Dose-dependent compensation responses of the hypothalamic-pituitary-gonadal-liver axis of zebrafish exposed to the fungicide prochloraz

Aquatic Toxicology

Volumn 160, Issue , 2015, Pages 69-75

  Dang, Yao ^a   Giesy, John P ^b,c,d,e   Wang, Jianghua ^a   Liu, Chunsheng ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

^c CITY UNIVERSITY OF HONG KONG   (Hong Kong)

^d UNIVERSITY OF HONG KONG   (Hong Kong)

^e NANJING UNIVERSITY   (China)

Author keywords

Aromatase inhibitor; Compensation responses; HPG axis; Prochloraz; Zebrafish

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; PROCHLORAZ; VITELLOGENIN; FUNGICIDE; IMIDAZOLE DERIVATIVE; WATER POLLUTANT;

COMPENSATION; ECOTOXICOLOGY; FISH; FUNGICIDE; INHIBITOR; PHYSIOLOGICAL RESPONSE; POLLUTION EXPOSURE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOLOGICAL MODEL; BRAIN LEVEL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSE LIVER FUNCTION RELATION; ECOTOXICOLOGY; ENVIRONMENTAL EXPOSURE; ER1 GENE; ER2BETA GENE; ESTRADIOL BLOOD LEVEL; GENE; GENE IDENTIFICATION; GENE LOCATION; GNRH GENE; GNRHR GENE; GONAD; HOMEOSTASIS; HYPOTHALAMUS HYPOPHYSIS GONAD SYSTEM; LHBETA GENE; LIVER LEVEL; NONHUMAN; PREDICTIVE VALUE; PRIORITY JOURNAL; STEROIDOGENESIS; TISSUE DISTRIBUTION; TRANSCRIPTION REGULATION; UPREGULATION; VTGS GENE; WATER POLLUTION INDICATOR; ZEBRA FISH; ANIMAL; BLOOD; BRAIN; DRUG EFFECTS; ENDOCRINE SYSTEM; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HYPOPHYSIS; HYPOTHALAMUS; LIVER; MALE; PHYSIOLOGY; TOXICITY; WATER POLLUTANT;

DANIO RERIO;

ANIMALS; BRAIN; ENDOCRINE SYSTEM; ENVIRONMENTAL EXPOSURE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; FUNGICIDES, INDUSTRIAL; GENE EXPRESSION REGULATION; GONADS; HYPOTHALAMUS; IMIDAZOLES; LIVER; MALE; PITUITARY GLAND; VITELLOGENINS; WATER POLLUTANTS, CHEMICAL; ZEBRAFISH;

EID: 84928695753     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2015.01.003     Document Type: Article

References (30)

1. Andersen C.L., Jensen J.L., Ørntoft T.F. Model-based variance estimation approach to identify genes suited for normalization: applied to bladder and colon cancer data sets. Cancer Res. 2004, 64:5245-5250.
2. 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., Wilson V.S. Effects of two fungicides with multiple modes of action on reproductive endocrine function in the fathead minnow (Pimephales promelas). Toxicol. Sci. 2005, 86:300-308.
3. 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. Toxocol. Chem. 2007, 26:1214-1223.
4. Ankley G.T., Bencic D.C., Cavallin J.E., Jensen K.M., kahl M.D., Makynen E.A., Martinović D., Mueller N.D., Wehmas 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.
5. Ankley G.T., Cavallin J.E., Durhan E.J., Jensen K.M., Kahl M.D., Makynen E.A., Thomas L.M., Wehmas L.C., Villeneuve D.L. A time-course analysis of effects of the steroidogenesis inhibitor ketoconazole on components of the hypothalamic-pituitary-gonadal axis of fathead minnows. Aquat. Toxicol. 2012, 114-115:88-95.
6. Blystone C.R., Lambright C.S., Howdeshell K.L., Furr J., Sternberg R.M., Butterworth B.C., Durhan E.J., Makynen E.A., Ankley G.T., Wilson V.S., Leblanc G.A., Gray L.E. Sensitivity of fetal rat testicular steroidogenesis to maternal prochloraz exposure and the underlying mechanism of inhibition. Toxicol. Sci. 2007, 97:512-519.
7. Breen M., Villeneuve D.L., Ankley G.T., Bencic D.C., Breen M.S., Watanabe K.H., Lloyd A.L., Conolly R.B. Developing predictive approaches to characterize adaptive responses of the reproductive endocrine axis to aromatase inhibition II computational modeling. Toxicol. Sci. 2013, 133:234-247.
8. Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L., Vandesompele J., Wittwer C.T. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Cilin. Chem. 2009, 55:611-622.
9. Han X.B., Yuen K.W.Y., Wu R.S.S. Polybrominated diphenyl ethers affect the reproduction and development, and alter the sex ratio of zebrafish (Danio rerio). Environ. Pollut. 2013, 182:120-126.
10. Liu C., Yu L., Deng J., Lam P.K.S., Wu R.S.S., Zhou B. Waterborne exposure to fluorotelomer alcohol 6:2 FTOH alters plasma sex hormone and gene transcription in the hypothalamic-pituitary-gonadal (HPG) axis of zebrafish. Aquat. Toxicol. 2009, 93:131-137.
11. Liu C., Zhang X., Deng J., Hecker M., Al-Khedhairy A., Giesy J.P., Zhou B. Effects of prochloraz or propylthiouracil on the cross-talk between the HPG: HPA and HPT axes in zebrafish. Environ. Sci. Technol. 2011, 45:769-775.
12. Marca Pereira M.L., Eppler E., Thorpe K.L., Wheeler J.R., Burkhardt-Holm P. Molecular and cellular effects of chemicals disrupting steroidogenesis during early ovarian development of brown trout (Salmo trutta fario). Environ. Toxicol. 2011, 29:199-206.
13. Marca Pereira M.L., Wheeler J.R., Thorpe K.L., Burkhardt-Holm P. Development of a ex vivo brown trout (Salmo trutta fario) gonad culture for assessing chemicals effects on steroidogenesis. Aquat. Toxicol. 2011, 101:500-511.
14. Mason J.I., Carr B.R., Murry B.A. Imidazole antimycotics: selective inhibitors of steroid aromatization and progesterone hydroxylation. Steroids 1987, 50:179-189.
15. Noriega N.C., Ostby J., Lambright C., Wilon V.S., Gray L.E. Late gestational exposure to the fungicide prochloraz delays the onset of parturition and causes reproductive malformations in male but not female rat offspring. Biol. Reprod. 2005, 72:1324-1335.
16. Sanderson J.T., Boerma J., Lansbergen G.W.A., van den Berg M. Induction and inhibition of aromatase (CYP19) activity by various classes of pesticides in H295R human adrenocortical carcinoma cells. Toxicol. Appl. Pharmacol. 2002, 182:44-54.
17. Skolness S.Y., Durhan E.J., Garcia-Reyero N., Jensen K.M., kahl M.D., Makynen E.A., Martinovic-Weigelt D., Perkins E., Villeneuve D.L., Ankley G.T. Effects of a short-term exposure to the fungicide prochloraz on endocrine function and gene expression in female fathead minnows (Pimephales promelas). Aquat. Toxicol. 2011, 103:170-178.
18. 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., Ankley G.T. A graphical systems model to facilitate hypothesis-duiven ecotoxicogenomics research on the teleost brain-pituitary-gonadal axis. Environ. Sci. Technol. 2007, 41:321-330.
19. Villeneuve D.L., Mueller N.D., Martinović D., Makynen E.A., Kahl M.D., Jensen K.M., Durhan E.J., Cavallin J.E., Bencic D., Ankley G.T. Direct effects compensation, and recovery in female fathead minnows exposed to a model aromatase inhibitor. Environ. Health Perspect. 2009, 117:624-631.
20. Villeneuve D.L., Wang R.L., Bencic D.C., Biales A.D., Martinović D., Lazorchak J.M., Toth G., Ankley G.T. Altered gene expression in the brain and ovaries of zebrafish (Danio rerio) exposed to the aromatase inhibitor fadrozole: microarray analysis and hypothesis generation. Environ. Toxicol. Chem. 2009, 28:1767-1782.
21. Villeneuve D.L., Breen M., Bencic D.C., Cavallin J.E., Jensen K.M., Makynen E.A., Thomas L.M., Wehmas L.C., Conolly R.B., Ankley G.T. Developing predictive approaches to characterize adaptive responses of the reproductive endocrine axis to aromatase inhibition I data generation in a small fish model. Toxicol. Sci. 2013, 133:225-233.
22. Vinggaard A.M., Hnida C., Breinholt V., Larsen J.C. Screening of selected pesticides for inhibition of CYP19 aromatase activity in vitro. Toxicol. In Vitro 2000, 14:227-234.
23. Yost E.E., Pow C.L., Hawkins M.B., Kullman S.W. Bridging the gap from screening assays to estrogenic effects in fish: potential roles of multiple estrogen receptor subtypes. Environ. Sci. Technol. 2014, 48:5211-5219.
24. Zhang X., Hecker M., Jones P.D., Newsted J., Au D., Kong R., Wu R.S.S., Giesy J.P. Responses of the medaka HPG axis PCR array and reproduction to prochloraz and ketoconazole. Environ. Sci. Technol. 2008, 42:6762-6769.
25. Zhang X., Hecker M., Park J.-W., Tompsett A.R., Newsted J., Nakayama K., Jones P.D., Au D., Kong R., Wu R.S.S., Giesy J.P. Real-time PCR array to study effects of chemicals on the hypothalamic-pituitary-gonadal axis of the Japanese medaka. Aquat. Toxicol. 2008, 88:173-182.
26. Zhang X., Hecker M., Park J.-W., Tompsett A.R., Jones P.D., Newsted J., Au D.W.T., Kong R., Wu R.S.S., Giesy J.P. Time-dependent transcriptional profiles of genes of the hypothalamic-pituitary-gonadal axis in medaka (Oryzias latipes) exposed to fadrozole and 17β-trenbolone. Environ. Toxocol. Chem. 2008, 27:2504-2511.
27. Zhou B., Liu C., Wang J., Lam P.K.S., Wu R.S.S. Primary cultured cells as sensitive in vitro model for assessment of toxicants-comparison to hepatocytes and gill epithelia. Aquat. Toxicol. 2006, 80:109-118.
28. van Haren L., Flinterman J.F., Rommerts F.F. Inhibition of the luteinizing hormone-dependent induction of cholesterol side chain cleavage enzyme in immature rat leydig cells by sertoli cell products. Eur. J. Endocrinol. 1995, 132:627-634.
29. van den Bossche H., Ruysschaert J.M., Defrise-Quertain F., Willemsens G., Cornelissen F., Marichal P., Cools W., Van Cutsem J. The interaction of miconazole and ketoconazole with lipids. Biochem. Pharmacol. 1982, 31:2609-2617.
30. van den Bossche H., Willemsens G., Cools W., Lauwers W.F.J., Le Jeune L. Biochemical effects of miconazole on fungi II. Inhibition of ergosterol biosynthesis in Canada albicans. Chem. Biol. Interact. 1987, 21:578-594.