Endocrine disruption caused by oral administration of atrazine in European quail (Coturnix coturnix coturnix)

Comparative Biochemistry and Physiology - C Toxicology and Pharmacology

Volumn 156, Issue 3-4, 2012, Pages 159-165

  De La Casa Resino, Irene ^a   Valdehita, Ana ^b   Soler, Francisco ^a   Navas, José María ^b   Pérez López, Marcos ^a  

^a UNIVERSITY OF EXTREMADURA   (Spain)

^b INIA   (Spain)

Author keywords

Atrazine; CYP1A4; Estradiol; Ethoxyresorufin O deethylase; European quail; Vitellogenin

Indexed keywords

ATRAZINE; CYTOCHROME P450 1A; CYTOCHROME P450 1A4; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ETHOXYRESORUFIN DEETHYLASE; MESSENGER RNA; UNCLASSIFIED DRUG; VITELLOGENIN;

ANIMAL EXPERIMENT; ARTICLE; BIOTRANSFORMATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; COTURNIX; ENZYME ACTIVITY; FEMALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPRODUCTION;

AMPHIBIA; ANIMALIA; AVES; COTURNIX COTURNIX; PHASIANIDAE; RATTUS;

EID: 84866432120     PISSN: 15320456     EISSN: 18781659     Source Type: Journal    
DOI: 10.1016/j.cbpc.2012.07.006     Document Type: Article

References (69)

1. N.H. Adams, P.E. Levi, and E. Hodgson In vitro studies of the metabolism of atrazine, simazine, and terbutryn in several vertebrate species J. Agric. Food Chem. 38 1990 1411 1417
2. M.J. Anderson, M.R. Miller, and D.E. Hinton In vitro modulation of 17 beta-estradiol-induced vitellogenin synthesis: effects of cytochrome P450 1A1 inducing compounds on rainbow trout (Oncorhynchus mykiss) liver cells Aquat. Toxicol. 34 1996 327 350
3. A. Arukwe, and A. Goksoyr Eggshell and egg yolk proteins in fish: hepatic proteins for the next generation: oogenetic, population, and evolutionary implications of endocrine disruption Comp. Hepatol. 2 2003 4
4. Astraulian Pesticides and Veterinary Mecicines Authority (APVMA) Atrazine toxicity: analysis of potential modes of action http://www.apvma.gov.au 2010
5. J.E. Bakke, J.D. Robbins, and V.J. Feil Metabolism of 2-methoxy-4-ethylamino-6-sec-butylamino-s-triazine by the dairy cow and the goat J. Agric. Food Chem. 19 1971 462 466
6. S. Boronat, S. Casado, J.M. Navas, and B. Piña Modulation of aryl hydrocarbon receptor transactivation by carbaryl, a nonconventional ligand FEBS J. 274 2007 4347 4359
7. M.D. Burke, and R.T. Mayer Ethoxyresorufin: direct fluorimetric assay of a microsomal O-dealkylation which is preferentially inducible by 3-methylcholanthrene Drug Metab. Dispos. 2 1974 583 588
8. L.W. Chang, G.P. Toth, D.A. Gordon, D.W. Graham, J.R. Meier, C.W. Knapp, F.J. deNoyelles, S. Campbell, and D.L. Lattier Responses of molecular indicators of exposure in mesocosms: common carp (Cyprinus carpio) exposed to the herbicides alachlor and atrazine Environ. Toxicol. Chem. 24 2005 190 197
9. G. Cimino-Reale, D. Ferrario, B. Casati, R. Brustio, C. Diodovich, A. Collotta, M. Vahter, and L. Gribaldo Combined in utero and juvenile exposure of mice to arsenate and atrazine in drinking water modulates gene expression and clonogenicity of myeloid progenitors Toxicol. Lett. 180 2008 59 66
10. K. Connor, J. Howell, I. Chen, H. Liu, K. Berhane, C. Sciarretta, S. Safe, and T. Zacharewski Failure of chloro-S-triazine-derived compounds to induce estrogen receptor-mediated responses in vivo and in vitro Fundam. Appl. Toxicol. 30 1996 93 101
11. R.L. Cooper, T.E. Stoker, J.M. Goldman, M.B. Parrish, and L. Tyrey Effect of atrazine on ovarian function in the rat Reprod. Toxicol. 10 1996 257 264
12. R.L. Cooper, J.M. Goldman, and T.E. Stoker Neuroendocrine and reproductive effects of contemporary-use pesticides Toxicol. Ind. Health 15 1999 26 36
13. R.L. Cooper, T.E. Stoker, L. Tyrey, J.M. Goldman, and W.K. McElroy Atrazine disrupts the hypothalamic control of pituitary-ovarian function Toxicol. Sci. 53 2000 297 307
14. M.S. Denison, and S.R. Nagy Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals Annu. Rev. Pharmacol. Toxicol. 43 2003 309 334
15. N.D. Denslow, M.C. Chow, K.J. Kroll, and L. Green Vitellogenin as a biomarker of exposure for estrogen or estrogen mimics Ecotoxicology 8 1999 385 398
16. X. Dong, L. Zhu, J. Wang, J. Wang, H. Xie, X. Hou, and W. Jia Effects of atrazine on cytochrome P450 enzymes of zebrafish (Danio rerio) Chemosphere 77 2009 404 412
17. A. Elbrecht, C.B. Lazier, A.A. Protter, and D.L. Williams Independent developmental programs for two estrogen-regulated genes Science 225 1984 639 641
18. M.L. Fernández-Cruz, A. Valdehita, M. Alonso, E. Mann, B. Herradón, and J.M. Navas Biological and chemical studies on aryl hydrocarbon receptor induction by the p53 inhibitor pifithrin-α and its condensation product pifithrin-β Life Sci. 88 2011 774 783
19. N. Hanioka, H. Jinno, T. Tanaka-Kagawa, T. Nishimura, and M. Ando In vitro metabolism of chlorotriazines: characterization of simazine, atrazine, and propazine metabolism using liver microsomes from rats treated with various cytochrome P450 inducers Toxicol. Appl. Pharmacol. 156 1999 195 205
20. T.B. Hayes, A. Collins, M. Lee, M. Mendoza, N. Noriega, A.A. Stuart, and 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
21. T. Hayes, K. Haston, M. Tsui, A. Hoang, C. Haeffele, and 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
22. T.B. Hayes, A.A. Stuart, M. Mendoza, A. Collins, N. Noriega, A. Vonk, G. Johnston, R. Liu, and 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 Suppl. 1 2006 134 141
23. T.B. Hayes, V. Khoury, A. Narayan, M. Nazir, A. Park, T. Brown, L. Adame, E. Chan, D. Buchholz, T. Stueve, and S. Gallipeau Atrazine induces complete feminization and chemical castration in male African clawed frogs (Xenopus laevis) Proc. Natl. Acad. Sci. U. S. A. 107 2010 4612 4617
24. J.C. Herve, D. Crump, S.P. Jones, L.J. Mundy, J.P. Giesy, M.J. Zwiernik, S.J. Bursian, P.D. Jones, S.B. Wiseman, Y. Wan, and S.W. Kennedy Cytochrome P4501A induction by 2,3,7,8-tetrachlorodibenzo-p-dioxin and two chlorinated dibenzofurans in primary hepatocyte cultures of three avian species Toxicol. Sci. 113 2010 380 391
25. R. Hussain, F. Mahmood, M.Z. Khan, A. Khan, and F. Muhammad Pathological and genotoxic effects of atrazine in male Japanese quail (Coturnix japonica) Ecotoxicology 20 2011 1 8
26. M.O. Islam, M. Hara, and J. Miyake Induction of P-glycoprotein, glutathione-S-transferase and cytochrome P450 in rat liver by atrazine Environ. Toxicol. Pharmacol. 12 2002 1 6
27. M. Jonsson, A. Abrahamson, B. Brunstrom, I. Brandt, K. Ingebrigtsen, and E.H. Jorgensen EROD activity in gill filaments of anadromous and marine fish as a biomarker of dioxin-like pollutants Comp. Biochem. Physiol. C 136 2003 235 243
28. Kentucky Department of Agriculture Guidelines for atrazine use and application for groundwater and surface water protection 2007 Kentucky Department of Agriculture Kentucky
29. T. Kiely, D. Donaldson, and A. Grube Pesticide Industry Sales And Usage - 2000 and 2001 Market Estimates U.S. Environmental Protection Agency, Office EPA-733-R-04-001 2004 33
30. J.J. Korte, M.D. Kahl, K.M. Jensen, M.S. Pasha, L.G. Parks, G.A. LeBlanc, and G.T. Ankley Fathead minnow vitellogenin: complementary DNA sequence and messenger RNA and protein expression after estradiol treatment Environ. Toxicol. Chem. 19 2000 972 981
31. C.B. Lazier Ontogeny of the vitellogenic response to estradiol and of the soluble nuclear oestrogen receptor in embryonic-chick liver Biochem. J. 174 1978 143 152
32. - ΔΔCT. method Methods 25 2001 402 408
33. M.G. Marin, and V. Matozzo Vitellogenin induction as a biomarker of exposure to estrogenic compounds in aquatic environments Mar. Pollut. Bull. 48 2004 835 839
34. V. Matozzo, F. Gagne, M.G. Marin, F. Ricciardi, and C. Blaise Vitellogenin as a biomarker of exposure to estrogenic compounds in aquatic invertebrates: a review Environ. Int. 34 2008 531 545
35. A. Mattsson, J.A. Olsson, and B. Brunstrom Selective estrogen receptor alpha activation disrupts sex organ differentiation and induces expression of vitellogenin II and very low-density apolipoprotein II in Japanese quail embryos Reproduction 136 2008 175 186
36. A. Mattsson, J.A. Olsson, and B. Brunstrom Activation of estrogen receptor alpha disrupts differentiation of the reproductive organs in chicken embryos Gen. Comp. Endocrinol. 172 2011 251 259
37. T.S. McMullin, J.M. Brzezicki, B.K. Cranmer, J.D. Tessari, and M.E. Andersen Pharmacokinetic modeling of disposition and time-course studies with [14C]atrazine J. Toxicol. Environ. Health A 66 2003 941 964
38. T.S. McMullin, M.E. Andersen, A. Nagahara, T.D. Lund, T. Pak, R.J. Handa, and W.H. Hanneman Evidence that atrazine and diaminochlorotriazine inhibit the estrogen/progesterone induced surge of luteinizing hormone in female Sprague-Dawley rats without changing estrogen receptor action Toxicol. Sci. 79 2004 278 286
39. C. Mehats, C.B. Andersen, M. Filopanti, S.L. Jin, and M. Conti Cyclic nucleotide phosphodiesterases and their role in endocrine cell signaling Trends Endocrinol. Metab. 13 2002 29 35
40. J.J. Nagler, S. Ruby, D.R. Idler, and Y.P. So Serum phosphoprotein phosphorus and calcium levels as reproductive indicators of vitellogenin in highly vitellogenic mature female and estradiol-injected immature rainbow trout (Salmo gairdneri) Can. J. Zool. 65 1987 2421 2425
41. J.M. Navas, and H. Segner Modulation of 7-ethoxyresorufin-O-deethylase (EROD) activity by estradiol and octylphenol Mar. Environ. Res. 50 2000 157 162
42. J.M. Navas, and H. Segner Estrogen-mediated suppression of cytochrome P4501A (CYP1A) expression in rainbow trout hepatocytes: role of estrogen receptor Chem. Biol. Interact. 138 2001 285 298
43. J.M. Navas, and H. Segner In vitro screening of the antiestrogenic activity of chemicals Expert Opin. Drug Metab. Toxicol. 4 2008 605 617
44. J.M. Navas, A. Chana, B. Herradón, and H. Segner Induction of cytochrome P4501A (CYP1A) by clotrimazole, a non-planar aromatic compound. Computational studies on structural features of clotrimazole and related imidazole derivatives Life Sci. 76 2004 699 714
45. F. Ohtake, K. Takeyama, T. Matsumoto, H. Kitagawa, Y. Yamamoto, K. Nohara, C. Tohyama, A. Krust, J. Mimura, P. Chambon, J. Yanagisawa, Y. Fujii-Kuriyama, and S. Kato Modulation of oestrogen receptor signalling by association with the activated dioxin receptor Nature 423 2003 545 550
46. M. Roberge, H. Hakk, and G. Larsen Atrazine is a competitive inhibitor of phosphodiesterase but does not affect the estrogen receptor Toxicol. Lett. 154 2004 61 68
47. I. Salaberria, B.H. Hansen, V. Asensio, P.A. Olsvik, R.A. Andersen, and B.M. Jenssen Effects of atrazine on hepatic metabolism and endocrine homeostasis in rainbow trout (Oncorhynchus mykiss) Toxicol. Appl. Pharmacol. 234 2009 98 106
48. J.T. Sanderson, W. Seinen, J.P. Giesy, and 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
49. J.T. Sanderson, R.J. Letcher, M. Heneweer, J.P. Giesy, and 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
50. R.H. Shimabukuro Atrazine metabolism and herbicidal selectivity Plant Physiol. 42 1967 1269 1276
51. T. Shimada, Y. Oda, E.M. Gillam, F.P. Guengerich, and K. Inoue Metabolic activation of polycyclic aromatic hydrocarbons and other procarcinogens by cytochromes P450 1A1 and P450 1B1 allelic variants and other human cytochromes P450 in Salmonella typhimurium NM2009 Drug Metab. Dispos. 29 2001 1176 1182
52. J.M.W. Smeets, I. van Holsteijn, J.P. Giesy, and M. van den Berg The anti-estrogenicity of Ah receptor agonists in carp (Cyprinus carpio) hepatocytes Toxicol. Sci. 52 1999 178 188
53. A.M. Soto, C. Sonnenschein, K.L. Chung, M.F. Fernandez, N. Olea, and F.O. Serrano The E-SCREEN assay as a tool to identify estrogens: an update on estrogenic environmental pollutants Environ. Health Perspect. 103 1995 113 122
54. L. Spano, C.R. Tyler, R. van Aerle, P. Devos, S.N. Mandiki, F. Silvestre, J.P. Thome, and 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
55. T.E. Stoker, S.C. Laws, D.L. Guidici, and R.L. Cooper 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 2000 50 59
56. M. Suzawa, and H.A. Ingraham The herbicide atrazine activates endocrine gene networks via non-steroidal NR5A nuclear receptors in fish and mammalian cells PLoS One 3 2008 e2117
57. R. Thibaut, and C. Porte Effects of endocrine disrupters on sex steroid synthesis and metabolism pathways in fish J. Steroid Biochem. Mol. Biol. 92 2004 485 494
58. D.E. Tillitt, D.M. Papoulias, J.J. Whyte, and C.A. Richter Atrazine reduces reproduction in fathead minnow (Pimephales promelas) Aquat. Toxicol. 99 2010 149 159
59. United States Environmental Protection Agency (U.S. EPA) Finalization of Atrazine IRED, and Completion of Tolerance Reassessment and Reregistration Eligibility Process (April 6, 2006) Science Chapter for Atrazine: Environmental Fate and Effects 2006 Office of Prevention, Pesticides and Toxic Substances Washington, DC
60. A.B. Victor-Costa, S.M.C. Bandeira, A.G. Oliveira, G.A.B. Mahecha, and C.A. Oliveira Changes in testicular morphology and steroidogenesis in adult rats exposed to atrazine Reprod. Toxicol. 29 2010 323 331
61. W. Wahli, I.B. Dawid, G.U. Ryffel, and R. Weber Vitellogenesis and the vitellogenin gene family Science 212 1981 298 304
62. C.L. Waller, and J.D. McKinney Three-dimensional quantitative structure activity relationships of dioxins and dioxin-like compounds: model validation and Ah receptor characterization Chem. Res. Toxicol. 8 1995 847 858
63. J.P. Whitlock Induction of cytochrome P4501A1 Annu. Rev. Pharmacol. Toxicol. 39 1999 103 125
64. WHO/IPCS (World Health Organization/International Petroleum Chemical Society) T. Damstra, S. Barlow, A. Bergman, R. Kavlock, G. Van Der Kraak, Global assessment of the state-of-the-science of endocrine disruptors. WHO/IPCS/EDC/02.2 2002 World Healh Organization Geneva, Switzerland
65. H.S. Wiley, L. Opresko, and R.A. Wallace New methods for the purification of vertebrate vitellogenin Anal. Biochem. 97 1979 145 152
66. K.W. Wilhelms, S.A. Cutler, J.A. Proudman, L.L. Anderson, and C.G. Scanes Atrazine and the hypothalamo-pituitary-gonadal axis in sexually maturing precocial birds: studies in male Japanese quail Toxicol. Sci. 86 2005 152 160
67. K.W. Wilhelms, S.A. Cutler, J.A. Proudman, R.V. Carsia, L.L. Anderson, and C.G. Scanes Lack of effects of atrazine on estrogen-responsive organs and circulating hormone concentrations in sexually immature female Japanese quail (Coturnix coturnix japonica) Chemosphere 65 2006 674 681
68. K.W. Wilhelms, K.F. Fitzpatrick, C.G. Scanes, and L.L. Anderson In ovo exposure to a triazine herbicide: effects of atrazine on circulating reproductive hormones and gonadal histology in young Japanese quail Arch. Environ. Contam. Toxicol. 51 2006 117 122
69. R. Wiskocil, P. Bensky, W. Dower, R.F. Goldberger, J.I. Gordon, and R.G. Deeley Coordinate regulation of two estrogen-dependent genes in avian liver Proc. Natl. Acad. Sci. U. S. A. 77 1980 4474 4478