Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-28T01:04:26.041Z Has data issue: false hasContentIssue false

Fertilisation competence of bovine normally matured or aged oocytes derived from different antral follicles: morphology, protein synthesis, H1 and MBP kinase activity

Published online by Cambridge University Press:  26 September 2008

Antonín Pavlok*
Affiliation:
Institute of Animal Physiology and Genetics, Academy of Sciences of the Czech Republic, Libeˇchov, Czech Republic
Petr Kaláb
Affiliation:
Institute of Animal Physiology and Genetics, Academy of Sciences of the Czech Republic, Libeˇchov, Czech Republic
Petr Bobák
Affiliation:
Institute of Animal Physiology and Genetics, Academy of Sciences of the Czech Republic, Libeˇchov, Czech Republic
*
Dr Antonín Pavlok, Institute of Animal Physiology and Genetics, Academy of Sciences of the Czech Republic, CZ-277 21 Liběchov, Czech Republic. Tel: 420 206 697147. Fax: 420 206 697186. e-mail: reprod@site.cas.cz.

Summary

We have investigated the fertilisation competence, protein synthesis, histone H1 kinase and myelin basic protein (MBP) kinase activities in three categories of bovine oocytes (derived from three size categories of follicles: M–medium, 2.5–5.0 mm; S–small, 1.5–2.5 mm; T – tiny, 1.0–1.5mm). In contrast to more or less normal meiotic maturation (85.6%) and fertilisation (70.8%) of M oocytes cultured for 24h, the fertilisation of M oocytes cultured for 40h was associated with increased rates of retarded male pronuclear development and retention of the second polar body. The S and T oocytes cultured for 24h or 40h were mostly arrested at defective late diakinesis - metaphase I (77.5–100%) stage. After fertilisation of S and T oocytes cultured for 24h no polar body was extruded and formation of one, three or four female pronuclei, together with mostly normal male pronuclei, was observed. The fertilisation of S and T oocytes after 40h culture resulted in a higher number of female and a decreased number of male pronuclei. A major change in the pattern of protein synthesis was associated with the resumption of meiosis. There were no significant differences in the profile of protein synthesis between oocyte categories in all groups either matured or fertilised. The H1 kinase activity reached comparable increased levels in oocytes of all categories matured for 24h and decreased during the 40h culture, most significantly in M oocytes. The MBP kinase activity was at approximately the same high level in all categories of oocytes after 24h of culture and remained stable until 40h. The fertilisation after 24h of culture resulted, in M oocytes, in low levels of both H1 and MBP kinase activities; in S oocytes, only H1 kinase was completely inactivated while MBP kinase activity decreased to some extent; in T oocytes, both H1 and MBP kinase activity decreased. Fertilisation of all oocyte categories after 40h culture resulted in complete inactivation of both these kinases to their basal levels.

Type
Article
Copyright
Copyright © Cambridge University Press 1997

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

Blobel, C.P., Wolfsberg, T.G., Turck, C.W., Myles, D.G., Primakoff, P. & White, J.M. (1992). A potential fusion peptide and an integrin ligand in a protein active in sperm-egg fusion. Nature 356, 248–52.CrossRefGoogle Scholar
Borsuk, E. & Tarkowski, A.K. (1989). Transformation of sperm nuclei into male pronuclei in nucleate and anucleate fragments of parthenogenetic mouse eggs. Gamete Res. 24, 471–81.CrossRefGoogle ScholarPubMed
Choi, T., Aoki, F., Mori, M., Yamashita, M., Nagahama, Y. & Kohmoto, K. (1991). Activation of p34cdc2 protein kinase activity in meiotic and mitotic cell cycles in mouse oocytes and embryos. Development 113, 789–95.CrossRefGoogle ScholarPubMed
Crozet, N., Kanˇka, J., Motlík, J. & Fulka, J. (1986). Nucleolar fine structure and RNA synthesis in bovine oocytes from antral follicles. Gamete Res. 14, 6573.CrossRefGoogle Scholar
Driancourt, M.A. (1991). Follicular dynamics in sheep and cattle. Theriogenology 35, 5579.CrossRefGoogle Scholar
Ducibella, T., Duffy, P., Reindollar, R. & Su, B. (1990). Changes in the distribution of mouse oocyte cortical granules and ability to undergo the cortical reaction during gonadotropin-stimulated meiotic maturation and aging in vivo. Biol. Reprod. 43, 870–6.CrossRefGoogle ScholarPubMed
Eppig, J.J., Schultz, R.M., O'Brien, M. & Chesnel, F. (1994). Relationship between the developmental programs con trolling nuclear and cytoplasmic maturation of mouse oocytes. Dev. Biol. 164, 19.CrossRefGoogle Scholar
Fair, T., Hyttel, P. & Greve, T. (1995). Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol. Reprod. Dev. 42, 437–42.CrossRefGoogle ScholarPubMed
Fissore, R.A. & Robl, J.M. (1992). Intracellular Ca2+ response of rabbit oocytes to electrical stimulation. Mol. Reprod. Dev. 32, 916.CrossRefGoogle ScholarPubMed
Fukui, Y., McGowan, L.T, James, R.W., Pugh, P.A. & Tervit, H.R. (1991). Factors affecting the in vitro development to blastocyst of bovine oocytes matured and fertilized in vitro. J. Reprod. Fertil. 92, 125–31.CrossRefGoogle ScholarPubMed
JrFulka, J., Jung, T. & Moor, R.M. (1992). The fall in biological maturation promoting factor (MPF) and histone H1 kinase activity during metaphase and telo phase in mouse oocytes. Mol. Reprod. Dev. 32, 378–82.CrossRefGoogle Scholar
Gall, L., Gall, F. & De Smedt, V.. (1993). Protein phosphorylation patterns during in vitro maturation of the goat oocyte. Mol. Reprod. Dev. 36, 500506.CrossRefGoogle ScholarPubMed
Hampl, A. & Eppig, J.J. (1995). Analysis of the mechanism(s) of metaphase I arrest in maturing mouse oocytes. Development 121, 925–33.CrossRefGoogle ScholarPubMed
Hyttel, P., Xu, K.P., Smith, S. & Greve, T. (1986). Ultrastructure of in-vitro oocyte maturation in cattle. J. Reprod. Fertil. 78, 615–25.CrossRefGoogle ScholarPubMed
Kaláb, P., Verlhac, M.-H., Kubiak, J., Colledge, W. & Maro, B. (1996). The activation of p90rsk in maturing mouse oocytes and eggs and during the first mitosis: MAP kinase independent and dependent activation. Development 122, 1957–64.CrossRefGoogle ScholarPubMed
Kalous, J., Kubelka, M., Rimkevičová, Z., Guerrier, P. & Motlík, J. (1993). Okadaic acid accelerates germinal vesicle breakdown and overcomes cycloheximide and 6-dimethylaminopurine block in cattle and pig oocytes. Dev. Biol. 157, 448–54.CrossRefGoogle ScholarPubMed
Kastrop, P.M.M., Bevers, M.M., Destre´e, O.H.J. & Kruip, T.A.M. (1990 a). Analysis of protein synthesis in morphologically classified bovine follicular oocytes before and after maturation in vitro. Mo!. Reprod. Dev. 26, 222–6.CrossRefGoogle ScholarPubMed
Kastrop, P.M.M., Bevers, M.M., Destre´e, O.H.J. & Kruip, T.A.M. (1990 b). Changes in protein synthesis and phosphorylation patterns during bovine oocyte maturation in vitro. J. Reprod. Fertil. 90, 305–10.CrossRefGoogle ScholarPubMed
Kastrop, P.M.M., Hulshof, S.C.J., Bevers, M.M., Destrée, O.H.J & Kruip, T.A.M. (1991). The effect of alpha-amanitin and cycloheximide on nuclear progression protein synthesis, and phosphorylation during bovine oocyte maturation in vitro. Mol. Reprod. Dev. 28, 249–54.CrossRefGoogle ScholarPubMed
Kubiak, J.Z., Weber, M., Ge´raud, G. & Maro, B. (1992). Cell cycle modification during the transitions between meiotic M-phases in mouse oocytes. J. Cell Sci. 102, 457–67.CrossRefGoogle ScholarPubMed
Kubiak, J.Z., Weber, M., Géraud, G., & Maro, B. (1992). Cell cycle modification during the transitions between meiotic M-phases in mouse oocytes. J. Cell Sci. 102, 457–67.CrossRefGoogle ScholarPubMed
Kubiak, J.Z., Weber, M., de Pennart, H., Winston, N.J. & Maro, B. (1993). The metaphase II arrest in mouse oocytes is controlled through microtubule dependent destruction of cyclin B in the presence of CSF. EMBO J. 12, 3773–8.CrossRefGoogle ScholarPubMed
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–95.CrossRefGoogle ScholarPubMed
Lu, K.H., Gordon, I., Chen, H.B., Gallagher, M. & McGovern, H. (1988). Birth of twins after transfer of cattle embryos produced by in vitro techniques. Vet. Rec. 122, 529–40.CrossRefGoogle ScholarPubMed
Moos, J., Visconti, P.E., Moore, G.D., Schultz, R.M. & Kopf, G.S. (1995). Potential role of mitogen-activated protein kinase in pronuclear envelope assembly and disassembly following fertilization of mouse eggs. Biol. Reprod. 53, 692–9.CrossRefGoogle ScholarPubMed
Motlík, J. & Kubelka, M. (1990). Cell-cycle aspects of growth and maturation of mammalian oocytes. Mol. Reprod. Dev. 27, 366–75.CrossRefGoogle ScholarPubMed
Motlík, J., Lie, B. & Shioya, Y. (1990). Two sensitivity levels of cattle oocytes to puromycin. Biol. Reprod. 43, 994–8.CrossRefGoogle ScholarPubMed
O'Neill, G.T. & Kaufman, M.H. (1987). Ovulation and fertilization of primary and secondary oocytes in LT/Sv strain mice. Gamete Res. 18, 2736.CrossRefGoogle ScholarPubMed
Parrish, J.J., Kim, C.I. & Bae, I.H. (1992). Current concepts of cell-cycle regulation and its relationship to oocyte maturation, fertilization and embryo development. Theriogenology 38, 277–96.CrossRefGoogle ScholarPubMed
Pavlok, A., Lucas-Hahn, A. & Niemann, H. (1992). Fertilization and developmental competence of bovine oocytes derived from different categories of antral follicles. Mol. Reprod. Dev. 31, 63–7.CrossRefGoogle ScholarPubMed
Pavlok, A., Kopečný, V., Lucas-Hahn, A., & Niemann, H. (1993). Transcriptional activity and nuclear ultrastructure of 8-cell bovine embryos developed by in vitro maturation and fertilization of oocytes from different growth categories of antral follicles. Mol. Reprod. Dev. 35, 233–43.CrossRefGoogle ScholarPubMed
Presice, G.A. & Yang, X. (1994). Nuclear dynamics of parthenogenesis of bovine oocytes matured in vitro for 20 and 40h and activated with combined ethanol and cyclo heximide treatment. Mol. Reprod. Dev. 37, 61–8.CrossRefGoogle Scholar
Sagata, N., Watanabe, N., Van de Woude, G.F. & Ikawa, Y. (1989). The c-mos proto-oncogene product is a cytostatic factor responsible for meiotic arrest in vertebrate eggs. Nature 342, 512–18.CrossRefGoogle ScholarPubMed
Šimon, M., Jílek, F. & JrFulka, J. (1989). Effect of cyclohex imide upon maturation of bovine oocytes. Reprod. Nutr. Dev. 29, 533–40.CrossRefGoogle Scholar
Sirard, M.A., Leibfried-Rutledge, M.L., Parrish, J.J., Ware, C.B. & First, N.L. (1988). The culture of bovine oocytes to obtain developmentally competent embryos. Biol. Reprod. 39, 546–55.CrossRefGoogle ScholarPubMed
Sirard, M.A., Florman, H.M., Leibfried-Rutledge, M.L., Barnes, F.L. & First, N.L. (1989). Timing of nuclear progression and protein synthesis necessary for meiotic maturation of bovine oocytes. Biol. Reprod. 40, 1257–63.CrossRefGoogle ScholarPubMed
Takano, H., Koyama, K., Kozai, C., Kato, Y. & Tsunoda, Y. (1993). Effect of aging of recipient oocytes on the development of bovine nuclear transfer embryos in vitro. Theriogenology 39, 909–17.CrossRefGoogle ScholarPubMed
Telford, N.A., Watson, A.J. & Schultz, G.A. (1990). Transition from maternal to embryonic control in early mammalian development: a comparison of several species [review]. Mol. Reprod. Dev. 26, 90100.CrossRefGoogle ScholarPubMed
Verlhac, M.-H., de Pennart, H., Maro, B., Cobb, M.H. & Clarke, H.J. (1993). MAP kinase becomes stably activated at metaphase and is associated with microtubule-organizing centres during meiotic maturation of mouse oocytes. Dev. Biol. 158, 330–40.CrossRefGoogle ScholarPubMed
Verlhac, M. H., Kubiak, J.Z., Clarke, H.J. & Maro, B. (1994). Microtubule and chromatin behaviour follow MAP kinase activity but not MPF activity during meiosis in mouse oocytes. Development 120, 1017–25.CrossRefGoogle Scholar
Webb, M., Howlett, S.K. & Maro, B. (1986). Parthenogenesis and cytoskeleton organization in aging mouse oocyte. J. Embryol. Exp. Morphol. 95, 131–45.Google Scholar
Yang, X., Jiang, S. & Foote, R.H. (1991). Age-dependent activation, enucleation and nuclear transfer of bovine oocytes matured in vitro and in vivo [abstract]. Biol. Reprod. 44, 141.Google Scholar
Yang, X., Jiang, S. & Foote, R.H. (1993). Bovine oocyte development following different oocyte maturation and sperm capacitation procedures. Mol. Reprod. Dev. 34, 94100.CrossRefGoogle ScholarPubMed