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Sperm head binding to epithelium of the oviduct isthmus is not an essential preliminary to mammalian fertilization - review

Published online by Cambridge University Press:  21 July 2010

R. H. F. Hunter*
Affiliation:
Institute for Reproductive Medicine, Hannover Veterinary University, Bünteweg 15, D-30559 Hannover, Germany.
*
All correspondence to: R.H.F. Hunter. Institute for Reproductive Medicine, Hannover Veterinary University, Bünteweg 15, D-30559 Hannover, Germany. Tel: +49 0511 953 8519. Fax: +49 0511 953 8504. e-mail: [email protected]

Summary

In endeavouring to understand the nature of sperm–oviduct interactions in mammals, attention was focused on experimental models in which fertilization can occur without a preliminary phase of sperm head binding to the isthmus epithelium. The ovarian endocrine milieu imposed on the oviduct tissues plays an important role in the binding phenomenon, although less so after the time of ovulation. Nonetheless, a sperm suspension introduced into the peritoneal cavity or surgical insemination directly into the oviduct ampulla before ovulation can result in fertilization, as can a surgical model in which the isthmus has been resected and the remaining portions of the duct reanastomosed. Mating or artificial insemination after ovulation in pigs permits rapid sperm transport to the site of fertilization, and the frequency of polyspermic penetration increases with the post-ovulatory age of eggs.

Strategies underlying sperm binding were considered, especially in terms of preovulatory sperm storage and suppression of full membranous maturation. These, in turn, raised the problem of how sperm binding in vitro to oviduct cells from prepuberal animals or to cells harvested during the luteal phase of the estrous cycle, or to cells from the ampulla or even the tracheal epithelium, can act to regulate sperm storage and maturation with precision. In an evolutionary perspective, preovulatory binding of diverse populations of cells to the endosalpinx may have developed as a form of fine tuning to assist in sperm selection, to synchronize completion of capacitation with the events of ovulation, and to promote monospermic fertilization by a controlled release of competent gametes.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

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References

Adams, C.E. (1969). Intraperitoneal insemination in the rabbit. J. Reprod. Fert. 18, 333–9.CrossRefGoogle ScholarPubMed
Beatty, R.A. (1957). Parthenogenesis and Polyploidy in Mammalian Development. Cambridge University Press, Cambridge, UK.Google Scholar
Bedford, J.M. (1982). Fertilisation. In Reproduction in Mammals, Book 1 (eds. Austin, C.R. & Short, R.V.) pp. 128–63. Cambridge: Cambridge University Press.Google Scholar
Bedford, J.M. (1983). Significance of the need for sperm capacitation before fertilisation in eutherian mammals. Biol. Reprod. 28, 108–20.CrossRefGoogle ScholarPubMed
Bomsel-Helmreich, O. (1965). Heteroploidy and embryonic death. In Preimplantation Stages of Pregnancy. Ciba Foundation Symposium (eds. Wolstenholme, G.E.W. & O'Connor, M.), pp. 246–67. London: Churchill.CrossRefGoogle Scholar
Chang, M.C. (1951). Fertilising capacity of spermatozoa deposited into the Fallopian tubes. Nature (London) 168, 697–8.CrossRefGoogle ScholarPubMed
Corner, G.W. (1923). Cyclic variation in uterine and tubal contraction waves. Amer. J. Anat. 32, 345–51.CrossRefGoogle Scholar
Fazeli, A., Duncan, A.E., Watson, P.F., Holt, W.V. (1999). Sperm–oviduct interaction: induction of capacitation and preferential binding of uncapacitated spermatozoa to oviductal cells in porcine species. Biol. Reprod. 60, 879–86.CrossRefGoogle ScholarPubMed
Gervasi, M.G., Rapanelli, M., Ribeiro, M.L., Farina, M., Billi, S., Franchi, A.M. & Martinez, S.P. (2009). The endocannabinoid system in bull sperm and bovine oviductal epithelium: role of anandamide in sperm–oviduct interaction. Reproduction 137, 403–14.CrossRefGoogle ScholarPubMed
Green, C.E., Bredl, J., Holt, W.V., Watson, P.F., Fazeli, A. (2001). Carbohydrate mediation of boar sperm binding to oviductal epithelial cells in vitro. Reproduction 122, 305–15.CrossRefGoogle ScholarPubMed
Gualtieri, R. & Talevi, R. (2003). Selection of highly fertilisation-competent bovine spermatozoa through adhesion to the Fallopian tube epithelium in vitro. Reproduction 125, 251–8.CrossRefGoogle Scholar
Gualtieri, R., Boni, R., Tosti, E., Zagami, M. & Talevi, R. (2005). Intracellular calcium and protein tyrosine phosphorylation during the release of bovine sperm adhering to the Fallopian tube epithelium in vitro. Reproduction 129, 5160.CrossRefGoogle Scholar
Gualtieri, R., Mollo, V., Duma, G. & Talevi, R. (2009). Redex control of surface protein sulphydrils in bovine spermatozoa reversibly modulates sperm adhesion to the oviductal epithelium and capacitation. Reproduction 138, 3343.CrossRefGoogle Scholar
Hadek, R. (1958). Intraperitoneal insemination of rabbit doe. Proc. Soc. Exp. Biol. Med. 99, 3940.CrossRefGoogle ScholarPubMed
Hunter, R.H.F. (1967). The effects of delayed insemination on fertilisation and early cleavage in the pig. J. Reprod. Fert. 13, 133–47.CrossRefGoogle ScholarPubMed
Hunter, R.H.F. (1972). Local action of progesterone leading to polyspermic fertilisation in pigs. J. Reprod. Fert. 31, 433–44.CrossRefGoogle ScholarPubMed
Hunter, R.H.F. (1978). Intraperitoneal insemination, sperm transport and capacitation in the pig. Anim. Reprod. Sci. 1, 167–79.CrossRefGoogle Scholar
Hunter, R.H.F. (1984). Pre-ovulatory arrest and peri-ovulatory redistribution of competent spermatozoa in the isthmus of the pig oviduct. J. Reprod. Fert. 72, 203–11.CrossRefGoogle ScholarPubMed
Hunter, R.H.F. (1993). Sperm:egg ratios and putative molecular signals to modulate gamete interactions in polytocous mammals. Mol. Reprod. Develop. 35, 324–7.CrossRefGoogle ScholarPubMed
Hunter, R.H.F. (1995). Ovarian endocrine control of sperm progression in the Fallopian tubes. Oxford Rev. Reprod. Biol. 17, 85125.Google Scholar
Hunter, R.H.F. (1996). Ovarian control of very low sperm:egg ratios of the commencement of mammalian fertilisation to avoid polyspermy. Mol. Reprod. Develop. 44, 417–22.3.0.CO;2-X>CrossRefGoogle ScholarPubMed
Hunter, R.H.F. (1997). Sperm dynamics in the female genital tract: interactions with Fallopian tube microenvironments. In Microscopy of Reproduction and Development: A Dynamic Approach (ed. Motta, P.M.) pp. 3545. Rome: Antonio Delfino Editore.Google Scholar
Hunter, R.H.F. (2003). Reflections upon sperm-endosalpingeal and sperm-zona pellucida interactions in vivo and in vitro. Reprod. Domestic Anim. 38, 147–54.CrossRefGoogle ScholarPubMed
Hunter, R.H.F. (2008). Sperm release from oviduct epithelial binding is controlled hormonally by peri-ovulatory Graafian follicles. Mol. Reprod. Develop. 75, 167–74.CrossRefGoogle ScholarPubMed
Hunter, R.H.F. & Dziuk, P.J. (1968). Sperm penetration of pig eggs in relation to the timing of ovulation and insemination. J. Reprod. Fert. 15, 199208.CrossRefGoogle Scholar
Hunter, R.H.F. & Léglise, P.C. (1971a). Polyspermic fertilisation following tubal surgery in pigs, with particular reference to the rôle of the isthmus. J. Reprod. Fert. 24, 233–46.CrossRefGoogle Scholar
Hunter, R.H.F. & Léglise, P.C. (1971b). Tubal surgery in the rabbit: fertilisation and polyspermy after resection of the isthmus. Amer. J. Anat. 132, 4552.CrossRefGoogle ScholarPubMed
Hunter, R.H.F. & Nichol, R. (1983). Transport of spermatozoa in the sheep oviduct: preovulatory sequestering of cells in the caudal isthmus. J. exp. Zool. 228, 121–8.CrossRefGoogle ScholarPubMed
Hunter, R.H.F. & Nichol, R. (1986). Post-ovulatory progression of viable spermatozoa in the sheep oviduct and the influence of multiple mating on their pre-ovulatory distribution. Brit. Vet. J. 142, 52–8.CrossRefGoogle ScholarPubMed
Hunter, R.H.F. & Rodriguez-Martinez, H. (2002). Analysing mammalian fertilisation: reservations and potential pitfalls with an in vitro approach. Zygote 10, 11–5.CrossRefGoogle ScholarPubMed
Hunter, R.H.F., Huang, W.T. & Holtz, W. (1998). Regional influences of the Fallopian tubes on the rate of boar sperm capacitation in surgically inseminated gilts. J. Reprod. Fert. 114, 1723.CrossRefGoogle ScholarPubMed
Mattner, P.E. (1963). Capacitation of ram spermatozoa and penetration of the ovine egg. Nature (London) 199, 772–3.CrossRefGoogle ScholarPubMed
Rowlands, I.W. (1958). Insemination by intraperitoneal injection. Proc. Soc. Stud. Fertil. 10, 150–7.Google Scholar
Seckinger, D.L. (1923). Spontaneous contractions of the Fallopian tube of the domestic pig with reference to the oestrous cycle. Bull. Johns Hopkins Hosp. 34, 236–9.Google Scholar
Thibault, C. (1967). Analyse comparée de la fécondation et de ses anomalies chez la brebis, la vache et la lapine. Ann. Biol. Anim. Bioch. Biophys. 7, 523.CrossRefGoogle Scholar
Wassarman, P.M. (1987). Early events in mammalian fertilisation. Ann. Rev. Cell. Biol. 3, 109–42.CrossRefGoogle Scholar
Wassarman, P.M. (1988). Zona pellucida glycoproteins. Ann. Rev. Biochem. 57, 415–42.CrossRefGoogle ScholarPubMed
Wislocki, G.B. & Guttmacher, A.F. (1924). Spontaneous peristalsis of the excised whole uterus and Fallopian tubes of the sow with reference to the ovulation cycle. Bull. Johns Hopkins Hosp. 35, 246–52.Google Scholar
Yanagimachi, R. (1994). Mammalian fertilisation. In The Physiology of Reproduction, 2nd edn, (eds. Knobil, E. & Neill, J.), pp. 189317. New York: Raven Press.Google Scholar
Yaniz, J.L., Lopez-Bejar, M., Santolaria, P., Rutlant, J. & Lopez-Gatius, F. (2002). Intraperitoneal insemination in mammals: a review. Reprod. Dom. Anim. 37, 7580.CrossRefGoogle ScholarPubMed