Endocrine-disrupting potentials of equine estrogens equilin, equilenin, and their metabolites, in the medaka Oryzias latipes: In silico and DNA microarray studies

Journal of Applied Toxicology

Volumn 35, Issue 9, 2015, Pages 1040-1048

  Uchida, Masaya ^a   Ishibashi, Hiroshi ^b   Yamamoto, Ryoko ^c   Koyanagi, Akiko ^a   Kusano, Teruhiko ^a   Tominaga, Nobuaki ^d   Ishibashi, Yasuhiro ^c   Arizono, Koji ^c  

^a Kyushu Medical Co Ltd   (Japan)

^b Kumamoto University   (Japan)

^c PREFECTURAL UNIVERSITY OF KUMAMOTO   (Japan)

^d ARIAKE NATIONAL COLLEGE OF TECHNOLOGY   (Japan)

Author keywords

DNA microarray; Docking simulation; Equine estrogen; Estrogen receptor ; Medaka

Indexed keywords

DIHYDROEQUILIN; EQUILENIN; EQUILIN; ESTROGEN RECEPTOR ALPHA; VITELLOGENIN; ENDOCRINE DISRUPTOR; ESTROGEN RECEPTOR BETA; LIGAND; PROTEIN BINDING; TRANSCRIPTOME; WATER POLLUTANT;

ADULT; ARTICLE; COMPUTER MODEL; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA MICROARRAY; GENE EXPRESSION PROFILING; HYDROGEN BOND; LIGAND BINDING; LONG TERM EXPOSURE; MALE; METABOLITE; MOLECULAR DOCKING; NONHUMAN; ONCOGENE RAS; ORYZIAS LATIPES; PRIORITY JOURNAL; UPREGULATION; ANIMAL; DRUG EFFECTS; LIVER; METABOLISM; ORYZIAS; TOXICITY; WATER POLLUTANT;

EQUIDAE; ORYZIAS LATIPES; ORYZIINAE;

ANIMALS; ENDOCRINE DISRUPTORS; EQUILENIN; EQUILIN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; LIGANDS; LIVER; MALE; MOLECULAR DOCKING SIMULATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORYZIAS; PROTEIN BINDING; TRANSCRIPTOME; WATER POLLUTANTS, CHEMICAL;

EID: 84937977517     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.3098     Document Type: Article

References (36)

1. Bhavnani BR. 1998. Pharmacokinetics and pharmacodynamics of conjugated equine estrogens: chemistry and metabolism. Proc. Soc. Exp. Biol. Med. 217: 6-16.
2. Bhavnani BR, Tam SP, Lu X. 2008. Structure activity relationships and differential interactions and functional activity of various equine estrogens mediated via estrogen receptors (ERs) ERα and ERβ. Endocrinology 149: 4857-4870.
3. Bolton JL, Thatcher GR. 2008. Potential mechanisms of estrogen quinone carcinogenesis. Chem. Res. Toxicol. 21: 93-101.
4. Chakraborty T, Shibata Y, Zhou LY, Katsu Y, Iguchi T, Nagahama Y. 2011. Differential expression of three estrogen receptor subtype mRNAs in gonads and liver from embryos to adults of the medaka, Oryzias latipes. Mol. Cell. Endocrinol. 333: 47-54.
5. Costache AD, Pullela PK, Kasha P, Tomasiewicz H, Sem DS. 2005. Homology-modeled ligand-binding domains of zebrafish estrogen receptors α, β1, and β2: from in silico to in vivo studies of estrogen interactions in Danio rerio as a model system. Mol. Endocrinol. 19: 2979-2990.
6. Delfosse V, Grimaldi M, Pons JL, Boulahtouf A, le Maire A, Cavailles V, Labesse G, Bourguet W, Balaguer P. 2012. Structural and mechanistic insights into bisphenols action provide guidelines for risk assessment and discovery of bisphenol A substitutes. Proc. Natl. Acad. Sci. U. S. A. 109: 14930-14935.
7. Fernández-Medarde A, Santos E. 2011. Ras in cancer and developmental diseases. Genes Cancer 2: 344-358.
8. Firestein R, Bass AJ, Kim SY, Dunn IF, Silver SJ, Guney I, Freed E, Ligon AH, Vena N, Ogino S, Chheda MG, Tamayo P, Finn S, Shrestha Y, Boehm JS, Jain S, Bojarski E, Mermel C, Barretina J, Chan JA, Baselga J, Tabernero J, Root DE, Fuchs CS, Loda M, Shivdasani RA, Meyerson M, Hahn WC. 2008. CDK8 is a colorectal cancer oncogene that regulates β-catenin activity. Nature 455: 547-551.
9. Gibson R, Smith MD, Spary CJ, Tyler CR, Hill EM. 2005. Mixtures of estrogenic contaminants in bile of fish exposed to wastewater treatment works effluents. Environ. Sci. Technol. 39: 2461-2471.
10. Griffin LB, January KE, Ho KW, Cotter KA, Callard GV. 2013. Morpholino-mediated knockdown of ERα, ERβa, and ERβb mRNAs in zebrafish (Danio rerio) embryos reveals differential regulation of estrogen-inducible genes. Endocrinology 154: 4158-4169.
11. Organization for Economic Co-operation and Development. 2004. Detailed review paper on fish screening assays for the detection of endocrine active substances. OECD Environment Health and Safety Publications Series on Testing and Assessment 47.
12. Halgren TA. 1996. Merck molecular force field. I. Basis, form, scope, parameterization, and performance of MMFF94. J. Comput. Chem. 17: 490-519.
13. Hersch AL, Stefanick ML, Stafford RS. 2004. National use of postmenopausal hormone therapy - annual; trends and response to recent evidence. JAMA 291: 47-53.
14. Inudo M, Ishibashi H, Matsumura N, Matsuoka M, Mori T, Taniyama S, Kadokami K, Koga M, Shinohara R, Hutchinson TH, Iguchi T, Arizono K. 2004. Effect of estrogenic activity, and phytoestrogen and organochlorine pesticide contents in an experimental fish diet on reproduction and hepatic vitellogenin production in medaka (Oryzias latipes). Comp. Med. 54: 673-680.
15. Inui M, Adachi T, Takenaka S, Inui H, Nakagawa M, Ueda M, Watanabe H, Mori C, Iguchi T, Miyatake K. 2003. Effect of UV screens and preservatives on vitellogenin and choriogenin production in male medaka (Oryzias latipes). Toxicology 194: 43-50.
16. Ishibashi H, Hirano M, Matsumura N, Watanabe N, Takao Y, Arizono K. 2006. Reproductive effects and bioconcentration of 4-nonylphenol in medaka fish (Oryzias latipes). Chemosphere 65: 1019-1026.
17. Ishibashi H, Matsumura N, Hirano M, Matsuoka M, Shiratsuchi H, Ishibashi Y, Takao Y, Arizono K. 2004. Effects of triclosan on the early life stages and reproduction of medaka Oryzias latipes and induction of hepatic vitellogenin. Aquat. Toxicol. 67: 167-179.
18. Ishibashi H, Yamauchi R, Matsuoka M, Kim JW, Hirano M, Yamaguchi A, Tominaga N, Arizono K. 2008. Fluorotelomer alcohols induce hepatic vitellogenin through activation of the estrogen receptor in male medaka (Oryzias latipes). Chemosphere 71: 1853-1859.
19. Ito M, Yuan CX, Malik S, Gu W, Fondell JD, Yamamura S, Fu ZY, Zhang X, Qin J, Roeder RG. 1999. Identity between TRAP and SMCC complexes indicates novel pathways for the function of nuclear receptors and diverse mammalian activators. Mol. Cell 3: 361-370.
20. Jinno A, Maruyama Y, Ishizuka M, Kazusaka A, Nakamura A, Fujita S. 2006. Induction of cytochrome P450-1A by the equine estrogen equilenin, a new endogenous aryl hydrocarbon receptor ligand. J. Steroid Biochem. Mol. Biol. 98: 48-55.
21. Kang YK, Guermah M, Yuan CX, Roeder RG. 2002. The TRAP/mediator coactivator complex interacts directly with estrogen receptors α and β through the TRAP220 subunit and directly enhances estrogen receptor function in vitro. Proc. Natl. Acad. Sci. U. S. A. 99: 2642-2647.
22. Labute P. 2008. The generalized Born/volume integral implicit solvent model: estimation of the free energy of hydration using London dispersion instead of atomic surface area. J. Comput. Chem. 29: 1693-1698.
23. Liehr JG. 2000. Is estradiol a genotoxic mutagenic carcinogen? Endocrine Rev. 21: 40-54.
24. Matsuzaki Y, Hosokai H, Mizuguchi Y, Fukamachi S, Shimizu A, Saya H. 2013. Establishment of HRAS(G12V) transgenic medaka as a stable tumor model for in vivo screening of anticancer drugs. PLoS One 8: e54424.
25. Nelson ER, Habibi HR. 2010. Functional significance of nuclear estrogen receptor subtypes in the liver of goldfish. Endocrinology 151: 1668-1676.
26. Spink DC, Zhang F, Hussain MM, Katz BH, Liu X, Hilker DR, Bolton JL. 2001. Metabolism of equilenin in MCF-7 and MDA-MB-231 human breast cancer cells. Chem. Res. Toxicol. 14: 572-581.
27. Tanenbaum DM, Wang Y, Williams SP, Sigler PB. 1998. Crystallographic comparison of the estrogen and progesterone receptor's ligand binding domains. Proc. Natl. Acad. Sci. U. S. A. 95: 5998-6003.
28. Tyler CR, Filby AL, Bickley LK, Cumming RI, Gibson R, Labadie P, Katsu Y, Liney KE, Shears JA, Silva-Castro V, Urushitani H, Lange A, Winter MJ, Iguchi T, Hill EM. 2009. Environmental health impacts of equine estrogens derived from hormone replacement therapy. Environ. Sci. Technol. 43: 3897-3904.
29. Uchida M, Takumi S, Tachikawa K, Yamauchi R, Goto Y, Matsusaki H, Nakamura H, Kagami Y, Kusano T, Arizono K. 2012. Toxicity evaluation of glyphosate agrochemical components using Japanese medaka (Oryzias latipes) and DNA microarray gene expression analysis. J. Toxicol. Sci. 37: 245-254.
30. Uchida M, Nakamura H, Kagami Y, Kusano T, Arizono K. 2010. Estrogenic effects of o, p'-DDT exposure in Japanese medaka (Oryzias latipes). J. Toxicol. Sci. 35: 605-608.
31. U.S. Environmental Protection Agency. 1998. Endocrine Disruptor Screening Program: Statement of Policy. Fed. Regist. 63: 71542-71568.
32. Wang J, Cieplak P, Kollman P. 2000. How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem. 21: 1049-1074.
33. Yamaguchi A, Ishibashi H, Kohra S, Arizono K, Tominaga N. 2005. Short-term effects of endocrine-disrupting chemicals on the expression of estrogen-responsive genes in male medaka (Oryzias latipes). Aquat. Toxicol. 72: 239-249.
34. Yamaguchi A, Ishibashi H, Kohra S, Arizono K, Kato K, Nakahama T, Kanno Y, Inouye Y, Tominaga N. 2009. Expression analysis of estrogen-responsive genes vitellogenin 1 and 2 in liver of male medaka (Oryzias latipes) exposed to selective ligands of estrogen receptor subtypes. J. Health Sci. 55: 930-938.
35. Yamaguchi A, Kato K, Arizono K, Tominaga N. 2014. Induction of the estrogen-responsive genes encoding choriogenin H and L in the liver of male medaka (Oryzias latipes) upon exposure to estrogen receptor subtype-selective ligands. J. Appl. Toxicol. (in press). DOI: 10.1002/jat.3063
36. Zhaobin Z, Jianying H. 2007. Development and validation of endogenous reference genes for expression profiling of medaka (Oryzias latipes) exposed to endocrine disrupting chemicals by quantitative real-time RT-PCR. Toxicol. Sci. 95: 356-368.