Transcriptomic concentration-response evaluation of valproic acid, cyproconazole, and hexaconazole in the neural Embryonic Stem Cell Test (ESTn)

Toxicological Sciences

Volumn 125, Issue 2, 2012, Pages 430-438

  Theunissen, Peter T ^a,b   Robinson, Joshua F ^a,b   Pennings, Jeroen L A ^a,b   De jong, Esther ^a,c   Claessen, Sandra M H ^b   Kleinjans, Jos C S ^b   Piersma, Aldert H ^a,b,c  

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

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Alternative test method; Embryonic stem cells; Neural differentiation; Neural embryonic stem cell test (ESTn); Toxicogenomics

Indexed keywords

CYPROCONAZOLE; FUNGICIDE; HEXACONAZOLE; STEROL; TRIAZOLE DERIVATIVE; UNCLASSIFIED DRUG; VALPROIC ACID;

ANIMAL CELL; ARTICLE; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG RESPONSE; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; GENE EXPRESSION PROFILING; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEURAL STEM CELL; NONHUMAN; TRANSCRIPTOMICS;

ANIMALIA; MURINAE;

EID: 84856078215     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr293     Document Type: Article

References (47)

1. Barrier, M., Jeffay, S., Nichols, H. P., Chandler, K. J., Hoopes, M. R., Slentz-Kesler, K., and Hunter, E. S., III (2011). Mouse embryonic stem cell adherent cell differentiation and cytotoxicity (ACDC) assay. Reprod. Toxicol. 31, 383-391.
2. Barrow, P. C. (2009). Reproductive toxicity testing for pharmaceuticals under ICH. Reprod. Toxicol. 28, 172-179.
3. Bendall, A. J., and Abate-Shen, C. (2000). Roles for Msx and Dlx homeoproteins in vertebrate development. Gene 247, 17-31.
4. Bolanos, J. P., Medina, J. M., and Williamson, D. H. (1990). Inhibition of sterol but not fatty acid synthesis by valproate in developing rat brain in vivo. Biochem J. 272, 251-253.
5. Bolstad, B. M., Irizarry, R. A., Astrand, M., and Speed, T. P. (2003). A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19, 185-193.
6. Brion, L., Gorostizaga, A., Gómez, N. V., Podestá, E. J., Cornejo Maciel, F., and Paz, C. (2011). Valproic acid alters mitochondrial cholesterol transport in Y1 adrenocortical cells. Toxicol. In Vitro 25, 7-12.
7. Callaerts, P., Halder, G., and Gehring, W. J. (1997). PAX-6 in development and evolution. Annu. Rev. Neurosci. 20, 483-532.
8. Dahlquist, K. D., Salomonis, N., Vranizan, K., Lawlor, S. C., and Conklin, B. R. (2002). GenMAPP, a new tool for viewing and analyzing microarray data on biological pathways. Nat. Genet. 31, 19-20.
9. Dai, M., Wang, P., Boyd, A. D., Kostov, G., Athey, B., Jones, E. G., Bunney, W. E., Myers, R. M., Speed, T. P., Akil, H., et al. (2005). Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res. 33, e175.
10. de Jong, E., Barenys, M., Hermsen, S. A., Verhoef, A., Ossendorp, B. C., Bessems, J. G., 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.
11. de Leeuw, W. C., Rauwerda, H., Jonker,M. J., and Breit, T.M. (2008). Salvaging Affymetrix probes after probe-level re-annotation. BMC Res. Notes 1, 66.
12. Duester, G. (2008). Retinoic acid synthesis and signaling during early organogenesis. Cell 134, 921-931.
13. Duncan, S. (2007). Teratogenesis of sodium valproate. Curr. Opin. Neurol. 20, 175-180.
14. Farah, C. A., and Leclerc, N. (2008). HMWMAP2: New perspectives on a pathway to dendritic identity. Cell Motil. Cytoskeleton 65, 515-527.
15. 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.
16. Ghannoum, M. A., and Rice, L. B. (1999). Antifungal agents: Mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin. Microbiol. Rev. 12, 501-517.
17. Glaser, K. B., Staver, M. J., Waring, J. F., Stender, J., Ulrich, R. G., and Davidsen, S. K. (2003). Gene expression profiling of multiple histone deacetylase (HDAC) inhibitors: Defining a common gene set produced by HDAC inhibition in T24 and MDA carcinoma cell lines. Mol. Cancer Ther. 2, 151-163.
18. Göttlicher, M., Minucci, S., Zhu, P., Krämer, O. H., Schimpf, A., Giavara, S., Sleeman, J. P., Lo Coco, F., Nervi, C., Pelicci, P. G., et al. (2001). Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J. 20, 6969-6978.
19. Gustavsen, M. W., von Krogh, K., Taubøll, E., Zimmer, K. E., Dahl, E., Olsaker, I., Ropstad, E., and Verhaegen, S. (2009). Differential effects of antiepileptic drugs on steroidogenesis in a human in vitro cell model. Acta Neurol. Scand. Suppl. 189, 14-21.
20. Herrmann, B. G., Labeit, S., Poustka, A., King, T. R., and Lehrach, H. (1990). Cloning of the T gene required in mesoderm formation in the mouse. Nature 343, 617-622.
21. Huang, D. W., Sherman, B. T., Tan, Q., Collins, J. R., Alvord, W. G., Roayaei, J., Stephens, R., Baseler, M. W., Lane, H. C., and Lempicki, R. A. (2007). The DAVID gene functional classification tool: A novel biological module-centric algorithm to functionally analyze large gene lists. Genome Biol. 8, R183.
22. Irizarry, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U., and Speed, T. P. (2003). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264.
23. Jergil, M., Kultima, K., Gustafson, A. L., Dencker, L., and Stigson, M. (2009). Valproic acid-induced deregulation in vitro of genes associated in vivo with neural tube defects. Toxicol. Sci. 108, 132-148.
24. Machera, K. (1995). Developmental toxicity of cyproconazole, an inhibitor of fungal ergosterol biosynthesis, in the rat. Bull. Environ. Contam. Toxicol. 54, 363-369.
25. Marx-Stoelting, P., Adriaens, E., Ahr, H. J., Bremer, S., Garthoff, B., Gelbke, H. P., Piersma, A., Pellizzer, C., Reuter, U., Rogiers, V., et al. (2009). A review of the implementation of the embryonic stem cell test (EST). The report and recommendations of an ECVAM/ReProTect Workshop. Altern. Lab. Anim. 37, 313-328.
26. Meador, K., Reynolds, M. W., Crean, S., Fahrbach, K., and Probst, C. (2008). Pregnancy outcomes in women with epilepsy: A systematic review and metaanalysis of published pregnancy registries and cohorts. Epilepsy Res. 81, 1-13.
27. Mehnert, J. M., and Kelly, W. K. (2007). Histone deacetylase inhibitors: Biology and mechanism of action. Cancer J. 13, 23-29.
28. Meno, C., Saijoh, Y., Fujii, H., Ikeda, M., Yokoyama, T., Yokoyama, M., Toyoda, Y., and Hamada, H. (1996). Left-right asymmetric expression of the TGF beta-family member lefty in mouse embryos. Nature 381, 151-155.
29. Oliveros, J. C. (2007). VENNY. An Interactive Tool for Comparing Lists with Venn Diagrams. Available at: http://bioinfogp.cnb.csic.es/tools/venny/index.html. Accessed September 20, 2011.
30. Paquette, J. A., Kumpf, S. W., Streck, R. D., Thomson, J. J., Chapin, R. E., and Stedman, D. B. (2008). Assessment of the embryonic stem cell test and application and use in the pharmaceutical industry. Birth Defects Res. B Dev. Reprod. Toxicol. 83, 104-111.
31. Pennings, J. L., van Dartel, D. A., Robinson, J. F., Pronk, T. E., and Piersma, A. H. (2011). Gene set assembly for quantitative prediction of developmental toxicity in the embryonic stem cell test. Toxicology 284, 63-71.
32. Phiel, C. J., Zhang, F., Huang, E. Y., Guenther, M. G., Lazar, M. A., and Klein, P. S. (2001). Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J. Biol. Chem. 276, 36734-36741.
33. Scholz, G., Genschow, E., Pohl, I., Bremer, S., Paparella, M., Raabe, H., Southee, J., and Spielmann, H. (1999). Prevalidation of the embryonic stem cell test (EST)-A new in vitro embryotoxicity test. Toxicol. In Vitro 13, 675-681.
34. Seiler, A., Visan, A., Buesen, R., Genschow, E., and Spielmann, H. (2004). Improvement of an in vitro stem cell assay for developmental toxicity: The use of molecular endpoints in the embryonic stem cell test. Reprod. Toxicol. 18, 231-240.
35. 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.
36. Stavridis, M. P., Collins, B. J., and Storey, K. G. (2010). Retinoic acid orchestrates fibroblast growth factor signalling to drive embryonic stem cell differentiation. Development 137, 881-890.
37. Theunissen, P. T., Pennings, J. L., Robinson, J. F., Claessen, S. M., Kleinjans, J. C., and Piersma, A. H. (2011). Time-response evaluation by transcriptomics of methylmercury effects on neural differentiation of murine embryonic stem cells. Toxicol. Sci. 122, 437-447.
38. Theunissen, P. T., Schulpen, S. H., van Dartel, D. A., Hermsen, S. A., van Schooten, F. J., and Piersma, A. H. (2010). An abbreviated protocol for multilineage neural differentiation of murine embryonic stem cells and its perturbation by methyl mercury. Reprod. Toxicol. 29, 383-392.
39. Uibel, F., Muhleisen, A., Kohle, C., Weimer, M., Stummann, T. C., Bremer, S., and Schwarz, M. (2010). ReProGlo: A new stem cell-based reporter assay aimed to predict embryotoxic potential of drugs and chemicals. Reprod. Toxicol. 30, 103-112.
40. van Dartel, D. A., Pennings, J. L., de la Fonteyne, L. J., Brauers, K. J., Claessen, S., van Delft, J. H., Kleinjans, J. C., and Piersma, A. H. (2011a). Concentration-dependent gene expression responses to flusilazole in embryonic stem cell differentiation cultures. Toxicol. Appl. Pharmacol. 251, 110-118.
41. van Dartel, D. A., Pennings, J. L., de la Fonteyne, L. J., Brauers, K. J., Claessen, S., van Delft, J. H., Kleinjans, J. C., and Piersma, A. H. (2011b). Evaluation of developmental toxicant identification using gene expression profiling in embryonic stem cell differentiation cultures. Toxicol. Sci. 119, 126-134.
42. van Dartel, D. A., Pennings, J. L., de la Fonteyne, L. J., van Herwijnen, M. H., van Delft, J. H., van Schooten, F. J., and Piersma, A. H. (2010a). Monitoring developmental toxicity in the embryonic stem cell test using differential gene expression of differentiation-related genes. Toxicol. Sci. 116, 130-139.
43. van Dartel, D. A., Pennings, J. L., Hendriksen, P. J., van Schooten, F. J., and Piersma, A. H. (2009). Early gene expression changes during embryonic stem cell differentiation into cardiomyocytes and their modulation by monobutyl phthalate. Reprod. Toxicol. 27, 93-102.
44. van Dartel, D. A., Pennings, J. L., van Schooten, F. J., and Piersma, A. H. (2010b). Transcriptomics-based identification of developmental toxicants through their interference with cardiomyocyte differentiation of embryonic stem cells. Toxicol. Appl. Pharmacol. 243, 420-428.
45. van der Jagt, K., Tørsløv, J., and de Bruijn, J. (2004). In Alternative Approaches Can Reduce the Use of Test Animals Under REACH. European Commission Report 2004, EUR 21 405 EN.
46. Yashiro, K., Zhao, X., Uehara, M., Yamashita, K., Nishijima, M., Nishino, J., Saijoh, Y., Sakai, Y., and Hamada, H. (2004). Regulation of retinoic acid distribution is required for proximodistal patterning and outgrowth of the developing mouse limb. Dev. Cell 6, 411-422.
47. Yu, X., Griffith, W. C., Hanspers, K., Dillman, J. F., III, Ong, H., Vredevoogd, M. A., and Faustman, E. M. (2006). A system-based approach to interpret dose- and time-dependent microarray data: Quantitative integration of gene ontology analysis for risk assessment. Toxicol. Sci. 92, 560-577.