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Accelerated modification of the zona pellucida is the primary cause of decreased fertilizability of oocytes in the 129 inbred mouse strain

Published online by Cambridge University Press:  21 December 2010

Toshiaki Hino ,
Kanako Oda ,
Kenji Nakamura ,
Hiroyuki Tateno ,
Yutaka Toyoda  and
Minesuke Yokoyama
Toshiaki Hino*
Affiliation:
Department of Biological Sciences, Asahikawa Medical University, 2–1 Midorigaoka-higashi, Asahikawa 078–8510, Japan. Mitsubishi Kagaku Institute of Life Sciences (MITILS), Tokyo, Japan.
Kanako Oda
Affiliation:
Mitsubishi Kagaku Institute of Life Sciences (MITILS), Tokyo, Japan. Center for Bioresource-based Researches, Brain Research Institute, Niigata University, Niigata, Japan.
Kenji Nakamura
Affiliation:
Mitsubishi Kagaku Institute of Life Sciences (MITILS), Tokyo, Japan.
Hiroyuki Tateno
Affiliation:
Department of Biological Sciences, Asahikawa Medical University, Hokkaido, Japan.
Yutaka Toyoda
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Hokkaido, Japan.
Minesuke Yokoyama
Affiliation:
Mitsubishi Kagaku Institute of Life Sciences (MITILS), Tokyo, Japan. Center for Bioresource-based Researches, Brain Research Institute, Niigata University, Niigata, Japan.
*
All correspondence to: Toshiaki Hino, Department of Biological Sciences, Asahikawa Medical University, 2–1 Midorigaoka-higashi, Asahikawa 078–8510, Japan. Tel: +81 166 68 2731. Fax: +81 166 68 2783. e-mail: [email protected]
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Summary

We investigated whether the small litter size in the 129 inbred mouse strain results from a reduction in oocyte fertilizability. Sensitivity of the zona pellucida to α-chymotrypsin was examined for oocytes collected at 14 h (shortly after ovulation), 17 h, and 20 h after hCG injection. Passage of spermatozoa through the zona pellucida (using an in vitro fertilization (IVF) technique) and the density of cortical granules were examined for oocytes collected at 14 and 17 h after hCG injection. The capability of the oolemma to fuse with the sperm plasma membrane was also evaluated by IVF using zona-free eggs. The zona pellucida became markedly resistant to the enzyme 17 h after hCG injection. IVF rates significantly decreased at this time. In addition, there was a significant reduction in the density of cortical granules. When zona-free oocytes were inseminated, high fertilization rates were obtained at both 17 and 14 h after hCG injection. These results indicate that accelerated modification of the zona pellucida primarily causes a decreased fertilizability of oocytes in 129 mice, resulting in the low reproductive performance of this strain.

Keywords

129 mouseCortical granulesFertilityOocyteZona pellucida
Type
Research Article
Information
Zygote , Volume 19 , Issue 4 , November 2011 , pp. 315 - 322
Copyright
Copyright © Cambridge University Press 2010

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References

Barlow, P., Englert, Y., Puissant, F., Lejeune, B., Delvigne, A., Van Rysselberge, M. & Leroy, F. (1990). Fertilization failure in IVF: why and what next? Hum. Reprod. 5, 451–6.CrossRefGoogle ScholarPubMed
Barros, C. & Yanagimachi, R. (1971). Induction of zona reaction in golden hamster eggs by cortical granule material. Nature 233, 268–9.CrossRefGoogle ScholarPubMed
Braden, A.W.H. (1962). Spermatozoon penetration and fertilization in the mouse. Symp. Genet. Biol. Italica Pavia Italy 9, 94–101.Google Scholar
Braden, A.W.H. & Austin, C.R. (1954). Fertilization of the mouse egg and the effect of delayed coitus and of hot-shock treatment. Aust. J. Biol. Sci. 7, 552–65.CrossRefGoogle ScholarPubMed
Buhi, W.C. (2002). Characterization and biological roles of oviduct-specific, oestrogen-dependent glycoprotein. Reproduction 123, 355–62.CrossRefGoogle ScholarPubMed
Byers, S.L., Payson, S.J. & Taft, R.A. (2006). Performance of ten inbred mouse strains following assisted reproductive technologies (ARTs). Theriogenology 65, 1716–26.CrossRefGoogle ScholarPubMed
Collas, P., Balise, J.J., Hofmann, G.A. & Robl, J.M. (1989). Electrical activation of mouse oocytes. Theriogenology 32, 835–44.CrossRefGoogle ScholarPubMed
Coy, P., Cánovas, S., Mondéjar, I., Saavedra, M.D., Romar, R., Grullón, L., Matás, C. & Avilés, M. (2008). Oviduct-specific glycoprotein and heparin modulate sperm-zona pellucida interaction during fertilization and contribute to the control of polyspermy. Proc. Natl. Acad. Sci. USA 105, 15809–14.CrossRefGoogle Scholar
Ducibella, T., Anderson, E., Albertini, D.F., Aalberg, J. & Rangarajan, S. (1988). Quantitative studies of changes in cortical granule number and distribution in the mouse oocyte during meiotic maturation. Dev. Biol. 130, 184–97.CrossRefGoogle ScholarPubMed
Edwards, R.G. & Gates, A.H. (1959). Timing of the stages of the maturation divisions, ovulation, fertilization and the first cleavage of eggs of adult mice treated with gonadotrophins. J. Endocrinol. 18, 292–304.CrossRefGoogle ScholarPubMed
Evans, M.J. & Kaufman, M.H. (1981). Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154–6.CrossRefGoogle ScholarPubMed
Festing, M.F.W. (1979). Inbred Strains in Biomedical Research. pp. 137–266. New York: Oxford University Press.CrossRefGoogle Scholar
Fulton, B.P. & Whittingham, D.G. (1978). Activation of mammalian oocytes by intracellular injection of calcium. Nature 273, 149–51.CrossRefGoogle ScholarPubMed
Gulyas, B.J. & Yuan, L.C. (1985). Cortical reaction and zona hardening in mouse oocytes following exposure to ethanol. J. Exp. Zool. 233, 269–76.CrossRefGoogle Scholar
Hino, T., Oda, K., Nakamura, K., Toyoda, Y. & Yokoyama, M. (2009). Low fertility in vivo resulting from female factors causes small litter size in 129 inbred mice. Reprod. Med. Biol. 8, 157–61.CrossRefGoogle ScholarPubMed
Kawai, Y., Hata, T., Suzuki, O. & Matsuda, J. (2006). The relationship between sperm morphology and in vitro fertilization ability in mice. J. Reprod. Dev. 52, 561–8.CrossRefGoogle ScholarPubMed
Krzanowska, H. (1972). Rapidity of removal in vitro of the cumulus oophorus and the zona pellucida in different strains of mice. J. Reprod. Fert. 31, 7–14.CrossRefGoogle ScholarPubMed
Kubiak, J.Z. (1989). Mouse oocytes gradually develop the capacity for activation during the metaphase II arrest. Dev. Biol. 136, 537–45.CrossRefGoogle ScholarPubMed
Lyng, R. & Shur, B.D. (2009). Mouse oviduct-specific glycoprotein is an egg-associated ZP3-independent sperm-adhesion ligand. J. Cell Sci. 122, 3894–906.CrossRefGoogle ScholarPubMed
Männikkö, M., Törmälä, R.M., Tuuri, T., Haltia, A., Martikainen, H., Ala-Kokko, L., Tapanainen, J.S. & Lakkakorpi, J.T. (2005). Association between sequence variations in genes encoding human zona pellucida glycoproteins and fertilization failure in IVF. Hum. Reprod. 20, 1578–85.CrossRefGoogle ScholarPubMed
Martin, G.R. (1981). Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma. Proc. Natl. Acad. Sci. USA. 78, 7634–8.CrossRefGoogle ScholarPubMed
Matin, A. (2007). What leads from dead-end? Cell. Mol. Life Sci. 64, 1317–22.CrossRefGoogle ScholarPubMed
Mintz, B. & Gearhart, J.D. (1973). Subnormal zona pellucida change in parthenogenetic mouse embryos. Dev. Biol. 31, 178–84.CrossRefGoogle ScholarPubMed
Molloy, D., Harrison, K., Breen, T. & Hennessey, J. (1991). The predictive value of idiopathic failure to fertilization on the first in vitro fertilization attempt. Fertil. Steril. 56, 285–9.CrossRefGoogle ScholarPubMed
Nagasawa, H., Miyamoto, M. & Fujimoto, M. (1973). Reproductivity in inbred strains of mice and project for their efficient production. Jikken Dobutsu 22, 119–26. [In Japanese]Google ScholarPubMed
Nomura, T. & Katsuki, M. (eds.) (1987). Hassei Kougaku Jikken Manual, p. 15. Tokyo: Kodansha-Scientific. [In Japanese]Google Scholar
Olds-Clarke, P. (1996). How does poor motility alter sperm fertilizing ability? J. Androl. 17, 183–6.CrossRefGoogle ScholarPubMed
Roest, J., Van Heusden, A.M., Zeilmaker, G.H. & Verhoeff, A. (1998). Treatment policy after poor fertilization in the first IVF cycle. J. Assist. Reprod. Genet. 15, 18–21.CrossRefGoogle ScholarPubMed
Sato, K. (1979). Polyspermy – preventing mechanisms in mouse eggs fertilized in vitro. J. Exp. Zool. 210, 353–59.CrossRefGoogle ScholarPubMed
Schmell, E.D. & Gulyas, B.J. (1980). Ovoperoxidase activity in ionophore treated mouse eggs. II. Evidence for the enzyme's role in hardening the zona pellucida. Gamete Res. 3, 279–90.CrossRefGoogle Scholar
Smithberg, M. (1953). The effect of different proteolytic enzymes on the zona pellucida of mouse ova. Anat. Rec. 117, 554.Google Scholar
Stevens, L.C. (1967). The biology of teratomas. Adv. Morphog. 6, 1–31.CrossRefGoogle ScholarPubMed
Suzuki-Migishima, R., Hino, T., Takabe, M., Oda, K., Migishima, F., Morimoto, Y., & Yokoyama, M. (2009). Marked improvement of fertility of cryopreserved C57BL/6J mouse sperm by depletion of Ca2+ in medium. J. Reprod. Dev. 55, 386–92.CrossRefGoogle ScholarPubMed
Sztein, J.M., Farley, J.S. & Mobraaten, L.E. (2000). In vitro fertilization with cryopreserved inbred mouse sperm. Biol. Reprod. 63, 1774–80.Google ScholarPubMed
Toyoda, Y., Yokoyama, M. & Hosi, T. (1971a). Studies on the fertilization of mouse eggs in vitro. I. In vitro fertilization of eggs by fresh epididymal sperm. Jpn. J. Anim. Reprod. 16, 147–51.Google Scholar
Toyoda, Y., Yokoyama, M. & Hosi, T. (1971b). Studies on the fertilization of mouse eggs in vitro. II. Effects of in vitro preincubation of spermatozoa on time of sperm penetration of mouse eggs in vitro. Jpn. J. Anim. Reprod. 16, 152–7.CrossRefGoogle Scholar
Verley, F.A., Grahn, D., Leslie, W.P. & Hamilton, K.F. (1967). Sex ration of mice as possible indicator of mutation rate for sex-linked lethals. J. Hered. 58, 285–90.CrossRefGoogle Scholar
Xu, Z., Abbott, A., Kopf, G.S., Schultz, R.M. & Ducibella, T. (1997). Spontaneous activation of ovulated mouse eggs: time-dependent effects on M-phase exit, cortical granule exocytosis, maternal messenger ribonucleic acid recruitment, and inositol 1,4,5-trisphosphate sensitivity. Biol. Reprod. 57, 743–50.CrossRefGoogle ScholarPubMed