Hostname: page-component-848d4c4894-4hhp2 Total loading time: 0 Render date: 2024-05-08T08:18:12.248Z Has data issue: false hasContentIssue false
  • English
  • Français

Outstanding questions concerning sperm-epithelial binding in the mammalian oviduct*

Published online by Cambridge University Press:  14 July 2015

Ronald Henry Fraser Hunter  and
Joaquín Gadea
Ronald Henry Fraser Hunter*
Affiliation:
Ladfield, Oxnam, Jedburgh, TD86RJ, Roxburghshire, Scotland, UK. Sidney Sussex College, University of Cambridge, UK.
Joaquín Gadea
Affiliation:
Department of Physiology, Veterinary Faculty, University of Murcia, International Excellence Campus for Higher Education and Research (Campus Mare Nostrum) and Institute for Biomedical Research of Murcia IMIB-Arrixaca, Murcia, Spain.
*
All correspondence to: R.H.F. Hunter. Ladfield, Oxnam, Jedburgh, TD86RJ, Roxburghshire, Scotland, UK
Get access Rights & Permissions [Opens in a new window]

Summary

Preovulatory binding of viable spermatozoa in the oviduct isthmus is widely accepted as a preliminary to fertilization, but details of physiological events associated with epithelial binding and release from binding are themselves little understood. Important questions include the potential number, distribution and stability of such sites in the caudal isthmus, whether multiple molecular forms of binding exist within a single-mated individual, and whether some sites are more favourable than others for the maintenance of preovulatory sperm viability. Also to be resolved is whether spermatozoa interact with the first available binding sites in the isthmus, whether spermatozoa from second or subsequent matings bind closer to the site of fertilization, and whether the first spermatozoa entering the oviduct are those that will be released first with impending ovulation. Ideally, future research needs to focus on a fertilizing spermatozoon monitored in vivo and not on spermatozoa destined to remain on or in the zona pellucida or in the lower reaches of the oviduct.

Keywords

EndosalpinxFertilizationOviductOvulationPolyspermySpermatozoa
Type
Research Article
Information
Zygote , Volume 24 , Issue 3 , June 2016 , pp. 389 - 395
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Presented at the 10th Anniversary Conference of the Lower Saxony Virtual Centre for Reproductive Medicine at the University of Veterinary Medicine Hannover, May 2014, and at the M.C. Chang Memorial Symposium, University of Murcia, November 2014.

References

Bahat, A., Tur-Kaspa, I., Gakamsky, A., Giojalas, L.C., Breitbart, H. & Eisenbach, M. (2003). Thermotaxis of mammalian sperm cells: a potential navigation mechanism in the female genital tract. Nat. Med. 9, 149–50.Google Scholar
Baillie, H.S., Pacey, A.A., Warren, M.A., Scudamore, I.W. & Barratt, C.L.R. (1997). Greater numbers of human spermatozoa associate with endosalpingeal cells derived from the isthmus compared with those from the ampulla. Hum. Reprod. 12, 1985–92.Google Scholar
Beatty, R.A. (1957). Parthenogenesis and Polyploidy in Mammalian Development. Cambridge: Cambridge University Press.Google Scholar
Bomsel-Helmreich, O. (1965). Heteroploidy and embryonic death. In Ciba Foundation Symposium – Preimplantation Stages of Pregnancy (eds Wolstenholme, G.E.W. & O'Connor, M.), pp. 246–269. John Wiley & Sons, Ltd. Google Scholar
Bosch, P. & Wright, R. (2005). The oviductal sperm reservoir in domestic mammals. Arch. Med. Vet. 37, 95.Google Scholar
Coy, P. & Aviles, M. (2010). What controls polyspermy in mammals, the oviduct or the oocyte? Biol. Rev. Camb. Philos. Soc. 85, 593–605.Google Scholar
Coy, P., Garcia-Vazquez, F.A., Visconti, P.E. & Aviles, M. (2012). Roles of the oviduct in mammalian fertilization. Reproduction 144, 649–60.CrossRefGoogle ScholarPubMed
Chen, S., Einspanier, R. & Schoen, J. (2013). In vitro mimicking of estrous cycle stages in porcine oviduct epithelium cells: estradiol and progesterone regulate differentiation, gene expression, and cellular function. Biol. Reprod. 89, 54.CrossRefGoogle ScholarPubMed
DeMott, R.P., Lefebvre, R. & Suarez, S.S. (1995). Carbohydrates mediate the adherence of hamster sperm to oviductal epithelium. Biol. Reprod. 52, 1395–403.Google Scholar
Dobrinski, I., Ignotz, G.G., Thomas, P.G. & Ball, B.A. (1996). Role of carbohydrates in the attachment of equine spermatozoa to uterine tubal (oviductal) epithelial cells in vitro . Am. J. Vet. Res. 57, 1635–9.CrossRefGoogle ScholarPubMed
Druart, X., Cognie, J., Baril, G., Clement, F., Dacheux, J.L. & Gatti, J.L. (2009). In vivo imaging of in situ motility of fresh and liquid stored ram spermatozoa in the ewe genital tract. Reproduction 138, 45–53.CrossRefGoogle ScholarPubMed
Einer-Jensen, N. & Hunter, R.H.F. (2005). Counter-current transfer in reproductive biology. Reproduction 129, 9–18.Google Scholar
Fléchon, J.E. & Hunter, R.H.F. (1981). Distribution of spermatozoa in the utero-tubal junction and isthmus of pigs, and their relationship with the luminal epithelium after mating: a scanning electron microscope study. Tissue Cell 13, 127–39.Google Scholar
Gawronska, B., Paukku, T., Huhtaniemi, I., Wasowicz, G. & Ziecik, A.J. (1999). Oestrogen-dependent expression of LH/hCG receptors in pig Fallopian tube and their role in relaxation of the oviduct. J. Reprod. Fertil. 115, 293–301.CrossRefGoogle ScholarPubMed
Gawronska, B., Stepien, A. & Ziecik, A.J. (2000). Effect of estradiol and progesterone on oviductal LH-receptors and LH-dependent relaxation of the porcine oviduct. Theriogenology 53, 659–72.Google Scholar
Hafez, E.S.E. & Blandau, R. (1969). The Mammalian Oviduct: Comparative Biology and Methodology. Chicago: University of Chicago Press.Google Scholar
Hafez, E.S.E. & Thibault, C. (1973). Sperm transport, survival and fertilising ability in vertebrates., INSERM, Paris.Google Scholar
Hancock, J.L. (1959). Polyspermy of pig ova. Anim. Prod. 1, 103–6.Google Scholar
Henning, H., Petrunkina, A.M., Harrison, R.A. & Waberski, D. (2012). Bivalent response to long-term storage in liquid-preserved boar semen: a flow cytometric analysis. Cytometry A 81, 576–87.Google Scholar
Hung, P.H. & Suarez, S.S. (2012). Alterations to the bull sperm surface proteins that bind sperm to oviductal epithelium. Biol. Reprod. 87, 88.Google Scholar
Hunter, R.H.F. (1967). The effects of delayed insemination on fertilization and early cleavage in the pig. J. Reprod. Fertil. 13, 133–47.Google Scholar
Hunter, R.H.F. (1972). Fertilization in the pig: sequence of nuclear and cytoplasmic events. J. Reprod. Fertil. 29, 395–406.Google Scholar
Hunter, R.H.F. (1973). Polyspermic fertilization in pigs after tubal deposition of excessive numbers of spermatozoa. J. Exp. Zool. 183, 57–63.Google Scholar
Hunter, R.H.F. (1974). Chronological and cytological details of fertilization and early embryonic development in the domestic pig. Sus scrofa. Anat. Rec. 178, 169–85.CrossRefGoogle ScholarPubMed
Hunter, R.H.F. (1976). Sperm–egg interactions in the pig: monospermy, extensive polyspermy, and the formation of chromatin aggregates. J. Anat. 122, 43–59.Google Scholar
Hunter, R.H.F. (1980). Physiology and technology of reproduction in female domestic animals. Academic Press.Google Scholar
Hunter, R.H.F. (1993). Sperm:egg ratios and putative molecular signals to modulate gamete interactions in polytocous mammals. Mol. Reprod. Dev. 35, 324–7.Google Scholar
Hunter, R.H.F. (1995). Local action of progesterone leading to polyspermic fertilization in pigs. Oxford Rev. Reprod. Biol. 17, 85–124.Google Scholar
Hunter, R.H.F. (1996). Ovarian control of very low sperm/egg ratios at the commencement of mammalian fertilisation to avoid polyspermy. Mol. Reprod. Dev. 44, 417–22.Google Scholar
Hunter, R.H.F. (2001). Histophysiology of the Fallopian tubes in relation to sperm binding, release, and completion of capacitation. Ital. J. Anat. Embryol. 106, 279–89.Google Scholar
Hunter, R.H.F. (2002). Vital aspects of Fallopian tube physiology in pigs. Reprod. Domes. Anim. 37, 186–90.Google Scholar
Hunter, R.H.F. (2003a). Physiology of the Graafian follicle and Ovulation. Cambridge: Cambridge University Press.Google Scholar
Hunter, R.H.F. (2003b). Reflections upon sperm-endosalpingeal and sperm-zona pellucida interactions in vivo and in vitro . Reprod. Domes. Anim. 38, 147–54.Google Scholar
Hunter, R.H.F. (2005). Fallopian tube physiology: preliminaries to monospermic fertilization and cellular events post-fertilization. In New Mechanisms for Tissue-Selective Estrogen-Free Contraception (Eds, Croxatto, H.B., Schürmann, R., Fuhrmann, U. & Schellschmidt, I.), pp. 245–261. Berlin: Springer.Google Scholar
Hunter, R.H.F. (2008). Sperm release from oviduct epithelial binding is controlled hormonally by peri-ovulatory Graafian follicles. Mol. Reprod. Dev. 75, 167–74.Google Scholar
Hunter, R.H.F. (2011). Sperm head binding to epithelium of the oviduct isthmus is not an essential preliminary to mammalian fertilization – review. Zygote 19, 265–9.Google Scholar
Hunter, R.H.F. (2012). Components of oviduct physiology in eutherian mammals. Biol. Rev. Camb. Philos. Soc. 87, 244–55.Google Scholar
Hunter, R.H.F. & Dziuk, P.J. (1968). Sperm penetration of pig eggs in relation to the timing of ovulation and insemination. J. Reprod. Fertil. 15, 199–208.Google Scholar
Hunter, R.H.F. & Gadea, J. (2014). Cross-talk between free and bound spermatozoa to modulate initial sperm:egg ratios at the site of fertilization in the mammalian oviduct. Theriogenology 82, 367–72.Google Scholar
Hunter, R.H.F. & Nichol, R. (1986). A preovulatory temperature gradient between the isthmus and ampulla of pig oviducts during the phase of sperm storage. J. Reprod. Fertil. 77, 599–606.Google Scholar
Hunter, R.H.F., Cook, B. & Poyser, N.L. (1983). Regulation of oviduct function in pigs by local transfer of ovarian steroids and prostaglandins: a mechanism to influence sperm transport. Eur. J. Obstet. Gynecol. Reprod. Biol. 14, 225–32.Google Scholar
Hunter, R.H.F., Fléchon, B. & Fléchon, J.E. (1987). Pre- and peri-ovulatory distribution of viable spermatozoa in the pig oviduct: a scanning electron microscope study. Tissue Cell 19, 423–36.Google Scholar
Hunter, R.H.F., Fléchon, B. & Fléchon, J.E. (1991). Distribution, morphology and epithelial interactions of bovine spermatozoa in the oviduct before and after ovulation: a scanning electron microscope study. Tissue Cell 23, 641–56.Google Scholar
Jansen, R.P. (1978). Fallopian tube isthmic mucus and ovum transport. Science 201, 349–51.Google Scholar
Jewell, P.A., Hall, S.J. & Rosenberg, M.M. (1986). Multiple mating and siring success during natural oestrus in the ewe. J. Reprod. Fertil. 77, 81–9.Google Scholar
Lefebvre, R., Lo, M.C. & Suarez, S.S. (1997). Bovine sperm binding to oviductal epithelium involves fucose recognition. Biol. Reprod. 56, 1198–204.Google Scholar
Mburu, J.N., Einarsson, S., Lundeheim, N. & Rodriguez-Martinez, H. (1996). Distribution, number and membrane integrity of spermatozoa in the pig oviduct in relation to spontaneous ovulation. Anim. Reprod. Sci. 45, 109–21.Google Scholar
Mburu, J.N., Rodriguez-Martinez, H. & Einarsson, S. (1997). Changes in sperm ultrastructure and localisation in the porcine oviduct around ovulation. Anim. Reprod. Sci. 47, 137–48.Google Scholar
Petrunkina, A.M. & Harrison, R.A. (2010). Systematic misestimation of cell subpopulations by flow cytometry: a mathematical analysis. Theriogenology 73, 839–47.Google Scholar
Piko, L. (1961). La polyspermie chez les animaux. Ann. Biol. Anim. Biochim. Biophys. 1, 323–83.Google Scholar
Polge, C., Salamon, S. & Wilmut, I. (1970). Fertilizing capacity of frozen boar semen following surgical insemination. Vet. Rec. 87, 424–9.CrossRefGoogle ScholarPubMed
Rath, D., Schuberth, H.J., Coy, P. & Taylor, U. (2008). Sperm interactions from insemination to fertilization. Reprod. Domes. Anim. 43 (Suppl. 5), 2–11.Google Scholar
Rickard, J.P., Pini, T., Soleilhavoup, C., Cognie, J., Bathgate, R., Lynch, G.W., Evans, G., Maxwell, W.M., Druart, X. & de Graaf, S.P. (2014). Seminal plasma aids the survival and cervical transit of epididymal ram spermatozoa. Reproduction 148, 469–78.Google Scholar
Rodriguez-Martinez, H. (2007). Role of the oviduct in sperm capacitation. Theriogenology 68 (Suppl. 1), S138–46.Google Scholar
Rodriguez-Martinez, H., Tienthai, P., Suzuki, K., Funahashi, H., Ekwall, H. & Johannisson, A. (2001). Involvement of oviduct in sperm capacitation and oocyte development in pigs. Reproduction 58 (Suppl.), 129–45.Google Scholar
Schmid, S., Henning, H., Oldenhof, H., Wolkers, W.F., Petrunkina, A.M. & Waberski, D. (2013). The specific response to capacitating stimuli is a sensitive indicator of chilling injury in hypothermically stored boar spermatozoa. Andrology 1, 376–86.Google Scholar
Smith, T.T. & Yanagimachi, R. (1991). Attachment and release of spermatozoa from the caudal isthmus of the hamster oviduct. J. Reprod. Fertil. 91, 567–73.Google Scholar
Suarez, S.S. (2006). Gamete and zygote transport. In Knobil & Neill's Physiology of Reproduction, 3rd edn (eds Neill, J.D., Plant, T.M., Pfaff, D.W., Challis, J.R.G., de Kretser, D.M., Richards, J.S. & Wassarman, P.M.), pp. 113–145. St Louis: Academic Press.Google Scholar
Suarez, S.S. (2008). Regulation of sperm storage and movement in the mammalian oviduct. Int. J. Dev. Biol. 52, 455–62.Google Scholar
Suarez, S.S., Katz, D.F., Owen, D.H., Andrew, J.B. & Powell, R.L. (1991a). Evidence for the function of hyperactivated motility in sperm. Biol. Reprod. 44, 375–81.Google Scholar
Suarez, S.S. & Pacey, A.A. (2006). Sperm transport in the female reproductive tract. Hum. Reprod. Update 12, 23–37.Google Scholar
Suarez, S.S., Redfern, K., Raynor, P., Martin, F. & Phillips, D.M. (1991b). Attachment of boar sperm to mucosal explants of oviduct in vitro: possible role in formation of a sperm reservoir. Biol. Reprod. 44, 998–1004.Google Scholar
Talevi, R. & Gualtieri, R. (2010). Molecules involved in sperm-oviduct adhesion and release. Theriogenology 73, 796–801.Google Scholar
Thibault, C. (1959). Analyse de la fécondation de l'oeuf de la truie après accouplement ou insémination artificielle. Annales de Zootechnie, Serie D Supplement, pp. 165–177.Google Scholar
Thibault, C. (1973). Sperm transport and storage in vertebrates. J. Reprod. Fertil. Suppl. 18, 39–53.Google Scholar
Töpfer-Petersen, E., Wagner, A., Friedrich, J., Petrunkina, A., Ekhlasi-Hundrieser, M., Waberski, D. & Drommer, W. (2002). Function of the mammalian oviductal sperm reservoir. J. Exp. Zool. 292, 210–5.Google Scholar
Waberski, D., Magnus, F., Ardon, F., Petrunkina, A.M., Weitze, K.F. & Topfer-Petersen, E. (2006). Binding of boar spermatozoa to oviductal epithelium in vitro in relation to sperm morphology and storage time. Reproduction 131, 311–8.Google Scholar
Yanagimachi, R. (1998). Mammalian fertilization. In The Physiology of Reproduction, vol. 1 (eds Knobil, E. & Neill, J.D.), pp. 135–85. New York, Raven Press.Google Scholar
Yaniz, J.L., Lopez-Gatius, F., Santolaria, P. & Mullins, K.J. (2000). Study of the functional anatomy of bovine oviductal mucosa. Anat. Rec. 260, 268–78.Google Scholar