Developmental exposure to bisphenol a impairs the uterine response to ovarian steroids in the adult

Endocrinology

Volumn 149, Issue 11, 2008, Pages 5848-5860

  Varayoud, Jorgelina ^a   Ramos, Jorge G ^a   Bosquiazzo, Verónica L ^a   Muñoz de Toro, Mónica ^a   Luque, Enrique H ^a  

^a UNIVERSIDAD NACIONAL DEL LITORAL   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; DIETHYLSTILBESTROL; MESSENGER RNA; RETINOIC ACID; THYROID HORMONE RECEPTOR;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DECIDUALIZATION; FEMALE; GENE EXPRESSION; GENE SILENCING; HORMONAL REGULATION; HORMONE SUBSTITUTION; HOX GENE; HOXA10 GENE; HOXA11 GENE; IMMUNOFLUORESCENCE; NEWBORN; NONHUMAN; OVARIECTOMY; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROMOTER REGION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ALGORITHMS; ANIMALS; ANIMALS, NEWBORN; CELL PROLIFERATION; DIETHYLSTILBESTROL; ESTROGENS, NON-STEROIDAL; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GONADAL STEROID HORMONES; HOMEODOMAIN PROTEINS; MODELS, BIOLOGICAL; OVARY; PHENOLS; RATS; RATS, WISTAR; STROMAL CELLS; UTERUS;

EID: 54349096788     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-0651     Document Type: Article

References (61)

1. Colborn T, vom Saal FS, Soto AM 1993 Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect 101: 378-384
2. Li S, Hursting SD, Davis BJ, McLachlan JA, Barrett JC 2003 Environmental exposure, DNA methylation, and gene regulation: lessons from diethylstilbestrol-induced cancers. Ann N Y Acad Sci 983:161-169
3. Couse JF, Dixon D, Yates M, Moore AB, Ma L, Maas R, Korach KS 2001 Estrogen receptor-α knockout mice exhibit resistance to the developmental effects of neonatal diethylstilbestrol exposure on the female reproductive tract. Dev Biol 238:224-238
4. Herbst AL, Ulfelder H, Poskanzer DC 1971 Adenocarcinoma of the vagina. Association of maternal stilbestrol therapy with tumor appearance in young women. N Engl J Med 284:878-881
5. 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
6. Li S, Hansman R, Newbold R, Davis B, McLachlan JA, Barrett JC 2003 Neonatal diethylstilbestrol exposure induces persistent elevation of c-fos expression and hypomethylation in its exon-4 in mouse uterus. Mol Carcinog 38:78-84
7. Satokata I, Benson G, Maas R 1995 Sexually dimorphic sterility phenotypes in Hoxa10-deficient mice. Nature 374:460-463
8. Bagot CN, Troy PJ, Taylor HS 2000 Alteration of maternal Hoxa10 expression by in vivo gene transfection affects implantation. Gene Ther 7:1378-1384
9. Hsieh-Li HM, Witte DP, Weinstein M, Branford W, Li H, Small K, Potter SS 1995 Hoxa 11 structure, extensive antisense transcription, and function in male and female fertility. Development 121:1373-1385
10. Yao MW, Lim H, Schust DJ, Choe SE, Farago A, Ding Y, Michaud S, Church GM, Maas RL 2003 Gene expression profiling reveals progesterone-mediated cell cycle and immunoregulatory roles of Hoxa-10 in the preimplantation uterus. Mol Endocrinol 17:610-627
11. Gendron RL, Paradis H, Hsieh-Li HM, Lee DW, Potter SS, Markoff E 1997 Abnormal uterine stromal and glandular function associated with maternal reproductive defects in Hoxa-11 null mice. Biol Reprod 56:1097-1105
12. 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
13. CERHR, NTP-CERHR expert panel report on reproductive and developmental toxicity of bisphenol A 2007 Center for the evaluation of risks to human reproduction (CERHR), U.S. National Toxicology Program (NTP). http://cerhr.niehs.nih.gov/chemicals/bisphenol/BPAFinalEPVF112607.pdf
14. Taylor JA, Welshons WV, vom Saal FS 2008 No effect of route of exposure (oral; subcutaneous injection) on plasma bisphenol A throughout 24 h after administration in neonatal female mice. Reprod Toxicol 25:169-176
15. U.S. Environmental Protection Agency 1993 http://www.epa.gov/iris/ subst/0356.htm. Bisphenol A, CASRN 80-05-7, IRIS, Integrated Risk Information System
16. Newbold RR 2004 Lessons learned from perinatal exposure to diethylstilbestrol. Toxicol Appl Pharmacol 199:142-150
17. vom Saal FS, Hughes C 2005 An extensive new literature concerning low-dose effects of bisphenol A shows the need for a new risk assessment. Environ Health Perspect 113:926-933
18. vom Saal FS, Welshons WV 2006 Large effects from small exposures. II. The importance of positive controls in low-dose research on bisphenol A. Environ Res 100:50-76
19. 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
20. Richter CA, Birnbaum LS, Farabollini F, Newbold RR, Rubin BS, Talsness CE, Vandenbergh JG, Walser-Kuntz DR, vom Saal FS 2007 In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol 24:199-224
21. Ramos JG, Varayoud J, Sonnenschein C, Soto AM, Muñoz-de-Toro M, Luque EH 2001 Prenatal exposure to low doses of bisphenol A alters the periductal stroma and glandular cell function in the rat ventral prostate. Biol Reprod 65: 1271-1277
22. Markey CM, Luque EH, Muñoz-de-Toro M, 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
23. Ramos JG, Varayoud J, Kass L, Rodriguez H, Costabel L, Muñoz-de-Toro M, Luque EH 2003 Bisphenol a induces both transient and permanent histofunctional alterations of the hypothalamic-pituitary-gonadal axis in prenatally exposed male rats. Endocrinology 144:3206-3215
24. Durando M, Kass L, Piva J, Sonnenschein C, Soto AM, Luque EH, Muñoz-de-Toro M 2007 Prenatal bisphenol A exposure induces preneoplastic lesions in the mammary gland in Wistar rats. Environ Health Perspect 115:80-86
25. Muñoz-de-Toro M, Markey CM, Wadia PR, Luque EH, Rubin BS, Sonnenschein C, Soto AM 2005 Perinatal exposure to bisphenol-A alters peripubertal mammary gland development in mice. Endocrinology 146:4138-4147
26. Monje L, Varayoud J, Luque EH, Ramos JG 2007 Neonatal exposure to bisphenol A modifies the abundance of estrogen receptor α transcripts with alternative 5′-untranslated regions in the female rat preoptic area. J Endocrinol 194:201-212
27. Stoker C, Rey F, Rodriguez H, Ramos JG, Sirosky P, Larriera A, Luque EH, Muñoz-de-Toro M 2003 Sex reversal effects on Caiman latirostris exposed to environmentally relevant doses of the xenoestrogen bisphenol A. Gen Comp Endocrinol 133:287-296
28. Stoker C, Beldoménico PM, Bosquiazzo VL, Zayas MA, Rey F, Rodríguez H, Muñoz-de-Toro M, Luque EH 2008 Developmental exposure to endocrine disruptor chemicals alters follicular dynamics and steroid levels in Caiman latirostris. Gen Comp Endocrinol 156:603-612
29. 1 phase of the cell cycle requires temporal and cell-specific hormone-dependent changes on cell cycle regulators. Endocrinology 144:5450-5458
30. Paria BC, Reese J, Das SK, Dey SK 2002 Deciphering the cross-talk of implantation: advances and challenges. Science 296:2185-2188
31. Higuchi R, Fockler C, Dollinger G, Watson R 1993 Kinetic PCR analysis: real-time monitoring of DNA amplification reactions. Biotechnology 11:1026-1030
32. Rey F, Ramos JG, Stoker C, Bussmann LE, Luque EH, Muñoz-de-Toro M 2006 Vitellogenin detection in Caiman latirostris (Crocodylia: Alligatoridae): a tool to assess environmental estrogen exposure in wildlife. J Comp Physiol [B] 176:243-251
33. Kass L, Varayoud J, Ortega H, Muñoz-de-Toro M, Luque EH 2000 Detection of bromodeoxyuridine in formalin-fixed tissue. DNA denaturation following microwave or enzymatic digestion pretreatment is required. Eur J Histochem 44:185-191
34. Muñoz-de-Toro M, Maffini MV, Kass L, Luque EH 1998 Proliferative activity and steroid hormone receptor status in male breast carcinoma. J Steroid Biochem Mol Biol 67:333-339
35. Ramos JG, Varayoud J, Bosquiazzo VL, Luque EH, Muñoz-de-Toro M 2002 Cellular turnover in the rat uterine cervix and its relationship to estrogen and progesterone receptor dynamics. Biol Reprod 67:735-742
36. Weibel ER 1969 Stereological principles for morphometry in electron microscopic cytology. Int Rev Cytol 26:235-302
37. Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB 1996 Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA 93:9821-9826
38. Li LC, Dahiya R 2002 MethPrimer: designing primers for methylation PCRs. Bioinformatics 18:1427-1431
39. Thomassin H, Kress C, Grange T 2004 MethylQuant: a sensitive method for quantifying methylation of specific cytosines within the genome. Nucleic Acids Res 32:e168
40. Bartol FF, Wiley AA, Bagnell CA 2006 Uterine development and endometrial programming. Soc Reprod Fertil Suppl 62:113-130
41. Mericskay M, Carta L, Sassoon D 2005 Diethylstilbestrol exposure in utero: a paradigm for mechanisms leading to adult disease. Birth Defects Res A Clin Mol Teratol 73:133-135
42. Taylor HS 2000 The role of HOX genes in the development and function of the female reproductive tract. Semin Reprod Med 18:81-89
43. Fei X, Chung H, Taylor HS 2005 Methoxychlor disrupts uterine Hoxa10 gene expression. Endocrinology 146:3445-3451
44. Smith CC, Taylor HS 2007 Xenoestrogen exposure imprints expression of genes (Hoxa10) required for normal uterine development. FASEB J 21:239-246
45. Taylor HS, Fei X 2005 Emx2 regulates mammalian reproduction by altering endometrial cell proliferation. Mol Endocrinol 19:2839-2846
46. Zhang X, Chen CH, Confino E, Barnes R, Milad M, Kazer RR 2005 Increased endometrial thickness is associated with improved treatment outcome for selected patients undergoing in vitro fertilization-embryo transfer. Fertil Steril 83:336-340
47. Markey CM, Wadia PR, Rubin BS, Sonnenschein C, Soto AM 2005 Longterm effects of fetal exposure to low doses of the xenoestrogen bisphenol-A in the female mouse genital tract. Biol Reprod 72:1344-1351
48. Velarde MC, Geng Y, Eason RR, Simmen FA, Simmen RC 2005 Null mutation of Kruppel-like factor9/basic transcription element binding protein-1 alters peri-implantation uterine development in mice. Biol Reprod 73:472-481
49. Gargett BE, Chan RW 2006 Endometrial stem/progenitor cells and proliferative disorders of the endometrium. Minerva Ginecol 58:511-526
50. Privalsky ML 2004 The role of corepressors in transcriptional regulation by nuclear hormone receptors. Annu Rev Physiol 66:315-360
51. Daikoku T, Tranguch S, Friedman DB, Das SK, Smith DF, Dey SK 2005 Proteomic analysis identifies immunophilin FK506 binding protein 4 (FKBP52) as a downstream target of Hoxa10 in the periimplantation mouse uterus. Mol Endocrinol 19:683-697
52. 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
53. Timms BG, Howdeshell KL, Barton L, Bradley S, Richter CA, Vom Saal FS 2005 Estrogenic chemicals in plastic and oral contraceptives disrupt development of the fetal mouse prostate and urethra. Proc Natl Acad Sci USA 102: 7014-7019
54. Nagel SC, Hagelbarger JL, McDonnell DP 2001 Development of an ER action indicator mouse for the study of estrogens, selective ER modulators (SERMs), and Xenobiotics. Endocrinology 142:4721-4728
55. Gould JC, Leonard LS, Maness SC, Wagner BL, Conner K, Zacharewski T, Safe S, McDonnell DP, Gaido KW 1998 Bisphenol A interacts with the estrogen receptor alpha in a distinct manner from estradiol. Mol Cell Endocrinol 142:203-214
56. Nishizawa H, Imanishi S, Manabe N 2005 Effects of exposure in utero to bisphenol a on the expression of aryl hydrocarbon receptor, related factors, and xenobiotic metabolizing enzymes in murine embryos. J Reprod Dev 51:593-605
57. Li S, Ma L, Chiang T, Burow M, Newbold RR, Negishi M, Barrett JC, McLachlan JA 2001 Promoter CpG methylation of Hox-a10 and Hox-a11 in mouse uterus not altered upon neonatal diethylstilbestrol exposure. Mol Carcinog 32:213-219
58. Spencer TE, Hayashi K, Hu J, Carpenter KD 2005 Comparative developmental biology of the mammalian uterus. Curr Top Dev Biol 68:85-122
59. Jones RL, Salamonsen LA, Critchley HO, Rogers PA, Affandi B, Findlay JK 2000 Inhibin and activin subunits are differentially expressed in endometrial cells and leukocytes during the menstrual cycle, in early pregnancy and in women using progestin-only contraception. Mol Hum Reprod 6:1107-1117
60. Caniggia I, Lye SJ, Cross JC 1997 Activin is a local regulator of human cytotrophoblast cell differentiation. Endocrinology 138:3976-3986
61. He ZY, Liu HC, Mele CA, Barmat L, Veeck LL, Davis O, Rosenwaks Z 1999 Expression of inhibin/activin subunits and their receptors and binding proteins in human preimplantation embryos. J Assist Reprod Genet 16:73-80