Decreased vitellogenin inducibility and 17β-estradiol levels correlated with reduced egg production in killifish (Fundulus heteroclitus) from Newark Bay, NJ

Aquatic Toxicology

Volumn 105, Issue 1-2, 2011, Pages 1-12

  Bugel, Sean M ^a,b   White, Lori A ^b   Cooper, Keith R ^a  

^a Rutgers University   (United States)

^b The State University of New Jersey   (United States)

Author keywords

Adaptation; Attenuation; Biomarkers; Dose response; Endocrine disruption; Fecundity; Fish reproduction; Fundulus heteroclitus; Killifish; Vitellogenin

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; VITELLOGENIN;

ADAPTATION; BIOMARKER; EGG; ENDOCRINE DISRUPTOR; ESTROGENIC COMPOUND; ESTUARINE POLLUTION; FECUNDITY; FISH; INHIBITION; PHENOTYPE; PHYSIOLOGY; XENOBIOTICS;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AQUATIC ENVIRONMENT; ARTICLE; CYPRINODONTIFORMES; DOWN REGULATION; ECOTOXICOLOGY; EGG PRODUCTION; EMBRYO; EMBRYO MORTALITY; FEMALE; FEMALE FERTILITY; GEOGRAPHIC DISTRIBUTION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEA POLLUTION; UNITED STATES;

ANIMALS; EMBRYO, NONMAMMALIAN; ENVIRONMENTAL MONITORING; ESTRADIOL; FEMALE; FUNDULIDAE; MALE; OVUM; REPRODUCTION; RNA, MESSENGER; VITELLOGENINS; WATER POLLUTANTS;

NEW JERSEY; NEWARK BAY; UNITED STATES;

CYPRINODONTOIDEI; FUNDULUS HETEROCLITUS;

EID: 79958851569     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2011.03.013     Document Type: Article

References (68)

1. Abramoff M.D., Magelhaes P.J., Ram S.J. Image processing with ImageJ. Biophoton. Int. 2004, 11(7):36-42.
2. Anderson M.J., Miller M.R., Hinton D.E. In vitro modulation of 17β-estradiol-induced vitellogenin synthesis: effects of cytochrome P4501A1 inducing compounds on rainbow trout (Oncorhynchus mykiss) liver cells. Aquat. Toxicol. 1996, 34:327-350.
3. Ankley G.T., Miller D.H., Jensen K.M., Villeneuve D.L., Marinović D. Relationship of plasma sex steroid concentrations in female fathead minnows to reproductive success and population status. Aquat. Toxicol. 2008, 88:69-74.
4. Arcand-Hoy L.D., Benson W.H. Fish reproduction: an ecologically relevant indicator of endocrine disruption. Environ. Toxicol. Chem. 1998, 17(1):49-57.
5. Arzuaga X., Elskus A. Evidence for resistance to benzo[a]pyrene and 3,4,3′,4′-tetrachlorobiphenyl in a chronically polluted Fundulus heteroclitus population. Mar. Environ. Res. 2002, 54(3-5):247-251.
6. Baldigo B.P., Sloan R.J., Smith S.B., Denslow N.D., Blazer V.S., Gross T.S. Polychlorinated biphenyls, mercury, and potential endocrine disruption in fish from the Hudson River, New York, USA. Aquat. Sci. 2006, 68:206-228.
7. Bemanian V., Male R., Goksøyr A. The aryl hydrocarbon receptor-mediated disruption of vitellogenin synthesis in the fish liver: cross-talk between AhR- and ERα-signaling pathways. Comp. Hepatol. 2004, 3(2).
8. 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(7):1405-1414.
9. Bugel S.M., White L.A., Cooper K.R. Impaired reproductive health of killifish (Fundulus heteroclitus) inhabiting Newark Bay NJ, a chronically contaminated estuary. Aquat. Toxicol. 2010, 96(3):182-193.
10. Burnett K.G., Bain L.J., Baldwin W.S., Callard G.V., Cohen S., Di Giulio R.T., Evans D.H., Gómez-Chiarri, Hahn M.E., Hoover C.A., Karchner S.I., Katoh F., Maclatchy D.L., Marshall W.S., Meyer J.N., Nacci D.E., Oleksiak M.F., Rees B.B., Singer T.D., Stegeman J.J., Towle D.W., Van Veld P.A., Vogelbein W.K., Whitehead A., Winn R.N., Crawford D.L. Fundulus as the premier teleost model in environmental biology: opportunities for new insights using genomics. Comp. Biochem. Physiol. Part D: Genomics Proteomics 2007, 2(4):257-286.
11. Casillas E., Misitano D.A., Johnson L.L., Rhodes L.D., Collier T.K., Steine J.E., McCain B.B., Varanasi U. Inducibility of spawning and reproductive success of female English sole (Parophys vetulus) from urban and nonurban areas of Puget Sound, Washington. Mar. Environ. Res. 1991, 21:99-122.
12. Cerdá J., Calman B.G., LaFleur G.J., Limesand S. Pattern of vitellogenesis and follicle maturational competence during the ovarian follicular cycle of Fundulus heteroclitus. Gen. Comp. Endocrinol. 1996, 103:24-35.
13. Dimou K.N., Pecchioli J.A. The New Jersey toxics reduction workplan for NY-NJ Harbor: distribution of PCDD/Fs in ambient waters. Water Air Soil Pollut.: Focus 2006, 6:5-16.
14. Elskus A.A., Monosson E., McElroy A.E., Stegeman J.J., Woltering D.S. Altered CYP1A expression in Fundulus heteroclitus adults and larvae: a sign of pollutant resistance?. Aquat. Toxicol. 1999, 45:99-113.
15. Fitzsimons J.D. A critical review of the effects of contaminants on early life stage mortality of lake trout in the Great Lakes. J. Great Lakes Res. 1995, 21(Suppl. 1):267-276.
16. Franczak A., Nynca A., Valdez K.E., Mizinga K.M., Petroff B.K. Effects of acute and chronic exposure to the aryl hydrocarbon receptor agonist 2,3,7,8-tetrachlorodibenzo-p-dioxin on the transition to reproductive senescence in female Sprague-Dawley rats. Biol. Reprod. 2006, 74:125-130.
17. Gräns J., Wassmur B., Celander M.C. One-way inhibiting cross-talk between arylhydrocarbon receptor (AhR) and estrogen receptor (ER) signaling in primary cultures of rainbow trout hepatocytes. Aquat. Toxicol. 2010, 100:263-270.
18. 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.
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., Tarrant A.M., Nacci D., Hahn M.E., Callard G.V. Estrogen responses in killifish (Fundulus heteroclitus) from polluted and unpolluted environments are site- and gene-specific. Aquat. Toxicol. 2010, 99:291-299.
21. Hsiao S., Greeley M.S., Wallace R.A. Reproductive cycling in female Fundulus heteroclitus. Biol. Bull. 1994, 186:271-284.
22. Huntley S.L., Bonnevie N.L., Wenning R.J. Polycyclic aromatic hydrocarbon and petroleum hydrocarbon contamination in sediment from the Newark Bay Estuary, New Jersey. Arch. Environ. Contam. Toxicol. 1995, 28:93-107.
23. Hutz R.J. Reproductive endocrine disruption by environmental xenobiotics that modulate the estrogen-signaling pathway, particularly tetrachlorodibenzo-p-dioxin (TCDD). J. Reprod. Dev. 1999, 45(1):1-12.
24. Iannuzzi T.J., Armstrong T.N., Long E.R., Iannuzzi J., Ludwig D.F. Sediment quality triad assessment of an industrialized estuary of the northeastern USA. Environ. Monit. Assess. 2008, 139:257-275.
25. 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(2):194-202.
26. Kanungo J., Petrino T.R., Wallace R.A. Oogenesis in Fundulus heteroclitus. VI. Establishment and verification of conditions for vitellogenin incorporation by oocytes in vitro. J. Exp. Zool. 1990, 254:313-321.
27. Kidd K.A., Blanchfield P.J., Mills K.H., Palace V.P., Evans R.E., Lazorchak J.M., Flick R.W. Collapse of a fish population after exposure to a synthetic estrogen. Proc. Natl. Acad. Sci. U.S.A. 2007, 104(21):8897-8901.
28. King Heiden T.C., Carvan M.J., Hutz R.J. Inhibition of follicular development, vitellogenesis, and serum 17ß-estradiol concentrations in zebrafish following chronic, sublethal dietary exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Chemosphere 2006, 90(2):490-499.
29. King Heiden T.C., Struble C.A., Rise M.L., Hessner M.J., Hutz R.J., Carvan M.J. Molecular targets of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) within the zebrafish ovary: insights into TCDD-induced endocrine disruption and reproductive toxicity. Reprod. Toxicol. 2008, 25:47-57.
30. King Heiden T.C., Spitzhergen J., Heideman W., Peterson R.E. Persistent adverse effects on health and reproduction caused by exposure of zebrafish to 2,3,7,8-tetrachlorodibenzo-p-dioxin during early development and gonad differentiation. Toxicol. Sci. 2009, 109(1):75-87.
31. LaFleur G.J., Byrne M.B., Kanungo J., Nelson L.A., Greenberg R.M., Wallace R.A. Fundulus heteroclitus vitellogenin: the deduced primary structure of a piscine precursor to noncrystalline, liquid-phase yolk protein. J. Mol. Evol. 1995, 41:505-521.
32. LaFleur G.J., Byrne M.B., Haux C., Greenberg R., Wallace R.A. Liver-derived cDNAs: vitellogenins and vitelline envelope protein precursors (choriogenins). Proceedings of the 5th International Symposium on the Reproductive Physiology of Fish 1995, 336-338. The University of Texas at Austin, Austin, TX. F.W. Goetz, P. Thomas (Eds.).
33. LaFleur G.J., Raldúa D., Fabra M., Carnevali O., Denslow N., Wallace R.A., Cerdá J. Derivation of major yolk proteins from parental vitellogenins and alternative processing during oocyte maturation in Fundulus heteroclitus. Biol. Reprod. 2005, 73:815-824.
34. Litten S. New York/New Jersey Harbor Contaminant Assessment and Reduction Project (CARP) 2003, New York State Department of Environmental Conservation, Albany, New York, Available from: http://www.hudsonriver.org/.
35. McArdle M.E., McElroy A.E., Elskus A.A. Enzymatic and estrogenic responses in fish exposed to organic pollutants in the New York-New Jersey (USA) Harbor Complex. Environ. Toxicol. Chem. 2004, 4:953-959.
36. McArdle M., Elskus A., McElroy A., Larsen B., Benson W., Schlenk D. Estrogenic and CYP1A response of mummichogs and sunshine bass to sewage effluent. Mar. Environ. Res. 2000, 50:175-179.
37. Menuet A., Adrio F., Kah O., Pakdel F. Regulation and function of estrogen receptors: comparative aspects. Hormones and Their Receptors in Fish Reproduction 2005, World Scientific Publishing Company, Singapore. P. Melamed, N. Sherwood (Eds.).
38. Mortensen A.S., Arukwe A. Interactions between estrogen- and Ah-Receptor signaling pathways in primary culture of salmon hepatocytes exposed to nonylphenol and 3,3′,4,4′-tetrachlorobiphenyl (congener 77). Comp. Hepatol. 2007, 6(2).
39. Miller D.H., Jensen K.M., Villeneuve D.L., Kahl M.D., Makynen E.A., Durhan E.J., Ankley G.T. Linkage of biochemical responses to population-level effects: a case study with vitellogenin in the fathead minnow (Pimephales promelas). Environ. Toxicol. Chem. 2007, 26(3):521-527.
40. Muñoz G.R., Panero M.A., Powers C.W. Pollution Prevention and Management Strategies for Dioxins in the New York/New Jersey Harbor 2006, New York Academy of Sciences, New York, NY, Available from: http://www.nyas.org.
41. Nacci D.E., Champlin D., Jayaraman S. Adaptation of the estuarine fish Fundulus heteroclitus (Atlantic killifish) to polychlorinated biphenyls (PCBs). Estuaries Coasts 2010, 33:853-864.
42. Nash J.P., Kime D.E., Van der Ven L.T., Wester P.W., Brion F., Stahlschmidt-Allner P., Tyler C.R. Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environ. Health Perspect. 2004, 112:1725-1733.
43. Navas J.M., Segner H. Antiestrogenicity of ß-naphthoflavone and PAHs in cultured rainbow trout hepatocytes: evidence for a role of the aryl hydrocarbon receptor. Aquat. Toxicol. 2000, 51:79-92.
44. Nelson E.R., Habibi H.R. Functional significance of nuclear estrogen receptor subtypes in the liver of goldfish. Endocrinology 2010, 151(4):1668-1676.
45. NY-NJ Harbor Estuary Program (NY-NJ HEP), 2006. Harbor-wide water quality monitoring report for the New York, New Jersey Harbor Estuary. Available from: http://www.harborestuary.org/.
46. Ohtake F., Baba A., Fujii-Kuriyama Y., Kato S. Intrinsic AhR function underlies cross-talk of dioxins with sex hormone signaling. Biochem. Biophys. Res. Commun. 2008, 370:541-546.
47. Pait A.S., Nelson J.O. Vitellogenesis in male Fundulus heteroclitus (killifish) induced by selected estrogenic compounds. Aquat. Toxicol. 2003, 64:331-342.
48. Panero M., Boehme S., Muñoz G. Pollution Prevention and Management Strategies for Polychlorinated Biphenyls in the New York/New Jersey Harbor 2005, New York Academy of Sciences, New York, NY, Available from: http://www.nyas.org.
49. Patiño R., Sullivan C.V. Ovarian follicle growth, maturation, and ovulation in teleost fish. Fish Physiol. Biochem. 2002, 26:57-70.
50. Petroff B.K., Gao X., Roxman K.K., Terranova P.F. Interaction of estradiol and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in an ovulation model: evidence for systemic potentiation and local ovarian effects. Reprod. Toxicol. 2000, 14:247-255.
51. Prince R., Cooper K.R. Comparison of the effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on chemically impacted and non-impacted subpopulations of Fundulus heteroclitus I: TCDD toxicity. Environ. Toxicol. Chem. 1995, 14:579-587.
52. Prince R., Cooper K.R. Comparison of the effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on chemically impacted and non-impacted subpopulations of Fundulus heteroclitus II: Metabolic considerations. Environ. Toxicol. Chem. 1995, 14:589-596.
53. Rempel M.A., Shlenk D. Effects of environmental estrogens and antiandrogens on endocrine function, gene regulation, and health in fish. Int. Rev. Cell Mol. Biol. 2008, 267:207-252.
54. Safe S., Wormke M. Inhibitory aryl hydrocarbon receptor-estrogen receptor α cross-talk and mechanisms of action. Chem. Res. Toxicol. 2003, 16(7):807-816.
55. Sellin M.K., Snow D.D., Kolok A.S. Reductions in hepatic vitellogenin and estrogen receptor alpha expression by sediments from an agriculturally impacted waterway. Aquat. Toxicol. 2010, 96:103-108.
56. Selman K., Wallace R.A. Oogenesis in Fundulus heteroclitus III. Vitellogenesis. J. Exp. Zool. 1983, 226:441-457.
57. Shi Z., Valdez K.E., Ting A.Y., Franczak A., Gum S.L., Petroff B.K. Ovarian endocrine disruption underlies premature reproductive senescence following environmentally relevant chronic exposure to the aryl hydrocarbon receptor agonist 2,3,7,8-tetrachlorodibenzo-p-dioxin. Biol. Reprod. 2007, 76:198-202.
58. 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.
59. Taylor M.H., Leach G.J., DiMichele L., Levitan W.M., Jacob W.F. Lunar spawning cycle in the mummichog Fundulus heteroclitus (Pisces Cyprinodontidae). Copeia 1979, 2:291-297.
60. Thomas P. The endocrine system. The Toxicology of Fishes 2008, 457-488. Taylor & Francis Group, FL. R.T. Di Giulio, D.E. Hinton (Eds.).
61. Thorpe K.L., Benstead R., Hutchinson T.H., Tyler C.R. Associations between altered vitellogenin concentrations and adverse health effects in fathead minnow (Pimephales promelas). Aquat. Toxicol. 2007, 85:176-183.
62. Todorov J.R., Elskus A.A., Schlenk D., Ferguson P.L., Brownawell B.J., McElroy A.E. Estrogenic responses of larval sunshine bass (Morone saxatilis×M. chrysops) exposed to New York city sewage effluent. Mar. Environ. Res. 2002, 54:691-695.
63. Tyler C.R., Sumpter J.P. Oocyte growth and development in teleosts. Rev. Fish Biol. Fish. 1996, 6:287-318.
64. 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.
65. Vaccaro E., Meucci V., Intorre L., Soldani G., Di Bello D., Longo V., Gervasi P.G., Pretti C. Effects of 17β-estradiol, 4-nonylphenol and PCB 126 on the estrogenic activity and phase 1 and 2 biotransformation enzymes in male sea bass (Dicentrarchus labrax). Aquat. Toxicol. 2005, 75(4):293-305.
66. Wilson, T.P., Bonin, J.L., 2007. Concentrations and loads of organic compounds and trace elements in tributaries to Newark and Raritan Bays, New Jersey. U.S. Geological Survey Scientific Investigations Report 2007-5059, 177 p. Available from: http://www.usgs.gov/.
67. Wormke M., Stoner M., Saville B., Walker K., Abdelrahim M., Burghardt R., Safe S. The aryl hydrocarbon receptor mediates degradation of estrogen receptor α through activation of proteasomes. Mol. Cell. Biol. 2003, 23(6):1843-1855.
68. Zabel E.W., Cook P.M., Peterson R.E. Toxic equivalency factors of polychlorinated dibenzo-p-dioxin, dibenzofuran and biphenyl congeners based on early life stage mortality in rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 1995, 21:315-328.