Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-18T06:07:25.670Z Has data issue: false hasContentIssue false

Chromosomes of mouse primary spermatocytes undergo meiotic divisions after incorporation into homologous immature oocytes

Published online by Cambridge University Press:  26 September 2008

Atsuo Ogura*
Affiliation:
Department of Veterinary Science, National Institute of Health, Tokyo, Japan
Teruhiko Wakayama
Affiliation:
Department of Veterinary Science, National Institute of Health, Tokyo, Japan
Osamu Suzuki
Affiliation:
Department of Veterinary Science, National Institute of Health, Tokyo, Japan
Tae-Young Shin
Affiliation:
Department of Veterinary Science, National Institute of Health, Tokyo, Japan
Junichiro Matsuda
Affiliation:
Department of Veterinary Science, National Institute of Health, Tokyo, Japan
Yoshiro Kobayashi
Affiliation:
Department of Veterinary Science, National Institute of Health, Tokyo, Japan
*
Atsuo Ogura, Department of Veterinary Science, National Institute of Health, 1–23–1, Toyama, Shinjuku, Tokyo 162, Japan. Fax: +81-3-5285-1150. e-mail: aogxura@nih.go.jp.

Summary

The primary spermatocytes used were male germ cells at prophase I. The present study was undertaken to see whether bivalent chromosomes of mouse primary spermatocytes can undergo meiotic divisions within maturing oocytes and participate in subsequent embryonic development. Primary spermatocytes (pachytene to diplotene) freshly collected from the testes of mature males were electrofused with immature oocytes shortly before or after germinal vesicle breakdown. After culture in MEM-α medium for 15 h, most (> 90%) of the oocytes containing spermatocyte chromosomes underwent maturation and arrested at metaphase II (Mil). Among 23 Mil oocytes examined, 17 (74%) had one group of chromosomes and one polar body, indicating that male chromosomes had intermingled with those of the females and completed the first meiotic division. Chromosome analyses of these Mil oocytes demonstrated their diploidy. The metaphase chromosomes were transferred to enucleated Mil oocytes freshly recovered from superovulated mice. After artificial activation, the reconstructed Mil oocytes resumed meiosis and developed to the morula/blastocyst stage. However, no pups were born following embryo transfer into recipient females. These findings indicate that the chromosomes of primary spermatocytes undergo meiotic divisions in maturing oocytes and participate in the formation of diploid embryos.

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

Chatot, C.L., Ziomek, C.A., Bavister, B.D., Lewis, J.L. & Torres, I. (1989). An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. J. Reprod. Fertil. 86, 679–88.Google Scholar
Ferrara, T.A., Alikani, M., Reing, A., Garrisi, G.J., Blake, M, Levron, J. & Cohen, J. (1996). Morphology of the human oolemma: a parameter for evaluating cytoplasmic maturation. Annual meeting of the American Society for Reproductive Medicine, p. 335.Google Scholar
Katoh, M. & Tanaka, N. (1980). Relationship between chromosome aberrations in the first-cleavage metaphase and unscheduled DNA synthesis following paternal MMS treatment (in Japanese with English abstract). Jpn. J. Genet. 55, 5565.Google Scholar
Kimura, Y. & Yanagimachi, R. (1995 a). Mouse oocytes injected with testicular spermatozoa or round spermatids can develop into normal offspring. Development 121, 2397–405.CrossRefGoogle ScholarPubMed
Kimura, Y. & Yanagimachi, R. (1995 b). Development of normal mice from oocytes injected with secondary spermatocyte nuclei. Biol. Reprod. 53, 855–62.CrossRefGoogle ScholarPubMed
Kimura, Y. & Yanagimachi, R. (1995 c). Intracytoplasmic sperm injection in the mouse. Biol. Reprod. 52, 709–20.Google Scholar
Kono, T., Obata, Y, Yoshimizu, T., Nakahara, T. & Carroll, J. (1996). Epigenetic modifications during oocyte growth correlate with extended parthenogenetic development in the mouse. Nature Genet. 13, 91–4.Google Scholar
Ogura, A. & Yanagimachi, R. (1993). Round spermatid nuclei injected into hamster oocytes form pronuclei and participate in syngamy. Biol. Reprod. 48, 219–25.Google Scholar
Ogura, A., Yanagimachi, R. & Usui, N. (1993). Behavior of hamster and mouse round spermatid nuclei incorporated into mature oocytes by electrofusion. Zygote 1, 18.Google Scholar
Ogura, A., Matsuda, J. & Yanagimachi, R. (1994). Birth of normal young following fertilization of mouse oocytes with round spermatids by electrofusion. Proc. Natl. Acad. Sci. USA 91, 7460–2.CrossRefGoogle Scholar
Ogura, A., Yamamoto, Y, Suzuki, O., Takano, K., Waka-yama, T., Mochida, K. & Kimura, H. (1996). In vitro fertilization and microinsemination with round spermatids for propagation of nephrotic genes in mice. Theriogen-ology 45, 1141–9.Google Scholar
Sofikitis, N.V., Miyagawa, I., Agapitos, E., Pasyianos, P., Toda, T., Hellstrom, W. J. G. & Kawamura, H. (1994). Reproductive capacity of the nucleus of the male gamete after completion of meiosis. J. Assist. Reprod. Genet. 11, 335–41.Google Scholar
Tesarik, J., Mendoza, C. & Testart, J. (1995). Viable embryos from injection of round spermatids into oocytes N. Engl. J. Med. 333,525.CrossRefGoogle ScholarPubMed
Tsunoda, Y, Yasui, T., Nakamura, K., Uchida, T. & Sugie, T. (1986). Effect of cutting the zona pellucida on the pro-nuclear transplantation in the mouse. J. Exp. Zool. 240, 119–25.CrossRefGoogle Scholar
Wiltshire, T., Park, C, Caldwell, K.A. & Handel, M.A. (1995). Induced premature G2/M-phase transition in pa-chytene spermatocytes includes events unique to meiosis. Dev. Biol. 169, 557–67.Google Scholar
Yanagida, K., Yanagimachi, R., Perreault, S. D. & Kleinfeld, R. G. (1991). Thermostability of sperm nuclei assessed by microinjection into hamster oocytes. Biol. Reprod. 44, 440–7.Google Scholar