Bisphenol-A exposure during the period of blastocyst implantation alters uterine morphology and perturbs measures of estrogen and progesterone receptor expression in mice

Reproductive Toxicology

Volumn 30, Issue 3, 2010, Pages 393-400

  Berger, Robert G ^a   Foster, Warren G ^a   deCatanzaro, Denys ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Bisphenol A; Estrogen receptor alpha; Implantation; Progesterone receptor; Uterine luminal epithelial cells

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ESTROGEN RECEPTOR; PROGESTERONE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS LUTEUM; ENDOMETRIUM CELL; ESTROGEN ACTIVITY; FEMALE; FIRST TRIMESTER PREGNANCY; MOUSE; NIDATION; NONHUMAN; PRENATAL EXPOSURE; PROTEIN EXPRESSION; REPRODUCTIVE TOXICITY;

ANIMALS; BLOTTING, WESTERN; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO IMPLANTATION; ESTROGEN RECEPTOR ALPHA; ESTROGENS, NON-STEROIDAL; FEMALE; GESTATIONAL AGE; IMMUNOHISTOCHEMISTRY; LACTOFERRIN; LINEAR MODELS; MICE; MICE, INBRED STRAINS; OVARY; PHENOLS; PREGNANCY; RECEPTORS, PROGESTERONE; UTERUS;

MUS;

EID: 77956425701     PISSN: 08906238     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.reprotox.2010.06.006     Document Type: Article

References (77)

1. Burridge E. Bisphenol A: product profile. Eur Chem News 2003, 17:14-20.
2. Krishnan A.V., Stathis P., Permuth S.F., Tokes L., Feldman D. Bisphenol-A: an estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology 1993, 132:2279-2286.
3. Olea N., Pulgar R., Pérez P., Olea-Serrano F., Rivas A., Novillo-Fertrell A., et al. Estrogenicity of resin-based composites and sealants used in dentistry. Environ Health Perspect 1996, 104:298-305.
4. Biles J.E., White K.D., McNeal T.P., Begley T.H. Determination of the diglycidyl ether of bisphenol A and its derivatives in canned foods. J Agric Food Chem 1999, 47:1965-1969.
5. Matsumoto A., Kunugita N., Kitagawa K., Isse T., Oyama T., Foureman G.L., et al. A levels in human urine. Environ Health Perspect 2003, 111:101-104.
6. 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 human reference population. Environ Health Perspect 2005, 113:391-395.
7. Schönfelder 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.
8. Kuruto-Niwa R., Tateoka Y., Usuki Y., Nozawa R. Measurement of bisphenol A concentrations in human colostrum. Chemosphere 2007, 66:1160-1164.
9. Sun Y., Irie M., Kishikawa N., Wada M., Kuroda N., Nakashima K. Determination of bisphenol A in human breast milk by HPLC with column-switching and fluorescence detection. Biomed Chromatogr 2004, 18:501-507.
10. Ye X., Kuklenyik Z., Needham L.L., Calafat A.M. Measuring environmental phenols and chlorinated organic chemicals in breast milk using automated on-line column-switching-high performance liquid chromatography-isotope dilution tandem mass spectrometry. J Chromatogr B 2006, 831:110-115.
11. Dodds E.C., Lawson W. Synthetic oestrogenic agents without the phenanthrene nucleus. Nature 1936, 137:996.
12. Brotons J.A., Olea-Serrano M.F., Villalobos M., Olea N. Xenoestrogens released from lacquer coating in food cans. Environ Health Perspect 1994, 103:608-612.
13. Berger R.G., Hancock T., deCatanzaro D. Influence of oral and subcutaneous bisphenol-A on intrauterine implantation of fertilized ova in inseminated female mice. Reprod Toxicol 2007, 23:138-144.
14. Al-Hiyasat A.S., Darmani H., Elbetieha A.M. Effects of bisphenol A on adult male mouse fertility. Eur J Oral Sci 2002, 110:163-167.
15. Al-Hiyasat A.S., Darmani H., Elbetieha A.M. Leached components from dental composites and their effects on fertility of female mice. Eur J Oral Sci 2004, 112:267-272.
16. Tohei A., Suda S., Taya K., Hashimoto T., Kogo H., Bisphenol A inhibits testicular functions and increase luteinizing hormone secretion in adult male rats. Exp Biol Med 2001, 226:216-221.
17. Savabieasfahani M., Kannan K., Astapova O., Evans N.P., Padmanabhan V. Developmental programming: differential effects of prenatal exposure to bisphenol-A or methoxychlor on reproductive function. Endocrinology 2006, 147:5956-5966.
18. Berger R.G., Shaw J., deCatanzaro D. Impact of acute bisphenol-A exposure upon intrauterine implantation of fertilized ova and urinary levels of progesterone and 17β-estradiol. Reprod Toxicol 2008, 26:94-99.
19. Tsutsui T., Tamura Y., Yagi E., Hasegawa K., Masayuki T., Maizumi N., et al. Bisphenol-A induces cellular transformation, aneuploidy and DNA adduct formation in cultured Syrian hamster embryo cells. Int J Cancer 1998, 75:290-294.
20. Howdeshell K.L., Hotchkiss A.K., Thayer K.A., Vandenbergh J.G., vom Saal F.S. Exposure to bisphenol A advances puberty. Nature 1999, 401:763-764.
21. Takai Y., Tsutsumi O., Ikezuki Y., Kamei Y., Osuga Y., Yano T., et al. Preimplantation exposure to bisphenol A advances postnatal development. Reprod Toxicol 2001, 15:71-74.
22. Fujimoto T., Kubo K., Aou S. Prenatal exposure to bisphenol A impairs sexual differentiation of exploratory behavior and increases depression-like behavior in rats. Brain Res 2006, 106:849-855.
23. Nakagami A., Negishi T., Kawasaki K., Imai N., Nishida Y., Ihara T., et al. Alterations in male infant behaviors towards its mother by prenatal exposure to bisphenol A in cynomolgus monkeys (Macaca fascicularis) during early suckling period. Psychoneuroendocrinology 2009, 34:1189-1197.
24. Hunt P.A., Koehler K.E., Susiarjo M., Hodges C.A., Ilagan A., Voigt R.C., et al. exposure causes meiotic aneuploidy in the female mouse. Curr Biol 2003, 13:546-553.
25. Ashby J., Tinwell H., Haseman J. Lack of effects for low dose levels of bisphenol A and diethylstilbestrol on the prostate gland of CF1 mice exposed in utero. Regul Toxicol Pharmacol 1999, 30:156-166.
26. Cagen S.Z., Weachter J.M., Dimond S.S., Breslin W.J., Butala J.H., Jekat F.W., et al. Normal reproductive organ development in Wistar rats exposed to bisphenol A in the drinking water. Regul Toxicol Pharmacol 1999, 30:130-139.
27. Ema M., Fujii S., Furukawa M., Kiguchi M., Ikka T., Harazono A. Rat two-generation reproductive toxicity study of bisphenol A. Reprod Toxicol 2001, 15:505-523.
28. Tyl R.W., Myers C.B., Marr M.C., Thomas B.F., Keimowitz A.R., Brine D.R., et al. Three-generation reproductive toxicity study of dietary bisphenol A in CD Sprague-Dawley rats. Toxicol Sci 2002, 68:121-146.
29. Ryan B.C., Hotchkiss A.K., Crofton K.M., Gray L.E. In utero and lactational exposure to bisphenol A, in contrast to ethinyl estradiol, does not alter sexually dimorphic behavior, puberty, fertility and anatomy of female LE rats. Toxicol Sci 2010, 114:133-148.
30. Gray G.M., Cohen J.T., Cunha G., Hughes C., McConnell E.E., Rhomberg L., et al. Weight of the evidence evaluation of low-dose reproductive and developmental effects of bisphenol A. Human Ecol Risk Assess 2004, 10:875-921.
31. Foster W.G., Neal M.S., Han M.S., Dominguez M.M. Environmental contaminants and human infertility: hypothesis or cause for concern?. J Toxicol Env Heal B 2008, 11:162-176.
32. Goodman J.E., Witorsh R.J., McConnell E.E., Sipes I.G., Slayton T.M., Yu C.J., et al. Weight-of-evidence evaluation of reproductive and developmental effects of low doses of bisphenol A. Crit Rev Toxicol 2009, 39:1-75.
33. deCatanzaro D., MacNiven E., Ricciuti F. Comparison of the adverse effects of adrenal and ovarian steroids on early pregnancy in mice. Psychoneuroendocrinology 1991, 16:525-536.
34. deCatanzaro D., Baptista M.A.S., Spironello-Vella E. Administration of minute quantities of 17β-estradiol on the nasal area terminates early pregnancy in inseminated female mice. Pharmacol Biochem Behav 2001, 69:503-509.
35. deCatanzaro D., Beaton E.A., Khan A., Vella E. Urinary oestradiol and testosterone levels from novel male mice approach values sufficient to disrupt early pregnancy in nearby inseminated females. Reproduction 2006, 132:309-317.
36. Tachibana T., Wakimoto Y., Nakamuta N., Phichitraslip T., Wakitani S., Kusakabe K., et al. Effects of bisphenol A (BPA) on placentation and survival of the neonates in mice. J Reprod Dev 2007, 53:509-514.
37. Kim J.C., Shin H.C., Cha S.W., Koh W.S., Chung M.K., Han S.S. Evaluation of developmental toxicity in rats exposed to the environmental estrogen bisphenol A during pregnancy. Life Sci 2001, 69:2611-2625.
38. Papaconstantinou A., Umbreit T.H., Fisher B.R., Goering P.L., Lappas N.T., Brown K.M. Bisphenol A-induced increase in uterine weight and alterations in uterine morphology in ovariectomized B6C3F1 mice: role of the estrogen receptor. Toxicol Sci 2000, 56:332-339.
39. Steinmetz R., Mitchern 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.
40. Cook J.C., Kaplan A.M., Davis L.G., O'Connor J. Development of a tier I screening battery for detecting endocrine-active compounds (EACs). Regul Toxicol Pharm 1997, 26:60-68.
41. Markey C.M., Wadia P.R., Rubin B.S., Sonnenschein C., Soto A.M. Long-term effects of fetal exposure to low doses of the xenoestrogen bisphenol-A in the female mouse genital tract. Biol Reprod 2005, 72:1344-1351.
42. Markey C.M., Michaelson C.L., Veson E.C., Sonnenschein C., Soto A.M. The mouse uterotrophic assay: a reevaluation of its validity in assessing the estrogenicity of bisphenol A. Environ Health Perspect 2001, 109:55-60.
43. Pentecost B.T., Teng C.T. Lactotransferrin is the major estrogen inducible protein of mouse uterine secretions. J Biol Chem 1987, 262:10134-10139.
44. Newbold R.R., Teng C.T., Beckman W.C., Jefferson W.N., Hanson R.B., Miller J.V., et al. Fluctuations of lactoferrin protein and messenger ribonucleic acid in the reproductive tract of the mouse during the estrous cycle. Biol Reprod 1992, 47:903-915.
45. McMaster M.T., Dey S.K., Andrews G.K. Association of monocytes and neutrophils with early events of blastocyst implantation in mice. J Reprod Fertil 1993, 99:561-569.
46. Mehmood Z., Smith A.G., Tucker J.J., Chuzel F., Carmichael N.G. The development of methods for assessing the in vivo oestrogen-like effects of xenobiotics in CD-1 mice. Food Chem Toxicol 2000, 38:493-501.
47. deCatanzaro D., MacNiven E. Psychogenic pregnancy disruption in mammals. Neurosci Biobehav Rev 1992, 16:43-53.
48. Jefferson W.N., Padilla-Banks E., Newbold R.R. Adverse effects on female development and reproduction in CD-1 mice following neonatal exposure to the phytoestrogen genistein at environmentally relevant doses. Biol Reprod 2005, 73:798-806.
49. Bradford M.M. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal Biochem 1976, 72:248-254.
50. Pedhazur E.J. Multiple regression in behavioral research 1982, Holt, Rinehart and Winston, New York. 2nd ed.
51. Mukku V.R., Kirkland J.L., Hardy M., Stancel G.M. Hormonal control of uterine growth: temporal relationships between estrogen administration and deoxyribonucleic acid synthesis. Endocrinology 1982, 111:480-487.
52. Dey S.K., Lim H. Implantation. The physiology of reproduction 2006, 593-678. Raven Press, New York. E. Knobil, J.D. Neill (Eds.).
53. Paria B.C., Huet-Hudson Y.M., Dey S.K. Blastocyst's state of activity determines the " window" of implantation in the receptive mouse uterus. Proc Natl Acad Sci USA 1993, 90:10159-10162.
54. Roblero L.S., Garavagno A.C. Effect of oestradiol-17β and progesterone on oviductal transport and early development of mouse embryos. J Reprod Fertil 1979, 57:91-95.
55. Huet H., Andrews G.K., Dey S.K. Cell type-specific localization of c-myc protein in the mouse uterus: modulation by steroid hormones and analysis of the periimplantation period. Endocrinology 1989, 125:1683-1693.
56. Potter S.W., Gaza G., Morris J.E. Estradiol induces E-cadherin degradation in mouse uterine epithelium during the estrous cycle and early pregnancy. J Cell Physiol 1996, 169:1-14.
57. Ma W., Song H., Das S.K., Bibhash C.P., Dey S.K. Estrogen is a critical determinant that specifies the duration of the window of uterine receptivity for implantation. Proc Natl Acad Sci USA 2003, 100:2963-2968.
58. Paria B.C., Lim H., Wang X.N., Liehr J., Das S.K., Dey S.K. Coordination of differential effects of primary estrogen and catecholestrogen on two distinct targets mediate embryo implantation in the mouse. Endocrinology 1998, 139:5235-5246.
59. Burdick H.O., Whitney R. Acceleration of the rate of passage of fertilized ova through the fallopian tubes of mice by massive injections of an estrogenic substance. Endocrinology 1937, 21:637-643.
60. Banik U.K., Pincus G. Estrogens and transport of ova in the rat. Proc Soc Exp Biol Med 1964, 116:1032-1034.
61. Greenwald G.S. Species differences in egg transport in response to exogenous estrogen. Anat Rec 1967, 157:163-172.
62. Takai Y., Tsutsumi O., Ikezuki Y., Hiroi H., Osuga Y., Yano T., et al. Estrogen receptor-mediated effects of bisphenol A on preimplantation mouse embryos. Biochem Biophys Res Commun 2000, 270:918-921.
63. Tan J., Paria B.C., Dey S.K., Das S.K. Differential uterine expression of estrogen and progesterone receptors correlates with uterine preparation for implantation and decidualization in the mouse. Endocrinology 1999, 140:5310-5321.
64. Mote P.A., Arnett-Mansfield R.L., Gava N., DeFazio A., Mulac-Jericevic B., Conneely O.M., et al. Overlapping and distinct expression of progesterone receptors A and B in mouse uterus and mammary gland during the estrous cycle. Endocrinology 2006, 147:5503-5512.
65. Milgrom E., Thi L., Atger M., Baulieu E.E. Mechanisms regulating the concentration and the conformation of progesterone receptor(s) in the uterus. J Biol Chem 1973, 248:6366-6374.
66. Parczyk K., Madjno R., Michna H., Nishino Y., Schneider M.R. Progesterone receptor repression by estrogens in rat uterine epithelial cells. J Steroid Biochem Mol Biol 1997, 63:309-316.
67. Tibbetts T.A., Mendoza-Meneses M., O'Malley B.W., Conneely O.M. Mutual and intercompartmental regulation of estrogen receptor and progesterone receptor expression in the mouse uterus. Biol Reprod 1998, 59:1143-1152.
68. McMaster M.T., Teng C.T., Dey S.K., Andrews G.K. Lactoferrin in the mouse uterus: analyses of the preimplantation period and regulation by ovarian steroids. Mol Endocrinol 1992, 6:101-111.
69. Ward P.P., Mendoza-Meneses M., Mulac-Jericevic B., Cunningham G.A., Saucedo-Cárdenas O., Teng C.T., et al. Restricted spatiotemporal expression of lactoferrin during murine embryonic development. Endocrinology 1999, 140:1852-1860.
70. Völkel W., Colnot T., Csanady G.A., Filser J.G., Dekant W. Metabolism and kinetics of bisphenol A in humans at low doses following oral administration. Chem Res Toxicol 2002, 15:1281-1287.
71. Völkel W., Bittner N., Dekant W. Quantitation of bisphenol A and bisphenol A glucuronide in biological samples by high performance liquid chromatography-tandem mass spectrometry. Drug Metab Dispos 2005, 33:1748-1757.
72. Kurebayashi H., Betsui H., Ohno Y. Disposition of a low dose of 14C-bisphenol A in male rats and main biliary excretion as BPA glucuronide. Toxicol Sci 2003, 73:17-25.
73. Thomas P., Dong J. 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 2006, 102:175-179.
74. Powel C.E., Soto A.M., Sonnenschein C. Identification and characterization of membrane estrogen receptor from MCF7 estrogen-target cells. J Steroid Biochem Mol Biol 2001, 7:97-108.
75. Aronica S.M., Kraus W.L., Katzenellenbogen B.S. Estrogen action via the cAMP signaling pathway: stimulation of adenylate cyclase and cAMP-regulated gene transcription. Proc Natl Acad Sci USA 1994, 91:8517-8521.
76. Le Mellay V., Grosse B., Lieberherr M. Phopholipase C β and membrane action of calcitriol and estradiol. J Biol Chem 1997, 272:11902-11907.
77. Pedram A., Razandi M., Aitkenhead M., Hughes C.C.W., Levin E.R. Integration of the non-genomic and genomic actions of estrogen. J Biol Chem 2002, 277:50768-50775.