 2002,12(23):2023-2028. [42] Villunger A, Toruno C, Carbonneau S, et al. Interdependence of bad and puma during ionizing-radiation-induced apoptosis [J]. PLOS ONE, 2014,9(2):88151. [43] Asoglu M R, Gabbay B R, Turan O M, et al. Exposure of the developing heart to diabetic environment and early cardiac assessment: A review [J]. Echocardiography, 2018,35(2):244-257. [44] Ren F, Ji C, Huang Y, et al. AHR-mediated ROS production contributes to the cardiac developmental toxicity of PM2.5 in zebrafish embryos [J]. Science of the Total Environment, 2020,719:135097. |
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