Activation of estrogen receptor alpha disrupts differentiation of the reproductive organs in chicken embryos

General and Comparative Endocrinology

Volumn 172, Issue 2, 2011, Pages 251-259

  Mattsson, Anna ^a   Olsson, Jan A ^b   Brunström, Björn ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b Swedish University of Agricultural Sciences   (Sweden)

Author keywords

Chicken embryo; Estrogen receptor; M llerian ducts; Ovotestis; Sex differentiation

Indexed keywords

APOLIPOPROTEIN C2; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA;

ANIMAL TISSUE; ARTICLE; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; FEMALE; GENE; GENE EXPRESSION; LIVER; MALE; MUELLERIAN DUCT; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY DEVELOPMENT; PRIORITY JOURNAL; SEX DIFFERENTIATION; TESTIS DEVELOPMENT; VERY LOW DENSITY APOLIPOPROTEIN II GENE; VITELLOGENIN II GENE;

EID: 79955713986     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2011.03.010     Document Type: Article

References (63)

1. Abinawanto, Shimada K., Saito N. Sex-reversal effects of non-steroidal aromatase inhibitor on aromatase (P450arom) mRNA expression in adult chicken gonads. Jpn. Poult. Sci. 1997, 34:158-168.
2. Andrews J.E., Smith C.A., Sinclair A.H. Sites of estrogen receptor and aromatase expression in the chicken embryo. Gen. Comp. Endocrinol. 1997, 108:182-190.
3. J. Axelsson, Differentiation of brain and reproductive organs in birds: Effects of environmental contaminants, Acta Universitatis Upsaliensis (2008), Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, 414, Uppsala University, ISBN: 978-91-554-7141-5.
4. Berg C., Blomqvist A., Holm L., Brandt I., Brunström B., Ridderstråle Y. Embryonic exposure to oestrogen causes eggshell thinning and altered shell gland carbonic anhydrase expression in the domestic hen. Reproduction 2004, 128:455-461.
5. Berg C., Halldin K., Brunström B. Effects of bisphenol A and tetrabromobisphenol A on sex organ development in quail and chicken embryos. Environ. Toxicol. Chem. 2001, 20:2836-2840.
6. Berg C., Halldin K., Fridolfsson A.K., Brandt I., Brunström B. The avian egg as a test system for endocrine disrupters: effects of diethylstilbestrol and ethynylestradiol on sex organ development. Sci. Total Environ. 1999, 233:57-66.
7. Berg C., Holm L., Brandt I., Brunström B. Anatomical and histological changes in the oviducts of Japanese quail, Coturnix japonica, after embryonic exposure to ethynyloestradiol. Reproduction 2001, 121:155-165.
8. Brock M.L., Shapiro D.J. Estrogen stabilizes vitellogenin mRNA against cytoplasmic degradation. Cell 1983, 34:207-214.
9. Brunström B., Axelsson J., Halldin K. Effects of endocrine modulators on sex differentiation in birds. Ecotoxicology 2003, 12:287-295.
10. Brunström B., Axelsson J., Mattsson A., Halldin K. Effects of estrogens on sex differentiation in Japanese quail and chicken. Gen. Comp. Endocrinol. 2009, 163:97-103.
11. Cochrane A.W., Deeley R.G. Estrogen-dependent activation of the avian very low density apolipoprotein II and vitellogenin genes. Transient alterations in mRNA polyadenylation and stability early during induction. J. Mol. Biol. 1988, 203:555-567.
12. Elbrecht A., Lazier C.B., Protter A.A., Williams D.L. Independent developmental programs for two estrogen-regulated genes. Science 1984, 225:639-641.
13. Elbrecht A., Smith R.G. Aromatase enzyme activity and sex determination in chickens. Science 1992, 255:467-470.
14. Elbrecht A., Williams D.L., Blue M.L., Lazier C.B. Differential ontogeny of estrogen responsiveness in the chick embryo liver. Can. J. Biochem. 1981, 59:606-612.
15. Evans M.I., Silva R., Burch J.B. Isolation of chicken vitellogenin I and III cDNAs and the developmental regulation of five estrogen-responsive genes in the embryonic liver. Genes Dev. 1988, 2:116-124.
16. Fridolfsson A.-K., Ellegren H. A simple and universal method for molecular sexing of non-ratite birds. J. Avian Biol. 1999, 30:116-121.
17. Fry D.M., Toone C.K. DDT-induced feminization of gull embryos. Science 1981, 213:922-924.
18. Gong A., Freking F.W., Wingfield J., Schlinger B.A., Arnold A.P. Effects of embryonic treatment with fadrozole on phenotype of gonads, syrinx, and neural song system in zebra finches. Gen. Comp. Endocrinol. 1999, 115:346-353.
19. Guioli S., Lovell-Badge R. PITX2 controls asymmetric gonadal development in both sexes of the chick and can rescue the degeneration of the right ovary. Development 2007, 134:4199-4208.
20. Ha Y., Tsukada A., Saito N., Shimada K. Changes in mRNA expression of MMP-2 in the Müllerian duct of chicken embryo. Gen. Comp. Endocrinol. 2004, 139:131-136.
21. Halldin K. Impact of endocrine disrupting chemicals on reproduction in Japanese quail. Domest. Anim. Endocrinol. 2005, 29:420-429.
22. Halldin K., Holm L., Ridderstråle Y., Brunström B. Reproductive impairment in Japanese quail (Coturnix japonica) after in ovo exposure to o, p'-DDT. Arch. Toxicol. 2003, 77:116-122.
23. Hanafy A.M., Sasanami T., Ichikawa K., Shimada K., Mori M. Estrogen receptor binding of xenoestrogens and phytoestrogens in Japanese quail (Coturnix japonica). J. Poultry Sci. 2004, 41:30-37.
24. Hanafy A.M., Sasanami T., Mori M. Binding of xenoestrogens and phytoestrogens to estrogen receptor β of Japanese quail (Coturnix japonica). J. Poultry Sci. 2005, 42:238-244.
25. Hanafy A.M., Sasanami T., Mori M. Effects of diethylstilbestrol and ethinylestradiol on gene transcription of very low-density apolipoprotein II in the liver of Japanese quail, Coturnix japonica. Environ. Toxicol. Chem. 2006, 25:1354-1359.
26. Harrington W.R., Sheng S., Barnett D.H., Petz L.N., Katzenellenbogen J.A., Katzenellenbogen B.S. Activities of estrogen receptor alpha- and beta-selective ligands at diverse estrogen responsive gene sites mediating transactivation or transrepression. Mol. Cell. Endocrinol. 2003, 206:13-22.
27. Holm L., Blomqvist A., Brandt I., Brunström B., Ridderstråle Y., Berg C. Embryonic exposure to o, p'-DDT causes eggshell thinning and altered shell gland carbonic anhydrase expression in the domestic hen. Environ. Toxicol. Chem. 2006, 25:2787-2793.
28. Ichikawa K., Ha Y., Tsukada A., Saito N., Shimada K. Effect of endocrine disruptors on mRNA expression of vitellogenin (VTG) II and very low density lipoprotein (apo VLDL) II in the liver of quail embryos. J. Poultry Sci. 2003, 40:45-52.
29. Ishimaru Y., Komatsu T., Kasahara M., Katoh-Fukui Y., Ogawa H., Toyama Y., Maekawa M., Toshimori K., Chandraratna R.A., Morohashi K., Yoshioka H. Mechanism of asymmetric ovarian development in chick embryos. Development 2008, 135:677-685.
30. Kamata R., Takahashi S., Shimizu A., Morita M., Shiraishi F. In ovo exposure quail assay for risk assessment of endocrine disrupting chemicals. Arch. Toxicol. 2006, 80:857-867.
31. Koba N., Mori M., Ha Y., Mizushima S., Tsukada A., Saito N., Ono T., Shimada K. Effects of aromatase inhibitor (Fadrozole)-induced sex-reversal on gonadal differentiation and mRNA expression of P450arom, AMH and ERα in embryos and growth in posthatching quail. J. Poultry Sci. 2008, 45:116-1124.
32. Kuiper G.G.J.M., Carlsson B., Grandien K., Enmark E., Häggblad J., Nilsson S., Gustafsson J.-Å. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors α and β. Endocrinology 1997, 138:863-870.
33. Lazier C.B. Ontogeny of the vitellogenic response to oestradiol and of the soluble nuclear oestrogen receptor in embryonic-chick liver. Biochem. J. 1978, 174:143-152.
34. MacLaughlin D.T., Hutson J.M., Donahoe P.K. Specific estradiol binding in embryonic Müllerian ducts: a potential modulator of regression in the male and female chick. Endocrinology 1983, 113:141-145.
35. Marin M.G., Matozzo V. Vitellogenin induction as a biomarker of exposure to estrogenic compounds in aquatic environments. Mar. Pollut. Bull. 2004, 48:835-839.
36. Mattsson A., Brunström B. Effects on differentiation of reproductive organs and sexual behaviour in Japanese quail by excessive embryonic ERalpha activation. Reprod. Fertil. Dev. 2010, 22:416-425.
37. Mattsson A., Mura E., Brunström B., Panzica G., Halldin K. Selective activation of estrogen receptor alpha in Japanese quail embryos affects reproductive organ differentiation but not the male sexual behavior or the parvocellular vasotocin system. Gen. Comp. Endocrinol. 2008, 159:150-157.
38. Mattsson A., Olsson J.A., Brunström B. Selective estrogen receptor α activation disrupts sex organ differentiation and induces expression of vitellogenin II and very low-density apolipoprotein II in Japanese quail embryos. Reproduction 2008, 136:175-186.
39. Meyers M.J., Sun J., Carlson K.E., Marriner G.A., Katzenellenbogen B.S., Katzenellenbogen J.A. Estrogen receptor-beta potency-selective ligands: structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J. Med. Chem. 2001, 44:4230-4251.
40. Muller P.Y., Janovjak H., Miserez A.R., Dobbie Z. Processing of gene expression data generated by quantitative real-time RT-PCR. BioTechniques 2002, 32:1372-1379.
41. Nimpf J., Schneider W.J. Receptor-mediated lipoprotein transport in laying hens. J. Nutr. 1991, 121:1471-1474.
42. Ottinger M.A., Lavoie E., Thompson N., Barton A., Whitehouse K., Barton M., Abdelnabi M., Quinn M., Panzica G., Viglietti-Panzica C. Neuroendocrine and behavioral effects of embryonic exposure to endocrine disrupting chemicals in birds. Brain Res. Rev. 2008, 57:376-385.
43. Perrin F.M., Stacey S., Burgess A.M., Mittwoch U. A quantitative investigation of gonadal feminization by diethylstilboestrol of genetically male embryos of the quail Coturnix coturnix japonica. J. Reprod. Fertil. 1995, 103:223-226.
44. Pike A.C., Brzozowski A.M., Hubbard R.E., Bonn T., Thorsell A.G., Engström O., Ljunggren J., Gustafsson J.Å., Carlquist M. Structure of the ligand-binding domain of oestrogen receptor beta in the presence of a partial agonist and a full antagonist. EMBO J. 1999, 18:4608-4618.
45. Rissman E.F., Ascenzi M., Johnson P., Adkins-Regan E. Effect of embryonic treatment with oestradiol benzoate on reproductive morphology, ovulation and oviposition and plasma LH concentrations in female quail (Coturnix coturnix japonica). J. Reprod. Fertil. 1984, 71:411-417.
46. Romanoff A.L. The Avian Embryo 1960, The Macmillan Company, New York.
47. Sakimura M., Tsukada A., Usami M., Hanzawa S., Saito N., Ohno Y., Shimada K. Effect of estradiol and nonylphenol on mRNA expression of estrogen receptors α and β, and cytochrome P450 aromatase in the gonad of chicken embryos. J. Poultry Sci. 2002, 39:302-309.
48. Scheib D. Effects and role of estrogens in avian gonadal differentiation. Differentiation 1983, 23(Suppl.):S87-S92.
49. Sensel M.G., Binder R., Lazier C.B., Williams D.L. Reactivation of apolipoprotein II gene transcription by cycloheximide reveals two steps in the deactivation of estrogen receptor-mediated transcription. Mol. Cell Biol. 1994, 14:1733-1742.
50. Shibuya K., Mizutani M., Sato K., Itabashi M., Nunoya T. Comparative evaluation of sex reversal effects of natural and synthetic estrogens in sex reversal test using F1 (AWE×WE). J. Poultry Sci. 2005, 42:119-129.
51. Shibuya K., Wada M., Mizutani M., Sato K., Itabashi M., Sakamoto T. Vitellogenin detection and chick pathology are useful endpoints to evaluate endocrine-disrupting effects in avian one-generation reproduction study. Environ. Toxicol. Chem. 2005, 24:1654-1666.
52. Shimada K., Ha Y., Tsukada A., Saito N., Maekawa S., Nishizuka M., Imagawa M. In vitro and in vivo screening of endocrine disrupting chemicals with estrogenic activity in Japanese quail. Avian Poultry Biol. Rev. 2005, 16:19-27.
53. Smith C.A., Sinclair A.H. Sex determination in the chicken embryo. J. Exp. Zool. 2001, 290:691-699.
54. Stauffer S.R., Coletta C.J., Tedesco R., Nishiguchi G., Carlson K., Sun J., Katzenellenbogen B.S., Katzenellenbogen J.A. Pyrazole ligands: structure-affinity/activity relationships and estrogen receptor-alpha-selective agonists. J. Med. Chem. 2000, 43:4934-4947.
55. Sumpter J.P., Jobling S. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ. Health Perspect. 1995, 103(Suppl. 7):173-178.
56. Sun J., Baudry J., Katzenellenbogen J.A., Katzenellenbogen B.S. Molecular basis for the subtype discrimination of the estrogen receptor-beta-selective ligand, diarylpropionitrile. Mol. Endocrinol. 2003, 17:247-258.
57. Sun J., Huang Y.R., Harrington W.R., Sheng S., Katzenellenbogen J.A., Katzenellenbogen B.S. Antagonists selective for estrogen receptor alpha. Endocrinology 2002, 143:941-947.
58. Vaillant S., Dorizzi M., Pieau C., Richard-Mercier N. Sex reversal and aromatase in chicken. J. Exp. Zool. 2001, 290:727-740.
59. Willier B.H., Gallagher T.F., Koch F.C. Sex-modification in the chick embryo resulting from injections of male and female hormones. Proc. Natl. Acad. Sci. USA 1935, 21:625-631.
60. Wiskocil R., Bensky P., Dower W., Goldberger R.F., Gordon J.I., Deeley R.G. Coordinate regulation of two estrogen-dependent genes in avian liver. Proc. Natl. Acad. Sci. USA 1980, 77:4474-4478.
61. Wolff E. Old experiments and new trends in avian sex differentiation. In Vitro 1979, 15:6-10.
62. Woods J.E., Brazzill D.M. Plasma 17 beta-estradiol levels in the chick embryo. Gen. Comp. Endocrinol. 1981, 44:37-43.
63. Woods J.E., Simpson R.M., Moore P.L. Plasma testosterone levels in the chick embryo. Gen. Comp. Endocrinol. 1975, 27:543-547.