Bisphenol-A rapidly enhanced passive avoidance memory and phosphorylation of NMDA receptor subunits in hippocampus of young rats

Toxicology and Applied Pharmacology

Volumn 255, Issue 2, 2011, Pages 221-228

  Xu, Xiaohong ^a   Li, Tao ^a   Luo, Qingqing ^a   Hong, Xing ^a   Xie, Lingdan ^a   Tian, Dong ^a  

^a ZHEJIANG NORMAL UNIVERSITY   (China)

Author keywords

Bisphenol A; Estrogen receptor; Extracellular signal regulated kinase; N methyl d aspartate receptor; Passive avoidance memory

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 4,4' ISOPROPYLIDENEDIPHENOL; ESTRADIOL BENZOATE; ESTROGEN RECEPTOR BETA; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; RECEPTOR BLOCKING AGENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; FOOTSHOCK; HIPPOCAMPUS; LATENT PERIOD; NONHUMAN; PASSIVE AVOIDANCE; PROTEIN PHOSPHORYLATION; PUERPERIUM; RAT; SIGNAL TRANSDUCTION;

ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; BUTADIENES; ENDOCRINE DISRUPTORS; ENZYME INHIBITORS; ESTRADIOL; ESTROGEN ANTAGONISTS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HIPPOCAMPUS; MALE; MEMORY; NITRILES; PHENOLS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE;

RATTUS; RODENTIA;

EID: 80051583704     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2011.06.022     Document Type: Article

References (54)

1. Adams M.M., Fink S.E., Janssen W.G., Shah R.A., Morrison J.H. Estrogen modulates synaptic N-methyl-d-aspartate receptor subunit distribution in the aged hippocampus. J. Comp. Neurol. 2004, 474(3):419-426.
2. Amateau K.S., Alt J.J., Stamps C.L., Mccarthy M. Brain estradiol content in newborn rats: Sex differences, regional heterogeneity, and possible de Novo synthesis by the female telencephalon. Endocrinology 2004, 145:2906-2917.
3. Ballini C., Corte L.D., Pazzagli M., Colivicchi M.A., Pepeu G., Tipton K.F., Giovannini M.G. Extracellular levels of brain aspartate, glutamate and GABA during an inhibitory avoidance response in the rat. J. Neurochem. 2008, 106(3):1035-1043.
4. Bi R., Broutman G., Foy M.R., Thompson R.F., Baudry M. The tyrosine kinase and mitogen-activation protein kinase pathways mediate multiple effects of estrogen in hippocampus. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:3602-3607.
5. Bi R., Foy M.R., Vouimba R.M., Thompson R.F., Baudry M. Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:13391-13395.
6. Brothwell S.L.C., Barber J.L., Monaghan D.T., Jane D.E., Gibb A.J., Jones S. NR2B- and NR2D-containing synaptic NMDA receptors in developing rat substantia nigra pars compacta dopaminergic neurones. J. Physiol. 2008, 586:739-750.
7. Cammarota M., Bevilaqua L.R.M., Medina J.H., Izquierdo I. Studies on short-term avoidance memory. Neural plasticity and memory: from genes to brain imaging 2007, 193-208. CRC Press, Boca Raton. F. Bermudez-Rattoni (Ed.).
8. Chen L., Xu X., Tian D. Effects of environmental estrogen bisphenol-A on development of brain and behaviour. Sci. China C Life Sci. 2009, 39:1111-1119.
9. Dang V.H., Nguyen T.H., Lee G.S., Choi K.C., Jeung E.B. In vitro exposure to xenoestrogens induces growth hormone transcription and release via estrogen receptor-dependent pathways in rat pituitary GH3 cells. Steroids 2009, 74:707-714.
10. Fernandez S.M., Lewis M.C., Pechenino A.S., Harburger L.L., Orr P.T., Gresack J.E., Schafe G.E., Frick K.M. Estradiol-induced enhancement of object memory consolidation involves hippocampal extracellular signal-regulated kinase activation and membrane-bound estrogen receptors. J. Neurosci. 2008, 28(35):8660-8667.
11. Fiala J.C., Feinberg M., Popov V., Harris K.M. Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J. Neurosci. 1998, 18:8900-8911.
12. Filardo E.J. Epidermal growth factor receptor (EGFR) transactivation by estrogen via the G-protein-coupled receptor, GPR30: a novel signaling pathway with potential significance for breast cancer. J. Steroid Biochem. Mol. Biol. 2002, 80:231-238.
13. Foy M.R., Xu J., Xie X., Brinton R.D., Thompson R.F., Berger T.W. 17beta-estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation. J. Neurophysiol. 1999, 81:925-929.
14. Fried G., Andersson E., Csöregh L., Enmark E., Gustafsson J.A., Aanesen A., Osterlund C. Estrogen receptor beta is expressed in human embryonic brain cells and is regulated by 17beta-estradiol. Eur. J. Neurosci. 2004, 20:2345-2354.
15. Fujimoto T., Kubo K., Aou S. Prenatal exposure to bisphenol A impairs sexual differentiation of exploratory behavior and increases depression-like behavior in rats. Brain Res. 2006, 1068:49-55.
16. Goncalves C.R., Cunha R.W., Barros D.M., Martínez P.E. Effects of prenatal and postnatal exposure to a low dose of bisphenol A on behavior and memory in rats. Environ. Toxicol. Pharmacol. 2010, 30(2):195-201.
17. Hiramatsu M., Sasaki M., Kameyama T. Effects of dynorphin A-(1-13) on carbon monoxide-induced delayed amnesia in mice studied in a step-down type passive avoidance task. Eur. J. Pharmacol. 1995, 282:185-191.
18. Hiroi H., Tsutsumi O., Momoeda M., Takai Y., Osuga Y., Taketani Y. Differential interactions of bisphenol A and 17beta-estradiol with estrogen receptor alpha (ERalpha) and ERbeta. Endocr. J. 1999, 46:773-778.
19. Huemmeke M., Eysel U.T., Mittmann T. Lesion-induced enhancement of LTP in rat visual cortex is mediated by NMDA receptors containing the NR2B subunit. J. Physiol. 2004, 559:875-882.
20. Kelly M.J., Levin E.R. Rapid actions of plasma membrane estrogen receptors. Trends Endocrinol. Metab. 2001, 12:152-156.
21. Kim C.S., Sapienza P.P., Ross I.A., Johnson W., Luu H.M.D., Hutter J.C. Distribution of bisphenol A in the neuroendocrine organs of female rats. Toxicol. Ind. Health 2004, 20:41-50.
22. Konur S., Yuste R. Imaging the motility of dendritic protrusions and axon terminals: roles in axon sampling and synaptic competition. Mol. Cell Neurosci. 2004, 27:427-440.
23. Kurosawa T., Hiroi H., Tsutsumi O., Ishikawa T., Osuga Y., Fujiwara T., Inoue S., Muramatsu M., Momoeda M., Taketani Y. The activity of BPA depends on both the estrogen receptor subtype and the cell type. Endocr. J. 2002, 49(4):465-471.
24. Lee S., Suk K., Kim I.K., Jang I.S., Park J.W., Johnson V.J., et al. Signaling pathways of bisphenol A-induced apoptosis in hippocampal neuronal cells: role of calcium-induced reactive oxygen species, mitogen-activated protein kinases, and nuclear factor-kappa B. J. Neurosci. Res. 2008, 86:2932-2942.
25. Leranth C., Hajszan T., Szigeti-Buck K., Bober J., MacLusky N.J. Bisphenol A prevents the synaptogenic response to estradiol in hippocampus and prefrontal cortex of ovariectomized nonhuman primates. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:14187-14191.
26. Liao G.Y., Wagner D.A., Hsu M.H., Leonard J.P. Evidence for direct protein kinase-C mediated modulation of N-methyl-d-aspartate receptor current. Mol. Pharmacol. 2001, 59:960-964.
27. MacLusky N.J., Hajszan T., Leranth C. The environmental estrogen bisphenol A inhibits estradiol-induced hippocampal synaptogenesis. Environ. Health Perspect. 2005, 113:675-679.
28. Maren S. What the amygdala does and doesn't do in aversive learning. Learn. Mem. 2003, 10:306-308.
29. McCarthy M.M. Estradiol and the developing brain. Physiol. Rev. 2008, 88:91-124.
30. Miyagawa K., Narita M., Narita M., Akama H., Suzuki T. Memory impairment associated with a dysfunction of the hippocampal cholinergic system induced by prenatal and neonatal exposures to bisphenol-A. Neurosci. Lett. 2007, 418(3):236-241.
31. Morohoshi K., Yamamoto H., Kamata R., Shiraishi F., Koda T., Morita M. Estrogenic activity of 37 components of commercial sunscreen lotions evaluated by in vitro assays. Toxicol. In Vitro 2005, 19:457-469.
32. Mukai H., Tsurugizawa T., Murakami G., Kominami S., Ishii H., Ogiue-Ikeda M., Takata N., Tanabe N., Furukawa A., Hojo Y., Ooishi Y., Morrison J.H., Janssen W.G.M., Rose J.A., Chambon P., Kato S., Izumi S., Yamazaki T., Kimoto T., Kawato S. Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons. J. Neurochem. 2007, 100:950-967.
33. Nakamura K., Itoh K., Sugimoto T., Fushiki S. Prenatal exposure to bisphenol A affects adult murine neocortical structure. Neurosci. Lett. 2007, 420:100-105.
34. Negishi T., Kawasaki K., Takatori A., Ishii Y., Kyuwa S., Kuroda Y., Yoshikawa Y. Effects of perinatal exposure to bisphenol A on the behavior of offspring in F344 rats. Environ. Toxicol. Pharmacol. 2003, 14:99-108.
35. Ogiue-Ikeda M., Tanabe N., Mukai H., Hojo Y., Murakami G., Tsurugizawa T., Takata N., Kimoto T., Kawato S. Rapid modulation of synaptic plasticity by estrogens as well as endocrine disrupters in hippocampal neurons. Brain Res. Rev. 2008, 57:363-375.
36. 2+/calmodulin-dependent protein kinase II catalysis by N-methyl-d-aspartate receptor subunit 2B. Biochem. J. 2009, 419:123-132.
37. Raz L., Khan M.M., Mahesh V.B., Vadlamudi R.K., Brann D.W. Rapid estrogen signaling in the brain. Neurosignals 2008, 16:140-153.
38. Rezayat M., Niasari H., Ahmadi S., Parsaei L., Zarrindast M. N-methyl-d-aspartate receptors are involved in lithium-induced state-dependent learning in mice. J. Psychopharmacol. 2010, 24(6):915-921.
39. Richter C.A., Birnbaum L.S., Farabollini F., Newbold R.R., Rubin B.S., Talsness C.E., Vandenbergh J.G., Walser-Kuntz D.R., Saal F.S. In vivo effects of bisphenol A in laboratory rodent studies. Reprod. Toxicol. 2007, 24:199-224.
40. Romeo R.D., McCarthy J.B., Wang A., Milner T.A., McEwen B.S. Sex differences in hippocampal estradiol-induced N-methyl-d-aspartic acid binding and ultrastructural localization of estrogen receptor-alpha. Neuroendocrinology 2005, 81(6):391-399.
41. Sarantis K., Matsokis N., Angelatou F. Synergistic interaction of Dopamine D1 and glutamate NMDA receptors in rat hippocampus and prefrontal cortex: involvement of ERK1/2 signaling. Neuroscience 2009, 163:1135-1145.
42. Sheng M., Pak D.T. Glutamate receptor anchoring proteins and the molecular organization of excitatory synapses. Ann. NY Acad. Sci. 1999, 868:483-493.
43. Suzuki T., Mitake S., Murata S. Presence of up-stream and downstream components of a mitogen-activated protein kinase pathway in the PSD of the rat forebrain. Brain Res. 1999, 840:36-44.
44. 2+ signaling induced by Bisphenol A in cultured rat hippocampal neurons. Neuroendocrinol. Lett. 2006, 27:97-104.
45. Tingley W.G., Ehlers M.D., Kameyama K., Doherty C., Ptak J.B., Riley C.T., Huganir R.L. Characterization of protein kinase A and protein kinase C phosphorylation of the N-methyl-d-aspartate receptor NR1 subunit using phosphorylation site-specific antibodies. J. Biol. Chem. 1997, 272:5157-5166.
46. Watson C.S., Bulayeva N.N., Wozniak A.L., Alyea R.A. Xenoestrogens are potent activators of nongenomic estrogenic responses. Steroids 2007, 72:124-134.
47. Weiland N.G., Orikasa C., Hayashi S., McEwen B.S. Distribution and hormone regulation of estrogen receptor immunoreactive cells in the hippocampus of male and female rats. J. Comp. Neurol. 1997, 388(4):603-612.
48. Welshons W.V., Nagel S.C., Vom Saal F.S. Large effects from small exposures. III. Endocrine mechanisms mediating effects of bisphenol A at levels of human exposure. Endocrinology 2006, 147:S56-S69.
49. Woolley C.S., McEwen B.S. Estradiol regulates hippocampal dendritic spine density via an N-methyl-d-aspartate receptor-dependent mechanism. J. Neurosci. 1994, 14:7680-7687.
50. 2+ influx via L-type calcium channels activates the Src/ERK/cyclic-AMP response element binding protein signal pathway and BCL-2 expression in rat hippocampal neurons: a potential initiation mechanism for estrogen-induced neuroprotection. Neuroscience 2005, 135:59-72.
51. Xu X., Wang Y., Zhang J., Luo Q., Ye Y., Ruan Q. Perinatal exposure to bisphenol-A changes N-methyl-d-aspartate receptor expression in hippocampus of male rat offspring. Environ. Toxicol. Chem. 2010, 29:176-181.
52. Xu X., Zhang J., Wang Y., Ye Y., Luo Q. Perinatal exposure to bisphenol-A impairs learning-memory by concomitant down-regulation of N-methyl-d-aspartate receptors of hippocampus in male offspring mice. Horm. Behav. 2010, 58(2):326-333.
53. Xu X., Ye Y., Li T., Chen L., Tian D., Luo Q., Lu M. Bisphenol-A rapidly promotes dynamic changes in hippocampal dendritic morphology through estrogen receptor-mediated pathway by concomitant phosphorylation of NMDA receptor subunit NR2B. Toxicol. Appl. Pharmacol. 2010, 249(2):188-196.
54. Zsarnovszky A., Le H.H., Wang H.S., Belcher S.M. Ontogeny of rapid estrogen-mediated extracellular signal-regulated kinase signaling in the rat cerebellar cortex: potent nongenomic agonist and endocrine disrupting activity of the xenoestrogen bisphenol A. Endocrinology 2005, 146:5388-5396.