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Loss of Bmal1 decreases oocyte fertilization, early embryo development and implantation potential in female mice

Published online by Cambridge University Press:  03 May 2016

Jian Xu ,
Yan Li ,
Yizi Wang ,
Yanwen Xu  and
Canquan Zhou
Jian Xu
Affiliation:
Reproductive Medicine Center, Guangzhou Women and Children's Medical Center, Guangzhou, Guangzhou Medical University, China. Reproductive Medicine Center, First Affiliated Hospital of Sun Yat-sen University, Guangzhou, China; Guangdong Provincial Key Laboratory of Reproductive Medicine, Guangdong, China.
Yan Li
Affiliation:
Reproductive Medicine Center, Henan Provincial People's Hospital, Zhengzhou, Henan, China. Reproductive Medicine Center, First Affiliated Hospital of Sun Yat-sen University, Guangzhou, China; Guangdong Provincial Key Laboratory of Reproductive Medicine, Guangdong, China.
Yizi Wang
Affiliation:
Reproductive Medicine Center, First Affiliated Hospital of Sun Yat-sen University, Guangzhou, China; Guangdong Provincial Key Laboratory of Reproductive Medicine, Guangdong, China.
Yanwen Xu*
Affiliation:
Reproductive Medicine Center, First Affiliated Hospital of Sun Yat-sen University, 58 Zhongshan Road II, Guangzhou, China.
Canquan Zhou*
Affiliation:
Reproductive Medicine Center, First Affiliated Hospital of Sun Yat-sen University, 58 Zhongshan Road II, Guangzhou, China.
*
All correspondence to: Yanwen Xu or Canquan Zhou. Reproductive Medicine Center, First Affiliated Hospital of Sun Yat-sen University, 58 Zhongshan Road II, Guangzhou, China. E-mail: [email protected] or [email protected]
All correspondence to: Yanwen Xu or Canquan Zhou. Reproductive Medicine Center, First Affiliated Hospital of Sun Yat-sen University, 58 Zhongshan Road II, Guangzhou, China. E-mail: [email protected] or [email protected]
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Summary

Biological clock genes expressed in reproductive tissues play important roles in maintaining the normal functions of reproductive system. However, disruption of female circadian rhythm on oocyte fertilization, preimplantation embryo development and blastocyst implantation potential is still unclear. In this study, ovulation, in vivo and in vitro oocyte fertilization, embryo development, implantation and intracellular reactive oxygen species (ROS) levels in ovary and oviduct were studied in female Bmal1+/+ and Bmal1−/− mice. The number of naturally ovulated oocyte in Bmal1−/− mice decreased (5.2 ± 0.8 vs 7.8 ± 0.8, P < 0.001), with an increasing abnormal oocyte ratio (20.4 ± 3.5 vs 11.7 ± 2.0%, P = 0.001) after superovulation. Significantly lower fertilization rate and obtained blastocyst number were observed in Bmal1−/− female mice either mated with wild-type in vivo or fertilized by sperm from wild-type male mice in vitro (all P < 0.05). Interestingly, in vitro fertilization rate of oocytes derived from Bmal1−/− increased significantly compared with in vivo study (P < 0.01). After transferring blastocysts derived from Bmal1+/+ and Bmal1−/− female mice to pseudopregnant mice, the implantation sites of the latter decreased 5 days later (8.0 ± 0.8 vs 5.3 ± 1.0, P = 0.005). The intracellular ROS levels in the ovary on proestrus day and in the oviduct on metestrus day increased significantly in Bmal1−/− mice compared with that of Bmal1+/+ mice. Deletion of the core biological clock gene Bmal1 significantly decreases oocyte fertilization rate, early embryo development and implantation potential in female mice, and these may be possibly caused by excess ROS levels generated in ovary and oviduct.

Keywords

Bmal1−/− miceEmbryo developmentFertilizationImplantationROS
Type
Research Article
Information
Zygote , Volume 24 , Issue 5 , October 2016 , pp. 760 - 767
Copyright
Copyright © Cambridge University Press 2016 

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References

Agarwal, A., Aponte-Mellado, A., Premkumar, B.J., Shaman, A. & Gupta, S. (2012). The effects of oxidative stress on female reproduction: a review. Reprod. Biol. Endocrinol. 10, 49.CrossRefGoogle ScholarPubMed
Al-Gubory, K.H., Garrel, C., Faure, P. & Sugino, N. (2012). Roles of antioxidant enzymes in corpus luteum rescue from reactive oxygen species-induced oxidative stress. Reprod. Biomed. Online 25, 551–60.Google Scholar
Baker, F.C. & Driver, H.S. (2007). Circadian rhythms, sleep, and the menstrual cycle. Sleep Med. 8, 613–22.Google Scholar
Bedaiwy, M.A., Falcone, T., Mohamed, M.S., Aleem, A.A., Sharma, R.K., Worley, S.E., Thornton, J. & Agarwal, A. (2004). Differential growth of human embryos in vitro: role of reactive oxygen species. Fertil. Steril. 82, 593–600.Google Scholar
Boden, M.J., Varcoe, T.J., Voultsios, A. & Kennaway, D.J. (2010). Reproductive biology of female Bmal1 null mice. Reproduction 139, 1077–90.CrossRefGoogle ScholarPubMed
Bunger, M.K., Wilsbacher, L.D., Moran, S.M., Clendenin, C., Radcliffe, L.A., Hogenesch, J.B., Simon, M.C., Takahashi, J.S. & Bradfield, C.A. (2000). Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 103, 1009–17.CrossRefGoogle ScholarPubMed
Byers, S.L., Wiles, M.V., Dunn, S.L. & Taft, R.A. (2012). Mouse estrous cycle identification tool and images. PLoS One 7, e35538.Google Scholar
Chu, A., Zhu, L., Blum, I.D., Mai, O., Leliavski, A., Fahrenkrug, J., Oster, H., Boehm, U. & Storch, K.F. (2013). Global but not gonadotrope-specific disruption of Bmal1 abolishes the luteinizing hormone surge without affecting ovulation. Endocrinology 154, 2924–35.Google Scholar
Gamble, K.L., Resuehr, D. & Johnson, C.H. (2013). Shift work and circadian dysregulation of reproduction. Front. Endocrinol. (Lausanne) 4, 92.Google Scholar
Green, M., Bass, S. & Spear, B. (2009). A device for the simple and rapid transcervical transfer of mouse embryos eliminates the need for surgery and potential post-operative complications. Biotechniques 47, 919–24.Google Scholar
Kennaway, D.J., Varcoe, T.J. & Mau, V.J. (2003). Rhythmic expression of clock and clock-controlled genes in the rat oviduct. Mol. Hum. Reprod. 9, 503–7.CrossRefGoogle ScholarPubMed
Kondratov, R.V., Kondratova, A.A., Gorbacheva, V.Y., Vykhovanets, O.V. & Antoch, M.P. (2006). Early aging and age-related pathologies in mice deficient in BMAL1, the core component of the circadian clock. Genes Dev. 20, 1868–73.Google Scholar
Kovanen, L., Saarikoski, S.T., Aromaa, A., Lonnqvist, J. & Partonen, T. (2010). ARNTL (BMAL1) and NPAS2 gene variants contribute to fertility and seasonality. PLoS One 5, e10007.Google Scholar
Lawson, C.C., Whelan, E.A., Lividoti, H.E., Spiegelman, D., Schernhammer, E.S. & Rich-Edwards, J.W. (2011). Rotating shift work and menstrual cycle characteristics. Epidemiology 22, 305–12.CrossRefGoogle ScholarPubMed
Liu, Y., Johnson, B.P., Shen, A.L., Wallisser, J.A., Krentz, K.J., Moran, S.M., Sullivan, R., Glover, E., Parlow, A.F., Drinkwater, N.R., Schuler, L.A. & Bradfield, C.A. (2014). Loss of BMAL1 in ovarian steroidogenic cells results in implantation failure in female mice. Proc. Natl. Acad. Sci. USA 111, 14295–300.CrossRefGoogle ScholarPubMed
Lowrey, P.L. & Takahashi, J.S. (2011). Genetics of circadian rhythms in mammalian model organisms. Adv. Genet. 74, 175–230.Google Scholar
Matsuzuka, T., Ozawa, M., Nakamura, A., Ushitani, A., Hirabayashi, M. & Kanai, Y. (2005). Effects of heat stress on the redox status in the oviduct and early embryonic development in mice. J. Reprod. Dev. 51, 281–7.Google Scholar
Patel, S.A., Velingkaar, N.S. & Kondratov, R.V. (2014). Transcriptional control of antioxidant defense by the circadian clock. Antioxid. Redox Signal 20, 2997–3006.Google Scholar
Ratajczak, C.K., Boehle, K.L. & Muglia, L.J. (2009). Impaired steroidogenesis and implantation failure in Bmal1−/− mice. Endocrinology 150, 1879–85.CrossRefGoogle ScholarPubMed
Reppert, S.M. & Weaver, D.R. (2002). Coordination of circadian timing in mammals. Nature 418, 935–41.Google Scholar
Sellix, M.T. & Menaker, M. (2010). Circadian clocks in the ovary. Trends Endocrinol. Metab. 21, 628–36.CrossRefGoogle ScholarPubMed
Shkolnik, K., Tadmor, A., Ben-Dor, S., Nevo, N., Galiani, D. & Dekel, N. (2011). Reactive oxygen species are indispensable in ovulation. Proc. Natl. Acad. Sci. USA 108, 1462–7.CrossRefGoogle ScholarPubMed
Tamura, H., Takasaki, A., Miwa, I., Taniguchi, K., Maekawa, R., Asada, H., Taketani, T., Matsuoka, A., Yamagata, Y., Shimamura, K., Morioka, H., Ishikawa, H., Reiter, R.J. & Sugino, N. (2008). Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. J. Pineal Res. 44, 280–7.Google Scholar
Wang, F., Tian, X., Zhang, L., Tan, D., Reiter, R.J. & Liu, G. (2013). Melatonin promotes the in vitro development of pronuclear embryos and increases the efficiency of blastocyst implantation in murine. J. Pineal Res. 55, 267–74.Google Scholar