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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Comparison of maturational and developmental parameters of oocytes recovered from prepubertal and adult pigs

Koji Ikeda A and Yoshiyuki Takahashi A B
+ Author Affiliations
- Author Affiliations

A Laboratory of Theriogenology, Department of Veterinary Clinical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo 060-0818, Japan.

B To whom correspondence should be addressed. email: ytaka@vetmed.hokudai.ac.jp

Reproduction, Fertility and Development 15(4) 215-221 https://doi.org/10.1071/RD02077
Submitted: 17 September 2002  Accepted: 23 May 2003   Published: 23 May 2003

Abstract

To clarify the cause(s) of the differences between the developmental competence of prepubertal and adult porcine oocytes, the following were examined: (i) the meiotic progression, p34cdc2 kinase activity, ooplasm diameter and response to activation stimuli of the oocytes; and (ii) the development of parthenotes and nuclear transfer (NT) embryos obtained using oocytes recovered from prepubertal and adult pigs. Oocytes were recovered from 4- to 8-mm follicles of abattoir-derived ovaries. There were no apparent differences in the morphology of the germinal vesicle, nuclear maturation rate, activity of p34cdc2 kinase or response to parthenogenetic stimulation between prepubertal and adult oocytes. Before and after maturation culture, the ooplasm diameters of prepubertal oocytes were smaller than those of adult oocytes. Parthenotes and NT embryos derived from prepubertal gilt oocytes showed a lower rate of development to the blastocyst stage than those derived from adult oocytes. These results suggest that lower developmental competence of prepubertal oocytes may be caused by their inability to complete ooplasmic maturation, and that this is not because of altered oocyte maturation kinetics and/or p34cdc2 kinase activity. Furthermore, the smaller diameter of the ooplasm of prepubertal oocytes indicates that most oocytes that have routinely recovered from prepubertal gilt ovarian follicles are still in the growing phase and have immature ooplasm.

Extra keywords: activation


Acknowledgments

The authors are deeply indebted to Dr Masami Suzuki, Dr Maki Ikawa and Ms Masumi Kagawa for their technical assistance. We thank the staff at the Ebetsu Meat Inspection Office (Hokkaido, Japan) for supplying the ovaries. This study was supported by a Grant-in-Aid for scientific research (Nos. 10556058 and 12480248) from the Japan Society for the Promotion of Science.


References

Betthauser, J. , Forsberg, E. , Augenstein, M. , Childs, L. , and Eilertsen, K. , et al. (2000). Production of cloned pigs from in vitro systems Nature Biotechnol. 18, 1055–9.
Crossref | GoogleScholarGoogle Scholar |

Cheong, H. T. , Ikeda, K. , Martinez Diaz, M. A. , Katagiri, S. , and Takahashi, Y. (2000). Development of reconstituted pig embryos by nuclear transfer of cultured cumulus cells Reprod. Fertil. Dev. 12, 15–20.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Dominko, T. , and First, N. L. (1997). Timing of meiotic progression in bovine oocytes and its effect on early embryo development Mol. Reprod. Dev. 47, 456–67.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Eppig, J. J. , and Schroeder, A. C. (1989). Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro.  Biol. Reprod. 41, 268–76.
PubMed |

Fair, T. , Hyttel, P. , and Greve, T. (1995). Bovine oocyte diameter in relation to maturational competence and transcriptional activity Mol. Reprod. Dev. 42, 437–42.
PubMed |

Gandolfi, F. , Milanesi, E. , Pocar, P. , Luciano, A. M. , Brevini, T. A. , Acocella, F. , Lauria, A. , and Armstrong, D. T. (1998). Comparative analysis of calf and cow oocytes during in vitro maturation Mol. Reprod. Dev. 49, 168–75.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Hirao, Y. , Tsuji, Y. , Miyano, T. , Okano, A. , Miyake, M. , Kato, S. , and Moor, R. M. (1995). Association between p34cdc2 levels and meiotic arrest in pig oocytes during early growth Zygote 3, 325–32.
PubMed |

Ikeda, K. , and Takahashi, Y. (2001). Effect of maturational age of porcine oocytes on the induction of activation and development in vitro following somatic cell nuclear transfer J. Vet. Med. Sci. 63, 1003–8.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ikeda, K. , and Takahashi, Y. (2002). Effect of butyrolactone I on the inhibition of meiotic resumption of porcine oocytes and subsequent development following somatic cell nuclear transfer J. Mamm. Ova Res. 19, 46–51.
Crossref | GoogleScholarGoogle Scholar |

Ito, J. , Shimada, M. , and Terada, T. (2001). Progression of nuclear maturation and p34cdc2 kinase activity in porcine oocytes during in vitro culture in different media J. Mamm. Ova Res. 18, 39–43.
Crossref | GoogleScholarGoogle Scholar |

Khatir, H. , Lonergan, P. , and Mermillod, P. (1998). Kinetics of nuclear maturation and protein profiles of oocytes from prepubertal and adult cattle during in vitro maturation Theriogenology 50, 917–29.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Kühholzer, B. , Hawley, R. J. , Lai, L. , Kolber-Simonds, D. , and Prather, R. S. (2001). Clonal lines of transgenic fibroblast cells derived from the same fetus result in different development when used for nuclear transfer in pigs Biol. Reprod. 64, 1695–8.
PubMed |

Ledda, S. , Bogliolo, L. , Calvia, P. , Leoni, G. , and Naitana, S. (1997). Meiotic progression and developmental competence of oocytes collected from juvenile and adult ewes J. Reprod. Fertil. 109, 73–8.
PubMed |

Ledda, S. , Bogliolo, L. , Leoni, G. , and Naitana, S. (2001). Cell coupling and maturation-promoting factor activity in in vitro-matured prepubertal and adult sheep oocytes Biol. Reprod. 65, 247–52.
PubMed |

Lévesque, J. T. , and Sirard, M. A. (1994). Proteins in oocytes from calves and adult cows before maturation: Relationship with their development capacity Reprod. Nutr. Dev. 34, 133–9.
PubMed |

Marchal, R. , Feugang, J. M. , Perreau, C. , Venturi, E. , Terqui, M. , and Mermillod, P. (2001). Meiotic and developmental competence of prepubertal and adult swine oocytes Theriogenology 56, 17–29.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Marchal, R. , Vigneron, C. , Perreau, C. , Bali-Papp, A. , and Mermillod, P. (2002). Effect of follicle size on meiotic and developmental competence of porcine oocytes Theriogenology 57, 1523–32.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Martinez Diaz, M. A. , Ikeda, K. , and Takahashi, Y. (2002). Effects of cycloheximide treatment and interval between fusion and activation on in vitro development of pig nuclear transfer embryos Reprod. Fertil. Dev. 14, 191–7.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Mermillod, P. , Le Bourhis, D. , Lonergan, P. , Khatir, H. , and Heyman, Y. (1998). Assessment of cytoplasmic competence of prepubertal calf oocytes by use of nuclear transfer Theriogenology 49, 187.(Abstract.)
Crossref | GoogleScholarGoogle Scholar |

Motlík, J. , and Fulka, J. (1976). Breakdown of the germinal vesicle in pig oocytes in vivo and in vitro  J. Exp. Zool. 198, 155–62.
PubMed |

Motlík, J. , Crozet, N. , and Fulka, J. (1984). Meiotic competence in vitro of pig oocytes isolated from early antral follicles J. Reprod. Fertil. 72, 323–8.
PubMed |

Naito, K. , Daen, F. P. , and 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.
PubMed |

O’Brien, J. K. , Dwarte, D. , Ryan, J. P. , Maxwell, W. M. , and Evans, G. (1996). Developmental capacity, energy metabolism and ultrastructure of mature oocytes from prepubertal and adult sheep Reprod. Fertil. Dev. 8, 1029–37.
PubMed |

O’Brien, J. K. , Dwarte, D. , Ryan, J. P. , Maxwell, W. M. C. , and Evans, G. (2000). Comparison of in vitro maturation, in vitro fertilization, metabolism and ultrastructure of oocytes from prepubertal and adult pigs Reprod. Dom. Anim. 35, 101–7.
Crossref | GoogleScholarGoogle Scholar |

Otoi, T. , Yamamoto, K. , Koyama, N. , Tachikawa, S. , and Suzuki, T. (1997). Bovine oocyte diameter in relation to developmental competence Theriogenology 48, 769–74.
Crossref | GoogleScholarGoogle Scholar |

Petters, R. M. , and Wells, K. D. (1993). Culture of pig embryos J. Reprod. Fertil. Suppl. 48, 61–73.
PubMed |

Revel, F. , Mermillod, P. , Peynot, N. , Renard, J. P. , and Heyman, Y. (1995). Low developmental capacity of in vitro-matured and fertilized oocytes from calves compared with that of cows J. Reprod. Fertil. 103, 115–20.
PubMed |

Salamone, D. F. , Damiani, P. , Fissore, R. A. , Robl, J. M. , and Duby, R. T. (2001). Biochemical and developmental evidence that ooplasmic maturation of prepubertal bovine oocyte is compromised Biol. Reprod. 64, 1761–8.
PubMed |

Sato, E. , Matsuo, M. , and Miyamoto, H. (1990). Meiotic maturation of bovine oocytes in vitro: Improvement of meiotic competence by dibutyryl cyclic adenosine 3′,5′-monophosphate J. Anim. Sci. 68, 1182–7.
PubMed |

Sorensen, R. A. , and Wassarman, P. M. (1976). Relationship between growth and meiotic maturation of the mouse oocyte Dev. Biol. 50, 531–6.
PubMed |

Steeves, T. E. , and Gardner, D. K. (1999). Metabolism of glucose, pyruvate, and glutamine during the maturation of oocytes derived from pre-pubertal and adult cows Mol. Reprod. Dev. 54, 92–101.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Susko-Parrish, J. L. , Leibfried-Rutledge, M. L. , Northey, D. L. , Schutzkus, V. , and First, N. L. (1994). Inhibition of protein kinases after an induced calcium transient causes transition of bovine oocytes to embryonic cycles without meiotic completion Dev. Biol. 166, 729–39.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Takahashi, Y. , and First, N. L. (1992). In vitro development of bovine one-cell embryos: Influence of glucose, lactate, pyruvate, amino acids and vitamins Theriogenology 37, 963–78.
Crossref | GoogleScholarGoogle Scholar |

Wang, W. H. , Abeydeera, L. R. , Cantley, T. C. , and Day, B. N. (1997). Effects of oocyte maturation media on development of pig embryos produced by in vitro fertilization J. Reprod. Fertil. 111, 101–8.
PubMed |

Yang, X. , Kubota, C. , Suzuki, H. , Taneja, M. , Bols, P. E. , and Presicce, G. A. (1998). Control of oocyte maturation in cows—biological factors Theriogenology 49, 471–82.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Yoon, K. W. , Shin, T. Y. , Park, J. I. , Roh, S. , Lim, J. M. , Lee, B. C. , Hwang, W. S. , and Lee, E. S. (2000). Development of porcine oocytes from pre-ovulatory follicles of different sizes after maturation in media supplemented with follicular fluids Reprod. Fertil. Dev. 12, 133–9.
PubMed |

Yoshioka, K. , Suzuki, C. , Tanaka, A. , Anas, I. M. K. , and Iwamura, S. (2002). Birth of piglets derived from porcine zygotes cultured in a chemically defined medium Biol. Reprod. 66, 112–19.
PubMed |