Exposure to exogenous 17β-oestradiol disrupts P450aromB mRNA expression in the brain and gonad of adult fathead minnows (Pimephales promelas)

Aquatic Toxicology

Volumn 60, Issue 3-4, 2002, Pages 285-299

  Halm, S ^b   Pounds, N ^c   Maddix, S ^b   Rand Weaver, M ^b   Sumpter, J P ^b   Hutchinson, T H ^c   Tyler, C R ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b BRUNEL UNIVERSITY   (United Kingdom)

^c ASTRAZENECA   (United Kingdom)

Author keywords

Aromatase; Brain; Competitive RT PCR; E2; Endocrine disruption; Gene expression; Gonads; In vivo; Pimephales promelas

Indexed keywords

AROMATASE; CYTOCHROME P450 AROMATASE BETA; CYTOCHROME P450 ISOENZYME; ESTRADIOL; MESSENGER RNA; UNCLASSIFIED DRUG; VITELLOGENIN;

ESTROGENIC COMPOUND; GENE EXPRESSION; POLLUTION EFFECT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; ESTROGEN ACTIVITY; FEMALE; GENE EXPRESSION; MALE; NONHUMAN; OVARY DEVELOPMENT; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN INDUCTION; REPRODUCTIVE TOXICITY; SEX DIFFERENCE; SEXUAL MATURATION; TESTIS DEVELOPMENT; ANIMAL; ANIMAL DISEASE; BIOSYNTHESIS; BLOOD; BODY WEIGHT; BRAIN; CYPRINIFORMES; DRUG EFFECT; ENZYMOLOGY; GENETICS; METABOLISM; OVARY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TESTIS;

CYPRINIFORMES; PIMEPHALES; PIMEPHALES PROMELAS; VERTEBRATA;

ANIMALS; AROMATASE; BODY WEIGHT; BRAIN; CYPRINIDAE; ESTRADIOL; FEMALE; GENE EXPRESSION; MALE; OVARY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEXUAL MATURATION; TESTIS; VITELLOGENINS;

EID: 0037201922     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-445X(02)00011-5     Document Type: Article

References (57)

1. Abdelgadir S.E., Resko J.A., Ojeda S.R., Lephart E.D., McPhaul M.J., Roselli C.E. Androgens regulate aromatase cytochrome-P450 messenger-ribonucleic-acid in rat-brain. Endocrinology. 135:1994;395-401.
2. Abinawanto K., Shimada K., Yoshida K., Saito N. Effects of aromatase inhibitor on sex differentiation and levels of P450(17 alpha) and P450(arom) messenger ribonucleic acid of gonads in chicken embryos. Gen. Comp. Endocrinol. 102:1996;241-246.
3. Afonso L.O.B., Iwama G.K., Smith J., Donaldson E.M. Effects of the aromatase inhibitor Fadrozole on plasma sex steroid secretion and oocyte maturation in female coho salmon (Oncorhynchus kisutch) during vitellogenesis. Fish Physiol. Biochem. 20:1999;231-241.
4. Allen Y., Scott A.P., Matthiessen P., Haworth S., Thain J.E., Feist S. Survey of estrogenic activity in United Kingdom estuarine and coastal waters and its effects on gonadal development of the flounder Platichthys flesus. Environ. Toxicol. Chem. 18:1999;1791-1800.
5. Billard R., Breton B., Richard M. On the inhibitory effect of some steroids on spermatogenesis in adult rainbow-trout (Salmo Gairdneri). Can. J. Zool. 59:1981;1479-1487.
6. Billard R., Richard M., Rombauts R. Inhibition of spermatogenesis and vitellogenesis in rainbow trout by hormonal additives in the diet. Progr. Fish-Cult. 44:1982;15-18.
7. Borg B. Androgens in teleost fishes. Comp. Biochem. Physiol. 109C:1994;219-245.
8. Carragher J.F., Sumpter J.P., Pottinger T.G., Pickering A.D. The deleterious effects of cortisol implantation on reproductive function in 2 species of trout, Salmo Trutta L and Salmo Gairdneri Richardson. Gen. Comp. Endocrinol. 76:1989;310-321.
9. Chang X.T., Kobayashi T., Kajiura H., Nakamura M., Nagahama Y. Isolation and characterization of the cDNA encoding the tilapia (Oreochromis niloticus) cytochrome P450 aromatase (P450arom): Changes in P450arom mRNA, protein and enzyme activity in ovarian follicles during oogenesis. J. Mol. Endocrinol. 18:1997;57-66.
10. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate phenol chloroform extraction. Anal. Biochem. 162:1987;156-159.
11. Colborn T., Saal F.S.V., Soto A.M. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ. Health Perspect. 101:1993;378-384.
12. Condeca J.B., Canario A.V.M. The effect of estrogen on the gonads and on in vitro conversion of androstenedione to testosterone, 11-ketotestosterone, and estradiol-17 beta in Sparus aurata (Teleostei, sparidae). Gen. Comp. Endocrinol. 116:1999;59-72.
13. Conover W.J. Practical Nonparametric Statistics. 1980;Wiley New York.
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. 32:1998;1549-1558.
15. Gelinas D., Pitoc G.A., Callard G.V. Isolation of a goldfish brain cytochrome P450 aromatase cDNA: mRNA expression during the seasonal cycle and after steroid treatment. Mol. Cell. Endocrinol. 138:1998;81-93.
16. Halm S., Rand-Weaver M., Sumpter J.P., Tyler C.R. Cloning and molecular characterization of an ovarian-derived (brain-like) P450 aromatase cDNA and development of a competitive RT-PCR assay to quantify its expression in the fathead minnow (Pimephales promelas). Fish Physiol. Biochem. 24:2001;49-62.
17. Harries J.E., Runnalls T., Hill E., Harris C.A., Maddix S., Sumpter J.P., Tyler C.R. Development of a reproductive performance test for endocrine disrupting chemicals using pair-breeding fathead minnows (Pimephales promelas). Environ. Sci. Technol. 34:2000;3003-3011.
18. Harris C., Santos E., Pottinger T.G., Tyler C.R., Sumpter J.P. Nonylphenol affects gonadotrophin levels in the pituitary and plasma of female rainbow trout (Oncorhynchus mykiss). Environ. Sci. Technol. 35:2001;2909-2916.
19. Jensen K.M., Korte J.J., Kahl M.D., Pasha M.S., Ankley G.T. Aspects of basic reproductive biology and endocrinology in the fathead minnow (Pimephales promelas). Comp. Biochem. Physiol. 128C:2001;127-141.
20. Jeyasuria P., Place A.R. Embryonic brain-gonadal axis in temperature-dependent sex determination of reptiles: a role for P450 aromatase (CYP19). J. Exp. Zool. 281:1998;428-449.
21. 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. 15:1996;194-202.
22. Kellogg C.K., Lundin A. Brain androgen-inducible aromatase is critical for adolescent organization of environment-specific social interaction in male rats. Horm. Behav. 35:1999;155-162.
23. Kime D.E., Ebrahimi M. Synthesis of 17,20 alpha- and 17,20 beta-dihydroxy-4-pregnen-3- ones, 11-ketotestosterone and their conjugates by gills of teleost fish. Fish Physiol. Biochem. 17:1997;117-121.
24. Kishida M., Callard G.V. Distinct cytochrome P450 aromatase isoforms in zebrafish (Danio rerio) brain and ovary are differentially programmed and estrogen regulated during early development. Endocrinology. 142:2001;740-750.
25. Kobayashi M., Aida K., Hanyu I. Hormone changes during the ovulatory cycle in goldfish. Gen. Comp. Endocrinol. 69:1988;301-307.
26. Kramer V.J., Miles-Richardson S., Pierens S.L., Giesy J.P. Reproductive impairment and induction of alkaline-labile phosphate, a biomarker of estrogen exposure, in fathead minnows (Pimephales promelas) exposed to waterborne 17 beta-estradiol. Aquat. Toxicol. 40:1998;335-360.
27. Kwon J.Y., Haghpanah V., Kogson-Hurtado L.M., McAndrew B.J., Penman D.J. Masculinization of genetic female Nile tilapia (Oreochromis niloticus) by dietary administration of an aromatase inhibitor during sexual differentiation. J. Exp. Zool. 287:2000;46-53.
28. Kwon J.Y., McAndrew B.J., Penman D.J. Cloning of brain aromatase gene and expression of brain and ovarian aromatase gene during sexual differentiation in genetic male and female Nile tilapia Oreochromis niloticus. Mol. Reprod. Dev. 59:2001;359-370.
29. Lephart E.D. A review of brain aromatase cytochrome P450. Brain Res. Rev. 22:1996;1-26.
30. Loomis A.K., Thomas P. Binding characteristics of estrogen receptor (ER) in Atlantic Croaker (Micropogonias undulatus) testis: different affinity for estrogens and xenobiotics from that of hepatic ER. Biol. Reprod. 61:1999;51-60.
31. Miles-Richardson S.R., Kramer V.J., Fitzgerald S.D., Render J.A., Yamini B., Barbee S.J., Giesy J.P. Effects of waterborne exposure of 17-estradiol on secondary sex characteristics and gonads of fathead minnows (Pimephales promelas). Aquat. Toxicol. 51:2000;273-274.
32. Nozu K., Dufau M.L., Catt K.J. Estradiol receptor-mediated regulation of steroidogenesis in gonadotropin-desensitized Leydig cells. J. Biol. Chem. 256:1981;1915-1922.
33. Orlando E.F., Denslow N.D., Folmar L.C., Guillette L.J. A comparison of the reproductive physiology of largemouth bass, Micropterus salmoides, collected from the Escambia and Blackwater Rivers in Florida. Environ. Health Perspect. 107:1999;199-204.
34. Panter G.H., Thompson R.S., Sumpter J.P. Adverse reproductive effects in male fathead minnows (Pimephales promelas) exposed to environmentally relevant concentrations of the natural oestrogens, oestradiol and oestrone. Aquat. Toxicol. 42:1998;243-253.
35. Pottinger T.G., Yeomans W.E., Carrick T.R. Plasma cortisol and 17 beta-oestradiol levels in roach exposed to acute and chronic stress. J. Fish Biol. 54:1999;525-532.
36. Robertson K.M., O'Donnell L., Jones M.E.E., Meachem S.J., Boon W.C., Fisher C.R., Graves K.H., McLachlan R.I., Simpson E.R. Impairment of spermatogenesis in mice lacking a functional aromatase (cyp 19) gene. Proc. Natl. Acad. Sci. USA. 96:1999;7986-7991.
37. 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. 34:2000;1521-1528.
38. Routledge E.J., Sheahan D., Desbrow C., Brighty G.C., Waldock M., Sumpter J.P. Identification of estrogenic chemicals in STW effluent. 2. In vivo responses in trout and roach. Environ. Sci. Technol. 32:1998;1559-1565.
39. Schlinger B.A., Greco C., Bass A. Aromatase activity in the hindbrain vocal control region of a teleost fish: divergence among males with alternative reproductive tactics. Proc. R. Soc. Lond. B. 266:1999;131-136.
40. Sharpe R.M. Reproductive biology - Do males rely on female hormones? Nature. 390:1997;447-448.
41. Shore L.S., Gurevitz M., Shemesh M. Estrogen as an environmental pollutant. Bull. Environ. Contam. Toxicol. 51:1993;361-366.
42. Simpson E.R., Michael M.D., Agarwal V.R., Michael M.D., Bulun S.E., Hinshelwood M.M., Graham-Lorence S., Sun T., Fisher C.R., Qin K., Mendelson C.R. Aromatase expression in health and disease. Conn P.M. Recent Progress in Hormone Research., Proceedings of the 1996 Conference. 1997;185-214 The Endocrine Society Press Bethesda.
43. Stumpf M., Ternes T.A., Haberer K., Baumann W. Nachweis von natürlichen und synthetischen Östrogenen in Kläranlagen und Flieβgewässern. Vom Wasser. 87:1996;251-261.
44. Tabak H.H., Bloomhuff R.N., Bunch R.L. Ovulation-inhibiting hormones in untreated and treated wastewaters. Dev. Ind. Microbiol. 11:1970;497-519.
45. Tanaka M., Telecky T.M., Fukada S., Adachi S., Chen S., Nagahama Y. Cloning and sequence-analysis of the cDNA-encoding P-450 aromatase (P450arom) from a rainbow trout (Oncorhynchus mykiss) ovary-relationship between the amount of P450arom messenger-RNA and the production of estradiol-17-beta in the ovary. J. Mol. Endocrinol. 8:1992;53-61.
46. Tanaka M., Fukada S., Matsuyama M., Nagahama Y. Structure and promoter analysis of the cytochrome-P-450 aromatase gene of the teleost fish, Medaka (Oryzias latipes). J. Biochem. 117:1995;719-725.
47. Tchoudakova, A., Callard, G.V., 1996. Molecular cloning of the 5′-flanking region of the goldfish brain aromatase promoter. Proc. Soc. Neurosci., Washington, D.C.
48. Tchoudakova A., Callard G.V. Identification of multiple CYP19 genes encoding different cytochrome P450 aromatase isozymes in brain and ovary. Endocrinology. 139:1998;2179-2189.
49. Thorpe K., Hetheridge M., Hutchinson T.H., Scholze M., Sumpter J.P., Tyler C.R. Assessing the biological effects of binary mixtures of environmental oestrogens using vitellogenin induction in juvenile rainbow trout (Onchorhynchus mykiss). Environ. Sci. Technol. 35:2001;2476-2481.
50. Trant J.M., Lehrter J., Gregory T., Nunez S., Wunder J. Expression of cytochrome P450 aromatase in the channel catfish, Ictalurus punctatus. J. Steroid Biochem. Mol. Biol. 61:1997;393-397.
51. Tsai C.-L., Wang L.-H., Chang C.-F., Kao C.-C. Effects of gonadal steroids on brain serotonergic and aromatase activity during the critical period of sexual differentiation in tilapia, Oreochromis mossambicus. J. Neuroendocrinol. 49:2000;894-898.
52. Turner K.J., Morley M., Atanassova N., Swanston I.D., Sharpe R.M. Effect of chronic administration of an aromatase inhibitor to adult male rats on pituitary and testicular function and fertility. J. Endocrinol. 164:2000;225-238.
53. Tyler C.R., Routledge E.J. Oestrogenic effects in fish in English rivers with evidence of their causation. Pure Appl. Chem. 70:1998;1795-1804.
54. Tyler C.R., vanderEerden B., Jobling S., Panter G., Sumpter J.P. Measurement of vitellogenin, a biomarker for exposure to oestrogenic chemicals, in a wide variety of cyprinid fish. J. Comp. Physiol. 166B:1996;418-426.
55. Tyler C.R., van Aerle 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. 18:1999;337-347.
56. van Aerle R., Jobling S., Christiansen L., Sumpter J.P., Tyler C.R. Evidence for sexual disruption in a second species of freshwater fish (gudgeon, Gobio gobio) living in UK rivers receiving sewage treatment works effluents. Environ. Toxicol. Chem. 20:2001;2841-2847.
57. Wibbels T., Crews D. Putative aromatase inhibitor induces male sex determination in a female unisexual lizard and in a turtle with temperature-dependent sex determination. J. Endocrinol. 141:1994;259-299.