Low levels of the herbicide atrazine alter sex ratios and reduce metamorphic success in Rana pipiens tadpoles raised in outdoor mesocosms

Environmental Health Perspectives

Volumn 118, Issue 4, 2010, Pages 552-557

  Langlois, Valérie S ^a   Carew, Amanda C ^a   Pauli, Bruce D ^b   Wade, Michael G ^c   Cooke, Gerard M ^d   Trudeau, Vance L ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b ENVIRONMENT CANADA   (Canada)

^c Environmental Health Sciences Bureau   (Canada)

^d TOXICOLOGY RESEARCH DIVISION   (Canada)

Author keywords

5 reductase; Amphibians; Aromatase; Atrazine; Enzyme activity; Feminization; Gonadal development; Metamorphosis; Northern leopard frog; Real time RT PCR

Indexed keywords

AROMATASE; ATRAZINE; DEIODINASE TYPE 3; ESTROGEN RECEPTOR ALPHA; ETHINYLESTRADIOL; MESSENGER RNA; OXIDOREDUCTASE; STEROID 5BETA REDUCTASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; CHEMICAL ANALYSIS; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; FEMINIZATION; FROG; GENE EXPRESSION; GENETIC ANALYSIS; GONAD DEVELOPMENT; MESOCOSM; METAMORPHOSIS; NONHUMAN; OOCYTE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEX DIFFERENCE; TADPOLE;

ANIMALS; ATRAZINE; FEMALE; HERBICIDES; LARVA; MALE; METAMORPHOSIS, BIOLOGICAL; RANA PIPIENS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEX RATIO;

AMPHIBIA; ANIMALIA; RANA PIPIENS;

EID: 77951671436     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.0901418     Document Type: Article

References (54)

1. Aranda A, Pascual A. 2001. Nuclear hormone receptors and gene expression. Physiol Rev 81:1269-1304.
2. ASTM. 2000. Standard Guide for Conducting Acute Toxicity Test with Fishes, Macroinvertebrates and Amphibians. West Conhohocken, PA: American Society for Testing and Materials.
3. Brodeur JC, Svartz G, Perez-Coll CS, Marino DJ, Herkovits J. 2009. Comparative susceptibility to atrazine of three developmental stages of Rhinella arenarum and influence on metamorphosis: non-monotonous acceleration of the time to climax and delayed tail resorption. Aquat Toxicol 91:161-170.
4. Carr JA, Gentles A, Smith EE, Goleman WL, Urquidi LJ, Thuett K, et al. 2003. Response of larval Xenopus laevis to atrazine: assessment of growth, metamorphosis, and gonadal and laryngeal morphology. Environ Toxicol Chem 22:396-405.
5. Chardard D, Dournon C. 1999. Sex reversal by aromatase inhibitor treatment in the newt Pleurodeles waltl. J Exp Zool 283:43-50.
6. Coady K, Murphy M, Villeneuve D, Hecker M, Jones P, Carr J, et al. 2004. Effects of atrazine on metamorphosis, growth, and gonadal development in the green frog (Rana clamitans). J Toxicol Environ Health A 67:941-957.
7. Coady KK, Murphy MB, Villeneuve DL, Hecker M, Jones PD, Carr JA, et al. 2005. Effects of atrazine on metamorphosis, growth, laryngeal and gonadal development, aromatase activity, and sex steroid concentrations in Xenopus laevis. Ecotoxicol Environ Saf 62:160-173.
8. Connor K, Howell J, Chen I, Liu H, Berhane K, Sciarretta C, et al. 1996. Failure of chloro-s-triazine-derived compounds to induce estrogen receptor-mediated responses in vivo and in vitro. Fundam Appl Toxicol 30:93-101.
9. Croteau MC. 2009. Chronic exposure to UV-B radiation and 4-tert-octylphenol disrupt metamorphosis and the thyroid system of Northern leopard frog (Rana pipiens) tadpoles [PhD Thesis]. Ottawa, Ontario, Canada:University of Ottawa.
10. Diana SG, Resetarits WJ, Schaeffer DJ, Beckmen KB, Beasley VR. 2000. Effects of atrazine on amphibian growth and survival in artificial aquatic communities. Environ Toxicol Chem 19:2961-2967.
11. Duarte P, Hogan NS, Lean D, Trudeau VL. 2006. Regulation and endocrine disruption of aromatase in the brain of developing Rana pipiens [Abstract]. In: 27th Annual Meeting of the Society of Environmental Toxicology and Chemistry of North America, 5-9 November 2006, Montreal, Québec, Canada. Abstract 559. Available: http://montreal.setac.org/montreal/pdf/SETAC_abstractbook_2006.pdf [accessed 3 March 2010].
12. Duarte-Guterman P, Langlois VS, Hodgkinson K, Pauli BD, Cooke GM, Wade MG, et al. 2010. The aromatase inhibitor fadrozole and the 5-reductase inhibitor finasteride affect gonadal differentiation and gene expression in the frog Silurana tropicalis. Sex Dev 3:333-341
13. Fan W, Yanase T, Morinaga H, Gondo S, Okabe T, Nomura M, et al. 2007. Herbicide atrazine activates SF-1 by direct affinity and concomitant co-activators recruitments to induce aromatase expression via promoter II. Biochem Biophys Res Commun 355:1012-1018.
14. Filby AL, Thorpe KL, Maack G, Tyler CR. 2007. Gene expression profiles revealing the mechanisms of anti-androgen-and estrogen-induced feminization in fish. Aquat Toxicol 81:219-231.
15. Freeman JL, Rayburn AL. 2005. Developmental impact of atrazine on metamorphing Xenopus laevis as revealed by nuclear analysis and morphology. Environ Toxicol Chem 24:1648-1653.
16. Garavini C, Cristofori M. 1984. The effect of 5-alpha-dihydrotestosterone and 5-beta-dihydrotestosterone on erythropoiesis of the newt, Triturus cristatus carnifex (Laur). Gen Comp Endocrinol 54:188-193.
17. Goleman WL, Carr JA, Anderson TA. 2002. Environmentally relevant concentrations of ammonium perchlorate inhibit thyroid function and alter sex ratios in developing Xenopus laevis. Environ Toxicol Chem 21:590-597.
18. Gosner K. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183-190.
19. Graymore M, Stagnitti F, Allinson G. 2001. Impacts of atrazine in aquatic ecosystems. Environ Int 26:483-495.
20. Hayes T, Collins A, Lee M, Mendoza M, Noriega N, Stuart AA, et al. 2002a. Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc Natl Acad Sci USA 99:5476-5480.
21. Hayes T, Haston K, Tsui M, Hoang A, Haeffele C, Vonk A. 2002b. Herbicides: feminization of male frogs in the wild. Nature 419:895-896.
22. Hayes T, Haston K, Tsui M, Hoang A, Haeffele C, Vonk A. 2003. Atrazine-induced hermaphroditism at 0.1 ppb in American leopard frogs (Rana pipiens): laboratory and field evidence. Environ Health Perspect 111:568-575.
23. Hayes TB. 2004. There is no denying this: defusing the confusion about atrazine. BioScience 54:1138-1149.
24. Hayes TB, Stuart AA, Mendoza M, Collins A, Noriega N, Vonk A, et al. 2006. Characterization of atrazine-induced gonadal malformations in African clawed frogs (Xenopus laevis) and comparisons with effects of an androgen antagonist (cyproterone acetate) and exogenous estrogen (17β-estradiol): support for the demasculinization/feminization hypothesis. Environ Health Perspect 114(suppl 1):134-141.
25. Hecker M, Kim WJ, Park JW, Murphy MB, Villeneuve D, Coady KK, et al. 2005a. Plasma concentrations of estradiol and testosterone, gonadal aromatase activity and ultrastructure of the testis in Xenopus laevis exposed to estradiol or atrazine. Aquat Toxicol 72:383-396.
26. Hecker M, Park JW, Murphy MB, Jones PD, Solomon KR, Van Der Kraak G, et al. 2005b. Effects of atrazine on CYP19 gene expression and aromatase activity in testes and on plasma sex steroid concentrations of male African clawed frogs (Xenopus laevis). Toxicol Sci 86:273-280.
27. Heneweer M, van den Berg M, Sanderson JT. 2004. A comparison of human H295R and rat R2C cell lines as in vitro screening tools for effects on aromatase. Toxicol Lett 146:183-194.
28. 3 exposure on thyroid hormone-and estrogen-responsive genes in Rana pipiens. Gen Comp Endocrinol 154:5-15.
29. Hogan NS, Duarte P, Wade MG, Lean DR, Trudeau VL. 2008. Estrogenic exposure affects metamorphosis and alters sex ratios in the Northern leopard frog (Rana pipiens): identifying critically vulnerable periods of development. Gen Comp Endocrinol 156:515-523.
30. Holloway AC, Anger DA, Crankshaw DJ, Wu M, Foster WG. 2008. Atrazine-induced changes in aromatase activity in estrogen sensitive target tissues. J Appl Toxicol 28:260-270.
31. Hua WY, Bennett ER, Maio XS, Metcalfe CD, Letcher RJ. 2006. Seasonality effects on pharmaceuticals and S-triazine herbicides in wastewater effluent and surface water from the Canadian side of the upper Detroit River. Environ Toxicol Chem 25:2356-2365.
32. Kloas W, Lutz I, Springer T, Krueger H, Wolf J, Holden L, et al. 2009. Does atrazine influence larval development and sexual differentiation in Xenopus laevis? Toxicol Sci 107:376-384.
33. Kondo KH, Kai MH, Setoguchi Y, Eggertsen G, Sjoblom P, Setoguchi T, et al. 1994. Cloning and expression of cDNA of human delta(4)-3-oxosteroid 5-beta-reductase and substrate-specificity of the expressed enzyme. Eur J Biochem 219:357-363.
34. Kornilovskaya IN, Gorelaya MV, Usenko VS, Gerbilsky LV, Berezin VA. 1996. Histological studies of atrazine toxicity on the thyroid gland in rats. Biomed Environ Sci 9:60-66.
35. Langlois VS, Duarte-Guterman P, Ing S, Pauli BD, Cooke GM, Trudeau VL. 2010. Fadrozole and finasteride exposures modulate sex steroid- and thyroid hormone-related gene expression in Silurana (Xenopus) tropicalis early larval development. Gen Comp Endocrinol 166:417-427.
36. Langlois VS, Zhang D, Cooke G, Trudeau VL. 2009. Evolution of steroid 5-α-reductases and comparison of their function with 5-β-reductase. Gen Comp Endocrinol; doi:10.1016/j.ygcen.2009.08.004 [Online 15 August 2009].
37. Larson DL, McDonald S, Fivizzani AJ, Newton WE, Hamilton SJ. 1998. Effects of the herbicide atrazine on Ambystoma tigrinum metamorphosis: duration, larval growth, and hormonal response. Physiol Zool 71:671-679.
38. Lenkowski JR, Reed JM, Deininger L, McLaughlin KA. 2008. Perturbation of organogenesis by the herbicide atrazine in the amphibian Xenopus laevis. Environ Health Perspect 116:223-230.
39. Lephart ED. 1996. A review of brain aromatase cytochrome P450. Brain Res Brain Res Rev 22:1-26.
40. Levy G, Lutz I, Kruger A, Kloas W. 2004. Bisphenol-A induces feminization in Xenopus laevis tadpoles. Environ Res 94:102-111.
41. Lutz I, Blodt S, Kloas W. 2005. Regulation of estrogen receptors in primary cultured hepatocytes of the amphibian Xenopus laevis as estrogenic biomarker and its application in environmental monitoring. Comp Biochem Physiol C Toxicol Pharmacol 141:384-392.
42. Manzon RG, Denver RJ. 2004. Regulation of pituitary thyrotropin gene expression during Xenopus metamorphosis: negative feedback is functional throughout metamorphosis. J Endocrinol 182:273-285.
43. Navarro-Martin L, Blazquez M, Piferrer F. 2009. Masculinization of the European sea bass (Dicentrarchus labrax) by treatment with an androgen or aromatase inhibitor involves different gene expression and has distinct lasting effects on maturation. Gen Comp Endocrinol 160:3-11.
44. Oka T, Tooi O, Mitsui N, Miyahara M, Ohnishi Y, Takase M, et al. 2008. Effect of atrazine on metamorphosis and sexual differentiation in Xenopus laevis. Aquat Toxicol 87:215-226.
45. Orton F, Carr JA, Handy RD. 2006. Effects of nitrate and atrazine on larval development and sexual differentiation in the Northern leopard frog Rana pipiens. Environ Toxicol Chem 25:65-71.
46. Richard-Mercier N, Dorizzi M, Desvages G, Girondot M, Pieau C. 1995. Endocrine sex reversal of gonads by the aromatase inhibitor letrozole (CGS 20267) in Emys orbicularis, a turtle with temperature-dependent sex determination. Gen Comp Endocrinol 100:314-326.
47. Roberge M, Hakk H, Larsen G. 2004. Atrazine is a competitive inhibitor of phosphodiesterase but does not affect the estrogen receptor. Toxicol Lett 154:61-68.
48. Shi Y-B. 1999. Amphibian Metamorphosis. New York:Wiley-Liss.
49. Simpson ER, Mahendroo MS, Means GD, Kilgore MW, Hinshelwood MM, Graham-Lorence S, et al. 1994. Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr Rev 15:342-355.
50. Solomon KR, Carr JA, Du Preez LH, Giesy JP, Kendall RJ, Smith EE, et al. 2008. Effects of atrazine on fish, amphibians, and aquatic reptiles: a critical review. Crit Rev Toxicol 38:721-772.
51. Stoker TE, Laws SC, Guidici DL, Cooper RL. 2000. The effect of atrazine on puberty in male Wistar rats: an evaluation in the protocol for the assessment of pubertal development and thyroid function. Toxicol Sci 58:50-59.
52. Storrs SI, Kiesecker JM. 2004. Survivorship patterns of larval amphibians exposed to low concentrations of atrazine. Environ Health Perspect 112:1054-1057.
53. Tavera-Mendoza L, Ruby S, Brousseau P, Fournier M, Cyr D, Marcogliese D. 2002a. Response of the amphibian tadpole (Xenopus laevis) to atrazine during sexual differentiation of the testis. Environ Toxicol Chem 21:527-531.
54. Tavera-Mendoza L, Ruby S, Brousseau P, Fournier M, Cyr D, Marcogliese D. 2002b. Response of the amphibian tadpole Xenopus laevis to atrazine during sexual differentiation of the ovary. Environ Toxicol Chem 21:1264-1267.