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Maturation of hamster oocytes under chemically defined conditions and sperm penetration through the zona pellucida

Published online by Cambridge University Press:  26 September 2008

Seiji Kito  and
Barry Bavister
Seiji Kito
Affiliation:
Department of Animal Health and Biomedical Sciences, University of Wisconsin-Madison, Madison, Wisconsin, USA.
Barry Bavister*
Affiliation:
Department of Animal Health and Biomedical Sciences, University of Wisconsin-Madison, Madison, Wisconsin, USA.
*
Dr Barry D. Bavister, Dept of AHABS, University of Wisconsin-Madison, 1655 Lindon Drive, Madison, WI 53706, USA. Telephone: +1 (608) 262-0728. Fax: +1 (608) 262-7420.
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Summary

This study aimed to achieve high frequencies of nuclear maturation and penetrability through the zona pellucida of hamster oocytes cultured under protein-free conditions. Completion of nuclear maturation by cumulus-intact, immature oocytes (79% metaphase II stage) was depressed (37% p < 0·05) by adding four amino acids (glutamine, isoleucine, methionine and phenylalanine) reported necessary for nuclear maturation of cumulus-free oocytes. Following in vitro maturation, cumulus cells were removed and oocytes were inseminated with capacitated sperm, but after 6 h sperm:egg co-incubation, only 24% of in vitro matured oocytes were penetrated compared with 60% of in vivo matured oocytes (p < 0·05). Time required for zona lysis by α-chymotrypsin was not significantly different among in vitro and in vivo matured oocytes and 1-cell embryos. Addition to the maturation medium of soybean trypsin inhibitor or fetuin, both known to inhibit the zona reaction in vitro, did not improve penetrability of in vitro matured oocytes, implying that in hamsters, unlike other rodent species, a premature zona reaction is unlikely to be responsible for inhibiting sperm penetration. When oocytes were incubated with 20% periovulatory oviductal fluid (OF) for another 3 h after maturation, penetration was significantly improved (60% vs 37% with and without OF, respectively; p < 0·05), but was not equivalent to penetration of in vivo matured follicular oocytes similarly treated with OF (84%, p < 0·05)However, zona penetration was further improved by increasing sperm concentration from 1·0 × 104 (66%) to 5·0 or 10·0 × 104 sperm/ml (89%, p < 0·05). This study shows that nuclear maturation of hamster oocytes can occur in chemically defined medium, and indicates that a deficiency in the zona of in vitro matured oocytes can be overcome by preincubation with OF and insemination at high sperm conccentration.

Keywords

Amino acidsHamsterNuclear maturationOviductal fluidSperm concentration
Type
Article
Information
Zygote , Volume 4 , Issue 3 , August 1996 , pp. 199 - 210
Copyright
Copyright © Cambridge University Press 1996

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References

Albertini, E. & Anderson, E. (1979). The appearance and structure of the intercellular connections during the ontogeny of the rabbit ovarian follicle with special reference to gap junction. J. Cell Biol. 2, 234–50.Google Scholar
Barnett, D.K. & Bavister, B.D. (1992). Hypotaurine requirement for in vitro development of golden hamster one-cell embryos into morulae and blastocysts, and production of term offspring from in vitro-fertilized ova. Biol. Reprod. 47, 297–304.CrossRefGoogle ScholarPubMed
Bavister, B.D. (1989). A consistently successful procedure for in vitro fertilization of golden hamster eggs. Gamete Res. 23, 139–58.CrossRefGoogle ScholarPubMed
Bavister, B.D. (1995). Culture of preimplantation embryos: facts and artifacts. Hum. Reprod. Update. 1, 91–148.CrossRefGoogle Scholar
Bavister, B.D., Leibfried, M.L. & Leiberman, G. (1983). Development of preimplantation embryos of the golden hamster in a defined culture medium. Biol. Reprod. 28, 235–47.CrossRefGoogle Scholar
Boatman, D.E. & Magnoni, G.E. (1995). Identification of a sperm penetration factor in the oviduct of the golden hamster. Biol. Reprod. 52, 199–207.CrossRefGoogle ScholarPubMed
Boatman, D.E. & Felson, S.E. & Kimura, J. (1994). Changes in morphology, sperm penetration and fertilization of ovulated hamster eggs induced by oviductal exposure. Hum. Reprod. 9, 519–26.CrossRefGoogle ScholarPubMed
Chen, L., Wert, S.E., Hendrix, E.M., Russell, P.T., Cannon, M. & Larsen, W.J. (1990). Hyaluronic acid synthesis and gapjuction endocytosis are necessary for normal expansion of the cumulus mass. Mol. Reprod. Dev. 26, 236–47.CrossRefGoogle ScholarPubMed
De Felici, M. & Siracusa, G. (1982). Spontaneous hardening of the zona pellucida of mouse oocytes during in vitro culture. Gamete. Res. 6, 107–13.CrossRefGoogle Scholar
De Felici, M., Salustri, A. & Siracusa, G. (1985). ‘Spontaneous’ hardening of the zona pellucida of mouse oocytes during in vitro culture. II. The effects of follicular fluid and glycosaminoglycans. Gamete Res. 12, 227–35.CrossRefGoogle Scholar
Donahue, R.P. (1968). Maturation of the mouse oocytes in vitro. I. Sequence and tirning of nuclear progression. J. Exp. Zool. 169, 237–50.CrossRefGoogle ScholarPubMed
Downs, S.M., Schroeder, A.C. & Eppig, J.J. (1986). Serum maintains the fertilizability of mouse oocytes matured in vitro by preventing hardening of the zona pellucida. Gamete Res. 15, 115–22.CrossRefGoogle Scholar
Ducibella, T., Duffy, P., Reindollar, R. & Su, B. (1990 a). Changes in the distribution of mouse oocyte cortical granules and ability to undergo the cortical reaction during gonadotropin-stimulated meioitic maturation and aging in vivo. Biol. Reprod. 43, 870–6.CrossRefGoogle Scholar
Ducibella, T., Kurawawa, S., Rangarajan, S., Kopf, G.S. & Schutz, R.M. (1990 b). Precocious loss of cortical granules during mouse oocyte meiotic maturation and correlation with an egg-induced modification of the zona pellucida. Dev. Biol. 137, 46–55.CrossRefGoogle ScholarPubMed
Eppig, J.J., Schroeder, A.C. & O'Brien, M.J. (1992). Developmental capacity of mouse oocytes matured in vitro: effects of gonadotrophic stimulation, follicular origin and oocyte size. J.Reprod. Fertil. 95, 119–27.CrossRefGoogle ScholarPubMed
Eppig, J.J.Schultz, R.M., O'Brien, M. & Chesnel, F. (1994). Relationship between the developmental programs controlling nuclear and cytoplasmic maturation of mouse oocytes. Dev. Biol. 164, 1–9.CrossRefGoogle ScholarPubMed
Fraser, L.R. & Drury, L.M. (1975). The relationship between sperm concentration and fertilization in vitro of mouse eggs. Biol. Reprod. 13, 513–18.CrossRefGoogle ScholarPubMed
Gwatkin, R.B.L. & Haidri, A.A. (1973). Requirements for the maturation of hamster oocytes in vitro. Exp. Cell Re. 76, 1–7.CrossRefGoogle ScholarPubMed
Gwatkin, R.B.L., Williams, D.T., Hartmann, J.F. & Kniazuk, M. (1973). The zona reaction of hamster and mouse eggs: production in vitro by a trypsin-like protease from cortical granules. I. Reprod. Fertil. 32, 259–65.CrossRefGoogle ScholarPubMed
Harper, K.M. & Brackett, B.J. (1993). Bovine blastocyst development after in vitro maturation in a defined medium with epidermal growth factor and low concentration of gonadotropins. Biol. Reprod. 48, 409–16.CrossRefGoogle Scholar
Hoodbhoy, T.Talbot, P. (1994). Mammalian cortical granules: contensts, fate, and function. Mol. Reprod. Dev. 39, 439–48.CrossRefGoogle ScholarPubMed
Iwamatsu, T. & Yanagimachi, R. (1975). Maturation in vitro of ovarian oocytes of prepubertal and adult hamsters. J.Reprod. Fertil. 45, 83–90.CrossRefGoogle ScholarPubMed
Kalab, P., Kopf, G.S. & Schultz, R.M. (1991). Modifications of the mouse zona pellucida during oocyte maturation and egg activation: effects of newborn calf serum and fetuin. Biol. Reprod. 45, 783–7.CrossRefGoogle ScholarPubMed
Kalab, P., Schultz, R.M. & Kopf, G.S. (1993). Modifications of the mouse zona pellucida during oocyte maturation: inhibitory effects of follicular fluid, fetuin, and α2HS-glycoprotein. Biol. Reprod. 49, 561–7.CrossRefGoogle Scholar
Kito, S. & Bavister, B.D. (1994). Kinetics of sperm penetration and fertilization in matured follicular vs ovulated ova of golden hamsters. Biol. Reprod. Suppl. 51, 146.Google Scholar
Kito, S. & Bavister, B.D. (1996). Kinetics of sperm penetration and fertilization in vitro in hamster follicular and oviductal ova. J.Exp.Zool. 274, 373–83.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Leibfried, M.L. & Bavister, B.D. (1983). Fertilizability of in vitro matured oocytes from golden hamsters. J. Exp. Zool. 226, 481–5.CrossRefGoogle ScholarPubMed
Leibfried-Rutledge, M.L., Critser, E.S. & First, N.L. (1986). Effects of fetal calf serum and bovine serum albumin on in vitro maturation and fertilization of bovine and hamster cumulus-oocyte complexes. Biol. Reprod. 35, 850–7.CrossRefGoogle ScholarPubMed
Malette, B., Paquette, Y., Merlen, Y. & Bleau, G. (1995). Oviductins possess chitinase– and mucin–like domains: a lead in the search for the biological function of these oviductin-specific ZP-associating glycoproteins. Mol Reprod. Dev. 41, 384–97.CrossRefGoogle ScholarPubMed
Mandai, Y., Tuiki, A., Yoshida, H., Chida, S., Chan, W., Tamura, M., Murakami, T., Tozawa, H., Fukuya, T., Yajima, A. & Hoshiai, H. (1992). Fertizability of in vitro matured hamster follicular oocytes. J. Fertil. Implant. (Tokyo) 9, 223–6.Google Scholar
McKiernan, S.H., Bavister, B.D., & Tasca, R.J. (1991). Energy substrate requirements for in vitro development of hamster 1- and 2-cell embryos to the blastocyst stage. Hum. Reprod. 6, 64–75.CrossRefGoogle Scholar
McKiernan, S.H., Clayton, M.K. & Bavister, B.D. (1995). Analysis of stimulatory and inhibitory arnino in vitro. Mol. Reprod. Dev. 42, 188–99.CrossRefGoogle Scholar
Miller, D., Gong, X., Decker, G. & shur, B.D. (1993 a). Egg cortical granule N-acetylglucosaminidase is required for the mouse zona block to polyspermy. J. Cell Biol. 123, 1431–40.CrossRefGoogle ScholarPubMed
Miller, D., Gong, X. & shur, B.D. (1993 b). Sperm require β-N-acetylgylglucosaminidase to penetrate through the egg zona pellucida. Development. 118, 1279–89.CrossRefGoogle ScholarPubMed
Oehninger, S., Veeck, L., Franken, D., Kruger, T.F., Acosta, A.A. & Hodgen, G.D. (1991). Human preovulatory oocytes have a higher sperm-binding ability than immature oocytes under hemizona assay conditions: evidence supporting the concept of ‘zona maturation’. Fert. Steril. 55, 1165–70.CrossRefGoogle ScholarPubMed
Okada, A., Yanagimachi, R. & Yanagimachi, H. (1986). Development of a cortical granule-free area of cortex and the perivitelline space in the hamster oocyte during maturation and following ovulation. J. Submicrosc. Cytol. 18, 233–47.Google ScholarPubMed
Pincus, G. & Enzmann, E.V. (1935). The comparative behavior of mammalian eggs in vitro and in vivo. I. the activation of ovarian eggs. J. Exp. Med. 62, 665–75.CrossRefGoogle ScholarPubMed
Racowsky, C. & Satterlie, R.A. (1985). Metabolic, fluorescent dye and electrical coupling between hamster oocytes and cumulus cells during meiotic maturation in vivo and and in vitro. Dev. Biol. 108, 191–202.CrossRefGoogle ScholarPubMed
Rose, T.A.&Bavister, B.D. (1992). Effect of oocyte maturation medium on in vitro development of in vitro fertilized bovine embryos.CrossRefGoogle Scholar
Saeki, K., Hoshi, M., Leibfried-Rutledge, M.L. & First, N.L. (1991). in vitro fertilization and development of bovine oocytes matured in serum-free medium. Biol. Reprod. 44, 256–60.CrossRefGoogle ScholarPubMed
Schramm, R.D. & Bavister, B.D. (1994). Follicle-stimulating hormone, priming of rhesus morkeus enhances meiotic and developmental competence of oocytes matured in vitro. Biol. Reprod. 51, 904–12.CrossRefGoogle ScholarPubMed
Schroeder, A.C. & Eppig, J.J. (1984). The developmental capacity of mouse oocytes that matured spontaneously in vitro is normal. Dev. Biol. 102, 493–7.CrossRefGoogle Scholar
Schroeder, A.C.Schultz, R.M., Kopf, G.S., Taylor, F.R., Backer, R.B.&Eppig, J.J. (1990). Fetuin inhibits zona pellucida hardering and conversion of ZP2 to ZP2f during spontaneous mouse oocyte maturation in vitro in the absence of serum. Biol. Reprod. 43, 891–7.CrossRefGoogle Scholar
Siddiquey, A.k. & Cohen, J. (1982). in vitro fertilization in the mouse and the relevance of different sperm/egg concentrations and volumes. J. Reprod. Fertil. 66, 237–42.CrossRefGoogle ScholarPubMed
Vanderhyden, B.C. & Armstrong, D.T. (1989). Role of cumulus cells and serum of the in vitro maturation, fertilization and subsequent development of rat oocytes. Biol. Reprod. 40, 720–8.CrossRefGoogle ScholarPubMed
Wolf, D.P., Byrd, W., Danadekar, P.&Quigley, M.M. (1984). Sperm concentration and fertilization of human eggs in vitro. Biol. Reprod. 31, 837–48.CrossRefGoogle ScholarPubMed
Yanagimachi, R. (1994). Mammaliam fetilization. In the physiology of Reproduction, 2nd, E., Knobil & J.D., Neil, 189–317. New York: Raven Press.Google Scholar
Yang, C.H. & Yanagimachi, R. (1989). Difference between mature ovarian and oviductal oocytes: a study using the golden hamster. Hum. Reprod. 4, 63–71.CrossRefGoogle ScholarPubMed
Zhang, X., Rutledge, J.&Armstrong, D.T. (1991). Studies on zona hardening in rat oocytes that are matured in vitro in a serum-free medium. Mol. Reprod. Dev. 28, 292–6.CrossRefGoogle Scholar
Zar, J.H. (1984). Biostatistical Analysis. Englewood Cliffs, NJ: Prentice-Hall.Google Scholar