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The ability of whale haploid spermatogenic cells to induce calcium oscillations and its relevance to oocyte activation

Published online by Cambridge University Press:  01 May 2007

K. Amemiya ,
M. Hirabayashi ,
H. Ishikawa ,
Y. Fukui  and
S. Hochi
K. Amemiya
Affiliation:
Faculty of Textile Science and Technology, Shinshu University, Ueda, Nagano 386–8567, Japan.
M. Hirabayashi
Affiliation:
National Institute for Physiological Sciences, Okazaki, Aichi 444–8787, Japan.
H. Ishikawa
Affiliation:
The Institute of Cetacean Research, Chuo-ku, Tokyo 104–0055, Japan.
Y. Fukui
Affiliation:
Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido 080–8555, Japan.
S. Hochi*
Affiliation:
Faculty of Textile Science and Technology, Shinshu University, Ueda, Nagano 386–8567, Japan.
*
All correspondence to: Shinichi Hochi, Faculty of Textile Science and Technology, Shinshu University, Ueda, Nagano 386–8567, Japan. Tel: +81 268 21 5350. Fax: +81 268 21 5830. e-mail: [email protected]
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Summary

Interspecies microinsemination assay was applied to examine the ability of minke whale haploid spermatogenic cells to induce Ca2+ oscillations and oocyte activation. Populations of round spermatids (RS), early-stage elongating spermatids (e-ES), late-stage elongating spermatids (1-ES) and testicular spermatozoa (TS) were cryopreserved in the presence of 7.5% glycerol on board ship in the Antarctic Ocean. Repetitive increases of intracellular Ca2+ concentration occurred in 0, 65, 81 and 96% of BDF1 mouse oocytes injected with the postthaw RS, e-ES, 1-ES and TS, respectively. A normal pattern of the Ca2+ oscillations was observed in 26–47% of the responding oocytes. Most oocytes that exhibited Ca2+ oscillations, regardless of the oscillation pattern, resumed meiosis (83–94%). These results indicate that whale spermatogenic cells acquire SOAF activity, which is closely related to their Ca2+ oscillation-inducing ability at the relatively early stage of spermiogenesis.

Keywords

Ca2+ oscillationsMinke whaleMouse assaySOAFSpermiogenesis
Type
Research Articles
Information
Zygote , Volume 15 , Issue 2 , May 2007 , pp. 103 - 108
Copyright
Copyright © Cambridge University Press 2007

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References

Amemiya, K., Iwanami, Y., Kobayashi, T., Terao, T., Fukui, Y., Ishikawa, H., Ohsumi, S., Hirabayashi, M. & Hochi, S. (2004). Acquirement of oocyte-activating factor in Antarctic minke whale (Balaenoptera bonaerensis) spermatogenic cells, assessed by meiosis resumption of microinseminated mouse oocytes. J. Mamm. Ova. Res. 21, 149–56.CrossRefGoogle Scholar
Brackett, B.G. & Oliphant, G. (1975). Capacitation of rabbit spermatozoa in vitro. Biol. Reprod. 12, 260–74.Google Scholar
Chatot, C.L., Lewis, J.L., Torres, I. & Ziomek, A. (1990). Development of 1-cell embryos from different strains of mice in CZB medium. Biol. Reprod. 42, 432–40.Google Scholar
Cox, L.J., Larman, M.G., Saunders, C.M., Hashimoto, Swann, K. & Lai, F.A. (2002). Sperm phospholipase Czete from humans and cynomolgus monkeys triggers Ca oscillations, activation and development of mouse oocytes. Reproduction 124, 611–23.CrossRefGoogle ScholarPubMed
Cuthbertson, K.W., Whittingham, D.G. & Cobbold, P.H. (1981). Free Ca increases in exponential phases during mouse oocyte activation. Nature 294, 754–7.CrossRefGoogle Scholar
Gordo, A.C., Wu, H., He, C.L. & Fissore, R.A. (2000). Injection of sperm cytosolic factor into mouse metaphase II oocytes induces different developmental fates according to the frequency [Ca2+]i oscillations and oocyte age. Bio. Reprod. 62, 1370–9.Google Scholar
Haigo, K., Yamauchi, Y., Yazama, F., Yanagimachi, R. & Horiuchi, T. (2004). Full-term development of hamster embryos produced by injection of round spermatids into oocytes. Biol. Reprod. 71, 194–8.Google Scholar
Hanada, A. & Chang, M.C. (1972). Penetration of zona-free eggs by spermatozoa of different species. Biol. Reprod. 6, 300–9.CrossRefGoogle Scholar
Hirabayashi, M., Kato, M., Aoto, T., Ueda, M. & Hochi, S. (2002). Rescue of infertile transgenic rat lines by intracytoplasmic injection of cryopreserved round spermatids. Mol Reprod. Dev. 62, 295–9.Google Scholar
Kimura, Y., Yanagimachi, R., Kuretake, S., Bortkiewicz, H., Perry, A.C.F. & Yanagimachi, H. (1998). Analysis of mouse oocyte activation suggests the involvement of sperm perinuclear material. Biol. Reprod. 58, 1407–15.CrossRefGoogle ScholarPubMed
Kobayashi, T., Amemiya, K., Takeuchi, K., Tsujioka, T., Tominaga, K., Hirabayashi, M., Ishikawa, H., Fukui, Y. & Hochi, S. (2006). Contribution of spermatozoal centrosomes to microtubule-organizing centre in Antarctic minke whale (Balaenoptera bonaerensis). Zygote 14, 45–51.CrossRefGoogle ScholarPubMed
Mogoe, T., Fukui, Y., Ishikawa, H. & Ohsumi, S. (1998). Effect of diluent composition and temperature on motility and viability after liquid storage and cryopreservation of minke whale (Balaenoptera bonaerensis) spermatozoon. Mar. Mamm. Sci. 14, 854–60.CrossRefGoogle Scholar
Ogonuki, N., Sankai, T., Yagami, K., Shikano, T., Oda, S., Miyazaki, S. & Ogura, A. (2001). Activity of sperm-borne oocyte-activating factor in spermatozoa and spermatogenic cells from cynomolgus monkeys and its localization after oocyte activation. Biol. Reprod. 65, 351–7.Google Scholar
Ogonuki, N., Inoue, K., Miki, H., Mochida, K., Hatori, M., Okada, H., Takeiri, S., Shimozawa, N., Nagashima, H., Sankai, T. & Ogura, A. (2005). Differential development of rabbit embryos following microinsemination with sperm and spermatids. Mol. Reprod. Dev. 72, 411–7.CrossRefGoogle ScholarPubMed
Ogura, A., Matsuda, J., Asano, T., Suzuki, O. & Yanagimachi, R. (1996). Mouse oocytes injected with cryopreserved round spermatids can develop into normal offspring. J. Assist. Reprod. Genet. 5, 431–4.CrossRefGoogle Scholar
Ryan, T.A. (1960). Significance tests for multiple comparisons of proportions, variances, and other statistics. Psychol. Bull. 57, 318–28.Google Scholar
Rybouchkin, A., Dozortsev, D., De Sutter, P., Quin, C. & Dhont, M. (1995). Intracytoplasmic injection of human spermatozoa into mouse oocytes: a useful model to investigate the oocyte-activating capacity and the karyotype of human spermatozoa. Hum. Reprod. 10, 1130–5.Google Scholar
Saunders, C.M., Larman, M.G., Parrington, J., Cox, L.J., Royse, J., Blayney, L.M., Swann, K. & Lai, F.A. (2002). PLCζ: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development. Development 129, 3533–44.Google Scholar
Sousa, M., Mendoza, C., Barros, A. & Tesarik, J. (1996). Calcium responses of human oocytes after intracytoplasmic injection of leukocytes, spermatocytes and round spermatids. Mol. Hum. Reprod. 2, 853–7.CrossRefGoogle ScholarPubMed
Stricker, S.A. (1999). Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev. Biol. 211, 157–76.CrossRefGoogle ScholarPubMed
Sun, F.Z., Hoyland, J., Huang, X., Mason, W. & Moor, R.W. (1992). A comparison of intracellular changes in porcine eggs after fertilization and electroactivation. Development 115, 947–56.CrossRefGoogle ScholarPubMed
Swann, K. (1990). A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs. Development 110, 1295–302.Google Scholar
Terada, Y., Nakamura, S., Simerly, C., Hewitson, L., Murakami, T., Yaegashi, N., Okamura, K. & Schatten, G. (2004). Centrosomal function assessment in human sperm using heterologous ICSI with rabbit eggs: a new male factor infertility assay. Mol. Reprod. Dev. 67, 360–5.Google Scholar
Tesarik, J., Mendoza, C. & Testart, J. (1995). Viable embryos from injection of round spermatids into oocytes. New Engl. J. Med. 333, 525.CrossRefGoogle ScholarPubMed
Yazawa, H., Yanagida, K., Katayose, H., Hayashi, S. & Sato, A. (2000). Comparison of oocyte activation and Ca2+ oscillation-inducing abilities of round/elongated spermatids of mouse, hamster, rat, rabbit and human assessed by mouse oocyte activation assay. Hum. Reprod. 15, 2582–90.CrossRefGoogle ScholarPubMed