Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-19T22:58:31.483Z Has data issue: false hasContentIssue false

Comparison of the effects of BPA and BPAF on oocyte spindle assembly and polar body release in mice

Published online by Cambridge University Press:  30 April 2015

Kei Nakano
Affiliation:
Laboratory of Animal Reproduction and Development, Graduate School of Agricultural Science, Tohoku University, Sendai 981–8555, Japan.
Manami Nishio
Affiliation:
Laboratory of Animal Reproduction and Development, Graduate School of Agricultural Science, Tohoku University, Sendai 981–8555, Japan.
Norio Kobayashi
Affiliation:
Laboratory of Animal Reproduction and Development, Graduate School of Agricultural Science, Tohoku University, Sendai 981–8555, Japan.
Yuuki Hiradate
Affiliation:
Laboratory of Animal Reproduction and Development, Graduate School of Agricultural Science, Tohoku University, Sendai 981–8555, Japan.
Yumi Hoshino
Affiliation:
Laboratory of Animal Reproduction and Development, Graduate School of Agricultural Science, Tohoku University, Sendai 981–8555, Japan.
Eimei Sato
Affiliation:
Laboratory of Animal Reproduction and Development, Graduate School of Agricultural Science, Tohoku University, Sendai 981–8555, Japan.
Kentaro Tanemura*
Affiliation:
Laboratory of Animal Reproduction and Development, Graduate School of Agricultural Science, Tohoku University, Sendai 981-8555, Japan.
*
All correspondence to: Kentaro Tanemura. Laboratory of Animal Reproduction and Development, Graduate School of Agricultural Science, Tohoku University, Sendai 981-8555, Japan. Tel:/Fax: +81 22 717 8687. E-mail: [email protected]

Summary

Bisphenol AF (BPAF), a homolog of bisphenol A (BPA), is a widely used environmental chemical that has adverse effects on reproduction. The aim of this study was to analyse the effects of BPA and BPAF exposure on oocyte maturation in vitro. Oocytes were cultured in the presence of BPA or BPAF (2, 20, 50 or 100 μg/ml) for 18 h. At concentrations of 50 and 100 μg/ml, BPA and BPAF inhibited oocyte maturation, with BPAF treatment causing a sharp decrease in the number of oocytes reaching maturity. Oocytes were exposed to BPA or BPAF at 2 μg/ml and cultured for different durations (6, 9, 12, 15 or 18 h). Both BPAF and BPA caused a cell cycle delay under these conditions. Oocytes cultured in the presence of BPA or BPAF (50 μg/ml) for 21 h were tested for the localization of α-tubulin and MAD2 using immunofluorescence. High concentrations of BPAF induced cell cycle arrest through the activation of the spindle assembly checkpoint. After 12 h of culture in BPAF (50 μg/ml), oocytes were transferred to control medium for 9 h. Only 63.3% oocytes treated in this manner progressed to metaphase II (MII). Oocytes exposed to high doses of BPA experienced a cell cycle delay, but managed to progress to MII when the culture period was prolonged. In addition, MAD2 was localized in the cytoplasm of these oocytes. In conclusion, both BPAF and BPA exposure affected oocyte maturation, however BPAF and BPA have differential effects on SAC activity.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Akahori, Y., Nakai, M., Yamasaki, K., Takatsuki, M., Shimohigashi, Y. & Ohtaki, M. (2008). Relationship between the results of in vitro receptor binding assay to human estrogen receptor alpha and in vivo uterotrophic assay: comparative study with 65 selected chemicals. Toxicol. In Vitro 22, 225–31.CrossRefGoogle ScholarPubMed
Bae, B., Jeong, J.H. & Lee, S.L. (2002). The quantification and characterization of endocrine disruptor bisphenol-A leaching from epoxy resin. Water Sci. Technol. 46, 381–7.Google Scholar
Bermudez, D.S., Gray, L.E. Jr & Wilson, V.S. (2010). Modeling the interaction of binary and ternary mixtures of estradiol with bisphenol A and bisphenol AF in an in vitro estrogen-mediated transcriptional activation assay (T47D-KBluc). Toxicol. Sci. 116, 477–87.CrossRefGoogle Scholar
Biedermann, S., Tschudin, P. & Grob, K. (2010). Transfer of bisphenol A from thermal printer paper to the skin. Anal. Bioanal. Chem. 398, 571–6.Google Scholar
Blair, R.M., Fang, H., Branham, W.S., Hass, B.S., Dial, S.L., Moland, C.L., Tong, W., Shi, L., Perkins, R. & Sheehan, D.M. (2000). The estrogen receptor relative binding affinities of 188 natural and xenochemicals: structural diversity of ligands. Toxicol. Sci. 54, 138–53.Google Scholar
Bouskine, A., Nebout, M., Brucker-Davis, F., Benahmed, M. & 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, 1053–8.Google Scholar
Can, A., Semiz, O. & Cinar, O. (2005). Bisphenol-A induces cell cycle delay and alters centrosome and spindle microtubular organization in oocytes during meiosis. Mol. Hum. Reprod. 11, 389–96.Google Scholar
Carwile, J.L. & Michels, K.B. (2011). Urinary bisphenol A and obesity: NHANES 2003–2006. Environ. Res. 111, 825–30.Google Scholar
Ehrlich, S., Williams, P.L., Missmer, S.A., Flaws, J.A., Ye, X., Calafat, A.M., Petrozza, J.C., Wright, D. & Hauser, R. (2012). Urinary bisphenol A concentrations and early reproductive health outcomes among women undergoing IVF. Hum. Reprod. 27, 3583–92.Google Scholar
Eichenlaub-Ritter, U., Vogt, E., Cukurcam, S., Sun, F., Pacchierotti, F. & Parry, J. (2008). Exposure of mouse oocytes to bisphenol A causes meiotic arrest but not aneuploidy. Mutat. Res. 651 (1–2), 8292.Google Scholar
Gould, J.C., Leonard, L.S., Maness, S.C., Wagner, B.L., Conner, K., Zacharewski, T., Safe, S., McDonnell, D.P. & Gaido, K.W. (1998). Bisphenol A interacts with the estrogen receptor alpha in a distinct manner from estradiol. Mol. Cell. Endocrinol. 142, 203–14.Google Scholar
Homer, H.A., McDougall, A., Levasseur, M., Murdoch, A.P. & Herbert, M. (2005). Mad2 is required for inhibiting securin and cyclin B degradation following spindle depolymerisation in meiosis I mouse oocytes. Reproduction 130, 829–43.CrossRefGoogle ScholarPubMed
Hoshino, Y. & Sato, E. (2008). Protein kinase B (PKB/Akt) is required for the completion of meiosis in mouse oocytes. Dev. Biol. 314, 215–23.Google Scholar
Hoyt, M.A. (2001). A new view of the spindle checkpoint. J. Cell Biol. 154, 909–11.Google Scholar
Hunt, P.A., Koehler, K.E., Susiarjo, M., Hodges, C.A., Ilagan, A., Voigt, R.C., Thomas, S., Thomas, B.F. & Hassold, T.J. (2003). Bisphenol a exposure causes meiotic aneuploidy in the female mouse. Curr. Biol. 13, 546–53.CrossRefGoogle ScholarPubMed
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, 2839–41.CrossRefGoogle ScholarPubMed
Ishikawa, S., Machida, R., Hiraga, K., Hiradate, Y., Suda, Y. & Tanemura, K. (2014). Hanging drop monoculture for selection of optimal antioxidants during in vitro maturation of porcine oocytes. Reprod. Domest. Anim. 49, e2630.Google Scholar
Joskow, R., Barr, D.B., Barr, J.B., Calafat, A.M., Needham, L.L. & Rubin, C. (2006). Exposure to bisphenol A from bis-glycidyl dimethacrylate-based dental sealants. J. Am. Dent. Assoc. 137, 353–62.Google Scholar
Kallio, M., Eriksson, J.E. & Gorbsky, G.J. (2000). Differences in spindle association of the mitotic checkpoint protein Mad2 in mammalian spermatogenesis and oogenesis. Dev. Biol. 225, 112–23.Google Scholar
Kim, H.S., Han, S.Y., Yoo, S.D., Lee, B.M. & Park, K.L. (2001). Potential estrogenic effects of bisphenol-A estimated by in vitro and in vivo combination assays. J. Toxicol. Sci. 26, 111–8.Google Scholar
Kitamura, S., Suzuki, T., Sanoh, S., Kohta, R., Jinno, N., Sugihara, K., Yoshihara, S., Fujimoto, N., Watanabe, H. & Ohta, S. (2005). Comparative study of the endocrine-disrupting activity of bisphenol A and 19 related compounds. Toxicol. Sci. 84, 249–59.CrossRefGoogle Scholar
Kuiper, G.G., Lemmen, J.G., Carlsson, B., Corton, J.C., Safe, S.H., van der Saag, P.T., van der Burg, B. & Gustafsson, J.A. (1998). Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139, 4252–63.Google Scholar
Laws, S.C., Carey, S.A., Ferrell, J.M., Bodman, G.J. & Cooper, R.L. (2000). Estrogenic activity of octylphenol, nonylphenol, bisphenol A and methoxychlor in rats. Toxicol. Sci. 54, 154–67.Google Scholar
Lenie, S., Cortvrindt, R., Eichenlaub-Ritter, U. & Smitz, J. (2008). Continuous exposure to bisphenol A during in vitro follicular development induces meiotic abnormalities. Mutat. Res. 651 (1–2), 7181.Google Scholar
Liu, X., Matsushima, A., Okada, H., Tokunaga, T., Isozaki, K. & Shimohigashi, Y. (2007). Receptor binding characteristics of the endocrine disruptor bisphenol A for the human nuclear estrogen-related receptor gamma. Chief and corroborative hydrogen bonds of the bisphenol A phenol-hydroxyl group with Arg316 and Glu275 residues. FEBS J. 274, 6340–51.Google Scholar
Ma, W., Zhang, D., Hou, Y., Li, Y.H., Sun, Q.Y., Sun, X.F. & Wang, W.H. (2005). Reduced expression of MAD2, BCL2, and MAP kinase activity in pig oocytes after in vitro aging are associated with defects in sister chromatid segregation during meiosis II and embryo fragmentation after activation. Biol. Reprod. 72, 373–83.Google Scholar
Machtinger, R., Combelles, C.M., Missmer, S.A., Correia, K.F., Williams, P., Hauser, R. & Racowsky, C. (2013). Bisphenol-A and human oocyte maturation in vitro . Hum. Reprod. 28, 2735–45.CrossRefGoogle ScholarPubMed
Maney, T., Ginkel, L.M., Hunter, A.W. & Wordeman, L. (2000). The kinetochore of higher eucaryotes: a molecular view. Int. Rev. Cytol. 194, 67131.Google Scholar
Matsushima, A., Kakuta, Y., Teramoto, T., Koshiba, T., Liu, X., Okada, H., Tokunaga, T., Kawabata, S., Kimura, M. & Shimohigashi, Y. (2007). Structural evidence for endocrine disruptor bisphenol A binding to human nuclear receptor ERR gamma. J. Biochem. 142, 517–24.Google Scholar
Matsushima, A., Liu, X., Okada, H., Shimohigashi, M. & Shimohigashi, Y. (2010). Bisphenol AF is a full agonist for the estrogen receptor ERalpha but a highly specific antagonist for ERbeta. Environ. Health Perspect. 118, 1267–72.Google Scholar
Myers, J.P., vom Saal, F.S., Akingbemi, B.T., Arizono, K., Belcher, S., Colborn, T., Chahoud, I., Crain, D.A., Farabollini, F., Guillette, L.J. Jr, Hassold, T., Ho, S.M., Hunt, P.A., Iguchi, T., Jobling, S., Kanno, J., Laufer, H., Marcus, M., McLachlan, J.A., Nadal, A., Oehlmann, J., Olea, N., Palanza, P., Parmigiani, S., Rubin, B.S., Schoenfelder, G., Sonnenschein, C., Soto, A.M., Talsness, C.E., Taylor, J.A., Vandenberg, L.N., Vandenbergh, J.G., Vogel, S., Watson, C.S., Welshons, W.V. & Zoeller, R.T. (2009). Why public health agencies cannot depend on good laboratory practices as a criterion for selecting data: the case of bisphenol A. Environ. Health Perspect. 117, 309–15.Google Scholar
Nagel, S.C., vom Saal, F.S., Thayer, K.A., Dhar, M.G., Boechler, M. & 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, 70–6.Google Scholar
National Toxicology Program (NTP) (2008). Chemical information profile for bisphenol AF [CAS No. 1478–61–1], supporting nomination for toxicological evaluation by the National Toxicology Program. from http://ntp.niehs.nih.gov/ntp/htdocs/Chem_Background/ExSumPdf/BisphenolAF_093008_508.pdf Google Scholar
Niault, T., Hached, K., Sotillo, R., Sorger, P.K., Maro, B., Benezra, R. & Wassmann, K. (2007). Changing Mad2 levels affects chromosome segregation and spindle assembly checkpoint control in female mouse meiosis I. PLoS One 2, e1165.CrossRefGoogle ScholarPubMed
Nishio, M., Hoshino, Y., Tanemura, K. & Sato, E. (2014). Effect of single-oocyte culture system on in vitro maturation and developmental competence in mice. Reprod. Med. Biol. 13, 153–9.Google Scholar
Okada, H., Tokunaga, T., Liu, X., Takayanagi, S., Matsushima, A. & Shimohigashi, Y. (2008). Direct evidence revealing structural elements essential for the high binding ability of bisphenol A to human estrogen-related receptor-gamma. Environ. Health Perspect. 116, 32–8.Google Scholar
Pennie, W.D., Aldridge, T.C. & Brooks, A.N. (1998). Differen-tial activation by xenoestrogens of ER alpha and ER beta when linked to different response elements. J. Endocrinol. 158, R1114.Google Scholar
Pfeiffer, E., Rosenberg, B., Deuschel, S. & Metzler, M. (1997). Interference with microtubules and induction of micronuclei in vitro by various bisphenols. Mutat. Res. 390 (1–2), 2131.Google Scholar
Sasaki, N., Okuda, K., Kato, T., Kakishima, H., Okuma, H., Abe, K., Tachino, H., Tuchida, K. & Kubono, K. (2005). Salivary bisphenol-A levels detected by ELISA after restoration with composite resin. J. Mater. Sci. Mater. Med. 16, 297300.CrossRefGoogle ScholarPubMed
Shannon, K.B., Canman, J.C. & Salmon, E.D. (2002). Mad2 and BubR1 function in a single checkpoint pathway that responds to a loss of tension. Mol. Biol. Cell. 13, 3706–19.Google Scholar
Sheeler, C.Q., Dudley, M.W. & Khan, S.A. (2000). Environmental estrogens induce transcriptionally active estrogen receptor dimers in yeast: activity potentiated by the coactivator RIP140. Environ. Health Perspect. 108, 97103.CrossRefGoogle ScholarPubMed
Stout, M. (2008). National Toxicology Program http://ntp.niehs.nih.gov/ Google Scholar
Takayanagi, S., Tokunaga, T., Liu, X., Okada, H., Matsushima, A. & Shimohigashi, Y. (2006). Endocrine disruptor bisphenol A strongly binds to human estrogen-related receptor gamma (ERRgamma) with high constitutive activity. Toxicol. Lett. 167, 95105.Google Scholar
Wang, W.H. & Sun, Q.Y. (2006). Meiotic spindle, spindle checkpoint and embryonic aneuploidy. Front. Biosci. 11, 620–36.Google Scholar
Wassmann, K., Niault, T. & Maro, B. (2003). Metaphase I arrest upon activation of the Mad2-dependent spindle checkpoint in mouse oocytes. Curr. Biol. 13, 1596–608.CrossRefGoogle ScholarPubMed
Yang, Y., Yin, J., Yang, Y., Zhou, N., Zhang, J., Shao, B. & Wu, Y. (2012). Determination of bisphenol AF (BPAF) in tissues, serum, urine and feces of orally dosed rats by ultra-high-pressure liquid chromatography-electrospray tandem mass spectrometry. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 901, 93–7.CrossRefGoogle ScholarPubMed
Yu, H. (2002). Regulation of APC-Cdc20 by the spindle checkpoint. Curr. Opin. Cell Biol. 14, 706–14.Google Scholar
Zhang, D., Ma, W., Li, Y.H., Hou, Y., Li, S.W., Meng, X.Q., Sun, X.F., Sun, Q.F. & Wang, W.H. (2004). Intra-oocyte localization of MAD2 and its relationship with kinetochores, microtubules, and chromosomes in rat oocytes during meiosis. Biol. Reprod. 71, 740–8.CrossRefGoogle ScholarPubMed