Effects of perinatal exposure to low dose of bisphenol A on anxiety like behavior and dopamine metabolites in brain

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 39, Issue 2, 2012, Pages 273-279

  Matsuda, Shingo ^a   Matsuzawa, Daisuke ^a   Ishii, Daisuke ^a   Tomizawa, Haruna ^a   Sutoh, Chihiro ^a   Nakazawa, Ken ^a   Amano, Keiko ^b   Sajiki, Junko ^a   Shimizu, Eiji ^a  

^a CHIBA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b Seifuso Hospital   (Japan)

Author keywords

Anxiety; BPA; Dopamine; MAO; Sex differences

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; 4,4' ISOPROPYLIDENEDIPHENOL; AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME B; DOPAMINE;

ADULT ANIMAL; AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; CONTROLLED STUDY; DOPAMINE BRAIN LEVEL; DOPAMINE METABOLISM; DOPAMINERGIC SYSTEM; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPUS; JUVENILE ANIMAL; MALE; MEDULLA OBLONGATA; MOUSE; NONHUMAN; OPEN FIELD TEST; PERINATAL PERIOD; SEX DIFFERENCE;

3,4-DIHYDROXYPHENYLACETIC ACID; AMYGDALA; ANIMALS; ANXIETY; BENZHYDRYL COMPOUNDS; DOPAMINE; ENDOCRINE DISRUPTORS; FEMALE; HIPPOCAMPUS; MALE; MEDULLA OBLONGATA; MICE; MICE, INBRED C57BL; MONOAMINE OXIDASE; MOTOR ACTIVITY; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SEX CHARACTERISTICS;

EID: 84866976400     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2012.06.016     Document Type: Article

References (57)

1. Akingbemi B.T., Sottas C.M., Koulova A.I., Klinefelter G.R., Hardy M.P. Inhibition of testicular steroidogenesis by the xenoestrogen bisphenol A is associated with reduced pituitary luteinizing hormone secretion and decreased steroidogenic enzyme gene expression in rat Leydig cells. Endocrinology 2004, 145:592-603.
2. Bananej M., Karimi-Sori A., Zarrindast M.R., Ahmadi S. D1 and D2 dopaminergic systems in the rat basolateral amygdala are involved in anxiogenic-like effects induced by histamine. J Psychopharmacol 2012, 26:564-574.
3. Benachour N., Moslemi S., Sipahutar H., Seralini G.E. Cytotoxic effects and aromatase inhibition by xenobiotic endocrine disrupters alone and in combination. Toxicol Appl Pharmacol 2007, 222:129-140.
4. Braun J.M., Kalkbrenner A.E., Calafat A.M., Yolton K., Ye X., Dietrich K.N., et al. Impact of early-life bisphenol a exposure on behavior and executive function in children. Pediatrics 2011, 128:873-882.
5. Chen K., Holschneider D.P., Wu W., Rebrin I., Shih J.C. A spontaneous point mutation produces monoamine oxidase A/B knock-out mice with greatly elevated monoamines and anxiety-like behavior. J Biol Chem 2004, 279:39645-39652.
6. Chiavegatto S., Izidio G.S., Mendes-Lana A., Aneas I., Freitas T.A., Torrao A.S., et al. Expression of alpha-synuclein is increased in the hippocampus of rats with high levels of innate anxiety. Mol Psychiatry 2009, 14:894-905.
7. 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.
8. de la Mora M.P., Cardenas-Cachon L., Vazquez-Garcia M., Crespo-Ramirez M., Jacobsen K., Hoistad M., et al. Anxiolytic effects of intra-amygdaloid injection of the D1 antagonist SCH23390 in the rat. Neurosci Lett 2005, 377:101-105.
9. Farabollini F., Porrini S., Dessi-Fulgherit F. Perinatal exposure to the estrogenic pollutant bisphenol A affects behavior in male and female rats. Pharmacol Biochem Behav 1999, 64:687-694.
10. Fiedorowicz J.G., He J., Merikangas K.R. The association between mood and anxiety disorders with vascular diseases and risk factors in a nationally representative sample. J Psychosom Res 2011, 70:145-154.
11. Fornai F., Chen K., Giorgi F.S., Gesi M., Alessandri M.G., Shih J.C. Striatal dopamine metabolism in monoamine oxidase B-deficient mice: a brain dialysis study. J Neurochem 1999, 73:2434-2440.
12. Gioiosa L., Fissore E., Ghirardelli G., Parmigiani S., Palanza P. Developmental exposure to low-dose estrogenic endocrine disruptors alters sex differences in exploration and emotional responses in mice. Horm Behav 2007, 52:307-316.
13. Granata A.R., Woodruff G.N. Dopaminergic mechanisms in the nucleus tractus solitarius and effects on blood pressure. Brain Res Bull 1982, 8:483-488.
14. Honma T., Miyagawa M., Suda M., Wang R.S., Kobayashi K., Sekiguchi S. Effects of perinatal exposure to bisphenol A on brain neurotransmitters in female rat offspring. Ind Health 2006, 44:510-524.
15. Hsieh C.L. Dynamics of DNA methylation pattern. Curr Opin Genet Dev 2000, 10:224-228.
16. Ishido M., Yonemoto J., Morita M. Mesencephalic neurodegeneration in the orally administered bisphenol A-caused hyperactive rats. Toxicol Lett 2007, 173:66-72.
17. Kawamura Y., Inoue K., Nakazawa H., Yamada T., Maitani T. Shokuhin Eiseigaku Zasshi 2001, 42:13-17.
18. Kitahama K., Nagatsu I., Geffard M., Maeda T. Distribution of dopamine-immunoreactive fibers in the rat brainstem. J Chem Neuroanat 2000, 18:1-9.
19. Kubo K., Arai O., Omura M., Watanabe R., Ogata R., Aou S. Low dose effects of bisphenol A on sexual differentiation of the brain and behavior in rats. Neurosci Res 2003, 45:345-356.
20. Kunz N., Camm E.J., Somm E., Lodygensky G., Darbre S., Aubert M.L., et al. Developmental and metabolic brain alterations in rats exposed to bisphenol A during gestation and lactation. Int J Dev Neurosci 2011, 29:37-43.
21. MacLusky N.J., Naftolin F. Sexual differentiation of the central nervous system. Science 1981, 211:1294-1302.
22. Matsuda S., Matsuzawa D., Nakazawa K., Sutoh C., Ohtsuka H., Ishii D., et al. d-Serine enhances extinction of auditory cued fear conditioning via ERK1/2 phosphorylation in mice. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34:895-902.
23. Matsuda S., Saika S., Amano K., Shimizu E., Sajiki J. Changes in brain monoamine levels in neonatal rats exposed to bisphenol A at low doses. Chemosphere 2010, 78:894-906.
24. McConnell J., Angevine J.B.J. Time of neuron origin in the amygdaloid complex of the mouse. Brain Res 1983, 272:150-156.
25. Nakamura K., Itoh K., Yoshimoto K., Sugimoto T., Fushiki S. Prenatal and lactational exposure to low-doses of bisphenol A alters brain monoamine concentration in adult mice. Neurosci Lett 2010, 484:66-70.
26. Pandaranandaka J., Poonyachoti S., Kalandakanond-Thongsong S. Anxiolytic property of estrogen related to the changes of the monoamine levels in various brain regions of ovariectomized rats. Physiol Behav 2006, 87:828-835.
27. Patisaul H.B., Bateman H.L. Neonatal exposure to endocrine active compounds or an ERbeta agonist increases adult anxiety and aggression in gonadally intact male rats. Horm Behav 2008, 53:580-588.
28. Perera F., Vishnevetsky J., Herbstman J.B., Calafat A.M., Xiong W., Rauh V., et al. Prenatal bisphenol A exposure and child behavior in an inner city cohort. Environ Health Perspect 2012, [Epub ahead of print].
29. Phillips J.K., Goodchild A.K., Dubey R., Sesiashvili E., Takeda M., Chalmers J., et al. Differential expression of catecholamine biosynthetic enzymes in the rat ventrolateral medulla. J Comp Neurol 2001, 432:20-34.
30. Picazo O., Chuc-Meza E., Anaya-Martinez V., Jimenez I., Aceves J., Garcia-Ramirez M. 6-Hydroxydopamine lesion in thalamic reticular nucleus reduces anxiety behaviour in the rat. Behav Brain Res 2009, 197:317-322.
31. Reyes B.A., Van Bockstaele E.J. Divergent projections of catecholaminergic neurons in the nucleus of the solitary tract to limbic forebrain and medullary autonomic brain regions. Brain Res 2006, 1117:69-79.
32. 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.
33. Sajiki J., Takahashi K., Yonekubo J. Sensitive method for the determination of bisphenol-A in serum using two systems of high-performance liquid chromatography. J Chromatogr B Biomed Sci 1999, 736:255-261.
34. Sajiki J., Miyamoto F., Fukata H., Mori C., Yonekubo J., Hayakawa K. Bisphenol A (BPA) and its source in foods in Japanese markets. Food Addit Contam 2007, 24:103-112.
35. Schonfelder G., Wittfoht W., Hopp H., Talsness C.E., Paul M., Chahoud I. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ Health Perspect 2002, 110:703-707.
36. Shih J.C., Chen K. Regulation of MAO-A and MAO-B gene expression. Curr Med Chem 2004, 11:1995-2005.
37. Sun Y., Irie M., Kishikawa N., Wada M., Kuroda N., Nakashima K. Determination of bisphenol A in human breast milk by HPLC with column-switching and fluorescence detection. Biomed Chromatogr 2004, 18:501-507.
38. Takayanagi S., Tokunaga T., Liu X., Okada H., Matsushima A., Shimohigashi Y. Endocrine disruptor bisphenol A strongly binds to human estrogen-related receptor gamma (ERRgamma) with high constitutive activity. Toxicol Lett 2006, 167:95-105.
39. Tando S., Itoh K., Yaoi T., Ikeda J., Fujiwara Y., Fushiki S. Effects of pre- and neonatal exposure to bisphenol A on murine brain development. Brain Dev 2007, 29:352-356.
40. Tanida T., Warita K., Ishihara K., Fukui S., Mitsuhashi T., Sugawara T., et al. Fetal and neonatal exposure to three typical environmental chemicals with different mechanisms of action: mixed exposure to phenol, phthalate, and dioxin cancels the effects of sole exposure on mouse midbrain dopaminergic nuclei. Toxicol Lett 2009, 189:40-47.
41. Thiemann G., Watt C.A., Ledent C., Molleman A., Hasenohrl R.U. Modulation of anxiety by acute blockade and genetic deletion of the CB(1) cannabinoid receptor in mice together with biogenic amine changes in the forebrain. Behav Brain Res 2009, 200:60-67.
42. Thorpe L.W., Westlund K.N., Kochersperger L.M., Abell C.W., Denney R.M. Immunocytochemical localization of monoamine oxidases A and B in human peripheral tissues and brain. J Histochem Cytochem 1987, 35:23-32.
43. Tian Y.H., Baek J.H., Lee S.Y., Jang C.G. Prenatal and postnatal exposure to bisphenol a induces anxiolytic behaviors and cognitive deficits in mice. Synapse 2010, 64:432-439.
44. Tuchmann-Duplessis H., Auroux M., Haegel P. Illustrated human embryology 1974, Springer, New York. 1st ed.
45. Vandenberg L.N., Hauser R., Marcus M., Olea N., Welshons W.V. Human exposure to bisphenol A (BPA). Reprod Toxicol 2007, 24:139-177.
46. Vandenberg L.N., 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.
47. Wetherill Y.B., Akingbemi B.T., Kanno J., McLachlan J.A., Nadal A., Sonnenschein C., et al. In vitro molecular mechanisms of bisphenol A action. Reprod Toxicol 2007, 24:178-198.
48. Williams L.M., Gatt J.M., Schofield P.R., Olivieri G., Peduto A., Gordon E. 'Negativity bias' in risk for depression and anxiety: brain-body fear circuitry correlates, 5-HTT-LPR and early life stress. Neuroimage 2009, 47:804-814.
49. Wu M.V., et al. Estrogen masculinizes neural pathways and sex-specific behaviors. Cell 2009, 139:61-72.
50. 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.
51. Xu X., Tian D., Hong X., Chen L., Xie L. Sex-specific influence of exposure to bisphenol-A between adolescence and young adulthood on mouse behaviors. Neuropharmacology 2011, 61:565-573.
52. Yaoi T., Itoh K., Nakamura K., Ogi H., Fujiwara Y., Fushiki S. Genome-wide analysis of epigenomic alterations in fetal mouse forebrain after exposure to low doses of bisphenol A. Biochem Biophys Res Commun 2008, 376:563-567.
53. Yu C., Tai F., Song Z., Wu R., Zhang X., He F. Pubertal exposure to bisphenol A disrupts behavior in adult C57BL/6J mice. Environ Toxicol Pharmacol 2011, 31:88-99.
54. Zagon A., Totterdell S., Jones R.S. Direct projections from the ventrolateral medulla oblongata to the limbic forebrain: anterograde and retrograde tract-tracing studies in the rat. J Comp Neurol 1994, 340:445-468.
55. Zarrindast M.R., Naghdi-Sedeh N., Nasehi M., Sahraei H., Bahrami F., Asadi F. The effects of dopaminergic drugs in the ventral hippocampus of rats in the nicotine-induced anxiogenic-like response. Neurosci Lett 2010, 475:156-160.
56. Zhang Z., Chen K., Shih J.C., Teng C.T. Estrogen-related receptors-stimulated monoamine oxidase B promoter activity is down-regulated by estrogen receptors. Mol Endocrinol 2006, 20:1547-1561.
57. Zhou R., Bai Y., Yang R., Zhu Y., Chi X., Li L., et al. Abnormal synaptic plasticity in basolateral amygdala may account for hyperactivity and attention-deficit in male rat exposed perinatally to low-dose bisphenol-A. Neuropharmacology 2011, 60:789-798.