Changes in memory and synaptic plasticity induced in male rats after maternal exposure to bisphenol A

Toxicology

Volumn 322, Issue , 2014, Pages 51-60

  Wang, Chong ^a   Niu, Ruiyan ^a   Zhu, Yuchen ^a   Han, Haijun ^a   Luo, Guangying ^a   Zhou, Bingrui ^a   Wang, Jundong ^a  

^a SHANXI AGRICULTURAL UNIVERSITY   (China)

Author keywords

Bisphenol A; Glutamate receptors; Learning and memory; Synaptic marker; Synaptic structural

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; GLUTAMATE RECEPTOR; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; SEX HORMONE; SPINOPHILIN; SYNAPTOPHYSIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; BODY WEIGHT; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FEMALE; FETUS GROWTH; HABIT; HIPPOCAMPUS; LOCOMOTION; MALE; NERVE CELL PLASTICITY; NONHUMAN; OPEN FIELD TEST; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; RADIAL ARM MAZE TEST; RAT; SYNAPSE; SYNAPSE VESICLE; WORKING MEMORY;

BISPHENOL A; GLUTAMATE RECEPTORS; LEARNING AND MEMORY; SYNAPTIC MARKER; SYNAPTIC STRUCTURAL;

ANIMALS; BEHAVIOR, ANIMAL; BENZHYDRYL COMPOUNDS; BLOTTING, WESTERN; ESTROGENS, NON-STEROIDAL; FEMALE; GONADAL STEROID HORMONES; MALE; MATERNAL EXPOSURE; MATERNAL-FETAL EXCHANGE; MAZE LEARNING; MEMORY; MICROSCOPY, ELECTRON, TRANSMISSION; MOTOR ACTIVITY; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; RNA; SYNAPSES;

EID: 84901617609     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2014.05.001     Document Type: Article

References (76)

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, 474:419-426.
2. Alonso M., Medina J.H., Pozzo-Miller L. ERK1/2 activation is necessary for BDNF to increase dendritic spine density in hippocampal CA1 pyramidal neurons. Learn. Mem. 2004, 11:172-178.
3. Béïque J.-C., Andrade R. PSD-95 regulates synaptic transmission and plasticity in rat cerebral cortex. J. Physiol. 2003, 546:859-867.
4. Balakrishnan B., Henare K., Thorstensen E.B., Ponnampalam A.P., Mitchell M.D. Transfer of bisphenol A across the human placenta. Am. J. Obstet. Gynecol. 2010, 202:e1-e7.
5. Barnes C. Involvement of LTP in memory: are we searching under the street light?. Neuron 1995, 15:751-754.
6. Burns M.E., Augustine G.J. Synaptic structure and function: dynamic organization yields architectural precision. Cell 1995, 83:187-194.
7. Calafat A.M., Ye X., Wong L.Y., Reidy J.A., Needham L.L. Exposure of the US population to bisphenol A and 4-tertiary-octylphenol: 2003-2004. Environ. Health Perspect. 2008, 116:39-44.
8. Chapin R.E., Adams J., Boekelheide K., Gray L.E., Hayward S.W., Lees P.S., McIntyre B.S., Portier K.M., Schnorr T.M., Selevan S.G. NTP-CERHR expert panel report on the reproductive and developmental toxicity of bisphenol A. Birth Defects Res. B: Dev. Reprod. Toxicol. 2008, 83:157-395.
9. Chen X., Nelson C.D., Li X., Winters C.A., Azzam R., Sousa A.A., Leapman R.D., Gainer H., Sheng M., Reese T.S. PSD-95 is required to sustain the molecular organization of the postsynaptic density. J. Neurosci. 2011, 31:6329-6338.
10. Chung E., Genco M.C., Megrelis L., Ruderman J.V. Effects of bisphenol A and triclocarban on brain-specific expression of aromatase in early zebrafish embryos. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:17732-17737.
11. Citri A., Malenka R.C. Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 2007, 33:18-41.
12. Colbran R.J. Protein phosphatases and calcium/calmodulin-dependent protein kinase II-dependent synaptic plasticity. J. Neurosci. 2004, 24:8404-8409.
13. Cox K.H., Gatewood J.D., Howeth C., Rissman E.F. Gestational exposure to bisphenol A and cross-fostering affect behaviors in juvenile mice. Horm. Behav. 2010, 58:754-761.
14. Doerge D.R., Twaddle N.C., Vanlandingham M., Brown R.P., Fisher J.W. Distribution of bisphenol A into tissues of adult. neonatal, and fetal Sprague-Dawley rats. Toxicol. Appl. Pharmacol. 2011, 255:261-270.
15. Edwards F.A. Anatomy and electrophysiology of fast central synapses lead to a structural model for long-term potentiation. Physiol. Rev. 1995, 75:759-787.
16. Ehrlich I., Klein M., Rumpel S., Malinow R. PSD-95 is required for activity-driven synapse stabilization. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:4176-4181.
17. Ehrlich I., Malinow R. Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity. J. Neurosci. 2004, 24:916-927.
18. Eilam-Stock T., Serrano P., Frankfurt M., Luine V. Bisphenol-A impairs memory and reduces dendritic spine density in adult male rats. Behav. Neurosci. 2012, 126:175-185.
19. Feng W., Zhang M. Organization and dynamics of PDZ-domain-related supramodules in the postsynaptic density. Nat. Rev. Neurosci. 2009, 10:87-99.
20. Frye C., Bo E., Calamandrei G., Calzà L., Dessì-Fulgheri F., Fernández M., Fusani L., Kah O., Kajta M., Le Page Y., Patisaul H.B., Venerosi A., Wojtowicz A.K., Panzica G.C. Endocrine disrupters: a review of some sources, effects, and mechanisms of actions on behaviour and neuroendocrine systems. J. Neuroendocrinol. 2012, 24:144-159.
21. Gonçalves 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, 30:195-201.
22. Hajszan T., Leranth C. Bisphenol A interferes with synaptic remodeling. Front. Neuroendocrinol. 2010, 31:519-530.
23. Hao J., Rapp P.R., Leffler A.E., Leffler S.R., Janssen W.G., Lou W., McKay H., Roberts J.A., Wearne S.L., Hof P.R. Estrogen alters spine number and morphology in prefrontal cortex of aged female rhesus monkeys. J. Neurosci. 2006, 26:2571-2578.
24. Hojo Y., Murakami G., Mukai H., Higo S., Hatanaka Y., Ogiue-Ikeda M., Ishii H., Kimoto T., Kawato S. Estrogen synthesis in the brain-role in synaptic plasticity and memory. Mol. Cell. Endocrinol. 2008, 290:31-43.
25. Ito M. Long-term depression as a memory process in the cerebellum. Neurosci. Res. 1986, 3:531-539.
26. Itoh K., Yaoi T., Fushiki S. Bisphenol A, an endocrine-disrupting chemical, and brain development. Neuropathology 2012, 32:447-457.
27. Jašarević E., Williams S.A., Vandas G.M., Ellersieck M.R., Liao C., Kannan K., Roberts R.M., Geary D.C., Rosenfeld C.S. Sex and dose-dependent effects of developmental exposure to bisphenol A on anxiety and spatial learning in deer mice (Peromyscus maniculatus bairdii) offspring. Horm. Behav. 2012, 63:180-189.
28. Jones B.A., Watson N.V. Perinatal BPA exposure demasculinizes males in measures of affect but has no effect on water maze learning in adulthood. Horm. Behav. 2012, 61:605-610.
29. Küçük A., Gölgeli A., Saraymen R., Koç N. Effects of age and anxiety on learning and memory. Behav. Brain Res. 2008, 195:147-152.
30. Kandel E.R. The molecular biology of memory storage: a dialogue between genes and synapses. Science 2001, 294:1030-1038.
31. Kawamoto Y., Matsuyama W., Wada M., Hishikawa J., Chan M.P.L., Nakayama A., Morisawa S. Development of a physiologically based pharmacokinetic model for bisphenol A in pregnant mice. Toxicol. Appl. Pharmacol. 2007, 224:182-191.
32. Kim E., Sheng M. PDZ domain proteins of synapses. Nat. Rev. Neurosci. 2004, 5:771-781.
33. Kim K., Son T.G., Park H.R., Kim S.J., Kim H.S., Kim H.S., Kim T.S., Jung K.K., Han S.Y., Lee J. Potencies of bisphenol A on the neuronal differentiation and hippocampal neurogenesis. J. Toxicol. Environ. Health A 2009, 72:1343-1351.
34. Koch H.M., Kolossa-Gehring M., Schröter-Kermani C., Angerer J., Brüning T. Bisphenol A in 24h urine and plasma samples of the German Environmental Specimen Bank from 1995 to 2009: a retrospective exposure evaluation. J. Expo. Sci. Environ. Epidemiol. 2012, 22:610-616.
35. Komada M., Asai Y., Morii M., Matsuki M., Sato M., Nagao T. Maternal bisphenol A oral dosing relates to the acceleration of neurogenesis in the developing neocortex of mouse fetuses. Toxicology 2012, 295:31-38.
36. Kubwabo C., Kosarac I., Stewart B., Gauthier B.R., Lalonde K., Lalonde P.J. Migration of bisphenol A from plastic baby bottles, baby bottle liners and reusable polycarbonate drinking bottles. Food Addit. Contam. Part A: Chem. Anal. Control Expo. Risk Assess. 2009, 26:928-937.
37. Kunz N., Camm E.J., Somm E., Lodygensky G., Darbre S., Aubert M.L., Hüppi P.S., Sizonenko S.V., Gruetter R. Developmental and metabolic brain alterations in rats exposed to bisphenol A during gestation and lactation. Int. J. Dev. Neurosci. 2011, 29:37-43.
38. Kwon S.E., Chapman E.R. Synaptophysin regulates the kinetics of synaptic vesicle endocytosis in central neurons. Neuron 2011, 70:847-854.
39. LaKind J.S., Levesque J., Dumas P., Bryan S., Clarke J., Naiman D.Q. Comparing United States and Canadian population exposures from National Biomonitoring Surveys: bisphenol A intake as a case study. J. Expo. Sci. Environ. Epidemiol. 2012, 22:219-226.
40. 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.
41. Leranth C., Szigeti-Buck K., MacLusky N.J., Hajszan T. Bisphenol A prevents the synaptogenic response to testosterone in the brain of adult male rats. Endocrinology 2008, 149:988-994.
42. Li B., Otsu Y., Murphy T.H., Raymond L.A. Developmental decrease in NMDA receptor desensitization associated with shift to synapse and interaction with postsynaptic density-95. J. Neurosci. 2003, 23:11244-11254.
43. Lin Y., Skeberdis V.A., Francesconi A., Bennett M.V., Zukin R.S. Postsynaptic density protein-95 regulates NMDA channel gating and surface expression. J. Neurosci. 2004, 24:10138-10148.
44. Luine V. Sex steroids and cognitive function. J. Neuroendocrinol. 2008, 20:866-872.
45. MacLusky N., Hajszan T., Prange-Kiel J., Leranth C. Androgen modulation of hippocampal synaptic plasticity. Neuroscience 2006, 138:957-965.
46. MacLusky N.J., Hajszan T., Leranth C. The environmental estrogen bisphenol A inhibits estradiol-induced hippocampal synaptogenesis. Environ. Health Perspect. 2005, 113:675-679.
47. MacLusky N.J., Naftolin F. Sexual differentiation of the central nervous system. Science 1981, 211:1294-1302.
48. Meng X.H., Liu P., Wang H., Zhao X.F., Xu Z.-M., Chen G.H., Xu D.X. Gender-specific impairments on cognitive and behavioral development in mice exposed to fenvalerate during puberty. Toxicol. Lett. 2011, 203:245-251.
49. Migaud M., Charlesworth P., Dempster M., Webster L.C., Watabe A.M., Makhinson M., He Y., Ramsay M.F., Morris R.G., Morrison J.H. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 1998, 396:433-439.
50. Mukai H., Kimoto T., Hojo Y., Kawato S., Murakami G., Higo S., Hatanaka Y., Ogiue-Ikeda M. Modulation of synaptic plasticity by brain estrogen in the hippocampus. Biochim. Biophys. Acta 2010, 1800:1030-1044.
51. Nishikawa M., Iwano H., Yanagisawa R., Koike N., Inoue H., Yokota H. Placental transfer of conjugated bisphenol A and subsequent reactivation in the rat fetus. Environ. Health Perspect. 2010, 118:1196-1203.
52. Prut L., Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol. 2003, 463:3-33.
53. Ramos J.G., Varayoud J., Kass L., Rodríguez H., Costabel L., Muñoz-de-Toro M., Luque E.H. Bisphenol A induces both transient and permanent histofunctional alterations of the hypothalamic-pituitary-gonadal axis in prenatally exposed male rats. Endocrinology 2003, 144:3206-3215.
54. Rubin B.S., Lenkowski J.R., Schaeberle C.M., Vandenberg L.N., Ronsheim P.M., Soto A.M. Evidence of altered brain sexual differentiation in mice exposed perinatally to low, environmentally relevant levels of bisphenol A. Endocrinology 2006, 147:3681-3691.
55. Ryan B.C., Hotchkiss A.K., Crofton K.M., Gray L.E. In utero and lactational exposure to bisphenol A, in contrast to ethinyl estradiol, does not alter sexually dimorphic behavior, puberty, fertility, and anatomy of female LE rats. Toxicol. Sci. 2010, 114:133-148.
56. Ryan X.P., Alldritt J., Svenningsson P., Allen P.B., Wu G.-Y., Nairn A.C., Greengard P. The Rho-specific GEF Lfc interacts with neurabin and spinophilin to regulate dendritic spine morphology. Neuron 2005, 47:85-100.
57. Sanderson D.J., McHugh S.B., Good M.A., Sprengel R., Seeburg P.H., Rawlins J.N.P., Bannerman D.M. Spatial working memory deficits in GluA1 AMPA receptor subunit knockout mice reflect impaired short-term habituation. Evidence for Wagner's dual-process memory model. Neuropsychologia 2010, 48:2303-2315.
58. Schmitt U., Tanimoto N., Seeliger M., Schaeffel F., Leube R. Detection of behavioral alterations and learning deficits in mice lacking synaptophysin. Neuroscience 2009, 162:234-243.
59. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 2008, 3:1101-1108.
60. Schwarz J.M., Liang S.L., Thompson S.M., McCarthy M.M. Estradiol induces hypothalamic dendritic spines by enhancing glutamate release: a mechanism for organizational sex differences. Neuron 2008, 58:584-598.
61. Stein V., House D.R., Bredt D.S., Nicoll R.A. Postsynaptic density-95 mimics and occludes hippocampal long-term potentiation and enhances long-term depression. J. Neurosci. 2003, 23:5503-5506.
62. Stump D.G., Beck M.J., Radovsky A., Garman R.H., Freshwater L.L., Sheets L.P., Marty M.S., Waechter J.M., Dimond S.S., Van Miller J.P. Developmental neurotoxicity study of dietary bisphenol A in Sprague-Dawley rats. Toxicol. Sci. 2010, 115:167-182.
63. Tarsa L., Goda Y. Synaptophysin regulates activity-dependent synapse formation in cultured hippocampal neurons. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:1012-1016.
64. Thiels E., Klann E. Extracellular signal-regulated kinase, synaptic plasticity, and memory. Rev. Neurosci. 2001, 12:327-346.
65. Vandenberg L., Chahoud I., Heindel J.J., Padmanabhan V., Paumgartten F.J., Schoenfelder G. Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environ. Health Perspect. 2010, 118:1055-1070.
66. Vandenberg L.N., Maffini M.V., Sonnenschein C., Rubin B.S., Soto A.M. Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr. Rev. 2009, 30:75-95.
67. Watanabe S., Wang R.S., Miyagawa M., Kobayashi K., Suda M., Sekiguchi S., Honma T. Imbalance of testosterone level in male offspring of rats perinatally exposed to bisphenol A. Ind. Health 2003, 41:338-341.
68. Willhite C.C., Ball G.L., McLellan C.J. Derivation of a bisphenol A oral reference dose (RfD) and drinking-water equivalent concentration. J. Toxicol. Environ. Health B Crit. Rev. 2008, 11:69-146.
69. Wolff M.S., Engel S.M., Berkowitz G.S., Ye X., Silva M.J., Zhu C., Wetmur J., Calafat A.M. Prenatal phenol and phthalate exposures and birth outcomes. Environ. Health Perspect. 2008, 116:1092-1097.
70. Xi W., Lee C., Yeung W., Giesy J.P., Wong M., Zhang X., Hecker M., Wong C.K. Effect of perinatal and postnatal bisphenol A exposure to the regulatory circuits at the hypothalamus-pituitary-gonadal axis of CD-1 mice. Reprod. Toxicol. 2011, 31:409-417.
71. Xu X.H., Zhang J., Wang Y.M., Ye Y.P., Luo Q.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, 58:326-333.
72. Xu X., Xie L., Hong X., Ruan Q., Lu H., Zhang Q., Zhang G., Liu X. Perinatal exposure to bisphenol-A inhibits synaptogenesis and affects the synaptic morphological development in offspring male mice. Chemosphere 2013, 91:1073-1081.
73. Xu X., Zhang Z. Effects of estradiol benzoate on learning-memory behavior and synaptic structure in ovariectomized mice. Life Sci. 2006, 79:1553-1560.
74. Ye X., Pierik F.H., Hauser R., Duty S., Angerer J., Park M.M., Burdorf A., Hofman A., Jaddoe V.W., Mackenbach J.P. Urinary metabolite concentrations of organophosphorous pesticides, bisphenol A, and phthalates among pregnant women in Rotterdam, the Netherlands: the Generation R study. Environ. Res. 2008, 108:260-267.
75. Zhou W., Liu J., Liao L., Han S., Liu J. Effect of bisphenol A on steroid hormone production in rat ovarian theca-interstitial and granulosa cells. Mol. Cell. Endocrinol. 2008, 283:12-18.
76. 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.