Mode of action of human pharmaceuticals in fish: The effects of the 5-alpha-reductase inhibitor, dutasteride, on reproduction as a case study

Aquatic Toxicology

Volumn 128-129, Issue , 2013, Pages 113-123

  Margiotta Casaluci, Luigi ^a   Hannah, Robert E ^b   Sumpter, John P ^a  

^a BRUNEL UNIVERSITY   (United Kingdom)

^b GLAXOSMITHKLINE   (United States)

Author keywords

5 Alpha reductase; Anti androgen; Fish; Pharmaceutical; Read across; Reproductive toxicology

Indexed keywords

11 OXOTESTOSTERONE; DUTASTERIDE; ESTRADIOL; STEROID 5ALPHA REDUCTASE; TESTOSTERONE; VITELLOGENIN;

DOSE-RESPONSE RELATIONSHIP; DRUG; ECOTOXICOLOGY; ENZYME ACTIVITY; FISH; INHIBITION; REPRODUCTION;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; CASE STUDY; CONCENTRATION RESPONSE; CONTROLLED STUDY; EGG PRODUCTION; EMBRYO; ENVIRONMENTAL EXPOSURE; ENZYME INHIBITION; ESTRADIOL BLOOD LEVEL; FEMALE; FEMALE FERTILITY; HATCHING; HISTOPATHOLOGY; MALE; MALE FERTILITY; MALE GENITAL TRACT PARAMETERS; MORPHOMETRICS; NONHUMAN; NUPTIAL TUBERCLE NUMBER; NUPTIAL TUBERCLE PROMINENCE; PIMEPHALES PROMELAS; PRIORITY JOURNAL; REPRODUCTIVE TOXICITY; SEMEN ANALYSIS; SPAWNING; SPERM LINEARITY; SPERM STRAIGHTNESS; SPERMATOZOON MOTILITY; TESTOSTERONE BLOOD LEVEL; TOXICITY TESTING;

5-ALPHA REDUCTASE INHIBITORS; ANIMALS; AZASTEROIDS; BODY SIZE; CYPRINIDAE; FEMALE; GONADAL STEROID HORMONES; GONADS; MALE; REPRODUCTION; SEX CHARACTERISTICS; SPERMATOZOA; VITELLOGENINS; WATER; WATER POLLUTANTS, CHEMICAL;

MAMMALIA; PIMEPHALES PROMELAS; TELEOSTEI;

EID: 84871833923     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2012.12.003     Document Type: Article

References (44)

1. Abaigar T., Holt W.V., Harrison R.A.P., Del Barrio G. Sperm subpopulations in boar (Sus scrofa) and gazelle (Gazella dama mhorr) semen as revealed by pattern analysis of computer-assisted motility assessments. Biology of Reproduction 1999, 60:32-41.
2. Ankley G.T., Brooks B.W., Huggett D.B., Sumpter J.P. Repeating history: pharmaceuticals in the environment. Environmental Science and Technology 2007, 41(24):8211-8217.
3. Ankley G.T., Jensen K.M., Kahl M.D., Korte J.J., Makynen E.A. Description and evaluation of a short-term reproduction test with the fathead minnow (Pimephales promelas). Environmental Toxicology and Chemistry 2001, 20(6):1276-1290.
4. Berninger J.P., Brooks B.W. Leveraging mammalian pharmaceutical toxicology and pharmacology data to predict chronic fish responses to pharmaceuticals. Toxicology Letters 2010, 193(1):69-78.
5. Belbin L. PATN Pattern Analysis Package 1993, CSIRO, Lyneham, Australia.
6. Borg B. Androgens in teleost fishes. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology & Endocrinology 1994, 109(3):219-245.
7. Christen V., Hickmann S., Rechenberg B., Fent K. Highly active human pharmaceuticals in aquatic systems: a concept for their identification based on their mode of action. Aquatic Toxicology 2010, 96(3):167-181.
8. Cunningham V.L., Binks S.P., Olson M.J. Human health risk assessment from the presence of human pharmaceuticals in the aquatic environment. Regulatory Toxicology and Pharmacology 2009, 53(1):39-45.
9. Drummond A.E. The role of steroids in follicular growth. Reproductive Biology and Endocrinology 2006, 4:16.
10. EMEA (European Medicine Agency) Committee for Medicinal Products for Human Use (CHMP): Guideline on the Environmental Risk Assessment of Medicinal Products for Human Use 2006, http://www.emea.europa.eu/pdfs/human/swp/444700en.pdf.
11. Gage M.J.G., Macfarlane C.P., Yeates S., Ward R.G., Searle J.B., Parker G.A. Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Current Biology 2004, 14(1):44-47.
12. Goodarzi M.O., Dumesic D.A., Chazenbalk G., Azziz R. Polycystic ovary syndrome: etiology, pathogenesis and diagnosis. Nature Reviews Endocrinology 2011, 7(4):219-231.
13. GSK, 2001. Dutasteride Pharmacology/Toxicology Review and Evaluation. US FDA application number: 21-319.
14. Gunnarsson L., Jauhiainen A., Kristiansson E., Nerman O., Larsson D.G.J. Evolutionary conservation of human drug targets in organisms used for environmental risk assessments. Environmental Science and Technology 2008, 42(15):5807-5813.
15. Hala D.N., Van Look K., Holt W.V., Jobling S. Validation of a method for measuring sperm quality and quantity in reproductive toxicity tests with pair-breeding male fathead minnows (Pimephales promelas). ILAR Journal 2009, 50(4):1-10.
16. Harries J.E., Runnalls T., Hill E., Harris C.A., Maddix S., Sumpter J.P., Tyler C.R. Development of a reproductive performance test for endocrine disrupting chemicals using pair-breeding fathead minnows (Pimephales promelas). Environmental Science and Technology 2000, 34(14):3003-3011.
17. Holt W.V., Hernandez M., Warrell L., Satake N. The long and the short of sperm selection in vitro and in vivo: swim-up techniques select for the longer and faster swimming mammalian sperm. Journal of Evolutionary Biology 2010, 23(3):598-608.
18. Huggett D.B., Cook J.C., Ericson J.F., Williams R.T. A theoretical model for utilizing mammalian pharmacology and safety data to prioritize potential impacts of human pharmaceuticals to fish. Human and Ecological Risk Assessment 2003, 9(7):1789-1799.
19. Jensen K.M., Kahl M.D., Makynen E.A., Korte J.J., Leino R.L., Butterworth B.C., Ankley G.T. Characterization of responses to the antiandrogen flutamide in a short-term reproduction assay with the fathead minnow. Aquatic Toxicology 2004, 70(2):99-110.
20. Kime D.E., Van Look K.J.W., McAllister B.G., Huyskens G., Rurangwa E., Ollevier F. Computer-assisted sperm analysis (CASA) as a tool for monitoring sperm quality in fish. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology & Endocrinology 2001, 130(4):425-433.
21. Kortner T.M., Rocha E., Silva P., Castro L.F.C., Arukwe A. Genomic approach in evaluating the role of androgens on the growth of Atlantic cod (Gadus morhua) previtellogenic oocytes. Comparative Biochemistry and Physiology Part D: Genomics & Proteomics 2008, 3(3):205-218.
22. Kostich M.S., Lazorchak J.M. Risks to aquatic organisms posed by human pharmaceutical use. Science of the Total Environment 2008, 389(2/3):329-339.
23. Lahnsteiner F., Berger B., Weismann T., Patzner R.A. Determination of semen quality of the rainbow trout, Oncorhynchus mykiss, by sperm motility, seminal plasma parameters, and spermatozoal metabolism. Aquaculture 1998, 163(1/2):163-181.
24. Mahendroo M.S., Cala K.M., Russell D.W. 5 Alpha-reduced androgens play a key role in murine parturition. Molecular Endocrinology 1996, 10(4):380-392.
25. Margiotta-Casaluci L., Sumpter J. 5 Alpha-dihydrotestosterone is a potent androgen in the fathead minnow (Pimephales promelas). General and Comparative Endocrinology 2011, 171(3):309-318.
26. Margiotta-Casaluci, L., Courant, F., Antignac, J.P., Le Bizec, B., Sumpter, J.P. Identification and quantification of 5α-dihydrotestosterone in the teleost fathead minnow (Pimephales promelas) by gas chromatography-tandem mass spectrometry, submitted for publication.
27. Martinovic D., Blake L.S., Durhan E.J., Greene K.J., Kahl M.D., Jensen K.M., Makynen E.A., Villeneuve D.L., Ankley G.T. Reproductive toxicity of vinclozolin in the fathead minnow: confirming an anti-androgenic mode of action. Environmental Toxicology and Chemistry 2008, 27(2):478-488.
28. McCormick J.H., Stokes G.N., Hermanutz R.O. Oocyte atresia and reproductive success in fathead minnows (Pimephales promelas) exposed to acidified hardwater environments. Archives of Environment Contamination and Toxicology 1989, 18(1/2):207-214.
29. McDonald J.H. Handbook of Biological Statistics 2009, Sparky House Publishing, Baltimore. 2nd ed.
30. OECD, 2006. Report of the validation of the 21-day fish screening assay for the detection of endocrine substances (phase 1B). ENV/JM/MONO (29). Series on Testing and Assessment Number 61, Paris, France.
31. Owen S.F., Giltrow E., Huggett D.B., Hutchinson T.H., Saye J., Winter M.J., Sumpter J.P. Comparative physiology, pharmacology and toxicology of beta-blockers: mammals versus fish. Aquatic Toxicology 2007, 82(3):145-162.
32. Panter G.H., Glennon Y.C., Robinson J., Hargreaves A., Murray-Smith R. Effects of the anti-androgen, bicalutamide, in a reduced life-cycle study with the fathead minnow (Pimephales promelas). Aquatic Toxicology 2012, 114:31-38.
33. Runnalls T., Margiotta-Casaluci L., Kugathas S., Sumpter J.P. Pharmaceuticals in the aquatic environment: steroids and anti-steroids as high priorities for research. Human and Ecological Risk Assessment 2010, 16(6):1318-1338.
34. Rurangwa E., Roelants I., Huyskens G., Ebrahimi M., Kime D.E., Ollevier F. The minimum effective spermatozoa: egg ratio for artificial insemination and the effects of mercury on sperm motility and fertilization ability in Clarias gariepinus. Journal of Fish Biology 1998, 53(2):402-413.
35. Scott A.P., Mackenzie D.S., Stacey N.E. Endocrine changes during natural spawning in the white sucker, Catostomus commersoni. 2. Steroid-hormones. General and Comparative Endocrinology 1984, 56(3):349-359.
36. Seiler J.P. Pharmacodynamic activity of drugs and ecotoxicology - can the two be connected?. Toxicology Letters 2002, 131(1/2):105-115.
37. Smith R.J.F. Seasonal changes in the histology of the gonads and dorsal skin of the fathead minnow, Pimephales promelas. Canadian Journal of Zoology 1978, 56:2103-2109.
38. Sumpter J.P., Jobling S. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environmental Health Perspectives 1995, 103:173-178. 10.2307/3432529.
39. Tsilchorozidou T., Honour J.W., Conway G.S. Altered cortisol metabolism in polycystic ovary syndrome: insulin enhances 5 alpha-reduction but not the elevated adrenal steroid production rates. Journal of Clinical Endocrinology and Metabolism 2003, 88(12):5907-5913.
40. US EPA Histopathology Guidelines for the Fathead Minnow (Pimephales promelas) 21-day Reproduction Assay 2006, US EPA, Duluth, MN.
41. Villeneuve D.L., Blake L.S., Brodin J.D., Cavallin J.E., Durhan E.J., Jensen K.M., Kahl M.D., Makynen E.A., Martinovic D., Mueller N.D., Ankley G.T. Effects of a 3 beta-hydroxysteroid dehydrogenase inhibitor, trilostane, on the fathead minnow reproductive axis. Toxicological Sciences 2008, 104(1):113-123.
42. Winter M.J., Lillicrap A.D., Caunter J.E., Schaffner C., Alder A.C., Ramil M., Ternes T.A., Giltrow E., Sumpter J.P., Hutchinson T.H. Defining the chronic impacts of atenolol on embryo-larval development and reproduction in the fathead minnow (Pimephales promelas). Aquatic Toxicology 2008, 86(3):361-369.
43. Winter M.J., Owen S.F., Murray-Smith R., Panter G.H., Hetheridge M.J., Kinter L.B. Using data from drug discovery and development to aid the aquatic environmental risk assessment of human pharmaceuticals: concepts, considerations, and challenges. Integrated Environmental Assessment and Management 2010, 6(1):38-51.
44. Zar J.H. Biostatistical Analysis 1999, Prentice Hall, Upper Saddle River, NJ. 4th ed.