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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)
  • Received : 2010.04.07
  • Accepted : 2010.04.27
  • Published : 2010.04.30

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

References

  1. Baccarelli, A. and Bollati, V. (2009). Epigenetics and environmental chemicals. Curr. Opin. Pediatr. 21, 243-251. https://doi.org/10.1097/MOP.0b013e32832925cc
  2. Bardo, M. T. (1998). Neuropharmacological mechanisms of drug reward: beyond dopamine in the nucleus accumbens. Crit. Rev. Neurobiol. 12, 37-67. https://doi.org/10.1615/CritRevNeurobiol.v12.i1-2.30
  3. 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. https://doi.org/10.1126/science.7046051
  4. 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.
  5. 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. https://doi.org/10.1016/S0300-483X(03)00056-8
  6. 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. https://doi.org/10.1677/JOE-07-0017
  7. 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)
  8. 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. https://doi.org/10.1002/syn.890200209
  9. 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. https://doi.org/10.1073/pnas.0703739104
  10. 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. https://doi.org/10.1152/physrev.1995.75.2.393
  11. 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. https://doi.org/10.1289/ehp.02110s3409
  12. Fellin, T. and Carmignoto, G. (2004). Neurone-to-astrocyte signalling in the brain represents a distinct multifunctional unit. J. Physiol. 559, 3-15. https://doi.org/10.1113/jphysiol.2004.063214
  13. 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. https://doi.org/10.1006/taap.1996.8069
  14. Hammond, R., Blaess, S. and Abeliovich, A. (2009). Sonic hedgehog is a chemoattractant for midbrain dopaminergic axons. PLoS One 4, e7007. https://doi.org/10.1371/journal.pone.0007007
  15. Haydon, P. G. (2001). GLIA: listening and talking to the synapse. Nat. Rev. Neurosci. 2, 185-193. https://doi.org/10.1038/35058528
  16. 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. https://doi.org/10.1158/0008-5472.CAN-06-0516
  17. 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. https://doi.org/10.1038/44517
  18. 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. https://doi.org/10.1016/S0378-4347(00)00351-0
  19. 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. https://doi.org/10.1046/j.1471-4159.2003.01698.x
  20. 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. https://doi.org/10.1016/S0013-9351(03)00062-8
  21. 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. https://doi.org/10.1523/JNEUROSCI.4506-03.2004
  22. 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.
  23. Koob, G. F. (1992). Drugs of abuse: anatomy, pharmacology and function of reward pathways. Trends Pharmacol. Sci. 13, 177-184. https://doi.org/10.1016/0165-6147(92)90060-J
  24. 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. https://doi.org/10.1016/S0304-3940(01)01760-8
  25. 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. https://doi.org/10.1002/jnr.21739
  26. 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. https://doi.org/10.1038/76536
  27. 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. https://doi.org/10.1016/S0303-7207(99)00133-1
  28. Levant, B. (1997). The $D_3$ dopamine receptor: neurobiology and potential clinical relevance. Pharmacol. Rev. 49, 231-252.
  29. 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. https://doi.org/10.1126/science.8493557
  30. 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. https://doi.org/10.1016/S1385-299X(02)00145-9
  31. 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. https://doi.org/10.1016/j.neulet.2007.01.088
  32. 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.
  33. 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. https://doi.org/10.1016/0006-8993(87)90564-6
  34. 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. https://doi.org/10.1111/j.1365-2826.2006.01434.x
  35. 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. https://doi.org/10.1016/j.neulet.2003.11.027
  36. 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. https://doi.org/10.1016/j.neulet.2003.12.119
  37. 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. https://doi.org/10.1080/13556210410001674059
  38. 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. https://doi.org/10.1210/jc.2002-020209
  39. Nakagawa, Y. and Tayama, S. (2000). Metabolism and cytotoxicity of bisphenol A and other bisphenols in isolated rat hepatocytes. Arch. Toxicol. 74, 99-105. https://doi.org/10.1007/s002040050659
  40. Narita, M., Funada, M. and Suzuki, T. (2001). Regulations of opioid dependence by opioid receptor types. Pharmacol. Ther. 89, 1-15. https://doi.org/10.1016/S0163-7258(00)00099-1
  41. 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. https://doi.org/10.1016/j.neulet.2006.04.014
  42. 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. https://doi.org/10.1111/j.1369-1600.2007.00048.x
  43. 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.
  44. 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. https://doi.org/10.1093/toxsci/kfi278
  45. 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.
  46. Riddle, R. and Pollock, J. D. (2003). Making connections: the development of mesencephalic dopaminergic neurons. Brain Res. Dev. Brain Res. 147, 3-21. https://doi.org/10.1016/j.devbrainres.2003.09.010
  47. 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. https://doi.org/10.1016/S0165-0173(97)00046-5
  48. Sigmundson, H. K. (1994). Pharmacotherapy of schizophrenia: a review. Can. J. Psychiatry 39, S70-75.
  49. 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. https://doi.org/10.1016/j.ejphar.2003.08.094
  50. 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. https://doi.org/10.1038/347146a0
  51. 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. https://doi.org/10.1073/pnas.89.21.10178
  52. Suzuki, T. (1996). Conditioned place preference in mice. Meth. Find. Exp. Clin. Pharmacol. 18, 75-83.
  53. 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. https://doi.org/10.1016/S0306-4522(02)00935-1
  54. 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. https://doi.org/10.1046/j.1471-4159.2002.00967.x
  55. Temple, S. (2001). The development of neural stem cells. Nature 414, 112-117. https://doi.org/10.1038/35102174
  56. 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. https://doi.org/10.1016/0306-4522(88)90041-3
  57. 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. https://doi.org/10.1006/excr.1999.4691
  58. 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. https://doi.org/10.1016/0306-4522(96)00159-5
  59. 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. https://doi.org/10.1016/j.bbrc.2008.09.028
  60. 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. https://doi.org/10.1210/me.10.12.1656
  61. 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. https://doi.org/10.1152/ajpcell.1997.273.4.C1143

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