Effect of atrazine on metamorphosis and sexual differentiation in Xenopus laevis

Aquatic Toxicology

Volumn 87, Issue 4, 2008, Pages 215-226

  Oka, Tomohiro ^a   Tooi, Osamu ^a   Mitsui, Naoko ^a   Miyahara, Maki ^a   Ohnishi, Yuta ^a   Takase, Minoru ^b   Kashiwagi, Akihiko ^b   Shinkai, Tadashi ^c   Santo, Noriaki ^d   Iguchi, Taisen ^e  

^a IDEA Consultants Inc ^*  (Japan)

^b HIROSHIMA UNIVERSITY   (Japan)

^c TOKYO METROPOLITAN INSTITUTE OF GERONTOLOGY   (Japan)

^d FUKUYAMA UNIVERSITY   (Japan)

^e OKAZAKI INSTITUTE FOR INTEGRATIVE BIOSCIENCE   (Japan)

Author keywords

17 estradiol; All ZZ male; Aromatase; Atrazine; Hepatocyte culture; Hermaphrodite; Vitellogenin; Xenopus laevis

Indexed keywords

AROMATASE; ATRAZINE; ESTRADIOL; HERBICIDE; MESSENGER RNA; TOXIC SUBSTANCE; VITELLOGENIN;

ATRAZINE; ENDOCRINE DISRUPTOR; ENZYME ACTIVITY; FROG; HERMAPHRODITE; LARVA; MALE; METAMORPHOSIS; POLLUTION EFFECT; REPRODUCTION; SEXUAL MATURITY; WILD POPULATION;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; FEMALE; GONAD; IN VITRO STUDY; LARVA; LIVER CELL; MALE; METAMORPHOSIS; NONHUMAN; PRIORITY JOURNAL; REPRODUCTIVE TOXICITY; SEX DIFFERENTIATION; TADPOLE; XENOPUS LAEVIS;

AMPHIBIA; XENOPUS LAEVIS;

EID: 43049150090     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2008.02.009     Document Type: Article

References (65)

1. R.A. Alford P.M. Dixon J.H. Pechmann Ecology. Global amphibian population declines Nature 412 2001 499 500
2. J.W. Allran W.H. Karasov Effects of atrazine and nitrate on northern leopard frog ( Rana pipiens ) larvae exposed in the laboratory from posthatch through metamorphosis Environ. Toxicol. Chem. 19 2000 2850 2855
3. C. Bögi G. Levy I. Lutz W. Kloas Functional genomics and sexual differentiation in amphibians Comp. Biochem. Physiol. B 133 2002 559 570
4. C. Bögi J. Schwaiger H. Ferling U. Mallow C. Steineck F. Sinowatz W. Kalbfus R.D. Negele I. Lutz W. Kloas Endocrine effects of environmental pollution on Xenopus laevis and Rana temporaria Environ. Res. 93 2003 195 201
5. C. Carey C.J. Bryant Possible interrelations among environmental toxicants, amphibian development, and decline of amphibian populations Environ. Health Perspect. 103 1995 13 17
6. J.A. Carr A. Gentles E.E. Smith W.L. Goleman L.J. Urquidi K. Thuett R.J. Kendall J.P. Giesy T.S. Gross K.R. Solomon G. Van Der Kraak Response of larval Xenopus laevis to atrazine: assessment of growth, metamorphosis, and gonadal and laryngeal morphology Environ. Toxicol. Chem. 22 2003 396 405
7. C.Y. Chang E. Witschi Breeding of sex-reversed males of Xenopus laevis Daudin Proc. Soc. Exp. Biol. Med. 89 1955 150 152
8. C.Y. Chang E. Witschi Genic control and hormonal reversal of sex differentiation in Xenopus Proc. Soc. Exp. Biol. Med. 93 1956 140 144
9. M.S. Christn L. Menard A.D. Gendron S. Ruby D. Cyr D.J. Marcogliese L. Rollins-Smith M. Fournier Effects of agricultural pesticides on the immune system of Xenopus laevis and Rana pipiens Aquat. Toxicol. 67 2004 33 43
10. K. Coady M. Murphy D. Villeneuve M. Hecker P. Jones J. Carr K. Solomon E. Smith G. Van Der Kraak R. Kendall J. Giesy Effects of atrazine on metamorphosis, growth, and gonadal development in the green frog ( Rana clamitans ) J. Toxicol. Environ. Health 67 2004 941 957
11. K.K. Coady M.B. Murphy D.L. Villeneuve M. Hecker P.D. Jones J.A. Carr K.R. Solomon E.E. Smith G. Van Der Kraak R.J. Kendall J.P. Giesy Effects of atrazine on metamorphosis, growth, laryngeal and gonadal development, aromatase activity, and sex steroid concentrations in Xenopus laevis Ecotoxicol. Environ. Saf. 62 2005 160 173
12. T. Colborn F.S. vom Saal A.M. Soto Review. Developmental effects of endocrine-disrupting chemicals in wildlife and humans Environ. Health Perspect. 101 1993 378 384
13. T. Colborn Environmental estrogens: health implications for humans and wildlife Environ. Health Perspect. 103 1995 135 136
14. J.P. Collins A. Storfer Global amphibian declines: sorting the hypothesis Divers. Distrib. 9 2003 89 98
15. P. Daszak L. Berger A.A. Cunningham A.D. Hyatt D.E. Green R. Speare Emerging infectious diseases and amphibian population declines Emerg. Infect. Dis. 5 1999 735 748
16. L.H. Du Preez P.J. Jansen van Rensburg A.M. Jooste J.A. Carr J.P. Giesy T.S. Gross P.J. Kendall E.E. Smith G. Van Der Kraak K.R. Solomon Seasonal exposures to triazine and other pesticides in surface waters in the Western Highveld corn-production region in South Africa Environ. Pollut. 135 2005 131 141
17. L.H. Du Preez N. Kunene G.J. Everson J.A. Carr J.P. Giesy T.S. Gross A.J. Hosmer R.J. Kendall E.E. Smith K.R. Solomon G.J. Van Der Kraak Reproduction, larval growth, and reproductive development in African clawed frogs ( Xenopus laevis ) exposed to atrazine Chemosphere 71 2008 546 552
18. The Environment Agency, Japan Standard Protocols for Measurement of Environmental Chemicals 1998 The Environment Agency Japan
19. W. Fan T. Yanase H. Morinaga S. Gondo T. Okabe M. Nomura T.B. Hayes R. Takayanagi H. Nawata 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 2007 1012 1018
20. W. Fan T. Yanase H. Morinaga S. Gondo T. Okabe M. Nomura T. Komatsu K. Morohashi T.B. Hayes R. Takayanagi H. Nawata Atrazine-induced aromatase expression is SF-1 dependent: implications for endocrine disruption in wildlife and reproductive cancers in humans Environ. Health Perspect. 115 2007 720 727
21. T.B. Hayes A. Collins M. Lee M. Mendoza N. Noriega A.A. Stuart A. Vonk Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses Proc. Natl. Acad. Sci. U.S.A. 99 2002 5476 5480
22. T. Hayes K. Haston M. Tsui A. Hoang C. Haeffele A. Vonk Atrazine-induced hermaphroditism at 0.1 ppb in American leopard frogs (Rana pipiens): laboratory and field evidence Environ. Health Perspect. 111 2003 568 575
23. T.B. Hayes P. Case S. Chui D. Chung C. Haeffele K. Haston M. Lee V.P. Mai Y. Marjuoa J. Parker M. Tsui Pesticide mixtures, endocrine disruption, and amphibian declines: are we underestimating the impact? Environ. Health Perspect. 114 2006 40 50
24. T.B. Hayes A.A. Stuart M. Mendoza A. Collins N. Noriega A. Vonk G. Johnston R. Liu D. Kpodzo 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 (17beta-estradiol): support for the demasculinization/feminization hypothesis Environ. Health Perspect. 114 2006 134 141
25. M. Hecker W.J. Kim J.-W. Park M.B. Murphy D. Villeneuve K.K. Coady P.D. Jones K.R. Solomon G. Van Der Kraak J.A. Carr E.E. Smith L. Du Preez R.J. Kendall J.P. Giesy 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 2005 383 396
26. M. Hecker J.-W. Park M.B. Murphy P.D. Jones K.R. Solomon G. Van Der Kraak J.A. Carr E.E. Smith L. Du Preez R.J. Kendall J.P. Giesy 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 2005 273 280
27. J.E. Houlahan C.S. Findlay B.R. Schmidt A.H. Meyer S.L. Kuzmin Quantitative evidence for global amphibian population declines Nature 404 2000 752 755
28. G.E. Howe R. Gillis R.C. Mowbray Effect of chemical synergy and larval stage on the toxicity of atrazine and alachlor to amphibian larvae Environ. Toxicol. Chem. 17 1998 519 525
29. T. Iguchi Y. Ohta Y. Fukazawa N. Takasugi Strain differences in the induction of polyovular follicles by neonatal treatment with diethylstilbestrol in mice Med. Sci. Res. 15 1987 1407 1408
30. A.M. Jooste L.H. Du Preez J.A. Carr J.P. Giesy T.S. Gross R.J. Kendall E.E. Smith G.L. Van Der Kraak K.R. Solomon Gonadal development of larval male Xenopus laevis exposed to atrazine in outdoor microcosms Environ. Sci. Technol. 39 2005 5255 5261
31. H. Kato T. Iwata Y. Katsu H. Watanabe Y. Ohta T. Iguchi Evaluation of estrogenic activity in diets for experimental animals using in vitro assay J. Agric. Food Chem. 52 2004 1410 1414
32. W. Kloas I. Lutz R. Einspanier Amphibians as a model to study endocrine disruptors: II. Estrogenic activity of environmental chemicals in vitro and in vivo Sci. Total Environ. 225 1999 59 68
33. Kloas, W., Opitz, R., Lutz, I., 2003. Ringtest: effects of pesticides and other chemicals on thyroid system in the amphibian Xenopus laevis . Federal Environmental Agency Research Report 20067409. Berlin, Germany.
34. P.A. Krieg S.M. Varnum W.M. Wormington D.A. Melton The mRNA encoding elongation factor 1-α (EF-1 α) is a major transcript at the midblastula transition in Xenopus Dev. Biol. 133 1989 93 100
35. D.L. Larson S. McDonald A.J. Fivizzani W.E. Newton S.J. Hamilton Effects of the herbicide atrazine on Ambystoma tigrinum metamorphosis: duration, larval growth, and hormonal response Physiol. Zool. 71 1998 671 679
36. G. Levy I. Lutz A. Krüger W. Kloas Bisphenol A induces feminization in Xenopus laevi s tadpoles Environ. Res. 94 2004 102 111
37. X. Long R. Steinmetz N. Ben-Jonathan A. Caperell-Grant P.C. Young K.P. Nephew R.M. Bigsby Strain differences in vaginal responses to the xenoestrogen bisphenol A Environ. Health Perspect. 108 2000 243 247
38. K. Mikamo E. Witschi Functional sex-reversal in genetic females of Xenopus laevis , induced by implanted testes Genetics 48 1963 1411 1421
39. S.M. Miller C.W. Sweet J.V. DePino K.C. Hornbuckle Atrazine and nutrients in precipitation: results from the Lake Michigan mass balance study Environ. Sci. Technol. 34 1999 55 61
40. N. Mitsui O. Tooi A. Kawahara Sandwich ELISAs for quantification of Xenopus laevis vitellogenin and albumin and their application to measurement of estradiol-17 beta effects on whole animals and primary-cultured hepatocytes Comp. Biochem. Physiol. C 135 2003 305 313
41. N. Mitsui O. Tooi A. Kawahara Vitellogenin-inducing activities of natural, synthetic, and environmental estrogens in primary cultured Xenopus laevis hepatocytes Comp. Biochem. Physiol. C 146 2007 581 587
42. M. Miyahara H. Ishibashi M. Inudo H. Nishijima T. Iguchi L.J. Giillette Jr. K. Arizono Estrogenic activity of diet to estrogen receptors- α and -β in an experimental animal J. Health Sci. 49 2003 481 491
43. K. Miyashita N. Shimizu S. Osanai S. Miyata Sequence analysis and expression of the P450 aromatase and estrogen receptor genes in the Xenopus ovary J. Steroid Biochem. Mol. Biol. 75 2000 101 107
44. S. Miyata S. Koike T. Kubo Hormonal reversal and the genetic control of sex differentiation in Xenopus Zool. Sci. 16 1999 335 340
45. M.B. Murphy M. Hecker K.K. Coady A.R. Tompsett P.D. Jones L.H. Du Preez G.J. Everson K.R. Solomon J.A. Carr E.E. Smith R.J. Kendall G. Van Der Kraak J.P. Giesy Atrazine concentrations, gonadal gross morphology and histology in ranid frogs collected in Michigan agricultural areas Aquat. Toxicol. 76 2006 230 245
46. P.O. Nieuwkoop J. Faber Normal Table of Xenopus laevis (Daudin) 1956 North-Holland Amsterdam p. 252
47. S. Oda N. Tatarazako M. Dorgerloh R.D. Johnson K. Ole Kusk D. Leverett S. Marchini T. Nakari T. Williams T. Iguchi Strain difference in sensitivity to 3,4-dichloroaniline and insect growth regulator, fenoxycarb, in Daphnia magna Ecotoxicol. Environ. Saf. 67 2007 399 405
48. T. Oka N. Mitsui M. Hinago M. Miyahara T. Fujii O. Tooi N. Santo H. Urushitani T. Iguchi Y. Hanaoka H. Mikamid All ZZ male Xenopus laevis provides a clear sex-reversal test for feminizing endocrine disruptors Ecotoxicol. Environ. Saf. 63 2006 236 243
49. R. Opitz T. Braunbeck C. Bögi D.B. Pickford G. Nentwig J. Oehlmann O. Tooi I. Lutz W. Kloas Description and initial evaluation of a Xenopus metamorphosis assay for detection of thyroid system-disrupting activities of environmental compounds Environ. Toxicol. Chem. 24 2005 653 664
50. F. Orton J.A. Carr R.D. Handy Effects of nitrate and atrazine on larval development and sexual differentiation in the northern leopard frog Rana pipiens Environ. Toxicol. Chem. 25 2006 65 71
51. D.B. Pickford M.J. Hetheridge J.E. Caunter A.T. Hall T.H. Hutchinson Assessing chronic toxicity of bisphenol A to larvae of the African clawed frog ( Xenopus laevis ) in a flow-through exposure system Chemosphere 53 2003 223 235
52. R. Pohjanvirta M. Viluksela J.T. Tuomisto M. Unkila J. Karasinska M.-A. Franc M. Holowenko J.V. Giannone P.A. Harper J. Tuomisto A.B. Okey Physicochemical differences in the AH receptors of the most TCDD-susceptible and the most TCDD-resistant rat strains Toxicol. Appl. Pharmacol. 155 1999 82 95
53. J.T. Sanderson W. Seinen J.P. Giesy M. van den Berg 2-Chloro-s-triazine herbicides induce aromatase (CYP19) activity in H295R human adrenocortical carcinoma cells: a novel mechanism for estrogenicity? Toxicol. Sci. 54 2000 121 127
54. J.T. Sanderson R.J. Letcher M. Heneweer J.P. Giesy M. van den Berg 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
55. E.R. Simpson M.S. Mahendroo G.D. Means M.W. Kilgore M.M. Hinshelwood S. Graham-Lorence B. Amarneh Y. Ito C.R. Fisher M.D. Michael C.R. Mendelson S.E. Bulun Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis Endocr. Rev. 15 1994 342 355
56. L. Spanó C.R. Tyler R. van Aerle P. Devos S.N.M. Mandiki F. Silvestre J.-P. Thomé P. Kestemont Effects of atrazine on sex steroid dynamics, plasma vitellogenin concentration and gonad development in adult goldfish ( Carassius auratus ) Aquat. Toxicol. 66 2004 369 379
57. J.L. Spearow P. Doemeny R. Sera R. Leffler M. Barkley Genetic variation in susceptibility to endocrine disruption by estrogen in mice Science 285 1999 1259 1261
58. K.R. Solomon D.B. Baker P. Richards K.R. Dixon S.J. Klaine T.W. LaPoint R.J. Kendall J.M. Giddings J.P. Giesy J.L.W. Hall C.P. Weiskopf W. Williams Ecological risk assessment of atrazine in North American surface waters Environ. Toxicol. Chem. 15 1996 31 74
59. K. Sone M. Hinago A. Kitayama J. Morokuma N. Ueno H. Watanabe T. Iguchi Effects of 17β-estradiol, nonylphenol, and bisphenol-A on developing Xenopus laevis embryos Gen. Comp. Endocrinol. 138 2004 228 236
60. R. Steinmetz N.A. Mitchner A. Grant D.L. Allen R.M. Bigsby N. Ben-Jonathan The xenoestrogen bisphenol A induces growth, differentiation, and c-fos gene expression in the female reproductive tract Endocrinology 139 1998 2741 2747
61. L. Tavera-Mendoza S. Ruby P. Brousseau M. Fournier D. Cyr D. Marcogliese Response of the amphibian tadpole ( Xenopus laevis ) to atrazine during sexual differentiation of the testis Environ. Toxicol. Chem. 21 2002 527 531
62. L. Tavera-Mendoza S. Ruby P. Brousseau M. Fournier D. Cyr D. Marcogliese Response of the amphibian tadpole Xenopus laevis to atrazine during sexual differentiation of the ovary Environ. Toxicol. Chem. 21 2002 1264 1267
63. J.E. Tietge G.W. Holcombe K.M. Flynn P.A. Kosian J.J. Korte L.E. Anderson D.C. Wolf S.J. Degitz Metamorphic inhibition of Xenopus laevis by sodium perchlorate: effects on development and thyroid histology Environ. Toxicol. Chem. 24 2005 926 933
64. C.R. Tyler S. Jobling J.P. Sumpter Endocrine disruption in wildlife: a critical review of the evidence Crit. Rev. Toxicol. 28 1998 319 361
65. H. Watanabe A. Suzuki T. Mizutani S. Khono D.B. Lubahn H. Handa T. Iguchi Genome-wide analysis of changes in early gene expression induced by oestrogen Genes Cells 7 2002 497 507