Adolescent exposure to Bisphenol-A increases anxiety and sucrose preference but impairs spatial memory in rats independent of sex

Brain Research

Volumn 1529, Issue , 2013, Pages 56-65

  Diaz Weinstein, Samantha ^a   Villafane, Joseph J ^a   Juliano, Nicole ^a   Bowman, Rachel E ^a  

^a SACRED HEART UNIVERSITY   (United States)

Author keywords

Adolescence; Anxiety; Bisphenol A; Spatial memory; Sucrose preference

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; SUCROSE; BENZHYDRYL DERIVATIVE; ESTROGEN; PHENOL DERIVATIVE;

ADOLESCENT; ADOLESCENT DEVELOPMENT; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BEHAVIOR CHANGE; BODY WEIGHT; CONTROLLED STUDY; DRUG EXPOSURE; EXPLORATORY BEHAVIOR; FEMALE; FOOD INTAKE; FOOD PREFERENCE; LOCOMOTION; MALE; MAZE TEST; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; RAT; RECOGNITION; SEX DIFFERENCE; SPATIAL MEMORY; TASK PERFORMANCE; WEIGHT GAIN; ANALYSIS OF VARIANCE; ANIMAL; CHEMICALLY INDUCED; DECISION MAKING; DEPTH PERCEPTION; DRUG EFFECTS; MEMORY DISORDER; REACTION TIME; SEXUAL DEVELOPMENT; SPRAGUE DAWLEY RAT; TOXICITY;

ANIMALIA; RATTUS;

ANALYSIS OF VARIANCE; ANIMALS; ANXIETY; BENZHYDRYL COMPOUNDS; CHOICE BEHAVIOR; ESTROGENS, NON-STEROIDAL; EXPLORATORY BEHAVIOR; FEMALE; FOOD PREFERENCES; MALE; MAZE LEARNING; MEMORY DISORDERS; PHENOLS; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; SEX CHARACTERISTICS; SPACE PERCEPTION; SUCROSE;

EID: 84882602522     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.07.018     Document Type: Article

References (74)

1. E.I. Ahmed, J.L. Zehr, K.M. Schulz, B.H. Lorenz, L.L. DonCarlos, and C.L. Sisk Pubertal hormones modulate the addition of new cells to sexually Nat Neurosci. 11 2008 995 997
2. A.M. Aloisi, D. Della Seta, I. Ceccarelli, and F. Farabollini Bisphenol-A differently affects estrogen receptors-alpha in estrous-cycling and lactating female rats Neurosci. Lett. 310 2001 49 52
3. 2+ signals in pancreatic alpha-cells through a nonclassical membrane estrogen receptor within intact islets of langerhans Environ. Health Perspect. 113 8 2005 969 977
4. P.M. Alonso-Magdalena The estrogenic effect of bisphenol A disrupts pancreatic beta-cell function in vivo and induces insulin resistance Environ. Health Perspect. 114 2006 106 112
5. P. Alonso-Magdalena, A.B. Ropero, M.P. Carrera, C.R. Cederroth, M. Baquié, B.R. Gauthier, S. Nef, E. Stefani, and A. Nadal Pancreatic insulin content regulation by the estrogen receptor ER alpha PLoS One 3 4 2008 e2069
6. N.A. Andreollo, E.F. dos Santos, M.R. Araujo, and L.R. Lopes Rat's age versus human's age: what is the relationship? ABCD, Arq. Bras. Cir. Dig. 25 1 2012 49 51
7. S. Biedermann, P. Tschudin, and K. Grob Transfer of bisphenol A from thermal printer paper to the skin Anal. Bioanal. Chem. 398 2010 571 576
8. J.M. Braun, A.E. Kalkbrenner, A.M. Calafat, J.T. Bernert, X. Ye, M.J. Silva, D.B. Barr, S. Sathyanarayana, and B.P. Lanphear Variability and predictors of urinary bisphenol A concentrations during pregnancy Environ Health Perspect. 119 1 2011 131 137
9. A.M. Calafat, Z. Kuklenyik, J.A. Reidy, S.P. Caudill, J. Ekong, and L.L. Needham Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population Environ. Health Perspect. 113 2005 391 395
10. C. Chotiwat, and R.B.S. Harris Increased anxiety-like behavior during the post-stress period in mice exposed to repeated restraint stress Horm. Behav. 50 2006 489 495
11. T. Eilam-Stock, P. Serrano, M. Frankfurt, and V. Luine Bisphenol-A impairs memory and reduces dendritic spine density in adult male rats Behav. Neurosci. 126 1 2012 175 185
12. S.A. Ferguson, and E.P. Gray Aging effects on elevated plus maze behavior in spontaneously hypertensive, Wistar-Kyoto and Sprague-Dawley male and female rats Physiol. Behav. 85 2005 621 628
13. F. Farabollini, S. Porrini, and F. Dessi-Fulgheri Perinatal exposure to the estrogneic pollutant bisphenol a affects behavior in male and female rats Physiol. Behav. 64 1999 687 694
14. T. Fujimoto, K. Kubo, and S. Aou Prenatal exposure to bisphenol A impairs sexual differentiation of exploratory behvior and increases depression-like behavior in rats Brain Res. 1068 2006 49 55
15. T. Geens, L. Goeyens, and A. Covaci Are potential sources for human exposure to bisphenol-A overlooked? Int. J. Hyg. Environ. Health 215 5 2011 339 347
16. J.N. Giedd, J. Blumenthal, N.O. Jeffries, F.X. Castellanos, H. Liu, A. Zijdenbos, T. Paus, A.C. Evans, and J.L. Rapoport Brain development during childhood and adolescence: a longitudinal MRI study Nat. Neurosci. 2 10 1999 861 863
17. C.R. GonÒalves, R.W. Cunha, D.M. Barros, and P.E. Martine Effects of prenatal and postnaal exposure to a low dose of bisphenol A on behavior and memory in rats Environ. Toxicol. Pharmacol. 30 195-201 2010
18. T. Hajszan, and C. Leranth Bisphenol A interferes with synaptic remodeling Neuroendocrinology 31 4 2010 519 530
19. T. Hanaoka, N. Kawamura, K. Hara, and S. Tsugane Urinary bisphenol A and plasma hormone concentrations in male workers exposed to bisphenol A diglycidyl ether and mixed organic solvents Occup Environ Med. 59 2 2002 625 628
20. D.B. Hier, and W.F. Crowley Jr. Spatial ability in androgen-deficient men N. Engl. J. Med. 306 20 1982 1202 1205
21. K.L. Howdeshell, A.K. Hotchkiss, K.A. Thayer, J.G. Vandenbergh, and F.S. vom Saal Exposure to bisphenol A advances puberty Nature 401 6755 1999 63 64
22. M. Ishido, Y. Masuo, M. Kunimoto, S. Oka, and M. Morita Bisphenol A causes hyperactivity in the rat concomitantly with impairment of tyrosine hydroxylase immunoreactivity J. Neurosci. Res. 76 2004 423 433
23. A.L. Johnston, and S.E. File Sex differences in animal tests of anxiety Physiol. Behav. 49 1990 245 250
24. C.K. Jolly Detection of the anti-androgenic effect of endocrine disrupting environmental contaminants using in vivo and in vitro assays in the three-spined stickleback Aquat. Toxicol. 92 4 2009 228 239
25. M. Kiguchi, S. Fujita, H. Oki, N. Shimizu, A.R. Cools, and N. Koshikawa Behavioral characterisation of rats exposed neonatally to bisphenol-A: responses to a novel environmen and to methylphenidate challenge in a putative model of attention-deficit hyperactivity disorder J. Neural Transm. 115 2008 079 1085
26. K. Kubo, O. Arai, M. Omura, R. Watanabe, and R. Ogata Low dose effects of bisphenol A on sexual differentiation of the brain and behavior in rats Neurosci. Res. 45 2003 345 356
27. K. Kubo, O. Arai, R. Ogata, M. Omura, T. Hori, and S. Aou 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. 304 1-2 2001 73 76
28. J.C. Kwekel, V.G. Desai, C.L. Moland, W.S. Branham, and J.C. Fuscoe Age and sex dependent changes in liver gene expression during the life cycle of the rat BMC Genomics 11 2010 675
29. R.K. Lenroot, and J.N. Giedd Brain development in children and adolescents: insights from anatomical magnetic resonance imaging Neurosci. Biobehav. Rev. 30 6 2006 718 729
30. C. Leranth, T. Hajszan, K. Szigeti-Buck, J. Bober, and N.J. MacLusky Bisphenol A prevents the synaptogenic response to estradiol in hippocampus and prefrontal cortex of ovariectomized nonhuman primates PNAS 105 37 2008 13697 13698
31. C. Leranth, K. Klara Szigeti-Buck, N.J. MacLusky, and T. Hajszan Bisphenol A prevents the synaptogenic response to testosterone in the brain of adult male rat Endocrinology 149 3 2008 988 994
32. G.C. Loney, A.M. Torregrossa, J.C. Smith, A. Sclafani, and L.A. Eckel Rats display a robust bimodal preference profile for sucralose Chem. Senses 36 8 2011 733 745
33. N.H. MacLusky, T. Hajszan, and C. Leranth The environmental estrogen Bisphenol A inhibits estradiol-induced hippocampal synaptogenesis Environ. Health Perspect. 113 6 2005 675 679
34. H. Masuno, T. Kidani, K. Sekiya, K. Sakayama, T. Shiosaka, H. Yamamoto, and K. Honda Bisphenol A in combination with insulin can accelerate the conversion of 3T3-L1 fibroblasts to adipocytes J. Lipid Res. 43 5 2002 676 684
35. H. Masuno, J. Iwanami, T. Kidani, K. Sakayama, and K. Honda Bisphenol a accelerates terminal differentiation of 3T3-L1 cells into adipocytes through the phosphatidylinositol 3-kinase pathway Toxicol Sci. 84 2 2005 319 327
36. Y. Masuo, and M. Ishido Neurotoxicity of endocrine disruptors: possible involvement in brain development and neurodegeneration J. Toxicol. Environ. Health B Crit. Rev. 14 5-7 2011 346 369
37. M.J. Millan The neurobiology and control of anxious states Prog. Neurobiol. 70 2003 83 244
38. J. Miyawaki, K. Sakayama, H. Kato, H. Yamamoto, and H. Masuno Perinatal and postnatal exposure to bisphenol A increases adipose tissue mass and serum cholesterol level in mice J. Atheroscler. Thromb. 14 5 2007 245 252
39. S.C. Mueller, V. Temple, E. Oh, C. VanRyzin, A. Williams, B. Cornwell, C. Grillon, D.S. Pine, M. Ernst, and D.P. Merke Early androgen exposure modulates spatial cognition in congenital adrenal hyperplasia (CAH) Psychoneuroendocrinology 33 7 2008 973 980
40. T. Negishi, K. Kawasaki, A. Takatori, Y. Ishii, S. Kyuwa, Y. Kuroda, and Y. Yoshikawa Effects of perinatal exposure to bisphenol A on the behavior of offspring in F344 rats Environ.Toxicol. Pharmacol. 14 2003 99 108
41. Y. Nikaido, K. Yoshizawa, N. Danbara, M. Tsujita-Kyutoku, T. Yuri, N. Uehara, and A. Tsubura Effects of maternal xenoestrogen exposure on development of the reproductive tract and mammary gland in female CD-1 mouse offspring Reprod. Toxicol. 18 6 2004 803 811
42. J.L. Nunez, D.M. Lauschke, and J.M. Juraska Cell death in the development of the posterior cortex in male and female rats J. Comp. Neurol. 436 2001 32 41
43. J.L. Nunez, J. Sodhi, and J.M. Juraska Ovarian hormones after postnatal day 20 reduce neuron number in the rat primary visual cortex J. Neurobiol. 52 4 2002 312 321
44. H.B. Patisaul, and H.L. Bateman Neonatal exposure to endocrine active compounds or an ERbeta agonist increases adult anxiety and aggression in gonadally intact male rats Horm. Behav. 53 4 2008 580 588
45. H.B. Patisaul, A.E. Fortino, and E.K. Polston Differential disruption of nuclear volume and neuronal phenotype in the preoptic area by neonatal exposure to genistein and bisphenol-A Neurotoxicology 28 1 2006 1 12
46. P. Phrakonkham, S. Viengchareun, C. Belloir, M. Lombès, Y. Artur, and M.C. Canivenc-Lavier Dietary xenoestrogens differentially impair 3T3-L1 preadipocyte differentiation and persistently affect leptin synthesis J. Steroid Biochem. Mol. Biol. 110 1-2 2008 95 103
47. L.A. Poherecky, A. Sweeny, and P. Buckendahl Differential sensitivity to amphetamine's effect on open field behavior of psychosocially stressed male rats Psychopharmacology 218 1 2011 281 292
48. A. Poimenova, E. Markaki, C. Rahiotis, and E. Kitraki Corticosterone-regulated actions in the rat brain are affected by perinatal exposure to low dose of bisphenol A Neuroscience 167 3 2010 741 749
49. R. Quinn Comparing rat's to human's age: how old is my rat in people years? Nutrition 21 6 2005 775 777
50. A.B. Ropero, P. Alonso-Magdalena, E. Garcia-Garcia, C. Ripoll, E. Fuentes, and A. Nadal Bisphenol-A disruption of the endocrine pancreas and blood glucose homeostasis Int. J. Androl. 31 2 2008 194 200
51. B. Rubin Bisphenol A: an endocrine disruptor with widespread exposure and mutiple effects J. Steroid Biochem. Mol. Biol. 127 2011 27 34
52. B.S. Rubin, and A.M. Soto Bisphenol A: perinatal exposure and body weight Mol. Cell. Endocrinol. 304 2009 55 62
53. B.S. Rubin, J.R. Lenkowski, C.M. Schaeberle, L.N. Vandenberg, P.M. Ronsheim, and S.M. Soto Evidence of altered brain sexual differentiation in mice exposed to perinatally low environmentally relevant levels of bisphenol A Endocrinology 147 8 2006 3681 3691
54. B.S. Rubin, M.K. Murray, D.A. Damassa, J.C. King, and A.M. Soto Perinatal exposure to low doses of Bisphenol-A affect body weight, etrous cyclicity, and plasma LH levels Environ. Health Perspect. 109 2001 675 680
55. K. Sakurai, M. Kawazuma, T. Adachi, T. Harigaya, Y. Saito, N. Hashimoto, and C. Mori Bisphenol A affects glucose transport in mouse 3T3-F442A adipocytes Br. J. Pharmacol. 141 2 2004 209 214
56. K. Satoh, K. Ohyama, N. Aoki, M. Iida, and F. Nagai Study on anti-androgenic effects of bisphenol A diglycidyl ether (BADGE), bisphenol F diglycidyl ether (BFDGE) and their derivatives using cells stably transfected with human androgen receptor, AR-Ecoscreen Food Chem. Toxicol. 42 2004 983 993
57. A. Sclafani, and S. Mann Carbohydrate taste preferences in rats: glucose, sucrose, maltose, fructose and polycose compared Physiol. Behav. 40 5 1987 563 568
58. P. Sohoni, and J.P. Sumpter Several environmental oestrogens are also anti-androgens J. Endocrinol. 158 3 1998 327 339
59. R.W. Stahlhut, W.V. Welsons, and S.H. Swan Bisphenol A data in NHANES suggest longer than expected half-life, substantial nonfood exposure, or both Environ. Health Perspect. 117 2009 784 789
60. C.E. Talsness, A.J. Andrade, S.N. Kuriyama, J.A. Taylor, and F.S. vom Saal Components of plastic: experimental studies in animals and relevance for human health Philos. Trans. R. Soc. B 364 2009 2079 2096
61. J.A. Taylor, W.V. Welshons, and F.S. vom Saal No effect of route of exposure (oral; subcutaneous injection) on plasma Bisphenol A throughout 24 h after administration in neonatal female mice Reprod. Toxicol. 25 2 2008 169 176
62. Y.H. Tian, J.H. Baek, S.Y. Lee, and C.G. Jang Prenatal and postnatal exposure to Bisphenol A induces anxiolytic behaviors and cognitive deficits in mice Synapse 64 6 2010 432 439
63. U.S.E.P.A. Bisphenol A, CASRN 80-05-7. Integrated Risk Information System 1993 U.S. Environmental Protection Agency Washington, DC http://www.epa.gov/ iris/subst/0356.htm
64. E.S. Valenstein, J.W. Kakolewski, and V.E. Cox Sex differences in taste preference for glucose and saccharin solutions Science 56 3777 1967 942 943
65. L.N. Vandenberg, R. Hauser, M. Marcus, N. Olea, and W.V. Welsons Human exposure to bisphenol A (BPA) Reprod. Toxicol. 24 2007 139 177
66. L.N. Vandenberg, I. Chahoud, J.J. Heindel, V. Padmanabhan, F.J. Paumgartten, and G. Schoenfelder Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A Environ Health Perspect 118 8 2010 1055 1070
67. F.S. vom Saal, and C. Hughes An extensive new literature concerning low-dose effects of bisphenol A shows the need for a new risk assessment. Environ. Health Perspect. 113 8 2005 926 933
68. K. Wada, H. Sakamoto, K. Nishikawa, S. Sakuma, A. Nakajima, Y. Fujimoto, and Y. Kamisaki Life style-related diseases of the digestive system: endocrine disruptors stimulate lipid accumulation in target cells related to metabolic syndrome J. Pharmacol. Sci. 105 2 2007 133 137
69. X. Xiang, W. Huang, C.N. Haile, and T.A. Kosten Hippocampal GluR1 associates with behavior in the elevated plus maze and shows sex differences Behav. Brain Res. 222 2 2011 326 331
70. X.H. Xu, J. Zhang, Y.M. Wang, Y.P. Ye, and Q.Q. Luo Perinatal exposrue to bisphenol-A impairs learning-memory by concomitant down-regulation of N-methyl-d-aspartate receptors of hippocampus in male offspring mice Horm. Behav. 58 2 2010 326 333
71. X. Xu, L. Tan, T. Himi, M. Sadamatsu, S. Tsutsumi, M. Akaike, and N. Kato Changed preference for sweet taste in adulthood induced by perinatal exposure to bisphenol A - a probable link to overweight and obesity Neurotoxicol. Teratol. 33 2011 458 463
72. X. Xu, D. Tian, X. Hong, L. Chen, and L. Xie Sex-specific influence of exposure to bisphenol-A between adolescene and young adulthood on mouse behaviors Neuropharmacology 61 2011 565 (373)
73. X. Xu, X. Hong, L. Xie, Y. Yang, Q. Zhang, G. Zhang, and X. Liu Gestational and lactational exposure to bisphenol-A affects anxiety- and depression-like behaviors in mice Horm. Behav. 62 4 2012 480 490
74. D. Zalko, C. Jacques, H. Duplan, S. Breuls, and E. Perdu Viable skin efficiently absorbs and metabolizes bisphenol A Chemosphere 82 3 2011 424 430