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Early germinal vesicle breakdown is a predictor of high preimplantation developmental competent oocytes in mice

Published online by Cambridge University Press:  22 November 2016

Shogo Higaki ,
Masao Kishi ,
Keisuke Koyama ,
Masashi Nagano ,
Seiji Katagiri ,
Tatsuyuki Takada  and
Yoshiyuki Takahashi
Shogo Higaki*
Affiliation:
Laboratory of Cell Engineering, Department of Pharmaceutical Sciences, Ritsumeikan University, Nojihigashi 1-1-1, Kusatsu, Shiga 525 8577, Japan.
Masao Kishi
Affiliation:
Laboratory of Theriogenology, Department of Veterinary Clinical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Hokkaido 060–0818, Japan.
Keisuke Koyama
Affiliation:
Dairy Cattle Group, Konsen Agricultural Experiment Station, Hokkaido Research Organization, Nakashibetsu, Hokkaido 086–1135, Japan.
Masashi Nagano
Affiliation:
Laboratory of Theriogenology, Department of Veterinary Clinical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Hokkaido 060–0818, Japan.
Seiji Katagiri
Affiliation:
Laboratory of Theriogenology, Department of Veterinary Clinical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Hokkaido 060–0818, Japan.
Tatsuyuki Takada
Affiliation:
Laboratory of Cell Engineering, Department of Pharmaceutical Sciences, Ritsumeikan University, Kusatsu, Shiga 525–8577, Japan.
Yoshiyuki Takahashi
Affiliation:
Laboratory of Theriogenology, Department of Veterinary Clinical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Hokkaido 060–0818, Japan.
*
All correspondence to: Shogo Higaki. Laboratory of Cell Engineering, Department of Pharmaceutical Sciences, Ritsumeikan University, Nojihigashi 1-1-1, Kusatsu, Shiga 525 8577, Japan. Tel: +81 77 561 2266. E-mail: [email protected]
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Summary

The preselection of highly developmentally competent oocytes for in vitro maturation (IVM) is crucial for improving assisted reproductive technology. Although several intrinsic markers of oocyte quality are known to be closely related to the onset of nuclear maturation (germinal vesicle break down, GVBD), a direct comparison between GVBD timing and oocyte quality has never been reported. In this study, we established a non-invasive oocyte evaluation method based on GVBD timing for preselecting more developmental competent oocytes in mice. Because the O2 concentration during IVM may affect the nuclear kinetics, all experiments were performed under two distinct O2 concentrations: 20% and 5% O2. First, we determined the time course of changes in nuclear maturation and preimplantation developmental competence of in vitro-matured oocytes to estimate GVBD timing in high developmental competent oocytes. Two-thirds of oocytes that underwent GVBD in early IVM seemed to mainly contribute to the blastocyst yield. To confirm this result, we compared the preimplantation developmental competence of the early and late GVBD oocytes. Cleavage and blastocyst formation rates of early GVBD oocytes (80.2% and 52.7% under 20% O2, respectively, and 67.6% and 47.3% under 5% O2, respectively) were almost double those of late GVBD oocytes (44.8% and 26.0% under 20% O2, respectively, and 40.4% and 17.9% under 5% O2, respectively). With no observable alterations by checking the timing of GVBD in preimplantation developmental competence, oocyte evaluation based on GVBD timing can be used as an efficient and non-invasive preselection method for high developmental competent oocytes.

Keywords

Developmental competenceGerminal vesicle breakdownMouseOocyte
Type
Research Article
Information
Zygote , Volume 25 , Issue 1 , February 2017 , pp. 41 - 48
Copyright
Copyright © Cambridge University Press 2016 

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References

Adam, A.A.G., Takahashi, Y., Katagiri, S. & Nagano, M. (2004). Effects of oxygen tension in the gas atmosphere during in vitro maturation, in vitro fertilization and in vitro culture on the efficiency of in vitro production of mouse embryos. Jpn. J. Vet. Res. 52, 77–84.Google Scholar
Banwell, K.M. & Thompson, J.G. (2008). In vitro maturation of mammalian oocytes: outcomes and consequences. Semin. Reprod. Med. 26, 162–74.Google Scholar
Banwell, K., Lane, M., Russell, D., Kind, K. & Thompson, J. (2007). Oxygen concentration during mouse oocyte in vitro maturation affects embryo and fetal development. Hum. Reprod. 22, 2768–75.Google Scholar
Bedford, J. (1971). Techniques and criteria used in the study of fertilization. In Daniel, J.C. (ed.). Methods in Mammalian Embryology, London: W.H. Freeman. pp. 37–63.Google Scholar
Bukowska, D., Kempisty, B., Piotrowska, H., Walczak, R., Sniadek, P., Dziuban, J., Brussow, K., Jaskowski, J. & Nowicki, M. (2012). The invasive and new non-invasive methods of mammalian oocyte and embryo quality assessment: a review. Vet. Med. 57, 169–76.Google Scholar
Catalá, M.G., Izquierdo, D., Uzbekova, S., Morató, R., Roura, M., Romaguera, R., Papillier, P. & Paramio, M.T. (2011). Brilliant cresyl blue stain selects largest oocytes with highest, mitochondrial activity, maturation-promoting factor activity and embryo developmental competence in prepubertal sheep. Reproduction 142, 517–27.Google Scholar
Chesnel, F. & Eppig, J.J. (1995). Synthesis and accumulation of p34cdc2 and cyclin B in mouse oocytes during acquisition of competence to resume meiosis. Mol. Reprod. Dev. 40, 503–8.Google Scholar
Christmann, L., Jung, T. & Moor, R.M. (1994). MPF components and meiotic competence in growing pig oocytes. Mol. Reprod. Dev. 38, 85–90.CrossRefGoogle ScholarPubMed
Dominko, T. & First, N.L. (1997). Timing of meiotic progression in bovine oocytes and its effect on early embryo development. Mol. Reprod. Dev. 47, 456–67.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
Donahue, R.P. (1968). Maturation of the mouse oocyte in. vitro. I. Sequence and timing of nuclear progression. J. Exp. Zool. 169, 237–49.Google Scholar
Eppig, J.J. & Wigglesworth, K. (1995). Factors affecting the developmental competence of mouse oocytes grown in vitro: oxygen concentration. Mol. Reprod. Dev. 42, 447–56.CrossRefGoogle ScholarPubMed
Erbach, G.T., Lawitts, J.A., Papaioannou, V.E. & Biggers, J.D. (1994). Differential growth of the mouse preimplantation embryo in chemically defined media. Biol. Reprod. 50, 1027–33.CrossRefGoogle ScholarPubMed
Fair, T. (2009). Mammalian oocyte development: checkpoints for competence. Reprod. Fertil. Dev. 22, 13–20.Google Scholar
Hashimoto, S., Minami, N., Takakura, R., Yamada, M., Imai, H. & Kashima, N. (2000). Low oxygen tension during in vitro maturation is beneficial for supporting the subsequent development of bovine cumulus–oocyte complexes. Mol. Reprod. Dev. 57, 353–60.3.0.CO;2-R>CrossRefGoogle ScholarPubMed
Kubiak, J.Z., Ciemerych, M.A., Hupalowska, A., Sikora-Polaczek, M. & Polanski, Z. (2008). On the transition from the meiotic to mitotic cell cycle during early mouse development. Int. J. Dev. Biol. 52, 201.Google Scholar
LaRosa, C. & Downs, S.M. (2006). Stress stimulates AMP-activated protein kinase and meiotic resumption in mouse oocytes. Biol. Reprod. 74, 585–92.Google Scholar
Ledda, S., Bogliolo, L., Leoni, G. & Naitana, S. (2001). Cell coupling and maturation-promoting factor activity in in vitro-matured prepubertal and adult sheep oocytes. Biol. Reprod. 65, 247–52.CrossRefGoogle ScholarPubMed
Liu, X.Y., Mal, S.F., Miao, D.Q., Liu, D.J., Bao, S. & Tan, J.H. (2005). Cortical granules behave differently in mouse oocytes matured under different conditions. Hum. Reprod. 20, 3402–13.Google Scholar
Messinger, S.M. & Albertini, D.F. (1991). Centrosome and microtubule dynamics during meiotic progression in the mouse oocyte. J. Cell. Sci. 100, 289–98.Google Scholar
Mingoti, G.Z, Castro, V.S.D.C., Méo, S.C., Barretto, L.S.S. & Garcia, J.M. (2011). The effects of macromolecular and serum supplements and oxygen tension during bovine in vitro procedures on kinetics of oocyte maturation and embryo development. In Vitro Cell. Dev. Biol-Anim. 47, 361–7.Google Scholar
Murray, A.W. & Kirschner, M.W. (1989). Cyclin synthesis drives the early embryonic cell cycle. Nature 339, 275–80.Google Scholar
Naito, K., Daen, F.P. & Toyoda, Y. (1992). Comparison of histone H1 kinase activity during meiotic maturation between two types of porcine oocytes matured in different media in vitro . Biol. Reprod. 47, 43–7.Google Scholar
Otoi, T., Yamamoto, K., Koyama, N., Tachikawa, S. & Suzuki, T. (1997). Bovine oocyte diameter in relation to developmental competence. Theriogenology 48, 769–74.CrossRefGoogle ScholarPubMed
Preis, K.A., Seidel, G.E. & Gardner, D.K. (2007). Reduced oxygen concentration improves the developmental competence of mouse oocytes following in. vitro maturation. Mol. Reprod. Dev. 74, 893–903.Google Scholar
Sirard, M.A., Richard, F., Blondin, P. & Robert, C. (2006). Contribution of the oocyte to embryo quality. Theriogenology 65, 126–36.Google Scholar
Son, W.Y., Lee, S.Y. & Lim, J.H. (2005). Fertilization, cleavage and blastocyst development according to the maturation timing of oocytes in. vitro maturation cycles. Hum. Reprod. 20, 3204–7.Google Scholar
Takahashi, Y. & First, N. (1992). In. vitro development of bovine one-cell embryos: influence of glucose, lactate, pyruvate, amino acids and vitamins. Theriogenology 37, 963–78.Google Scholar
Toyoda, Y. (1971). Studies on fertilization of mouse eggs in vitro. I. In vitro fertilization of eggs by fresh epididymal sperm. Jpn J. Anim. Reprod. 16, 147–51.Google Scholar
Wang, Q. & Sun, Q.Y. (2006). Evaluation of oocyte quality: morphological, cellular and molecular predictors. Reprod. Fertil. Dev. 19, 1–12.Google Scholar
Wu, Y.G., Liu, Y., Zhou, P., Lan, G.C., Han, D., Miao, D.Q. & Tamm, J.H. (2007). Selection of oocytes for in vitro maturation by brilliant cresyl blue staining: a study using the mouse model. Cell. Res. 17, 722–31.CrossRefGoogle ScholarPubMed
Zeilmaker, G., Hulsmann, W., Wensinck, F. & Verhamme, C. (1972). Oxygen-triggered mouse oocyte maturation in vitro and lactate utilization by mouse oocytes and zygotes. J. Reprod. Fertil. 29, 151–2.CrossRefGoogle ScholarPubMed