17α-Ethynylestradiol alters the immune response of the teleost gilthead seabream (Sparus aurata L.) both in vivo and in vitro

Developmental and Comparative Immunology

Volumn 36, Issue 3, 2012, Pages 547-556

  Cabas, Isabel ^a   Liarte, Sergio ^a   García Alcázar, Alicia ^b   Meseguer, José ^a   Mulero, Victoriano ^a   García Ayala, Alfonsa ^a  

^a UNIVERSITY OF MURCIA   (Spain)

^b Instituto Español de Oceanografía   (Spain)

Author keywords

Cytokines; Immune endocrine interactions; Inflammation; Macrophages; Vaccination

Indexed keywords

ALUMINUM; CANCER GROWTH FACTOR; ETHINYLESTRADIOL; HEMOCYANIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA;

ANTIBODY SPECIFICITY; ANTIBODY TITER; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EFFLUENT; ESTRADIOL BLOOD LEVEL; GENE EXPRESSION; GENE EXPRESSION PROFILING; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; LEUKOCYTE; MACROPHAGE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOCYTOSIS; PRIORITY JOURNAL; TELEOST; WASTE WATER MANAGEMENT;

SPARUS AURATA; TELEOSTEI;

EID: 84855830541     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2011.09.011     Document Type: Article

References (62)

1. Ahmed S.A. The immune system as a potential target for environmental estrogens (endocrine disrupters): a new emerging field. Toxicology 2000, 150:191-206.
2. Baronti C., Curini R., D́Ascenzo G., Di Corcia 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, 34:5059-5066.
3. Bols N.C., Brubacher J.L., Ganassin R.C., Lee L.E. Ecotoxicology and innate immunity in fish. Dev. Comp. Immunol. 2001, 25:853-873.
4. Brown K.H., Schultz I.R., Nagler J.J. Reduced embryonic survival in rainbow trout resulting from paternal exposure to the environmental estrogen 17alpha-ethynylestradiol during late sexual maturation. Reproduction 2007, 134:659-666.
5. 2-estradiol) versus a pharmacologic synthetic estrogen (17î±-ethinyl estradiol). Comparative and General Pharmacology. Master of Science in Biomedical & Veterinary Sciences 2007, 1-144. Blacksburg, Virginia.
6. Cabas I., Chaves-Pozo E., García Alcaraz A., Meseguer J., Mulero V., García-Ayala A. Dietary intake of 17a-ethinylestradiol promotes leukocytes infiltration in the gonad of the hermaphrodite gilthead seabream. Mol. Immunol. 2011, 48:2079-2086.
7. Chaves-Pozo E., Pelegrín P., Mulero V., Meseguer J., García-Ayala A. A role for acidophilic granulocytes in the testis of the gilthead seabream (Sparus aurata L., Teleostei). J. Endocrinology 2003, 179:165-174.
8. Chaves-Pozo E., Mulero V., Meseguer J., García Ayala A. An overview of cell renewal in the testis throughout the reproductive cycle of a seasonal breeding teleost. The gilthead seabream (Sparus aurata L.). Biol. Reprod. 2005, 72:593-601.
9. Chaves-Pozo E., Mulero V., Meseguer J., García-Ayala A. Professional phagocytic granulocytes of the bony fish gilthead seabream display functional adaptation to testicular microenvironment. J. Leukoc. Biol. 2005, 78:345-351.
10. Chaves-Pozo E., Liarte S., Vargas-Chacoff L., García-López A., Mulero V., Meseguer J. 17Beta-estradiol triggers postspawning in spermatogenically active gilthead seabream (Sparus aurata L.) males. Biol. Reprod. 2007, 76:142-148.
11. Chaves-Pozo E., Arjona F.J., García-López A., García-Alcázar A., Meseguer J., García-Ayala A. Sex steroids and metabolic parameter levels in a seasonal breeding fish (Sparus aurata L.). Gen. Comp. Endocrinol. 2008, 156:531-536.
12. Colborn T., vom Saal F.S., Soto A.M. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ. Health Perspect. 1993, 101:378-384.
13. De Wit M., Keil D., van der Ven K., Vandamme S., Witters E., De Coen W. An integrated transcriptomic and proteomic approach characterizing estrogenic and metabolic effects of 17 alpha-ethinylestradiol in zebrafish (Danio rerio). Gen. Comp. Endocrinol. 2010, 167:190-201.
14. 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.
15. Esteban M.A., Mulero V., Muñoz J., Meseguer J. Methodological aspects of assessing phagocytosis of Vibrio anguillarum by leucocytes of gilthead seabream (Sparus aurata L.) by flow cytometry and electron microscopy. Cell Tissue Res. 1998, 293:133-141.
16. Filby A.L., Neuparth T., Thorpe K.L., Owen R., Galloway T.S., Tyler C.R. Health impacts of estrogens in the environment, considering complex mixture effects. Environ. Health Perspect. 2007, 115:1704-1710.
17. García-Reyero N., Lavelle C.M., Escalon B.L., Martinovic D., Kroll K.J., Sorensen P.W., Denslow N.D. Behavioral and genomic impacts of a wastewater effluent on the fathead minnow. Aquat. Toxicol. 2011, 101:38-48.
18. Härkönen P.L., Väänänen H.K. Monocyte-macrophage system as a target for estrogen and selective estrogen receptor modulators. Ann. NY Acad. Sci. 2006, 1089:218-227.
19. Hashimoto S., Watanabe E., Ikeda M., Terao Y., Strüssmann C.A., Inoue M., Hara A. Effects of ethinylestradiol on medaka (Oryzias latipes) as measured by sperm motility and fertilization success. Arch. Environ. Contam. Toxicol. 2009, 56:253-259.
20. Hinteman T., Schneider C., Schöler H.F., Schneider R.J. Field study using two immunoassays for the determination of estradiol and ethinylestradiol in the aquatic environment. Water Res. 2006, 40:2287-2294.
21. Hogan N.S., Currie S., LeBlanc S., Hewitt L.M., MacLatchy D.L. Modulation of steroidogenesis and estrogen signalling in the estuarine killifish (Fundulus heteroclitus) exposed to ethinylestradiol. Aquat. Toxicol. 2010, 98:148-156.
22. Hou Y.Y., Suzuki Y., Aida K. Effects of steroid hormones on immunoglobulin M (IgM) in rainbow trout, Oncorhynchus mykiss. Fish Physiol. Biochem. 1999, 20:155-162.
23. Iwanowicz L.R., Ottinger C.A. Estrogens, estrogen receptors and their role as immunoregulators in fish. Fish Defenses. Vol. 1: Immunology 2009, 277-322. Science Publisher, Enfield. G. Zaccone, J. Meseguer, A. García-Ayala, B.G. Kapoor (Eds.).
24. Jin Y., Chen R., Liu W., Fu Z. Effect of endocrine disrupting chemicals on the transcription of genes related to the innate immune system in the early developmental stage of zebrafish (Danio rerio). Fish Shellfish Immunol. 2010, 28:854-861.
25. Johnson A.C., Aerni H.-R., Gerritsen A., Gibert M., Giger W., Hylland K., Jürgens M., Nakari T., Pickering A., Suter M.J., Svenson A., Wettstein F.E. Comparing steroid estrogen, and nonylphenol content across a range of European sewage plants with different treatment and management practices. Water Res. 2005, 39:47-58.
26. Kaptaner, B., Unal, G., 2010. Effects of 17alpha-ethynylestradiol and nonylphenol on liver and gonadal apoptosis and histopathology in Chalcalburnus tarichi. Environ. Toxicol. 1-13.
27. Kidd K.A., Blanchfield P.J., Mills K.H., Palace V.P., Evans R.E., Lazorchak J.M., Flick R.M. Collapse of a fish population after exposure to a synthetic estrogen. Proc. Natl. Acad. Sci. USA 2007, 104:8897-8901.
28. Köllner B., Wasserrab B., Kotterba G., Fischer U. Evaluation of immune functions of rainbow trout (Oncorhynchus mykiss)-how can environmental influences be detected?. Toxicol. Lett. 2002, 131:83-95.
29. Lai K.M., Scrimshaw M.D., Lester J.N. The effects of natural and synthetic steroid estrogens in relation to their environmental occurrence. Crit. Rev. Toxicol. 2002, 32:113-132.
30. Lai K.M., Scrimshaw M.D., Lester J.N. Prediction of the bioaccumulation factors and body burden of natural and synthetic estrogens in aquatic organisms in the river systems. Sci. Total Environ. 2002, 289:159-168.
31. Lange A., Katsu Y., Ichikawa R., Paull 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 17alpha-ethinylestradiol and associated expression dynamics of aromatases and estrogen receptors. Toxicol. Sci. 2008, 106:113-123.
32. Larsson D.G.J., Adolfsson-Erici M., Parkkonen J., Pettersson M., Berg A.H., Olsson P.E., Förlin L. Ethinyloestradiol-an undesired fish contraceptive?. Aquat. Toxicol. 1999, 45:91-97.
33. Law W.Y., Chen W.H., Song Y.L., Dufour S., Chang C.F. Differential in vitro suppressive effects of steroids on leukocyte phagocytosis in two teleosts, tilapia and common carp. Gen. Comp. Endocrinol. 2001, 121:163-172.
34. Legler J., Zeinstra L.M., Schuitemaker F., Lanser P.H., Bogerd J., Brouwer A., Vethaak A.D., De Voogt P., Murk A.J., Van der Burg B. Comparison of in vivo and in vitro reporter gene assays for short-term screening of estrogenic activity. Environ. Sci. Technol. 2002, 36:4410-4415.
35. Liarte S., Chaves-Pozo E., García Alcázar A., Mulero V., Meseguer J., García Ayala A. Testicular involution prior to sex change in gilthead seabream is characterized by a decrease in DMRT1 gene expression and by massive leukocyte infiltration. Reprod. Biol. Endocrinol. 2007, 5:20-35.
36. Liarte S., Chaves-Pozo E., Abellan E., Meseguer J., Mulero V., García-Ayala A. 17β-Estradiol regulates gilthead seabream professional phagocyte responses through macrophage activation. Dev. Comp. Immunol. 2011, 35:19-27.
37. Liarte S., Chaves-Pozo E., Abellan E., Meseguer J., Mulero V., Canario A.V., García-Ayala A. Estrogen-responsive genes in macrophages of the bony fish gilthead seabream: A transcriptomic approach. Dev. Comp. Immunol. 2011, 35:840-849.
38. Marlatt V.L., Lakoff J., Crump K., Martyniuk C.J., Watt J., Jewell L., Atkinson S., Blais J.M., Sherry J., Moon T.W., Trudeau V.L. Sex- and tissue-specific effects of waterborne estrogen on estrogen receptor subtypes and E2-mediated gene expression in the reproductive axis of goldfish. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2010, 156:92-101.
39. Martyniuk C.J., Gerrie E.R., Popesku J.T., Ekker M., Trudeau V.L. Microarray analysis in the zebrafish (Danio rerio) liver and telencephalon after exposure to low concentration of 17alpha-ethinylestradiol. Aquat. Toxicol. 2007, 84:38-49.
40. Milla S., Depiereux S., Kestemont P. The effects of estrogenic and androgenic endocrine disruptors on the immune system of fish: a review. Ecotoxicology 2011, 20:305-319.
41. Mulero V., Pelegrín P., Sepulcre M.P., Muñoz J., Meseguer J. A fish cell surface receptor defined by a mAb mediates leukocyte aggregation and deactivation. Dev. Comp. Immunol. 2001, 25:619-627.
42. Nash J.P., Kime D.E., Van der Ven L.T., Wester P.W., Brion F., Maack G., 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. Peters R.E., Courtenay S.C., Cagampan S., Hewitt M.L., MacLatchy D.L. Effects on reproductive potential and endocrine status in the mummichog (Fundulus heteroclitus) after exposure to 17alpha-ethynylestradiol in a short-term reproductive bioassay. Aquat. Toxicol. 2007, 85:154-166.
44. Pinto P.I., Passos A.L., Martins R.S., Power D.M., Canário A.V. Characterization of estrogen receptor beta b in sea bream (Sparus auratus): phylogeny, ligand-binding, and comparative analysis of expression. Gen. Comp. Endocrinol. 2006, 145:197-207.
45. Roca F.J., Sepulcre M.P., López-Castejón G., Meseguer J., Mulero V. The colony-stimulating factor-1 receptor is a specific marker of macrophages from the bony fish gilthead seabream. Mol. Immunol. 2006, 43:1418-1423.
46. Rodríguez L., Begtashi I., Zanuy S., Carrillo M. Development and validation of an enzyme inmunoassay for testosterone: effects of photoperiod on plasma testosterone levels and gonadal development in male sea bass (Dicentrarchus labrax L.) at puberty. Fish Physiol. Biochem. 2000, 23:141-150.
47. Saaristo M., Craft J.A., Lehtonen K.K., Björk H., Lindström K. Disruption of sexual selection in sand gobies (Pomatoschistus minutus) by 17alpha-ethinyl estradiol, an endocrine disruptor. Horm. Behav. 2009, 55:530-537.
48. Shved N., Berishvili G., Häusermann E., D'Cotta H., Baroiller J.F., Eppler E. Challenge with 17α-ethinylestradiol (EE2) during early development persistently impairs growth, differentiation, and local expression of IGF-I and IGF-II in immune organs of tilapia. Fish Shellfish Immunol. 2009, 26:524-530.
49. Snyder S.A., Keith T.L., Verbrugge D.A., Snyder E.M., Gross T.S., Kannan K., Giesy J.P. Analytical methods for detection of selected estrogenic compounds in aqueous mixtures. Environ. Sci. Technol. 1999, 33:2814-2820.
50. Straub R.H. The complex role of estrogens in inflammation. Endocr. Rev. 2007, 28:521-574.
51. Sumpter J.P., Jobling S. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ. Health Perspect. 1995, 103:173-178.
52. Sumpter J.P., Johnson A.C. Lessons from endocrine disruption and their application to other issues concerning trace organics in the aquatic environment. Environ Sci Technol. 2005, 39:4321-4332.
53. Ternes T.A., Kreckel P., Mueller J. Behaviour and occurrence of estrogens in municipal sewage treatment plants-II. Aerobic batch experiments with activated sludge. Sci. Total Environ. 1999, 225:91-99.
54. 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.
55. Tilton S.C., Foran C.M., Benson W.H. Relationship between ethinylestradiol-mediated changes in endocrine function and reproductive impairment in Japanese medaka (Oryzias latipes). Environ. Toxicol. Chem. 2005, 24:352-359.
56. 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.
57. Vos J.G., Dybing E., Greim H.A., Ladefoged O., Lambre C., Tarazona J.V., Brandt I., Vethaak A.D. Health effects of endocrine-disrupting chemicals on wildlife, with special reference to the European situation. Crit. Rev. Toxicol. 2000, 30:71-133.
58. Wang R., Belosevic M. Estradiol increases susceptibility of goldfish to Trypanosoma danilewskyi. Dev. Comp. Immunol. 1994, 18:377-387.
59. Wenger M., Sattler U., Goldschmidt-Clermont E., Segner H. 17Beta-estradiol affects the response of complement components and survival of rainbow trout (Oncorhynchus mykiss) challenged by bacterial infection. Fish Shellfish Immunol. 2011, 31:90-97.
60. Xu H., Yang J., Wang Y., Jiang Q., Chen H., Song H. Exposure to 17alpha-ethynylestradiol impairs reproductive functions of both male and female zebrafish (Danio rerio). Aquat. Toxicol. 2008, 88:1-8.
61. Yamaguchi T., Watanuki H., Sakai M. Effects of estradiol, progesterone and testosterone on the function of carp, Cyprinus carpio, phagocytes in vitro. Comp. Biochem. Physiol. C. Toxicol. Pharmacol. 2001, 129:49-55.
62. Ying G.G., Kookana R.S., Dillon P. Sorption and degradation of selected five endocrine disrupting chemicals in aquifer material. Water Res. 2003, 37:3785-3791.