Effects of perinatal bisphenol A exposure during early development on radial arm maze behavior in adult male and female rats

Neurotoxicology and Teratology

Volumn 42, Issue , 2014, Pages 17-24

  Sadowski, Renee N ^a   Park, Pul ^a   Neese, Steven L ^a   Ferguson, Duncan C ^a   Schantz, Susan L ^a   Juraska, Janice M ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

BPA; Cognition; Spatial learning; T4; Thyroxine

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; CORN OIL; FOLLITROPIN; LUTEINIZING HORMONE; THYROTROPIN; THYROXINE; BENZHYDRYL DERIVATIVE; ENDOCRINE DISRUPTOR; HORMONE; PHENOL DERIVATIVE;

ADULT; ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR DISORDER; COGNITIVE DEFECT; CONTROLLED STUDY; EXPOSURE; FEMALE; HORMONE DETERMINATION; MALE; NONHUMAN; PERINATAL PERIOD; PREGNANCY; PRIORITY JOURNAL; RADIAL ARM MAZE TEST; RAT; REFERENCE MEMORY; TASK PERFORMANCE; WEANING; WORKING MEMORY; ANIMAL; BLOOD; CHEMICALLY INDUCED; DRUG EFFECTS; LONG EVANS RAT; MAZE TEST; ORAL DRUG ADMINISTRATION; PRENATAL EXPOSURE; PSYCHOLOGY; SHORT TERM MEMORY; TOXICITY;

ADMINISTRATION, ORAL; ANIMALS; BENZHYDRYL COMPOUNDS; ENDOCRINE DISRUPTORS; FEMALE; FOLLICLE STIMULATING HORMONE; HORMONES; MALE; MAZE LEARNING; MEMORY, SHORT-TERM; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, LONG-EVANS;

EID: 84893391059     PISSN: 08920362     EISSN: 18729738     Source Type: Journal    
DOI: 10.1016/j.ntt.2014.01.002     Document Type: Article

References (65)

1. Adewale H.B., Jefferson W.N., Newbold R.R., Patisaul H.B. Neonatal bisphenol-a exposure alters rat reproductive development and ovarian morphology without impairing activation of gonadotropin-releasing hormone neurons. Biol Reprod 2009, 81:690-699.
2. Adriani W., Seta D.D., Dessi-Fulgheri F., Farabollini F., Laviola G. Altered profiles of spontaneous novelty seeking, impulsive behavior, and response to d-amphetamine in rats perinatally exposed to bisphenol A. Environ Health Perspect 2003, 111:395-401.
3. Atanassova N., McKinnell C., Turner K.J., Walker M., Fisher J.S., Morley M., et al. Comparative effects of neonatal exposure of male rats to potent and weak (environmental) estrogens on spermatogenesis at puberty and the relationship to adult testis size and fertility: evidence for stimulatory effects of low estrogen levels. Endocrinology 2000, 141:3898-3907.
4. Bai Y., Chang F., Zhou R., Jin P.P., Matsumoto H., Sokabe M., et al. Increase of anteroventral periventricular kisspeptin neurons and generation of E2-induced LH-surge system in male rats exposed perinatally to environmental dose of bisphenol-A. Endocrinology 2011, 152:1562-1571.
5. Beatty W.W. Hormonal organization of sex differences in play fighting and spatial behavior. Prog Brain Res 1984, 61:315-330.
6. Biedermann S., Tschudin P., Grob K. Transfer of bisphenol A from thermal printer paper to the skin. Anal Bioanal Chem 2010, 398:571-576.
7. Biles J.E., McNeal T.P., Begley T.H., Hollifield H.C. Determination of bisphenol-A in reusable polycarbonate food-contact plastics and migration to food-stimulating liquids. J Agric Food Chem 1997, 45:3541-3544.
8. Brotons J.A., Olea-Serrano M.F., Villalobos M., Pedraza V., Olea N. Xenoestrogens released from lacquer coatings in food cans. Environ Health Perspect 1995, 103:608-612.
9. Calafat A.M., Ye X., Wong L.Y., Reidy J.A., Needham L.L. Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003-2004. Environ Health Perspect 2008, 116:39-44.
10. Cardoso N., Pandolfi M., Ponzo O., Carbone S., Szwarcfarb B., Scacchi P., et al. Evidence to suggest glutamic acid involvement in bisphenol A effect at the hypothalamic level in prepubertal male rats. Neuro Endocrinol Lett 2010, 31:512-516.
11. Clancy B., Finlay B.L., Darlington R.B., Anand K.J. Extrapolating brain development from experimental species to humans. Neurotoxicology 2007, 28:931-937.
12. 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.
13. Dobbing J., Sands J. Comparative aspects of the brain growth spurt. Early Hum Dev 1979, 3:79-83.
14. Doerge D.R., Vanlandingham M., Twaddle N.C., Delclos K.B. Lactational transfer of bisphenol A in Sprague-Dawley rats. Toxicol Lett 2010, 199:372-376.
15. Ema M., Fujii S., Furukawa M., Kiguchi M., Ikka T., Harazono A. Rat two-generation reproductive toxicity study of bisphenol A. Reprod Toxicol 2001, 15:505-523.
16. Ferguson S.A., Law C.D., Abshire J.S. Developmental treatment with bisphenol a or ethinyl estradiol causes few alterations on early preweaning measures. Toxicol Sci 2011, 124:149-160.
17. Ferguson S.A., Law C.D., Abshire J.S. Developmental treatment with bisphenol A causes few alterations on measures of postweaning activity and learning. Neurotoxicol Teratol 2012, 34:598-606.
18. Fernandez M., Bourguignon N., Lux-Lantos V., Libertun C. Neonatal exposure to bisphenol a and reproductive and endocrine alterations resembling the polycystic ovarian syndrome in adult rats. Environ Health Perspect 2010, 118:1217-1222.
19. Fujimoto T., Kubo K., Aou S. Prenatal exposure to bisphenol A impairs sexual differentiation of exploratory behavior and increases depression-like behavior in rats. Brain Res 2006, 1068:49-55.
20. 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.
21. Goncalves C.R., Cunha R.W., Barros D.M., Martinez 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. Gould J.C., Leonard L.S., Maness S.C., Wagner B.L., Conner K., Zacharewski T., et al. Bisphenol A interacts with the estrogen receptor alpha in a distinct manner from estradiol. Mol Cell Endocrinol 1998, 142:203-214.
23. Honma S., Suzuki A., Buchanan D.L., Katsu Y., Watanabe H., Iguchi T. Low dose effect of in utero exposure to bisphenol A and diethylstilbestrol on female mouse reproduction. Reprod Toxicol 2002, 16:117-122.
24. Howdeshell K.L., Hotchkiss A.K., Thayer K.A., Vandenbergh J.G., vom Saal F.S. Exposure to bisphenol A advances puberty. Nature 1999, 401:763-764.
25. Kato H., Furuhashi T., Tanaka M., Katsu Y., Watanabe H., Ohta Y., et al. Effects of bisphenol A given neonatally on reproductive functions of male rats. Reprod Toxicol 2006, 22:20-29.
26. Kendig E.L., Buesing D.R., Christie S.M., Cookman C.J., Gear R.B., Hugo E.R., et al. Estrogen-like disruptive effects of dietary exposure to bisphenol A or 17alpha-ethinyl estradiol in CD1 mice. Int J Toxicol 2012, 31:537-550.
27. Kobayashi K., Miyagawa M., Wang R.S., Sekiguchi S., Suda M., Honma T. Effects of in utero and lactational exposure to bisphenol A on somatic growth and anogenital distance in F1 rat offspring. Ind Health 2002, 40:375-381.
28. Kobayashi K., Miyagawa M., Wang R.S., Suda M., Sekiguchi S., Honma T. Effects of in utero and lactational exposure to bisphenol A on thyroid status in F1 rat offspring. Ind Health 2005, 43:685-690.
29. Krishnan A.V., Stathis P., Permuth S.F., Tokes L., Feldman D. Bisphenol-A: an estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology 1993, 132:2279-2286.
30. Kubo K., Arai O., Ogata R., Omura M., Hori T., Aou S. 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 2001, 304:73-76.
31. 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.
32. Kuiper G.G., Carlsson B., Grandien K., Enmark E., Haggblad J., Nilsson S., et al. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors α and β. Endocrinology 1997, 138:863-870.
33. Kuiper G.G., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., van der Saag P.T., et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 1998, 139:4252-4263.
34. LaBuda C.J., Mellgren R.L., Hale R.L. Sex differences in the acquisition of a radial maze task in the CD-1 mouse. Physiol Behav 2002, 76:213-217.
35. Mishima N., Higashitani F., Teraoka K., Yoshioka R. Sex differences in appetitive learning of mice. Physiol Behav 1986, 37:263-268.
36. Miyawaki J., Sakayama K., Kato H., Yamamoto H., Masuno H. Perinatal and postnatal exposure to bisphenol A increases adipose tissue mass and serum cholesterol level in mice. J Atheroscler Thromb 2007, 14:245-252.
37. Moriyama K., Tagami T., Akamizu T., Usui T., Saijo M., Kanamoto N., et al. Thyroid hormone action is disrupted by bisphenol A as an antagonist. J Clin Endocrinol Metab 2002, 87:5185-5190.
38. Nakamura K., Itoh K., Dai H., Han L., Wang X., Kato S., et al. Prenatal and lactational exposure to low-doses of bisphenol A alters adult mice behavior. Brain Dev 2012, 34:57-63.
39. Negishi T., Kawasaki K., Takatori A., Ishii Y., Kyuwa S., Kuroda Y., et al. Effects of perinatal exposure to bisphenol A on the behavior of offspring in F344 rats. Environ Toxicol Pharmacol 2003, 14:99-108.
40. Newbold R.R., Jefferson W.N., Padilla-Banks E. Long-term adverse effects of neonatal exposure to bisphenol A on the murine female reproductive tract. Reprod Toxicol 2007, 24:253-258.
41. Nikaido Y., Yoshizawa K., Danbara N., Tsujita-Kyutoku M., Yuri T., Uehara N., et al. Effects of maternal xenoestrogen exposure on development of the reproductive tract and mammary gland in female CD-1 mouse offspring. Reprod Toxicol 2004, 18:803-811.
42. NTP (National Toxicology Program) NTP-CERHR monograph on the potential human reproductive and developmental effects of bisphenol A 2008, [08-5994].
43. Olea N., Pulgar R., Perez P., Olea-Serrano F., Rivas A., Novillo-Fertrell A., et al. Estrogenicity of resin-based composites and sealants used in dentistry. Environ Health Perspect 1996, 104:298-305.
44. Ozaki A., Yamaguchi Y., Fujita T., Kuroda K., Endo G. Chemical analysis and genotoxicological safety assessment of paper and paperboard used for food packaging. Food Chem Toxicol 2004, 42:1323-1337.
45. 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.
46. 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.
47. 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.
48. Ryan B.C., Vandenbergh J.G. Developmental exposure to environmental estrogens alters anxiety and spatial memory in female mice. Horm Behav 2006, 50:85-93.
49. 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.
50. Sandi C., Loscertales M., Guaza C. Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze. Eur J Neurosci 1997, 9:637-642.
51. Schneider M.J., Fiering S.N., Thai B., Wu S.Y., St Germain E., Parlow A.F., et al. Targeted disruption of the type 1 selenodeiodinase gene (Dio1) results in marked changes in thyroid hormone economy in mice. Endocrinology 2006, 147:580-589.
52. Seymoure P., Dou H., Juraska J. Sex differences in radial arm performance: Influence of rearing environment and room cues. Psychobiology 1996, 24:33-37.
53. Somm E., Schwitzgebel V.M., Toulotte A., Cederroth C.R., Combescure C., Nef S., et al. Perinatal exposure to bisphenol a alters early adipogenesis in the rat. Environ Health Perspect 2009, 117:1549-1555.
54. Stump D.G., Beck M.J., Radovsky A., Garman R.H., Freshwater L.L., Sheets L.P., et al. Developmental neurotoxicity study of dietary bisphenol A in Sprague-Dawley rats. Toxicol Sci 2010, 115:167-182.
55. Taylor M.A., Swant J., Wagner J.J., Fisher J.W., Ferguson D.C. Lower thyroid compensatory reserve of rat pups after maternal hypothyroidism: correlation of thyroid, hepatic, and cerebrocortical biomarkers with hippocampal neurophysiology. Endocrinology 2008, 149:3521-3530.
56. Tees R.C., Midgley G., Nesbit J.C. The effect of early visual experience on spatial maze learning in rats. Dev Psychobiol 1981, 14:425-438.
57. Tinwell H., Haseman J., Lefevre P.A., Wallis N., Ashby J. Normal sexual development of two strains of rat exposed in utero to low doses of bisphenol A. Toxicol Sci 2002, 68:339-348.
58. Tyl R.W., Myers C.B., Marr M.C., Thomas B.F., Keimowitz A.R., Brine D.R., et al. Three-generation reproductive toxicity study of dietary bisphenol A in CD Sprague-Dawley rats. Toxicol Sci 2002, 68:121-146.
59. Tyl R.W., Myers C.B., Marr M.C., Sloan C.S., Castillo N.P., Veselica M.M., et al. Two-generation reproductive toxicity study of dietary bisphenol A in CD-1 (Swiss) mice. Toxicol Sci 2008, 104:362-384.
60. Volkel W., Colnot T., Csanady G.A., Filser J.G., Dekant W. Metabolism and kinetics of bisphenol a in humans at low doses following oral administration. Chem Res Toxicol 2002, 15:1281-1287.
61. Volkel W., Bittner N., Dekant W. Quantitation of bisphenol A and bisphenol A glucuronide in biological samples by high performance liquid chromatography-tandem mass spectrometry. Drug Metab Dispos 2005, 33:1748-1757.
62. Williams C.L., Meck W.H. The organizational effects of gonadal steroids on sexually dimorphic spatial ability. Psychoneuroendocrinology 1991, 16:155-176.
63. Xu X., Liu Y., Sadamatsu M., Tsutsumi S., Akaike M., Ushijima H., et al. Perinatal bisphenol A affects the behavior and SRC-1 expression of male pups but does not influence on the thyroid hormone receptors and its responsive gene. Neurosci Res 2007, 58:149-155.
64. 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.
65. Zoeller R.T., Bansal R., Parris C. Bisphenol-A, an environmental contaminant that acts as a thyroid hormone receptor antagonist in vitro, increases serum thyroxine, and alters RC3/neurogranin expression in the developing rat brain. Endocrinology 2005, 146:607-612.