Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Synchronisation of canine germinal vesicle stage oocytes prior to in vitro maturation alters the kinetics of nuclear progression during subsequent resumption of meiosis

Carol Hanna A , Suzanne Menges A , Duane Kraemer A and Charles R. Long A B
+ Author Affiliations
- Author Affiliations

A Texas A and M University, College of Veterinary Medicine, Department of Physiology and Pharmacology, College Station, TX 77843-4466, USA.

B Corresponding author. Email: clong@cvm.tamu.edu

Reproduction, Fertility and Development 20(5) 606-614 https://doi.org/10.1071/RD07227
Submitted: 20 December 2007  Accepted: 7 April 2008   Published: 21 May 2008

Abstract

Inhibition of meiosis before in vitro maturation (IVM) can improve meiotic competence in immature mammalian oocytes. Therefore, meiosis-inhibiting agents were evaluated singularly for the ability to arrest and synchronise germinal vesicle (GV) stage canine oocytes, and the most effective treatments were combined to improve meiotic resumption rates. Oocytes cultured in 2 ng mL–1 oestradiol (E2), 10 IU mL–1 eCG, or both (EG) for 72 h resulted in significantly fewer oocytes resuming meiosis in EG than the control, E2, or with eCG. Oocytes cultured in 50 or 100 μmol L–1 of butyrolactone 1 or roscovitine (ROS) for up to 48 h did not resume meiosis nor increase subsequent meiotic resumption rates following IVM. A combination of 50 μmol L–1 ROS and EG treatment for 48 h significantly increased the proportion of canine oocytes in meiotic arrest. More importantly, following 48 h of IVM, ROS+EG-treated oocytes demonstrated a dramatic increase in the ability to resume meiosis compared with the non-treated controls (51.3 ± 8.2% and 10.8 ± 4.5%, respectively; P < 0.05). These data indicate that chemical and biological meiotic inhibitors are effective at inducing GV arrest in canine oocytes. Furthermore, these inhibitors are reversible and beneficial to subsequent meiotic resumption in vitro.


Acknowledgements

The authors of this paper would like thank Kim Green and JoAnne Stokes for technical assistance and acknowledge Bio-Arts Research Corporation, Mill Valley, California, USA, for providing funding for this project.


References

Adona P. R., Pires P. R., Quetglas M. D., and Leal C. L. (2007). Prematuration of bovine oocytes with butyrolactone I: effects on meiosis progression, cytoskeleton, organelle distribution and embryo development. Anim. Reprod. Sci., in press.

Adona, P. R. , Pires, P. R. , Quetglas, M. D. , Schwarz, K. R. , and Leal, C. L. (2008). Nuclear maturation kinetics and in vitro embryo development of cattle oocytes prematured with butyrolactone I combined or not combined with roscovitine. Anim. Reprod. Sci. 104, 389–397.
Crossref | GoogleScholarGoogle Scholar | PubMed | Nickson D. A., Boyd J. S., Eckersall P. D., Ferguson J. M., Harvey M. J. A., and Renton J. P. (1993). Molecular biological methods for monitoring oocyte maturation and in vitro fertilization in bitches. J. Reprod. Fertil. 47(Suppl.), 231–240.

Oh, H. J. , Fibrianto, Y. H. , Kim, M. K. , Jang, G. , Hossein, M. S. , Kim, H. J. , Kang, S. K. , Lee, B. C. , and Hwang, W. S. (2005). Effects of canine serum collected from dogs at different estrous cycle stages on in vitro nuclear maturation of canine oocytes. Zygote 13, 227–232.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Olson, P. N. , Bowen, R. A. , Behrendt, M. D. , Olson, J. D. , and Nett, T. M. (1982). Concentrations of reproductive hormones in canine serum throughout late anestrus, proestrus and estrus. Biol. Reprod. 27, 1196–1206.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Otoi, T. , Fujii, M. , Tanaka, M. , Ooka, A. , and Suzuki, T. (2000). Canine oocyte diameter in relation to meiotic competence and sperm penetration. Theriogenology 54, 535–542.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Otoi, T. , Shimizu, R. , Naoi, H. , Wongsrikeao, P. , Agung, B. , and Taniguchi, M. (2006). Meiotic competence of canine oocytes embedded in collagen gel. Reprod. Domest. Anim. 41, 17–21.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Otoi, T. , Shin, T. , Kraemer, D. C. , and Westhusin, M. (2007). Role of cumulus cells on in vitro maturation of canine oocytes. Reprod. Domest. Anim. 42, 184–189.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ponderato, N. , Crotti, G. , Turini, P. , Duchi, R. , Galli, C. , and Lazzari, G. (2002). Embryonic and foetal development of bovine oocytes treated with a combination of butyrolactone I and roscovitine in an enriched medium prior to IVM and IVF. Mol. Reprod. Dev. 62, 513–518.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Rodrigues, B. A. , and Rodrigues, J. L. (2003). Meiotic response of in vitro-matured canine oocytes under different proteins and heterologous hormone supplementation. Reprod. Domest. Anim. 38, 58–62.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Rodrigues, B. A. , Dos Santos, L. C. , and Rodrigues, J. L. (2006). The effect of hyaluronan concentrations in hST-supplemented TCM 199 on in vitro nuclear maturation of bitch cumulus-oocyte complexes. Theriogenology 66, 1673–1676.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Silva, A. R. , Morato, R. G. , and Silva, L. D. M. (2004). The potential for gamete recovery from non-domestic canids and felids. Anim. Reprod. Sci. 81, 159–175.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Silva, A. R. , Cardoso, R. C. , and Silva, L. D. M. (2006). Influence of temperature during glycerol addition and post-thaw dilution on the quality of canine frozen semen. Reprod. Domest. Anim. 41, 74–78.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Songsasen, N. , and Wildt, D. E. (2005). Size of the donor follicle, but not stage of reproductive cycle or seasonality, influences meiotic competency of selected domestic dog oocytes. Mol. Reprod. Dev. 72, 113–119.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Songsasen, N. , Yu, I. , Gomez, M. , and Liebo, S. P. (2003). Effects of meiosis-inhibiting agents and equine chorionic gonadotropin on nuclear maturation of canine oocytes. Mol. Reprod. Dev. 65, 435–445.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Songsasen, N. , Spindler, R. E. , and Wildt, D. E. (2007). Requirement for, and patterns of, pyruvate and glutamine metabolism in the domestic dog oocyte in vitro. Mol. Reprod. Dev. 74, 870–877.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Vanhoutte, L. , De Sutter, P. , Nogueira, D. , Gerris, J. , Dhont, M. , and Van der Elst, J. (2007). Nuclear and cytoplasmic maturation of in vitro-matured human oocytes after temporary nuclear arrest by phosphodiesterase 3-inhibitor. Hum. Reprod. 22, 1239–1246.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Vannucchi, C. I. , de Oliveira, C. M. , Marques, M. G. , Assumpcao, M. E. O. A. , and Visintin, J. A. (2006). In vitro canine oocyte nuclear maturation in homologous oviductal cell co-culture with hormone- supplemented media. Theriogenology 66, 1677–1681.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Verstegen, J. P. , Onclin, K. , and Iguer-Ouada, M. (2005). Long-term motility and fertility conservation of chilled canine semen using egg yolk added Tris-glucose extender in vitro and in vivo studies. Theriogenology 64, 720–733.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ververidis, H. N. , Boscos, C. M. , Stefanakis, A. , and Krambovitis, E. (2002). Use of enzyme-immunoassay for oestradiol-17beta and progesterone quantification in canine serum. Anim. Reprod. Sci. 69, 53–64.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Weng, Y. C. , Sha, S. W. , Chiou, C. M. , Tang, P. C. , Yang, J. H. , and Ju, J. C. (2007). Butyrolactone I reversibly alters nuclear configuration, perioplasmic microtubules and development of porcine oocytes. Theriogenology 67, 509–519.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wickramasinghe, D. , Ebert, K. M. , and Albertini, D. F. (1991). Meiotic competence acquisition is associated with the appearance of M-phase characteristics in growing mouse oocytes. Dev. Biol. 143, 162–172.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Willingham-Rocky, L. A. , Hinrichs, K. , Westhusin, M. E. , and Kraemer, D. C. (2003). Effects of stage of oestrous cycle and progesterone supplementation during culture on maturation of canine oocytes in vitro. Reproduction 126, 501–508.
Crossref | GoogleScholarGoogle Scholar | PubMed |