Molecular characterization of estrogen receptor genes in Gobiocypris rarus and their expression upon endocrine disrupting chemicals exposure in juveniles

Aquatic Toxicology

Volumn 101, Issue 1, 2011, Pages 276-287

  Wang, Houpeng ^a   Wang, Jingjing ^a   Wu, Tingting ^a   Qin, Fang ^a   Hu, Xiaoqi ^a   Wang, Lihong ^a   Wang, Zaizhao ^a  

^a NORTHWEST A F UNIVERSITY   (China)

Author keywords

Endocrine disrupting chemicals; Estrogen receptor; Gobiocypris rarus; Quantitative real time PCR

Indexed keywords

4 NONYLPHENOL; 4,4' ISOPROPYLIDENEDIPHENOL; COMPLEMENTARY DNA; ENDOCRINE DISRUPTOR; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGEN RECEPTOR BETA1; ESTROGEN RECEPTOR BETA2; ETHINYLESTRADIOL; MESSENGER RNA; UNCLASSIFIED DRUG; VITELLOGENIN;

AMINO ACID; ENDOCRINE DISRUPTOR; ESTROGENIC COMPOUND; GENE EXPRESSION; MOLECULAR ECOLOGY; PHYLOGENY; REAL TIME;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYPRINIFORMES; FERTILIZATION; FISH; GENE EXPRESSION; GENE EXPRESSION PROFILING; GOBIOCYPRIS RARUS; GONAD; INTESTINE; LIVER; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANOGENESIS; PHYLOGENETIC TREE; PIMEPHALES PROMELAS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; REPRODUCTION; RUTILUS RUTILUS; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE; TANICHTHY ALBONUBES; TESTIS; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CLUSTER ANALYSIS; CYPRINIDAE; ENDOCRINE DISRUPTORS; ETHINYL ESTRADIOL; FEMALE; GENE EXPRESSION REGULATION; GONADS; INTESTINES; LIVER; MALE; MOLECULAR SEQUENCE DATA; PHENOLS; PHYLOGENY; POLYMERASE CHAIN REACTION; RECEPTORS, ESTROGEN; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

CYPRINIDAE; GOBIOCYPRIS RARUS; PIMEPHALES PROMELAS; RUTILUS RUTILUS; VERTEBRATA;

EID: 78649907374     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2010.10.009     Document Type: Article

References (75)

1. Acconcia F., Marino M. Synergism between genomic and non-genomic estrogen action mechanisms. IUBMB Life 2003, 55:145-150.
2. Allen Y., Matthiessen P., Scott A.P., Haworth S., Feist S., Thain J.E. The extent of oestrogenic contamination in the UK estuarine and marine environments-further surveys of flounder. Sci. Total Environ. 1999, 233:5-20.
3. Andreassen T.K., Skjoedt K., Korsgaard B. Upregulation of estrogen receptor alpha and vitellogenin in eelpout (Zoarces viviparus) by waterborne exposure to 4-tert-octylphenol and 17 beta-estradiol. Comp. Biochem. Physiol. C 2005, 140:340-346.
4. Arukwe A., Celius T., Walther B.T., Goksøyr A. Plasma levels of vitellogenin and eggshell zona radiata proteins in 4-nonylphenol and o,p-DDT treated juvenile Atlantic salmon (Salmo salar). Mar. Environ. Res. 1998, 46:133-136.
5. Arukwe A., Celius T., Walther B.T., Goksoyr A. Effects of xenoestrogen treatment on zona radiata protein and vitellogenin expression in Atlantic salmon (Salmo salar). Aquat. Toxicol. 2000, 49:159-170.
6. Arukwe A., Knudsen F.R., Goksoyr A. Fish zona radiata (eggshell) protein: a sensitive biomarker for environmental estrogens. Environ. Health Perspect. 1997, 105:418-422.
7. Baker L., Meldrum K.K., Wang M., Sankula R., Vanam R., Raiesdana A., Tsai B., Hile K., Brown J.W., Meldrum D.R. The role of estrogen in cardiovascular disease. J. Surg. Res. 2003, 115:325-344.
8. Brzozowski A.M., Pike A.C.W., Dauter Z., Hubbard R.E., Bonn T., Engstrom O., Ohman L., Greene G.L., Gustafsson J.A., Carlquist M. Molecular basis of agonism and antagonism in the oestrogen receptor. Nature 1997, 389:753-758.
9. Bunone G., Briand P.A., Miksicek R.J., Picard D. Activation of the unliganded estrogen receptor by EGF involves in MAP kinase pathway and direct phosphorylation. EMBO J. 1996, 15:2174-2183.
10. Celius T., Haugen T.B., Grotmol T., Walther B.T. A sensitive zonagenetic assay for rapid in vitro assessment of estrogenic potency of xenobiotics and mycotoxins. Environ. Health Perspect. 1999, 107:63-68.
11. Cousins I.T., Staples C.A., Klecka G.M., Mackay D. A multimedia assessment of the environmental fate of BPA. Hum. Ecol. Risk Assess. 2002, 8:1107-1135.
12. Crain D.A., Eriksen M., Iguchi T., Jobling S., Laufer H., LeBlanc G.A., Guillette L.J. An ecological assessment of bisphenol-A: evidence from comparative biology. Reprod. Toxicol. 2007, 24:225-239.
13. Danielian P.S., White R., Lees J.A., Parker M.G. Identification of a conserved region required for hormone dependent transcriptional activation by steroid-hormone receptors. EMBO J. 1992, 11:1025-1033.
14. Dorrington J.H., Bendell J.J., Khan S.A. Interactions between FSH, estradiol-17-beta and transforming growth factor-beta regulate growth and differentiation in the rat gonad. J. Steroid Biochem. Mol. Biol. 1993, 44:441-447.
15. Edwards D.P. Regulation of signal transduction pathways estrogen and progesterone. Annu. Rev. Physiol. 2005, 67:335-376.
16. Ekena K., Weis K.E., Katzenellenborgen J.A., Katzenellenbogen B.S. Identification of amino acids in the hormone binding domain of the human estrogen receptor important in estrogen binding. J. Biol. Chem. 1996, 271:20053-20059.
17. Filby A.L., Tyler C.R. Molecular characterization of estrogen receptors 1, 2a, and 2b and their tissue and ontogenic expression profiles in fathead minnow (Pimephales promelas). Biol. Reprod. 2005, 73:648-662.
18. Flouriot G., Pakdel F., Ducouret B., Ledrean Y., Valotaire Y. Differential regulation of two genes implicated in fish reproduction: Vitellogenin and estrogen receptor genes. Mol. Reprod. Dev. 1997, 48:317-323.
19. Folmar L.C., Hemmer M., Hemmer R., Bowman C., Kroll K., Denslow N.D. Comparative estrogenicity of estradiol, ethynyl estradiol, and diethylstilbestrol in an in vivo male sheepshead minnow (Cyprinodon variegatus), vitellogenin bioassay. Aquat. Toxicol. 2000, 49:77-88.
20. Frank G.R. Role of estrogen and androgen in pubertal skeletal physiology. Med. Pediatr. Oncol. 2003, 41:217-221.
21. Gagne F., Blaise C., Salazar M., Salazar S., Hansen P.D. Evaluation of estrogenic effects of municipal effluents to the freshwater mussel Elliptio complanata. Comp. Biochem. Physiol. C 2001, 128:213-225.
22. Guiguen Y., Baroiller J.F., Ricordel M.J., Iseki K., McMeel O.M., Martin S.A., Fostier A. Involvement of estrogen in the process of sex differentiation in two fish species: the rainbow trout (Oncorhynchus mykiss) and a Tilapia (Oreochromis niloticus). Mol. Reprod. Dev. 1999, 54:154-162.
23. Haerd T., Gustafsson J.A. Structure and function of the DNA-binding domain of the glucocorticoid receptor and other members of the nuclear receptor supergene family. Acc. Chem. Res. 1993, 26:644-650.
24. Hawkins M.B., Thomas P. The unusual binding properties of the third distinct teleost estrogen receptor subtype ERβa are accompanied by highly conserved amino acid changes in the ligand binding domain. Endocrinology 2004, 145:2968-2977.
25. Hayashi H., Nishimoto A., Oshima N., Iwamuro S. Expression of the estrogen receptor alpha gene in the anal fin of Japanese medaka. Oryzias latipes, by environmental concentration of bisphenol A. J. Toxicol. Sci. 2007, 32:91-96.
26. Hawkins M.B., Thornton J.W., Crews D., Skipper J.K., Dotte A., Thomas P. Identification of a third estrogen receptor and reclassification of estrogen receptors in teleosts. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:10751-10756.
27. Hemmer M.J., Bowman C.J., Hemmer B.L., Friedman S.D., Marcovich D., Kroll K.J., Denslow N.D. Vitellogenin mRNA regulation and plasma clearance in male sheepshead minnows. (Cyprinodon variegatus) after cessation of exposure to 17[beta]-estradiol and p-nonylphenol. Aquat. Toxicol. 2002, 58:99-112.
28. Jin Y., Chen R., Sun L., Qian H., Liu W., Fu Z. Induction of estrogen-responsive gene transcription in the embryo, larval, juvenile and adult life stages of zebrafish as biomarkers of short-term exposure to endocrine disrupting chemicals. Comp. Biochem. Physiol. C 2009, 150:414-420.
29. Jobling S., Sheahan D., Osborne J.A., Matthiessen P., Sumpter J.P. Inhibition of testicular growth in rainbow trout (Oncorhynchus mykiss) exposed to estrogenic alkylphenolic chemicals. Environ. Toxicol. Chem. 1996, 15:194-202.
30. Jobling S., Beresford N., Nolan M., Rodgers-Gray T., Brighty G.C., Sumpter J.P., Tyler C.R. Altered sexual maturation and gamete production in wild roach (Rutilus rutilus) living in rivers that receive treated sewage effluents. Biol. Reprod. 2002, 66:272-281.
31. Jobling S., Coey S., Whitmore J.G., Kime D.E., Van Look K.J.W., McAllister B.G., Beresford N., Henshaw A.C., Brighty G., Tyler C.R., Sumpter J.P. Wild intersex roach (Rutilus rutilus) have reduced fertility. Biol. Reprod. 2002, 67:515-524.
32. Kazeto Y., Place A.R., Trant J.M. Effects of endocrine disrupting chemicals on the expression of CYP19 genes in zebrafish (Danio rerio) juveniles. Aquat. Toxicol. 2004, 69:25-34.
33. Kitano T., Yoshinaga N., Shiraishi E., Koyanagi T., Abe S. Tamoxifen induces masculinization of genetic females and regulates P450 aromatase and Mullerian inhibiting substance mRNA expression in Japanese flounder (Paralichthys olivaceus). Mol. Reprod. Dev. 2007, 74:1171-1177.
34. Kovacs E.J., Messingham K.A., Gregory M.S. Estrogen regulation of immune responses after injury. Mol. Cell. Endocrinol. 2002, 193:129-135.
35. Krust A., Green S., Argos P., Kumar V., Walter P., Bornert J.M., Chambon P. The chicken oestrogen receptor sequence: homology with v-er-A and the human oestrogen and glucocorticoid receptor. EMBO J. 1986, 5:891-897.
36. Langston W.J., Burt G.R., Chesman B.S., Vane C.H. Partitioning, bioavailability and effects of oestrogens and xeno-oestrogens in the aquatic environment. J. Mar. Biol. 2005, 85:1-31.
37. Liao T., Guo Q.L., Jin S.W., Cheng W., Xu Y. Comparative responses in rare minnow exposed to 17β-estradiol during different life stages. Fish Physiol. Biochem. 2009, 35:341-349.
38. Liu Z., Wu F., Jiao B., Zhang X., Hu C., Huang B., Zhou L., Huang X., Wang Z., Zhang Y., Nagahama Y., Cheng C.H.K., Wang D. Molecular cloning of doublesex and mab-3-related transcription factor 1, forkhead transcription factor gene 2, and two types of cytochrome P450 aromatase in Southern catfish and their possible roles in sex differentiation. J. Endocrinol. 2007, 194:223-241.
39. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
40. Marino M., Galluzzo P., Ascenzi P. Estrogen signaling multiple pathways to impact gene transcription. Curr. Genomics 2006, 7:497-508.
41. Menuet A., Page Y.L., Torres O., Kern L., Kah O., Pakdel F. Analysis of the estrogen regulation of the zebrafish estrogen receptor (ER) reveals distinct effects of ERα, ERβ1 and ERβ2. J. Mol. Endocrinol. 2004, 32:975-986.
42. Menuet A., Pellegrini E., Anglade I., Blaise O., Laudet V., Kah O., Pakdel F. Molecular characterization of three estrogen receptor forms in zebrafish: binding characteristics, transactivation properties, and tissue distributions. Biol. Reprod. 2002, 66:1881-1892.
43. Meucci V., Arukwe A. Transcriptional modulation of brain and hepatic estrogen receptor and P450arom isotypes in juvenile Atlantic salmon (Salmo salar) after waterborne exposure to the xenoestrogen, 4-nonylphenol. Aquat. Toxicol. 2006, 77:167-177.
44. Murphy C.A., Rose K.A., Thomas P. Modeling vitellogenesis in female fish exposed to environmental stressors: predicting the effects of endocrine disturbance due to exposure to a PCB mixture and cadmium. Reprod. Toxicol. 2005, 19:395-409.
45. O'Connor J.C., Chapin R.E. Critical evaluation of observed adverse effects of endocrine active substances on reproduction and development, the immune system, and the nervous system. Pure Appl. Chem. 2003, 75:2099-2123.
46. O'Donnell L., Robertson K.M., Jones M.E., Simpson E.R. Estrogen and spermatogenesis. Endocr. Rev. 2001, 22:289-318.
47. O'Dowd B.F., Nguyen T., Marchese A., Cheng R., Lynch K.R., Heng H.H.Q., Kolakowski L.F., George S.R. Discovery of three novel G-protein-coupled receptor genes. Genomics 1998, 47:310-313.
48. Pakdel F., Feon S., Le Gac F., Le Menn F., Valotaire Y. In vivo estrogen induction of hepatic estrogen receptor mRNA and correlation with vitellogenin mRNA in rainbow trout. Mol. Cell. Endocrinol. 1991, 75:205-212.
49. Park I.S., Kim J.H., Cho S.H., Kim D.S. Sex differentiation and hormonal sex reversal in the bagrid catfish Pseudobagrus fulvidraco (Richardson). Aquaculture 2004, 232:183-193.
50. Park K., Kwak I. Molecular effects of endocrine-disrupting chemicals on the Chironomus riparius estrogen-related receptor gene. Chemosphere 2010, 79:934-941.
51. Petit F.G., Metivier R., Valotaire Y., Pakdel F. Synergism between a half-site and an imperfect estrogen-responsive element, and coorperation with COUP-TFI are required for estrogen receptor (ER) to achieve a maximal estrogen-stimulation of rainbow trout ER gene. Eur. J. Biochem. 1999, 259:385-395.
52. Purdom C.E., Hardiman P.A., Bye V.V., Eno N.C., Tyler C.R., Sumpter J.P. Estrogenic effects of effluents from sewage treatment works. Chem. Ecol. 1994, 8:275-285.
53. Rempel M.A., Schlenk D. Effects of environmental estrogens and antiandrogens on endocrine function, gene regulation and health in fish. International Review of Cell and Molecular Biology 2008, 251-296. Elsevier Inc., Amsterdam. K.W. Jeon (Ed.).
54. Richards J.S. Hormonal control of gene expression in the ovary. Endocr. Rev. 1994, 15:725-751.
55. Vom saal F.S., Timms B.G., Montano M.M., Palanza P., Thayer K.A., Nagel S.C., Dhar M.D., Ganjam V.K., Parmigiani S., Welshons W.V. Prostate enlargement in mice due to fetal exposure to low doses of estradiol or diethylstilbestrol and opposite effects at high doses. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:2056-2061.
56. Sabo-Attwood T., Kroll K.J., Denslow N.D. Differential expression of largemouth bass (Micropterus salmoides) estrogen receptor isotypes alpha, beta, and gamma by estradiol. Mol. Cell. Endocrinol. 2004, 218:107-118.
57. Schmid T., Gonzalez-Valero J., Rufli H., Dietrich D.R. Determination of vitellogenin kinetics in male fathead minnows (Pimephales promelas). Toxicol. Lett. 2002, 131:65-74.
58. Seo J.S., Lee Y., Jung S., Kim I., Yoon Y., Lee J. Nonylphenol modulates expression of androgen receptor and estrogen receptor genes differently in gender types of the hermaphroditic fish Rivulus marmoratus. Biochem. Biophys. Res. Commun. 2006, 346:213-223.
59. Sharpe R.M. The roles of oestrogen in the male. Trends Endocrinol. Metab. 1998, 9:371-377.
60. Sun L.W., Zha J.M., Spear P.A., Wang Z.J. Tamoxifen effects on the early life stages and reproduction of Japanese medaka (Oryzias latipes). Environ. Toxicol. Pharmcol. 2007, 24:23-29.
61. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
62. Thomas-Jones E., Thorpe K., Harrison N., Thomas G., Morris C., Hutchinson T.H. Dynamics of estrogen biomarker responses in rainbow trout exposed to 17β-estradiol and 17α-ethinylestradiol. Environ. Toxicol. Chem. 2003, 22:3001-3008.
63. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The ClustalX Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25:4876-4882.
64. Thornton J.W. Evolution of vertebrate steroid receptors from an ancestral estrogen receptor by ligand exploitation and serial genome expansions. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:5671-5676.
65. Toran-Allerand C.D. Minireview: a plethora of estrogen receptors in the brain: where will it end?. Endocrinology 2004, 145:1069-1074.
66. Tyler C.R., Jobling S., Sumpter J.P. Endocrine disruption in wildlife: a critical review of the evidence. Crit. Rev. Toxicol. 1998, 28:319-361.
67. Wang J., Liu X., Wang H., Wu T., Hu X., Qin F., Wang Z. Expression of two cytochrome P450 aromatase genes is regulated by endocrine disrupting chemicals in rare minnow Gobiocypris rarus juveniles. Comp. Biochem. Physiol. C 2010, 152:313-320.
68. Wang J.W. Spawning performance and development of oocytes in Gobiocypris rarus. Acta Hydrobiol. Sin. 1999, 23:161-166.
69. Welshons W.V., Nagel S.C., Vom Saal F.S. Large effects from small exposures. III. Endocrine mechanisms mediating effects of bisphenol A at levels of human exposure. Endocrinology 2006, 147:S56-S69.
70. Yamaguchi A., Ishibashi H., Kohra S., Arizono K., Tominaga N. Short-term effects of endocrine-disrupting chemicals on the expression of estrogen-responsive genes in male medaka (Oryzias latipes). Aquat. Toxicol. 2005, 72:239-249.
71. Zha J., Wang Z., Wang N., Ingersoll C. Histological alternation and vitellogenin induction in adult rare minnow (Gobiocypris rarus) after exposure to ethynylestradiol and nonylphenol. Chemosphere 2007, 66:488-495.
72. Zha J., Sun L., Spear P.A., Wang Z. Comparison of ethinylestradiol and nonylphenol effects on reproduction of Chinese rare minnows (Gobiocypris rarus). Ecotoxicol. Environ. Safety 2008, 71:390-399.
73. Zha J., Sun L., Zhou Y., Spear P.A., Ma M., Wang Z. Assessment of 17α-ethinylestradiol effects and underlying mechanisms in a continuous, multigeneration exposure of the Chinese rare minnow. Toxicol. Appl. Pharmacol. 2008, 226:298-308.
74. Zhang X., Hecker M., Park J., Tompsett A.R., Newsted J., Nakayam K., Jones P.D., Au D., Kong R., Wu R..S.S., Giesy J.P. Real-time PCR array to study effects of chemicals on the hypothalamic-pituitary-gonadal axis of the Japanese medaka. Aquat. Toxicol. 2008, 88:173-182.
75. Zhang X., Zha J., Li W., Yang L., Wang Z. Effect of 2, 4-dichlorophenol on the expression of vitellogenin and estrogen receptor genes and physiology impairments in Chinese rare minnow (Gobiocypris rarus). Environ. Toxicol. 2008, 23:694-701.