Sexual reprogramming and estrogenic sensitization in wild fish exposed to ethinylestradiol

Environmental Science and Technology

Volumn 43, Issue 4, 2009, Pages 1219-1225

  Lange, Anke ^a   Paull, Gregory C ^a   Coe, Tobias S ^a   Katsu, Yoshinao ^b   Urushitani, Hiroshi ^b   Iguchi, Taisen ^b   Tyler, Charles R ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EARLY LIVES; ESTROGENIC CHEMICALS; ETHINYLESTRADIOL; FEMALE POPULATIONS; FRESHWATER FISHES; FUNCTIONAL CAPABILITIES; OVARIAN DEVELOPMENT; REPRODUCTIVE SUCCESS; RUTILUS RUTILUS; SEXUAL DEVELOPMENT; WASTEWATER TREATMENT WORKS;

EFFLUENTS; FISH; MEATS; WASTEWATER; WASTEWATER RECLAMATION;

WASTEWATER TREATMENT;

ESTROGEN; ETHINYLESTRADIOL;

CONCENTRATION (COMPOSITION); CYPRINID; ESTROGENIC COMPOUND; FEMINIZATION; PHYSIOLOGICAL RESPONSE; POLLUTION EXPOSURE; REPRODUCTIVE SUCCESS; SEX REVERSAL; WILD POPULATION;

ARTICLE; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FEMALE; FEMINIZATION; FRESHWATER FISH; HERMAPHRODITISM; MALE; MATURATION; NONHUMAN; OVARY DEVELOPMENT; REPRODUCTIVE SUCCESS; RIVER; SENSITIZATION; SEX TRANSFORMATION; SEXOLOGY; SEXUAL DEVELOPMENT; WASTE WATER MANAGEMENT;

ANIMALS; ETHINYL ESTRADIOL; FEMALE; FISHES; GENE EXPRESSION REGULATION; GONADS; MALE; SEX CHARACTERISTICS; SEX RATIO; SEXUAL DEVELOPMENT; TIME FACTORS; VITELLOGENINS;

EURASIA; EUROPE; UNITED KINGDOM; WESTERN EUROPE;

RUTILUS RUTILUS;

EID: 64349115774     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es802661p     Document Type: Article

References (50)

1. Hotchkiss, A. K.; Rider, C. V.; Blystone, C. R.; Wilson, V. S.; Hartig, P. C.; Ankley, G. T.; Foster, P. M.; Gray, C. L.; Gray, L. E. Fifteen years after "Wingspread"-environmental endocrine disrupters and human and wildlife health: Where we are today and where we need to go. Toxicol. Sci 2008, 105, 235-259.
2. Harries, J. E.; Janbakhsh, A.; Jobling, S.; Matthlessen, P.; Sumpter, J. P.; Tyler, C. R. Estrogenic potency of effluent from two sewage treatment works in the United Kingdom. Environ. Toxicol. Chem. 1999, 18, 932-937.
3. Jobling, S.; Nolan, M.; Tyler, C. R.; Brighty, G.; Sumpter, J. P. Widespread sexual disruption in wild fish. Environ. Sci. Technol. 1998, 32, 2498-2506.
4. van Aerle, R.; Nolan, M.;Jobling, S.; Christiansen, L. B.; Sumpter, J. P.; Tyler, C. R. Sexual disruption in a second species of wild cyprinid fish (the gudgeon, Gobio gobio) in United Kingdom freshwaters. Environ. Toxicol. Chem. 2001, 20, 2841-2847.
5. Flammarion, P.; Brion, F.; Babut, M.; Garric, J.; Migeon, B.; Noury, P.; Thybaud, E.; Tyler, C. R.; Palazzi, X. Induction of fish vitellogenin and alterations in testicular structure: Preliminary results of estrogenic effects in chub (Leuclscus cephalus). Esptaxicology 2000, 9, 127-135.
6. Hecker, M.; Tyler, C. R.; Hoffmann, M.; Maddix, S.; Karbe, L Plasma biomarkers in fish provide evidence for endocrine modulation in the Elbe River, Germany. Environ. Sci. Technol. 2002, 36, 2311-2321.
7. Vajda, A. M.; Barber, L. B.; Gray, J. L.; Lopez, E. M.; Woodling, J. D.; Norris, D. O. Reproductive disruption in fish downstream from an estrogenic wastewater effluent. Environ. Sci. Technol. 2008, 42, 3407-3414.
8. Aerni, H. R.; Kobler, B.; Rutlshauser, B. V.; Wettstein, F. E.; Fischer, R.; Giger, W.; Hungerbuhler, A.; Marazuela, M. D.; Peter, A.; Schonenberger, R.; Vogeli, A. C.; Suter, M. J. F.; Eggen, R. I. L. Combined biological and chemical assessment of estrogenic activities in wastewater treatment plant effluents. Anal. Bioanal. Chem. 2004, 378, 688-696.
9. Nichols, K. M.; Miles-Richardson, S. R.; Snyder, E. M.; Giesy, J. P. Effects of exposure to municipal wastewater in situ on the reproductive physiology of the fathead minnow (Pimephales prometas). Environ. Toxicol. Chem. 1999, 18, 2001-2012.
10. Bjerregaard, L. B.; Korsgaard, B.; Bjerregaard, P. Intersex in wild roach (Rutilus rutilus) from Danish sewage effluent-receiving streams. Esptoxicol. Environ. Saf. 2006, 64, 321-328.
11. Minier, C.; Caltot, G.; Leboulanger, F.; Hill, E. M. An investigation of the incidence of intersex fish in Seine-Maritime and Sussex regions, Analusis 2000, 28, 801-806.
12. Jobling, S.; Coey, S.; Whitmore, J. G.; Kirne, 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.
13. 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.
14. Rodgers-Gray, T. P.; Jobling, S.; Morris, S.; Kelly, C.; Kirby, S.; Janbakhsh, A.; Harries, J. E.; Waldock, M. J.; Sumpter, J. P.; Tyler, C. R. Long-term temporal changes in the estrogenic composition of treated sewage effluent and its biological effects on fish. Environ. Sci Technol. 2000, 34, 1521-1528.
15. Liney, K. E.; Jobling, S.; Shears, J. A.; Simpson, P.; Tyler, C. R. Assessing the sensitivity of different life stages for sexual disruption in roach (Rutilus rutilus) exposed to effluents from wastewater treatment works. Environ. Health Perspect. 2005, 113, 1299-1307.
16. Strüssmann, C. A.; Nakamura, M. Morphology, endocrinology, and environmental modulation of gonadal sex differentiation in teleost fishes. Fish Physiol. Biochem. 2002, 26, 13-29.
17. Segner, H.; Navas, J. M.; Schäfers, C.; Wenzel, A. Potencies of estrogenic compounds in in vitro screening assays and in life cycle tests with zebrafish in vivo. Esptoxtcol. Environ. Saf. 2003, 54, 315-322.
18. Larsson, D. G. J.; Adolfsson-Erici, M.; Parkkonen, J.; Pettersson, M.; Berg, A. H.; Olsson, P. E.; Forlin, L. Ethinyloestradiol -an undeslred fish contraceptive. Aauat. Toxicol. 1999, 45, 9197.
19. Baronti, C.; Curini, R.; D'Ascenzo, G.; Di Coreia, A.; Gentili, A.; Samperi, R. Monitoring natural and synthetic estrogens at activated sludge sewage treatment plants and in a receiving river water. Environ. Sci. Technol. 2000, 34, 50595066.
20. Belfroid, A. C.; Van der Horst, A.; Vethaak, A. D.; Schäfer, A. J.; Rijs, G. B. J.; Wegener, J.; Cofino, W. P. Analysis and occurrence of estrogenic hormones and their glucuronides in surface water and waste water in The Netherlands. Sci Total Environ. 1999, 225, 101-108.
21. Cargouët, M.; Perdiz, D.; Mouatassim-Souali, A.; TamisierKarolak, S.; Levi, Y. Assessment of river contamination by estrogenic compounds in Paris area (France). Sci Total Envtron. 2004, 324, 55-66.
22. Desbrow, C.; Routledge, E. J.; Brighty, G. C.; Sumpter, J. P.; Waldock, M. Identification of estrogenic chemicals in STW effluent. 1. Chemical fractionation and in vitro biological screening. Environ. Sci Technol. 1998, 32, 1549-1558.
23. Kuch, H. M.; Ballschmiter, K. Determination of endocrinedisrupting phenolic compounds and estrogens in surface and drinking water by HRGC-(NCD-MS in the picogram per liter range. Environ. Sci Technol. 2001, 35, 3201-3206.
24. Rutishauser, B. V.; Pesonen, M.; Escher, B. I.; Ackermann, G. E.; Aerni, H. R.; Suter, M. J. F.; Eggen, R. I. L. Comparative analysis of estrogenic activity in sewage treatment plant effluents involving three in vitro assays and chemical analysis of steroids. Environ. Toxicol. Chem. 2004, 23, 857-864.
25. Temes, T. A.; Stumpf, M.; Mueller, J.; Haberer, K.;Wilken, R. D.; Servos, M. Behavior and occurrence of estrogens in municipal sewage treatment plants - I. Investigations in Germany, Canada and Brazil. Sci Total Environ. 1999, 225, 81-90.
26. Williams, R. J.; Johnson, A. C.; Smith, J. J. L.; Kanda, R. Steroid estrogens profiles along river stretches arising from sewage treatment works discharges. Environ. Sci. Technol. 2003, 37, 1744-1750.
27. Lange, A; Katsu, Y; Ichlkawa, R.; Pauli, G. C.; Chidgey, L. L.; Coe, T. S.; Iguchi, T.; Tyler, C. R. Altered sexual development in roach (Rutilus rutilus) exposed to environmental concentrations of the pharmaceutical 17α-ethinylestradiol and associated expression dynamics of aromatases and estrogen receptors. Toxicol. Sci. 2008, 106, 113-123.
28. Larsen, M. G.; Hansen, K. B.; Henriksen, P. G.; Baatrup, E. Male zebrafish (Danto rerio) courtship behaviour resists the feminising effects of 17 α-ethinyloestradiol - morphological sexual characteristics do not. Aauat. Toxicol. 2008, 87, 234-244.
29. Nash, J. P.; Kime, D. E.; Van der Ven, L. T. M.; Wester, P. W.; Brion, F.; Maack, G.; Stahlschmidt-Allner, P.; Tyler, C. R. Longterm exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environ. Health Perspect. 2004, 112, 1725-1733.
30. Länge, R.; Hutchinson, T. H.; Croudace, C. P.; Siegmund, F.; Schweinfurth, H.; Hampe, P.; Panter, G. H.; Sumpter, J. P. Effects of the synthetic estrogen 17α-ethinylestradiol on the life-cycle of the fathead minnow (Ptmephales prometas). Environ. Toxicol Chem. 2001, 20, 1216-1227.
31. Schultz, I. R.; Skillman, A.; Nicolas, J. M.; Cyr, D. G.; Nagler, J. J. Short-term exposure to 17 alpha-ethynylestradiol decreases the fertility of sexually maturing male rainbow trout (Oncorhynchus mykiss). Environ. Toxicol. Chem. 2003, 22, 1272-1280.
32. Jirtle, R. L.; Sander, M.; Barrett, J. C. Genomic imprinting and environmental disease susceptibility. Environ. Health Perspect. 2000, 108, 271-278.
33. Miyagawa, S.; Katsu, Y.; Watanabe, H.; Iguchi, T. Estrogenindependent activation of erbBs signaling and estrogen receptor a in the mouse vagina exposed neonatally to diethylstilbestrol. Oncogene 2004, 23, 340-349.
34. Pauli, G. C.; Lange, A.; Henshaw, A. C.; Tyler, C. R. Ontogeny of sexual development In the roach (Rutilus rutilus) and its interrelationships with growth and age. I. Morphol. 2008, 269, 884-895.
35. Katsu, Y.; Lange, A.; Ichikawa, R.; Urushitani, H.; Paull, G. C.; Cahill, L. L.; Jobling, S.; Tyler, C. R.; Iguchi, T. Functional associations between two estrogen receptors, environmental estrogens and sexual disruption in the roach (Rutilus rutilus). Environ. Sci Technol. 2007, 41, 3368-3374.
36. Tyler, C. R.; van Aerie, R.; Hutchinson, T. H.; Maddix, S.; Trip, H. An in vivo testing system for endocrine disruptors in fish early life stages using induction of vitellogenin. Environ. Toxicol. Chem 1999, 18, 337-347.
37. Devlin, R. H.; Nagahama, Y. Sex determination and sex differentiation in fish: An overview of genetic, physiological, and environmental influences. Aauaculture 2002, 208, 191-364.
38. Environment Agency. The Identification of Oestrogentc Effects in Wild Fish - Phase II; R&D Technical Report W2-014/TR; Bristol, U.K., 2002; available at http://publlcations.envlronmentagency.gov.uk/epages/eapublications. storefront (accessed June 18, 2008).
39. Thorpe, K. L.; Gross-Sorokin, M.; Johnson, I.; Brighty, G.; Tyler, C. R. An assessment of the model of concentration addition for predicting the estrogenic activity of chemical mixtures in wastewater treatment works effluents. Environ. Health Perspect. 2006, 114, 90-97.
40. Thorpe, K. L.; Cummings, R. I.; Hutchinson, T. H.; Scholze, M.; Brighty, G.; Sumpter, J. P.; Tyler, C. R. Relative potencies and combination effects of steroidal estrogens in fish. Environ. Sci. Technol. 2003, 37, 1142-1149.
41. Moggs, J. G. Molecular responses to xenoestrogens: Mechanistic insights from toxicogenomics. Toxlcology 2005, 213, 177-193.
42. Jirtle, R. L.; Skinner, M. K. Environmental epigenomics and disease susceptibility. Nat. Rev. Genet. 2007, 8, 253-262.
43. McLachlan, J. A; Burow, M.; Chiang, T. C; Li, S. F. Gene imprinting in developmental toxicology: A possible interface between physiology and pathology. Toxicol. Lett. 2001, 120, 161164.
44. Aniagu, S. O.;Williams, T. D.;Allen, Y; Katsladaki, I.; Chipman, J. K. Global genomic methylation levels in the liver and gonads of the three-spine stickleback (Gasterosteus aculeatus) after exposure to hexabromocyclododecane and 17β-oestradiol. Environ. Int. 2008, 34, 310-317.
45. Contractor, R. G.; Foran, C. M.; Li, S. F.; Willett, K. L. Evidence of gender- and tissue-specific promoter methylation and the potential for ethinylestradiol-induced changes in Japanese medaka (Oryztas latipes) estrogen receptor and aromatase genes. I. Toxicol. Environ. Health, A 2004, 67, 1-22.
46. Jobling, S.; Williams, R.; Johnson, A.; Taylor, A.; Gross-Sorokin, M.; Nolan, M.; Tyler, C. R.; van Aerie, R.; Santos, E.; Brighty, G. Predicted exposures to steroid estrogens in U.K. rivers correlate with widespread sexual disruption in wild fish populations. Environ. Health Perspect. 2006, 114, 32-39.
47. Fenske, M.; Maack, G.; Schäfers, C.; Segner, H. An environmentally relevant concentration of estrogen induces arrest of male gonad development in zebrafish Danio rerio. Environ. Toxicol. Chem. 2005, 24, 1088-1098.
48. Maunder, R. J.; Matthiessen, P.; Sumpter, J. P.; Pottinger, T. G. Impaired reproduction in three-spined sticklebacks exposed to ethinyl estradiol as juveniles. Biol Reprod. 2007, 77, 999-1006.
49. Ankley, G. T.; Miller, D. H.; Jensen, K. M.; Villeneuve, D. L.; Martinovic, D. Relationship of plasma sex steroid concentrations in female fathead minnows to reproductive success and population status. Aauat. Toxicol. 2008, 88, 69-74.
50. Tyler, C. R.; Sumpter, J. P. Oocyte growth and development in teleosts. Rev. Fish Biol. Fish. 1996, 6, 287-318.