Estrogen responses in killifish (Fundulus heteroclitus) from polluted and unpolluted environments are site- and gene-specific

Aquatic Toxicology

Volumn 99, Issue 2, 2010, Pages 291-299

  Greytak, Sarah R ^a   Tarrant, Ann M ^b   Nacci, Diane ^c   Hahn, Mark E ^b   Callard, Gloria V ^a  

^a Boston University   (United States)

^b WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^c U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Adaptation; Biomarkers; Environmental pollutants; Estrogen receptors; Killifish; Resistance; Responses; Tolerance

Indexed keywords

AROMATASE; ESTROGEN; MESSENGER RNA; VITELLOGENIN; BIOLOGICAL MARKER; ESTROGEN RECEPTOR ALPHA; WATER POLLUTANT;

ABNORMALITY; BIOMARKER; DOSE-RESPONSE RELATIONSHIP; ECOTOXICOLOGY; ENDOCRINE DISRUPTOR; EPIDEMIOLOGY; ESTROGENIC COMPOUND; EXPERIMENTAL STUDY; FISH; HYPOTHESIS TESTING; LABORATORY METHOD; POLLUTION EFFECT; POLLUTION EXPOSURE; POLLUTION TOLERANCE; SUPERFUND;

AGE DISTRIBUTION; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYPRINODONTIFORMES; DEVELOPMENTAL DISORDER; EMBRYO; EMBRYO DEVELOPMENT; ENVIRONMENTAL EXPOSURE; ESTROGEN ACTIVITY; EVOLUTIONARY ADAPTATION; FUNDULUS HETEROCLITUS; GENE EXPRESSION REGULATION; GENE TARGETING; LARVA; MALE; NONHUMAN; POLLUTION; PRIORITY JOURNAL; PROGENY; REPRODUCTIVE TOXICITY; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; DRUG EFFECTS; FEMALE; FUNDULIDAE; GENETICS; METABOLISM; PHYSIOLOGY; TOXICITY; WATER POLLUTANT;

ANIMALS; AROMATASE; BIOLOGICAL MARKERS; ENVIRONMENTAL EXPOSURE; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; FUNDULIDAE; GENE EXPRESSION REGULATION; MALE; VITELLOGENINS; WATER POLLUTANTS, CHEMICAL;

MASSACHUSETTS; NEW BEDFORD HARBOR; UNITED STATES;

CYPRINODONTOIDEI; FUNDULUS HETEROCLITUS;

EID: 77955558573     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2010.05.009     Document Type: Article

References (62)

1. Armstrong P.B., Child J.S. Stages in the normal development of Fundulus heteroclitus. Biol. Bull. 1965, 128:143-168.
2. Anway M.D., Skinner M.K. Transgenerational effects of the endocrine disruptor vinclozolin on the prostate transcriptome and adult onset disease. Prostate 2008, 68:517-529.
3. Baker H.J., Shapiro D.J. Rapid accumulation of vitellogenin messenger RNA during secondary estrogen stimulation of Xenopus laevis. J. Biol. Chem. 1978, 253:4521-4524.
4. Bello S.M. Characterization of resistance to halogenated aromatic hydrocarbons in a population of Fundulus heteroclitus from a marine superfund site. Joint Program in Oceanography/Applied Ocean Science and Engineering 1999, Massachusetts Institute of Technology and Woods Hole Oceanographic Institute, Woods Hole, p. 211.
5. Bello S.M., Franks D.G., Stegeman J.J., Hahn M.E. Acquired resistance to Ah receptor agonists in a population of Atlantic killifish (Fundulus heteroclitus) inhabiting a marine superfund site: in vivo and in vitro studies on the inducibility of xenobiotic metabolizing enzymes. Toxicol. Sci. 2001, 60:77-91.
6. Bergeron J.M., Crews D., McLachlan J.A. PCBs as environmental estrogens: turtle sex determination as a biomarker of environmental contamination. Environ. Health Perspect. 1994, 102:780-781.
7. Black D.E., Gutjahr-Gobell R., Pruell R.J., Bergen B., Mills L., McElroy A.E. Reproduction and polychlorinated biphenyls in Fundulus heteroclitus (Linnaeus) from New Bedford Harbor, Massachusetts, USA. Environ. Toxicol. Chem. 1998, 17:1405-1414.
8. Buckman A.H., Brown S.B., Hoekstra P.F., Solomon K.R., Fisk A.T. Toxicokinetics of three polychlorinated biphenyl technical mixtures in rainbow trout (Oncorhynchus mykiss). Environ. Toxicol. Chem. 2004, 23:1725-1736.
9. Chang H.S., Anway M.D., Rekow S.S., Skinner M.K. Transgenerational epigenetic imprinting of the male germline by endocrine disruptor exposure during gonadal sex determination. Endocrinology 2006, 147:5524-5541.
10. Cook P.M., Robbins J.A., Endicott D.D., Lodge K.B., Guiney P.D., Walker M.K., Zabel E.W., Peterson R.E. Effects of aryl hydrocarbon receptor-mediated early life stage toxicity on lake trout populations in Lake Ontario during the 20th century. Environ. Sci. Technol. 2003, 37:3864-3877.
11. Dasmahapatra A.K., Wimpee B.A., Trewin A.L., Hutz R.J. 2,3,7,8-Tetrachlorodibenzo-p-dioxin increases steady-state estrogen receptor-beta mRNA levels after CYP1A1 and CYP1B1 induction in rat granulosa cells in vitro. Mol. Cell. Endocrinol. 2001, 182:39-48.
12. DeCastro B.R., Korrick S.A., Spengler J.D., Soto A.M. Estrogenic activity of polychlorinated biphenyls present in human tissue and the environment. Environ. Sci. Technol. 2006, 40:2819-2825.
13. Edinger R.S., Mambo E., Evans M.I. Estrogen-dependent transcriptional activation and vitellogenin gene memory. Mol. Endocrinol. 1997, 11:1985-1993.
14. Edmunds S.E., Stubbs A.P., Santos A.A., Wilkinson M.L. Estrogen and androgen regulation of sex hormone binding globulin secretion by a human liver cell line. J. Steroid Biochem. Mol. Biol. 1990, 37:733-739.
15. Faqi A.S., Dalsenter P.R., Merker H.J., Chahoud I. Effects on developmental landmarks and reproductive capability of 3,3',4,4'-tetrachlorobiphenyl and 3,3',4,4',5-pentachlorobiphenyl in offspring of rats exposed during pregnancy. Hum. Exp. Toxicol. 1998, 17:365-372.
16. Foote R.H. Fertility of rabbit sperm exposed in vitro to cadmium and lead. Reprod. Toxicol. 1999, 13:443-449.
17. Gray L.E., Ostby J.S., Kelce W.R. A dose-response analysis of the reproductive effects of a single gestational dose of 2,3,7,8-tetrachlorodibenzo-p-dioxin in male Long Evans Hooded rat offspring. Toxicol. Appl. Pharmacol. 1997, 146:11-20.
18. Gray L.E., Wolf C., Mann P., Ostby J.S. In utero exposure to low doses of 2,3,7,8-tetrachlorodibenzo-p-dioxin alters reproductive development of female Long Evans hooded rat offspring. Toxicol. Appl. Pharmacol. 1997, 146:237-244.
19. Greytak S.R., Callard G.V. Cloning of three estrogen receptors (ER) from killifish (Fundulus heteroclitus): differences in populations from polluted and reference environments. Gen. Comp. Endocrinol. 2007, 150:174-188.
20. Greytak S.R., Champlin D., Callard G.V. Isolation and characterization of two cytochrome P450 aromatase forms in killifish (Fundulus heteroclitus): differential expression in fish from polluted and unpolluted environments. Aquat. Toxicol. 2005, 71:371-389.
21. Hahn M.E., Karchner S.I., Franks D.G., Merson R.R. Aryl hydrocarbon receptor polymorphisms and dioxin resistance in Atlantic killifish (Fundulus heteroclitus). Pharmacogenetics 2004, 14:131-143.
22. Harris M., Zacharewski T., Safe S. Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin and related compounds on the occupied nuclear estrogen receptor in MCF-7 human breast cancer cells. Cancer Res. 1990, 50:3579-3584.
23. Herynk M.H., Fuqua S.A. Estrogen receptor mutations in human disease. Endocr. Rev. 2004, 25:869-898.
24. Honma S., Suzuki A., Buchanan D.L., Katsu Y., Watanabe H., Iguchi T. Low dose effect of in utero exposure to bisphenol A and diethylstilbestrol on female mouse reproduction. Reprod. Toxicol. 2002, 16:117-122.
25. Hyams, D., CurveExpert v.1.3. 2005.
26. Kishida M., McLellan M., Miranda J.A., Callard G.V. Estrogen and xenoestrogens upregulate the brain aromatase isoform (P450aromB) and perturb markers of early development in zebrafish (Danio rerio). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2001, 129:261-268.
27. Klinge C.M., Bowers J.L., Kulakosky P.C., Kamboj K.K., Swanson H.I. The aryl hydrocarbon receptor (AHR)/AHR nuclear translocator (ARNT) heterodimer interacts with naturally occurring estrogen response elements. Mol. Cell. Endocrinol. 1999, 157:105-119.
28. Layton A.C., Sanseverino J., Gregory B.W., Easter J.P., Sayler G.S., Schultz T.W. In vitro estrogen receptor binding of PCBs: measured activity and detection of hydroxylated metabolites in a recombinant yeast assay. Toxicol. Appl. Pharmacol. 2002, 180:157-163.
29. Lind P.M., Eriksen E.F., Sahlin L., Edlund M., Orberg J. Effects of the antiestrogenic environmental pollutant 3,3',4,4',5-pentachlorobiphenyl (PCB #126) in rat bone and uterus: diverging effects in ovariectomized and intact animals. Toxicol. Appl. Pharmacol. 1999, 154:236-244.
30. Loukovaara M., Carson M., Adlercreutz H. Regulation of sex-hormone-binding globulin production by endogenous estrogens in vitro. Biochem. Biophys. Res. Commun. 1995, 206:895-901.
31. Menuet A., Le Page Y., Torres O., Kern L., Kah O., Pakdel F. Analysis of the estrogen regulation of the zebrafish estrogen receptor (ER) reveals distinct effects of ERalpha, ERbeta1 and ERbeta2. J. Mol. Endocrinol. 2004, 32:975-986.
32. Menuet A., Pellegrini E., Brion F., Gueguen M.M., Anglade I., Pakdel F., Kah O. Expression and estrogen-dependent regulation of the zebrafish brain aromatase gene. J. Comp. Neurol. 2005, 485:304-320.
33. Nacci D., Coiro L., Champlain D., Ayaraman S., McKinney R., Gleason W.R.M.T., Specker J.J., Cooper K. Adaptations of wild populations of the estuarine fish Fundulus heteroclitus to persistent environmental contaminants. Mar. Biol. 1999, 134:9-17.
34. Ogawa S., Inoue S., Watanabe T., Orimo A., Hosoi T., Ouchi Y., Muramatsu M. Molecular cloning and characterization of human estrogen receptor betacx: a potential inhibitor ofestrogen action in human. Nucleic Acids Res. 1998, 26:3505-3512.
35. Ohtake F., Baba A., Takada I., Okada M., Iwasaki K., Miki H., Takahashi S., Kouzmenko A., Nohara K., Chiba T., Fujii-Kuriyama Y., Kato S. Dioxin receptor is a ligand-dependent E3 ubiquitin ligase. Nature 2007, 446:562-566.
36. Ohtake F., Takeyama K., Matsumoto T., Kitagawa H., Yamamoto Y., Nohara K., Tohyama C., Krust A., Mimura J., Chambon P., Yanagisawa J., Fujii-Kuriyama Y., Kato S. Modulation of oestrogen receptor signalling by association with the activated dioxin receptor. Nature 2003, 423:545-550.
37. Oppenheimer J.M. The normal stages of Fundulus heteroclitus. Anat. Rec. 1937, 68:1-15.
38. Pait A.S., Nelson J.O. Vitellogenesis in male Fundulus heteroclitus (killifish) induced by selected estrogenic compounds. Aquat Toxicol. 2003, 64:331-342.
39. Pankhurst N., Stacey N., Peter R. An evaluation of techniques for the administration of 17b-estradiol to teleosts. Aquaculture 1986, 52:145-155.
40. Phillips B., Harrison P. Overview of the Endocrine Disruptor Issue 1999, Royal Society of Chemistry, Cambridge, UK.
41. Piferrer F., Donaldson E. Uptake and clearance of exogenous estradiol-17b and testosterone during the early development of coho salmon (Oncorhynchus kisutch), including eggs, alevins and fry. Fish Physiol. Biochem. 1994, 13:219-232.
42. Powell W.H., Bright R., Bello S.M., Hahn M.E. Developmental and tissue-specific expression of AHR1, AHR2, and ARNT2 in dioxin-sensitive and -resistant populations of the marine fish Fundulus heteroclitus. Toxicol. Sci. 2000, 57:229-239.
43. Rankouhi T.R., Sanderson J.T., van Holsteijn I., van Leeuwen C., Vethaak A.D., van den Berg M. Effects of natural and synthetic estrogens and various environmental contaminants on vitellogenesis in fish primary hepatocytes: comparison of bream (Abramis brama) and carp (Cyprinus carpio). Toxicol. Sci. 2004, 81:90-102.
44. Roos A., Greyerz E., Olsson M., Sandegren F. The otter (Lutra lutra) in Sweden-population trends in relation to sigma DDT and total PCB concentrations during 1968-99. Environ. Pollut. 2001, 111:457-469.
45. Saceda M., Lippman M.E., Chambon P., Lindsey R.L., Ponglikitmongkol M., Puente M., Martin M.B. Regulation of the estrogen receptor in MCF-7 cells by estradiol. Mol. Endocrinol. 1988, 2:1157-1162.
46. Saidapur S.K., Gramapurohit N.P., Shanbhag B.A. Effect of sex steroids on gonadal differentiation and sex reversal in the frog, Rana curtipes. Gen. Comp. Endocrinol. 2001, 124:115-123.
47. Sawyer S.J., Gerstner K.A., Callard G.V. Real-time PCR analysis of cytochrome P450 aromatase expression in zebrafish: gene specific tissue distribution, sex differences, developmental programming, and estrogen regulation. Gen. Comp. Endocrinol 2006.
48. Shibata H., Spencer T.E., Onate S.A., Jenster G., Tsai S.Y., Tsai M.J., O'Malley B.W. Role of co-activators and co-repressors in the mechanism of steroid/thyroid receptor action. Recent Prog. Horm. Res. 1997, 52:141-164.
49. Simon P. Q-Gene: processing quantitative real-time RT-PCR data. Bioinformatics 2003, 19:1439-1440.
50. Tarrant A.M., Greytak S.R., Callard G.V., Hahn M.E. Estrogen receptor-related receptors in the killifish Fundulus heteroclitus: diversity, expression, and estrogen responsiveness. J. Mol. Endocrinol. 2006, 37:105-120.
51. Teo B.Y., Tan N.S., Lim E.H., Lam T.J., Ding J.L. A novel piscine vitellogenin gene: structural and functional analyses of estrogen-inducible promoter. Mol. Cell. Endocrinol. 1998, 146:103-120.
52. Tian Y., Ke S., Thomas T., Meeker R.J., Gallo M.A. Regulation of estrogen receptor mRNA by 2,3,7,8-tetrachlorodibenzo-p-dioxin as measured by competitive RT-PCR. J. Biochem. Mol. Toxicol. 1998, 12:71-77.
53. Tian Y., Ke S., Thomas T., Meeker R.J., Gallo M.A. Transcriptional suppression of estrogen receptor gene expression by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). J. Steroid Biochem. Mol. Biol. 1998, 67:17-24.
54. Toscano V., Balducci R., Bianchi P., Guglielmi R., Mangiantini A., Sciarra F. Steroidal and non-steroidal factors in plasma sex hormone binding globulin regulation. J. Steroid Biochem. Mol. Biol. 1992, 43:431-437.
55. Urushitani H., Nakai M., Inanaga H., Shimohigashi Y., Shimizu A., Katsu Y., Iguchi T. Cloning and characterization of estrogen receptor alpha in mummichog, Fundulus heteroclitus. Mol. Cell. Endocrinol. 2003, 203:41-50.
56. Wang X., Porter W., Krishnan V., Narasimhan T.R., Safe S. Mechanism of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)-mediated decrease of the nuclear estrogen receptor in MCF-7 human breast cancer cells. Mol. Cell. Endocrinol. 1993, 96:159-166.
57. Weaver G. PCB contamination in and around New Bedford, Mass. Environ. Sci. Technol. 1983, 18:22A-27A.
58. Willingham E., Crews D. Sex reversal effects of environmentally relevant xenobiotic concentrations on the red-eared slider turtle, a species with temperature-dependent sex determination. Gen. Comp. Endocrinol. 1999, 113:429-435.
59. Wolf C.J., Ostby J.S., Gray L.E. Gestational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) severely alters reproductive function of female hamster offspring. Toxicol. Sci. 1999, 51:259-264.
60. Wormke M., Stoner M., Saville B., Walker K., Abdelrahim M., Burghardt R., Safe S. The aryl hydrocarbon receptor mediates degradation of estrogen receptor alpha through activation of proteasomes. Mol. Cell. Biol. 2003, 23:1843-1855.
61. Yeoh C.G., Schreck C.B., Fitzpatrick M.S., Feist G.W. In vivo steroid metabolism in embryonic and newly hatched steelhead trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 1996, 102:197-209.
62. Zuo Y., Zhang K., Deng Y. Occurrence and photochemical degradation of 17alpha-ethinylestradiol in Acushnet River Estuary. Chemosphere 2006, 63:1583-1590.