Effects of a 3β-hydroxysteroid dehydrogenase inhibitor, trilostane, on the fathead minnow reproductive axis

Toxicological Sciences

Volumn 104, Issue 1, 2008, Pages 113-123

  Villeneuve, Daniel L ^a   Blake, Lindsey S ^a   Brodin, Jeffrey D ^a   Cavallin, Jenna E ^a   Durhan, Elizabeth J ^a   Jensen, Kathleen M ^a   Kahl, Michael D ^a   Makynen, Elizabeth A ^a   Martinović, Dalma ^a   Mueller, Nathaniel D ^a   Ankley, Gerald T ^a  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Endocrine disruption; Fish; Gene expression; Reproduction; Steroidogenesis

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; ESTRADIOL; MESSENGER RNA; PROGESTERONE; TRILOSTANE; VITELLOGENIN; 3 (OR 17) BETA HYDROXYSTEROID DEHYDROGENASE; 3 (OR 17)-BETA-HYDROXYSTEROID DEHYDROGENASE; ANDROSTANOLONE; AROMATASE; AROMATASE INHIBITOR; DRUG DERIVATIVE; ENDOCRINE DISRUPTOR; HYDROXYSTEROID DEHYDROGENASE;

ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; EGG PRODUCTION; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; FISH; GENITAL SYSTEM DISEASE; GONAD; HISTOPATHOLOGY; HORMONE SYNTHESIS; IN VITRO STUDY; MALE; NONHUMAN; OVARY; PIMEPHALES PROMELAS; PROTEIN BLOOD LEVEL; REPRODUCTIVE SUCCESS; REPRODUCTIVE TOXICITY; RNA TRANSCRIPTION; SPAWNING; STEROIDOGENESIS; TESTIS SIZE; ANIMAL; BLOOD; CYPRINIFORMES; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; REPRODUCTION; TESTIS;

PIMEPHALES PROMELAS; VERTEBRATA;

17-HYDROXYSTEROID DEHYDROGENASES; ANIMALS; AROMATASE; AROMATASE INHIBITORS; CYPRINIDAE; DIHYDROTESTOSTERONE; ENDOCRINE DISRUPTORS; ESTRADIOL; FEMALE; GENE EXPRESSION REGULATION; MALE; OVARY; REPRODUCTION; RNA, MESSENGER; TESTIS; VITELLOGENINS;

EID: 45549097242     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfn073     Document Type: Article

References (61)

1. Andric, S. A., Kostic, T. S., Stojilkovic, S. S., and Kovacevic, R. Z. (2000). Inhibition of rat testicular androgenesis by a polychlorinated biphenyl mixture aroclor 1248. Biol. Reprod. 62, 1882-1888.
2. Ankley, G. T., Defoe, D. L., Kahl, M. D., Jensen, K. M., Makynen, E. A., Miracle, A., Hartig, P., Gray, L. E., Cardon, M., and Wilson, V. (2004). Evaluation of the model anti-androgen flutamide for assessing the mechanistic basis of responses to an androgen in the fathead minnow (Pimephales promelas). Environ. Sci. Technol. 38, 6322-6327.
3. Ankley, G. T., Jensen, K. M., Durhan, E. J., Makynen, E. A., Butterworth, B. C., Kahl, M. D., Villeneuve, D. L., Linnum, A., Gray, L. E., Cardon, M., et al. (2005a). Effects of two fungicides with multiple modes of action on reproductive endocrine function in the fathead minnow (Pimephales promelas). Toxicol. Sci. 86, 300-308.
4. Ankley, G. T., Jensen, K. M., Kahl, M. D., Korte, J. J., and Makynen, E. A. (2001). Description and evaluation of a short-term reproduction test with the fathead minnow (Pimephales promelas). Environ. Toxicol. Chem. 20, 1276-1290.
5. Ankley, G. T., Jensen, K. M., Kahl, M. D., Makynen, E. A., Blake, L. S., Greene, K. J., Johnson, R. D., and Villeneuve, D. L. (2007). Ketoconazole in the fathead minnow (Pimephales promelas): Reproductive toxicity and biological compensation. Environ. Toxicol. Chem. 26, 1214-23.
6. Ankley, G. T., Jensen, K. M., Makynen, E. A., Kahl, M. D., Korte, J. J., Hornung, M. W., Henry, T. R., Denny, J. S., Leino, R. L., Wilson, V. S., et al. (2003). Effects of the androgenic growth promoter 17-β-trenbolone on fecundity and reproductive endocrinology of the fathead minnow. Environ. Toxicol. Chem. 22, 1350-1360.
7. Ankley, G. T., Kahl, M. D., Jensen, K. M., Hornung, M. W., Korte, J. J., Makynen, E. A., and Leino, R. L. (2002). Evaluation of the aromatase inhibitor fadrozole in a short-term reproduction assay with the fathead minnow (Pimephales promelas). Toxicol. Sci. 67, 121-130.
8. Ankley, G. T., Kuehl, D. W., Kahl, M. D., Jensen, K. M., Linnum, A., Leino, R. L., and Villeneuve, D. L. (2005b). Reproductive and developmental toxicity and bioconcentration of perfluorooctanesulfonate (PFOS) in a partial-life cycle test with the fathead minnow (Pimephales promelas). Environ. Toxicol. Chem. 24, 2316-2324.
9. Arukwe, A., and Goksøyr, A. (2003). Eggshell and egg yolk proteins in fish: Hepatic proteins for the next generation: Oogenetic, population, and evolutionary implications of endocrine disruption. Comp. Hepatol. 2, 1-21.
10. Bhattacharyya, S., Sen, U., Bhattacharyya, S. P., and Mukherjee, D. (2000). Identification of maturation-inducing steroid in a freshwater perch Anabas testudineus and differential responses of intact follicles and denuded oocytes to cyclic AMP in oocyte maturation. J. Exp. Zool. 287, 294-303.
11. Borg, B. (1994). Androgens in teleost fishes. Comp. Biochem. Physiol. Part C. 109, 219-245.
12. Ekman, D. R., Teng, Q., Jensen, K. M., Martinovic, D., Villeneuve, D. L., Ankley, G. T., and Collette, T. W. (2007). NMR analysis of male fathead minnow urinary metabolites: A potential approach for studying impacts of chemical exposures. Aquat. Toxicol. 85, 104-112.
13. Erbs, M., Hoerger, C. C., Hartmann, N., and Bucheli, T. D. (2007). Quantification of six phytoestrogens at the nanogram per liter level in aqueous environmental samples using 13C3-labeled internal standards. J. Agric. Food Chem. 55, 8339-8345.
14. Fukutake, M., Takahashi, M., Ishida, K., Kawamura, H., Sugimura, T., and Wakabayashi, K. (1996). Quantification of genistein and genistin in soybeans and soybean products. Food. Chem. Toxicol. 34, 457-461.
15. Jensen, K. M., Kahl, M. D., Makynen, E. A., Korte, J. J., Leino, R. L., Butterworth, B. C., and Ankley, G. T. (2004). Characterization of responses to the antiandrogen flutamide in a short-term reproduction assay with the fathead minnow. Aquat. Toxicol. 70, 99-110.
16. Jensen, K. M., Korte, J. J., Kahl, M. D., Pasha, M. S., and Ankley, G. T. (2001). Aspects of basic reproductive biology and endocrinology in the fathead minnow (Pimephales promelas). Comp. Biochem. Physiol. C 128, 127-141.
17. Kawanishi, M., Takamura-Enya, T., Ermawati, R., Shimohara, C., Sakamoto, M., Matsukawa, K., Matsuda, T., Murahashi, T., Matsui, S., Wakabayashi, K., et al. (2004). Detection of genistein as an estrogenic contaminant of river water in Osaka. Environ. Sci. Technol. 38 6424-6429.
18. King, W. T., Thomas, P., and Sullivan, C. V. (1994). Hormonal regulation of final maturation of striped bass oocytes in vitro. Gen. Comp. Endocrinol. 96, 223-233.
19. Kiparissis, Y., Hughes, R., Metcalfe, C., and Ternes, T. (2001). Identification of the isoflavonoid genistein in bleached kraft mill effluent. Environ. Sci. Technol. 35, 2423-2427.
20. Komanicky, P., Spark, R. F., and Melby, J. C. (1978). Treatment of Cushing's syndrome with trilostane (WIN 24,540), an inhibitor of adrenal steroid biosynthesis. J. Clin. Endocrinol. Metab. 47, 1042-1051.
21. Korte, J. J., Kahl, M. D., Jensen, K. M., Pasha, M. S., Parks, L. G., LeBlanc, G. A., and Ankley, G. T. (2000). Fathead minnow vitellogenin: Complementary DNA sequence and messenger RNA and protein expression after 17B-estradiol treatment. Environ. Toxicol. Chem. 19, 972-981.
22. Kumar, R., Ijiri, S., and Trant, J. (2001). Molecular biology of channel catfish gonadotropin receptors: 2. Complementary DNA cloning, functional expression, and seasonal gene expression of the follicle-stimulating hormone receptor. Biol. Reprod. 65, 710-717.
23. Makynen, E., Kahl, M., Jensen, K., Tietge, J., Wells, K., Van der Kraak, G., and Ankley, G. (2000). Effects of the mammalian antiandrogen vinclozolin on development and reproduction of the fathead minnow. Aquat. Toxicol. 48, 461-475.
24. Martinović, D., Blake, L. S., Durban, E. J., Greene, K. J., Kahl, M. D., Jensen, K. M., Makynen, E. A., Villeneuve, D. L., and Ankley, G. T. (2008). Reproductive toxicity of vinclozolin in the fathead minnow: Confirming an anti-androgenic mode of action. Environ. Toxicol. Chem. 27, 478-488.
25. Mathieu, M., Mensah-Nyagan, A. G., Vallarino, M., Do-Rego, J. L., Beaujean, D., Vaudry, D., Luu-The, V., Pelletier, G., and Vaudry, H. (2001). Immunohistochemical localization of 3 beta-hydroxysteroid dehydrogenase and 5 alpha-reductase in the brain of the African lungfish Protopterus annectens. J. Comp. Neurol. 438, 123-135.
26. McMaster, M. E., Munkittrick, K. R., Jardine, J. J., Robinson, R. D., and Van Der Kraak, G. J. (1995). Protocol for measuring in vitro steroid production by fish gonadal tissue. Canadian Technical Report of Fisheries and Aquatic Sciences 1961 1-78
27. McVey, M. J., and Cooke, G. M. (2003). Inhibition of rat testis microsomal 3beta-hydroxysteroid dehydrogenase activity by tributyltin. J. Steroid Biochem. Mol. Biol. 86, 99-105.
28. Mensah-Nyagan, A. G., Feuilloley, M., Dupont, E., Do-Rego, J. L., Leboulenger, F., Pelletier, G., and Vaudry, H. (1994). Immunocytochemical localization and biological activity of 3 beta-hydroxysteroid dehydrogenase in the central nervous system of the frog. J. Neurosci. 14, 7306-7318.
29. Miles-Richardson, S., Kramer, V., Fitzgerald, S., Render, J., Yamini, B., Barbee, S., and Giesy, J. (1999). Effects of waterborne exposure of 17β-estradiol on secondary sex characteristics and gonads of fathead minnows (Pimephales promelas). Aquat. Toxicol. 47, 129-145.
30. Miller, D. H., Jensen, K. M., Villeneuve, D. L., Kahl, M. D., Makynen, E. A., Durhan, E. J., and Ankley, G. T. (2007) Linkage of biochemical responses to population-level effects: A case study with vitellogenin in the fathead minnow (Pimephales promelas). Environ. Toxicol. Chem. 26, 521-527.
31. Miller, W. (1988). Molecular biology of steroid hormone synthesis. Endocr. Rev. 9, 295-318.
32. Miller, W. L. (2005). Minireview: Regulation of steroidogenesis by electron transfer. Endocrinology 146, 2544-2550.
33. Mondal, S., Mukhopadhyay, B., and Bhattacharya, S. (1997). Inorganic mercury binding to fish oocyte plasma membrane induces steroidogenesis and translatable messenger RNA synthesis. Biometals 10, 285-290.
34. Mukherjee, D., Sen, U., Paul, S., and Bhattacharyya, S. P. (2006). In vitro effects of insulin-like growth factors and insulin on oocyte maturation and maturation-inducing steroid production in ovarian follicles of common carp, Cyprinus carpio. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 144, 63-77.
35. Nagahama, Y. (1997). 17 alpha,20 beta-dihydroxy-4-pregnen-3-one, a maturation-inducing hormone in fish oocytes: Mechanisms of synthesis and action. Steroids 62, 190-196.
36. Norris, D. O. (2007). In Vertebrate Endocrinology, 4th ed. Academic Press, New York.
37. Ohno, S., Matsumoto, N., Watanabe, M., and Nakajin, S. (2004). Flavonoid inhibition of overexpressed human 3beta-hydroxysteroid dehydrogenase type II. J. Steroid Biochem. Mol. Biol. 88, 175-182.
38. Ohno, S., Shinoda, S., Toyoshima, S., Nakazawa, H., Makino, T., and Nakajin, S. (2002). Effects of flavonoid phytochemicals on cortisol production and on activities of steroidogenic enzymes in human adrenocortical H295R cells. J. Steroid Biochem. Mol. Biol. 80 355-363.
39. Pandey, A. V., and Miller, W. L. (2005). Regulation of 17,20 lyase activity by cytochrome b5 and by serine phosphorylation of P450c17. J. Biol. Chem. 280, 13265-13271.
40. Parrott, J. L., and Blunt, B. R. (2005). Life-cycle exposure of fathead minnows (Pimephales promelas) to an ethinylestradiol concentration below 1 ng/L reduces egg fertilization success and demasculinizes males. Environ. Toxicol. 20, 131-141.
41. Patiño, R., Yoshizaki, G., Thomas, P., and Kagawa, H. (2001). Gonadotropic control of ovarian follicle maturation: The two-stage concept and its mechanism. Comp. Biochem. Physiol. Part B. 129 427-439.
42. Petrino, T. R., Lin, Y. W., and Wallace, R. A. (1989). Steroidogenesis in Fundulus heteroclitus. I. Production of 17 alpha-hydroxy,20 beta-dihydroprogesterone, testosterone, and 17 beta-estradiol by prematurational follicles in vitro. Gen. Comp. Endocrinol. 73 147-156.
43. Potts, G. O., Creange, J. E., Hardomg, H. R., and Schane, H. P. (1978). Trilostane, an orally active inhibitor of steroid biosynthesis. Steroids 32, 257-267.
44. Sakamoto, H., Ukena, K., and Tsutsui, K. (2001). Activity and localization of 3beta-hydroxysteroid dehydrogenase/ delta5-delta4-isomerase in the zebra-fish central nervous system. J. Comp. Neurol. 439, 291-305.
45. Stocco, D. (2001). StAR protein and the regulation of steroid hormone biosynthesis. Annu. Rev. Physiol. 63, 193-213.
46. Stocco, D., and Clark, B. (1996). Regulation of the acute production of steroids in steroidogenic cells. Endocr. Rev. 17, 221-244.
47. Thomas, P., Zhu, Y., and Pace, M. (2002). Progestin membrane receptors involved in the meiotic maturation of teleost oocytes: A review with some new findings. Steroids 67, 511-517.
48. Touitou, Y., Auzeby, A., Bogdan, A., Luton, J. P., and Galan, P. (1984). 11 beta-Hydroxy-11-ketosteroids equilibrium, a source of misinterpretation in steroid synthesis: Evidence through the effects of trilostane on 11 beta-hydroxysteroid dehydrogenase in sheep and human adrenals in vitro. J. Steroid Biochem. 20, 763-768.
49. Trudeau, V. (1997). Neuroendocrine regulation of gonadotropin II release and gonadal growth in the goldfish, Carassius auratus. Rev. Reprod. 2, 55-68.
50. Trudeau, V. L., Spanswick, D., Fraser, E. J., Lariviéte, K., Crump, D., Chiu, S., MacMillan, M., and Schulz, R. W. (2000). The role of amino acid neurotransmitters in the regulation of pituitary gonadotropin release in fish. Biochem. Cell Biol. 78, 241-259.
51. Tyler, C., and Sumpter, J. (1996). Oocyte growth and development in teleosts. Rev. Fish Biol. Fisher. 6, 287-318.
52. Ukena, K., Honda, Y., Inai, Y., Kohchi, C., Lea, R. W., and Tsutsui, K. (1999). Expression and activity of 3beta-hydroxysteroid dehydrogenase/ delta5-delta4-isomerase in different regions of the avian brain. Brain. Res. 818, 536-542.
53. US EPA. (2002). A Short-Term Test Method for Assessing the Reproductive Toxicity of Endocrine-Disrupting Chemicals using the Fathead Minnow (Pimephales promelas) EPA/600/R-01/067. US EPA, Office of Research and Development, National Health and Environmental Effects Research Laboratory, Mid-Continent Ecology Division
54. Villeneuve, D. L., Ankley, G. T., Makynen, E. A., Blake, L. S., Greene, K. J., Higley, E. B., Newsted, J. L., Giesy, J. P., and Hecker, M. (2007b). Comparison of fathead minnow ovary explant and H295R cell-based steroidogenesis assays for identifying endocrine-active chemicals. Ecotoxicol. Environ. Saf. 68, 20-32.
55. Villeneuve, D. L, Blake, L. S., Brodin, J. D., Greene, K. J., Knoebl, I., Miracle, A. L., Martinovic, D., and Ankley, G. T. (2007c). Transcription of key genes regulating gonadal steroidogenesis in control and ketoconazole- or vinclozolin-exposed fathead minnows. Toxicol. Sci. 98, 395-407.
56. Villeneuve, D. L., Knoebl, I., Kahl, M. D., Jensen, K. M., Hammermeister, D. E., Greene, K. J., Blake, L. S., and Ankley, G. T. (2006a). Relationship between brain and ovary aromatase activity and isoform-specific aromatase mRNA expression in the fathead minnow (Pimephales promelas). Aquat. Toxicol. 76, 353-368.
57. Villeneuve, D. L., Larkin, P., Knoebl, I. Miracle, A. L., Kahl, M. D., Jensen, K. M., Makynen, E. A., Durhan, E. J., Carter, B. J., Denslow, N. D., and Ankley, G. T. (2007a). A graphical systems model to facilitate hypothesis-driven ecotoxicogenomics research on the teleost brain-pituitaty-gonadal axis. Environ. Sci. Technol. 41, 321-330.
58. Villeneuve, D. L., Miracle, A. L., Jensen, K. J., Degitz, S. J., Kahl, M. D., Korte, J. J., Greene, K. J., Blake, L. S., Linnum, A. L., and Ankley, G. T. (2001d). Development of quantitative real-time PCR assays for fathead minnow (Pimephales promelas) gonadotropin β subunit mRNAs to support endocrine disruptor research. Comp. Biochem. Physiol. C. 145, 171-183.
59. Villeneuve, D. L., Murphy, M. B., Kahl, M. D., Jensen, K. M., Butterworth, B. C., Makynen, E. A., Durban, E. J., Linnum, A., Laino, R. L., Curtis, L. R., et al. (2006b). Evaluation of the methoxytriazine herbicide prometon using a short-term fathead minnow reproduction test and a suite of in vitro bioassays. Environ. Toxicol: Chem. 25, 2143-2153.
60. Weber, G. M., and Sullivan, C. V. (2000). Effects of insulin-like growth factor-I on in vitro final oocyte maturation and ovarian steroidogenesis in striped bass, Morone saxatilis. Biol. Reprod. 63, 1049-1057.
61. Wong, C. K., and Keung, W. M. (1999). Bovine adrenal 3β-hydroxysteroid dehydrogenase (E.C. 1.1.1.145)/5-ene-4-ene isomerase (E.C. 5.3.3.1): Characterization and its inhibition by isoflavones. J. Steroid Biochem. Mol. Biol. 71, 191-202.