Developmental and metabolic brain alterations in rats exposed to bisphenol A during gestation and lactation

International Journal of Developmental Neuroscience

Volumn 29, Issue 1, 2011, Pages 37-43

  Kunz, Nicolas ^a,b   Camm, Emily Jane ^b   Somm, Emmanuel ^b   Lodygensky, Gregory ^b   Darbre, Stéphanie ^b   Aubert, Michel Lucien ^b   Hüppi, Petra Susan ^b   Sizonenko, Stéphane Vladimir ^b   Gruetter, Rolf ^a,b,c  

^a EPFL   (Switzerland)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Bisphenol A; Brain development; Cerebral metabolism; Malate aspartate shuttle; Mitochondria; Nuclear magnetic resonance

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ASPARTIC ACID; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMIC ACID; MALIC ACID; MYELIN BASIC PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN DEVELOPMENT; BRAIN GROWTH; BRAIN METABOLISM; CONTROLLED STUDY; CORPUS CALLOSUM; GLUCOSE OXIDATION; HIPPOCAMPUS; HISTOPATHOLOGY; LACTATION; MOTOR CORTEX; MYELINATION; NEWBORN; NONHUMAN; PERINATAL DRUG EXPOSURE; PREGNANCY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; SOMATOSENSORY CORTEX;

ANIMALS; ASPARTIC ACID; BRAIN; ENDOCRINE DISRUPTORS; ENERGY METABOLISM; ESTROGENS, NON-STEROIDAL; FEMALE; GLUTAMIC ACID; HUMANS; LACTATION; MAGNETIC RESONANCE SPECTROSCOPY; MALE; NEUROGLIA; NEURONS; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 78650170729     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2010.09.009     Document Type: Article

References (53)

1. Adachi T., Takanaga H., Sakurai Y., Ishido M., Kunimoto M., Asou H. Influence of cell density and thyroid hormone on glial cell development in primary cultures of embryonic rat cerebral hemisphere. J. Neurosci. Res. 2002, 69:61-71.
2. Aydogan M., Korkmaz A., Barlas N., Kolankaya D. The effect of vitamin C on bisphenol A, nonylphenol and octylphenol induced brain damages of male rats. Toxicology 2008, 249:35-39.
3. Bindhumol V., Chitra K.C., Mathur P.P. Bisphenol A induces reactive oxygen species generation in the liver of male rats. Toxicology 2003, 188:117-124.
4. Cai Z., Lin S., Fan L.W., Pang Y., Rhodes P.G. Minocycline alleviates hypoxic-ischemic injury to developing oligodendrocytes in the neonatal rat brain. Neuroscience 2006, 137:425-435.
5. Calafat A.M., Kuklenyik Z., Reidy J.A., Caudill S.P., Ekong J., Needham L.L. Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ. Health Perspect. 2005, 113:391-395.
6. Chaban V.V., Lakhter A.J., Micevych P. A membrane estrogen receptor mediates intracellular calcium release in astrocytes. Endocrinology 2004, 145:3788-3795.
7. Choi I.S., Cho J.H., Park E.J., Park J.W., Kim S.H., Lee M.G., Choi B.J., Jang I.S. Multiple effects of bisphenol A, an endocrine disrupter, on GABA(A) receptors in acutely dissociated rat CA3 pyramidal neurons. Neurosci. Res. 2007, 59:8-17.
8. Dessi-Fulgheri F., Porrini S., Farabollini F. Effects of perinatal exposure to bisphenol A on play behavior of female and male juvenile rats. Environ. Health Perspect. 2002, 110(Suppl. 3):403-407.
9. Facciolo R.M., Alo R., Madeo M., Canonaco M., Dessi-Fulgheri F. Early cerebral activities of the environmental estrogen bisphenol A appear to act via the somatostatin receptor subtype sst(2). Environ. Health Perspect. 2002, 110(Suppl. 3):397-402.
10. Farabollini F., Porrini S., Della Seta D., Bianchi F., Dessi-Fulgheri F. Effects of perinatal exposure to bisphenol A on sociosexual behavior of female and male rats. Environ. Health Perspect. 2002, 110(Suppl. 3):409-414.
11. Fujimaki K., Arakawa C., Yoshinaga J., Watanabe C., Serizawa S., Imai H., Shiraishi H., Mizumoto Y. Estimation of intake level of bisphenol A in Japanese pregnant women based on measurement of urinary excretion level of the metabolite. Nippon Eiseigaku Zasshi 2004, 59:403-408.
12. Gruetter R. Automatic, localized in vivo adjustment of all first- and second-order shim coils. Magn. Reson. Med. 1993, 29:804-811.
13. Hosli E., Jurasin K., Ruhl W., Luthy R., Hosli L. Colocalization of androgen, estrogen and cholinergic receptors on cultured astrocytes of rat central nervous system. Int. J. Dev. Neurosci. 2001, 19:11-19.
14. Ikemoto S., Witkin B., Zangen A., Wise R. Rewarding Effects of AMPA Administration into the Supramammillary or Posterior Hypothalamic Nuclei But Not the Ventral Tegmental Area. J. Neurosci. 2004, 24:5758-5765.
15. Ikezuki Y., Tsutsumi O., Takai Y., Kamei Y., Taketani Y. Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum. Reprod. 2002, 17:2839-2841.
16. Ishido M., Masuo Y., Kunimoto M., Oka S., Morita M. Bisphenol A causes hyperactivity in the rat concomitantly with impairment of tyrosine hydroxylase immunoreactivity. J. Neurosci. Res. 2004, 76:423-433.
17. Kabuto H., Amakawa M., Shishibori T. Exposure to bisphenol A during embryonic/fetal life and infancy increases oxidative injury and causes underdevelopment of the brain and testis in mice. Life Sci. 2004, 74:2931-2940.
18. Kabuto H., Hasuike S., Minagawa N., Shishibori T. Effects of bisphenol A on the metabolisms of active oxygen species in mouse tissues. Environ. Res. 2003, 93:31-35.
19. Kubo T., Maezawa N., Osada M., Katsumura S., Funae Y., Imaoka S. Bisphenol A, an environmental endocrine-disrupting chemical, inhibits hypoxic response via degradation of hypoxia-inducible factor 1alpha (HIF-1alpha): structural requirement of bisphenol A for degradation of HIF-1alpha. Biochem. Biophys. Res. Commun. 2004, 318:1006-1011.
20. Lee S., Suk K., Kim I.K., Jang I.S., Park J.W., Johnson V.J., Kwon T.K., Choi B.J., Kim S.H. 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-kappaB. J. Neurosci. Res. 2008, 86:2932-2942.
21. 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.
22. Maclusky N.J., Hajszan T., Leranth C. The environmental estrogen bisphenol a inhibits estradiol-induced hippocampal synaptogenesis. Environ. Health Perspect. 2005, 113:675-679.
23. Miyatake M., Miyagawa K., Mizuo K., Narita M., Suzuki T. Dynamic changes in dopaminergic neurotransmission induced by a low concentration of bisphenol-A in neurones and astrocytes. J. Neuroendocrinol. 2006, 18:434-444.
24. Nakagawa Y., Tayama S. Metabolism and cytotoxicity of bisphenol A and other bisphenols in isolated rat hepatocytes. Arch. Toxicol. 2000, 74:99-105.
25. Nakamura K., Itoh K., Yaoi T., Fujiwara Y., Sugimoto T., Fushiki S. Murine neocortical histogenesis is perturbed by prenatal exposure to low doses of bisphenol A. J. Neurosci. Res. 2006, 84:1197-1205.
26. 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.
27. Ooe H., Taira T., Iguchi-Ariga S.M., Ariga H. Induction of reactive oxygen species by bisphenol A and abrogation of bisphenol A-induced cell injury by DJ-1. Toxicol. Sci. 2005, 88:114-126.
28. Palanza P., Gioiosa L., Vom Saal F.S., Parmigiani S. Effects of developmental exposure to bisphenol A on brain and behavior in mice. Environ. Res. 2008, 108:150-157.
29. Paris F., Balaguer P., Terouanne B., Servant N., Lacoste C., Cravedi J.P., Nicolas J.C., Sultan C. Phenylphenols, biphenols, bisphenol-A and 4-tert-octylphenol exhibit alpha and beta estrogen activities and antiandrogen activity in reporter cell lines. Mol. Cell. Endocrinol. 2002, 193:43-49.
30. Pfeuffer J., Tkac I., Provencher S.W., Gruetter R. Toward an in vivo neurochemical profile: quantification of 18 metabolites in short-echo-time (1)H NMR spectra of the rat brain. J. Magn. Reson. 1999, 141:104-120.
31. Provencher S.W. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn. Reson. Med. 1993, 30:672-679.
32. Raman L., Tkac I., Ennis K., Georgieff M.K., Gruetter R., Rao R. In vivo effect of chronic hypoxia on the neurochemical profile of the developing rat hippocampus. Brain Res. Dev. Brain Res. 2005, 156:202-209.
33. Ranjit N., Siefert K., Padmanabhan V. Bisphenol-A and disparities in birth outcomes: a review and directions for future research. J. Perinatol. 2009, 30:2-9.
34. Rao R., Tkac I., Townsend E.L., Gruetter R., Georgieff M.K. Perinatal iron deficiency alters the neurochemical profile of the developing rat hippocampus. J. Nutr. 2003, 133:3215-3221.
35. Rasband, W.S., 1997-2009. ImageJ, Bethesda, MD, USA, http://rsb.info.nih.gov/ij/.
36. Rubin B.S., Murray M.K., Damassa D.A., King J.C., Soto A.M. Perinatal exposure to low doses of bisphenol A affects body weight, patterns of estrous cyclicity, and plasma LH levels. Environ. Health Perspect. 2001, 109:675-680.
37. Sato K., Matsuki N., Ohno Y., Nakazawa K. Effects of 17beta-estradiol and xenoestrogens on the neuronal survival in an organotypic hippocampal culture. Neuroendocrinology 2002, 76:223-234.
38. Sato K., Matsuki N., Ohno Y., Nakazawa K. Estrogens inhibit l-glutamate uptake activity of astrocytes via membrane estrogen receptor alpha. J. Neurochem. 2003, 86:1498-1505.
39. 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:A703-A707.
40. Seiwa C., Nakahara J., Komiyama T., Katsu Y., Iguchi T., Asou H. Bisphenol A exerts thyroid-hormone-like effects on mouse oligodendrocyte precursor cells. Neuroendocrinology 2004, 80:21-30.
41. Shikimi H., Sakamoto H., Mezaki Y., Ukena K., Tsutsui K. Dendritic growth in response to environmental estrogens in the developing Purkinje cell in rats. Neurosci. Lett. 2004, 364:114-118.
42. Silva A.J. Molecular and cellular cognitive studies of the role of synaptic plasticity in memory. J. Neurobiol. 2003, 54:224-237.
43. Somm E., Schwitzgebel V.M., Toulotte A., Cederroth C.R., Combescure C., Nef S., Aubert M.L., Huppi P.S. Perinatal exposure to bisphenol a alters early adipogenesis in the rat. Environ. Health Perspect. 2009, 117:1549-1555.
44. Takeuchi T., Tsutsumi O. Serum bisphenol a concentrations showed gender differences, possibly linked to androgen levels. Biochem. Biophys. Res. Commun. 2002, 291:76-78.
45. 1H NMR spectroscopy. Magn. Reson. Med. 2003, 50:24-32.
46. 1H NMR spectroscopy of rat brain at 1ms echo time. Magn. Reson. Med. 1999, 41:649-656.
47. 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.
48. Vom Saal F.S., Cooke P.S., Buchanan D.L., Palanza P., Thayer K.A., Nagel S.C., Parmigiani S., Welshons W.V. A physiologically based approach to the study of bisphenol A and other estrogenic chemicals on the size of reproductive organs, daily sperm production, and behavior. Toxicol. Ind. Health 1998, 14:239-260.
49. Xing L., Xu Y., Xiao Y., Shang L., Liu R., Wei X., Jiang J., Hao W. Embryotoxic and teratogenic effects of the combination of bisphenol A and genistein on in vitro cultured postimplantation rat embryos. Toxicol. Sci. 2010, 115:577-588.
50. Yamaguchi H., Zhu J., Yu T., Sasaki K., Umetsu H., Kidachi Y., Ryoyama K. Low-level bisphenol A increases production of glial fibrillary acidic protein in differentiating astrocyte progenitor cells through excessive STAT3 and Smad1 activation. Toxicology 2006, 226:131-142.
51. Ye X., Kuklenyik Z., Needham L.L., Calafat A.M. Quantification of urinary conjugates of bisphenol A, 2,5-dichlorophenol, and 2-hydroxy-4-methoxybenzophenone in humans by online solid phase extraction-high performance liquid chromatography-tandem mass spectrometry. Anal. Bioanal. Chem. 2005, 383:638-644.
52. Zhou R., Zhang Z., Zhu Y., Chen L., Sokabe M., Chen L. Deficits in development of synaptic plasticity in rat dorsal striatum following prenatal and neonatal exposure to low-dose bisphenol A. Neuroscience 2009, 159:161-171.
53. Zoeller R.T. Environmental chemicals impacting the thyroid: targets and consequences. Thyroid 2007, 17:811-817.