Bisphenol A alters the development of the rhesus monkey mammary gland

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 21, 2012, Pages 8190-8195

  Tharp, Andrew P ^a   Maffini, Maricel V ^a   Hunt, Patricia A ^b   VandeVoort, Catherine A ^c   Sonnenschein, Carlos ^a   Soto, Ana M ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Endocrine disruptor; Internal dose; Mammogenesis; Morphogenesis; Perinatal exposure

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREAST DEVELOPMENT; CELL DIFFERENTIATION; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; GESTATIONAL AGE; IMMUNOLOCALIZATION; MATERNAL SERUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHESUS MONKEY;

AIR POLLUTANTS, OCCUPATIONAL; ANIMALS; ENDOCRINE DISRUPTORS; EPITHELIUM; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; MACACA MULATTA; MAMMARY GLANDS, ANIMAL; OVARY; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

MACACA MULATTA; PRIMATES; RODENTIA;

EID: 84861434210     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1120488109     Document Type: Article

References (52)

1. Dianin AP (1891) Products of ketone condensation with phenols (translated from Russian). 23:488-506.
2. Dodds EC, Lawson W (1936) Synthetic estrogenic agents without the phenanthrene nucleus. Nature 137:996.
3. Burridge E (2008) Chemical profile: Bisphenol A. ICIS Chemical Business 274:48.
4. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV (2007) Human exposure to bisphenol A (BPA). Reprod Toxicol 24:139-177. (Pubitemid 47385100)
5. Calafat AM, Ye X, Wong LY, Reidy JA, Needham LL (2008) Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003-2004. Environ Health Perspect 116:39-44.
6. Braun JM, et al. (2009) Prenatal bisphenol A exposure and early childhood behavior. Environ Health Perspect 117:1945-1952.
7. Lang IA, et al. (2008) Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. J Am Med Assoc 300:1303-1310.
8. Li DK, et al. (2010) Relationship between urine bisphenol-A level and declining male sexual function. J Androl 31:500-506.
9. Taylor JA, et al. (2011) Similarity of bisphenol A pharmacokinetics in rhesus monkeys and mice: Relevance for human exposure. Environ Health Perspect 119:422-430.
10. Vandenberg LN, et al. (2010) Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environ Health Perspect 118: 1055-1070.
11. Stahlhut RW, Welshons WV, Swan SH (2009) Bisphenol A data in NHANES suggest longer than expected half-life, substantial nonfood exposure, or both. Environ Health Perspect 117:784-789.
12. Zalko D, Jacques C, Duplan H, Bruel S, Perdu E (2011) Viable skin efficiently absorbs and metabolizes bisphenol A. Chemosphere 82:424-430.
13. Kuiper GGJM, et al. (1998) Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139:4252-4263. (Pubitemid 28513713)
14. Alonso-Magdalena P, Morimoto S, Ripoll C, Fuentes E, Nadal A (2006) The estrogenic effect of bisphenol A disrupts pancreatic beta-cell function in vivo and induces insulin resistance. Environ Health Perspect 114:106-112. (Pubitemid 43056876)
15. Krishnan AV, Stathis P, Permuth SF, Tokes L, Feldman D (1993) Bisphenol-A: An estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology 132:2279-2286. (Pubitemid 23156872)
16. Shioda T, et al. (2006) Importance of dosage standardization for interpreting transcriptomal signature profiles: Evidence from studies of xenoestrogens. Proc Natl Acad Sci USA 103:12033-12038. (Pubitemid 44215806)
17. Howdeshell KL, et al. (2003) Bisphenol A is released from used polycarbonate animal cages into water at room temperature. Environ Health Perspect 111:1180-1187. (Pubitemid 36939399)
18. Markey CM, Luque EH, Munoz De Toro MM, Sonnenschein C, Soto AM (2001) In utero exposure to bisphenol A alters the development and tissue organization of the mouse mammary gland. Biol Reprod 65:1215-1223. (Pubitemid 32927590)
19. Vandenberg LN, Maffini MV, Sonnenschein C, Rubin BS, Soto AM (2009) Bisphenol-A and the great divide: A review of controversies in the field of endocrine disruption. Endocr Rev 30:75-95.
20. Chung E, Genco MC, Megrelis L, Ruderman JV (2011) Effects of bisphenol A and triclocarban on brain-specific expression of aromatase in early zebrafish embryos. Proc Natl Acad Sci USA 108:17732-17737.
21. Soriano S, et al. (2012) Rapid insulinotropic action of low doses of bisphenol-A on mouse and human islets of Langerhans: Role of estrogen receptor β. PLoS ONE 7: e31109.
22. Richter CA, et al. (2007) In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol 24:199-224. (Pubitemid 47385096)
23. Cabaton NJ, et al. (2011) Perinatal exposure to environmentally relevant levels of bisphenol A decreases fertility and fecundity in CD-1 mice. Environ Health Perspect 119:547-552.
24. vom Saal FS, et al. (2007) Chapel Hill bisphenol A expert panel consensus statement: Integration of mechanisms, effects in animals and potential to impact human health at current levels of exposure. Reprod Toxicol 24:131-138. (Pubitemid 47385099)
25. Vandenberg LN, et al. (2007) Exposure to the xenoestrogen bisphenol-A alters development of the fetal mammary gland. Endocrinology 148:116-127. (Pubitemid 46021444)
26. Muñoz-de-Toro MM, et al. (2005) Perinatal exposure to bisphenol-A alters peripubertal mammary gland development in mice. Endocrinology 146:4138-4147.
27. Markey CM, Coombs MA, Sonnenschein C, Soto AM (2003) Mammalian development in a changing environment: Exposure to endocrine disruptors reveals the developmental plasticity of steroid-hormone target organs. Evol Dev 5:1-9.
28. Vandenberg LN, et al. (2008) Perinatal exposure to the xenoestrogen bisphenol-A induces mammary intraductal hyperplasias in adult CD-1 mice. Reprod Toxicol 26: 210-219.
29. Fenton SE (2006) Endocrine-disrupting compounds and mammary gland development: Early exposure and later life consequences. Endocrinology 147(Suppl): S18-S24.
30. Ayyanan A, et al. (2011) Perinatal exposure to bisphenol a increases adult mammary gland progesterone response and cell number. Mol Endocrinol 25:1915-1923.
31. Wadia PR, et al. (2007) Perinatal bisphenol A exposure increases estrogen sensitivity of the mammary gland in diverse mouse strains. Environ Health Perspect 115: 592-598. (Pubitemid 46585532)
32. Murray TJ, Maffini MV, Ucci AA, Sonnenschein C, Soto AM (2007) Induction of mammary gland ductal hyperplasias and carcinoma in situ following fetal bisphenol A exposure. Reprod Toxicol 23:383-390. (Pubitemid 46602926)
33. Durando M, et al. (2007) Prenatal bisphenol A exposure induces preneoplastic lesions in the mammary gland in Wistar rats. Environ Health Perspect 115:80-86. (Pubitemid 46050286)
34. Jenkins S, et al. (2009) Oral exposure to bisphenol a increases dimethylbenzanthracene- induced mammary cancer in rats. Environ Health Perspect 117:910-915.
35. Betancourt AM, Eltoum IA, Desmond RA, Russo J, Lamartiniere CA (2010) In utero exposure to bisphenol A shifts the window of susceptibility for mammary carcinogenesis in the rat. Environ Health Perspect 118:1614-1619.
36. Moral R, et al. (2008) Effect of prenatal exposure to the endocrine disruptor bisphenol A on mammary gland morphology and gene expression signature. J Endocrinol 196: 101-112. (Pubitemid 351234575)
37. Yang M, Ryu JH, Jeon R, Kang D, Yoo KY (2009) Effects of bisphenol A on breast cancer and its risk factors. Arch Toxicol 83:281-285.
38. Palmer JR, et al. (2006) Prenatal diethylstilbestrol exposure and risk of breast cancer. Cancer Epidemiol Biomarkers Prev 15:1509-1514. (Pubitemid 44299324)
39. Cohn BA, Wolff MS, Cirillo PM, Sholtz RI (2007) DDT and breast cancer in young women: New data on the significance of age at exposure. Environ Health Perspect 115:1406-1414. (Pubitemid 47628331)
40. Monfort SL, et al. (1987) Comparison of serum estradiol to urinary estrone conjugates in the rhesus macaque (Macaca mulatta). Biol Reprod 37:832-837.
41. Schwartz NB (2010) Endocrinology: Basic and Clinical Principles, eds Melmed S, Conn PM (Humana, Totowa, NJ), pp 367-374.
42. MacLusky NJ, Hajszan T, Leranth C (2005) The environmental estrogen bisphenol a inhibits estradiol-induced hippocampal synaptogenesis. Environ Health Perspect 113:675-679. (Pubitemid 40862177)
43. Leranth C, Hajszan T, Szigeti-Buck K, Bober J, MacLusky NJ (2008) Bisphenol A prevents the synaptogenic response to estradiol in hippocampus and prefrontal cortex of ovariectomized nonhuman primates. Proc Natl Acad Sci USA 105:14187-14191.
44. Jimenez DF, Tarantal AF (2003) Fetal gender determination in early first trimester pregnancies of rhesus monkeys (Macaca mulatta) by fluorescent PCR analysis of maternal serum. J Med Primatol 32:315-319. (Pubitemid 38008521)
45. Friedrichs N, Steiner S, Buettner R, Knoepfle G (2007) Immunohistochemical expression patterns of AP2alpha and AP2gamma in the developing fetal human breast. Histopathology 51:814-823. (Pubitemid 350179422)
46. Moumen M, et al. (2011) The mammary myoepithelial cell. Int J Dev Biol 55:763-771.
47. Sun P, Yuan Y, Li A, Li B, Dai X (2010) Cytokeratin expression during mouse embryonic and early postnatal mammary gland development. Histochem Cell Biol 133:213-221.
48. Prins GS, Ye SH, Birch L, Ho SM, Kannan K (2011) Serum bisphenol A pharmacokinetics and prostate neoplastic responses following oral and subcutaneous exposures in neonatal Sprague-Dawley rats. Reprod Toxicol 31:1-9.
49. Soto AM, Vandenberg LN, Maffini MV, Sonnenschein C (2008) Does breast cancer start in the womb? Basic Clin Pharmacol Toxicol 102:125-133. (Pubitemid 351143422)
50. Lamartiniere CA, Jenkins S, Betancourt AM, Wang J, Russo J (2011) Exposure to the endocrine disruptor Bisphenol A alters susceptibility for mammary cancer. Horm Mol Biol Clin Investig 5:45-52.
51. Li T, et al. (2005) The association of measured breast tissue characteristics with mammographic density and other risk factors for breast cancer. Cancer Epidemiol Biomarkers Prev 14:343-349. (Pubitemid 40270095)
52. Maffini MV, Soto AM, Calabro JM, Ucci AA, Sonnenschein C (2004) The stroma as a crucial target in rat mammary gland carcinogenesis. J Cell Sci 117:1495-1502. (Pubitemid 38559824)