Effects of exposure to 17α-ethynylestradiol during sexual differentiation on the transcriptome of the African clawed frog (Xenopus laevis)

Environmental Science and Technology

Volumn 47, Issue 9, 2013, Pages 4822-4828

  Tompsett, Amber R ^a   Wiseman, Steve ^a   Higley, Eric ^a   Giesy, John P ^a,b   Hecker, Markus ^a,c  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b CITY UNIVERSITY OF HONG KONG   (Hong Kong)

^c University of Saskatchewan   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AFRICAN CLAWED FROG; BIOLOGICAL EFFECTS; EXPRESSION ANALYSIS; MOLECULAR CHANGES; QUANTITATIVE POLYMERASE CHAIN REACTION; SEXUAL DIFFERENTIATIONS; SMALL SAMPLE SIZE; STEROID BIOSYNTHESIS;

BIOCHEMISTRY; HORMONES; RNA;

POLYMERASE CHAIN REACTION;

ETHINYLESTRADIOL; THYROID HORMONE; TRANSCRIPTOME;

ESTROGENIC COMPOUND; FROG; GENE EXPRESSION; HORMONE; PHENOTYPE; POLLUTION EFFECT; POLLUTION EXPOSURE; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; SIGNALING;

ANIMAL EXPERIMENT; ARTICLE; GENE EXPRESSION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; QUANTITATIVE ANALYSIS; SEX DIFFERENTIATION; SIGNAL TRANSDUCTION; SPERMATOGENESIS; TADPOLE; TESTIS DEVELOPMENT; XENOPUS LAEVIS;

ANIMALS; ENVIRONMENTAL EXPOSURE; ETHINYL ESTRADIOL; SEX DIFFERENTIATION; TRANSCRIPTOME; WATER POLLUTANTS, CHEMICAL; XENOPUS LAEVIS;

AFRICA;

EID: 84877625008     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es400436y     Document Type: Article

References (51)

1. Chang, C.; Witschi, E. Breeding of sex-reversed males of Xenopus laevis Daudin Proc. Soc. Exp. Biol. Med. 1955, 89, 150-152
2. Witschi, E.; Foote, C.; Chang, C. Modification of sex differentiation by steroid hormones in a tree frog (Pseudacris nigrita triseriata Wied) Proc. Soc. Exp. Biol. Med. 1958, 97, 196-197
3. Villalpando, I.; Merchant-Larios, H. Determination of the sensitive stages for gonadal sex-reversal in Xenopus laevis tadpoles Int. J. Dev. Biol. 1990, 34, 281-285
4. Bogi, C.; Schwaiger, J.; Ferling, H.; Mallow, U.; Steineck, C.; Sinowatz, F.; Kalbfus, W.; Negele, R.; Lutz, I.; Kloas, W. Endocrine effects of environmental pollution on Xenopus laevis and Rana temporaria Environ. Res. 2003, 93, 195-201
5. Pettersson, I.; Arukwe, A.; Lundstedt-Enkel, K.; Mortensen, A.; Berg, C. Persistant sex-reversal and oviducal agenesis in adult Xenopus (Silurana) tropicalis frogs following larval exposure to the environmental pollutant ethinylestradiol Aquat. Toxicol. 2006, 79, 356-365
6. Gyllenhammar, I.; Holm, L.; Eklund, R.; Berg, C. Reproductive toxicity in Xenopus tropicalis after developmental exposure to environmental concentrations of ethynylestradiol Aquat. Toxicol. 2008, 91, 171-178
7. Hu, F.; Smith, E.; Carr, J. Effects of larval exposure to estradiol on spermatogenesis and in vitro gonadal steroid secretion in African clawed frogs, Xenopus laevis Gen. Comp. Endrocrinol. 2008, 155, 190-200
8. Ankley, G.; Brooks, B.; Huggett, D.; Sumpter, J. Repeating history: pharmaceuticals in the environment Environ. Sci. Technol. 2007, 41, 8211-8217
9. Hanselman, T.; Graetz, D.; Wilkie, A. Manure-borne estrogens as potential environmental contaminants: a review Environ. Sci. Technol. 2003, 37, 5471-5478
10. Lutz, I.; Kloas, W.; Springer, T.; Holden, L.; Wolf, J.; Krueger, H.; Hosmer, A. Development, standardization, and refinement of procedures for evaluating effects of endocrine active compounds on development and sexual differentiation of Xenopus laevis Anal. Bioanal. Chem. 2008, 390, 2031-2048
11. Tompsett, A.; Wiseman, S.; Higley, E.; Pryce, S.; Chang, H.; Giesy, J.; Hecker, M. Effects of 17α-ethynylestradiol on sexual differentiation and development of the African clawed frog (Xenopus laevis) Comp. Biochem. Physiol., Part C: Toxicol. Pharmacol. 2012, 156, 202-210
12. Yoshimoto, S.; Okada, E.; Umemoto, H.; Tamura, K.; Uno, Y.; Nishida-Umehara, C.; Matsuda, Y.; Takamatsu, N.; Shiba, T.; Ito, M. A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis Proc. Natl. Acad. Sci. 2008, 105, 2469-2474
13. Garcia-Reyero, N.; Perkins, E. Systems biology: leading the revolution in ecotoxicology Environ. Toxicol. Chem. 2011, 30, 265-273
14. Ankley, G.; Bencic, D.; Breen, M.; Collette, T.; Conolly, R.; Denslow, N.; Edwards, S.; Ekman, D.; Garcia-Reyero, N.; Jensen, K.; Lazorchak, J.; Martinovic, D.; Miller, D.; Perkins, E.; Orlando, E.; Villeneuve, D.; Wang, R.; Watanabe, K. Endocrine disrupting chemicals in fish: developing exposure indicators and predictive models of effects based on mechanism of action Aquat. Toxicol. 2009, 92, 168-178
15. Ankley, G.; Bennett, R.; Erickson, R.; Hoff, D.; Hornung, M.; Johnson, R.; Mount, D.; Nichols, J.; Russom, C.; Schmieder, P.; Serrano, J.; Tietge, J.; Villeneuve, D. Adverse outcome pathways: a conceptual framework to support ecotoxicology research and risk assessment Environ. Toxicol. Chem. 2010, 29, 730-741
16. Chang, H.; Wan, Y.; Naile, J.; Zhang, X.; Wiseman, S.; Hecker, M.; Lam, M.; Giesy, J.; Jones, P. Simultaneous quantification of multiple classes of phenolic compounds in blood plasma by liquid chromatography-electrospray tandem mass spectrometry J. Chromatogr., A 2010, 1217, 506-513
17. Tompsett, A.; Wiseman, S.; Higley, E.; Giesy, J.; Hecker, M. Effects of exposure to 17α-ethynylestradiol during larval development on growth, sexual differentiation, and abundances of transcripts in the liver of the wood frog (Lithobates sylvaticus) Aquat. Toxicol. 2013, 126, 42-51
18. Mortazavi, A.; Williams, B.; McCue, K.; Schaeffer, L.; Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq Nat. Methods 2008, 5, 621-628
19. Brooks, M.; Rajasimha, H.; Roger, J.; Swaroop, A. Next-generation sequencing facilitates quantitative analysis of wild-type and Nrl-/- retinal transcriptomes Mol. Vision 2011, 17, 3034-3054
20. Jung, K.; Friede, T.; Beissbarth, T. Reporting FDR analogous confidence intervals for the log fold change of differentially expressed genes BMC Bioinf. 2011, 12, 288-296
21. Glaus, P.; Honkela, A.; Rattray, M. Identifying differentially expressed transcripts from RNA-seq data with biological variation Bioinformatics 2012, 28, 1721-1728
22. Cosena, A.; Gotz, S.; Garca-Gomez, J.; Terol, J.; Talon, M.; Robles, M. Blast2go: a universal tool for annotation, visualization and analysis in functional genomics research Bioinformatics 2005, 21, 3674-3676
23. Gotz, S.; Garcia-Gomez, J.; Terol, J.; Williams, T.; Nagarai, S.; Nueda, M.; Robles, M.; Talon, M.; Dopazo, J.; Conesa, A. High-throughput functional annotation and data mining with the blast2go suite Nucleic Acids Res. 2008, 36, 3420-3435
24. Simon, P. Q-Gene: processing quantitative real-time RT-PCR data Bioinformatics 2003, 19, 1439-1440
25. Nieuwkoop, P.; Faber, J. Normal table of Xenopus laevis (Daudin): A systematical and chronological survey of the development from the fertilized egg till the end of metamorphosis; 2nd ed.; Garland Publishing, Inc.: New York and London, 1994.
26. Wolf, J.; Lutz, I.; Kloas, W.; Springer, T.; Holden, L.; Krueger, H.; Hosmer, A. Effects of 17β-estradiol exposure on Xenopus laevis gonadal histopathology Environ. Toxicol. Chem. 2010, 29, 1091-1105
27. Higashi, E.; Fukami, T.; Itoh, M.; Kyo, S.; Inoue, M.; Yokoi, T.; Nakajima, M. Human CYP2A6 is induced by estrogen via estrogen receptor Drug Metab. Dispos. 2007, 35, 1935-1941
28. Seo, Y.; Sanyal, S.; Kim, H.; Won, D.; An, J.; Amano, T.; Zavacki, A.; Kwon, H.; Shi, Y.; Kim, W.; Kang, H.; Moore, D.; Choi, H. FOR, a novel orphan nuclear receptor related to Farnesoid X Receptor J. Biol. Chem. 2002, 277, 17836-17844
29. Nguyen, P.; Lee, R.; Conley, A.; Sneyd, J.; Soboleva, T. Variation in 3-beta-hydroxysteroid dehydrogenase activity and in pregnenolone supply rate can paradoxically alter androstenedione synthesis J. Steroid Biochem. Mol. Biol. 2012, 128, 12-20
30. Filby, A.; Thorpe, K.; Maack, G.; Tyler, C. Gene expression profiles revealing the mechanisms of anti-androgen- and estrogen-induced feminization in fish Aquat. Toxicol. 2007, 81, 219-231
31. Tompsett, A. Effects of exposure to 17α-ethynylestradiol during larval development on the African clawed frog (Xenopus laevis) and the wood frog (Rana sylvatica). Ph.D. Dissertation, University of Saskatchewan, Saskatoon, SK, 2012.
32. Asahi, H.; Takase, M.; Yuge, M.; Matsui, K.; Mori, M.; Fujita, T.; Nakamura, M. Expression of FTZ-F1 alpha in transgenic Xenopus embryos and oocytes Dev., Growth Differ. 2002, 44, 509-516
33. Takase, M.; Nakajima, T.; Nakamura, M. FTZ-F1 alpha is expressed in the developing gonad of frogs Biochim. Biophys. Acta 2000, 1494, 195-200
34. Duarte-Guterman, P.; Langlois, V.; Hodgkinson, K.; Pauli, B.; Cooke, G.; Wade, M.; Trudeau, V. The aromatase inhibitor fadrozole and the 5-reductase inhibitor finasteride affect gonadal differentiation and gene expression in the frog Silurana tropicalis Sex. Dev. 2010, 3, 333-341
35. Lee, S.; Privalsky, M. Heterodimers of retinoic acid receptors and thyroid hormone receptors display unique combinatorial regulatory properties Mol. Endocrinol. 2005, 19, 863-878
36. Umesono, K.; Giguere, V.; Glass, C.; Rosenfeld, M.; Evans, R. Retinoic acid and thyroid hormone induce gene expression through a common responsive element Nature 1988, 336, 262-265
37. Shi, Y.-B. Amphibian Metamorphosis: From Morphology to Molecular Biology; Wiley-Liss, Inc.: New York, NY, 2000.
38. Das, B.; Matsuda, H.; Fujimoto, K.; Sun, G.; Matsuura, K.; Shi, Y.-B. Molecular and genetic studies suggest that thyroid hormone receptor is both necessary and sufficient to mediate the developmental effects of thyroid hormone Gen. Comp. Endrocrinol. 2010, 168, 174-180
39. Degitz, S.; Holcombe, G.; Flynn, K.; Kosian, P.; Korte, J.; Tietge, J. Progress towards development of an amphibian-based thyroid screening assay using Xenopus laevis. Organismal and thryroidal responses to the model compounds 6-propylthiouracil, methimazole, and thyroxine Toxicol. Sci. 2005, 87, 353-364
40. Goleman, W.; Carr, J.; Anderson, T. Environmentally relevant concentrations of ammonium perchlorate inhibit thyroid function and alter sex ratios in developing Xenopus laevis Environ. Toxicol. Chem. 2002, 21, 590-597
41. Smith, D.; Penning, T.; Ansari, A.; Munday, K.; Akhtar, M. Oestrogen-induced cholesterol and fatty acid biosynthesis in Xenopus laevis liver during vitellogenic response Biochem. J. 1978, 174, 353-361
42. Sharpe, R.; MacLatchy, D. Lipid dynamics in goldfish (Carassius auratus) during a period of gonadal recrudescence: effects of beta-sitosterol and 17 beta-estradiol exposure Comp. Biochem. Physiol., Part C: Toxicol. Pharmacol. 2007, 145, 507-517
43. Ekman, D.; Teng, Q.; Villeneuve, D.; Kahl, M.; Jensen, K.; Durhan, E.; Ankley, G.; Collette, T. Profiling lipid metabolites yields unique information on sex- and time-dependent responses of fathead minnows (Pimephales promelas) exposed to 17 alpha-ethynylestradiol Metabolomics 2009, 5, 22-32
44. Miranda, C.; Wang, J.; Henderson, M.; Buhler, D. Purification and characterization of hepatic steroid hydroxylases from untreated rainbow trout Arch. Biochem. Biophys. 1989, 268, 227-238
45. Thibaut, R.; Debrauwer, L.; Perdu, E.; Goksoyr, A.; Cravedi, J.; Arukwe, A. Regio-specific hydroxylation of nonylphenol and the involvement of CYP2K- and CYP2M-like iso-enzymes in the Atlantic salmon (Salmo salar) Aquat. Toxicol. 2002, 56, 177-190
46. Wiseman, S.; He, Y.; Gamal El-Din, M.; Martin, J.; Jones, P.; Hecker, M.; Giesy, J. Transcriptional responses of male fathead minnows exposed to oil sands process-affected water Comp. Biochem. Physiol., Part C: Toxicol. Pharmacol. 2013, 157, 227-235
47. Git, A.; Dvinge, H.; Salmon-Divon, M.; Osborne, M.; Kutter, C.; Hadfield, J.; Bertone, P.; Caldas, C. Systematic comparison of microarray profiling, real-time PCR, and next-generation sequencing technologies for measuring differential microRNA expression RNA 2010, 16, 991-1006
48. Marioni, J.; Mason, C.; Mane, S.; Stephens, M.; Gilad, Y. RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays Genome Res. 2008, 18, 1509-1517
49. t' Hoen, P.; Ariyurek, Y.; Thygesen, H.; Vreugdenhil, E.; Vossen, R.; de Menezes, R.; Boer, J.; van Ommen, G.; den Dunnen, J. Deep sequencing-based expression analysis shows major advances in robustness, resolution and inter-lab portability over five microarray platforms Nucleic Acids Res. 2008, 36, 141-151
50. Kolpin, D.; Furlong, E.; Meyer, M.; Thurman, E.; Zaugg, S.; Barber, L.; Buxton, H. Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999-2000 Environ. Sci. Technol. 2002, 36, 1202-1211
51. Kolpin, D.; Furlong, E.; Meyer, M.; Thurman, E.; Zaugg, S.; Barber, L.; Buxton, H. Response to comment on ″Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999-2000: A national reconnaissance″ Environ. Sci. Technol. 2002, 36, 4007-4008