Sex specific impact of perinatal bisphenol A (BPA) exposure over a range of orally administered doses on rat hypothalamic sexual differentiation

NeuroToxicology

Volumn 36, Issue , 2013, Pages 55-62

  McCaffrey, Katherine A ^a   Jones, Brian ^b   Mabrey, Natalie ^a   Weiss, Bernard ^b   Swan, Shanna H ^c   Patisaul, Heather B ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Dopamine; Endocrine disruption; Estrogen; Hypothalamus; Sexually dimorphic

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; CALBINDIN; ESTRADIOL; TYROSINE 3 MONOOXYGENASE;

ADULT ANIMAL; ADULTHOOD; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOVENTRAL PERIVENTRICULAR NUCLEUS; ARTICLE; CELL COUNT; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEMASCULINIZATION; EMBRYO; FEMALE; HYPOTHALAMUS; LONG EVANS RAT; MALE; MASCULINIZATION; NEUROANATOMY; NONHUMAN; PRENATAL EXPOSURE; PREOPTIC AREA; PRIORITY JOURNAL; PROGENY; RAT; REPRODUCTION; SEX DIFFERENCE; SEX DIFFERENTIATION;

ADMINISTRATION, ORAL; AIR POLLUTANTS, OCCUPATIONAL; ANALYSIS OF VARIANCE; ANIMALS; BENZHYDRYL COMPOUNDS; CALBINDINS; CELL COUNT; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; HYPOTHALAMUS; MALE; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, LONG-EVANS; SEX DIFFERENTIATION; TYROSINE 3-MONOOXYGENASE;

RATTUS;

EID: 84875803097     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2013.03.001     Document Type: Article

References (81)

1. Balcombe J.P., Barnard N.D., Sandusky C. Laboratory routines cause animal stress. Contemp Top Lab Anim Sci Am Assoc Lab Anim Sci 2004, 43:42-51.
2. Becker J.B., Arnold A.P., Berkley K.J., Blaustein J.D., Eckel L.A., Hampson E., et al. Strategies and methods for research on sex differences in brain and behavior. Endocrinology 2005, 146:1650-1673.
3. 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.
4. Bleier R., Byne W., Siggelkow I. Cytoarchitectonic sexual dimorphisms of the medial preoptic and anterior hypothalamic areas in guinea pig, rat, hamster, and mouse. J Comp Neurol 1982, 212:118-130.
5. Bloch G.J., Gorski R.A. Estrogen/progesterone treatment in adulthood affects the size of several components of the medial preoptic area in the male rat. J Comp Neurol 1988, 275:613-622.
6. Bodo C., Kudwa A.E., Rissman E.F. Both estrogen receptor-alpha and -beta are required for sexual differentiation of the anteroventral periventricular area in mice. Endocrinology 2006, 147:415-420.
7. Bonthuis P.J., Cox K.H., Searcy B.T., Kumar P., Tobet S., Rissman E.F. Of mice and rats: key species variations in the sexual differentiation of brain and behavior. Front Neuroendocrinol 2010, 31:341-358.
8. Braun J.M., Kalkbrenner A.E., Calafat A.M., Bernert J.T., Ye X., Silva M.J., et al. Variability and predictors of urinary bisphenol A concentrations during pregnancy. Environ Health Perspect 2011, 119:131-137.
9. Braun J.M., Yolton K., Dietrich K.N., Hornung R., Ye X., Calafat A.M., et al. Prenatal bisphenol A exposure and early childhood behavior. Environ Health Perspect 2009, 117:1945-1952.
10. Cabaton N.J., Wadia P.R., Rubin B.S., Zalko D., Schaeberle C.M., Askenase M.H., et al. Perinatal exposure to environmentally relevant levels of bisphenol A decreases fertility and fecundity in CD-1 mice. Environ Health Perspect 2011, 119:547-552.
11. 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.
12. Cao J., Mickens J.A., McCaffrey K.A., Leyrer S.M., Patisaul H.B. Neonatal bisphenol A exposure alters sexually dimorphic gene expression in the postnatal rat hypothalamus. Neurotoxicology 2012, 33:23-36.
13. Cao J., Patisaul H.B. Sexually dimorphic expression of hypothalamic estrogen receptors alpha and beta and Kiss1 in neonatal male and female rats. J Comp Neurol 2011, 519:2954-2977.
14. Chapin R.E., Adams J., Boekelheide K., Gray L.E., Hayward S.W., Lees P.S., et al. NTP-CERHR expert panel report on the reproductive and developmental toxicity of bisphenol A. Birth defects research part B. Develop Reprod Toxicol 2008, 83:157-395.
15. Davis E.C., Popper P., Gorski R.A. The role of apoptosis in sexual differentiation of the rat sexually dimorphic nucleus of the preoptic area. Brain Res 1996, 734:10-18.
16. Davis E.C., Shryne J.E., Gorski R.A. Structural sexual dimorphisms in the anteroventral periventricular nucleus of the rat hypothalamus are sensitive to gonadal steroids perinatally, but develop peripubertally. Neuroendocrinology 1996, 63:142-148.
17. De Vries G.J. Minireview: sex differences in adult and developing brains: compensation, compensation, compensation. Endocrinology 2004, 145:1063-1068.
18. Doerge D.R., Twaddle N.C., Vanlandingham M., Brown R.P., Fisher J.W. Distribution of bisphenol A into tissues of adult, neonatal, and fetal Sprague-Dawley rats. Toxicol Appl Pharmacol 2011, 255:261-270.
19. 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.
20. Dohler K.D., Coquelin A., Davis F., Hines M., Shryne J.E., Gorski R.A. Differentiation of the sexually dimorphic nucleus in the preoptic area of the rat brain is determined by the perinatal hormone environment. Neurosci Lett 1982, 33:295-298.
21. Dohler K.D., Coquelin A., Davis F., Hines M., Shryne J.E., Gorski R.A. Pre- and postnatal influence of testosterone propionate and diethylstilbestrol on differentiation of the sexually dimorphic nucleus of the preoptic area in male and female rats. Brain Res 1984, 302:291-295.
22. Engel S.M., Levy B., Liu Z., Kaplan D., Wolff M.S. Xenobiotic phenols in early pregnancy amniotic fluid. Reprod Toxicol 2006, 21:110-112.
23. Fader A.J., Hendricson A.W., Dohanich G.P. Estrogen improves performance of reinforced T-maze alternation and prevents the amnestic effects of scopolamine administered systemically or intrahippocampally. Neurobiol Learn Mem 1998, 69:225-240.
24. FAO/WHO Toxicological and health aspects of bisphenol A: report of joint FAO/WHO expert meeting and report of stakeholder meeting on bisphenol A 2011, World Health Organization.
25. 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 Off J Soc Toxicol 2011, 124:149-160.
26. Ford M.M., Eldridge J.C., Samson H.H. Determination of an estradiol dose-response relationship in the modulation of ethanol intake. Alcohol Clin Exp Res 2004, 28:20-28.
27. Geens T., Aerts D., Berthot C., Bourguignon J.P., Goeyens L., Lecomte P., et al. A review of dietary and non-dietary exposure to bisphenol-A. Food Chem Toxicol 2012, 50:3725-3740.
28. Gerall A.A., Dunlap J.L., Sonntag W.E. Reproduction in aging normal and neonatally androgenized female rats. J Comp Physiol Psychol 1980, 94:556-563.
29. Gilmore R.F., Varnum M.M., Forger N.G. Effects of blocking developmental cell death on sexually dimorphic calbindin cell groups in the preoptic area and bed nucleus of the stria terminalis. Biol Sex Differ 2012, 3:5.
30. Glaser J.R., Glaser E.M. Stereology, morphometry, and mapping: the whole is greater than the sum of its parts. J Chem Neuroanat 2000, 20:115-126.
31. 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. Critic Rev Toxicol 2006, 36:387-457.
32. Gorski R.A., Gordon J.H., Shryne J.E., Southam A.M. Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Brain Res 1978, 143:333-346.
33. Gorski R.A., Harlan R.E., Jacobson C.D., Shryne J.E., Southam A.M. Evidence for the existence of a sexually dimorphic nucleus in the preoptic area of the rat. J Comp Neurol 1980, 193:529-539.
34. Grumbach M.M. The neuroendocrinology of human puberty revisited. Horm Res 2002, 57:2-14.
35. Haseman J.K., Bailer A.J., Kodell R.L., Morris R., Portier K. Statistical issues in the analysis of low-dose endocrine disruptor data. Toxicol Sci 2001, 61:201-210.
36. 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.
37. Hengstler J.G., Foth H., Gebel T., Kramer P.J., Lilienblum W., Schweinfurth H., et al. Critical evaluation of key evidence on the human health hazards of exposure to bisphenol A. Critic Rev Toxicol 2011, 41:263-291.
38. Hoffman G.E., Le W.W. Just cool it! Cryoprotectant anti-freeze in immunocytochemistry and in situ hybridization. Peptides 2004, 25:425-431.
39. 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.
40. Ikezuki Y., Tsutsumi O., Takai Y., Kamei Y., Taketani Y. Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Human Reprod 2002, 17:2839-2841.
41. Jones B.A., Shimell J.J., Watson N.V. Pre- and postnatal bisphenol A treatment results in persistent deficits in the sexual behavior of male rats, but not female rats, in adulthood. Horm Behav 2010.
42. Kwon S., Stedman D.B., Elswick B.A., Cattley R.C., Welsch F. Pubertal development and reproductive functions of Crl:CD BR Sprague-Dawley rats exposed to bisphenol A during prenatal and postnatal development. Toxicol Sci Off J Soc Toxicol 2000, 55:399-406.
43. Laws S.C., Carey S.A., Ferrell J.M., Bodman G.J., Cooper R.L. Estrogenic activity of octylphenol, nonylphenol, bisphenol A and methoxychlor in rats. Toxicol Sci 2000, 54:154-167.
44. Long X., Steinmetz R., Ben-Jonathan N., Caperell-Grant A., Young P.C., Nephew K.P., et al. Strain differences in vaginal responses to the xenoestrogen bisphenol A. Environ Health Perspect 2000, 108:243-247.
45. McCarthy M.M., Wright C.L., Schwarz J.M. New tricks by an old dogma: mechanisms of the organizational/activational hypothesis of steroid-mediated sexual differentiation of brain and behavior. Horm Behav 2009, 55:655-665.
46. Murakami S., Arai Y. Neuronal death in the developing sexually dimorphic periventricular nucleus of the preoptic area in the female rat: effect of neonatal androgen treatment. Neurosci Lett 1989, 102:185-190.
47. Nagao T., Saito Y., Usumi K., Kuwagata M., Imai K. Reproductive function in rats exposed neonatally to bisphenol A and estradiol benzoate. Reprod Toxicol 1999, 13:303-311.
48. Nahar M.S., Liao C., Kannan K., Dolinoy D.C. Fetal liver bisphenol A concentrations and biotransformation gene expression reveal variable exposure and altered capacity for metabolism in humans. J Biochem Mol Toxicol 2012, 27(2):116-123.
49. NTP. Carcinogenesis Bioassay of Bisphenol A (CAS No. 80-05-7) in F344 Rats and B6C3F1 Mice (Feed Study). Natl Toxicol Program Tech Rep Ser. 1982; 215:1-116.
50. 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.
51. Patchev A.V., Gotz F., Rohde W. Differential role of estrogen receptor isoforms in sex-specific brain organization. FASEB J 2004, 18:1568-1570.
52. Patisaul H.B., Fortino A.E., Polston E.K. Neonatal genistein or bisphenol-A exposure alters sexual differentiation of the AVPV. Neurotoxicol Teratol 2006, 28:111-118.
53. Patisaul H.B., Fortino A.E., Polston E.K. Differential disruption of nuclear volume and neuronal phenotype in the preoptic area by neonatal exposure to genistein and bisphenol-A. Neurotoxicology 2007, 28:1-12.
54. Patisaul H.B., Roberts S.C., Mabrey N., McCaffrey K.A., Gear R.B., Braun J., et al. Accumulation and endocrine disrupting effects of the flame retardant mixture firemaster((R)) 550 in rats: an exploratory assessment. J Biochem Mol Toxicol 2013, 27:124-136.
55. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2007, Academic Press, London. 6th ed.
56. Rhees R.W., Al-Saleh H.N., Kinghorn E.W., Fleming D.E., Lephart E.D. Relationship between sexual behavior and sexually dimorphic structures in the anterior hypothalamus in control and prenatally stressed male rats. Brain Res Bull 1999, 50:193-199.
57. Rhees R.W., Shryne J.E., Gorski R.A. Onset of the hormone-sensitive perinatal period for sexual differentiation of the sexually dimorphic nucleus of the preoptic area in female rats. J Neurobiol 1990, 21:781-786.
58. Rhees R.W., Shryne J.E., Gorski R.A. Termination of the hormone-sensitive period for differentiation of the sexually dimorphic nucleus of the preoptic area in male and female rats. Brain Res Dev Brain Res 1990, 52:17-23.
59. 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.
60. Roselli C.E., Larkin K., Resko J.A., Stellflug J.N., Stormshak F. The volume of a sexually dimorphic nucleus in the ovine medial preoptic area/anterior hypothalamus varies with sexual partner preference. Endocrinology 2004, 145:478-483.
61. 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.
62. Sathyanarayana S., Braun J.M., Yolton K., Liddy S., Lanphear B.P. Case report: high prenatal bisphenol a exposure and infant neonatal neurobehavior. Environ health Perspect 2011, 119:1170-1175.
63. Schmitz C., Hof P.R. Design-based stereology in neuroscience. Neuroscience 2005, 130:813-831.
64. Sickel M.J., McCarthy M.M. Calbindin-D28K immunoreactivity is a marker for a subdivision of the sexually dimorphic nucleus of the preoptic area of the rat: developmental profile and gonadal steroid modulation. J Neuroendocrinol 2000, 12:397-402.
65. Simerly R.B. Hormonal control of the development and regulation of tyrosine hydroxylase expression within a sexually dimorphic population of dopaminergic cells in the hypothalamus. Brain Res Mol Brain Res 1989, 6:297-310.
66. Simerly R.B. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Ann Rev Neurosci 2002, 25:507-536.
67. Simerly R.B., Swanson L.W., Gorski R.A. The distribution of monoaminergic cells and fibers in a periventricular preoptic nucleus involved in the control of gonadotropin release: immunohistochemical evidence for a dopaminergic sexual dimorphism. Brain Res 1985, 330:55-64.
68. Simerly R.B., Swanson L.W., Handa R.J., Gorski R.A. Influence of perinatal androgen on the sexually dimorphic distribution of tyrosine hydroxylase-immunoreactive cells and fibers in the anteroventral periventricular nucleus of the rat. Neuroendocrinology 1985, 40:501-510.
69. Steinmetz R., Mitchner N.A., Grant A., Allen D.L., Bigsby R.M., Ben-Jonathan N. The xenoestrogen bisphenol A induces growth, differentiation, and c-fos gene expression in the female reproductive tract. Endocrinology 1998, 139:2741-2747.
70. Takagi H., Shibutani M., Masutomi N., Uneyama C., Takahashi N., Mitsumori K., et al. Lack of maternal dietary exposure effects of bisphenol A and nonylphenol during the critical period for brain sexual differentiation on the reproductive/endocrine systems in later life. Arch Toxicol 2004, 78:97-105.
71. Tarttelin M.F., Gorski R.A. Postnatal influence of diethylstilbestrol on the differentiation of the sexually dimorphic nucleus in the rat is as effective as perinatal treatment. Brain Res 1988, 456:271-274.
72. Taylor J.A., Vom Saal F.S., Welshons W.V., Drury B., Rottinghaus G., Hunt P.A., et al. Similarity of bisphenol A pharmacokinetics in Rhesus monkeys and mice: relevance for human exposure. Environ Health Perspect 2012, 119(4):422-430.
73. Teeguarden J.G., Calafat A.M., Ye X., Doerge D.R., Churchwell M.I., Gunawan R., et al. Twenty-four hour human urine and serum profiles of bisphenol a during high-dietary exposure. Toxicol Sci 2011, 123:48-57.
74. Twaddle N.C., Churchwell M.I., Vanlandingham M., Doerge D.R. Quantification of deuterated bisphenol A in serum, tissues, and excreta from adult Sprague-Dawley rats using liquid chromatography with tandem mass spectrometry. Rapid Commun Mass Spectrom 2010, 24:3011-3020.
75. 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.
76. Wallen K. Hormonal influences on sexually differentiated behavior in nonhuman primates. Front Neuroendocrinol 2005, 26:7-26.
77. Wiegand S.J., Terasawa E. Discrete lesions reveal functional heterogeneity of suprachiasmatic structures in regulation of gonadotropin secretion in the female rat. Neuroendocrinology 1982, 34:395-404.
78. 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.
79. Wright C.L., Schwarz J.S., Dean S.L., McCarthy M.M. Cellular mechanisms of estradiol-mediated sexual differentiation of the brain. Trends Endocrinol Metab 2010, 21:553-561.
80. Yang S.L., Chen Y.Y., Hsieh Y.L., Jin S.H., Hsu H.K., Hsu C. Perinatal androgenization prevents age-related neuron loss in the sexually dimorphic nucleus of the preoptic area in female rats. Develop Neurosci 2004, 26:54-60.
81. Yeo M., Berglund K., Hanna M., Guo J.U., Kittur J., Torres M.D., et al. Bisphenol A delays the perinatal chloride shift in cortical neurons by epigenetic effects on the Kcc2 promoter. Proc Natl Acad Sci U S A 2013, 110(11):4315-4320.