Concentration-response analysis of differential gene expression in the zebrafish embryotoxicity test following flusilazole exposure

Toxicological Sciences

Volumn 127, Issue 1, 2012, Pages 303-312

  Hermsen, Sanne A B ^a,b,c   Pronk, Tessa E ^a,b   van den Brandhof, Evert Jan ^a   van der Ven, Leo T M ^a   Piersma, Aldert H ^a,c  

^a NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Alternative test; Concentration response; Flusilazole; Toxicogenomics; Triazole; Zebrafish embryotoxicity test

Indexed keywords

FLUSILAZOLE; RETINOL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; DRUG EXPOSURE; DRUG MECHANISM; EMBRYO; EMBRYOTOXICITY; FATTY ACID METABOLISM; FERTILIZATION; GENE EXPRESSION; GENE FUNCTION; GENETIC REGULATION; MICROARRAY ANALYSIS; NONHUMAN; PREDICTION; SENSITIVITY ANALYSIS; STEROIDOGENESIS; TRANSCRIPTOMICS; VITAMIN METABOLISM; ZEBRA FISH;

EID: 84860154353     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfs092     Document Type: Article

References (55)

1. Andersen, M. E., Clewell, H. J., Bermudez, E., Willson, G. A., and Thomas, R. S. (2008). Genomic signatures and dose-dependent transitions in nasal epithelial responses to inhaled formaldehyde in the rat. Toxicol. Sci. 105, 368-383.
2. Baird, T. D., and DeLorenzo, M. E. (2010). Descriptive and mechanistic toxicity of conazole fungicides using the model test alga Dunaliella tertiolecta (Chlorophyceae). Environ. Toxicol 25, 213-220.
3. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B (Methodological) 57, 289-300.
4. Brannen, K. C., Panzica-Kelly, J. M., Danberry, T. L., and Augustine-Rauch, K. A. (2010). Development of a zebrafish embryo teratogenicity assay and quantitative prediction model. Birth Defects Res. B Dev. Reprod. Toxicol. 89, 66-77.
5. Cui, X., and Churchill, G. A. (2003). Statistical tests for differential expression in cDNA microarray experiments. Genome Biol. 4, 210.
6. Daston, G. P. (2008). Gene expression, dose-response, and phenotypic anchoring: Applications for toxicogenomics in risk assessment. Toxicol. Sci. 105, 233-234.
7. Daston, G. P., and Naciff, J. M. (2005). Gene expression changes related to growth and differentiation in the fetal and juvenile reproductive system of the female rat: Evaluation of microarray results. Reprod. Toxicol. 19, 381-394.
8. Daston, G. P., and Naciff, J. M. (2010). Predicting developmental toxicity through toxicogenomics. Birth Defects Res. C Embryo Today 90, 110-117.
9. de Jong, E., Barenys, M., Hermsen, S. A. B., Verhoef, A., Ossendorp, B. C., Bessems, J. G. M., and Piersma, A. H. (2011). Comparison of the mouse embryonic stem cell test, the rat whole embryo culture and the zebrafish embryotoxicity test as alternative methods for developmental toxicity testing of six 1,2,4-triazoles. Toxicol. Appl. Pharmacol. 253, 103-111.
10. Dobbs-McAuliffe, B., Zhao, Q., and Linney, E. (2004). Feedback mechanisms regulate retinoic acid production and degradation in the zebrafish embryo. Mech. Dev. 121, 339-350.
11. Embry, M. R., Belanger, S. E., Braunbeck, T. A., Galay-Burgos, M., Halder, M., Hinton, D. E., Léonard, M. A., Lillicrap, A., Norberg-King, T., and Whale, G. (2010). The fish embryo toxicity test as an animal alternative method in hazard and risk assessment and scientific research. Aquat. Toxicol. 97, 79-87.
12. Emoto, Y., Wada, H., Okamoto, H., Kudo, A., and Imai, Y. (2005). Retinoic acid-metabolizing enzyme Cyp26a1 is essential for determining territories of hindbrain and spinal cord in zebrafish. Dev. Biol. 278, 415-427.
13. European Union (EU). (2010). Directive 2010/63/EU of the European parliament and of the council of 22 September 2010 on the protection of animals used for scientific purposes. Off. J. EU L276, 33-79.
14. Farag, A. T., and Ibrahim, H. H. (2007). Developmental toxic effects of antifungal flusilazole administered by gavage to mice. Birth Defects Res. B Dev. Reprod. Toxicol. 80, 12-17.
15. Feng, L., Hernandez, R. E., Waxman, J. S., Yelon, D., and Moens, C. B. (2010). Dhrs3a regulates retinoic acid biosynthesis through a feedback inhibition mechanism. Dev. Biol. 338, 1-14.
16. Fleming, A. (2007). Zebrafish as an alternative model organism for disease modelling and drug discovery: Implications for the 3Rs. NC3Rs 10, 1-7.
17. Genschow, E., Spielmann, H., Scholz, G., Pohl, I., Seiler, A., Clemann, N., Bremer, S., and Becker, K. (2004). Validation of the embryonic stem cell test in the international ECVAM validation study on three in vitro embryotoxicity tests. Altern. Lab. Anim. 32, 209-244.
18. Goetz, A. K., and Dix, D. J. (2009a). Mode of action for reproductive and hepatic toxicity inferred from a genomic study of triazole antifungals. Toxicol. Sci. 110, 449-462.
19. Goetz, A. K., and Dix, D. J. (2009b). Toxicogenomic effects common to triazole antifungals and conserved between rats and humans. Toxicol. Appl. Pharmacol. 238, 80-89.
20. Goetz, A. K., Rockett, J. C., Ren, H., Thillainadarajah, I., and Dix, D. J. (2009). Inhibition of rat and human steroidogenesis by triazole antifungals. Syst. Biol. Reprod. Med. 55, 214-226.
21. Hermsen, S. A. B., Pronk, T. E., van den Brandhof, E. J., van der Ven, L. T., and Piersma, A. H. (2011a). Chemical class-specific gene expression changes in the zebrafish embryo after exposure to glycol ether alkoxy acids and 1,2,4-triazole antifungals. Reprod. Toxicol. 32, 245-252.
22. Hermsen, S. A. B., van den Brandhof, E.-J., van der Ven, L. T. M., and Piersma, A. H. (2011b). Relative embryotoxicity of two classes of chemicals in a modified zebrafish embryotoxicity test and comparison with their in vivo potencies. Toxicol. In Vitro 25, 745-753.
23. Hester, S. D., Wolf, D. C., Nesnow, S., and Thai, S.-F. (2006). Transcriptional profiles in liver from rats treated with tumorigenic and non-tumorigenic triazole conazole fungicides: Propiconazole, triadimefon, and myclobutanil. Toxicol. Pathol. 34, 879-894.
24. Hill, A. J., Teraoka, H., Heideman, W., and Peterson, R. E. (2005). Zebrafish as a model vertebrate for investigating chemical toxicity. Toxicol. Sci. 86, 6-19.
25. Huang, D. W., Sherman, B. T., and Lempicki, R. A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57.
26. Janssen, R., Pennings, J., Hodemaekers, H., Buisman, A., van Oosten, M., de Rond, L., Ozturk, K., Dormans, J., Kimman, T., and Hoebee, B. (2007). Host transcription profiles upon primary respiratory syncytial virus infection. J. Virol. 81, 5958-5967.
27. Kerr, M. K., Martin, M., and Churchill, G. A. (2000). Analysis of variance for gene expression microarray data. J. Comput. Biol. 7, 819-837.
28. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
29. Liden, M., and Eriksson, U. (2006). Understanding retinol metabolism: Structure and function of retinol dehydrogenases. J. Biol. Chem. 281, 13001-13004.
30. Marotta, F., and Tiboni, G. M. (2010). Molecular aspects of azoles-induced teratogenesis. Expert Opin. Drug Metab. Toxicol. 6, 461-482.
31. McGrath, P., and Li, C.-Q. (2008). Zebrafish: A predictive model for assessing drug-induced toxicity. Drug Discov. Today 13, 394-401.
32. Menegola, E., Broccia, M. L., Di Renzo, F., and Giavini, E. (2001). Antifungal triazoles induce malformations in vitro. Reprod. Toxicol. 15, 421-427.
33. Menegola, E., Broccia, M. L., Di Renzo, F., and Giavini, E. (2006). Postulated pathogenic pathway in triazole fungicide induced dysmorphogenic effects. Reprod. Toxicol. 22, 186-195.
34. Naciff, J. M., Hess, K. A., Overmann, G. J., Torontali, S. M., Carr, G. J., Tiesman, J. P., Foertsch, L. M., Richardson, B. D., Martinez, J. E., and Daston, G. P. (2005). Gene expression changes induced in the testis by transplacental exposure to high and low doses of 17{alpha}-ethynyl estradiol, genistein, or bisphenol A. Toxicol. Sci. 86, 396-416.
35. Nagel, R. (2002). DarT: The embryo test with the Zebrafish Danio rerio- a general model in ecotoxicology and toxicology. Altex 19(Suppl. 1), 38-48.
36. Niederreither, K., McCaffery, P., Dräger, U. C., Chambon, P., and Dollé, P. (1997). Restricted expression and retinoic acid-induced downregulation of the retinaldehyde dehydrogenase type 2 (RALDH-2) gene during mouse development. Mech. Dev. 62, 67-78.
37. O'Byrne, S. M., Wongsiriroj, N., Libien, J., Vogel, S., Goldberg, I. J., Baehr, W., Palczewski, K., and Blaner, W. S. (2005). Retinoid absorption and storage is impaired in mice lacking lecithin:retinol acyltransferase (LRAT). J. Biol. Chem. 280, 35647-35657.
38. Papis, E., Bernardini, G., Gornati, R., Menegola, E., and Prati, M. (2007). Gene expression in Xenopus laevis embryos after Triadimefon exposure. Gene Expr. Patterns 7, 137-142.
39. Pearson, K. (1901). On lines and planes of closest fit to systems of points in space. Philos. Mag. 2, 559-572.
40. Piersma, A. H., Genschow, E., Verhoef, A., Spanjersberg, M. Q., Brown, N. A., Brady, M., Burns, A., Clemann, N., Seiler, A., and Spielmann, H. (2004). Validation of the postimplantation rat whole-embryo culture test in the international ECVAM validation study on three in vitro embryotoxicity tests. Altern. Lab. Anim. 32, 275-307.
41. Piersma, A. H., Hernandez, L. G., van Benthem, J., Muller, J. J., van Leeuwen, F. X., Vermeire, T. G., and van Raaij, M. T. (2011). Reproductive toxicants have a threshold of adversity. Crit. Rev. Toxicol. 41, 545-554.
42. Robinson, J. F., Guerrette, Z., Yu, X., Hong, S., and Faustman, E. M. (2010). A systems-based approach to investigate dose- and time-dependent methylmercury-induced gene expression response in C57BL/6 mouse embryos undergoing neurulation. Birth Defects Res. B Dev. Reprod. Toxicol. 89, 188-200.
43. Schilling, T. F., and Knight, R. D. (2001). Origins of anteroposterior patterning and Hox gene regulation during chordate evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356, 1599-1613.
44. Selderslaghs, I. W., Blust, R., and Witters, H. E. (2011). 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. doi:10.1016/j.reprotox.2011.08.003.
45. Slob, W. (2002). Dose-response modeling of continuous endpoints. Toxicol. Sci. 66, 298-312.
46. Spielmann, H., Seiler, A., Bremer, S., Hareng, L., Hartung, T., Ahr, H., Faustman, E., Haas, U., Moffat, G. J., Nau, H., et al. (2006). The practical application of three validated in vitro embryotoxicity tests. The report and recommendations of an ECVAM/ZEBET workshop (ECVAM workshop 57). Altern. Lab. Anim. 34, 527-538.
47. Strahle, U., Scholz, S., Geisler, R., Greiner, P., Hollert, H., Rastegar, S., Schumacher, A., Selderslaghs, I., Weiss, C., Witters, H., et al. (2011). Zebrafish embryos as an alternative to animal experiments-A commentary on the definition of the onset of protected life stages in animal welfare regulations. Reprod. Toxicol. doi:10.1016/j.reprotox.2011.06.121.
48. Tiboni, G. M., Marotta, F., and Carletti, E. (2009). Fluconazole alters CYP26 gene expression in mouse embryos. Reprod. Toxicol. 27, 199-202.
49. Trzaskos, J. M., and Henry, M. J. (1989). Comparative effects of the azolebased fungicide flusilazole on yeast and mammalian lanosterol 14 alphamethyl demethylase. Antimicrob. Agents Chemother. 33, 1228-1231.
50. Tully, D. B., Bao, W., Goetz, A. K., Blystone, C. R., Ren, H., Schmid, J. E., Strader, L. F., Wood, C. R., Best, D. S., Narotsky, M. G., et al. (2006). Gene expression profiling in liver and testis of rats to characterize the toxicity of triazole fungicides. Toxicol. Appl. Pharmacol. 215, 260-273.
51. van Dartel, D. A. M., Pennings, J. L. A., de la Fonteyne, L. J. J., Brauers, K. J. J., Claessen, S., van Delft, J. H., Kleinjans, J. C. S., and Piersma, A. H. (2011). Concentration-dependent gene expression responses to flusilazole in embryonic stem cell differentiation cultures. Toxicol. Appl. Pharmacol. 251, 110-118.
52. Wolfinger, R. D., Gibson, G., Wolfinger, E. D., Bennett, L., Hamadeh, H., Bushel, P., Afshari, C., and Paules, R. S. (2001). Assessing gene significance from cDNA microarray expression data via mixed models. J. Comput. Biol. 8, 625-637.
53. Wu, H., Kerr, M. K., Cui, X., and Churchill, G. A. (2003). MAANOVA: A software package for the analysis of spotted cDNA microarray experiments. In The Analyses of Gene Expression Data (G. Parmigiani, E. Garrett, R. Irizarry, and S. Zeger, Eds.), pp. 313, pp. 313-341. Springer, London, U.K.
54. Yang, L., Ho, N. Y., Alshut, R., Legradi, J., Weiss, C., Reischl, M., Mikut, R., Liebel, U., Müller, F., and Strähle, U. (2009). Zebrafish embryos as models for embryotoxic and teratological effects of chemicals. Reprod. Toxicol. 28, 245-253.
55. Yang, L., Kemadjou, J. R., Zinsmeister, C., Bauer, M., Legradi, J., Muller, F., Pankratz, M., Jakel, J., and Strahle, U. (2007). Transcriptional profiling reveals barcode-like toxicogenomic responses in the zebrafish embryo. Genome Biol. 8, R227.