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Variable Vitellogenin Response of Japanese Medaka (Oryzias latipes) to Weekly Estrogen Exposure

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Abstract

Japanese medaka (Oryzias latipes) is a valuable model organism in reproductive and developmental toxicity testing. The purpose of this experiment is to assess the response of medaka to aquatic estrogen exposure over the course of 1 year. Each week, three pairs of adult male medaka were exposed separately for 4 days (100% static renewal daily) to 17β-estradiol at a nominal level of 25 μg/l, with a fourth pair of fish exposed separately to an ethanol control. Vitellogenin (VTG) induction was observed each week, with hepatic and plasma VTG levels significantly higher (P < 0.001) than reported for ethanol control specimens. A significant (P < 0.001) increasing trend was observed for plasma VTG results over the duration of the study, whereas a decreasing trend (P = 0.030) of hepatic VTG was evident. A Durbin–Watson test, however, did not demonstrate any serial autocorrelation of hepatic (d = 1.180) or plasma (d = 1.311) VTG levels over the duration of the study. Time-series transformations of the hepatic and plasma VTG data did not reveal any significant seasonal or behavioral patterns. However, significant intermittent peaks in VTG production were observed in both tissue types during the study. These data indicate that some consideration must be taken to time long-term medaka exposures (>20 weeks) in order to eliminate any influence of cyclic changes on plasma VTG response. Alternatively, hepatic cytosolic measurement of VTG appears to show a more sensitive response to aquatic estrogen exposure.

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References

  • Arcand-Hoy LD, Benson WH (1998) Fish reproduction: an ecologically relevant indicator of endocrine disruption. Environ Toxicol Chem 17(1):49–57

    Article  CAS  Google Scholar 

  • Arcand-Hoy LD, Nimrod AC, Benson WH (1998) Endocrine-modulating substances in the environment: estrogenic effects of pharmaceutical products. Int J Toxicol 17:139–158

    Article  CAS  Google Scholar 

  • Balch GC, Mackenzie CA, Metcalfe CD (2004) Alterations to gonadal development and reproductive success in Japanese medaka (Oryzias latipes) exposed to 17α-ethinylestradiol. Environ Toxicol Chem 23(3):782–791

    Article  CAS  Google Scholar 

  • Bowman CJ, Kroll KJ, Hemmer MJ, Folmar LC, Denslow ND (2000) Estrogen-induced vitellogenin mRNA and protein in sheepshead minnow (Cyprinodon variegates). Gen Comp Endocrinol 120:300–313

    Article  CAS  Google Scholar 

  • Cheek AO, Brouwer TH, Carroll S, Manning S, McLachlan JA, Brouwer M (2001) Experimental evaluation of vitellogenin as a predictive biomarker for reproductive disruption. Environ Health Perspect 109(7):681–690

    Article  CAS  Google Scholar 

  • Chikae M, Ikeda R, Hasan Q, Morita Y, Tamiya E (2003) Effects of alkylphenols in adult male medaka: plasma vitellogenin goes up to the level of estrous female. Environ Toxicol Pharm 15(1):33–36

    Article  CAS  Google Scholar 

  • Denslow ND, Chow MM, Folmar LC, Bonomelli S, Heppell SA, Sullivan CV (1996) Development of Antibodies to Teleost Vitellogenins: potential biomarkers for environmental estrogens. In: Bengston DA, Henschel DS (eds) Environmental toxicology and risk assessment: biomarkers and risk assessment, vol 5, ASTM STP 1306. American Society for Testing and Materials, Philadelphia, PA, p 23

    Chapter  Google Scholar 

  • Devore JL, Peck RL (1986) Statistics, the exploration and analysis of data. West, St. Paul, MN

  • Dhillon R, Fox MG (2004) Growth-independent effects of temperature on age and size at maturity in Japanese medaka (Oryzias latipes). Copeia 1:37–45

    Article  Google Scholar 

  • Foran CM, Peterson BN, Benson WH (2002) Transgenerational and developmental exposure of Japanese medaka (Oryzias latipes) to ethinylestradiol results in endocrine and reproductive differences in the response to ethinylestradiol as adults. Toxicol Sci 68(2):389–402

    Article  CAS  Google Scholar 

  • Gronen S, Denslow N, Manning S, Barnes S, Barnes D, Brouwer M (1999) Serum vitellogenin levels and reproductive impairment of Japanese male medaka (Oryzias latipes) expose to 4-tert-octylphenol. Environ Health Perspect 107(5):385–390

    Article  CAS  Google Scholar 

  • Harries JE, Sheahan DA, Jobling S, Matthiessen P, Neall P, Sumpter JP, Tylor T, Zaman N (1997) Estrogenic activity in five United Kingdom rivers detected by measurements of vitellogenin in caged male trout. Environ Toxicol Chem 16(3):34–542

    Article  Google Scholar 

  • Heppell SA, Denslow ND, Folmar LC, Sullivan CV (1995) Universal assay of vitellogenin as a biomarker for environmental estrogens. Environ Health Perspect 103(Suppl 7):9–15

    Article  CAS  Google Scholar 

  • Howdeshell KL, Peterman PH, Judy BM, Taylor JA, Orazio CE, Ruhlen RL, vom Saal FS, Welshons WV (2003) Bisphenol A is released from polycarbonate animal cages into water at room temperature. Environ Health Perspect 111:1180–1187

    CAS  Google Scholar 

  • Idler DR, Ng TB (1983) Teleost gonadotropins: isolation, biochemistry and function. In: Hoar WS, Randal DJ, Donaldson EJ (eds) Fish physiology, vol 9A. Academic press, New York, pp 187–221

    Google Scholar 

  • Ishibashi H, Koyayashi M, Koshiishi T, Moriwaki T, Tachibana K, Tsuchimoto M, Soyano K, Iguchi T, Mori C, Arizono K (2002) Induction of plasma vitellogenin synthesis by the commercial fish diets in male goldfish (Carassius auratus) and dietary phytoestrogens. J Health Science 48:427–434

    Article  CAS  Google Scholar 

  • Lazier CB, MacKay ME (1993) Vitellogenin gene expression in teleost fish. In: Hochachka PW, Mommsen TP (eds) Molecular biology frontiers; Biochemistry and molecular biology of fishes, vol 2. Elsevier, Amsterdam, p 391

    Google Scholar 

  • Metcalfe CD, Gray MA, Kiparissis Y (1999) The Japanese medaka (Oryzias latipes): an in vivo model for assessing the impacts of aquatic contaminants on the reproductive success of fish. In: Rao SS (ed) Impact assessment of hazardous aquatic contaminants. Lewis, Boca Raton, FL, p 29

    Google Scholar 

  • Metcalfe TL, Metcalfe CD, Kiparissis Y, Niimi AJ, Foran CM, Benson WH (2000) Gonadal development and endocrine responses in Japanese medaka (Oryzias latipes) exposed to o, p’-DDT in water or through maternal transfer. Environ Toxicol Chem 19(7):1893–1900

    CAS  Google Scholar 

  • Ng TB, Idler RI (1983) Yolk formation and differentiation in teleost fishes. In: Hoar WS, Randall DJ, Donaldson EM (eds) Fish physiology IX. Academic press, Orlando, FL, p 373

    Google Scholar 

  • Nimrod AC, Benson WH (1997) Assessment of estrogenic activity in fish. In: Rolland RM, Gilbertson M, Peterson RE (eds) Chemically induced alterations in functional development and reproduction of fishes. SETAC, Pensacola, FL, p 87

    Google Scholar 

  • Nimrod AC, Benson WH (1998) Reproduction and development of Japanese medaka following an early life stage exposure to xenoestrogens. Aquat Toxicol 44(1–2):141–156

    Article  CAS  Google Scholar 

  • Schmid T, Gonzalez-Valero J, Rufli H, Dietrich DR (2002) Determination of vitellogenin kinetics in male fathead minnows (Pimephales promelas). Toxicol Lett 131(1–2):65–74

    Article  CAS  Google Scholar 

  • Seki M, Yokota H, Matsubara H, Tsuruda Y, Maeda M, Tadokoro H, Kobayashi K (2002) Effect of ethinylestradiol on the reproduction and induction of vitellogenin and testis-ova in medaka (Oryzias latipes). Environ Toxicol Chem 21(8):1692–1698

    CAS  Google Scholar 

  • Seki M, Yokota H, Matsubara H, Maeda M, Tadokoro H, Kobayashi K (2003) Fish full life-cycle testing for the weak estrogen 4-tert-octylphenol on medaka (Oryzias latipes). Environ Toxicol Chem 22(7):1487–1496

    CAS  Google Scholar 

  • Seki M, Yokota H, Matsubara H, Maeda M, Tadokoro H, Kobayashi K (2004) Fish full life-cycle testing for androgen methyltestosterone on medaka (Oryzias latipes). Environ Toxicol Chem 23(3):774–781

    Article  CAS  Google Scholar 

  • Smith JS, Thomas P (1991) Changes in hepatic estrogen-receptor concentrations during the annual reproductive and ovarian cycles of a marine teleost, the spotted seatrout, Cynoscion nebulosus. Gen Comp Endocrinol 81:234–245

    Article  CAS  Google Scholar 

  • Tabata A, Kashiwada S, Ohnishi Y, Ishikawa H, Miyamoto N, Itoh M, Magara Y (2001) Estrogenic influences of 17β-estradiol, p-nonylphenol and bis-phenol-A on Japanese medaka (Oryzias latipes) at detected environmental concentrations. Water Sci Technol 43(2):109–116

    CAS  Google Scholar 

  • Thompson S, Tilton F, Schlenk D, Benson WH (2000) Comparative vitellogenic responses in three teleost fish species: extrapolation to in situ field studies. Mar Environ Res 50(1–5):185–189

    Article  CAS  Google Scholar 

  • Weber LP, Balch GC, Metcalfe CD, Janz DM (2004) Increased kidney, liver and testicular cell death after chronic exposure to 17α-ethinylestradiol in medaka (Oryzias latipes). Environ Sci Technol 23(3):792–797

    CAS  Google Scholar 

  • Wilkinson L (1998) Systat for windows: statistics version 8.0 edition. SPSS Inc, Chicago, IL

    Google Scholar 

  • Yamamoto TS (1975) Medaka (Killifish) biology and strains. Keigaku, Tokyo, Japan

    Google Scholar 

  • Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice-Hall, Inc., Englewood Cliffs, NJ

    Google Scholar 

  • Zhang L, Khan IA, Foran CM (2002) Characterization of the estrogenic response to genistein in Japanese medaka (Oryzias latipes). Comp Biochem Phys C 132(2):203–211

    Google Scholar 

Download references

Acknowledgements

The authors would like to thank Bethany Peterson for help with the weekly exposures and tissue collection, and Marc Slattery for graduate fellowship support for K.E.M. This research was supported, in part, by the Environmental and Community Health Research program at the University of Mississippi and the United States Environmental Protection Agency (R82-7098-010), though it has not been subjected to the Agency’s peer and policy review and therefore does not necessarily reflect the views of the Agency, and no official endorsement should be inferred.

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Correspondence to Erin R. Bennett.

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Marsh, K.E., Paterson, G., Foran, C.M. et al. Variable Vitellogenin Response of Japanese Medaka (Oryzias latipes) to Weekly Estrogen Exposure. Arch Environ Contam Toxicol 58, 793–799 (2010). https://doi.org/10.1007/s00244-010-9468-7

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  • DOI: https://doi.org/10.1007/s00244-010-9468-7

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