A mixture of an environmentally realistic concentration of a phthalate and herbicide reduces testosterone in male fathead minnow (Pimephales promelas) through a novel mechanism of action

Aquatic Toxicology

Volumn 110-111, Issue , 2012, Pages 74-83

  Crago, Jordan ^a   Klaper, Rebecca ^a  

^a UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

Anti androgen; Endocrine disruption; Fathead minnow; Herbicides; Low dose; Phthalates

Indexed keywords

DI(2 ETHYLHEXYL)PHTHALIC ACID; ESTRADIOL; FOLLITROPIN BETA SUBUNIT; HORMONE RECEPTOR; LINURON; LUTEINIZING HORMONE BETA SUBUNIT; MESSENGER RNA; PLASTICIZER; STEROID; TESTOSTERONE; UNCLASSIFIED DRUG;

CATABOLISM; CONCENTRATION (COMPOSITION); CYPRINID; ENDOCRINE DISRUPTOR; HERBICIDE; HORMONE; PHTHALATE; PLASMA; RNA; STEROID; TESTOSTERONE;

ADULT ANIMAL; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYP3A4 GENE; ENVIRONMENTAL EXPOSURE; GENE; GENE EXPRESSION; HYPOPHYSIS; LIVER; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PIMEPHALES PROMELAS; PRIORITY JOURNAL; STEROID METABOLISM; STEROIDOGENESIS; SULT1ST2 GENE; SULT2A1 GENE; TESTIS; TESTOSTERONE BLOOD LEVEL;

ANDROGEN ANTAGONISTS; ANIMALS; CYPRINIDAE; DIETHYLHEXYL PHTHALATE; ESTRADIOL; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION; HERBICIDES; LINURON; LUTEINIZING HORMONE; MALE; RNA, MESSENGER; TESTOSTERONE; WATER POLLUTANTS, CHEMICAL;

MAMMALIA; PIMEPHALES PROMELAS;

EID: 84856028584     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2011.12.021     Document Type: Article

References (45)

1. Ankley G.T., Jensen K.M., Kahl M.D., Makynen E.A., Blake L.S., Greene K.J., Johnson R.D., Villeneuve D.L. Ketoconazole in the fathead minnow (Pimephales promelas) reproductive toxicity and biological compensation. Environ. Toxicol. Chem. 2007, 26:1214-1223.
2. Ankley G.T., Bencic D.C., Breen M.S., Collette T.W., Conolly R.B., Denslow N.D., Edwards S.W., Ekman D.R., Garcia-Reyero N., Jensen K.M., Lazorchak J.M., Martinovic D., Miller D.H., Perkins E.J., Orlando E.F., Villeneuve D.L., Wang R-L., Watanabe K.H. Endocrine disrupting chemicals in fish: developing exposure indicators and predictive models of effects based on mechanism of action. Aquat. Toxicol. 2009, 92:168-178.
3. Ankley G.T., Bencic D.C., Cavallin J.E., Jensen K.M., Kahl M.D., Makynen E.A., Martinovic D., Mueller N.D., Wehmans L.C., Villeneuve D.L. Dynamic nature of alterations in the endocrine system of fathead minnows exposed to the fungicide prochloraz. Toxicol. Sci. 2009, 112:344-353.
4. Aoki K.A., Harris C.A., Katsiadaki I., Sumpter J.P. Evidence suggesting that di-n-butyl phthalate has antiandrogenic effects in fish. Environ. Toxicol. Chem. 2011, 30:1338-1345.
5. Bélanger A., Hum D.W., Beaulieu M., Lévesque E., Guillemette C., Tchernof A., Bélanger G., Turgeon D., Dubois S. Characterization and regulation of UDP-glucuronosyltransferases in steroid target tissues. J. Steroid Biochem. Mol. Biol. 1998, 65:301-310.
6. Brian J.V., Harris C.A., Scholze M., Backhaus T., Booy P., Lamoree M., Pojana G., Jonkers N., Runnalls T., Bonfà A., Marcomini A., Sumpter J.P. Accurate prediction of the response of freshwater fish to a mixture of estrogenic chemicals. Environ. Health Perspect. 2005, 113:721-728.
7. Chatterjee B., Majumdar D., Ozbilen O., Roy A.K. Molecular cloning and characterization of the cDNA for the androgen repressible SMP-2 in the rat liver. J. Biol. Chem. 1987, 262:822-825.
8. Chatterjee B., Song C.S., Kim J.M., Roy A.K. Androgen and estrogen sulfotransferases of the rat liver. Chem. Biol. Interact. 1994, 92:273-279.
9. Clewell H.J., Thomas R.S., Kenyon E.M., Hughes M.F., Adair B.M., Gentry P.R., Yager J.W. Concentration- and time-dependent genomic changes in the mouse urinary bladder following exposure to arsenate in drinking water for up to twelve weeks. Toxicol. Sci. 2011, (July). [Epub ahead of print].
10. Cooper B.W., Cho T.M., Thompson P.M., Wallace A.D. Phthalate induction of CYP3A4 is dependent on glucocorticoid regulation of PXR expression. Toxicol. Sci. 2008, 103:268-277.
11. Correia A.D., Freitas S., Scholze M., Goncalves J.F., Booij P., Lamoree M.H., Mañanós E., Reis-Henriques M.A. Mixtures of estrogenic chemicals enhance vitellogenic response in sea bass. Environ. Health Perspect. 2007, 115(Suppl. 1):115-121.
12. Corton J.C., Bocos C., Moreno E.S., Merritt A., Cattley R.C., Gustafsson J.A. Peroxisome proliferators alter the expression of estrogen-metabolizing enzymes. Biochimie 1997, 79:151-162.
13. Eagon P.K., Chandar N., Epley M.J., Elm M.S., Brady E.P., Rao K.N. Di(2-ethylhexyl)phthalate-induced changes in liver estrogen metabolism and hyperplasia. Int. J. Cancer 1994, 58:736-743.
14. Fan L.Q., You L., Brown-Borg H., Brown S., Edwards R.J., Corton J.C. Regulation of phase I and phase II steroid metabolism enzymes by PPAR alpha activators. Toxicol 2004, 204:109-121.
15. Filby A.L., Thorpe K.L., Maack G., Tyler C.R. Gene expression profiles revealing the mechanisms of anti-androgen- and estrogen-induced feminization in fish. Aquat. Toxicol. 2007, 81:219-231.
16. Finne E.F., Cooper G.A., Koop B.F., Hylland K., Tollefsen K.E. Toxicogenomic responses in rainbow trout (Oncorhynchus mykiss) hepatocytes exposed to model chemicals and a synthetic mixture. Aquat. Toxicol. 2007, 81:293-303.
17. Foster P.M. Disruption of reproductive development in male rat offspring following in utero exposure to phthalate esters. Int. J. Androl. 2006, 29:140-147.
18. Frömme H., Küchler T., Otto T., Pilz K., Müller J., Wenzel A. Occurrence of phthalates and bisphenol A and F in the environment. Water Res. 2002, 36:1429-1438.
19. Gentry P.R., McDonald T.B., Sullivan D.E., Shipp A.M., Yager J.W., Clewell H.J. Analysis of genomic dose-response information on arsenic to inform key events in a mode of action for carcinogenicity. Environ. Mol. Mutagen. 2010, 51:1-14.
20. Gray L.E., Ostby J., Furr J., Price M., Veeramachaneni D.N., Parks L. Perinatal exposure to the phthalates DEHP, BBP, and DINP, but not DEP, DMP, or DoTP, alters sexual differentiation of the male rat. Toxicol. Sci. 2000, 58:350-365.
21. Hill E.M., Evans K.L., Horwood J., Rostkowski P., Oladapo F.O., Gibson R., Shears J.A., Tyler C.R. Profiles and some initial identifications of (anti)androgenic compounds in fish exposed to wastewater treatment works effluents. Environ. Sci. Technol. 2010, 44:1137-1143.
22. Hockley S.L., Arlt V.M., Brewer D., Giddings I., Phillips D.H. Time- and concentration-dependent changes in gene expression induced by benzo(a)pyrene in two human cell lines, MCF-7 and HepG2. BMC Genomics 2006, 7:260.
23. Hotchkiss A.K., Parks-Saldutti L.G., Ostby J.S., Lambright C., Furr J., Vandenbergh J.G., Gray L.E. A mixture of the antiandrogens linuron and butyl benzyl phthalate alters sexual differentiation of the male rat in a cumulative fashion. Biol. Reprod. 2004, 71:1852-1861.
24. Huang H., Wu Q. Cloning and comparative analyses of the zebrafish Ugt repertoire reveal its evolutionary diversity. PLoS ONE 2010, 5(e9144.). 10.1371/journal.pone.0009144.
25. Hurst C.H., Waxman D.J. Environmental phthalate monoesters activate pregnane X receptor-mediated transcription. Toxicol. Appl. Pharmacol. 2004, 199:266-274.
26. Jobling S., Reynolds T., White R., Parker M.G., Sumpter J.P. A variety of environmentally persistent chemicals, including some phthalate plasticizers, are weakly estrogenic. Environ. Health Perspect. 1995, 103:582-587.
27. Lambright C., Ostby J., Bobseine K., Wilson V., Hotchkiss A.K., Mann P.C., Gray L.E Cellular and molecular mechanisms of action of linuron: an antiandrogenic herbicide that produces reproductive malformations in male rats. Toxicology 2000, 56:389-399.
28. Liu K., Lehmann K.P., Sar M., Young S.S., Gaido K.W. Gene expression profiling following in utero exposure to phthalate esters reveals new gene targets in the etiology of testicular dysgenesis. Biol. Reprod. 2005, 73:180-192.
29. Martinović D., Blake L.S., Durhan E.J., Greene K.J., Jensen K.M., Kahl M.D., Makynen E.A., Villeneuve D.L., Ankley G.T. Reproductive toxicity of vinclozolin in the fathead minnow: confirming an anti-androgenic mode of action. Environ. Toxicol. Chem. 2008, 27:478-488.
30. Onorato T.M., Brown P.W., Morris P.L. Mono-(2-ethylhexyl) phthalate increases spermatocyte mitochondrial peroxiredoxin 3 and cyclooxygenase 2. J. Androl. 2008, 29:293-303.
31. Rider C.V., Furr J., Wilson V.S., Gray L.E. A mixture of seven antiandrogens induces reproductive malformations in rats. Int. J. Androl. 2008, 31:249-262.
32. Sonoda J., Xie W., Rosenfeld J.M., Barwick J.L., Guzelian P.S., Evans R.M. Regulation of a xenobiotic sulfonation cascade by nuclear pregnane X receptor (PXR). Proc. Natl. Acad. Sci. U.S.A. 2002, 99:13801-13806.
33. Strott C.A. Sulfonation and molecular action. Endocrinol. Rev. 2002, 23:703-732.
34. Sugahara T., Yang Y.S., Liu C.C., Pai T.G., Liu M.C. Sulphonation of dehydroepiandrosterone and neurosteroids: molecular cloning, expression, and functional characterization of a novel zebrafish SULT2 cytosolic sulphotransferase. Biochem. J. 2003, 375:785-791.
35. Takeuchi S., Iida M., Yabushita H., Matsuda T., Kojima H. In vitro screening for aryl hydrocarbon receptor agonistic activity in 200 pesticides using a highly sensitive reporter cell line, DR-EcoScreen cells, and in vivo mouse liver cytochrome P450-1A induction by propanil, diuron and linuron. Chemosphere 2008, 74:155-165.
36. Thibaut R., Porte C. Effects of endocrine disrupters on sex steroid synthesis and metabolism pathways in fish. J. Steroid Biochem. Mol. Biol. 2004, 92:485-494.
37. Uren-Webster T.M., Lewis C., Filby A.L., Paull G.C., Santos E.M. Mechanisms of toxicity of di(2-ethylhexyl) phthalate on the reproductive health of male zebrafish. Aquat. Toxicol. 2010, 99:360-369.
38. Wilson V.S., Cardon M.C., Thornton J., Korte J.J., Ankley G.T., Welch J., Gray L.E., Hartig P.C. Cloning and in vitro expression and characterization of the androgen receptor and isolation of estrogen receptor alpha from the fathead Minnow (Pimephales promelas). Environ. Sci. Technol. 2004, 38:6314-6321.
39. Wilson V.S., Lambright C.R., Furr J.R., Howdeshell K.L., Gray L.E. The herbicide linuron reduces testosterone production from the fetal rat testis during both in utero and in vitro exposures. Toxicol. Lett. 2009, 186:73-77.
40. Woudneh M.B., Ou Z., Sekela M., Tuominen T., Gledhill M. Pesticide multiresidues in waters of the Lower Fraser Valley, British Columbia, Canada Part I. Surface water. J. Environ. Qual. 2009, 38:940-947.
41. Yamazaki H., Shimada T. Progesterone and testosterone hydroxylation by cytochromes P450 2C19, 2C9, and 3A4 in human liver microsomes. Arch. Biochem. Biophys. 1997, 346:161-169.
42. You L. Steroid hormone biotransformation and xenobiotic induction of hepatic steroid metabolizing enzymes. Chem. Biol. Interact. 2004, 147:233-246.
43. Zhang B., Cheng Q., Ou Z., Lee J.H., Xu M., Kochar U., Ren S., Huang M., Pflug B.R., Xie W. Pregnane X receptor as a therapeutic target to inhibit androgen activity. Endocrinology 2010, 151:5721-5729.
44. Zhang H., Kong F.X., Wang S.H., Yu Y., Zhang M. Vitellogenin induction by a mixture of steroidal estrogens in freshwater fishes and relevant risk assessment. Environ. Toxicol. 2009, 24:484-491.
45. Zhao S., Fernald R.D. Comprehensive algorithm for quantitative real-time polymerase chain reaction. J. Comput. Biol. 2005, 12:1045-1062.