Developmental treatment with bisphenol A causes few alterations on measures of postweaning activity and learning

Neurotoxicology and Teratology

Volumn 34, Issue 6, 2012, Pages 598-606

  Ferguson, Sherry A ^a   Law, C Delbert ^a   Abshire, Jordan S ^a  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

Author keywords

Bisphenol A; Learning; Locomotor activity; Motor coordination; Novelty preference; Startle

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ETHINYLESTRADIOL;

ACOUSTIC REFLEX; ANIMAL HOUSING; ARTICLE; BIRTH; BREEDING; CONTROLLED STUDY; FEMALE; GESTATIONAL AGE; LATENT PERIOD; LEARNING; LOCOMOTION; MALE; MAZE TEST; MOTOR COORDINATION; NEUROTOXICOLOGY; NONHUMAN; OPEN FIELD BEHAVIOR; PERINATAL PERIOD; PRIORITY JOURNAL; PROGENY; RAT; STARTLE REFLEX; WEANING;

ACOUSTIC STIMULATION; ANIMALS; BEHAVIOR, ANIMAL; BENZHYDRYL COMPOUNDS; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTROGENS, NON-STEROIDAL; ETHINYL ESTRADIOL; FEMALE; MALE; MAZE LEARNING; MOTOR ACTIVITY; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; STARTLE REACTION; WEANING;

RATTUS;

EID: 84868239064     PISSN: 08920362     EISSN: 18729738     Source Type: Journal    
DOI: 10.1016/j.ntt.2012.09.006     Document Type: Article

References (64)

1. 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.
2. Ashby J., Lefevre P.A. The weanling male rat as an assay for endocrine disruption: preliminary observations. Regul Toxicol Pharmacol 1997, 26:330-337.
3. Bardo M.T., Neisewander J.L., Pierce R.C. Novelty-induced place preference behavior in rats: effects of opiate and dopaminergic drugs. Pharmacol Biochem Behav 1989, 32:683-689.
4. Beronius A., Ruden C., Hakansson H., Hanberg A. Risk to all or none? A comparative analysis of controversies in the health risk assessment of bisphenol A. Reprod Toxicol 2010, 29:132-146.
5. Boctor S.Y., Ferguson S.A. Neonatal NMDA receptor antagonist treatments have no effects on prepulse inhibition of postnatal day 25 Sprague-Dawley rats. Neurotoxicology 2009, 30:151-154.
6. Boctor S.Y., Ferguson S.A. Altered adult locomotor activity in rats from phencyclidine treatment on postnatal days 7, 9 and 11, but not repeated ketamine treatment on postnatal day 7. Neurotoxicology 2010, 31:42-54.
7. Bushnik T., Haines D., Levallois P., Levesque J., Van Oostdam J., Viau C. Lead and bisphenol A concentrations in the Canadian population. Health Rep 2010, 21:7-18.
8. Buynitsky T., Mostofsky D.I. Restraint stress in biobehavioral research: recent developments. Neurosci Biobehav Rev 2009, 33:1089-1098.
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. Carr R., Bertasi F., Betancourt A., Bowers S., Gandy B.S., Ryan P., et al. Effect of neonatal rat bisphenol a exposure on performance in the Morris water maze. J Toxicol Environ Health A 2003, 66:2077-2088.
11. Delclos K.B., Weis C.C., Bucci T.J., Olson G., Mellick P., Sadovova N., et al. Overlapping but distinct effects of genistein and ethinyl estradiol (EE(2)) in female Sprague-Dawley rats in multigenerational reproductive and chronic toxicity studies. Reprod Toxicol 2009, 27:117-132.
12. Doerge D.R., Twaddle N.C., Vanlandingham M., Fisher J.W. Pharmacokinetics of bisphenol A in neonatal and adult Sprague-Dawley rats. Toxicol Appl Pharmacol 2010, 247:158-165.
13. 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.
14. Dugard M.L., Tremblay-Leveau H., Mellier D., Caston J. Prenatal exposure to ethinylestradiol elicits behavioral abnormalities in the rat. Brain Res Dev Brain Res 2001, 129:189-199.
15. EFSA (European Food Safety Authority) Opinion of the scientific panel on food additives, flavourings, processing aids and materials in contact with food on a request from the commission related to 2,2-bis(4-hydroxyphenyl)propane. The EFSA Journal 2006, 428:1-75.
16. 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.
17. Environmental Protection Agency Guidelines for neurotoxicity risk assessment. Federal register 1998, 26926-26954.
18. Ferguson S.A., Berry K.J. Oral accutane (13-cis-retinoic acid) has no effects on spatial learning and memory in male and female Sprague-Dawley rats. Neurotoxicol Teratol 2007, 29:219-227.
19. Ferguson S.A., Boctor S.Y. Cocaine responsiveness or anhedonia in rats treated with methylphenidate during adolescence. Neurotoxicol Teratol 2010, 32:432-442.
20. Ferguson S.A., Delclos K.B., Newbold R.R., Flynn K.M. Dietary ethinyl estradiol exposure during development causes increased voluntary sodium intake and mild maternal and offspring toxicity in rats. Neurotoxicol Teratol 2003, 25:491-501.
21. 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.
22. Ferguson S.A., Law C.D., Smith M.E. Developmental ethinyl estradiol, but not bisphenol A, treatment increases juvenile play behavior of Sprague-Dawley rats 2011, 392. Society for Neuroscience, Washington, D.C., [03/VV62].
23. Ferguson SA, Law CD, Abshire JS. Few effects of developmental Bisphenol A treatment on the sexually dimorphic behaviors of male and female Sprague-Dawley rats. Unpublished data.
24. Food and Agriculture Organization of the United Nations, World Health Organization Joint FAO/WHO expert meeting to review toxicological and health aspects of bisphenol A: final report, including report of stakeholder meeting on bisphenol A, 1-5 November 2010 2011, WHO Press, Ottawa, Canada. Geneva, Switzerland.
25. 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.
26. 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.
27. Golub M.S., Wu K.L., Kaufman F.L., Li L.H., Moran-Messen F., Zeise L., et al. Bisphenol A: developmental toxicity from early prenatal exposure. Birth Defects Res B Dev Reprod Toxicol 2010, 89:441-466.
28. 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.
29. Goodman J.E., McConnell E.E., Sipes I.G., Witorsch R.J., Slayton T.M., Yu C.J., et al. An updated weight of the evidence evaluation of reproductive and developmental effects of low doses of bisphenol A. Crit Rev Toxicol 2006, 36:387-457.
30. Harrison F.E., Reiserer R.S., Tomarken A.J., McDonald M.P. Spatial and nonspatial escape strategies in the Barnes maze. Learn Mem 2006, 13:809-819.
31. He Z., Paule M.G., Ferguson S.A. Low oral doses of bisphenol A increase volume of the sexually dimorphic nucleus of the preoptic area in male, but not female, rats at postnatal day 21. Neurotoxicol Teratol 2012, 34:331-337.
32. Hiroi H., Tsutsumi O., Momoeda M., Takai Y., Osuga Y., Taketani Y. Differential interactions of bisphenol A and 17beta-estradiol with estrogen receptor alpha (ERalpha) and ERbeta. Endocr J 1999, 46:773-778.
33. Hunt P.A., Susiarjo M., Rubio C., Hassold T.J. The bisphenol A experience: a primer for the analysis of environmental effects on mammalian reproduction. Biol Reprod 2009, 81:807-813.
34. Kang J.H., Kondo F., Katayama Y. Human exposure to bisphenol A. Toxicology 2006, 226:79-89.
35. Lakind J.S., Naiman D.Q. Bisphenol A (BPA) daily intakes in the United States: estimates from the 2003-2004 NHANES urinary BPA data. J Expo Sci Environ Epidemiol 2008, 18:608-615.
36. Latendresse J.R., Bucci T.J., Olson G., Mellick P., Weis C.C., Thorn B., et al. Genistein and ethinyl estradiol dietary exposure in multigenerational and chronic studies induce similar proliferative lesions in mammary gland of male Sprague-Dawley rats. Reprod Toxicol 2009, 28:342-353.
37. Lewis E.M., Barnett J.F., Freshwater L., Hoberman A.M., Christian M.S. Sexual maturation data for Crl Sprague-Dawley rats: criteria and confounding factors. Drug Chem Toxicol 2002, 25:437-458.
38. Li A.A., Baum M.J., McIntosh L.J., Day M., Liu F., Gray L.E. Building a scientific framework for studying hormonal effects on behavior and on the development of the sexually dimorphic nervous system. Neurotoxicology 2008, 29:504-519.
39. Littell R.C., Milliken G.A., Stroup W.W., Wolfinger R. SAS system for mixed models 1996, SAS Publishing, Cary, NC.
40. Maccari S., Morley-Fletcher S. Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology 2007, 32(Suppl. 1):S10-S15.
41. McGivern R.F., Henschel D.M. Interaction of naltrexone with postnatal administration of testosterone and estrogen on neurobehavioral sexual differentiation in rats. Horm Behav 1990, 24:20-39.
42. Means L.W., Alexander S.R., O'Neal M.F. Those cheating rats: male and female rats use odor trails in a water-escape "working memory" task. Behav Neural Biol 1992, 58:144-151.
43. Miyagawa K., Narita M., Akama H., Suzuki T. Memory impairment associated with a dysfunction of the hippocampal cholinergic system induced by prenatal and neonatal exposures to bisphenol-A. Neurosci Lett 2007, 418:236-241.
44. 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.
45. National Research Council Guide for the care and use of laboratory animals 1996, National Academy Press, Washington DC.
46. Negishi T., Kawasaki K., Suzaki S., Maeda H., Ishii Y., Kyuwa S., et al. Behavioral alterations in response to fear-provoking stimuli and tranylcypromine induced by perinatal exposure to bisphenol A and nonylphenol in male rats. Environ Health Perspect 2004, 112:1159-1164.
47. OECD Test guideline 426. OECD guideline for the testing of chemicals. Developmental neurotoxicity study 2007.
48. Paris F., Balaguer P., Terouanne B., Servant N., Lacoste C., Cravedi J.P., et al. 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.
49. Peleg-Raibstein D., Yee B.K., Feldon J., Hauser J. The amphetamine sensitization model of schizophrenia: relevance beyond psychotic symptoms?. Psychopharmacology (Berl) 2009, 206:603-621.
50. Pierce R.C., Crawford C.A., Nonneman A.J., Mattingly B.A., Bardo M.T. Effect of forebrain dopamine depletion on novelty-induced place preference behavior in rats. Pharmacol Biochem Behav 1990, 36:321-325.
51. Richter C.A., Birnbaum L.S., Farabollini F., Newbold R.R., Rubin B.S., Talsness C.E., et al. In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol 2007, 24:199-224.
52. Ryan BC. Developmental exposure to environmental extrogens alters adult behavior in female rodents. [Ph.D.]. Raleigh: Dissertation, North Carolina State University; 2005.
53. 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.
54. Seliger D.L. Effects of age, sex, and brightness of field on open-field behaviors of rats. Percept Mot Skills 1977, 45:1059-1067.
55. Slob A.K., Huizer T., Van der Werff ten Bosch J.J. Ontogeny of sex differences in open-field ambulation in the rat. Physiol Behav 1986, 37:313-315.
56. 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.
57. Tominaga T., Negishi T., Hirooka H., Miyachi A., Inoue A., Hayasaka I., et al. Toxicokinetics of bisphenol A in rats, monkeys and chimpanzees by the LC-MS/MS method. Toxicology 2006, 226:208-217.
58. Viberg H., Fredriksson A., Buratovic S., Eriksson P. Dose-dependent behavioral disturbances after a single neonatal bisphenol A dose. Toxicology 2011, 290:187-194.
59. von Goetz N., Wormuth M., Scheringer M., Hungerbuhler K. Bisphenol a: how the most relevant exposure sources contribute to total consumer exposure. Risk Anal 2010, 30:473-487.
60. Weinstock M. Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol 2001, 65:427-451.
61. Wolstenholme J.T., Rissman E.F., Connelly J.J. The role of bisphenol A in shaping the brain, epigenome and behavior. Horm Behav 2011, 59:296-305.
62. Xiao Q., Li Y., Ouyang H., Xu P., Wu D. High-performance liquid chromatographic analysis of bisphenol A and 4-nonylphenol in serum, liver and testis tissues after oral administration to rats and its application to toxicokinetic study. J Chromatogr B Analyt Technol Biomed Life Sci 2006, 830:322-329.
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. Yamasaki K., Sawaki M., Noda S., Muroi T., Takatsuki M. Preputial separation and glans penis changes in normal growing Crj: CD (SD) IGS rats. Reprod Toxicol 2001, 15:533-536.