Zebrafish: A Marvel of High-Throughput Biology for 21st Century Toxicology

Current environmental health reports

Volumn 1, Issue 4, 2014, Pages 341-352

  Bugel, Sean M ^a   Tanguay, Robert L ^a   Planchart, Antonio ^b  

^a OREGON STATE UNIVERSITY   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Environmental exposure; High throughput screening; Human health; Zebrafish embryo model

Indexed keywords

EID: 84930382819     PISSN: None     EISSN: 21965412     Source Type: Journal    
DOI: 10.1007/s40572-014-0029-5     Document Type: Review

References (143)

1. Anonymous. Reduce, refine, replace. Nat Immunol. 2010;11(11):971.
2. Bailey J, Oliveri A, Levin ED. Zebrafish model systems for developmental neurobehavioral toxicology. Birth Defects Res C Embryo Today. 2013;99(1):14–23.
3. Gibert Y, Trengove MC, Ward AC. Zebrafish as a genetic model in pre-clinical drug testing and screening. Curr Med Chem. 2013;20(19):2458–66.
4. Lin S, Zhao Y, Nel AE, Lin S. Zebrafish: an in vivo model for nano EHS studies. Small. 2013;9(9–10):1608–18.
5. Helenius IT, Yeh JR. Small zebrafish in a big chemical pond. J Cell Biochem. 2012;113(7):2208–16.
6. Peterson RT, Macrae CA. Systematic approaches to toxicology in the zebrafish. Annu Rev Pharmacol Toxicol. 2012;52:433–53.
7. Sipes NS, Padilla S, Knudsen TB. Zebrafish: as an integrative model for twenty-first century toxicity testing. Birth Defects Res C Embryo Today. 2011;93(3):256–67.
8. Underwood MA, Gilbert WM, Sherman MP. Amniotic fluid: not just fetal urine anymore. J Perinatol. 2005;25(5):341–8.
9. Engel SM, Levy B, Liu Z, Kaplan D, Wolff MS. Xenobiotic phenols in early pregnancy amniotic fluid. Reprod Toxicol. 2006;21(1):110–2.
10. Foster WG, Chan S, Platt L, Hughes Jr CL. Detection of phytoestrogens in samples of second trimester human amniotic fluid. Toxicol Lett. 2002;129(3):199–205.
11. Miller MF, Chernyak SM, Domino SE, Batterman SA, Loch-Caruso R. Concentrations and speciation of polybrominated diphenyl ethers in human amniotic fluid. Sci Total Environ. 2012;417–418:294–8.
12. Luzardo OP, Mahtani V, Troyano JM, et al. Determinants of organochlorine levels detectable in the amniotic fluid of women from Tenerife Island (Canary Islands, Spain). Environ Res. 2009;109(5):607–13.
13. Nolte DL, Mason JR. Maternal ingestion of ortho-aminoacetophenone during gestation affects intake by offspring. Physiol Behav. 1995;58(5):925–8.
14. Chen M, Edlow AG, Lin T, et al. Determination of bisphenol-A levels in human amniotic fluid samples by liquid chromatography coupled with mass spectrometry. J Sep Sci. 2011;34(14):1648–55.
15. Ikezuki Y, Tsutsumi O, Takai Y, Kamei Y, Taketani Y. Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum Reprod. 2002;17(11):2839–41.
16. Brien JF, Loomis CW, Tranmer J, McGrath M. Disposition of ethanol in human maternal venous blood and amniotic fluid. Am J Obstet Gynecol. 1983;146(2):181–6.
17. Divers Jr WA, Wilkes MM, Babaknia A, Yen SS. Maternal smoking and elevation of catecholamines and metabolites in the amniotic fluid. Am J Obstet Gynecol. 1981;141(6):625–8.
18. Schmidt W, Pfaller K, Klima G. Optical and electron microscopy studies of human fetal membranes. 2. Chorion and decidua [in German. Zentralbl Gynakol. 1982;104(18):1137–48.
19. Howe K et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature. 2013;496(7446):498–503.
20. Ohno S. Evolution by gene duplication. Berlin: Springer-Verlag; 1970. p. xv. 160 p.
21. Taylor JS, Raes J. Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet. 2004;38:615–43.
22. Yan YL, Willoughby J, Liu D, et al. A pair of Sox: distinct and overlapping functions of zebrafish sox9 co-orthologs in craniofacial and pectoral fin development. Development. 2005;132(5):1069–83.
23. Kent J, Wheatley SC, Andrews JE, Sinclair AH, Koopman P. A male-specific role for SOX9 in vertebrate sex determination. Development. 1996;122(9):2813–22.
24. Bi W, Deng JM, Zhang Z, Behringer RR, de Crombrugghe B. Sox9 is required for cartilage formation. Nat Genet. 1999;22(1):85–9.
25. Xiong KM, Peterson RE, Heideman W. Aryl hydrocarbon receptor-mediated down-regulation of sox9b causes jaw malformation in zebrafish embryos. Mol Pharmacol. 2008;74(6):1544–53.
26. Planchart A, Mattingly CJ. 2,3,7,8-Tetrachlorodibenzo-p-dioxin upregulates FoxQ1b in zebrafish jaw primordium. Chem Res Toxicol. 2010;23(3):480–7.
27. Beis D, Stainier DY. In vivo cell biology: following the zebrafish trend. Trends Cell Biol. 2006;16(2):105–12.
28. Weber M, Huisken J. Light sheet microscopy for real-time developmental biology. Curr Opin Genet Dev. 2011;21(5):566–72.
29. Solnica-Krezel L, Schier AF, Driever W. Efficient recovery of ENU-induced mutations from the zebrafish germline. Genetics. 1994;136(4):1401–20.
30. Gaiano N et al. Insertional mutagenesis and rapid cloning of essential genes in zebrafish. Nature. 1996;383(6603):829–32.
31. Sander JD et al. Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nat Biotechnol. 2011;29(8):697–8.
32. Huang P et al. Heritable gene targeting in zebrafish using customized TALENs. Nat Biotechnol. 2011;29(8):699–700.
33. Hwang WY et al. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol. 2013;31(3):227–9. This study demonstrates the utility and application of the CRISPR-Cas system, which will greatly accelerate reverse genetic and mechanistic toxicological studies in the zebrafish.
34. Kettleborough RN et al. A systematic genome-wide analysis of zebrafish protein-coding gene function. Nature. 2013;496(7446):494–7.
35. Fisher BE. 20 years of toxicology. Environ Health Perspect. 1998;106(10):A484–7.
36. Vogel SA, Roberts JA. Why the toxic substances control act needs an overhaul, and how to strengthen oversight of chemicals in the interim. Health Aff (Millwood). 2011;30(5):898–905.
37. Wilson MP, Schwarzman MR. Toward a new U.S. chemicals policy: rebuilding the foundation to advance new science, green chemistry, and environmental health. Environ Health Perspect. 2009;117(8):1202–9.
38. Van der Wielen A. REACH: next step to a sound chemicals management. J Expo Sci Environ Epidemiol. 2007;17 Suppl 1:S2–6.
39. Carpenter DO. Polychlorinated biphenyls (PCBs): routes of exposure and effects on human health. Rev Environ Health. 2006;21(1):1–23.
40. Lindemann K. On the prognosis and therapy of severe abnormalities of the extremities [in German]. Acta Orthop Scand. 1962;32:298–306.
41. Lan SF, Starly B. Alginate based 3D hydrogels as an in vitro co-culture model platform for the toxicity screening of new chemical entities. Toxicol Appl Pharmacol. 2011;256(1):62–72.
42. Godoy P et al. Recent advances in 2D and 3D in vitro systems using primary hepatocytes, alternative hepatocyte sources and non-parenchymal liver cells and their use in investigating mechanisms of hepatotoxicity, cell signaling and ADME. Arch Toxicol. 2013;87(8):1315–530.
43. DesRochers TM, Suter L, Roth A, Kaplan DL. Bioengineered 3D human kidney tissue, a platform for the determination of nephrotoxicity. PLoS One. 2013;8(3):e59219.
44. Padilla S et al. Zebrafish developmental screening of the ToxCast™ Phase I chemical library. Reprod Toxicol. 2012;33(2):174–87.
45. Truong L et al. Multidimensional in vivo hazard assessment using zebrafish. Toxicol Sci. 2014;137(1):212–33. This study is currently the most comprehensive evaluation of developmental toxicity for a large library of chemicals (1,060 compounds), and highlights a truly high-throughput application for zebrafish in vivo toxicity screening.
46. Bonventre JA, White LA, Cooper KR. Craniofacial abnormalities and altered wnt and mmp mRNA expression in zebrafish embryos exposed to gasoline oxygenates ETBE and TAME. Aquat Toxicol. 2012;120–121:45–53.
47. Soares AR et al. Ethanol exposure induces upregulation of specific microRNAs in zebrafish embryos. Toxicol Sci. 2012;127(1):18–28.
48. Mattingly CJ, Hampton TH, Brothers KM, Griffin NE, Planchart A. Perturbation of defense pathways by low-dose arsenic exposure in zebrafish embryos. Environ Health Perspect. 2009;117(6):981–7.
49. Praskova E et al. Acute toxicity of acetylsalicylic acid to juvenile and embryonic stages of Danio rerio. Neuroendocrinol Lett. 2012;33 Suppl 3:72–6.
50. Beker van Woudenberg A et al. A category approach to predicting the developmental (neuro) toxicity of organotin compounds: the value of the zebrafish (Danio rerio) embryotoxicity test (ZET). Reprod Toxicol. 2013;41:35–44.
51. Schock EN et al. The effects of carbaryl on the development of zebrafish (Danio rerio) embryos. Zebrafish. 2012;9(4):169–78.
52. Hofsteen P, Plavicki J, Johnson SD, Peterson RE, Heideman W. Sox9b is required for epicardium formation and plays a role in TCDD-induced heart malformation in zebrafish. Mol Pharmacol. 2013;84(3):353–60.
53. Kim JY, Kim HH, Cho KH. Acute cardiovascular toxicity of sterilizers, PHMG, and PGH: severe inflammation in human cells and heart failure in zebrafish. Cardiovasc Toxicol. 2013;13(2):148–60.
54. Mathew LK, Simonich MT, Tanguay RL. AHR-dependent misregulation of Wnt signaling disrupts tissue regeneration. Biochem Pharmacol. 2009;77(4):498–507.
55. Hofsteen P, Mehta V, Kim MS, Peterson RE, Heideman W. TCDD inhibits heart regeneration in adult zebrafish. Toxicol Sci. 2013;132(1):211–21.
56. Coffin AB et al. Chemical screening for hair cell loss and protection in the zebrafish lateral line. Zebrafish. 2010;7(1):3–11.
57. Yang CT, Johnson SL. Small molecule-induced ablation and subsequent regeneration of larval zebrafish melanocytes. Development. 2006;133(18):3563–73.
58. Legler J et al. Effect-directed analysis of municipal landfill soil reveals novel developmental toxicants in the zebrafish Danio rerio. Environ Sci Technol. 2011;45(19):8552–8.
59. Fako VE, Furgeson DY. Zebrafish as a correlative and predictive model for assessing biomaterial nanotoxicity. Adv Drug Deliv Rev. 2009;61(6):478–86.
60. Chiu LL, Cunningham LL, Raible DW, Rubel EW, Ou HC. Using the zebrafish lateral line to screen for ototoxicity. J Assoc Res Otolaryngol. 2008;9(2):178–90.
61. Selderslaghs IW, Blust R, Witters HE. Feasibility study of the zebrafish assay as an alternative method to screen for developmental toxicity and embryotoxicity using a training set of 27 compounds. Reprod Toxicol. 2012;33(2):142–54.
62. Truong L, Mandrell D, Mandrell R, Simonich M, Tanguay RL. A rapid throughput approach identifies cognitive deficits in adult zebrafish from developmental exposure to polybrominated flame retardants. Neurotoxicology. 2014;43:134–42.
63. Antkiewicz DS, Peterson RE, Heideman W. Blocking expression of AHR2 and ARNT1 in zebrafish larvae protects against cardiac toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Sci. 2006;94(1):175–82.
64. Teraoka H et al. Induction of cytochrome P450 1A is required for circulation failure and edema by 2,3,7,8-tetrachlorodibenzo-p-dioxin in zebrafish. Biochem Biophys Res Commun. 2003;304(2):223–8.
65. Prasch AL et al. Aryl hydrocarbon receptor 2 mediates 2,3,7,8-tetrachlorodibenzo-p-dioxin developmental toxicity in zebrafish. Toxicol Sci. 2003;76(1):138–50.
66. Goodale BC et al. AHR2 mutant reveals functional diversity of aryl hydrocarbon receptors in zebrafish. PLoS One. 2012;7(1):e29346.
67. Staudt D, Stainier D. Uncovering the molecular and cellular mechanisms of heart development using the zebrafish. Annu Rev Genet. 2012;46:397–418.
68. Hassel D et al. Nexilin mutations destabilize cardiac Z-disks and lead to dilated cardiomyopathy. Nat Med. 2009;15(11):1281–8.
69. Smith KA et al. Dominant-negative ALK2 allele associates with congenital heart defects. Circulation. 2009;119(24):3062–9.
70. Sedmera D et al. Functional and morphological evidence for a ventricular conduction system in zebrafish and Xenopus hearts. Am J Physiol Heart Circ Physiol. 2003;284(4):H1152–60.
71. Bakkers J. Zebrafish as a model to study cardiac development and human cardiac disease. Cardiovasc Res. 2011;91(2):279–88.
72. Incardona JP et al. Exxon Valdez to Deepwater Horizon: comparable toxicity of both crude oils to fish early life stages. Aquat Toxicol. 2013;142–143:303–16.
73. Incardona JP, Linbo TL, Scholz NL. Cardiac toxicity of 5-ring polycyclic aromatic hydrocarbons is differentially dependent on the aryl hydrocarbon receptor 2 isoform during zebrafish development. Toxicol Appl Pharmacol. 2011;257(2):242–9.
74. McGee SP, Konstantinov A, Stapleton HM, Volz DC. Aryl phosphate esters within a major PentaBDE replacement product induce cardiotoxicity in developing zebrafish embryos: potential role of the aryl hydrocarbon receptor. Toxicol Sci. 2013;133(1):144–56.
75. Plavicki J, Hofsteen P, Peterson RE, Heideman W. Dioxin inhibits zebrafish epicardium and proepicardium development. Toxicol Sci. 2013;131(2):558–67.
76. Waits ER, Nebert DW. Genetic architecture of susceptibility to PCB126-induced developmental cardiotoxicity in zebrafish. Toxicol Sci. 2011;122(2):466–75.
77. Chen J, Carney SA, Peterson RE, Heideman W. Comparative genomics identifies genes mediating cardiotoxicity in the embryonic zebrafish heart. Physiol Genomics. 2008;33(2):148–58.
78. Chen J. Impaired cardiovascular function caused by different stressors elicits a common pathological and transcriptional response in zebrafish embryos. Zebrafish. 2013;10(3):389–400.
79. Lee SH, Kim HR, Han RX, Oqani RK, Jin DI. Cardiovascular risk assessment of atypical antipsychotic drugs in a zebrafish model. J Appl Toxicol. 2013;33(6):466–70.
80. Cheng H et al. A novel preclinical strategy for identifying cardiotoxic kinase inhibitors and mechanisms of cardiotoxicity. Circ Res. 2011;109(12):1401–9.
81. Zhu JJ et al. Human cardiotoxic drugs delivered by soaking and microinjection induce cardiovascular toxicity in zebrafish. J Appl Toxicol. 2014;34(2):139–48.
82. Lal H, Kolaja KL, Force T. Cancer genetics and the cardiotoxicity of the therapeutics. J Am Coll Cardiol. 2013;61(3):267–74.
83. Choi WY et al. In vivo monitoring of cardiomyocyte proliferation to identify chemical modifiers of heart regeneration. Development. 2013;140(3):660–6.
84. Huang CJ, Tu CT, Hsiao CD, Hsieh FJ, Tsai HJ. Germ-line transmission of a myocardium-specific GFP transgene reveals critical regulatory elements in the cardiac myosin light chain 2 promoter of zebrafish. Dev Dyn. 2003;228(1):30–40.
85. Kikuchi K et al. Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature. 2010;464(7288):601–5.
86. Poon KL, Liebling M, Kondrychyn I, Garcia-Lecea M, Korzh V. Zebrafish cardiac enhancer trap lines: new tools for in vivo studies of cardiovascular development and disease. Dev Dyn. 2010;239(3):914–26.
87. Kikuchi K et al. tcf21+ epicardial cells adopt non-myocardial fates during zebrafish heart development and regeneration. Development. 2011;138(14):2895–902.
88. McGrath P, Li CQ. Zebrafish: a predictive model for assessing drug-induced toxicity. Drug Discov Today. 2008;13(9–10):394–401.
89. Chu J, Sadler KC. New school in liver development: lessons from zebrafish. Hepatology. 2009;50(5):1656–63.
90. Goldstone JV et al. Identification and developmental expression of the full complement of cytochrome P450 genes in Zebrafish. BMC Genomics. 2010;11:643.
91. Kim KH et al. Cyp1a reporter zebrafish reveals target tissues for dioxin. Aquat Toxicol. 2013;134–135:57–65.
92. Mattingly CJ, McLachlan JA, Toscano Jr WA. Green fluorescent protein (GFP) as a marker of aryl hydrocarbon receptor (AhR) function in developing zebrafish (Danio rerio). Environ Health Perspect. 2001;109(8):845–9.
93. Noury P, Geffard O, Tutundjian R, Garric J. Non destructive in vivo measurement of ethoxyresorufin biotransformation by zebrafish prolarva: development and application. Environ Toxicol. 2006;21(4):324–31.
94. Power DM et al. Thyroid hormones in growth and development of fish. Comp Biochem Physiol C Toxicol Pharmacol. 2001;130(4):447–59.
95. Gorelick DA, Watson W, Halpern ME. Androgen receptor gene expression in the developing and adult zebrafish brain. Dev Dyn. 2008;237(10):2987–95.
96. Menuet A et al. Molecular characterization of three estrogen receptor forms in zebrafish: binding characteristics, transactivation properties, and tissue distributions. Biol Reprod. 2002;66(6):1881–92.
97. Levavi-Sivan B, Bogerd J, Mananos EL, Gomez A, Lareyre JJ. Perspectives on fish gonadotropins and their receptors. Gen Comp Endocrinol. 2010;165(3):412–37.
98. von Hofsten J, Olsson PE. Zebrafish sex determination and differentiation: involvement of FTZ-F1 genes. Reprod Biol Endocrinol. 2005;3:63.
99. Leal MC et al. Histological and stereological evaluation of zebrafish (Danio rerio) spermatogenesis with an emphasis on spermatogonial generations. Biol Reprod. 2009;81(1):177–87.
100. Clelland E, Peng C. Endocrine/paracrine control of zebrafish ovarian development. Mol Cell Endocrinol. 2009;312(1–2):42–52.
101. Griffin LB, January KE, Ho KW, Cotter KA, Callard GV. Morpholino-mediated knockdown of ERalpha, ERbetaa, and ERbetab mRNAs in zebrafish (Danio rerio) embryos reveals differential regulation of estrogen-inducible genes. Endocrinology. 2013;154(11):4158–69.
102. Bugel SM, White LA, Cooper KR. Inhibition of vitellogenin gene induction by 2,3,7,8-tetrachlorodibenzo-p-dioxin is mediated by aryl hydrocarbon receptor 2 (AHR2) in zebrafish (Danio rerio). Aquat Toxicol. 2013;126:1–8.
103. Petersen K et al. Transgenic (cyp19a1b-GFP) zebrafish embryos as a tool for assessing combined effects of oestrogenic chemicals. Aquat Toxicol. 2013;138–139:88–97.
104. Murk AJ, Legler J, Denison MS, et al. Chemical-activated luciferase gene expression (CALUX): a novel in vitro bioassay for Ah receptor active compounds in sediments and pore water. Fundam Appl Toxicol. 1996;33(1):149–60.
105. Heiden TK, Carvan 3rd MJ, Hutz RJ. Inhibition of follicular development, vitellogenesis, and serum 17beta-estradiol concentrations in zebrafish following chronic, sublethal dietary exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Sci. 2006;90(2):490–9.
106. King Heiden TC, Spitsbergen J, Heideman W, Peterson RE. Persistent adverse effects on health and reproduction caused by exposure of zebrafish to 2,3,7,8-tetrachlorodibenzo-p-dioxin during early development and gonad differentiation. Toxicol Sci. 2009;109(1):75–87.
107. Baker TR, Peterson RE, Heideman W. Using zebrafish as a model system for studying the transgenerational effects of dioxin. Toxicol Sci. 2014;138(2):403–11. This study demonstrates the utility of zebrafish to advance our understanding of transgenerational (epigenetic) inheritance, including parent-of-origin phenomenology.
108. Weger M et al. Real-time in vivo monitoring of circadian E-box enhancer activity: a robust and sensitive zebrafish reporter line for developmental, chemical and neural biology of the circadian clock. Dev Biol. 2013;380(2):259–73.
109. Suen MF et al. Assessments of the effects of nicotine and ketamine using tyrosine hydroxylase-green fluorescent protein transgenic zebrafish as biosensors. Biosens Bioelectron. 2013;42:177–85.
110. Sun Y, Dong Z, Jin T, et al. Imaging-based chemical screening reveals activity-dependent neural differentiation of pluripotent stem cells. Elife. 2013;2:e00508.
111. Raftery TD, Isales GM, Yozzo KL, Volz DC. High-content screening assay for identification of chemicals impacting spontaneous activity in zebrafish embryos. Environ Sci Technol. 2014;48(1):804–10.
112. Zhang X, Gong Z. Fluorescent transgenic zebrafish Tg(nkx2.2a:mEGFP) provides a highly sensitive monitoring tool for neurotoxins. PLoS One. 2013;8(2):e55474.
113. Kanungo J, Lantz S, Paule MG. In vivo imaging and quantitative analysis of changes in axon length using transgenic zebrafish embryos. Neurotoxicol Teratol. 2011;33(6):618–23.
114. Makhija DT, Jagtap AG. Studies on sensitivity of zebrafish as a model organism for Parkinson’s disease: comparison with rat model. J Pharmacol Pharmacother. 2014;5(1):39–46.
115. Da Costa MM, Allen CE, Higginbottom A, et al. A new zebrafish model produced by TILLING of SOD1-related amyotrophic lateral sclerosis replicates key features of the disease and represents a tool for in vivo therapeutic screening. Dis Model Mech. 2014;7(1):73–81.
116. Armstrong GA, Drapeau P. Loss and gain of FUS function impair neuromuscular synaptic transmission in a genetic model of ALS. Hum Mol Genet. 2013;22(21):4282–92.
117. Ciura S, Lattante S, Le Ber I, et al. Loss of function of C9orf72 causes motor deficits in a zebrafish model of amyotrophic lateral sclerosis. Ann Neurol. 2013;74(2):180–7.
118. Schmid B et al. Loss of ALS-associated TDP-43 in zebrafish causes muscle degeneration, vascular dysfunction, and reduced motor neuron axon outgrowth. Proc Natl Acad Sci U S A. 2013;110(13):4986–91.
119. McGown A et al. Early interneuron dysfunction in ALS: insights from a mutant sod1 zebrafish model. Ann Neurol. 2013;73(2):246–58.
120. Wager K, Russell C. Mitophagy and neurodegeneration: the zebrafish model system. Autophagy. 2013;9(11):1693–709.
121. Irons TD, MacPhail RC, Hunter DL, Padilla S. Acute neuroactive drug exposures alter locomotor activity in larval zebrafish. Neurotoxicol Teratol. 2010;32(1):84–90.
122. Sun EY, Josephson L, Kelly KA, Weissleder R. Development of nanoparticle libraries for biosensing. Bioconjug Chem. 2006;17(1):109–13.
123. Harper SL, Carriere JL, Miller JM, et al. Systematic evaluation of nanomaterial toxicity: utility of standardized materials and rapid assays. ACS Nano. 2011;5(6):4688–97.
124. Tang S et al. Cadmium sulfate and CdTe-quantum dots alter DNA repair in zebrafish (Danio rerio) liver cells. Toxicol Appl Pharmacol. 2013;272(2):443–52.
125. Zhang W et al. Toxicity assessment of zebrafish following exposure to CdTe QDs. J Hazard Mater. 2012;213–214:413–20.
126. Kim KT, Zaikova T, Hutchison JE, Tanguay RL. Gold nanoparticles disrupt zebrafish eye development and pigmentation. Toxicol Sci. 2013;133(2):275–88.
127. Bar-Ilan O, Albrecht RM, Fako VE, Furgeson DY. Toxicity assessments of multisized gold and silver nanoparticles in zebrafish embryos. Small. 2009;5(16):1897–910.
128. Christen V, Capelle M, Fent K. Silver nanoparticles induce endoplasmatic reticulum stress response in zebrafish. Toxicol Appl Pharmacol. 2013;272(2):519–28.
129. Griffitt RJ, Lavelle CM, Kane AS, Denslow ND, Barber DS. Chronic nanoparticulate silver exposure results in tissue accumulation and transcriptomic changes in zebrafish. Aquat Toxicol. 2013;130–131:192–200.
130. Lee KJ et al. In vivo quantitative study of sized-dependent transport and toxicity of single silver nanoparticles using zebrafish embryos. Chem Res Toxicol. 2012;25(5):1029–46.
131. Powers CM, Slotkin TA, Seidler FJ, Badireddy AR, Padilla S. Silver nanoparticles alter zebrafish development and larval behavior: distinct roles for particle size, coating and composition. Neurotoxicol Teratol. 2011;33(6):708–14.
132. Griffitt RJ, Hyndman K, Denslow ND, Barber DS. Comparison of molecular and histological changes in zebrafish gills exposed to metallic nanoparticles. Toxicol Sci. 2009;107(2):404–15.
133. Duan J, Yu Y, Li Y, Yu Y, Sun Z. Cardiovascular toxicity evaluation of silica nanoparticles in endothelial cells and zebrafish model. Biomaterials. 2013;34(23):5853–62.
134. Xiong D, Fang T, Yu L, Sima X, Zhu W. Effects of nano-scale TiO2, ZnO and their bulk counterparts on zebrafish: acute toxicity, oxidative stress and oxidative damage. Sci Total Environ. 2011;409(8):1444–52.
135. Clemente Z, Castro VL, Moura MA, Jonsson CM, Fraceto LF. Toxicity assessment of TiO(2) nanoparticles in zebrafish embryos under different exposure conditions. Aquat Toxicol. 2014;147:129–39.
136. Mandrell D et al. Automated zebrafish chorion removal and single embryo placement: optimizing throughput of zebrafish developmental toxicity screens. J Lab Autom. 2012;17(1):66–74.
137. Peravali R et al. Automated feature detection and imaging for high-resolution screening of zebrafish embryos. Biotechniques. 2011;50(5):319–24.
138. Saydmohammed M, Vollmer LL, Onuoha EO, Vogt A, Tsang M. A high-content screening assay in transgenic zebrafish identifies two novel activators of fgf signaling. Birth Defects Res C Embryo Today. 2011;93(3):281–7.
139. Yozzo KL, Isales GM, Raftery TD, Volz DC. High-content screening assay for identification of chemicals impacting cardiovascular function in zebrafish embryos. Environ Sci Technol. 2013;47(19):11302–10. This manuscript highlights recent advancements in high-content imaging and automated detection of cardiotoxicants in the zebrafish embryo model.
140. Paul SM et al. How to improve R&D productivity: the pharmaceutical industry’s grand challenge. Nat Rev Drug Discov. 2010;9(3):203–14.
141. Zon LI, Peterson RT. In vivo drug discovery in the zebrafish. Nat Rev Drug Discov. 2005;4(1):35–44.
142. North TE et al. Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis. Nature. 2007;447(7147):1007–11.
143. Ball J et al. Fishing for teratogens: a consortium effort for a harmonized zebrafish developmental toxicology assay. Toxicol Sci. 2014;139(1):210–9.