Exposure to bisphenol A results in a decline in mouse spermatogenesis
Guo-Liang Zhang A E , Xi-Feng Zhang B E , Yan-Min Feng A , Lan Li A , Evanna Huynh C , Xiao-Feng Sun A , Zhong-Yi Sun D and Wei Shen A F
+ Author Affiliations
- Author Affiliations
A Key Laboratory of Animal Reproduction and Germplasm Enhancement in Universities of Shandong, Qingdao Agricultural University, Qingdao 266109, China.
B College of Biological and Pharmaceutical Engineering, Wuhan Polytechnic University, Wuhan 430023, China.
C Department of Animal and Poultry Science, University of Guelph, Guelph, Ontario N1G2W1, Canada.
D Daping Hospital, Third Military Medical University, Chongqing 400038, China.
E Equal first authors.
F Corresponding author. Email: shenwei427@163.com
Reproduction, Fertility and Development 25(6) 847-859 https://doi.org/10.1071/RD12159
Submitted: 19 May 2012 Accepted: 19 July 2012 Published: 4 September 2012
Abstract
Bisphenol A (BPA), a chemical used in many consumer products, interferes with the endocrine system of mammals, including humans. The aim of the present study was to investigate the effect of BPA on spermatogenesis and semen quality. The objective of this study was to assess the effects of BPA on mouse spermatogenesis. CD1 mice were used in all experiments. Mice were treated with different doses of BPA (0, 20 and 40 μg kg–1 day–1from postnatal Day (PND) 3 to PND21, PND 35 or PND49. After 5 weeks BPA treatment, oestrogen receptor α expression was increased in mouse testis, whereas the meiotic progression of germ cells was slowed. Thus, both the quality and quantity of spermatozoa were decreased in 7-week-old mice. However, BPA had no effect on DNA methylation of imprinted genes such as Igf2, Igf2r, Peg3 and H19, in germ cells. In addition, exposure of male mice to BPA resulted in abnormal offspring that were smaller with a low-quality pelage when they were 35 days old. In conclusion, BPA hampers spermatogenesis and the subsequent development of offspring.
Additional keywords: DNA methylation, meiosis, oestrogen receptor.
References
Al-Hiyasat, A. S., Darmani, H., and Elbetieha, A. M. (2002). Effects of bisphenol A on adult male mouse fertility. Eur. J. Oral Sci. 110, 163–167.| Effects of bisphenol A on adult male mouse fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktF2gtbk%3D&md5=9e87a6f4ae5c3587614995999700aac3CAS | 12013561PubMed |
Balasinor, N. H., D’Souza, R., Nanaware, P., Idicula-Thomas, S., Kedia-Mokashi, N., He, Z., and Dym, M. (2010). Effect of high intratesticular estrogen on global gene expression and testicular cell number in rats. Reprod. Biol. Endocrinol. 8, 72.
| Effect of high intratesticular estrogen on global gene expression and testicular cell number in rats.Crossref | GoogleScholarGoogle Scholar | 20573204PubMed |
Bouskine, A., Nebout, M., Brucker-Davis, F., Benahmed, M., and Fenichel, P. (2009). Low doses of bisphenol A promote human seminoma cell proliferation by activating PKA and PKG via a membrane G-protein-coupled estrogen receptor. Environ. Health Perspect. 117, 1053–1058.
| 1:CAS:528:DC%2BD1MXptVOjt78%3D&md5=7aed608fb621f57523a8443f0672c76aCAS | 19654912PubMed |
Bromer, J. G., Zhou, Y., Taylor, M. B., Doherty, L., and Taylor, H. S. (2010). Bisphenol-A exposure in utero leads to epigenetic alterations in the developmental programming of uterine estrogen response. FASEB J. 24, 2273–2280.
| Bisphenol-A exposure in utero leads to epigenetic alterations in the developmental programming of uterine estrogen response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptV2ktLY%3D&md5=c9b4da4d939867d193c5b8deee450371CAS | 20181937PubMed |
Brotons, J. A., Olea-Serrano, M. F., Villalobos, M., Pedraza, V., and Olea, N. (1995). Xenoestrogens released from lacquer coatings in food cans. Environ. Health Perspect. 103, 608–612.
| Xenoestrogens released from lacquer coatings in food cans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmslCntbg%3D&md5=17b61b2f56b0ecd02ea2e11875444aedCAS | 7556016PubMed |
Brouwer, A., Ahlborg, U. G., Van den Berg, M., Birnbaum, L. S., Boersma, E. R., Bosveld, B., Denison, M. S., Gray, L. E., Hagmar, L., Holene, E., et al. (1995). Functional aspects of developmental toxicity of polyhalogenated aromatic hydrocarbons in experimental animals and human infants. Eur. J. Pharmacol. 293, 1–40.
| Functional aspects of developmental toxicity of polyhalogenated aromatic hydrocarbons in experimental animals and human infants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlvFKns7c%3D&md5=1f614af30b7b210611b78baf6c5eb70cCAS | 7545581PubMed |
Calafat, A. M., Kuklenyik, Z., Reidy, J. A., Caudill, S. P., Ekong, J., and Needham, L. L. (2005). Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ. Health Perspect. 113, 391–395.
| Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvFOktrc%3D&md5=44cdb6bed7f8b1ce70b8bbaa8b7a4d97CAS | 15811827PubMed |
Calafat, A. M., Ye, X., Wong, L. Y., Reidy, J. A., and Needham, L. L. (2008). Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003–2004. Environ. Health Perspect. 116, 39–44.
| Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003–2004.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhs12nsrw%3D&md5=8fc6628c32b08ac1030b6d02344a24d8CAS | 18197297PubMed |
Can, A., Semiz, O., and Cinar, O. (2005). Bisphenol-A induces cell cycle delay and alters centrosome and spindle microtubular organization in oocytes during meiosis. Mol. Hum. Reprod. 11, 389–396.
| Bisphenol-A induces cell cycle delay and alters centrosome and spindle microtubular organization in oocytes during meiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvFegsLk%3D&md5=b1eec2a6044c9e781969303a9e996de3CAS | 15879462PubMed |
Carreau, S., and Hess, R. A. (2010). Oestrogens and spermatogenesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 1517–1535.
| Oestrogens and spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVaisr3K&md5=f41359a14369402f234a44e13a24cf05CAS | 20403867PubMed |
Champagne, F. A., Weaver, I. C., Diorio, J., Dymov, S., Szyf, M., and Meaney, M. J. (2006). 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 147, 2909–2915.
| Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xlt1Wgsr0%3D&md5=f3468cf05f4ca4c008b62a650bc239caCAS | 16513834PubMed |
Chao, H. H., Zhang, X. F., Chen, B., Pan, B., Zhang, L. J., Li, L., Sun, X. F., Shi, Q. H., and Shen, W. (2012). Bisphenol A exposure modifies methylation of imprinted genes in mouse oocytes via the estrogen receptor signaling pathway. Histochem. Cell Biol. 137, 249–259.
| Bisphenol A exposure modifies methylation of imprinted genes in mouse oocytes via the estrogen receptor signaling pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpslKrsQ%3D%3D&md5=ca43430b3284d8189521d2308d5e00b9CAS | 22131059PubMed |
D’Cruz, S. C., Jubendradass, R., and Mathur, P. P. (2012). Bisphenol A induces oxidative stress and decreases levels of insulin receptor substrate 2 and glucose transporter 8 in rat testis. Reprod. Sci. 19, 163–172.
| Bisphenol A induces oxidative stress and decreases levels of insulin receptor substrate 2 and glucose transporter 8 in rat testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltlGrsr4%3D&md5=59a41ce7e705a9f82b8c4341671ca312CAS | 22101236PubMed |
Della Seta, D., Minder, I., Dessi-Fulgheri, F., and Farabollini, F. (2005). Bisphenol-A exposure during pregnancy and lactation affects maternal behavior in rats. Brain Res. Bull. 65, 255–260.
| Bisphenol-A exposure during pregnancy and lactation affects maternal behavior in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtlSrtrw%3D&md5=ec9919a57a94b4583b406b24cd64a732CAS | 15811589PubMed |
Dolinoy, D. C., Huang, D., and Jirtle, R. L. (2007). Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc. Natl Acad. Sci. USA 104, 13 056–13 061.
| Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1GhsL8%3D&md5=e567ceae095a6c9c72cd2e2413238f36CAS |
Dong, H. S., Li, L., Zhai, X. W., Sun, L. L., Zhang, P., Song, Z. H., Li, Z. B., Pan, Q. J., and Shen, W. (2009). Premeiotic fetal murine germ cells cultured in vitro form typical oocyte-like cells but do not progress through meiosis. Theriogenology 72, 219–231.
| Premeiotic fetal murine germ cells cultured in vitro form typical oocyte-like cells but do not progress through meiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsFSjtrg%3D&md5=40887f76273fb02cece3a450e2868f2aCAS | 19361852PubMed |
Eichenlaub-Ritter, U., Vogt, E., Cukurcam, S., Sun, F., Pacchierotti, F., and Parry, J. (2008). Exposure of mouse oocytes to bisphenol A causes meiotic arrest but not aneuploidy. Mutat. Res. 651, 82–92.
| 1:CAS:528:DC%2BD1cXitlGmt7s%3D&md5=9ae347197f188ac430807dbaa28cb1b0CAS | 18096426PubMed |
Enmark, E., and Gustafsson, J. A. (1999). Oestrogen receptors: an overview. J. Intern. Med. 246, 133–138.
| Oestrogen receptors: an overview.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtlCmtb8%3D&md5=d7d56086dcdb94aa498b43eb18b3da46CAS | 10447781PubMed |
George, O., Bryant, B. K., Chinnasamy, R., Corona, C., Arterburn, J. B., and Shuster, C. B. (2008). Bisphenol A directly targets tubulin to disrupt spindle organization in embryonic and somatic cells. ACS Chem. Biol. 3, 167–179.
| Bisphenol A directly targets tubulin to disrupt spindle organization in embryonic and somatic cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Sltrk%3D&md5=48ff2a702d0ccd0d9ee9d1a33d92fb82CAS | 18225860PubMed |
Gould, J. C., Leonard, L. S., Maness, S. C., Wagner, B. L., Conner, K., Zacharewski, T., Safe, S., McDonnell, D. P., and Gaido, K. W. (1998). BisphenolA interacts with the estrogen receptor alpha in a distinct manner from estradiol. Mol. Cell. Endocrinol. 142, 203–214.
| BisphenolA interacts with the estrogen receptor alpha in a distinct manner from estradiol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkvFOksLY%3D&md5=24fd9218703e7f23a1e6def5d6c2bd0dCAS | 9783916PubMed |
Hall, J. M., and McDonnell, D. P. (2005). Coregulators in nuclear estrogen receptor action: from concept to therapeutic targeting. Mol. Interv. 5, 343–357.
| Coregulators in nuclear estrogen receptor action: from concept to therapeutic targeting.Crossref | GoogleScholarGoogle Scholar | 16394250PubMed |
Hess, R. A. (2003). Estrogen in the adult male reproductive tract: a review. Reprod. Biol. Endocrinol. 1, 52.
| Estrogen in the adult male reproductive tract: a review.Crossref | GoogleScholarGoogle Scholar | 12904263PubMed |
Hirasawa, R., and Feil, R. (2010). Genomic imprinting and human disease. Essays Biochem. 48, 187–200.
| Genomic imprinting and human disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlKgsbzK&md5=8bf364dcb61346c43306ec12d2d71f6fCAS | 20822494PubMed |
Ho, S. M., Tang, W. Y., Belmonte de Frausto, J., and Prins, G. S. (2006). Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant 4. Cancer Res. 66, 5624–5632.
| Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant 4.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltFyjt70%3D&md5=2cefa861aac3efdbc165fb923ea8d2aeCAS | 16740699PubMed |
Hunt, P. A., Koehler, K. E., Susiarjo, M., Hodges, C. A., Ilagan, A., Voigt, R. C., Thomas, S., Thomas, B. F., and Hassold, T. J. (2003). Bisphenol a exposure causes meiotic aneuploidy in the female mouse. Curr. Biol. 13, 546–553.
| Bisphenol a exposure causes meiotic aneuploidy in the female mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXislChsb4%3D&md5=041e4d7ba9803b017981b61a7d84f9b0CAS | 12676084PubMed |
Ikezuki, Y., Tsutsumi, O., Takai, Y., Kamei, Y., and Taketani, Y. (2002). Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum. Reprod. 17, 2839–2841.
| Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XptFOrtb0%3D&md5=681ff0e5a6f5982f3af3025da3f8dab6CAS | 12407035PubMed |
Joseph, A., Shur, B. D., and Hess, R. A. (2011). Estrogen, efferent ductules, and the epididymis. Biol. Reprod. 84, 207–217.
| Estrogen, efferent ductules, and the epididymis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVelsbo%3D&md5=09b47aa0e2bc67cd1939a38e592c9de1CAS | 20926801PubMed |
Kipp, J. L., Kilen, S. M., Woodruff, T. K., and Mayo, K. E. (2007). Activin regulates estrogen receptor gene expression in the mouse ovary. J. Biol. Chem. 282, 36 755–36 765.
| Activin regulates estrogen receptor gene expression in the mouse ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVSgt7zO&md5=8fdf135f5df0896db08812455842d4aaCAS |
Kuiper, G. G., Carlsson, B., Grandien, K., Enmark, E., Haggblad, J., Nilsson, S., and Gustafsson, J. A. (1997). Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138, 863–870.
| Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXht1OksrY%3D&md5=6d1dc8b08e8d114eb95bc2c09830fa5eCAS | 9048584PubMed |
Kundakovic, M., and Champagne, F. A. (2011). Epigenetic perspective on the developmental effects of bisphenol A. Brain Behav. Immun. 25, 1084–1093.
| Epigenetic perspective on the developmental effects of bisphenol A.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXovFOis7s%3D&md5=be90aeea63b71d051a785d47e6899ff2CAS | 21333735PubMed |
Lagos-Cabré, R., and Moreno, R. D. (2012). Contribution of environmental pollutants to male infertily: A working model of germ cell apoptosis induced by plasticizers. Biol. Res. 45, 5–14.
| Contribution of environmental pollutants to male infertily: A working model of germ cell apoptosis induced by plasticizers.Crossref | GoogleScholarGoogle Scholar | 22688978PubMed |
La Salle, S., Mertineit, C., Taketo, T., Moens, P. B., Bestor, T. H., and Trasler, J. M. (2004). Windows for sex-specific methylation marked by DNA methyltransferase expression profiles in mouse germ cells. Dev. Biol. 268, 403–415.
| Windows for sex-specific methylation marked by DNA methyltransferase expression profiles in mouse germ cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXivVKns74%3D&md5=1f4faf5ec588b95b43cd1413d7994d31CAS | 15063176PubMed |
Li, E., Beard, C., and Jaenisch, R. (1993). Role for DNA methylation in genomic imprinting. Nature 366, 362–365.
| Role for DNA methylation in genomic imprinting.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlsFCm&md5=fc586279c6c5a623eef319a3755c9358CAS | 8247133PubMed |
Li, L., Keverne, E. B., Aparicio, S. A., Ishino, F., Barton, S. C., and Surani, M. A. (1999). Regulation of maternal behavior and offspring growth by paternally expressed Peg3. Science 284, 330–334.
| Regulation of maternal behavior and offspring growth by paternally expressed Peg3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitlOgt7Y%3D&md5=0e57a80c3a9e847f1a4f462a1b6745fcCAS | 10195900PubMed |
Li, X., and Rahman, N. (2008). Impact of androgen/estrogen ratio: lessons learned from the aromatase over-expression mice. Gen. Comp. Endocrinol. 159, 1–9.
| Impact of androgen/estrogen ratio: lessons learned from the aromatase over-expression mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1ensL7N&md5=264282f6297e95aa06c6a0aa96fef6d4CAS | 18762187PubMed |
Maffini, M. V., Rubin, B. S., Sonnenschein, C., and Soto, A. M. (2006). Endocrine disruptors and reproductive health: the case of bisphenol-A. Mol. Cell. Endocrinol. 254–255, 179–186.
| Endocrine disruptors and reproductive health: the case of bisphenol-A.Crossref | GoogleScholarGoogle Scholar | 16781053PubMed |
Nagel, S. C., vom Saal, F. S., Thayer, K. A., Dhar, M. G., Boechler, M., and Welshons, W. V. (1997). Relative binding affinity-serum modified access (RBA-SMA) assay predicts the relative in vivo bioactivity of the xenoestrogens bisphenol A and octylphenol. Environ. Health Perspect. 105, 70–76.
| Relative binding affinity-serum modified access (RBA-SMA) assay predicts the relative in vivo bioactivity of the xenoestrogens bisphenol A and octylphenol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXitleitLY%3D&md5=570d8b2d45fb9515b8a8c45047e5fa81CAS | 9074884PubMed |
Nakamura, K., Itoh, K., Yaoi, T., Fujiwara, Y., Sugimoto, T., and Fushiki, S. (2006). Murine neocortical histogenesis is perturbed by prenatal exposure to low doses of bisphenol A. J. Neurosci. Res. 84, 1197–1205.
| Murine neocortical histogenesis is perturbed by prenatal exposure to low doses of bisphenol A.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtF2rs7rL&md5=2241151518754a5df3c993626a3e6e12CAS | 16902998PubMed |
Nakamura, K., Itoh, K., Sugimoto, T., and Fushiki, S. (2007). Prenatal exposure to bisphenol A affects adult murine neocortical structure. Neurosci. Lett. 420, 100–105.
| Prenatal exposure to bisphenol A affects adult murine neocortical structure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtVKjur8%3D&md5=2a2486b8fdf3dfab8a1a708630f7550fCAS | 17532137PubMed |
Newbold, R. R., Hanson, R. B., Jefferson, W. N., Bullock, B. C., Haseman, J., and McLachlan, J. A. (2000). Proliferative lesions and reproductive tract tumors in male descendants of mice exposed developmentally to diethylstilbestrol. Carcinogenesis 21, 1355–1363.
| Proliferative lesions and reproductive tract tumors in male descendants of mice exposed developmentally to diethylstilbestrol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXltF2qsLk%3D&md5=eba212e21e63a59d6d8d243ba2b6e534CAS | 10874014PubMed |
Nielsen, M., Bjornsdottir, S., Hoyer, P. E., and Byskov, A. G. (2000). Ontogeny of oestrogen receptor alpha in gonads and sex ducts of fetal and newborn mice. J. Reprod. Fertil. 118, 195–204.
| 1:CAS:528:DC%2BD3cXpsl2mtw%3D%3D&md5=6a6c6b45e968bd752f2c50f09ede1045CAS | 10793642PubMed |
Ouchi, K., and Watanabe, H. (2002). Measurement of bisphenol A in human urine using liquid chromatography with multi-channel coulometric electrochemical detection. J. Chromatogr. B 780, 365–370.
| Measurement of bisphenol A in human urine using liquid chromatography with multi-channel coulometric electrochemical detection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xptlans7g%3D&md5=83aa265159cb9e6b64f7e86d31de487aCAS |
Palanza, P. L., Howdeshell, K. L., Parmigiani, S., and vom Saal, F. S. (2002). Exposure to a low dose of bisphenol A during fetal life or in adulthood alters maternal behavior in mice. Environ. Health Perspect. 110, 415–422.
| Exposure to a low dose of bisphenol A during fetal life or in adulthood alters maternal behavior in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltlWjsbs%3D&md5=cea8731a4910e13b53bfb0caf87d5cf2CAS | 12060838PubMed |
Palanza, P., Gioiosa, L., vom Saal, F. S., and Parmigiani, S. (2008). Effects of developmental exposure to bisphenol A on brain and behavior in mice. Environ. Res. 108, 150–157.
| Effects of developmental exposure to bisphenol A on brain and behavior in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Snt7jE&md5=a001c3d852e511bb550ab2840b28c5bfCAS | 18949834PubMed |
Pauler, F. M., and Barlow, D. P. (2006). Imprinting mechanisms: it only takes two. Genes Dev. 20, 1203–1206.
| Imprinting mechanisms: it only takes two.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltVyrtLk%3D&md5=f04171c83e43f4c0c179349f1f8eddbaCAS | 16702397PubMed |
Pfeiffer, E., Rosenberg, B., Deuschel, S., and Metzler, M. (1997). Interference with microtubules and induction of micronuclei in vitro by various bisphenols. Mutat. Res. 390, 21–31.
| 1:CAS:528:DyaK2sXit1egtrk%3D&md5=4a14bed36d23b9d07b3eaa2d90683460CAS | 9150749PubMed |
Reik, W., and Walter, J. (2001). Genomic imprinting: parental influence on the genome. Nat. Rev. Genet. 2, 21–32.
| Genomic imprinting: parental influence on the genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisVGjs70%3D&md5=f25b8ce87268a4a7cc8f7ffa22b0e288CAS | 11253064PubMed |
Robb, G. W., Amann, R. P., and Killian, G. J. (1978). Daily sperm production and epididymal sperm reserves of pubertal and adult rats. J. Reprod. Fertil. 54, 103–107.
| Daily sperm production and epididymal sperm reserves of pubertal and adult rats.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1M%2FltVegtg%3D%3D&md5=fa5604eb2f607b2867cae0246087b069CAS | 712697PubMed |
Routledge, E. J., White, R., Parker, M. G., and Sumpter, J. P. (2000). Differential effects of xenoestrogens on coactivator recruitment by estrogen receptor (ER) alpha and ER beta. J. Biol. Chem. 275, 35 986–35 993.
| Differential effects of xenoestrogens on coactivator recruitment by estrogen receptor (ER) alpha and ER beta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosVSktb8%3D&md5=e08ce2f7fa76f3330f3f2327733eb28eCAS |
Schönfelder, G., Wittfoht, W., Hopp, H., Talsness, C. E., Paul, M., and Chahoud, I. (2002). Parent bisphenol A accumulation in the human maternal–fetal–placental unit. Environ. Health Perspect. 110, 703–707.
| Parent bisphenol A accumulation in the human maternal–fetal–placental unit.Crossref | GoogleScholarGoogle Scholar |
Shi, M., Li, X. X., Song, B., Long, Y., Gui, Y. T., and Cai, Z. M. (2006). Identification of human testicular spermatogenic cells at diferent stages. J. Peking Univ. 38, 441–443.
Smita, S., Doshi, T., and Vanage, G. (2009). Neonatal exposure of male rats to bisphenol A impairs fertility and expression of sertoli cell junctional proteins in the testis. Toxicology 265, 56–67.
Song, Z., Min, L., Pan, Q., Shi, Q., and Shen, W. (2009). Maternal imprinting during mouse oocyte growth in vivo and in vitro. Biochem. Biophys. Res. Commun. 387, 800–805.
| Maternal imprinting during mouse oocyte growth in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVSntrvE&md5=838aa7288a82ae2d7a0afaeb9cc9eb55CAS | 19646963PubMed |
Surani, M. A. (1998). Imprinting and the initiation of gene silencing in the germ line. Cell 93, 309–312.
| Imprinting and the initiation of gene silencing in the germ line.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtFCjt7s%3D&md5=667cc76bc6bf3fee8bfa2afa0f74c215CAS | 9590162PubMed |
Tanikawa, M., Harada, T., Mitsunari, M., Onohara, Y., Iwabe, T., and Terakawa, N. (1998). Expression of c-kit messenger ribonucleic acid in human oocyte and presence of soluble c-kit in follicular fluid. J. Clin. Endocrinol. Metab. 83, 1239–1242.
| Expression of c-kit messenger ribonucleic acid in human oocyte and presence of soluble c-kit in follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitlynt74%3D&md5=1392b9e2eefdd59864c3b9249c840ebcCAS | 9543148PubMed |
Tian, H., Liu, Z., and Bai, Y. (2004). The methods often used for evaluating the mammalian sperm quality. J. Econ. Anim. 204, 198–201.
Trevor, G. C., John, A., Jacques, A., Gordon, H. W., Baker, C., Barratt, L. R., Hermanm, M. B., et al. (2010). ‘WHO laboratory manual for the examination and processing of human semen. 5th ed.’ (World Health Organization: Switzerland.)
Uzumcu, M., and Zachow, R. (2007). Developmental exposure to environmental endocrine disruptors: consequences within the ovary and on female reproductive function. Reprod. Toxicol. 23, 337–352.
| Developmental exposure to environmental endocrine disruptors: consequences within the ovary and on female reproductive function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksFegtLc%3D&md5=c3c5eb95f1cbcd2d58ed4142819b24e2CAS | 17140764PubMed |
Vandenberg, L. N., Hauser, R., Marcus, M., Olea, N., and Welshons, W. V. (2007). Human exposure to bisphenol A (BPA). Reprod. Toxicol. 24, 139–177.
| Human exposure to bisphenol A (BPA).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVCisL%2FL&md5=c2a4bc30cb54d3df44b7593fc383b7c7CAS | 17825522PubMed |
Veurink, M., Koster, M., and Berg, L. T. (2005). The history of DES, lessons to be learned. Pharm. World Sci. 27, 139–143.
| The history of DES, lessons to be learned.Crossref | GoogleScholarGoogle Scholar | 16096877PubMed |
Vom Saal, F. S., Cooke, P. S., Buchanan, D. L., Palanza, P., Thayer, K. A., Nagel, S. C., Parmigiani, S., and Welshons, W. V. (1998). A physiologically based approach to the study of bisphenol A and other estrogenic chemicals on the size of reproductive organs, daily sperm production, and behavior. Toxicol. Ind. Health 14, 239–260.
| 1:CAS:528:DyaK1cXjtFalurg%3D&md5=7caae87102d3be661e8f349cd8d6dbfcCAS | 9460178PubMed |
Westberry, J. M., Trout, A. L., and Wilson, M. E. (2010). Epigenetic regulation of estrogen receptor alpha gene expression in the mouse cortex during early postnatal development. Endocrinology 151, 731–740.
| Epigenetic regulation of estrogen receptor alpha gene expression in the mouse cortex during early postnatal development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVOqu7w%3D&md5=eb2198448b1f9ba9403928b2125c2384CAS | 19966177PubMed |
Xiao, S., Diao, H., Smith, M. A., Song, X., and Ye, X. (2011). Preimplantation exposure to bisphenol A (BPA) affects embryo transport, preimplantation embryo development, and uterine receptivity in mice. Reprod. Toxicol. 32, 434–441.
| 21907787PubMed |
Yamamoto, T., Yasuhara, A., Shiraishi, H., and Nakasugi, O. (2001). Bisphenol A in hazardous waste landfill leachates. Chemosphere 42, 415–418.
| Bisphenol A in hazardous waste landfill leachates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXoslOqu70%3D&md5=7eae39c965b9859c72dcc1ec2d8c2d88CAS | 11100793PubMed |
Yaoi, T., Itoh, K., Nakamura, K., Ogi, H., Fujiwara, Y., and Fushiki, S. (2008). Genome-wide analysis of epigenomic alterations in fetal mouse forebrain after exposure to low doses of bisphenol A. Biochem. Biophys. Res. Commun. 376, 563–567.
| Genome-wide analysis of epigenomic alterations in fetal mouse forebrain after exposure to low doses of bisphenol A.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1ensrfL&md5=c8ff416899c3427a3a8b0e663266100aCAS | 18804091PubMed |
Zhang, P., Chao, H. H., Sun, X., Li, L., Shi, Q., and Shen, W. (2010). Murine folliculogenesis in vitro is stage-specifically regulated by insulin via the Akt signaling pathway. Histochem. Cell Biol. 134, 75–82.
| Murine folliculogenesis in vitro is stage-specifically regulated by insulin via the Akt signaling pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVaitr4%3D&md5=0e13798b3b1a236a10cdecdf68437edeCAS | 20495820PubMed |
