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http://dx.doi.org/10.4062/biomolther.2010.18.2.125

Effects of Prenatal and Neonatal Exposure to Bisphenol A on the Development of the Central Nervous System  

Mizuo, Keisuke (Department of Toxicology, Hoshi University School of Pharmacy and Pharmaceutical Sciences)
Narita, Minoru (Department of Toxicology, Hoshi University School of Pharmacy and Pharmaceutical Sciences)
Miyagawa, Kazuya (Department of Toxicology, Hoshi University School of Pharmacy and Pharmaceutical Sciences)
Suzuki, Tsutomu (Department of Toxicology, Hoshi University School of Pharmacy and Pharmaceutical Sciences)
Publication Information
Biomolecules & Therapeutics / v.18, no.2, 2010 , pp. 125-134 More about this Journal
Abstract
Bisphenol A (BPA) is one of the most common endocrine disrupters. In the last decade, the number of studies concerning the effects of chronic treatment with BPA on the development of the central nervous system (CNS) has increased. However, little is known about the effects of chronic exposure to BPA on higher brain functions such as memory or psychomotor functions. Here, we report our following findings: (1) Prenatal and neonatal exposure to BPA enhances psychostimulant-induced rewarding effects, results in the up- or downregulation of dopamine receptors, causes memory impairment, and decreases choline acetyltransferase (ChAT) activity. (2) BPA activates astrocytes in vivo and in vitro. These findings suggest that prenatal and neonatal exposure to BPA affects the development of the CNS.
Keywords
Bisphenol A; Rewarding effect; Memory impairment; Astrocyte;
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1 Zetterstrom, R. H., Solomin, L., Mitsiadis, T., Olson, L. and Perlmann, T. (1996). Retinoid X receptor heterodimerization and developmental expression distinguish the orphan nuclear receptors NGFI-B, Nurr1, and Nor1. Mol. Endocrinol. 10, 1656-1666.   DOI
2 Baccarelli, A. and Bollati, V. (2009). Epigenetics and environmental chemicals. Curr. Opin. Pediatr. 21, 243-251.   DOI
3 Bardo, M. T. (1998). Neuropharmacological mechanisms of drug reward: beyond dopamine in the nucleus accumbens. Crit. Rev. Neurobiol. 12, 37-67.   DOI   ScienceOn
4 Bartus, R. T., Dean, R. L. 3rd, Beer, B. and Lippa, A. S. (1982). The cholinergic hypothesis of geriatric memory dysfunction. Science 217, 408-414.   DOI
5 Bayer, S. A., Wills, K. V., Triarhou, L. C. and Ghetti, B. (1995). Time of neuron origin and gradients of neurogenesis in midbrain dopaminergic neurons in the mouse. Exp. Brain Res. 105, 191-199.
6 Bindhumol, V., Chitra, K. C. and Mathur, P. P. (2003). Bisphenol A induces reactive oxygen species generation in the liver of male rats. Toxicology 188, 117-124.   DOI
7 Farabollini, F., Porrini, S., Della Seta, D., Bianchi, F. and Dessi- Fulgheri, F. (2002). Effects of perinatal exposure to bisphenol A on sociosexual behavior of female and male rats. Environ. Health Perspect. 110 (Suppl 3), 409-414.   DOI
8 Fellin, T. and Carmignoto, G. (2004). Neurone-to-astrocyte signalling in the brain represents a distinct multifunctional unit. J. Physiol. 559, 3-15.   DOI
9 Gaido, K. W., Leonard, L. S., Lovell, S., Gould, J. C., Babai, D., Portier, C. J. and McDonnell, D. P. (1997). Evaluation of chemicals with endocrine modulating activity in a yeast-based steroid hormone receptor gene transcription assay. Toxicol. Appl. Pharmacol. 143, 205-212.   DOI
10 Hammond, R., Blaess, S. and Abeliovich, A. (2009). Sonic hedgehog is a chemoattractant for midbrain dopaminergic axons. PLoS One 4, e7007.   DOI
11 Brailoiu, E., Dun, S. L., Brailoiu, G. C., Mizuo, K., Sklar, L. A., Oprea, T. I., Prossnitz, E. R. and Dun, N. J. (2007). Distribution and characterization of estrogen receptor G proteincoupled receptor 30 in the rat central nervous system. J. Endocrinol. 193, 311-321.   DOI
12 Kholodilov, N., Yarygina, O., Oo, T. F., Zhang, H., Sulzer, D., Dauer, W. and Burke, R. E. (2004). Regulation of the development of mesencephalic dopaminergic systems by the selective expression of glial cell line-derived neurotrophic factor in their targets. J. Neurosci. 24, 3136-3146.   DOI
13 Koeltzow, T. E., Xu, M., Cooper, D. C., Hu, X. T., Tonegawa, S., Wolf, M. E. and White, F. J. (1998). Alterations in dopamine release but not dopamine autoreceptor function in dopamine $D_3$ receptor mutant mice. J. Neurosci. 18, 2231-2238.
14 Koob, G. F. (1992). Drugs of abuse: anatomy, pharmacology and function of reward pathways. Trends Pharmacol. Sci. 13, 177-184.   DOI
15 Bromer, J. G., Zhou, Y., Taylor, M. B., Doherty, L. and Taylor, H. S. (2010). Bisphenol-A exposure in utero leads to epigenetic alterations in the developmental programming of uterine estrogen response. FASEB J. 24 (published online Feb 24)
16 Devoto, P., Collu, M., Muntoni, A. L., Pistis, M., Serra, G., Gessa, G. L. and Diana, M. (1995). Biochemical and electrophysiological effects of 7-OH-DPAT on the mesolimbic dopaminergic system. Synapse 20, 153-155.   DOI
17 Dolinoy, D. C., Huang, D. and Jirtle, R. L. (2007). Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc. Natl. Acad. Sci. U. S. A. 104, 13056-13061.   DOI
18 Miyagawa, K., Narita, M., Akama, H. and Suzuki, T. (2007a). Memory impairment associated with a dysfunction of the hippocampal cholinergic system induced by prenatal and neonatal exposures to bisphenol-A. Neurosci. Lett. 418, 236-241.   DOI
19 Dutar, P., Bassant, M. H., Senut, M. C. and Lamour, Y. (1995). The septohippocampal pathway: structure and function of a central cholinergic system. Physiol. Rev. 75, 393-427.   DOI
20 Marti, J., Wills, K. V., Ghetti, B. and Bayer, S. A. (2002). A combined immunohistochemical and autoradiographic method to detect midbrain dopaminergic neurons and determine their time of origin. Brain. Res. Brain. Res. Protoc. 9, 197-205.   DOI
21 Haydon, P. G. (2001). GLIA: listening and talking to the synapse. Nat. Rev. Neurosci. 2, 185-193.   DOI
22 Ho, S. M., Tang, W. Y., Belmonte de Frausto, J. and Prins, G. S. (2006). Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant 4. Cancer Res. 66, 5624-5632.   DOI
23 Howdeshell, K. L., Hotchkiss, A. K., Thayer, K. A., Vandenbergh, J. G. and vom Saal, F. S. (1999). Exposure to bisphenol A advances puberty. Nature 401, 763-764.   DOI
24 Inoue, K., Kato, K., Yoshimura, Y., Makino, T. and Nakazawa, H. (2000). Determination of bisphenol A in human serum by high-performance liquid chromatography with multi-electrode electrochemical detection. J. Chromatogr. B. Biomed. Sci. Appl. 749, 17-23.   DOI
25 Jin, L. Q., Goswami, S., Cai, G., Zhen, X. and Friedman, E. (2003). SKF83959 selectively regulates phosphatidylinositollinked $D_1$ dopamine receptors in rat brain. J. Neurochem. 85, 378-386.   DOI
26 Narita, M., Funada, M. and Suzuki, T. (2001). Regulations of opioid dependence by opioid receptor types. Pharmacol. Ther. 89, 1-15.   DOI
27 Kabuto, H., Hasuike, S., Minagawa, N. and Shishibori, T. (2003). Effects of bisphenol A on the metabolisms of active oxygen species in mouse tissues. Environ. Res. 93, 31-35.   DOI
28 Moriyama, K., Tagami, T., Akamizu, T., Usui, T., Saijo, M., Kanamoto, N., Hataya, Y., Shimatsu, A., Kuzuya, H. and Nakao, K. (2002). Thyroid hormone action is disrupted by bisphenol A as an antagonist. J. Clin. Endocrinol. Metab. 87, 5185-5190.   DOI
29 Nakagawa, Y. and Tayama, S. (2000). Metabolism and cytotoxicity of bisphenol A and other bisphenols in isolated rat hepatocytes. Arch. Toxicol. 74, 99-105.   DOI
30 Kubo, K., Arai, O., Ogata, R., Omura, M., Hori, T. and Aou, S. (2001). Exposure to bisphenol A during the fetal and suckling periods disrupts sexual differentiation of the locus coeruleus and of behavior in the rat. Neurosci. Lett. 304, 73-76.   DOI
31 Lee, S., Suk, K., Kim, I. K., Jang, I. S., Park, J. W., Johnson, V. J., Kwon, T. K., Choi, B. J. and Kim, S. H. (2008). Signaling pathways of bisphenol A-induced apoptosis in hippocampal neuronal cells: role of calcium-induced reactive oxygen species, mitogen-activated protein kinases, and nuclear factorkappaB. J. Neurosci. Res. 86, 2932-2942.   DOI
32 Lee, S. H., Lumelsky, N., Studer, L., Auerbach, J. M. and McKay, R. D. (2000). Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat. Biotechnol. 18, 675-679.   DOI
33 Lee, S. H. and Mouradian, M. M. (1999). Up-regulation of $D_{1A}$ dopamine receptor gene transcription by estrogen. Mol. Cell. Endocrinol. 156, 151-157.   DOI
34 Miyagawa, K., Narita, M., Niikura, K., Akama, H., Tsurukawa, Y. and Suzuki, T. (2007b). Changes in central dopaminergic systems with the expression of Shh or GDNF in mice perinatally exposed to bisphenol-A. Nihon Shinkei Seishin Yakurigaku Zasshi 27, 69-75.
35 Levant, B. (1997). The $D_3$ dopamine receptor: neurobiology and potential clinical relevance. Pharmacol. Rev. 49, 231-252.
36 Lin, L. F., Doherty, D. H., Lile, J. D., Bektesh, S. and Collins, F. (1993). GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 260, 1130-1132.   DOI
37 Schwartz, J. C., Diaz, J., Bordet, R., Griffon, N., Perachon, S., Pilon, C., Ridray, S. and Sokoloff, P. (1998). Functional implications of multiple dopamine receptor subtypes: the $D_1/D_3$ receptor coexistence. Brain Res. Brain Res. Rev. 26, 236-242.   DOI
38 Miyamoto, M., Kato, J., Narumi, S. and Nagaoka, A. (1987). Characteristics of memory impairment following lesioning of the basal forebrain and medial septal nucleus in rats. Brain Res. 419, 19-31.   DOI
39 Miyatake, M., Miyagawa, K., Mizuo, K., Narita, M. and Suzuki, T. (2006). Dynamic changes in dopaminergic neurotransmission induced by a low concentration of bisphenol-A in neurones and astrocytes. J. Neuroendocrinol. 18, 434-444.   DOI
40 Mizuo, K., Narita, M., Miyagawa, K., Okuno, E. and Suzuki, T. (2004a). Prenatal and neonatal exposure to bisphenol-A affects the morphine-induced rewarding effect and hyperlocomotion in mice. Neurosci. Lett. 356, 95-98.   DOI
41 Mizuo, K., Narita, M., Miyatake, M. and Suzuki, T. (2004b). Enhancement of dopamine-induced signaling responses in the forebrain of mice lacking dopamine $D_3$ receptor. Neurosci. Lett. 358, 13-16.   DOI
42 Narita, M., Mizuo, K., Mizoguchi, H., Sakata, M., Tseng, L. F. and Suzuki, T. (2003). Molecular evidence for the functional role of dopamine $D_3$ receptor in the morphine-induced rewarding effect and hyperlocomotion. J. Neurosci. 23, 1006-1012.
43 Mizuo, K., Narita, M., Yoshida, T. and Suzuki, T. (2004c). Functional changes in dopamine D3 receptors by prenatal and neonatal exposure to an endocrine disruptor bisphenol-A in mice. Addict Biol. 9, 19-25.   DOI
44 Narita, M., Miyagawa, K., Mizuo, K., Yoshida, T. and Suzuki, T. (2006). Prenatal and neonatal exposure to low-dose of bisphenol-A enhance the morphine-induced hyperlocomotion and rewarding effect. Neurosci. Lett. 402, 249-252.   DOI
45 Narita, M., Miyagawa, K., Mizuo, K., Yoshida, T. and Suzuki, T. (2007). Changes in central dopaminergic systems and morphine reward by prenatal and neonatal exposure to bisphenol-A in mice: evidence for the importance of exposure period. Addict Biol. 12, 167-172.   DOI
46 Ooe, H., Taira, T., Iguchi-Ariga, S. M. and Ariga, H. (2005). Induction of reactive oxygen species by bisphenol A and abrogation of bisphenol A-induced cell injury by DJ-1. Toxicol. Sci. 88, 114-126.   DOI
47 Pacheco, M. A. and Jope, R. S. (1997). Comparison of $[^3H]$ phosphatidylinositol and $[^3H]$phosphatidylinositol 4,5-bisphosphate hydrolysis in postmortem human brain membranes and characterization of stimulation by dopamine D1 receptors. J. Neurochem. 69, 639-644.
48 Riddle, R. and Pollock, J. D. (2003). Making connections: the development of mesencephalic dopaminergic neurons. Brain Res. Dev. Brain Res. 147, 3-21.   DOI
49 Sigmundson, H. K. (1994). Pharmacotherapy of schizophrenia: a review. Can. J. Psychiatry 39, S70-75.
50 Smidt, M. P., Smits, S. M. and Burbach, J. P. (2003). Molecular mechanisms underlying midbrain dopamine neuron development and function. Eur. J. Pharmacol. 480, 75-88.   DOI   ScienceOn
51 Sokoloff, P., Giros, B., Martres, M. P., Bouthenet, M. L. and Schwartz, J. C. (1990). Molecular cloning and characterization of a novel dopamine receptor $(D_3)$ as a target for neuroleptics. Nature 347, 146-151.   DOI
52 Surmeier, D. J., Eberwine, J., Wilson, C. J., Cao, Y., Stefani, A. and Kitai, S. T. (1992). Dopamine receptor subtypes colocalize in rat striatonigral neurons. Proc. Natl. Acad. Sci. U. S. A. 89, 10178-10182.   DOI
53 Suzuki, T. (1996). Conditioned place preference in mice. Meth. Find. Exp. Clin. Pharmacol. 18, 75-83.
54 Suzuki, T., Mizuo, K., Nakazawa, H., Funae, Y., Fushiki, S., Fukushima, S., Shirai, T. and Narita, M. (2003). Prenatal and neonatal exposure to bisphenol-A enhances the central dopamine $D_1$ receptor-mediated action in mice: enhancement of the methamphetamine-induced abuse state. Neuroscience 117, 639-644.   DOI
55 Takeuchi, Y., Fukunaga, K. and Miyamoto, E. (2002). Activation of nuclear $Ca^{2+}$/calmodulin-dependent protein kinase II and brain-derived neurotrophic factor gene expression by stimulation of dopamine D2 receptor in transfected NG108- 15 cells. J. Neurochem. 82, 316-328.   DOI
56 Temple, S. (2001). The development of neural stem cells. Nature 414, 112-117.   DOI
57 Voorn, P., Kalsbeek, A., Jorritsma-Byham, B. and Groenewegen, H. J. (1988). The pre- and postnatal development of the dopaminergic cell groups in the ventral mesencephalon and the dopaminergic innervation of the striatum of the rat. Neuroscience 25, 857-887.   DOI
58 Zhu, W. H., Conforti, L. and Millhorn, D. E. (1997). Expression of dopamine D2 receptor in PC-12 cells and regulation of membrane conductances by dopamine. Am. J. Physiol. 273, C1143-1150.   DOI
59 Wallen, A., Zetterstrom, R. H., Solomin, L., Arvidsson, M., Olson, L. and Perlmann, T. (1999). Fate of mesencephalic AHD2-expressing dopamine progenitor cells in NURR1 mutant mice. Exp. Cell Res. 253, 737-746.   DOI
60 Xiao, Q., Castillo, S. O. and Nikodem, V. M. (1996). Distribution of messenger RNAs for the orphan nuclear receptors Nurr1 and Nur77 (NGFI-B) in adult rat brain using in situ hybridization. Neuroscience 75, 221-230.   DOI
61 Yaoi, T., Itoh, K., Nakamura, K., Ogi, H., Fujiwara, Y. and Fushiki, S. (2008). Genome-wide analysis of epigenomic alterations in fetal mouse forebrain after exposure to low doses of bisphenol A. Biochem. Biophys. Res. Commun. 376, 563-567.   DOI