Perinatal exposure to environmentally relevant levels of bisphenol A decreases fertility and fecundity in CD-1 mice

Environmental Health Perspectives

Volumn 119, Issue 4, 2011, Pages 547-552

  Cabaton, Nicolas J ^a   Wadia, Perinaaz R ^a   Rubin, Beverly S ^a   Zalko, Daniel ^b   Schaeberle, Cheryl M ^a   Askenase, Michael H ^a   Gadbois, Jennifer L ^a   Tharp, Andrew P ^a   Whitt, Gregory S ^a   Sonnenschein, Carlos ^a   Soto, Ana M ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CEMAGREF   (France)

Author keywords

Biphasic dose response; Bisphenol A; Endocrine disruptor; Fecundity; Fertility; Fetal origins of adult disease; Perinatal exposure

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; DIETHYLSTILBESTROL;

ANIMAL EXPERIMENT; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FEMALE; LACTATION; MALE; MOUSE; NONHUMAN; PERINATAL PERIOD; PREGNANCY OUTCOME; PRENATAL EXPOSURE; PRIORITY JOURNAL; REPRODUCTIVE TOXICITY; SUBFERTILITY;

ANIMALS; ANIMALS, NEWBORN; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENTAL POLLUTANTS; FEMALE; FERTILITY; MICE; PHENOLS; REPRODUCTION;

MUS;

EID: 79955554674     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1002559     Document Type: Article

References (54)

1. Amara JF, Dannies PS. 1983. 17β-Estradiol has a biphasic effect on GH cell growth. Endocrinology 112:1141-1143.
2. Baird DD, Newbold R. 2005. Prenatal diethylstilbestrol (DES) exposure is associated with uterine leiomyoma development. Reprod Toxicol 20:81-84.
3. Bateson P, Barker D, Clutton-Brock T, Deb D, D'Udine B, Foley RA, et al. 2004. Developmental plasticity and human health. Nature 430:419-421.
4. Blair RM, Fang H, Branham WS, Hass BS, Dial SL, Moland CL, et al. 2001. The estrogen receptor relative binding affinities of 188 natural and xenochemicals: structural diversity of ligands. Toxicol Sci 54:138-153.
5. Calafat AM, Weuve J, Ye X, Jia LT, Hu H, Ringer S, et al. 2009. Exposure to bisphenol A and other phenols in neonatal intensive care unit premature infants. Environ Health Perspect 117:639-644.
6. 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.
7. Crain DA, Janssen SJ, Edwards TM, Heindel J, Ho S-M, Hunt P, et al. 2008. Female reproductive disorders: the roles of endocrine-disrupting compounds and developmental timing. Fertil Steril 90:911-940.
8. Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, Hauser R, Prins GS, Soto AM, et al. 2009. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev 30:293-342.
9. Gilbert SF, Epel D. 2009. Ecological Developmental Biology: Integrating Epigenetics, Medicine, and Evolution. Sunderland, MA:Sinauer Associates.
10. Honma S, Suzuki A, Buchanan DL, Katsu Y, Watanabe H, Iguchi T. 2002. Low dose effects of in utero exposure to bisphenol A and diethylstilbestrol on female mouse reproduction. Reprod Toxicol 16:117-122.
11. Howdeshell KL, Hotchkiss AK, Thayer KA, Vandenbergh JG, vom Saal FS. 1999. Exposure to bisphenol A advances puberty. Nature 401:763-764.
12. Hugo ER, Borcherding DC, Gersin KS, Loftus J, Ben-Jonathan N. 2008. Prolactin release by adipose explants, primary adipocytes, and LS14 adipocytes. J Clin Endocrinol Metab 93:4006-4012.
13. Ikezuki Y, Tsutsumi O, Takai Y, Kamei Y, Taketani Y. 2002. Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum Reprod 17:2839-2841.
14. Integrated Risk Information System (IRIS). Bisphenol A. (CASRN 80-05-7), Vol 2002. US-EPA IRIS Substance File. Available: http://www.epa.gov/iris/subst/0356.htm [accessed 28 February 2011].
15. Jaeg JP, Perdu E, Dolo L, Debrauwer L, Cravedi JP, Zalko D. 2004. Characterization of new bisphenol A metabolites produced by CD1 mice liver microsomes and S9 fractions. J Agric Food Chem 52:4935-4942.
16. Jensen TK, Sobotka T, Hansen MA, Pedersen AT, Lutz W, Skakkebaek NE. 2008. Declining trends in conception rates in recent birth cohorts of native Danish women: a possible role of deteriorating male reproductive health. Int J Androl 31:81-92.
17. Jouannet P, Wang C, Eustache F, Kold-Jensen T, Auger J. 2001. Semen quality and male reproductive health: the controversy about human sperm concentration decline. APMIS 109:333-344.
18. Maffini MV, Rubin BS, Sonnenschein C, Soto AM. 2006. Endocrine disruptors and reproductive health: the case of bisphenol A. Mol Cell Endocrinol 254-255:179-186.
19. 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.
20. Markey CM, Wadia PR, Rubin BS, Sonnenschein C, Soto AM. 2005. Long-term effects of fetal exposure to low doses of the xenoestrogen bisphenol-A in the female mouse genital tract. Biol Reprod 72:1344-1351.
21. McLachlan JA, Newbold RR, Bullock BC. 1980. Long-term effects on the female mouse genital tract associated with prenatal exposure to diethylstilbestrol. Cancer Res 40:3988-3999.
22. McLachlan JA, Newbold RR, Shah HC, Hogan MD, Dixon RL. 1982. Reduced fertility in female mice exposed transplacentally to diethylstilbestrol (DES). Fertil Steril 38:364-371.
23. Munoz de Toro MM, Markey CM, Wadia PR, Luque EH, Rubin BS, Sonnenschein C, et al. 2005. Perinatal exposure to bisphenol A alters peripubertal mammary gland development in mice. Endocrinology 146:4138-4147.
24. Myers JP, Zoeller RT, vom Saal FS. 2009. A clash of old and new scientific concepts in toxicity, with important implications for public health. Environ Health Perspect 117:1652-1655.
25. Myers P, Hessler W. 2007. Does 'the dose make the poison?' Available: http://www.environmentalhealthnews.org/sciencebackground/2007/2007-0415nmdrc.html [accessed 30 April 2007].
26. Newbold RR. 2008. Prenatal exposure to diethylstilbestrol (DES). Fertil Steril 89(2 Suppl):e55-e56; doi:10.1016/j.fertnstert.2008.01.062 [Online 4 March 2008].
27. Newbold RR, Padilla-Banks E, Jefferson WN, Heindel JJ. 2008. Effects of endocrine disruptors on obesity. Int J Androl 31:201-208.
28. Newbold RR, Tyrey S, Haney AF, McLachlan JA. 1983. Developmentally arrested oviduct: a structural and functional defect in mice following prenatal exposure to diethylstilbestrol. Teratology 27:417-426.
29. Olea N, Pulgar R, Perez P, Olea-Serrano F, Rivas A, Novillo-Fertrell A, et al. 1996. Estrogenicity of resin-based composites and sealants used in dentistry. Environ Health Perspect 104:298-305.
30. Padmanabhan V, Siefert K, Ransom S, Johnson T, Pinkerton J, Anderson L, et al. 2008. Maternal bisphenol-A levels at delivery: a looming problem? J Perinatol 28:258-263.
31. Rubin BS, Lenkowski JR, Schaeberle CM, Vandenberg LN, Ronsheim PM, Soto AM. 2006. Evidence of altered brain sexual differentiation in mice exposed perinatally to low environmentally relevant levels of bisphenol A. Endocrinology 147:3681-3691.
32. Rubin BS, Murray MK, Damassa DA, King JC, Soto AM. 2001. Perinatal exposure to low doses of bisphenol A affects body weight, patterns of estrous cyclicity and plasma LH levels. Environ Health Perspect 109:675-680.
33. Schönfelder G, Wittfoht W, Hopp H, Talsness CE, Paul M, Chahoud I. 2002. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ Health Perspect 110:A703-A707.
34. Silva E, Rajapakse N, Kortenkamp A. 2002. Something from "nothing"-eight weak estrogenic chemicals combined at concentrations below NOECs produce significant mixture effects. Environ Sci Technol 36:1751-1756.
35. Skakkebaek NE. 1998. Trends in male reproductive health. Environmental aspects. Adv Exp Med Biol 444:1-2.
36. Skakkebaek NE, Rajpert-DeMeyts E, Main KM. 2001. Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod 16:972-978.
37. Sonnenschein C, Olea N, Pasanen ME, Soto AM. 1989. Negative controls of cell proliferation: human prostate cancer cells and androgens. Cancer Res 49:3474-3481.
38. Soto AM, Chung KL, Sonnenschein C. 1994. The pesticides endosulfan, toxaphene, and dieldrin have estrogenic effects on human estrogen sensitive cells. Environ Health Perspect 102:380-383.
39. Soto AM, Fernandez MF, Luizzi MF, Oles Karasko AS, Sonnenschein C. 1997. Developing a marker of exposure to xenoestrogen mixtures in human serum. Environ Health Perspect 105:647-654.
40. Soto AM, Lin T-M, Justicia H, Silvia RM, Sonnenschein C. 1992. An "in culture" bioassay to assess the estrogenicity of xenobiotics. In: Chemically Induced Alterations in Sexual Development: The Wildlife/Human Connection (Colborn T, Clement C, eds). Princeton, NJ:Princeton Scientific Publishing, 295-309.
41. Soto AM, Sonnenschein C. 2010. Environmental causes of cancer: endocrine disruptors as carcinogens. Nat Rev Endocrinol 6:363-370.
42. Sun Y, Irie M, Kishikawa N, Wada M, Kuroda N, Nakashima K. 2004. Determination of bisphenol A in human breast milk by HPLC with column-switching and fluorescence detection. Biomed Chromatogr 18:501-507.
43. Thomas P, Dong J. 2006. Binding and activation of the seven-transmembrane estrogen receptor GPR30 by environmental estrogens: a potential novel mechanism of endocrine disruption. J Steroid Biochem Mol Biol 102:175-179.
44. Tollefsen KE. 2002. Interaction of estrogen mimics, singly and in combination, with plasma sex steroid-binding proteins in rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 56:215-225.
45. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. 2007. Human exposure to bisphenol A (BPA). Reprod Toxicol 24:139-177.
46. Vandenberg LN, Wadia PR, Schaeberle CM, Rubin BS, Sonnenschein C, Soto AM. 2006. The mammary gland response to estradiol: monotonic at the cellular level, non-monotonic at the tissue-level of organization? J Steroid Biochem Mol Biol 101:263-274.
47. Wadia PR, Vandenberg LN, Schaeberle CM, Rubin BS, Sonnenschein C, Soto AM. 2007. Perinatal bisphenol A exposure increases estrogen sensitivity of the mammary gland in diverse mouse strains. Environ Health Perspect 115:592-598.
48. Welshons WV, Nagel SC, vom Saal FS. 2006. Large effects from small exposures. III. Endocrine mechanisms mediating effects of bisphenol A at levels of human exposure. Endocrinology 147:S56-S69.
49. Welshons WV, Rottinghaus GE, Nonneman DJ, Dolan-Timpe M, Ross PF. 1990. A sensitive bioassay for detection of dietary estrogens in animal feeds. J Vet Diagn Invest 2(4):268-273.
50. Welshons WV, Thayer KA, Judy BM, Taylor JA, Curran EM, vom Saal FS. 2003. Large effects from small exposures: I. Mechanisms for endocrine-disrupting chemicals with estrogenic activity. Environ Health Perspect 111:994-1006
51. Wetherill YB, Petre CE, Monk KR, Puga A, Knudsen KE. 2002. The xenoestrogen bisphenol A induces inappropriate androgen receptor activation and mitogenesis in prostatic adenocarcinoma cells. Mol Cancer Ther 1:515-524.
52. ++ fluxes and prolactin release in GH3/B6 pituitary tumor cells. Environ Health Perspect 113:431-439.
53. Ye X, Pierik FH, Angerer J, Meltzer HM, Jaddoe VW, Tiemeier H, et al. 2009. Levels of metabolites of organophosphate pesticides, phthalates, and bisphenol A in pooled urine specimens from pregnant women participating in the Norwegian Mother and Child Cohort Study (MoBa). Int J Hyg Environ Health 212:481-491.
54. Zalko D, Soto AM, Dolo L, Dorio C, Ratahao E, Debrauwer L, et al. 2003. Biotransformations of bisphenol A in a mammalian model: answers and new questions raised by low-dose metabolic fate studies in pregnant CD1 mice. Environ Health Perspect 111:309-319.