Epigenetic perspective on the developmental effects of bisphenol A

Brain, Behavior, and Immunity

Volumn 25, Issue 6, 2011, Pages 1084-1093

  Kundakovic, Marija ^a   Champagne, Frances A ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Behavior; Bisphenol A; Brain development; DNA methylation; Endocrine disruptor; Epigenome; Estrogen receptor; Gene expression; Immune; Transgenerational

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL;

ANXIETY; BEHAVIOR; BRAIN; BRAIN DEVELOPMENT; DEVELOPMENTAL STAGE; DISEASE PREDISPOSITION; EMBRYO DEVELOPMENT; ENVIRONMENTAL EXPOSURE; EPIGENETICS; FETUS DEVELOPMENT; HEALTH HAZARD; HUMAN; IMMUNE SYSTEM; LEARNING; MATERNAL BEHAVIOR; MEMORY; MOLECULAR MECHANICS; NEUROENDOCRINE SYSTEM; NONHUMAN; NOTE; PERINATAL PERIOD; PRENATAL EXPOSURE; PRIORITY JOURNAL; SEX DIFFERENCE;

ANIMALS; BRAIN; CHILD; CHILD BEHAVIOR DISORDERS; DEVELOPMENTAL DISABILITIES; DISORDERS OF SEX DEVELOPMENT; ENDOCRINE DISRUPTORS; ENVIRONMENTAL EXPOSURE; EPIGENESIS, GENETIC; ESTROGENS, NON-STEROIDAL; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IMMUNE SYSTEM; IMMUNOLOGIC DEFICIENCY SYNDROMES; MENTAL DISORDERS; PHENOLS; PHENOTYPE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SIGNAL TRANSDUCTION;

EID: 79960223622     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2011.02.005     Document Type: Note

References (94)

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. Alizadeh M., Ota F., Hosoi K., Kato M., Sakai T., Satter M.A. Altered allergic cytokine and antibody response in mice treated with bisphenol A. J. Med. Invest. 2006, 53:70-80.
3. Alworth L.C., Howdeshell K.L., Ruhlen R.L., Day J.K., Lubahn D.B., Huang T.H., Besch-Williford C.L., vom Saal F.S. Uterine responsiveness to estradiol and DNA methylation are altered by fetal exposure to diethylstilbestrol and methoxychlor in CD-1 mice: effects of low versus high doses. Toxicol. Appl. Pharmacol. 2002, 183:10-22.
4. Andersen H.R., Andersson A.M., Arnold S.F., Autrup H., Barfoed M., Beresford N.A., Bjerregaard P., Christiansen L.B., Gissel B., Hummel R., Jorgensen E.B., Korsgaard B., Le Guevel R., Leffers H., McLachlan J., Moller A., Nielsen J.B., Olea N., Oles-Karasko A., Pakdel F., Pedersen K.L., Perez P., Skakkeboek N.E., Sonnenschein C., Soto A.M., et al. Comparison of short-term estrogenicity tests for identification of hormone-disrupting chemicals. Environ. Health Perspect. 1999, 107(Suppl. 1):89-108.
5. Anway M.D., Cupp A.S., Uzumcu M., Skinner M.K. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005, 308:1466-1469.
6. Anway M.D., Leathers C., Skinner M.K. Endocrine disruptor vinclozolin induced epigenetic transgenerational adult-onset disease. Endocrinology 2006, 147(12):5515-5523.
7. Anway M.D., Skinner M.K. Epigenetic transgenerational actions of endocrine disruptors. Endocrinology 2006, 147:S43-S49.
8. Berger S.L. The complex language of chromatin regulation during transcription. Nature 2007, 447:407-412.
9. Bernal A.J., Jirtle R.L. Epigenomic disruption: the effects of early developmental exposures. Birth Defects Res. A: Clin. Mol. Teratol. 2010, 88:938-944.
10. Biddie S.C. Chromatin architecture and the regulation of nuclear receptor inducible transcription. J. Neuroendocrinol. 2011, 23(1):94-106.
11. Biedermann S., Tschudin P., Grob K. Transfer of bisphenol A from thermal printer paper to the skin. Anal. Bioanal. Chem. 2010, 398:571-576.
12. Braun J.M., Yolton K., Dietrich K.N., Hornung R., Ye X., Calafat A.M., Lanphear B.P. Prenatal bisphenol A exposure and early childhood behavior. Environ. Health Perspect. 2009, 117:1945-1952.
13. Bromer J.G., Zhou Y., Taylor M.B., Doherty L., Taylor H.S. Bisphenol-A exposure in utero leads to epigenetic alterations in the developmental programming of uterine estrogen response. FASEB J. 2010, 24:2273-2280.
14. 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.
15. 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.
16. Champagne F.A., Curley J.P. Maternal regulation of estrogen receptor alpha methylation. Curr. Opin. Pharmacol. 2008, 8:735-739.
17. Champagne F.A., Weaver I.C., Diorio J., Dymov S., Szyf M., Meaney M.J. Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology 2006, 147:2909-2915.
18. Chapin R.E., Adams J., Boekelheide K., Gray L.E., Hayward S.W., Lees P.S., McIntyre B.S., Portier K.M., Schnorr T.M., Selevan S.G., Vandenbergh J.G., Woskie S.R. NTP-CERHR expert panel report on the reproductive and developmental toxicity of bisphenol A. Birth Defects Res. B: Dev. Reprod. Toxicol. 2008, 83:157-395.
19. Clayton E.M., Todd M., Dowd J.B., Aiello A.E. The impact of bisphenol A and triclosan on immune parameters in the US population, NHANES 2003-2006. Environ. Health Perspect. 2011, 119(3):390-396.
20. Cohn B.A., Wolff M.S., Cirillo P.M., Sholtz R.I. DDT and breast cancer in young women: new data on the significance of age at exposure. Environ. Health Perspect. 2007, 115:1406-1414.
21. Cooney C.A., Dave A.A., Wolff G.L. Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J. Nutr. 2002, 132:2393S-2400S.
22. 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.
23. Cummings A.M. Methoxychlor as a model for environmental estrogens. Crit. Rev. Toxicol. 1997, 27:367-379.
24. 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.
25. Doherty L.F., Bromer J.G., Zhou Y., Aldad T.S., Taylor H.S. In utero exposure to diethylstilbestrol (DES) or bisphenol-A (BPA) increases EZH2 expression in the mammary gland: an epigenetic mechanism linking endocrine disruptors to breast cancer. Horm. Cancer 2010, 1:146-155.
26. Dolinoy D.C., Huang D., Jirtle R.L. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc. Natl. Acad. Sci. USA 2007, 104:13056-13061.
27. Dolinoy D.C., Weidman J.R., Waterland R.A., Jirtle R.L. Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome. Environ. Health Perspect. 2006, 114:567-572.
28. 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.
29. Feng S., Jacobsen S.E., Reik W. Epigenetic reprogramming in plant and animal development. Science 2010, 330:622-627.
30. Fisher J.S. Environmental anti-androgens and male reproductive health: focus on phthalates and testicular dysgenesis syndrome. Reproduction 2004, 127:305-315.
31. Fuks F. DNA methylation and histone modifications: teaming up to silence genes. Curr. Opin. Genet. Dev. 2005, 15:490-495.
32. Funabashi T., Kawaguchi M., Furuta M., Fukushima A., Kimura F. Exposure to bisphenol A during gestation and lactation causes loss of sex difference in corticotropin-releasing hormone-immunoreactive neurons in the bed nucleus of the stria terminalis of rats. Psychoneuroendocrinology 2004, 29:475-485.
33. 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.
34. Golebiewska A., Atkinson S.P., Lako M., Armstrong L. Epigenetic landscaping during hESC differentiation to neural cells. Stem Cells 2009, 27:1298-1308.
35. Gore A.C. Developmental programming and endocrine disruptor effects on reproductive neuroendocrine systems. Front. Neuroendocrinol. 2008, 29:358-374.
36. Goto M., Takano-Ishikawa Y., Ono H., Yoshida M., Yamaki K., Shinmoto H. Orally administered bisphenol A disturbed antigen specific immunoresponses in the naive condition. Biosci. Biotechnol. Biochem. 2007, 71:2136-2143.
37. Gould J.C., Leonard L.S., Maness S.C., Wagner B.L., Conner K., Zacharewski T., Safe S., McDonnell D.P., Gaido K.W. Bisphenol A interacts with the estrogen receptor alpha in a distinct manner from estradiol. Mol. Cell. Endocrinol. 1998, 142:203-214.
38. Guerrero-Bosagna C., Settles M., Lucker B., Skinner M.K. Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS ONE 2010, 5.
39. Ho S.M., Tang W.Y., Belmonte de Frausto J., Prins G.S. Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant 4. Cancer Res. 2006, 66:5624-5632.
40. Igarashi A., Ohtsu S., Muroi M., Tanamoto K. Effects of possible endocrine disrupting chemicals on bacterial component-induced activation of NF-kappaB. Biol. Pharm. Bull. 2006, 29:2120-2122.
41. 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.
42. Jirtle R.L., Skinner M.K. Environmental epigenomics and disease susceptibility. Nat. Rev. Genet. 2007, 8:253-262.
43. Kavlock R., Cummings A. Mode of action: inhibition of androgen receptor function-vinclozolin-induced malformations in reproductive development. Crit. Rev. Toxicol. 2005, 35:721-726.
44. Kawai K., Murakami S., Senba E., Yamanaka T., Fujiwara Y., Arimura C., Nozaki T., Takii M., Kubo C. Changes in estrogen receptors alpha and beta expression in the brain of mice exposed prenatally to bisphenol A. Regul. Toxicol. Pharmacol. 2007, 47:166-170.
45. Kawai K., Nozaki T., Nishikata H., Aou S., Takii M., Kubo C. Aggressive behavior and serum testosterone concentration during the maturation process of male mice: the effects of fetal exposure to bisphenol A. Environ. Health Perspect. 2003, 111:175-178.
46. Klose R.J., Bird A.P. Genomic DNA methylation: the mark and its mediators. Trends Biochem. Sci. 2006, 31:89-97.
47. 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.
48. 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.
49. Kuiper G.G., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., van der Saag P.T., van der Burg B., Gustafsson J.A. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 1998, 139:4252-4263.
50. Kwack S.J., Kim K.B., Kim H.S., Yoon K.S., Lee B.M. Risk assessment of soybean-based phytoestrogens. J. Toxicol. Environ. Health A 2009, 72:1254-1261.
51. Lange U.C., Schneider R. What an epigenome remembers. Bioessays 2010, 32:659-668.
52. Li B., Carey M., Workman J.L. The role of chromatin during transcription. Cell 2007, 128:707-719.
53. Li S., Washburn K.A., Moore R., Uno T., Teng C., Newbold R.R., McLachlan J.A., Negishi M. Developmental exposure to diethylstilbestrol elicits demethylation of estrogen-responsive lactoferrin gene in mouse uterus. Cancer Res. 1997, 57:4356-4359.
54. Liu J., Casaccia P. Epigenetic regulation of oligodendrocyte identity. Trends Neurosci. 2010, 33:193-201.
55. McLachlan J.A. Environmental signaling: what embryos and evolution teach us about endocrine disrupting chemicals. Endocr. Rev. 2001, 22:319-341.
56. Metivier R., Gallais R., Tiffoche C., Le Peron C., Jurkowska R.Z., Carmouche R.P., Ibberson D., Barath P., Demay F., Reid G., Benes V., Jeltsch A., Gannon F., Salbert G. Cyclical DNA methylation of a transcriptionally active promoter. Nature 2008, 452:45-50.
57. Miao S., Gao Z., Kou Z., Xu G., Su C., Liu N. Influence of bisphenol a on developing rat estrogen receptors and some cytokines in rats: a two-generational study. J. Toxicol. Environ. Health A 2008, 71:1000-1008.
58. Miller F.D., Gauthier A.S. Timing is everything: making neurons versus glia in the developing cortex. Neuron 2007, 54:357-369.
59. Mills P.K., Yang R. Regression analysis of pesticide use and breast cancer incidence in California Latinas. J. Environ. Health 2006, 68:15-22. quiz 43-14.
60. Nakamura K., Itoh K., Sugimoto T., Fushiki S. Prenatal exposure to bisphenol A affects adult murine neocortical structure. Neurosci. Lett. 2007, 420:100-105.
61. 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.
62. Negishi T., Kawasaki K., Suzaki S., Maeda H., Ishii Y., Kyuwa S., Kuroda Y., Yoshikawa Y. 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.
63. Newbold R.R., Hanson R.B., Jefferson W.N., Bullock B.C., Haseman J., McLachlan J.A. Increased tumors but uncompromised fertility in the female descendants of mice exposed developmentally to diethylstilbestrol. Carcinogenesis 1998, 19:1655-1663.
64. Newbold R.R., Hanson R.B., Jefferson W.N., Bullock B.C., Haseman J., McLachlan J.A. Proliferative lesions and reproductive tract tumors in male descendants of mice exposed developmentally to diethylstilbestrol. Carcinogenesis 2000, 21:1355-1363.
65. Palanza P.L., Howdeshell K.L., Parmigiani S., vom Saal F.S. Exposure to a low dose of bisphenol A during fetal life or in adulthood alters maternal behavior in mice. Environ. Health Perspect. 2002, 110(Suppl. 3):415-422.
66. Patisaul H.B., Adewale H.B. Long-term effects of environmental endocrine disruptors on reproductive physiology and behavior. Front. Behav. Neurosci. 2009, 3:10.
67. Porrini S., Belloni V., Della Seta D., Farabollini F., Giannelli G., Dessi-Fulgheri F. Early exposure to a low dose of bisphenol A affects socio-sexual behavior of juvenile female rats. Brain Res. Bull. 2005, 65:261-266.
68. Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 2007, 447:425-432.
69. Reik W., Dean W., Walter J. Epigenetic reprogramming in mammalian development. Science 2001, 293:1089-1093.
70. Richter C.A., Birnbaum L.S., Farabollini F., Newbold R.R., Rubin B.S., Talsness C.E., Vandenbergh J.G., Walser-Kuntz D.R., vom Saal F.S. In vivo effects of bisphenol A in laboratory rodent studies. Reprod. Toxicol. 2007, 24:199-224.
71. Rosenfeld C.S. Animal models to study environmental epigenetics. Biol. Reprod. 2010, 82:473-488.
72. 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.
73. 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.
74. Smith C.C., Taylor H.S. Xenoestrogen exposure imprints expression of genes (Hoxa10) required for normal uterine development. FASEB J. 2007, 21:239-246.
75. Sohoni P., Sumpter J.P. Several environmental oestrogens are also anti-androgens. J. Endocrinol. 1998, 158:327-339.
76. Stanisic V., Lonard D.M., O'Malley B.W. Modulation of steroid hormone receptor activity. Prog. Brain Res. 2010, 181:153-176.
77. Takayanagi S., Tokunaga T., Liu X., Okada H., Matsushima A., Shimohigashi Y. Endocrine disruptor bisphenol A strongly binds to human estrogen-related receptor gamma (ERRgamma) with high constitutive activity. Toxicol. Lett. 2006, 167:95-105.
78. Tando S., Itoh K., Yaoi T., Ikeda J., Fujiwara Y., Fushiki S. Effects of pre- and neonatal exposure to bisphenol A on murine brain development. Brain Dev. 2007, 29:352-356.
79. Taylor J.A., Welshons W.V., vom Saal F.S. No effect of route of exposure (oral; subcutaneous injection) on plasma bisphenol A throughout 24h after administration in neonatal female mice. Reprod. Toxicol. 2008, 25:169-176.
80. Vandenberg L.N., Chahoud I., Heindel J.J., Padmanabhan V., Paumgartten F.J., Schoenfelder G. Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environ. Health Perspect. 2010, 118:1055-1070.
81. Veurink M., Koster M., Berg L.T. The history of DES, lessons to be learned. Pharm. World Sci. 2005, 27:139-143.
82. Vire E., Brenner C., Deplus R., Blanchon L., Fraga M., Didelot C., Morey L., Van Eynde A., Bernard D., Vanderwinden J.M., Bollen M., Esteller M., Di Croce L., de Launoit Y., Fuks F. The polycomb group protein EZH2 directly controls DNA methylation. Nature 2006, 439:871-874.
83. vom Saal F.S., Hughes C. An extensive new literature concerning low-dose effects of bisphenol A shows the need for a new risk assessment. Environ. Health Perspect. 2005, 113:926-933.
84. vom Saal F.S., Welshons W.V. Large effects from small exposures: II. The importance of positive controls in low-dose research on bisphenol A. Environ. Res. 2006, 100:50-76.
85. Welshons W.V., Nagel S.C., vom Saal F.S. Large effects from small exposures: III. Endocrine mechanisms mediating effects of bisphenol A at levels of human exposure. Endocrinology 2006, 147:S56-S69.
86. Westberry J.M., Trout A.L., Wilson M.E. Epigenetic regulation of estrogen receptor alpha gene expression in the mouse cortex during early postnatal development. Endocrinology 2010, 151:731-740.
87. Wetherill Y.B., Akingbemi B.T., Kanno J., McLachlan J.A., Nadal A., Sonnenschein C., Watson C.S., Zoeller R.T., Belcher S.M. In vitro molecular mechanisms of bisphenol A action. Reprod. Toxicol. 2007, 24:178-198.
88. Xu L.C., Sun H., Chen J.F., Bian Q., Qian J., Song L., Wang X.R. Evaluation of androgen receptor transcriptional activities of bisphenol A, octylphenol and nonylphenol in vitro. Toxicology 2005, 216:197-203.
89. 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.
90. Yan H., Takamoto M., Sugane K. Exposure to bisphenol A prenatally or in adulthood promotes T(H)2 cytokine production associated with reduction of CD4CD25 regulatory T cells. Environ. Health Perspect. 2008, 116:514-519.
91. Yaoi T., Itoh K., Nakamura K., Ogi H., Fujiwara Y., Fushiki S. Genome-wide analysis of epigenomic alterations in fetal mouse forebrain after exposure to low doses of bisphenol A. Biochem. Biophys. Res. Commun. 2008, 376:563-567.
92. Yoshino S., Yamaki K., Yanagisawa R., Takano H., Hayashi H., Mori Y. Effects of bisphenol A on antigen-specific antibody production, proliferative responses of lymphoid cells, and TH1 and TH2 immune responses in mice. Br. J. Pharmacol. 2003, 138:1271-1276.
93. Zhao Z., Fan L., Frick K.M. Epigenetic alterations regulate estradiol-induced enhancement of memory consolidation. Proc. Natl. Acad. Sci. USA 2010, 107:5605-5610.
94. Zhu Z., Edwards R.J., Boobis A.R. Increased expression of histone proteins during estrogen-mediated cell proliferation. Environ. Health Perspect. 2009, 117:928-934.