atrazine; Carassius auratus; endocrine disruption; sex steroids
Abstract :
[en] Sexually mature goldfish (Carassius auratus) of both sexes were exposed to two doses (100 and 1000 mug/l) of the widely used herbicide atrazine (2-chloro-4-ethylamino-6-isolropylamino-s-triazine) for a period of 21 days and effects on the concentrations of gonad and plasma sex steroids (testosterone (T), 17beta-estradiol (E2) and 11-ketotestosterone (11-KT)), plasma vitellogenin (VTG) and gonad histo-morphology assessed. Atrazine did not show any obvious estrogenic effect in males, as determined by a lack of vitellogenin induction. There were, however, effects of atrazine on plasma androgen concentrations (androgen dynamics) and tissue (plasma and gonad) estrogen concentrations in male goldfish; exposure to 1000 mug/l atrazine induced suppression in both testosterone and 11-ketotestosterone, and resulted in elevated 17beta-estradiol, after 21 day of exposure. Further, these suppressive effects on plasma androgens and the induction in estrogen were dose- and time-related. The highest atrazine exposure dose induced structural disruption in the testis and both 100 and 1000 mug/l induced elevated levels of atresia in ovaries. (C) 2003 Elsevier B.V. All rights reserved.
Allran J.W., Karasov W.H. Effects of atrazine and nitrate on northern leopard frog (Rana pipiens) larvae exposed in the laboratory from post hatch through metamorphosis. Environ. Toxicol. Chem. 19:2000;2850-2855.
Allran J.W., Karasov W.H. Effects of atrazine on embryos, larvae, and adults of anuran amphibians. Environ. Toxicol. Chem. 20:2001;769-775.
Carr, J.A., Gentles, A., Smith, E.E., Goleman, W.L., Urquidi, L.J., Thuett, K., Kendall, R.J., 2002. Response of larval Xenopus laevis to atrazine exposure: assessment of metamorphosis and gonadal and laryngeal morphology. In: Proceeding of 21st Conference of European Comparative Endocrinologist, 26-30 August, University of Bonn, p. 80.
Connor K., Howell J., Chen I., Liu H., Berhane K., Sciarretta C., Safe S., Zacherewski T. Failure of chloro-s-triazine-derived compounds to induce estrogen receptor-mediated responses in vivo and in vitro. Fund. Appl. Toxicol. 30:1996;93-101.
Cooper R.L., Stoker T.E., Tyrey L., Goldman J.M., McElroy W.K. Atrazine disrupts the hypothalamic control of pituary-ovarian function. Toxicol. Sci. 53:2000;297-307.
Crain D.A., Spiteri I.D., Guillette L.J. Jr. The functional and structural observations of the neonatal reproductive system of alligators exposed in ovo to atrazine, 2,4-D, or estradiol. Toxicol. Indus. Health. 15:1999;180-185.
D'Cotta H., Fostier A., Guiguen Y., Govoroun M., Baroiller J.-F. Search for genes involved in the temperature-induced gonadal sex differentiation in the tilapia, Oreochromis niloticus. J. Exp. Zool. 290:2001;574-585.
Diana S.G., Restaris W.J. Jr., Schaeffer D.J., Beckmen K.B., Beasley V.R. Effects of atrazine on amphibian growth and survival in artificial aquatic communities. Environ. Toxicol. Chem. 19:2000;2961-2967.
Donna A., Crosignani P., Robutti F., Betta P.G., Bocca R., Mariani N., Ferrario F. Triazine herbicides and ovarian epithelial neoplasms. Scand. J. Work Environ. Health. 15:1989;47-53.
Du Preez H.H., van Vuren J.H.J. Bioconcentration of atrazine in the banded tilapia, Tilapia sparrmanii. Comp. Biochem. Physiol. 101C:1992;651-655.
Fostier A., Jalabert B. Steroidogenesis in rainbow trout (Salmo gairdneri) at various preovulatory stages: changes in plasma hormone levels and in vivo and in vitro responses of the ovary to salmon gonadotropin. Fish Physiol. Biochem. 2:1986;87-99.
Friedmann A.S. Atrazine inhibition of testosterone production in rat males following peripubertal exposure. Reprod. Toxicol. 16:2002;275-279.
Gluth G., Hanke W. A comparison of physiological changes in carp, Cyprinus carpio, induced by several pollutants at sublethal concentrations. I. The dependency on exposure time. Ecotoxicol. Environ. Saf. 9:1985;179-188.
Goodbred S.L., Gilliom R.J., Gross T.S., Denslow N.P., Bryant W.L., Schoeb T.R. Reconnaissance of 17β-estradiol, 11-ketotestosterone, vitellogenin, and gonad histopathology in Common carp of United States Streams: potential for contaminant-induced endocrine disruption. US Geol. Survey Open-File Rep. 96-627:1997;1-47.
Hayes T.B., Collins A., Lee M., Mendoza M., Noriega N., Stuart A.A., Vonk A. Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. PNAS. 99:2002;5476-5480.
Hecker M., Tyler C.R., Hoffmann M., Maddix S., Karbe L. Plasma biomarkers in fish provide evidence for endocrine modulation in the Elbe River, Germany. Environ. Sci. Technol. 36:2002;2311-2321.
Huber W. Ecotoxicological relevance of atrazine in aquatic systems. Environ. Toxicol. Chem. 12:1993;1865-1881.
Ishibashi H., Tachibana K., Tsuchimoto M., Soyano K., Ishibashi Y., Nagae M., Kohra S., Takao Y., Tominaga N., Arizono K. In vivo testing system for determining the estrogenic activity of endocrine-disrupting chemicals (EDCs) in goldfish (Carassius auratus). J. Health Sci. 47:2001;213-218.
Janz D.M., Van Der Kraak G. Suppression of apoptosis by gonadotropin, 17β-estradiol, and epidermal growth factor in rainbow trout preovulatory ovarian follicles. Gen. Comp. Endocrinol. 105:1997;186-193.
Janz D.M., McMaster M.E., Munkittrick K.R., Van Der Kraak G. Elevated ovarian follicular apoptosis and heat shock protein-70 expression in white sucker exposed to bleached kraft pulp mill effluent. Toxicol. Appl. Pharmacol. 147:1997;391-398.
Kestemont P. Etude du cycle reproducteur du goujon, Gobio gobio L. 1. Variation saisonnière dans l'histologie de l'ovaire. J. Appl. Ichthyol. 3:1987;145-157.
Kettles M.A., Browning S.R., Prince T.S., Horstman S.W. Triazine herbicide exposure and breast cancer incidence: an ecological study of Kentucky counties. Environ. Health Perspect. 105:1997;1222-1227.
Langeron, M., 1942. Précis de microscopie technique- expérimentation-diagnostic. Masson et Cie, Paris.
Lee K.E., Blazer V.S., Denslow N.D., Goldstein R.M., Talmage P.J. Use of biological characteristic of common carp (Cyprinus carpio) to indicate exposure to hormonally active agents in selected minnesota streams, 1999. Water-Resources Invest. Rep. 00-4202:2000;1-47.
Moore A., Waring C.P. Mechanistic effects of a triazine pesticide on reproductive endocrine function in mature male Atlantic salmon (Salmo salar L.) parr. Pest. Biochem. Physiol. 62:1998;41-50.
Neškovic N., Elezovic I., Karan V., Poleksic V., Budimir M. Acute and subacute toxicity of atrazine to carp (Cyprinus carpio L.). Ecotoxicol. Environ. Saf. 25:1993;173-182.
Oulmi Y., Negele R.D., Braunbeck T. Segment specificity of the cytological response in rainbow trout (Oncorhynchus mykiss) renal tubules following prolonged exposure to sublethal concentrations of atrazine. Ecotoxicol. Environ. Saf. 32:1995;39-50.
Rinchard J., Kestemont P. Comparative study of reproductive biology in single - and multiple - spawner cyprinid fish. Morphological and histological features. J. Fish Biol. 49:1996;883-894.
Sanderson J.T., Seinen W., Giesy J.P., van den Berg M. 2-Chloro-s-triazine herbicides induce aromatase (CYP19) activity in H295R human adrenocortical carcinoma cells: a novel mechenism for estrogenicity. Toxicol. Sci. 54:2000;121-127.
Sanderson J.T., Letcher R.J., Heneweer M., Giesy J.P., van den Berg M. Effects of chloro-s-triazine herbicides and metabolites on aromatase activity in various human cell lines and on vitellogenin production in male carp hepatocytes. Environ. Health Perspect. 109:2001;1027-1031.
Simpson E.R., Mahendroo M.S., Means G.D., Kilgore M.W., Hinshelwood M.M., Graham-Laurence S., Amarneh B., Ito Y., Fisher C.R., Michael M.D., Mendelson C.R., Bulun S.E. Aromatase cytochrome P450, the enzyme responsible for estrogen byosinthesis. Endocrinol. Rev. 15:1994;342-354.
Sohoni P., Tyler C.R., Hurd K., Caunter J., Hetheridge M., Williams T., Woods C., Evans M., Toy R., Gargas M., Sumpter J.P. Reproductive effects of long-term exposure to bisphenol A in the fathead minnow (Pimephales promelas). Environ. Sci. Technol. 35:2001;2917-2925.
Solomon K.R., Baker D.B., Richards R.P., Dixon K.R., Klaine S.J., La Point T.W., Kendall R.R., Weisskopf C.P., Giddings J.M., Giesy J.P., Hall L.W. Jr., Williams W.M. Ecological risks assessment of atrazine in North America surface waters. Environ. Toxicol. Chem. 15:1996;31-76.
Stoker T.E., Robinette C.L., Cooper R. Maternal exposure to atrazine during lactation suppresses suckling-induced prolactin release and results in prostatitis in the adult offspring. Toxicol. Sci. 52:1999;68-79.
Sumpter J.P., Jobling S. Vitellogenesis as a biomarker for estrogenicity contamination of the aquatic environment. Environ. Health Perspect. 103(Suppl. 7):1995;173-178.
Tavera-Mendoza L., Ruby S., Brousseau P., Cyr M., Marcogliese D. Reponse of the amphibian tadpole (Xenopus laevis) to atrazine during sexual differentiation of the testis. Environ. Toxicol. Chem. 21:2002;527-531.
Toppari, J., Larsen, J.C., Christiansen, P., Giwercman, A., Grandjean, P., Guillette, L.J., Jr., Jegou, B., Jensen, T.K., Jouannet, P., Keiding, N., Leffers, H., McLachlan, J.A., Meyer, O., Muller, J., Rajpert-Demeyts, E., Scheike, T., Sharpe, R., Sumpter, J., Skakkebaek, N.E., 1995. Male reproductive health and environmental chemicals with estrogenic effects. Ministry of Environment and Energy, Denmark, Danish Environmental Protection Agency, Miljoprojekt nr. 290.
Trentacoste S.V., Friedmann A.S., Youker R.T., Breckenridge C.B., Zirkin B.R. Atrazine effects on testosterone levels and androgen-dependent reproductive organs in peripubertal male rats. J. Androl. 22:2001;142-148.
Tyler C.R., Sumpter J.P., Kawauchi H., Swanson P. Involvement of gonadotropin in the uptake of vitellogenin into vitellogenic oocytes. Gen. Comp. Endocrinol. 84:1991;291-299.
Tyler C.R., Jobling S., Sumpter J.P. Endocrine disruption in wildlife: a critical review of the evidence. Crit. Rev. Toxicol. 28:1998;319-361.
Tyler C.R., van Aerle R., Hutchinson T.H., Maddix S., Trip H. An in vivo testing system for endocrine disruptors in fish early life stages using induction of vitellogenin. Environ. Toxicol. Chem. 18:1999;337-347.
Vos J.G., Dybing E., Greim H.A., Lagefoged O., Lambré C., Tarazona J.V., Brandt I., Vethaak A.D. Health effects on endocrine-disrupting chemicals on wildlife, with special reference to European situation. Crit. Rev. Toxicol. 30:2000;71-133.
