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The oocyte activation and Ca2+ oscillation-inducing abilities of mouse and human dead (sonicated) spermatozoa

Published online by Cambridge University Press:  01 May 2009

Hiroyuki Yazawa ,
Kaoru Yanagida ,
Shoutaro Hayashi  and
Akira Sato
Hiroyuki Yazawa*
Affiliation:
Department of Obstetrics and Gynecology, Fukushima Red Cross Hospital, 11–31 Irie-cyo, Fukushima 960–8530, Japan.
Kaoru Yanagida
Affiliation:
Center for Infertility and IVF, International University of Health and Welfare, 537–1 Iguci, Nasuno-cyo Tochigi 329–2763, Japan.
Shoutaro Hayashi
Affiliation:
Department of Obstetrics and Gynecology, Fukushima Red Cross Hospital, 11–31 Irie-cyo, Fukushima 960–8530, Japan.
Akira Sato
Affiliation:
Department of Obstetrics and Gynecology, Fukushima Medical University, 1 Hikarigaoka, Fukushima 960–1295, Japan.
*
All correspondence to Hiroyuki Yazawa. Department of Obstetrics and Gynecology, Fukushima Red Cross Hospital, 11–31 Irie-cyo, Fukushima 960–8530, Japan. e-mail: [email protected]
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Summary

In ICSI procedures, it is well known that the selection of viable (live) spermatozoa and certain types of immobilization prior to injection is very important for obtaining successful results, but unfortunately there are rare situations when only immotile spermatozoa are available (such as in severe asthenozoospermia or necrozoospermia). In such cases, failure of oocyte activation after ICSI often occurs and may be due to the lack of SOAF (sperm-borne oocyte activating factor) activity. In order to investigate the SOAF activities of dead spermatozoa, mouse and human spermatozoa were immobilized (killed by sonication), maintained in THF medium for varying time intervals (up to 72 h) and then injected into mature unfertilized mouse oocytes. Injected mouse oocytes were examined for their activation, development into blastocysts and Ca2+ responses by imaging and confocal laser scanning microscope. The rates of oocyte activation, blastocyst development and normal patterns of Ca2+ oscillation from the killed-sperm-injected oocytes decreased gradually in accordance with the maintenance interval between sonication and injection. For injection with mouse sonicated spermatozoa, the rate of normal Ca2+ oscillations declined first (after a 3 h maintenance interval) and then blastocyst development was gradually obstructed (after approx. 10 h). The oocyte activation-inducing ability of dead spermatozoa was maintained for a relatively long period, but began to decline after 20 h. The activation rates and Ca2+ response of the oocytes that were injected with human sonicated spermatozoa decreased earlier than those injected with mouse spermatozoa. Although the oocyte activation-inducing ability was maintained for a relatively long time after the death of the spermatozoa, embryo development into blastocysts and the rate of normal Ca2+ oscillations declined after a short maintenance interval between sonication and injection. The Ca2+ response seemed to be the most sensitive indicator for the evaluating the SOAF activity of dead (killed) spermatozoa.

Keywords

Ca2+ oscillationDead spermICSIOocyte activationSonication
Type
Research Article
Information
Zygote , Volume 17 , Issue 2 , May 2009 , pp. 175 - 184
Copyright
Copyright © Cambridge University Press 2009

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References

Coward, K., Ponting, C.P., Chang, H.Y., Hibbitt, O., Savolainen, P., Jones, K. & Parrington, J. (2005). Phospholipase Cζ, the trigger of egg activation in mammals, is present in a non-mammalian species. Reproduction 130, 157–63.CrossRefGoogle Scholar
Cox, L.J., Larman, M.G., Saunders, C.M., Hashimoto, K., Swann, K. & Lai, F.A. (2002). Sperm phospholipase Cζ from humans and cynomolgus monkeys trigger Ca2+ oscillations, activation and development of mouse oocytes. Reproduction 124, 611–23.CrossRefGoogle ScholarPubMed
Dozortsev, D., Rybouchikin, A., De Sutter, P., Qian, C. & Dhout, M. (1995). Human oocyte activation following intercytoplasmic injection: the role of the sperm cell. Hum. Reprod. 10, 403–7.CrossRefGoogle Scholar
Eldar-Geva, T., Brooks, B., Camnar, P., Marqalioth, E.J., Zylber-Haran, E. & Silber, S.J. (2003). Successful pregnancy delivery after calcium ionophore oocyte activation in normozoospermic patient with pervious repeated failed fertilization after intracytoplasmic sperm injection. Fertil. Steril. 79 (Suppl. 3), 1656–8.CrossRefGoogle Scholar
Elliasson, R., Mossberg, B., Camnar, P., & Afzelius, B.A. (1977). The immotile cilia syndrome: a congenital ciliary abnormality as an etiologic factor in chronic airway infections and male sterility. New Engl. J. Med. 297, 1–6.CrossRefGoogle Scholar
Fujimoto, S., Yoshida, N., Fukui, T., Amanai, M., Isobe, T., Itagaki, C., Izumi, T. & Perry, C.F. (2004). Mammalian phospholipase Cζ induces oocyte activation from the sperm perinuclear matrix. Dev. Biol. 274, 370–83.CrossRefGoogle ScholarPubMed
Kasai, T., Hoshi, K, & Yanagimachi, R. (1999). Effect of sperm immobilization and demembranation on the oocyte activation rate in the mouse. Zygote 7, 187–93.CrossRefGoogle ScholarPubMed
Kimura, Y. & Yanagimachi, R. (1995a). Intracytoplasmic sperm injection in the mouse. Biol. Reprod. 52, 709–22.CrossRefGoogle ScholarPubMed
Kimura, Y. & Yanagimachi, R. (1995b). Mouse oocyte injected with testicular spermatozoa or round spermatids can develop into normal offspring. Development 121, 2397–405.CrossRefGoogle ScholarPubMed
Kono, T., Jones, J.T., Swann, K. & Whittingham, D.G. (1995). Nuclei from fertilized mouse embryos have calcium-releasing activity. Development 121, 1123–8.CrossRefGoogle ScholarPubMed
Kuretake, S., Kimura, Y., Hoshi, K. & Yanagimachi, R. (1996). Fertilization and development of mouse oocytes injected with isolated sperm heads. Biol. Reprod. 55, 789–95.CrossRefGoogle ScholarPubMed
Larman, M.G., Saunders, C.M., Carroll, J., Lai, F.A. & Swann, K. (2004). Cell cycle-dependent Ca2+ oscillations in mouse embryos are regulated by nuclear targeting of PLCzeta. J. Cell Sci. 117, 2513–21.CrossRefGoogle ScholarPubMed
Mizuno, K., Hoshi, K. & Huang, T. (2002). Fertilization and embryo development in a mouse ICSI model using human and mouse sperm after immobilization in polyvinylpyrrolidone. Hum. Reprod. 17, 2350–5.CrossRefGoogle Scholar
Nagy, ZP., Liu, J., Joris, H., Verheyeu, G., Tournaye, H., Camus, M., Derde, MP., Devroey, P. & Van Stierteghem, AC. (1995). The result of intracytoplasmic sperm injection is not related to any of the three basic parameters. Hum. Reprod. 10, 1123–9.CrossRefGoogle ScholarPubMed
Oda, S. (2006). Mammalian sperm factor and phospholipase C zeta. J. Mamm. Ova Res. 23, 2–9.CrossRefGoogle Scholar
Ogonuki, N., Sankai, T., Yagami, K., Shikano, T., Oda, S., Miyazaki, S. & Ogura, A. (2001). Activity of a sperm-borne oocyte-activating factor in spermatozoa and spermatogenic cells from cynomolgus monkey and its localization after oocyte activation. Biol. Reprod. 63, 351–7.CrossRefGoogle Scholar
Ogura, A., Matsuda, J. & Yanagimachi, R. (1994). Birth of normal young after electrofusion of mouse oocytes with round spermatids. Proc. Natl. Acad. Sci. USA 91, 7460–2.CrossRefGoogle ScholarPubMed
Rogers, N.T., Hobson, E., Pickering, S., Lai, F.A., Braude, P. & Swann, K. (2004). Phospholipase Cζ causes Ca2+ oscillations and parthenogenetic activation of human oocytes. Reproduction 128, 697–702.CrossRefGoogle ScholarPubMed
Rybouchkin, A., Benijts, J., Sutter, P.D. & Dhont, M. (1997). Disintegration of chromosomes in dead sperm cells as revealed by injection into mouse oocytes. Hum. Reprod. 12, 1683–98.CrossRefGoogle ScholarPubMed
Saunders, C.M., Larman, M.G., Parrington, J., Cox, L.J., Royse, J., Blayney, L.M., Swamm, K. & Lai, F.A. (2002). PLCζ: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development. Development 129, 3533–44.CrossRefGoogle Scholar
Sone, Y., Ito, M., Shirakawa, H., Shikano, T., Takaeuchi, H., Kinoshita, K. & Miyazaki, S. (2005). Nuclear translocation of phospholipase C-zeta, an egg-activating factor, during early embryonic development. Biochem. Biophys. Res. Commun. 330, 690–4.CrossRefGoogle ScholarPubMed
Suzuki, K., Yanagida, K. & Yanagimachi, R. (1998). Comparison of the media for isolation and storage of round spermatid nuclei before intracytoplasmic injection. J. Assist. Reprod. Genet. 15, 154–8.CrossRefGoogle ScholarPubMed
Tateno, H., Kimura, Y. & Yanagimachi, R. (2000). Sonication per se is not deleterious to sperm chromosomes as previously inferred. Biol. Reprod. 63, 341–6.CrossRefGoogle Scholar
Tesaric, J. & Sousa, M. (1995). More tham 90% of fertilization rates after intracytoplasmic sperm injection and artificial induction of oocytes activation with calciums ionophore, Fertil. Steril. 63, 342–9.Google Scholar
Yanagida, K., Yanagimachi, R, Perreault, S.D. & Kleinfeld, RG. (1991). Thermostability of sperm nuclei assessed by micro-injection into hamster oocytes. Biol. Reprod. 44, 440–7.CrossRefGoogle Scholar
Yanagida, K., Katayose, H., Yazawa, H. & Sato, A. (1999). Successful fertilization and pregnancy following ICSI and electric oocyte activation. Hum. Reprod. 14, 1307–11.CrossRefGoogle ScholarPubMed
Yanagida, K., Morozumi, K., Katayose, H., Hayashi, S. & Sato, A. (2006). Successful pregnancy after ICSI with strontium oocyte activation in low rates of fertilization. Reprod. Biomed. Online 13, 801–6.CrossRefGoogle ScholarPubMed
Yanagimachi, R. (1998). Intracytoplasmic sperm injection experiments using the mouse as model. Hum. Reprod. 13 (Suppl.), 87–98.CrossRefGoogle Scholar
Yanagimachi, R. (2005). Intracytoplasmic injection of spermatozoa nad spermatogenic cells: its biology and applications in human and animals. Reprod. Biomed. Online 10, 247–88.CrossRefGoogle Scholar
Yazawa, H., Yanagida, K., Katayose, H., Hayashi, S. & Sato, A. (2000). Comparision 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 Scholar
Yazawa, H., Yanagida, K. & Sato, A. (2001). Oocyte activation and Ca2+ oscillation-inducing abilities of mouse round/elongated spermatids and the developmental capacities of embryos from spermatid injection. Hum. Reprod. 16, 1221–8.CrossRefGoogle ScholarPubMed
Yazawa, H., Yanagida, K. & Sato, A. (2007). Human round spermatids form azoospermic men exhibit oocyte-activation and Ca2+ oscillation-inducing activities. Zygote 15, 337–46.CrossRefGoogle Scholar
Yoda, A., Oda, S., Shikano, Y., Kouchi, Z., Awaji, Y., Shirakawa, H., Kinoshita, K. & Miyazaki, S. (2004). Ca2+ oscillation-inducing phospholipase C zeta expressed in mouse eggs is accumulated to the pronucleus during egg activation. Dev. Biol. 268, 245–57.CrossRefGoogle Scholar
Yu, Y., Saunders, C.M., Lai, F.A. & Swann, K. (2007). Preimplantation development of mouse oocytes activated by different levels of human phospholipase C zeta. Hum. Reprod. published online November 14.Google Scholar