The environmental estrogen bisphenol A inhibits estradiol-induced hippocampal synaptogenesis

Environmental Health Perspectives

Volumn 113, Issue 6, 2005, Pages 675-679

  MacLusky, Neil J ^a   Hajszan, Tibor ^b,c   Leranth, Csaba ^b  

^a HELEN HAYES HOSPITAL   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Bisphenol A; CA1; Estradiol; Hippocampus; Spine synapse density

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ESTRADIOL; ESTROGEN;

AGING; AIR QUALITY STANDARD; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; COGNITION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DENDRITIC SPINE; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL PROTECTION; ESTROGEN SYNTHESIS; FEMALE; HIPPOCAMPUS; MEMORY; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SEX DIFFERENCE; SEXUAL DEVELOPMENT; SYNAPTOGENESIS; UNITED STATES;

ANIMALS; DENDRITIC SPINES; ESTRADIOL; ESTROGENS, NON-STEROIDAL; FEMALE; OVARIECTOMY; PHENOLS; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES;

ANIMALIA;

EID: 20844456812     PISSN: 00916765     EISSN: None     Source Type: Journal    
DOI: 10.1289/ehp.7633     Document Type: Article

References (45)

1. Ashby J. 2001. Increasing the sensitivity of the rodent uterotrophic assay to estrogens, with particular reference to bisphenol A. Environ Health Perspect 109:1091-1094.
2. Bi R, Foy MR, Vouimba RM, Thompson RF, Baudry M. 2001. Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway. Proc Natl Acad Sci USA 98:13391-13395.
3. Brede C, Fjeldal P, Skjevrak I, Herikstad H. 2003. Increased migration levels of bisphenol A from polycarbonate baby bottles after dishwashing, boiling and brushing. Food Addit Contam 20:684-689.
4. Canesi L, Betti M, Lorusso LC, Ciacci C, Gallo G. 2005. 'In vivo' effects of bisphenol A in Mytilus hemocytes: modulation of kinase-mediated signalling pathways. Aquat Toxicol 71:73-84.
5. Canesi L, Ciacci C, Betti M, Lorusso LC, Marchi B, Burattini S, et al. 2004. Rapid effects of 17beta-estradiol on cell signaling and function of Mytilus hemocytes. Gen Comp Endocrinol 136:58-71.
6. Carr R, Bertasi F, Betancourt A, Bowers S, Gandy BS, Ryan P, et al. 2003. Effect of neonatal rat bisphenol A exposure on performance in the Morris water maze. J Toxicol Environ Health A 66:2077-2088.
7. Degen GH, Janning P, Wittsiepe J, Upmeier A, Bolt HM. 2002. Integration of mechanistic data in the toxicological evaluation of endocrine modulators. Toxicol Lett 127:225-237.
8. DeLean A, Munson PJ, Rodbard D. 1978. Simultaneous analysis of families of sigmoidal curves: application to bioassay, radioligand assay and physiological dose-response curves. Am J Physiol 235:E97-E102.
9. EC Scientific Committee on Food. 2002. Opinion of the Scientific Committee on Food on Bisphenol A. Brussels:European Commission Health & Consumer Protection Directorate-General. Available: http://europa.eu.int/comm/food/fs/sc/scf/out128_en.pdf [aceessed 10 February 2005].
10. Farabollini F, Porrini S, Della Seta D, Bianchi F, Dessi-Fulgheri F. 2002. Effects of perinatal exposure to bisphenol A on socio-sexual behavior of female and male rats. Environ Health Perspect 110(suppl 3):409-414.
11. Gandy S. 2003. Estrogen and neurodegeneration. Neurochem Res 28:1003-1008.
12. Green PS, Bishop J, Simpkins JW. 1997. 17α-Estradiol exerts neuroprotective effects on SK-N-SH cells. J Neurosci 17:511-515.
13. Gundersen HJ, Jensen EB. 1987. The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229-263.
14. Hojo Y, Hattori TA, Enami T, Furukawa A, Suzuki K, Ishii HT, et al. 2004. Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017α and P450 aromatase localized in neurons. Proc Natl Acad Sci USA 101:865-870.
15. Howdeshell KL, Peterman PH, Judy BM, Taylor JA, Orazio CE, Ruhlen RL, et al. 2003. Bisphenol A is released from used polycarbonate animal cages into water at room temperature. Environ Health Perspect 111:1180-1187.
16. Kang JH, Kito K, Kondo F. 2003. Factors influencing the migration of bisphenol A from cans. J Food Prot 66:1444-1447.
17. Kousteni S, Bellido T, Plotkin Ll, O'Brien CA, Bodenner DL, Han L, et al. 2001. Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 104:719-730.
18. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, et al. 1998a. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139:4252-4263.
19. Kuiper GG, Shughrue PJ, Merchenthaler I, Gustafsson JA. 1998b. The estrogen receptor beta subtype: a novel mediator of estrogen action in neuroendocrine systems. Front Neuroendocrinol 19:253-286.
20. Leranth C, Hajszan T, MacLusky NJ. 2004. Androgens increase spine synapse density in the CA1 hippocampal subfield of ovariectomized female rats. J Neurosci 24:495-509.
21. Leranth C, Shanabrough M, Redmond DE Jr. 2002. Gonadal hormones are responsible for maintaining the integrity of spine synapses in the CA1 hippocampal subfield of female nonhuman primates. J Comp Neurol 447:34-42.
22. Levin-Allerhand JA, Lominska CE, Wang J, Smith JD. 2002. 17α-estradiol and 17β-estradiol treatments are effective in lowering cerebral amyloid-β levels in AβPPSWE transgenic mice. J Alzheimers Dis 4:449-457.
23. Lundeen SG, Carver JM, McKean ML, Winneker RC. 1997. Characterization of the ovariectomized rat model for the evaluation of estrogen effects on plasma cholesterol levels. Endocrinology 138:1552-1558.
24. MacLusky NJ, Luine VN, Hajszan T, Leranth C. 2005. The 17α and 17β isomers of estradiol both induce rapid spine synapse formation in the CA1 hippocampal subfield of ovariectomized female rats. Endocrinology 146:287-293.
25. McEwen B. 2002. Estrogen actions throughout the brain. Recent Prog Horm Res 57:357-384.
26. Moriyama K, Tagami T, Akamizu T, Usui T, Saijo M, Kanamoto N, et al. 2002. Thyroid hormone action is disrupted by bisphenol A as an antagonist. J Clin Endocrinol Metab 87:5185-5190.
27. Nathan BP, Barsukova AG, Shen F, McAsey M, Struble RG. 2004. Estrogen facilitates neurite extension via apolipoprotein E in cultured adult mouse cortical neurons. Endocrinology 145:3065-3073.
28. Quesada I, Fuentes E, Viso-Leon MC, Soria B, Ripoll C, Nadal A. 2002. Low doses of the endocrine disruptor bisphenol-A and the native hormone 17beta-estradiol rapidly activate transcription factor CREB. FASEB J 16:1671-1673.
29. Rusakov DA, Davies HA, Harrison E, Diana G, Richter-Levin G, Bliss TV, et al. 1997. Ultrastructural synaptic correlates of spatial learning in rat hippocampus. Neuroscience 80:69-77.
30. Safe SH, Pallaroni L, Yoon K, Gaido K, Ross S, McDonnell D. 2002. Problems for risk assessment of endocrine-active estrogenic compounds. Environ Health Perspect 110(suppl 6):925-929.
31. Sato K, Matsuki N, Ohno Y, Nakazawa K. 2002. Effects of 17beta-estradiol and xenoestrogens on the neuronal survival in an organotypic hippocampal culture. Neuroendocrinology 76:223-234.
32. Silva AJ. 2003. Molecular and cellular cognitive studies of the role of synaptic plasticity in memory. J Neurobiol 54:224-237.
33. Suzuki K, Ishikawa K, Sugiyama K, Furuta H, Nishimura F. 2000. Content and release of bisphenol A from polycarbonate dental products. Dent Mater J 19:389-395.
34. Toran-Allerand CD, Singh M, Setalo G Jr. 1999. Novel mechanisms of estrogen action in the brain: new players in an old story. Front Neuroendocrinol 20:97-121.
35. U.S. EPA. 1993. Bisphenol A, CASRN 80-05-7. Washington, DC:Integrated Risk Information System, U.S. Environmental Protection Agency. Available: http://www.epa.gov/iris/subst/0356.htm [accessed 10 February 2005].
36. U.S. EPA. 1998. Endocrine Disruptor Screening and Testing Advisory Committee (EDSTAC) Final Report. Washington, DC:U.S. Environmental Protection Agency. Available: http://www.epa.gov/scipoly/oscpendo/edspoverview/finalrpt.htm [accessed 10 February 2005].
37. Wade CB, Robinson S, Shapiro RA, Dorsa DM. 2001. Estrogen receptor (ER)α and ERβ exhibit unique pharmacologic properties when coupled to activation of the mitogen-activated protein kinase pathway. Endocrinology 142:2336-2342.
38. Weibel ER. 1979. Stereological Methods. London:Academic Press.
39. Wetherill YB, Petre CE, Monk KR, Puga A, Knudsen KE. 2002. The xenoestrogen bisphenol A induces inappropriate androgen receptor activation and mitogenesis in prostatic adenocarcinoma cells. Mol Cancer Ther 1:516-524.
40. Woolley CS, McEwen BS. 1992. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12:2549-2554.
41. Woolley CS, McEwen BS. 1994. Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. J Neurosci 14:7680-7687.
42. Yaffe K, Lui LY, Grady D, Cauley J, Kramer J, Cummings SR 2000. Cognitive decline in women in relation to non-protein-bound oestradiol concentrations. Lancet 356:708-712.
43. Yu X, Rajala RV, McGinnis JF, Li F, Anderson RE, Yan X, et al. 2004. Involvement of insulin/phosphoinositide 3-kinase/Akt signal pathway in 17 beta-estradiol-mediated neuroprotection. J Biol Chem 279:13086-13094.
44. Znamensky V, Akama KT, McEwen BS, Milner TA. 2003. Estrogen levels regulate the subcellular distribution of phosphorylated Akt in hippocampal CA1 dendrites. J Neurosci 23:2340-2347.
45. Zoeller RT, Bansal R, Parris C. 2005. Bisphenol-A, an environmental contaminant that acts as a thyroid hormone receptor antagonist in vitro, increases serum thyroxine, and alters RC3/neurogranin expression in the developing rat brain. Endocrinology 146:607-612.