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Zebrafish (Danio rerio) as an excellent vertebrate model for the development, reproductive, cardiovascular, and neural and ocular development toxicity study of hazardous chemicals

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Abstract

In the past decades, the type of chemicals has gradually increased all over the world, and many of these chemicals may have a potentially toxic effect on human health. The zebrafish, as an excellent vertebrate model, is increasingly used for assessing chemical toxicity and safety. This review summarizes the efficacy of zebrafish as a model for the study of developmental toxicity, reproductive toxicity, cardiovascular toxicity, neurodevelopmental toxicity, and ocular developmental toxicity of hazardous chemicals, and the transgenic zebrafish as biosensors are used to detect the environmental pollutants.

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References

  • Ali HFH, El-Sayed NM, Khodeer DM, Ahmed AAM, Hanna PA, Moustafa YMA (2020) Nano selenium ameliorates oxidative stress and inflammatory response associated with cypermethrin-induced neurotoxicity in rats. Ecotox Environ Safe 195:110479

    CAS  Google Scholar 

  • Ali S, Champagne DL, Spaink HP, Richardson MK (2011) Zebrafish embryos and larvae: a new generation of disease models and drug screens. Birth Defects Res 93:115–133

    CAS  Google Scholar 

  • Amsterdam A, Burgess S, Golling G, Chen WB, Sun ZX, Townsend K, Farrington S, Haldi M, Hopkins N (1999) A large-scale insertional mutagenesis screen in zebrafish. Genes Dev 13:2713–2724

    CAS  Google Scholar 

  • Andersen FA (2005) Amended final report on the safety assessment of polyacrylamide and acrylamide residues in cosmetics. Int J Toxicol 24:21–50

    CAS  Google Scholar 

  • Bakos K, Kovacs R, Balogh E, Sipos DK, Reining M, Gyomorei-Neuberger O, Balazs A, Kriszt B, Bencsik D, Csepeli A, Gazsi G, Hadzhiev Y, Urbanyi B, Mueller F, Kovacs B, Csenki Z (2019) Estrogen sensitive liver transgenic zebrafish (Danio rerio) line (Tg(vtg1:mCherry)) suitable for the direct detection of estrogenicity in environmental samples. Aquat Toxicol 208:157–167

    CAS  Google Scholar 

  • Balay SD, Widen SA, Waskiewicz AJ (2020) Analysis of zebrafish cryptochrome 2 and 4 expression in UV cone photoreceptors. Gene Expr Patterns 35:119100

    CAS  Google Scholar 

  • Baumann L, Ros A, Rehberger K, Neuhauss SCF, Segner H (2016) Thyroid disruption in zebrafish (Danio rerio) larvae: different molecular response patterns lead to impaired eye development and visual functions. Aquat Toxicol 172:44–55

    CAS  Google Scholar 

  • Bhatnagar A (2017) Environmental determinants of cardiovascular disease. Circ Res 121(2):162–180

    CAS  Google Scholar 

  • Blaze J, Roth TL (2015) Evidence from clinical and animal model studies of the long-term and transgenerational impact of stress on DNA methylation. Semin Cell Dev Biol 43:76–84

    CAS  Google Scholar 

  • Bournele D, Beis D (2016) Zebrafish models of cardiovascular disease. Heart Fail Rev 21(6):803–813

    CAS  Google Scholar 

  • Brannen KC, Chapin RE, Jacobs AC, Green ML (2016) Alternative models of developmental and reproductive toxicity in pharmaceutical risk assessment and the 3Rs. ILAR J 57(2):144–156

    CAS  Google Scholar 

  • Cao FJ, SoudersIIC L, Li PF, Adamovsky O, Pang S, Qiu LH, Martyniuk CJ (2019) Developmental toxicity of the fungicide ziram in zebrafish (Danio rerio). Chemosphere 214:303–313

    CAS  Google Scholar 

  • Cao FJ, Zhu LZ, Li H, Yu S, Wang CJ, Qiu LH (2016) Reproductive toxicity of azoxytrobin to adult zebrafish (Danio rerio). Environ Pollut 219:1109–1121

    CAS  Google Scholar 

  • Chakraborty C, Sharma AR, Sharma G, Lee SS (2016) Zebrafish: a complete animal model to enumerate the nanoparticle toxicity. J Nanobiotechnol 14(65)

  • Chen JF, Xiao YY, Gai ZX, Li R, Zhu ZX, Bai CL, Tanguay RL, Xu XJ, Huang CJ, Dong QX (2015) Reproductive toxicity of low level bisphenol A exposures in a two-generation zebrafish assay: evidence of male-specific effects. Aquat Toxicol 169:204–214

    CAS  Google Scholar 

  • Chen S, Gong ZY, Letcher RJ, Liu CS (2020) Promotion effect of liver tumor progression in male kras transgenic zebrafish induced by tris (1, 3-dichloro-2-propyl) phosphate. Ecotox Environ Safe 191:110220

    CAS  Google Scholar 

  • Chen YC, Priyadarshini M, Panula P (2009) Complementary developmental expression of the two tyrosine hydroxylase transcripts in zebrafish. Histochem Cell Biol 132(4):375–381

    CAS  Google Scholar 

  • Chew TW, Liu XJ, Liu L, Spitsbergen JM, Gong Z, Low BC (2014) Crosstalk of Ras and Rho: activation of RhoA abates Kras-induced liver tumorigenesis in transgenic zebrafish models. Oncogene 33:2717–2727

    CAS  Google Scholar 

  • Connors SL, Levitt P, Matthews SG, Slotkin TA, Johnston MV, Kinney HC, Johnson WG, Dailey RM, Zimmerman AW (2008) Fetal mechanisms in neurodevelopmental disorders. Pediatr Neurol 38(3):163–176

    Google Scholar 

  • Cornet C, Calzolari S, Miñana-Prieto R, Dyballa S, van Doornmalen E, Rutjes H, Savy T, D’Amico D, Terriente J (2017) ZeGlobalTox: an innovative approach to address organ drug toxicity using zebrafish. Int J Mol Sci 18:864

    Google Scholar 

  • De la Paz JF, Beiza N, Paredes-Zúñiga S, Hoare MS, Allende ML (2017) Triazole fungicides inhibit zebrafish hatching by blocking the secretory function of hatching gland cells. Int J Mol Sci 18(4):710

    Google Scholar 

  • Deeti S, O’Farrell S, Kennedy BN (2014) Early safety assessment of human oculotoxic drugs using the zebrafish visualmotor response. J Pharmacol Toxicol Methods 69(1):1–8

    CAS  Google Scholar 

  • Deveau AP, Bentley VL, Berman JN (2017) Using zebrafish models of leukemia to streamline drug screening and discovery. Exp Hematol 45:1–9

    CAS  Google Scholar 

  • Doe JE (2014) A proposal to improve clarity and communication in the EU Classification process for chemicals for carcinogenicity and reproductive and developmental toxicity. J Appl Toxicol 34(10):1068–1072

    CAS  Google Scholar 

  • Duan JC, Hu HJ, Li QL, Jiang LZ, Zou Y, Wang YP, Sun ZW (2016) Combined toxicity of silica nanoparticles and methylmercury on cardiovascular system in zebrafish (Danio rerio) embryos. Environ Toxicol Pharmacol 44:120–127

    CAS  Google Scholar 

  • Ducharme NA, Reif DM, Gustafsson JA, Bondesson M (2015) Comparison of toxicity values across zebrafish early life stages and mammalian studies: implications for chemical testing. Reprod Toxicol 55:3–10

    CAS  Google Scholar 

  • Ek F, Malo M, Andersson MÅ, Wedding C, Kronborg J, Svensson P, Waters S, Petersson P, Olsson R (2016) Behavioral analysis of dopaminergic activation in zebrafish and rats reveals similar phenotypes. ACS Chem Neurosci 7:633–646

    CAS  Google Scholar 

  • Ema M, Okuda H, Gamo M, Honda K (2017) A review of reproductive and developmental toxicity of silver nanoparticles in laboratory animals. Reprod Toxicol 67:149–164

    CAS  Google Scholar 

  • Esch CD, Slieker R, Wolterbeek A, Woutersen R, Groot DD (2012) Zebrafish as potential model for developmental neurotoxicity testing: a mini review. Neurotoxicol Teratol 34:545–553

    Google Scholar 

  • Fleisch VC, Neuhauss SCF (2010) Parallel visual cycles in the zebrafish retina. Prog Retin Eye Res 29(6):476–486

    Google Scholar 

  • Fontana BD, Mezzomo NJ, Kalueff AV, Rosemberg DB (2018) The developing utility of zebrafish models of neurological and neuropsychiatric disorders: a critical review. Exp Neurol 299:157–171

    Google Scholar 

  • Gao DX, Lin J, Ou KL, Chen Y, Li HB, Dai QH, Yu ZN, Zuo ZH, Wang CG (2018) Embryonic exposure to benzo(a)pyrene inhibits reproductive capability in adult female zebrafish and correlation with DNA methylation. Environ Pollut 240:403–411

    CAS  Google Scholar 

  • Gao DX, Wang CG, Xi ZH, Zhou YX, Wang YC, Zuo ZH (2017) Early-life benzo[a]pyrene exposure causes neurodegenerative syndromes in adult zebrafish (Danio rerio) and the mechanism involved. Toxicol Sci 157(1):74–84

    CAS  Google Scholar 

  • Gao DX, Wu MF, Wang CG, Wang YC, Zuo ZH (2015) Chronic exposure to low benzo[a]pyrene level causes neurodegenerative disease-like syndromes in zebrafish (Danio rerio). Aquat Toxicol 167:200–208

    CAS  Google Scholar 

  • Garcia GR, Noyes PD, Tanguay RL (2016) Advancements in zebrafish applications for 21st century toxicology. Pharmacol Ther 161:11–21

    CAS  Google Scholar 

  • Guo XC, Zhang SN, Lu SY, Zheng BH, Xie P, Chen J, Li GY, Liu CS, Wu Q, Cheng HC, Sang N (2018) Perfluorododecanoic acid exposure induced developmental neurotoxicity in zebrafish embryos. Environ Pollut 241:1018–1026

    CAS  Google Scholar 

  • Guo YY, Chen LG, Wu J, Hua JH, Yang LH (2019) Parental co-exposure to bisphenol A and nano-TiO2 causes thyroid endocrine disruption and developmental neurotoxicity in zebrafish offspring. Sci Total Environ 650(1):557–565

    CAS  Google Scholar 

  • Haddad T, Baginska E, Kümmerer K (2015) Transformation products of antibiotic and cytostatic drugs in the aquatic cycle that result from effluent treatment and abiotic/biotic reactions in the environment: an increasing challenge calling for higher emphasis on measures at the beginning of the pipe. Water Res 72:75–126

    CAS  Google Scholar 

  • Harada S, Yanbe M (2018) Adsorption by and artificial release of zinc and lead from porous concrete for recycling of adsorbed zinc and lead and of porous concrete to reduce urban non-point heavy metal runoff. Chemosphere 197:451–456

    CAS  Google Scholar 

  • He JH, Gao JM, Huang CJ, Li CQ (2014) Zebrafish models for assessing developmental and reproductive toxicity. Neurotoxicol Teratol 42:35–42

    Google Scholar 

  • He JH, Guo SY, ZhuF ZJJ, Chen YX (2013) A zebrafish phenotypic assay for assessing drug-induced hepatotoxicity. J Pharmacol Toxicol Methods 67(1):25–32

    CAS  Google Scholar 

  • Ho SM, Cheong A, Adgent MA, Veevers J, Suen AA, Tam NNC, Leung YK, Jefferson WN, Williams CJ (2017) Environmental factors, epigenetics, and developmental origin of reproductive disorders. Reprod Toxicol 68:85–104

    CAS  Google Scholar 

  • Homberg JR, Kyzar EJ, Nguyen M, Norton WH, Pittman J, Poudel MK, Gaikwad S, Nakamura S, Koshiba M, Yamanouchi H, Scattoni ML, Ullman JFP, Diamond DM, Kaluyeva AA, Parker MO, Klimenko VM, Apryatin SA, Brown RE, Kalueff AV (2016) Understanding autism and other neurodevelopmental disorders through experimental translational neurobehavioral models. Neurosci Biobehav Rev 65:292–312

    Google Scholar 

  • Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, Collin JE, Humphray S, McLaren K, Matthews L, McLaren S, Sealy I, Caccamo M, Churcher C, Scott C, Barrett JC, Koch R, Rauch GJ, White S, Chow W, Kilian B, Quintais LT, Guerra-Assuncao JA, Zhou Y, Gu Y, Yen J, Vogel JH, Eyre T, Redmond S, Banerjee R, Chi J, Fu B, Langley E, Maguire SF, Laird GK, Lloyd D, Kenyon E, Donaldson S, Sehra H, Almeida-King J, Loveland J, Trevanion S, Jones M, Quail M, Willey D, Hunt A, Burton J, Sims S, McLay K, Plumb B, Davis J, Clee C, Oliver K, Clark R, Riddle C, Elliot D, Threadgold G, Harden G, Ware D, Begum S, Mortimore B, Kerry G, Heath P, Phillimore B, Tracey A, Corby N, Dunn M, Johnson C, Wood J, Clark S, Pelan S, Griffiths G, Smith M, Glithero R, Howden P, Barker N, Lloyd C, Stevens C, Harley J, Holt K, Panagiotidis G, Lovell J, Beasley H, Henderson C, Gordon D, Auger K, Wright D, Collins J, Raisen C, Dyer L, Leung K, Robertson L, Ambridge K, Leongamornlert D, McGuire S, Gilderthorp R, Griffiths C, Manthravadi D, Nichol S, Barker G, Whitehead S, Kay M, Brown J, Murnane C, Gray E, Humphries M, Sycamore N, Barker D, Saunders D, Wallis J, Babbage A, Hammond S, Mashreghi-Mohammadi M, Barr L, Martin S, Wray P, Ellington A, Matthews N, Ellwood M, Woodmansey R, Clark G, Cooper J, Tromans A, Grafham D, Skuce C, Pandian R, Andrews R, Harrison E, Kimberley A, Garnett J, Fosker N, Hall R, Garner P, Kelly D, Bird C, Palmer S, Gehring I, Berger A, Dooley CM, Ersan-Urun Z, Eser C, Geiger H, Geisler M, Karotki L, Kirn A, Konantz J, Konantz M, Oberlander M, Rudolph-Geiger S, Teucke M, Lanz C, Raddatz G, Osoegawa K, Zhu B, Rapp A, Widaa S, Langford C, Yang F, Schuster SC, Carter NP, Harrow J, Ning Z, Herrero J, Searle SM, Enright A, Geisler R, Plasterk RH, Lee C, Westerfield M, de Jong PJ, Zon LI, Postlethwait JH, Nusslein-Volhard C, Hubbard TJ, Roest Crollius H, Rogers J, Stemple DL (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498–503

    CAS  Google Scholar 

  • Hu HJ, Zhang YN, Shi YF, Feng L, Duan JC, Sun ZW (2017) Microarray-based bioinformatics analysis of the combined effects of SiNPs and PbAc on cardiovascular system in zebrafish. Chemosphere 184:1298–1309

    CAS  Google Scholar 

  • Huang LX, Gao DX, Zhang YY, Wang CG, Zuo ZH (2014a) Exposure to low dose benzo[a]pyrene during early life stages causes symptoms similar to cardiac hypertrophy in adult zebrafish. J Hazard Mater 276:377–382

    CAS  Google Scholar 

  • Huang LX, Wang CG, Zhang YY, Wu MF, Zuo ZH (2013) Phenanthrene causes ocular developmental toxicity in zebrafish embryos and the possible mechanisms involved. J Hazard Mater 261:172–180

    CAS  Google Scholar 

  • Huang LX, Wang CG, Zhang YY, Li J, Zhong YF, Zhou YL, Chen YX, Zuo ZH (2012) Benzo[a]pyrene exposure influences the cardiac development and the expression of cardiovascular relative genes in zebrafish (Danio rerio) embryos. Chemosphere 87:369–375

    CAS  Google Scholar 

  • Huang LX, Zuo ZH, Zhang YY, Wang CG (2015) Toxicogenomic analysis in the combined effect of tributyltin and benzo[a]pyrene on the development of zebrafish embryos. Aquat Toxicol 158:157–164

    CAS  Google Scholar 

  • Huang LX, Zuo ZH, Zhang YY, Wu MF, Lin JJ, Wang CG (2014b) Use of toxicogenomics to predict the potential toxic effect of benzo[a]pyrene on zebrafish embryos: Ocular developmental toxicity. Chemosphere 108:55–61

    CAS  Google Scholar 

  • Huang MM, Jiao JJ, Wang J, Xia ZD, Zhang Y (2018a) Characterization of acrylamide-induced oxidative stress and cardiovascular toxicity in zebrafish embryos. J Hazard Mater 347:451–460

    CAS  Google Scholar 

  • Huang MM, Jiao JJ, Wang J, Xia ZD, Zhang Y (2018b) Exposure to acrylamide induces cardiac developmental toxicity in zebrafish during cardiogenesis. Environ Pollut 234:656–666

    CAS  Google Scholar 

  • Huang MM, Zhu FH, Jiao JJ, Wang J, Zhang Y (2019) Exposure to acrylamide disrupts cardiomyocyte interactions during ventricular morphogenesis in zebrafish embryos. Sci Total Environ 656:1337–1345

    CAS  Google Scholar 

  • Hung KWY, Suen MFK, Chen YF, Cai HB, Mo ZX, Yung KKL (2012) Detection of water toxicity using cytochrome P450 transgenic zebrafish as live biosensor: For polychlorinated biphenyls toxicity. Biosens Bioelectron 31(1):548–553

    CAS  Google Scholar 

  • International Agency for Research on Cancer (IARC) (1994) IARC monographs on the evaluation of the carcinogenic risks to humans, Some Industrial Chemicals. Ebrary Inc. Lyon 60:389–433

    Google Scholar 

  • Jang GH, Lee KY, Choi J, Kim SH, Lee KH (2016) Multifaceted toxicity assessment of catalyst composites in transgenic zebrafish embryos. Environ Pollut 216:755–763

    CAS  Google Scholar 

  • Jijie R, Solcan G, Nicoara M, Micu D, Strungaru SA (2020) Antagonistic effects in zebrafish (Danio rerio) behavior and oxidative stress induced by toxic metals and deltamethrin acute exposure. Sci Total Environ 698:134299

    CAS  Google Scholar 

  • Judson RS, Houck KA, Kavlock RJ, Knudsen TB, Martin MT (2010) In vitro screening of environmental chemicals for targeted testing prioritization: the ToxCast project. Environ Health Perspect 118:485–492

    CAS  Google Scholar 

  • Kalueff AV, Stewart AM, Gerlai R (2014) Zebrafish as an emerging model for studying complex brain disorders. Trends Pharmacol. Sci. 35(2):63–75

    CAS  Google Scholar 

  • Kanungo J, Cuevas E, Ali SF, Paule MG (2014) Zebrafish model in drug safety assessment. Curr Pharm Design 20:5416–5429

    CAS  Google Scholar 

  • Khoshnamvand M, Hao ZN, Fadare OO, Hanachi P, Chen YS, Liu JF (2020) Toxicity of biosynthesized silver nanoparticles to aquatic organisms of different trophic levels. Chemosphere 258:127346

    CAS  Google Scholar 

  • Kim J, Kim C, Oh H, Ryu B, Kim U, Lee JM, Jung CR, Park JH (2019) Trimethyltin chloride induces reactive oxygen species-mediated apoptosis in retinal cells during zebrafish eye development. Sci Total Environ 653:36–44

    CAS  Google Scholar 

  • King-Heiden TC, Mehta V, Xiong KM, Lanham KA, Antkiewicz DS, Ganser A, Heideman W, Peterson RE (2012) Reproductive and developmental toxicity of dioxin in fish. Mol Cell Endocrinol 354(1-2):121–138

    CAS  Google Scholar 

  • Komoike Y, Nomura-Komoike K, Matsuoka M (2020) Intake of acrylamide at the dietary relevant concentration causes splenic toxicity in adult zebrafish. Environ Res 189:109977

    CAS  Google Scholar 

  • Ladwani KD, Ramteke DS (2013) Assessment of poly aromatic hydrocarbon (PAH) dispersion in the near shore environment of Mumbai, India after a large scale oil spill. Bull Environ Contam Toxicol 90:515–520

    CAS  Google Scholar 

  • Laing LV, Viana J, Dempster EL, Trznadel M, Trunkfield LA, Uren Webster TM, van Aerle R, Paull GC, Wilson RJ, Mill J, Santos EM (2016) Bisphenol A causes reproductive toxicity, decreases dnmt1 transcription, and reduces global DNA methylation in breeding zebrafish (Danio rerio). Epigenetics 11(7):526–538

    CAS  Google Scholar 

  • Laptook AR, O’Shea TM, Shankaran S, Bhaskar B, Network NN (2005) Adverse neurodevelopmental outcomes among extremely low birth weight infants with a normal head ultrasound: prevalence and antecedents. Pediatrics 115:673–680

    Google Scholar 

  • Lele Z, Krone PH (1996) The zebrafish as a model system in developmental, toxicological and transgenic research. Biotechnol Adv 14(1):57–72

    CAS  Google Scholar 

  • Leong DP, Joseph PG, McKee M, Anand SS, Teo KK, Schwalm JD, Yusuf S (2017) Reducing the global burden of cardiovascular disease, Part 2. Circ Res 121(6):695–710

    CAS  Google Scholar 

  • Li H, Yu S, Cao FJ, Wang CJ, Zheng MQ, Li XF, Qiu LH (2018) Developmental toxicity and potential mechanisms of pyraoxystrobin to zebrafish (Danio rerio). Ecotox Environ Safe 151:1–9

    Google Scholar 

  • Li J, Liu JF, Zhang YH, Wang XD, Li WJ, Zhang HQ, Wang HL (2016) Screening on the differentially expressed miRNAs in zebrafish (Danio rerio) exposed to trace β-diketone antibiotics and their related functions. Aquat Toxicol 178:27–38

    CAS  Google Scholar 

  • Li K, Wu JQ, Jiang LL, Shen LZ, Li JY, He ZH, Wei P, Lv Z, He MF (2017) Developmental toxicity of 2,4-dichlorophenoxyacetic acid in zebrafish embryos. Chemosphere 171:40–48

    Google Scholar 

  • Li M, Liu XY, Feng XZ (2019a) Cardiovascular toxicity and anxiety-like behavior induced by deltamethrin in zebrafish (Danio rerio) larvae. Chemosphere 219:155–164

    CAS  Google Scholar 

  • Li WY, Jin DQ, Zhong TP (2019b) Photoreceptor cell development requires prostaglandin signaling in the zebrafish retina. Biochem Biophys Res Commun 510(2):230–235

    CAS  Google Scholar 

  • Liu HC, Chu TY, Chen LL, Gui WJ, Zhu GN (2017a) In vivo cardiovascular toxicity induced by acetochlor in zebrafish larvae. Chemosphere 181:600–608

    CAS  Google Scholar 

  • Liu HC, Chu TY, Chen LL, Gui WJ, Zhu GN (2017b) The cardiovascular toxicity of triadimefon in early life stage of zebrafish and potential implications to human health. Environ Pollut 231(1):1093–1103

    CAS  Google Scholar 

  • Liu XY, Zhang QP, Li SB, MiP CDY, Zhao X, Feng XZ (2018) Developmental toxicity and neurotoxicity of synthetic organic insecticides in zebrafish. Chemosphere 199:16–25

    CAS  Google Scholar 

  • Lopes FM, Junior ASV, Corcini CD, da Silva AC, Guazzelli VG, Tavares G, da Rosa CE (2014) Effect of glyphosate on the sperm quality of zebrafish Danio rerio. Aquat Toxicol 155:322–326

    CAS  Google Scholar 

  • Lor Y, Revak A, Weigand J, Hicks E, Howard DR, King-Heiden TC (2015) Juvenile exposure to vinclozolin shifts sex ratios and impairs reproductive capacity of zebrafish. Reprod Toxicol 58:111–118

    CAS  Google Scholar 

  • Lyall K, Croen L, Daniels J, Fallin MD, Ladd-Acosta C, Lee BK, Park BY, Snyder NW, Schendel D, Volk H, Windham GC, Newschaffer C (2017) The changing epidemiology of autism spectrum disorders. Annu. Rev. Public Health 38:81–102

    Google Scholar 

  • Ma YB, Lu CJ, Junaid M, Jia PP, Yang L, Zhang JH, Pei DS (2018) Potential adverse outcome pathway (AOP) of silver nanoparticles mediated reproductive toxicity in zebrafish. Chemosphere 207:320–328

    CAS  Google Scholar 

  • Malhotra N, Chen JR, Sarasamma S, Audira G, Siregar P, Liang ST, Lai YH, Lin GM, Ger TR, Hsiao CD (2019) Ecotoxicity assessment of Fe3O4 magnetic nanoparticle exposure in adult zebrafish at an environmental pertinent concentration by behavioral and biochemical testing. Nanomaterials 9(6):873

    CAS  Google Scholar 

  • Mandy W, Lai MC (2016) Annual research review: the role of the environment in the developmental psychopathology of autism spectrum condition. J Child Psychol Psychiatry 57(3):271–292

    Google Scholar 

  • Manjunatha B, Park SH, Kim K, Kundapur RR, Lee SJ (2018) Pristine graphene induces cardiovascular defects in zebrafish (Danio rerio) embryogenesis. Environ Pollut 243:246–254

    CAS  Google Scholar 

  • Maskaoui K, Zhou JL, Hong HS, Zhang ZL (2002) Contamination by poly-cyclic aromatic hydro-carbons in the Jiulong River Estuary and Western Xiamen Sea China. Environ Pollut 118:109–122

    CAS  Google Scholar 

  • McGrath P, Li CQ (2008) Zebrafish: a predictive model for assessing drug-induced toxicity. Drug Discov Today 13(9):394–401

    CAS  Google Scholar 

  • Meshalkina DA, Kizlyk MN, Kysil EV, Collier AD, Echevarria DJ, Abreu MS, Barcellos LJG, Song C, Warnick JE, Kyzar EJ, Kalueff AV (2018) Zebrafish models of autism spectrum disorder. Exp Neurol 299:207–216

    CAS  Google Scholar 

  • Miller GW, Chandrasekaran V, Yaghoobi B, Lein PJ (2018) Opportunities and challenges for using the zebrafish to study neuronal connectivity as an endpoint of developmental neurotoxicity. Neurotoxicology 67:102–111

    CAS  Google Scholar 

  • Monteiro L, Moens T, Lynen F, Traunspurger W (2019a) Effects of the water-soluble fraction of a crude oil on freshwater meiofauna and nematode assemblages. Ecotox Environ Safe 176:186–195

    CAS  Google Scholar 

  • Monteiro L, Traunspurger W, Lynen F, Moens T (2019b) Effects of the water-soluble fraction of a crude oil on estuarine meiofauna: a microcosm approach. Mar Environ Res 147:113–125

    CAS  Google Scholar 

  • Moon WK, Atique U, An KG (2020) Ecological risk assessments and eco-toxicity analyses using chemical, biological, physiological responses, DNA damages and gene-level biomarkers in Zebrafish (Danio rerio) in an urban stream. Chemosphere 239:124754

    CAS  Google Scholar 

  • Mu XY, Pang S, Sun XZ, Gao JJ, Chen JY, Chen XF, Li XF, Wang CJ (2013) Evaluation of acute and developmental effects of difenoconazole via multiple stage zebrafish assays. Environ Pollut 175:147–157

    CAS  Google Scholar 

  • Nasri A, Allouche M, Hannachi A, Harrath AH, Aldahmash W, Alwasel S, Mahmoudi E, Beyrem H, Boufahja F (2020) Restructuring of a meiobenthic assemblage after sediment contamination with an antibacterial compound: case study of ciprofloxacin. Ecotox Environ Safe 205:111084

    CAS  Google Scholar 

  • Nishimura Y, Murakami S, Ashikawa Y, Sasagawa S, Umemoto N, Shimada Y, Tanaka T (2015) Zebrafish as a system toxicology model for developmental neurotoxicity testing. Congenit Anom 55:1–16

    Google Scholar 

  • Nogueira V, Sousa CT, Araujo JP, Pereira R (2020) Evaluation of the toxicity of nickel nanowires to freshwater organisms at concentrations and short-term exposures compatible with their application in water treatment. Aquat Toxicol 105595

  • North TE, Goessling W, Walkley CR, Lengerke C, Kopani KR, Lord AM, Weber GJ, Bowman TV, Jang I, Grosser T, FitzGerald GA, Daley GQ, Orkin SH, Zon LI (2007) Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis. Nature 447:1007–1011

    CAS  Google Scholar 

  • O’Flaherty R, Bergin A, Flampouri E, Mota LM, Obaidi I, Quigley A, Xie YJ, Butler M (2020) Mammalian cell culture for production of recombinant proteins: a review of the critical steps in their biomanufacturing. Biotechnol Adv 43:107552

    Google Scholar 

  • Oikonomou E, Lazaros G, Georgiopoulos G, Christoforatou E, Papamikroulis GA, Vogiatzi G, Chasikidis C, Zacharia E, Giannaki A, Bourouki E, Mavratzas T, Stofa E, Papakonstantinou M, Tousouli M, Tousoulis D (2016) Environment and cardiovascular disease: rationale of the corinthia study. Hell J Cardiol:194–197

  • Oliveira JD, Chadili E, Piccini B, Turies C, Maillot-Maréchal E, Palluel O, Pardon P, Budzinski H, Cousin X, Brion F, Hinfray N (2020) Refinement of an OECD test guideline for evaluating the effects of endocrine disrupting chemicals on aromatase gene expression and reproduction using novel transgenic cyp19a1a-eGFP zebrafish. Aquat Toxicol 220:105403

    Google Scholar 

  • Orbach SM, Ehrich MF, Rajagopalan P (2018) High-throughput toxicity of chemicals and mixtures in organotypic multi-cellular cultures of primary human hepatic cells. Toxicol in Vitro 51:83–94

    CAS  Google Scholar 

  • Ou HC, Santos F, Raible DW, Simon JA, Rubel EW (2010) Drug screening for hearing loss: using the zebrafish lateral line to screen for drugs that prevent and cause hearing loss. Drug Discov Today 15(7-8):265–271

    CAS  Google Scholar 

  • Padilla S, Corum D, Padnos B, Hunter DL, Beam A, Houck KA, Sipes N, Kleinstreuer N, Knudsen T, Dix DJ, Reif DM (2012) Zebrafish developmental screening of the ToxCastTM Phase I chemical library. Reprod Toxicol 33(2):174–187

    CAS  Google Scholar 

  • Panula P, Sallinen V, Sundvik M, Kolehmainen J, Torkko V (2006) Modulatory neurotransmitter systems and behavior: towards zebrafish models of neurodegenerative diseases. Zebrafish 3(2):235–247

    CAS  Google Scholar 

  • Perkins JT, Petriello MC, Newsome BJ, Hennig B (2016) Polychlorinated biphenyls and links to cardiovascular disease. Environ Sci Pollut Res Int 23(3):2160–2172

    CAS  Google Scholar 

  • Qiao RX, Deng YF, Zhang SH, Wolosker MB, Zhu QD, Ren HQ, Zhang Y (2019) Accumulation of different shapes of microplastics initiates intestinal injury and gut microbiota dysbiosis in the gut of zebrafish. Chemosphere 236:124334

    CAS  Google Scholar 

  • Ranjani TS, Pitchika GK, Yedukondalu K, Gunavathi Y, Daveedu T, Sainath SB, Philip GH, Pradeepkiran JA (2020) Phenotypic and transcriptomic changes in zebrafish (Danio rerio) embryos/larvae following cypermethrin exposure. Chemosphere 249:126148

    CAS  Google Scholar 

  • Rennekamp AJ, Peterson RT (2015) 15 years of zebrafish chemical screening. Curr Opin Chem Biol 24:58–70

    CAS  Google Scholar 

  • Richardson JR, Fitsanakis V, Westerink RHS, Kanthasamy AG (2019) Neurotoxicity of pesticides. Acta Neuropathol 138:343–362

    CAS  Google Scholar 

  • Richardson R, Tracey-White D, Webster A, Moosajee M (2017) The zebrafish eye-a paradigm for investing human ocular genetics. Eye 31:68–86

    CAS  Google Scholar 

  • Richetti SK, Rosemberg DB, Ventura-Lima J, Monserrat JM, Bogo MR, Bonan CD (2011) Acetylcholinesterase activity and antioxidant capacity of zebrafish brain is altered by heavy metal exposure. NeuroToxicology 32(1):116–122

    CAS  Google Scholar 

  • Roy NM, Ochs J, Zambrzycka E, Anderson A (2016) Glyphosate induces cardiovascular toxicity in Danio rerio. Environ Toxicol Pharmacol 46:292–300

    CAS  Google Scholar 

  • Rosenfeld CS (2010) Animal models to study environmental epigenetics. Biol Reprod 82(3):473–488

    CAS  Google Scholar 

  • Selderslaghs IWT, Hooyberghs J, Blust R, Witters HE (2013) Assessment of the developmental neurotoxicity of compounds by measuring locomotor activity in zebrafish embryos and larvae. Neurotoxicol Teratol 37:44–56

    CAS  Google Scholar 

  • Seritrakul P, Gross JM (2019) Genetic and epigenetic control of retinal development in zebrafish. Curr Opin Neurobiol 59:120–127

    CAS  Google Scholar 

  • Shen C, Zhou YX, Ruan JP, Chuang YJ, Wang CG, Zuo ZH (2018) Generation of a Tg(cyp1a-12DRE:EGFP) transgenic zebrafish line as a rapid in vivo model for detecting dioxin-like compounds. Aquat Toxicol 205:174–181

    CAS  Google Scholar 

  • Shen C, Zhou YX, Tang C, He CY, Zuo ZH (2020) Developmental exposure to mepanipyrim induces locomotor hyperactivity in zebrafish (Danio rerio) larvae. Chemosphere 256:127106

    CAS  Google Scholar 

  • Shen R, Yu YC, Lan R, Yu R, Yuan Z, Xia ZN (2019) The cardiovascular toxicity induced by high doses of gatifloxacin and ciprofloxacin in zebrafish. Environ Pollut 254:112861

    CAS  Google Scholar 

  • Shi GH, Guo H, Sheng N, Cui QQ, Pan YT, Wang JX, Guo Y, Dai JY (2018b) Two-generational reproductive toxicity assessment of 6:2 chlorinated polyfluorinated ether sulfonate (F-53B, a novel alternative to perfluorooctane sulfonate) in zebrafish. Environ Pollut 243:1517–1527

    CAS  Google Scholar 

  • Shi QP, Tsui MMP, Hu CY, Lam JCW, Zhou BS, Chen LG (2019) Acute exposure to triphenyl phosphate (TPhP) disturbs ocular development and muscular organization in zebrafish larvae. Ecotox Environ Safe 179:119–126

    CAS  Google Scholar 

  • Shi QP, Wang M, Shi FQ, Yang LH, Guo YY, Feng CL, Liu JF, Zhou BS (2018a) Developmental neurotoxicity of triphenyl phosphate in zebrafish larvae. Aquat Toxicol 203:80–87

    CAS  Google Scholar 

  • Shi WJ, Huang GY, Jiang YX, Ma DD, Chen HX, Huang MZ, Hou LP, Xie LT, Ying GG (2020) Medroxyprogesterone acetate affects eye growth and the transcription of associated genes in zebrafish. Ecotox Environ Safe 193:110371

    CAS  Google Scholar 

  • Sieber S, Grossen P, Bussmann J, Campbell F, Kros A, Witzigmann D, Huwyler J (2019) Zebrafish as a preclinical in vivo screening model for nanomedicines. Adv Drug Deliv Rev 151-152:152–168

    CAS  Google Scholar 

  • Sifakis S, Androutsopoulos VP, Tsatsakis AM, Spandidos DA (2017) Human exposure to endocrine disrupting chemicals: effects on the male and female reproductive systems. Environ Toxicol Pharmacol 51:56–70

    CAS  Google Scholar 

  • Smith CJ, Perfetti TA, Rumple MA, Rodgman A, Doolittle DJ (2000) “IARC group 2A carcinogens” reported in cigarette mainstream smoke. Food Chem Toxicol 38:371–383

    CAS  Google Scholar 

  • Strungaru SA, Robea MA, Plavan G, Todirascu-Ciornea E, Ciobica A, Nicoara M (2018) Acute exposure to methylmercury chloride induces fast changes in swimming performance, cognitive processes and oxidative stress of zebrafish (Danio rerio) as reference model for fish community. J Trace Elem Med Biol 47:115–123

    CAS  Google Scholar 

  • Suen MFK, Chan WS, Hung KWY, Chen YF, Mo ZX, Yung KKL (2013) Assessments of the effects of nicotine and ketamine using tyrosine hydroxylase-green fluorescent protein transgenic zebrafish as biosensors. Biosens Bioelectron 42:177–185

    CAS  Google Scholar 

  • Sun GJ, Li YQ (2019) Exposure to DBP induces the toxicity in early development and adverse effects on cardiac development in zebrafish (Danio rerio). Chemosphere 218:76–82

    CAS  Google Scholar 

  • Sun JL, Zhang Q, Wang ZP, Yan B (2013) Effects of nanotoxicity on female reproductivity and fetal development in animal models. Int J Mol Sci 14(5):9319–9337

    Google Scholar 

  • Teixidó E, Barenys M, Piqué E, Llocbet JM, Gómez-Catalán J (2019) Cardiovascular effects of PCB 126 (3,3´,4,4´,5-pentachlorobiphenyl) in zebrafish embryos and impact of co-exposure to redox modulating chemicals. Int J Mol Sci 20(5):1065

    Google Scholar 

  • Tierney KB (2011) Behavioural assessments of neurotoxic effects and neurodegeneration in zebrafish. Biochim Biophys Acta Mol basis Dis 1812(3):381–389

    CAS  Google Scholar 

  • Tsai MS, Chen MH, Lin CC, Liu CY, Chen PC (2019) Children’s environmental health based on birth cohort studies of Asia (2) - air pollution, pesticides, and heavy metals. Environ Res 179:108754

    CAS  Google Scholar 

  • Turner A, Lewis M (2018) Lead and other heavy metals in soils impacted by exterior legacy paint in residential areas of south west England. Sci Total Environ 619-620:1206–1213

    CAS  Google Scholar 

  • Udvadia AJ, Linney E (2003) Windows into development: historic, current, and future perspectives on transgenic zebrafish. Dev Biol 256:1–17

    CAS  Google Scholar 

  • Uren Webster TM, Laing LV, Florance H, Santos EM (2014) Effects of glyphosate and its formulation, roundup, on reproduction in zebrafish (Danio rerio). Environ Sci Technol 48:1271–1279

    CAS  Google Scholar 

  • Vargas R, Ponce-Canchihuamán J (2017) Emerging various environmental threats to brain and overview of surveillance system with zebrafish model. Toxicol Rep 4:467–473

    Google Scholar 

  • Wang HL, Zhou LQ, Meng Z, Su ML, Zhang SH, Huang PZ, Jiang F, Liao XJ, Cao ZG, Lu HQ (2019a) Clethodim exposure induced development toxicity and behaviour alteration in early stages of zebrafish life. Environ Pollut 255(1):113218

    CAS  Google Scholar 

  • Wang HL, Meng Z, Zhou LQ, Cao ZG, Liao XJ, Ye RF, Lu HQ (2019b) Effects of acetochlor on neurogensis and behaviour in zebrafish at early developmental stages. Chemosphere 220:954–964

    CAS  Google Scholar 

  • Wang YC, Shen C, Wang CG, Zhou YX, Gao DX, Zuo ZH (2018) Maternal and embryonic exposure to the water soluble fraction of crude oil or lead induces behavioral abnormalities in zebrafish (Danio rerio), and the mechanisms involved. Chemosphere 191:7–16

    CAS  Google Scholar 

  • Wang YC, Zhong HX, Wang CG, Gao DX, Zhou YL, Zuo ZH (2016) Maternal exposure to the water soluble fraction of crude oil, lead and their mixture induces autism-like behavioral deficits in zebrafish (Danio rerio) larvae. Ecotox Environ Safe 134:23–30

    CAS  Google Scholar 

  • Weber GJ, Sepúlveda MS, Peterson SM, Lewis SS, Freeman JL (2013) Transcriptome alterations following developmental atrazine exposure in zebrafish are associated with disruption of neuroendocrine and reproductive system function, cell cycle, and carcinogenesis. Toxicol Sci 132(2):458–466

    CAS  Google Scholar 

  • Woodruff TJ, Axelrad DA, Kyle AD, Nweke O, Miller GG, Hurley BJ (2004) Trends in environmentally related childhood illnesses. Pediatrics 113(4):1133–1140

    Google Scholar 

  • Wu MF, Wu D, Wang CG, Guo ZZ, Li BW, Zuo ZH (2016) Hexabromocyclododecane exposure induces cardiac hypertrophy and arrhythmia by inhibiting miR-1 expression via up-regulating of the homeobox gene Nkx2.5. J Hazard Mater 302:304–313

    CAS  Google Scholar 

  • Wu MF, Zuo ZH, Li BW, Huang LX, Chen M, Wang CG (2013) Effects of low-level hexabromocyclododecane (HBCD) exposure on cardiac development in zebrafish embryos. Ecotoxicology 22:1200–1207

    CAS  Google Scholar 

  • Wu YQ, Yang QH, Chen M, Zhang Y, Zuo ZH, Wang CG (2018a) Fenbuconazole exposure impacts the development of zebrafish embryos. Ecotox Environ Safe 158:293–299

    CAS  Google Scholar 

  • Wu YQ, Zuo ZH, Chen M, Zhou YX, Yang QH, Zhuang SS, Wang CG (2018b) The developmental effects of low-level procymidone towards zebrafish embryos and involved mechanism. Chemosphere 193:928–935

    CAS  Google Scholar 

  • Wu YQ, Zhang Y, Chen M, Yang QH, Zhuang SS, Lv LJ, Zuo ZH, Wang CG (2019) Exposure to low-level metalaxyl impacts the cardiac development and function of zebrafish embryos. J Environ Sci 85:1–8

    Google Scholar 

  • Xiao WY, Li YW, Chen QL, Liu ZH (2018) Tributyltin impaired reproductive success in female zebrafish through disrupting oogenesis, reproductive behaviors and serotonin synthesis. Aquat Toxicol 200:206–216

    CAS  Google Scholar 

  • Xie SL, Junaid M, Bian WP, Luo JJ, Syed JH, Wang C, Xiong WX, Ma YB, Niu A, Yang XJ, Zou JX, Pei DS (2018) Generation and application of a novel transgenic zebrafish line Tg(cyp1a:mCherry) as an in vivo assay to sensitively monitor PAHs and TCDD in the environment. J Hazard Mater 344:723–732

    CAS  Google Scholar 

  • Xu HY, Li CX, Suklai P, Zeng QH, Chong R, Gong ZY (2018) Differential sensitivities to dioxin-like compounds PCB 126 and PeCDF between Tg(cyp1a:gfp) transgenic medaka and zebrafish larvae. Chemosphere 192:24–30

    CAS  Google Scholar 

  • Xu Y, Cui B, Ran R, Liu Y, Chen HP, Kai GY, Shi JX (2014) Risk assessment, formation, and mitigation of dietary acrylamide: current status and future prospects. Food Chem Toxicol 69:1–12

    CAS  Google Scholar 

  • Zakaria ZZ, Benslimane FM, Nasrallah GK, Shurbaji S, Younes NN, Mraiche F, Da’as SI, Yalcin HC (2018) Using zebrafish for investigating the molecular mechanisms of drug-induced cardiotoxicity. BioMed Res Int:1642684

  • Zhang C, Wang J, Zhang S, Zhu LS, Du ZK, Wang JH (2017) Acute and subchronic toxicity of pyraclostrobin in zebrafish (Danio rerio). Chemosphere 188:510–516

    CAS  Google Scholar 

  • Zhang W, Sheng N, Wang MH, Zhang HX, Dai JY (2016) Zebrafish reproductive toxicity induced by chronic perfluorononanoate exposure. Aquat Toxicol 175:269–276

    CAS  Google Scholar 

  • Zhang X, Hong Q, Yang L, Zhang M, Guo XR, Chi X, Tong ML (2015) PCB1254 exposure contributes to the abnormalities of optomotor responses and influence of the photoreceptor cell development in zebrafish larvae. Ecotox Environ Safe 118:133–138

    CAS  Google Scholar 

  • Zhang YY, Huang LX, Wang CG, Gao DX, Zuo ZH (2013a) Phenanthrene exposure produces cardiac defects during embryo development of zebrafish (Danio rerio) through activation of MMP-9. Chemosphere 93:1168–1175

    CAS  Google Scholar 

  • Zhang YY, Huang LX, Zuo ZH, Chen YX, Wang CG (2013b) Phenanthrene exposure causes cardiac arrhythmia in embryonic zebrafish via perturbing calcium handling. Aquat Toxicol 142-143:26–32

    CAS  Google Scholar 

  • Zhang YY, Wang CG, Huang LX, Chen R, Chen YX, Zuo ZH (2012) Low-level pyrene exposure causes cardiac toxicity in zebrafish (Danio rerio) embryos. Aquat Toxicol 114-115:119–124

    CAS  Google Scholar 

  • Zhou LH, Zhou MQ, Tan HD, Xiao MX (2020a) Cypermethrin-induced cortical neurons apoptosis via the Nrf2/ARE signaling pathway. Pestic Biochem Physiol 165:104547

    CAS  Google Scholar 

  • Zhou YX, Shen C, Ruan JP, He CY, Chen M, Wang CG, Zuo ZH (2020b) Generation and application of a Tg(cyp1a:egfp) transgenic marine medaka (Oryzias melastigma) line as an in vivo assay to sensitively detect dioxin-like compounds in the environment. J Hazard Mater 391:122192

    CAS  Google Scholar 

  • Zhu J, Tang L, Qiao SL, Wang LJ, Feng YM, Wang L, Wu Q, Ding P, Zhang Z, Li L (2020) Low-dose methylmercury exposure impairs the locomotor activity of zebrafish: Role of intestinal inositol metabolism. Environ Res 190:110020

    CAS  Google Scholar 

  • Zhu JJ, Xu YQ, He JH, Yu HP, Huang CJ, Gao JM, Dong QX, Xuan YX, Li CQ (2014) Human cardiotoxic drugs delivered by soaking and microinjection induce cardiovascular toxicity in zebrafish. J Appl Toxicol 34(2):139–148

    CAS  Google Scholar 

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Funding

This work was supported by the Natural Science Foundation of Fujian Province of China (No. 2018 J01067).

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  1. Key Laboratory of Ministry of Education for Subtropical Wetland Ecosystem Research, School of Life Sciences, Xiamen University, Xiangan South Road, Xiamen, 361002, Fujian, China

    Chao Shen & Zhenghong Zuo

  2. State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, 361002, Fujian, China

    Zhenghong Zuo

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  1. Chao Shen
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Chao Shen: conceptualization; literature search; writing—original draft preparation; writing—review and editing

Zhenghong Zuo: funding acquisition; resources; supervision; writing—review and editing

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Correspondence to Zhenghong Zuo.

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Shen, C., Zuo, Z. Zebrafish (Danio rerio) as an excellent vertebrate model for the development, reproductive, cardiovascular, and neural and ocular development toxicity study of hazardous chemicals. Environ Sci Pollut Res 27, 43599–43614 (2020). https://doi.org/10.1007/s11356-020-10800-5

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