Effects of 17 β-estradiol exposure on Xenopus laevis gonadal histopathology

Environmental Toxicology and Chemistry

Volumn 29, Issue 5, 2010, Pages 1091-1105

  Wolf, Jeffrey C ^a   Lutz, Ilka ^b   Kloas, Werner ^b,c   Springer, Timothy A ^d   Holden, Larry R ^e   Krueger, Henry O ^d   Hosmer, Alan J ^f  

^a EXPERIMENTAL PATHOLOGY LABORATORIES INC   (United States)

^b LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

^c HUMBOLDT UNIVERSITY   (Germany)

^d Wildlife International Ltd   (United States)

^e Sielken and Associates   (United States)

^f SYNGENTA CROP PROTECTION   (United States)

Author keywords

Amphibians; Endocrine disruption; Estradiol; Frogs; Xenopus laevis

Indexed keywords

EFFECTIVE CONCENTRATION; ENDOCRINE DISRUPTION; ENDOCRINE DISRUPTOR; ENVIRONMENTAL CONTAMINANT; ESTROGENIC EFFECT; LABORATORY PRACTICES; MICROSCOPIC EVALUATION; MORPHOLOGIC CHANGES; NATURAL ESTROGEN; REPRODUCIBILITIES; XENOPUS LAEVIS;

BIOASSAY;

EXPERIMENTS;

ESTRADIOL; WATER POLLUTANT;

BIOASSAY; CHEMICAL POLLUTANT; CONCENTRATION (COMPOSITION); ENDOCRINE DISRUPTOR; ESTROGENIC COMPOUND; EXPERIMENTAL STUDY; FROG; HISTOPATHOLOGY; MORPHOLOGY; PHYSIOLOGICAL RESPONSE; POLLUTION EXPOSURE; SEX HORMONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EMBRYO; EXPOSURE; FEMALE; GENOTYPE; GONADAL DISEASE; GOOD LABORATORY PRACTICE; HISTOPATHOLOGY; MALE; NONHUMAN; PEER REVIEW; PHENOTYPE; PRIORITY JOURNAL; REPRODUCIBILITY; SEMINIFEROUS TUBULE; STATISTICAL ANALYSIS; TESTIS; VALIDATION STUDY; XENOPUS LAEVIS; ANIMAL; DISORDER OF SEX DEVELOPMENT; DRUG EFFECTS; LARVA; OVARY; PATHOLOGY; TOXICITY; WATER POLLUTANT; XENOPUS;

ANIMALS; ESTRADIOL; FEMALE; LARVA; MALE; OVARY; REPRODUCIBILITY OF RESULTS; SEX REVERSAL, GONADAL; TESTIS; WATER POLLUTANTS, CHEMICAL; XENOPUS; DISORDERS OF SEX DEVELOPMENT;

AMPHIBIA; ANURA; XENOPUS LAEVIS;

EID: 77953593980     PISSN: 07307268     EISSN: 15528618     Source Type: Journal    
DOI: 10.1002/etc.133     Document Type: Article

References (55)

1. Eertmans F, Dhooge W, Stuyvaert S, Comhaire F. 2003. Endocrine disruptors: Effects on male fertility and screening tools for their assessment. Toxicol In Vitro 17:515-524.
2. Lutz I, Kloas W. 1999. Amphibians as a model to study endocrine disruptors: I.Environmental pollution and estrogen receptor binding. Sci Total Environ 225:49-57.
3. Khanal SK, Xie B, Thompson ML, Sung S, Ong SK, Van Leeuwent J. 2006. Fate, transport, and biodegradation of natural estrogens in the environment and engineered systems. Environ Sci Technol 40:6537-6546.
4. Hanselman TA, Graetz DA, Wilkie AC. 2003. Manure-borne estrogens as potential environmental contaminants: A review. Environ Sci Technol 37:5471-5478.
5. Coady KK, Murphy MB, Villeneuve DL, Hecker M, Jones PD, Carr JA, Solomon KR, Smith EE, Van Der Kraak G, Kendall RJ, Giesy JP. 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.
6. Hecker M, Giesy JP, Jones PD, Jooste AM, Carr JA, Solomon KR, Smith EE, Van Der Kraak G, Kendall RJ, du Preez L., 2004. Plasma sex steroid concentrations and gonadal aromatase activities inAfrican clawed frogs (Xenopus laevis) from South Africa. Environ Toxicol Chem 23:1996-2007.
7. Hecker M, Park J-W, Murphy MB, Jones PD, Solomon KR, Van Der Kraak G, Carr JA, Smith EE, du Preez L, Kendall RJ, Giesy JP. 2005. 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). Toxiol Sci 86:273-280.
8. Bögi C, Levy G, Lutz I, Kloas W. 2002. Functional genomics and sexual differentiation in amphibians.Comp Biochem Physiol B 133:559-570.
9. Urbatzka R, Bottero S, Mandich A, Lutz I, Kloas W. 2007. Endocrine disrupting chemicals (EDC) with (anti)estrogenic and (anti)androgenic modes of action affecting reproductive biology of Xenopus laevis: I. Effects on sex steroid levels and biomarker expression. Comp Biochem Phys C 144:310-318.
10. Iwabuchi J, Wako S, Tanaka T, Ishikawa A, Yoshida Y, Miyata S. 2007. Analysis of the p450 aromatase gene expression in the Xenopus brain and gonad. J Steroid Biochem Mol Biol 107:149-155.
11. Urbatzka R, Lutz I, Kloas W. 2007b. Aromatase, steroid-5-alpha-reductase type 1 and type 2 mRNA expression in gonads and in brain of Xenopus laevis during ontogeny. Gen Comp Endocrinol 153:280-288.
12. Oka T, Mitsui N, Hinago M, Miyahara M, Fujii T, Tooi O, Santo N, Urushitani H, Iguchi T, Hanaoka Y, Mikami H. 2006. All ZZ male Xenopus laevis provides a clear sex-reversal test for feminizing endocrine disruptors. Ecotoxicol Environ Saf 63:236-243.
13. Oka T, Tooi O, Mitsui N, Miyahara M, Ohnishi Y, Takase M, Kashiwagi A, Shinkai T, Santo N, Iguchi T. 2008. Effect of atrazine on metamorphosis and sexual differentiation in Xenopus laevis. Aquat Toxicol 87:215-226.
14. Matsumura N, Ishibashi H, Hirano M, Nagao Y, Watanabe N, Shiratsuchi H, Kai T, Nishimura T, Kashiwagi A, Arizono K. 2005. Effects of nonylphenol and triclosan on production of plasma vitellogenin and testosterone in male South African clawed frogs (Xenopus laevis). Biol Pharm Bull 28:1748-1751.
15. Cong L, Qin ZF, Xiang-Ning J, Yang L, Zhou J-M, Xu X-B. 2006. Xenopus laevis is a potential alternative model animal species to study reproductive toxicity of phytoestrogens. Aquat Toxicol 77:250-256.
16. Levy G, Lutz I, Kruger A, Kloas W. 2004. Bisphenol A induces feminization in Xenopus laevis tadpoles. Environ Res 94:102-111.
17. Pickford DB, Hetheridge MJ, Caunter JE, Hall AT, Hutchinson TH. 2003. Assessing chronic toxicity of bisphenol A to larvae of the African clawed frog (Xenopus laevis) in a flow-through exposure system. Chemosphere 53:223-235.
18. Kloas W, Lutz I, Einspanier R. 1999. Amphibians as a model to study endocrine disruptors: II. Estrogenic activity of environmental chemicals in vitro and in vivo. Sci Total Environ 225:59-68.
19. Carr JA, Gentles A, Smith EE, Goleman WL, Urquidi LJ, Thuett K, Kendall RJ, Giesy JP, Gross TS, Solomon KR, Van Der Kraak G. 2003. Response of larval Xenopus laevis to atrazine: Assessment of growth, metamorphosis, and gonadal and laryngeal morphology. Environ Toxicol Chem 22:396-405.
20. Coady KK, Murphy MB, Villenueve DL, Hecker M, Jones PD, Carr JA, Solomon KR, Smith EE, Van Der Kraak G, Kendall RJ, Giesy JP. 2004. Effects of atrazine on metamorphosis, growth, and gonadal development in the green frog (Rana clamitans). J Toxicol Env Heal A 67:941-957.
21. Hayes TB, Collins A, Lee M, Mendoza M, Noriega N, Stuart AA, Vonk A. 2002. Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc Natl Acad Sci USA 99:5476-5480.
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, Stuart AA, Mendoza M, Collins A, Noriega N, Vonk A, Johnston G, Liu R, Kpodzo D. 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 (17 β-estradiol): Support for the demasculization/feminization hypothesis. Environ Health Perspect 114:134-141.
24. Cevasco A, Urbatzka R, Bottero S, Massari A, Pedemonte F, Kloas W, Mandich A. 2008. Endocrine disrupting chemicals (EDC) with (anti)estrogenic and (anti)androgenic modes of action affecting reproductive biology of Xenopus laevis: II. Effects on gonad histomorphology. Comp Biochem Phys C 147:241-251.
25. Jooste AM, Du Preez LH, Carr JA, Giesy JP, Gross TS, Kendall RJ, Smith EE, Van Der Kraak GL, Solomon KR. 2005. Gondal development of larval male Xenopus laevis exposed to atrazine in outdoor microcosms. Environ Sci Technol 39:5255-5261.
26. MacKenzie CA, Berrill M, Metcalfe C, Pauli BD. 2003. Gonadal differentiation in frogs exposed to estrogenic and antiestrogenic compounds. Environ Toxicol Chem 22:2466-2475.
27. 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.
28. Park BJ, Kidd K. 2005. Effects of the synthetic estrogen ethinylestradiol on the early life stages of mink frogs and green frogs in the wild and in situ. Environ Toxicol Chem 24:2027-2036.
29. Pettersson I, Arukwe A, Lundstedt-Enkel K, Mortensen AS, Berg C. 2006. Persistent sex-reversal and oviducal agenesis in adult Xenopus (Silurana) tropicalis frogs following larval exposure to the environmental pollutant ethynylestradiol. Aquat Toxicol 79:356-365.
30. Kloas W, Lutz I. 2006. Amphibians as model to study endocrine disruptors. J Chromatogr A 1130:16-27.
31. Murphy MB, Hecker M, Coady KK, Tompsett AR, Jones PD, DuPreez LH, Everson GJ, Solomon KR, Carr JA, Smith EE, Kendall RJ, Van Der Kraak G, Giesy JP. 2006. Atrazine concentrations, gonadal gross morphology and histology in ranid frogs collected in Michigan agricultural areas. Aquat Toxicol 76:230-245.
32. Solomon KR, Carr JA, Du Preez LH, Giesy JP, Kendall RJ, Smith EE, Van Der Kraak GJ. 2008. Effects of atrazine on fish, amphibians, and aquatic reptiles: A critical review. Crit Rev Toxicol 38:721-772.
33. Hecker M, Murphy MB, Coady KK, Villeneuve DL, Jones PD, Carr JA, Solomon KR, Smith EE, Van Der Kraak G,Gross T,Du Preez L, Kendall RJ, Giesy JP. 2006. Terminology of gonadal anomalies in fish and amphibians resulting from chemical exposures. Rev Environ Contam Toxicol 187:103-131.
34. Kloas W, Lutz I, Springer T, Krueger H, Wolf J, Holden L, Hosmer A. 2009. Does atrazine influence larval development and sexual differentiation in Xenopus laevis? Toxicol Sci 107:376-384.
35. American Society for Testing Materials. 2003. Standard guide for conducting acute toxicity tests on test material with fishes, macro-invertebrates, and amphibians. E729-96 (2007) In Annual Book of Standards, Vol.11 06,West Conshohocken, PA, p 22.
36. Crissman JW, Goodman DG, Hildebrandt PK, Maronpot RR, Prater DA, Riley JH, Seaman WJ, Thake DC. 2004. Best practices guideline: Toxicologic histopathology. Toxicol Pathol 32:126-131.
37. Code of Federal Regulations. 2003. Federal Insecticide, Fungicide and RodenticideAct: Good Laboratory Practice Standards. 40 CFR Part 160. U.S. Government Printing Office, Washington, DC.
38. Ministry of Health, Labour and Welfare. 1977. GLP Standard Ordinance for Nonclinical Laboratory Studies on Safety of Drugs, Ordinance 21. Tokyo, Japan.
39. Organization for Economic Co-operation and Development. 1997. Principles of Good Laboratory Practice and Compliance Monitoring, Number 1, ENV/MC/CHEM(98)17. Paris, France.
40. Lutz I, Kloas W, Springer TA, Holden LR, Wolf JC, Krueger HO, Hosmer AJ. 2008. Development, standardization and refinement of procedures used for the evaluation of endocrine active compounds (EAC) on the development and sexual differentiation of Xenopus laevis. Anal Bioanal Chem 390:2031-2048.
41. De Boever P, Demare W, Vanderperren E, Cooreman K, Bossier P, Verstraete W. 2001. Optimization of a yeast estrogen screen and its applicability to study the release of estrogenic isoflavones from a soygerm powder. Environ Health Perspect 109:691-697.
42. Thomas KV, Hurst MR, Matthiessen P, McHugh M, Smith A, Waldock MJ. 2002. An assessment of in vitro androgenic activity and the identification of environmental androgensin United Kingdom estuaries. Environ Toxicol Chem 21:1456-1461.
43. Nieuwkoop PD, Faber J. 1994. Normal Table of Xenopus laevis (Daudin). Garland Publishing, New York, NY, USA.
44. The Society of Toxicologic Pathologists. 1991. Peer review in toxico-logic pathology: Some recommendations. Toxicol Pathol 19:290-292.
45. The Society of Toxicologic Pathologists. 1997. Documentation of pathology peer review. Toxicol Pathol 25:655.
46. Snedecor GW, Cochran WG. 1980. Statistical Methods, 7th ed. Iowa State University Press, Ames, IA, USA.
47. Manly BFJ. 1997. Randomization, Bootstrap, and Monte Carlo Methods in Biology, 2nd ed. Chapman & Hall, London, UK.
48. Piegorsch WW, Bailer AJ. 1997. Statistics for Environmental Biology and Toxicology, Chapman & Hall, London, UK.
49. Agresti A. 2002. Categorical Data Analysis, 2nd ed. Wiley-Interscience, Hoboken, NJ, USA.
50. Van Gansen P, Schram A. 1972. Evolution of the nucleoli during oogenesis in Xenopus laevis studied by electron microscopy. J Cell Sci 10:339-367.
51. Schmid M, Steinlein C. 1991. Chromosome handling in amphibia. Chromosoma 101:123-132.
52. Smith EE, Du Preez L,Gentles A, Solomon KR, Tandler B, Carr JA, Van Der Kraak G, Kendall RJ, Giesy JP, Gross T. 2005. Assessment of laryngeal muscle and testicular cell types in Xenopus laevis (Anura pipidae) inhabiting maize and non-maize growing areas of South Africa. Afr J Herpetol 54:69-76.
53. Du Preez HH, Kunene N,Hanner R, Giesy JP, Hosmer AJ, Solomon KR, Van Der Kraak GJ. 2009. Population-specific incidence of testicular ovarian follicles in Xenopus laevis from South Africa: A potential issue in endocrine testing. Aquat Toxicol 95:10-16.
54. Villalpando I, Merchant-Larios H. 1990. Determination of the sensitive stages for gonadal sex-reversal in Xenopus laevis tadpoles. Int J Dev Biol 34:281-285.
55. Ogielska M, Kotusz A. 2004. Pattern and rate of ovary differentiation with referenceto somatic development in anuran amphibians.J Morphol 259:41-54.