Environmentally relevant exposure to 17α-ethinylestradiol affects the telencephalic proteome of male fathead minnows

Aquatic Toxicology

Volumn 98, Issue 4, 2010, Pages 344-353

  Martyniuk, Christopher J ^a   Kroll, Kevin J ^a   Doperalski, Nicholas J ^a   Barber, David S ^a   Denslow, Nancy D ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

ITRAQ; Map Tau protein; Pimephales promelas; Quantitative proteomics

Indexed keywords

CALMODULIN; EPENDYMIN; ESTRADIOL; ETHINYLESTRADIOL; HISTONE; MESSENGER RNA; PHOSPHOPROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ABUNDANCE; CONCENTRATION (COMPOSITION); ECOTOXICOLOGY; ESTROGENIC COMPOUND; FISH; NERVOUS SYSTEM; POLLUTION EXPOSURE; PROTEIN; PROTEOMICS; RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ECOTOXICOLOGY; ENVIRONMENTAL EXPOSURE; ESTRADIOL BLOOD LEVEL; FEEDBACK SYSTEM; GENE EXPRESSION; LONG TERM POTENTIATION; MALE; NERVE CELL NETWORK; NEUROENDOCRINE SYSTEM; NONHUMAN; NUCLEOTIDE SEQUENCE; PIMEPHALES PROMELAS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN SYNTHESIS REGULATION; PROTEOMICS; SIGNAL TRANSDUCTION; TELENCEPHALON; TRANSCRIPTION REGULATION; WATER CONTAMINATION;

ANIMALS; CYPRINIDAE; ENVIRONMENTAL EXPOSURE; ETHINYL ESTRADIOL; FISH PROTEINS; MALE; PROTEOME; TELENCEPHALON; WATER POLLUTANTS, CHEMICAL;

PIMEPHALES PROMELAS; VERTEBRATA;

EID: 77953685523     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2010.03.007     Document Type: Article

References (49)

1. Anglade I., Zandbergen T., Kah O. Origin of the pituitary innervation in the goldfish. Cell. Tissue Res. 1993, 273:345-355.
2. Ankley G.T., Miller D.H., Jensen K.M., Villeneuve D.L., Martinović D. Relationship of plasma sex steroid concentrations in female fathead minnows to reproductive success and population status. Aquat. Toxicol. 2008, 88:69-74.
3. Bowman C.J., Kroll K.J., Gross T.G., Denslow N.D. Estradiol-induced gene expression in largemouth bass (Micropterus salmoides). Mol. Cell. Endocrinol. 2002, 196:67-77.
4. Brännvall K., Korhonen L., Lindholm D. Estrogen-receptor-dependent regulation of neural stem cell proliferation and differentiation. Mol. Cell. Neurosci. 2002, 21:512-520.
5. Cardwell J.R., Sorensen P.W., Van der Kraak G.J., Liley N.R. Effect of dominance status on sex hormone levels in laboratory and wild-spawning male trout. Gen. Comp. Endocrinol. 1996, 101:333-341.
6. Chen F., David D., Ferrari A., Götz J. Posttranslational modifications of tau-role in human tauopathies and modeling in transgenic animals. Curr. Drug Targets. 2004, 5:503-515.
7. Colman J.R., Baldwin D., Johnson L.L., Scholz N.L. Effects of the synthetic estrogen, 17alpha-ethinylestradiol, on aggression and courtship behavior in male zebrafish (Danio rerio). Aquat. Toxicol. 2009, 91:346-354.
8. Córdoba Montoya D.A., Carrer H.F. Estrogen facilitates induction of long term potentiation in the hippocampus of awake rats. Brain Res. 1997, 778:430-438.
9. Dineley K.T., Weeber E.J., Atkins C., Adams J.P., Anderson A.E., Sweatt J.D. Leitmotifs in the biochemistry of LTP induction: amplification, integration and coordination. J. Neurochem. 2001, 77:961-971.
10. Ferreira A., Caceres A. Estrogen-enhanced neurite growth: evidence for a selective induction of Tau and stable microtubules. J. Neurosci. 1991, 11:392-400.
11. Fine M.L., Keefer D.A., Russel-Mergenthal H. Autoradiographic localization of estrogen-concentrating cells in the brain and pituitary of the oyster toadfish. Brain Res. 1990, 536:207-219.
12. Frye C.A., Duffy C.K., Walf A.A. Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task. Neurobiol. Learn Mem. 2007, 88:208-216.
13. Galea L.A., Spritzer M.D., Barker J.M., Pawluski J.L. Gonadal hormone modulation of hippocampal neurogenesis in the adult. Hippocampus 2006, 16:225-232.
14. García Pedrero J.M., Del Rio B., Martínez-Campa C., Muramatsu M., Lazo P.S., Ramos S. Calmodulin is a selective modulator of estrogen receptors. Mol. Endocrinol. 2002, 16:947-960.
15. Garcia-Segura L.M., Diz-Chaves Y., Perez-Martin M., Darnaudéry M. Estradiol, insulin-like growth factor-I and brain aging. Psychoneuroendocrinology 2007, 32:S57-61.
16. Halm S., Pounds N., Maddix S., Rand-Weaver M., Sumpter J.P., Hutchinson T.H., Tyler C.R. Exposure to exogenous 17beta-oestradiol disrupts p450aromB mRNA expression in the brain and gonad of adult fathead minnows (Pimephales promelas). Aquat. Toxicol. 2002, 60:285-299.
17. Hawkins M.B., Godwin J., Crews D., Thomas P. The distributions of the duplicate oestrogen receptors ER-beta a and ER-beta b in the forebrain of the Atlantic croaker (Micropogonias undulatus): evidence for subfunctionalization after gene duplication. Proc. Biol. Sci. 2005, 272:633-641.
18. Hoffmann J.L., Torontali S.P., Thomason R.G., Lee D.M., Brill J.L., Price B.B., Carr G.J., Versteeg D.J. Hepatic gene expression profiling using Genechips in zebrafish exposed to 17alpha-ethynylestradiol. Aquat. Toxicol. 2006, 79:233-246.
19. Jensen B., Taylor M. Lipid transport in female Fundulus heteroclitus during the reproductive season. Fish Physiol. Biochem. 2002, 25:141-151.
20. Kelly M.J., Qiu J., Wagner E.J., Rønnekleiv O.K. Rapid effects of estrogen on G protein-coupled receptor activation of potassium channels in the central nervous system (CNS). J. Steroid Biochem. Mol. Biol. 2002, 83:187-193.
21. 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. USA 2007, 104:8897-8901.
22. Kim J.S., Kim H.Y., Kim J.H., Shin H.K., Lee S.H., Lee Y.S., Son H. Enhancement of rat hippocampal long-term potentiation by 17 beta-estradiol involves mitogen-activated protein kinase-dependent and -independent components. Neurosci. Lett. 2002, 332:65-69.
23. Kim Y.S., Stumpf W.E., Sar M. Topography of estrogen target cells in the forebrain of goldfish, Carassius auratus. J. Comp. Neurol. 1978, 182:611-620.
24. Lustig R.H., Hua P., Yu W., Ahmad F.J., Baas P.W. An in vitro model for the effects of estrogen on neurons employing estrogen receptor-transfected PC12 cells. J. Neurosci. 1994, 14:3945-3957.
25. Marlatt V.L., Martyniuk C.J., Zhang D., Xiong H., Watt J., Xia X., Moon T., Trudeau V.L. Auto-regulation of estrogen receptor subtypes and gene expression profiling of 17beta-estradiol action in the neuroendocrine axis of male goldfish. Mol. Cell. Endocrinol. 2008, 283:38-48.
26. Martinez de la Escalera G., Weiner R.I. Hypothalamic regulation of microtubule-associated protein phosphorylation in lactotrophs. Neuroendocrinology 1992, 55:327-335.
27. Martinović D., Hogarth W.T., Jones R.E., Sorensen P.W. Environmental estrogens suppress hormones, behavior, and reproductive fitness in male fathead minnows. Environ. Toxicol. Chem. 2007, 26:271-278.
28. Martyniuk C.J., Alvarez S., McClung S., Villeneuve D.L., Ankley G.T., Denslow N.D. Quantitative proteomic profiles of androgen receptor signaling in the liver of fathead minnows (Pimephales promelas). J. Proteome Res. 2009, 8:2186-2200.
29. Martyniuk C.J., Denslow N.D. Towards functional genomics in fish using quantitative proteomics. Gen. Comp. Endocrinol. 2009, 164:135-141.
30. 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.
31. Martyniuk C.J., Xiong H., Crump K., Chiu S., Sardana R., Nadler A., Gerrie E.R., Xia X., Trudeau V.L. Gene expression profiling in the neuroendocrine brain of male goldfish (Carassius auratus) exposed to 17alpha-ethinylestradiol. Physiol. Genomics 2006, 27:328-336.
32. Matsuno A., Takekoshi S., Sanno N., Utsunomiya H., Ohsugi Y., Saito N., Kanemitsu H., Tamura A., Nagashima T., Osamura R.Y., Watanabe K. Modulation of protein kinases and microtubule-associated proteins and changes in ultrastructure in female rat pituitary cells: effects of estrogen and bromocriptine. J. Histochem. Cytochem. 1997, 45:805-813.
33. Morissette M., Jourdain S., Al Sweidi S., Menniti F.S., Ramirez A.D., Di Paolo T. Role of estrogen receptors in neuroprotection by estradiol against MPTP toxicity. Neuropharmacology 2007, 52:1509-1520.
34. Mouriec K., Pellegrini E., Anglade I., Menuet A., Adrio F., Thieulant M.L., Pakdel F., Kah O. Synthesis of estrogens in progenitor cells of adult fish brain: evolutive novelty or exaggeration of a more general mechanism implicating estrogens in neurogenesis?. Brain Res. Bull. 2008, 75:274-280.
35. Muriach B., Carrillo M., Zanuy S., Cerdá-Reverter J.M. Distribution of estrogen receptor 2 mRNAs (Esr2a and Esr2b) in the brain and pituitary of the sea bass (Dicentrarchus labrax). Brain Res. 2008, 1210:126-141.
36. Neumann D., Scherson T., Ginzburg I., Littauer U.Z., Schwartz M. Regulation of mRNA levels for microtubule proteins during nerve regeneration. FEBS Lett. 1983, 162:270-276.
37. Nikitin A., Egorov S., Daraselia N., Mazo I. Pathway studio--the analysis and navigation of molecular networks. Bioinformatics 2003, 19:2155-2157.
38. Pasmanik M., Callard G.V. Aromatase and 5 alpha-reductase in the teleost brain, spinal cord, and pituitary gland. Gen. Comp. Endocrinol. 1985, 60:244-251.
39. Pellegrini E., Mouriec K., Anglade I., Menuet A., Le Page Y., Gueguen M.M., Marmignon M.H., Brion F., Pakdel F., Kah O. Identification of aromatase-positive radial glial cells as progenitor cells in the ventricular layer of the forebrain in zebrafish. J. Comp. 2007, 501:150-167.
40. Reyna-Neyra A., Arias C., Ferrera P., Morimoto S., Camacho-Arroyo I. Changes in the content and distribution of microtubule associated protein 2 in the hippocampus of the rat during the estrous cycle. J. Neurobiol. 2004, 60:473-480.
41. Rozen S., Skaletsky H.J. Primer3 on the WWW for general users and for biologist programmers. Bioinformatics Methods and Protocols: Methods in Molecular Biology 2000, 365-386. Humana Press, Totowa, NJ. S. Krawetz, S. Misener (Eds.).
42. Sá S.I., Madeira M.D. Estrogen modulates the sexually dimorphic synaptic connectivity of the ventromedial nucleus. J. Comp. Neurol. 2005, 484:68-79.
43. Salbert G., Bonnec G., Le Goff P., Boujard D., Valotaire Y., Jego P. Localization of the estradiol receptor mRNA in the forebrain of the rainbow trout. Mol. Cell Endocrinol. 1991, 76:173-180.
44. Salierno J.D., Kane A.S. 17alpha-ethinylestradiol alters reproductive behaviors, circulating hormones, and sexual morphology in male fathead minnows (Pimephales promelas). Environ. Toxicol. Chem. 2009, 28:953-961.
45. Shilov I.V., Seymour S.L., Patel A.A., Loboda A., Tang W.H., Keating S.P., Hunter C.L., Nuwaysir L.M., Schaeffer D.A. The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol. Cell. Proteomics 2007, 6:1638-1655.
46. Tchoudakova A., Kishida M., Wood E., Callard G.V. Promoter characteristics of two cyp19 genes differentially expressed in the brain and ovary of teleost fish. J. Steroid Biochem. Mol. Biol. 2001, 78:427-439.
47. Wenning G.K., Stefanova N., Jellinger K.A., Poewe W., Schlossmacher M.G. Multiple system atrophy: a primary oligodendrogliopathy. Ann. Neurol. 2008, 64:239-246.
48. Yin G.G., Kookana R.S., Ru Y.J. Occurrence and fate of hormone steroids in the environment. Environ. Int. 2002, 28:545-551.
49. Zhang D., Popesku J.T., Martyniuk C.J., Xiong H., Duarte P., Yao L., Xia X., Trudeau V.L. Profiling neuroendocrine gene expression changes following fadrozole-induced estrogen decline in the female goldfish. Physiol. Genomics 2009, 38:351-361.