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Inhibition of sperm-egg fusion in the hamster and mouse by carbohydrates

Published online by Cambridge University Press:  26 September 2008

Ruben H. Ponce ,
Umbert A. Urch  and
Ryuzo Yanagimachi
Ruben H. Ponce
Affiliation:
University of Hawaii shool of Medicine, Hawaii, and University of california, Davis, california, USA
Umbert A. Urch*
Affiliation:
University of Hawaii shool of Medicine, Hawaii, and University of california, Davis, california, USA
Ryuzo Yanagimachi
Affiliation:
University of Hawaii shool of Medicine, Hawaii, and University of california, Davis, california, USA
*
U.A.Urch, Section of Molecular and Cellular Biology, University of California, Davis, CA 95616, USA. 916-752-3085.
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Summary

After spermatozoa bind to and penetrate the extracellular matrix of the egg, the zona pellucida, they adhere to and fuse with the plasma membrane of the egg. Since sperm–egg fusion may involve membrane glycoproteins and/or carbohydrate binding proteins, we sought to test this hypothesis by challenging sperm–egg fusion in hamster and in mouse with added carbohydrates. In this study, a number of carbohydrate and glycoconjugates were examined for their ability to inhibit sperm–eggfusion. In the hamster, D(+)-glucosamine, D(+)-galactosamine, albumin-bovine-glucosamide and-galactosamide, fucoidan and dextran sulphate inhibited the fusion of spermatozoa with zona-free eggs. The same effects were seen in the mouse, except for the toxic effects of D(+)-galactosamine. These facts suggest a role of carbohydrate binding proteins or glycoproteins in the fertilisation process at the level of binding to and fusing with the oolemma.

Keywords

EggFertilisationMembrane fusionSpermatozoa
Type
Article
Information
Zygote , Volume 2 , Issue 3 , August 1994 , pp. 253 - 262
Copyright
Copyright © Cambridge University Press 1994

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References

Ahuja, K.K. (1982). Fertilization studies in the hamster. Exp. Cell Res. 140, 353–62.CrossRefGoogle ScholarPubMed
Anderson, D.J., Abbott, A.F.Jack, R.M. (1993). The role of complement component C3b and its receptors in spermoocyte interaction. Proc. Nati. Acad. Sci., USA 90, 10051–5.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
Bedford, J.M. & Cooper, G.W. (1978). Membrane fusion events in the fertilization of vertebrate eggs. Cell Surface Rev. 5, 65–125.Google Scholar
Bedford, J.M., Moore, H.D.M. & Franklin, L.E. (1979). Significance of the equatorial segment of the acrosome of the spermatozoon in eutherian animals. Exp. Cell Res. 119, 119–26.CrossRefGoogle Scholar
Bleil, J.D. & Wassarman, F.L. (1988). Galactose terminus of O-linked oligosaccharides of mouse egg zona pellucida glycoprotein ZP3 is essential for the glycoproteins's sperm receptor activity. Proc. Natl. Acad. Sci., USA 85, 6778–82.CrossRefGoogle Scholar
Blobel, C.F., Wolfsberg, T.G., Turck, C.W., Myles, D.G., Primakoff, P. & White, J.M. (1992). A potential fusion peptide and an integrin domain in a protein active in sperm-fusion. Nature 356, 248–52.CrossRefGoogle Scholar
Boldt, J. & Wolf, D.P. (1986). An improved method for isolation of fertile zona-free mouse eggs. Gamete Res. 13, 213–22.CrossRefGoogle Scholar
Boldt, J., Howe, A.M., Parkerson, J.B., Gunter, L.E. & Kuehn, E. (1989). Carbohydrate involvement in sperm–egg fusion in mice. Biol. Reprod. 40, 887–96.CrossRefGoogle ScholarPubMed
Bronson, R.A., Fusi, F.M. & Fleit, H.B. (1992). Monoclonal antibodies identify Fcγ receptors on unfertilized human oocytes but not spermatozoa. J. Reprod. Immunol. 21, 293–307.CrossRefGoogle Scholar
De Angelis, P.L. & Glabe, G.C. (1987). Polysaccharide structural features that are critical for the binding of sulfated fucans to bindin, the adhesive protein from sea urchin. J. Biol. Chem. 262, 13946–52.CrossRefGoogle ScholarPubMed
Draviand, E. & Mortimer, D. (1988). Role for fucose-sulfaterich carbohydrates in the penetration of zona pellucidafree hamster eggs by hamster spermatozoa. Gamete Res. 21, 353–8.CrossRefGoogle Scholar
Dunbar, B.S., Prasd, S.V. & Timmons, T.M. (1991). Comparative structure and function of mammalian zonae pellucidae. In A Comparative Overview of Mammalian Fertilization, ed. Dunbar, B.S. & O'Rand, M.G., pp. 97–114. New York: Plenum Press.CrossRefGoogle Scholar
Fleming, A.D. & Yanagimachi, R. (1980). Superovulation and superpregnancy in the golden hamster. Dev. Growth Differ. 22, 103–12.CrossRefGoogle ScholarPubMed
Foltz, K.R. & Lennarz, W.J. (1993) The molecular basis of sea urchin gamete interactions at the egg plasma membrane. Dev. Biol. 158, 46–61.CrossRefGoogle ScholarPubMed
Fusi, F.M., Vignali, M., Busacca, M. & Bronson, R.A. (1992). Evidence for the presence of integrin cell adhesion receptor on the oolemma of unfertilized human oocytes. Mol. Reprod. Dev. 31, 215–22.CrossRefGoogle ScholarPubMed
Fusi, F.M., Vignali, M., Gailit, J. & Bronson, R.A. 1993. Mammalian oocytes exhibit specific recognition of the RGD (arg-gly-asp) tripeptide and express oolemmal integrins. Mol. Reprod. Devl. 36, 212–19.CrossRefGoogle ScholarPubMed
Glabe, G.C., Grabel, L.B., Vacquier, V.D. & Rosen, S.D. (1982). Carbohydrate specificity of sea urchin bindin: a cell surface lectin mediated sperm egg adhesion. J. Cell Biol. 94, 123–8.CrossRefGoogle ScholarPubMed
Huang, T.T.F. & Yanagimachi, R. (1984). Fucoidan inhibits attachment of guinea pig spermatozoa to the zona pellucida through binding to the inner acrosomal membrane and equatorial segment domains. Exp. Cell Res. 153, 363–73.CrossRefGoogle Scholar
Huang, T.T.F Jr, Ohzu, E. & Yanagimachi, R. 1982. Evidence suggesting that L-fucose is part of a recognition signal for sperm-zona attachment in mammals. Gamete Res. 5, 355–61.CrossRefGoogle Scholar
Knudsen, K.A. (1991). Fusion of myoblasts. In Membrane Fusion, ed. Wilchut, J. & Hoekstra, D., pp. 601–26. New York: Marcel Dekker.Google Scholar
Macek, M.B. & Shur, B.D. (1988). Protein-carbohydrate complementarity in mammalian gamete recognition. Gamete Ret. 29, 93–109.CrossRefGoogle Scholar
Miller, D.J. & Ax, R.L. 1990. Carbohydrates and fertilization in animals. Mol. Reprod. Dev. 26, 184–98.CrossRefGoogle ScholarPubMed
Myles, D.G. (1993). Molecular mechanisms of sperm-egg membrane binding and fusion in mammals. Dev. Biol. 158, 35–45.CrossRefGoogle ScholarPubMed
Oehninger, S., Acosta, A.A. & Hodgen, G.D. (1990a). Antagonistic and agonist properties of saccharide moieties in the hemizona assay. Fertil. Steril. 53, 143–9.CrossRefGoogle ScholarPubMed
Oehninger, S., Clark, G.F., Acosta, A.A. & Hodgen, G.D. (1990b). Nature of the inhibitory effect of complex saccharide moieties on the tight binding of human spermatozoa to the human zona pellucida. Ferfil. Steril. 55, 165–9.CrossRefGoogle Scholar
Oehninger, S., Clark, G.F., Fulgam, D., Blackmore, P.F., Mahony, M.C., Acosta, A.A. & Hodgen, G.D. (1992). Effect of fucoidan on human sperm-zona pellucida interactions. J. Androl. 13, 519–25.CrossRefGoogle ScholarPubMed
Ohnishi, S. (1988). Fusion of viral envelope with cellular membranes. In Current Topics in Membranes and Transport, ed. Bonner, F., vol. 32, pp. 257–96. Orlando: Academic Press.Google Scholar
Okabe, M., Yagasaki, M., Matzno, S., Nagira, M., Kohama, Y. & Mimura, T. (1989). Glucosamine enhanced sperm-egg binding but inhibited sperm-egg fusion in mouse. Experientia 45, 193–4.CrossRefGoogle Scholar
Peterson, R.N., Russell, L.D. & Hunt, W.P. (1984). Evidence for specific binding of uncapacitated boar spermatozoa to porcine zonae pellucidae in vitro. J. Exp. Zool. 231, 137–47.CrossRefGoogle ScholarPubMed
Ponce, R.H., Yanagimachi, R., Urch, U., Yamagata, T. & Ito, M. (1993). Retention of hamster oolemma fusibility with spermatozoa after various enzyme treatments: a search for the molecules involved in sperm-egg fusion. Zygote. 1, 163–71.CrossRefGoogle ScholarPubMed
Saling, P., Irons, G. & Waibel, R. (1985). Mouse sperm antigens that participate in fertilization. I. Inhibition of sperm fusion with the egg plasma membrane using monoclonal antibodies. Biol. Reprod. 33, 515–26.CrossRefGoogle ScholarPubMed
Shalgi, R., Matityahu, A. & Nebel, L. (1986). The role of carbohydrates in sperm-egg interaction in rats. Biol. Reprod. 34, 446–52.CrossRefGoogle ScholarPubMed
Takano, H., Yanagimachi, R. & Urch, U.A. (1993). Evidence that acrosin activity is important for the development of fusibility of mammalian spermatozoa with the oolemma:inhibitor studies using the golden hamster. Zygote 1, 79–91.CrossRefGoogle ScholarPubMed
Tanphaichitr, N., Smith, J. & Mongkolsirikieart, S. & Gradil, C. & Lingwood, C.A. (1993). Role of gamete specific sulfoglycolipid immobilizing protein on mouse sperm-egg binding. Dev. Biol. 156, 164–75.CrossRefGoogle ScholarPubMed
Toyoda, Y., Yokoyama, M. & Hoshi, F. (1971). Studies on the fertilization of mouse eggs in vitro. I. In vitro fertilization of eggs by fresh epididymal sperm. Jpn. J. Anim. Reprod. 16, 147–52.Google Scholar
Ward, C.R. & Storey, B.T. (1984). Determination of time course of capacitation in mouse spermatozoa using a chlortetracycline fluorescence assay. Dev. Biol. 104, 287–96.CrossRefGoogle ScholarPubMed
Wassarman, P.M. (1990). Profile of a mammalian sperm receptor. Development 108, 1–17.CrossRefGoogle ScholarPubMed
Yanagimachi, R. (1978). Calcium requirement for sperm-egg fusion in mammals. Biol. Reprod. 19, 949–58.CrossRefGoogle ScholarPubMed
Yanagimachi, R. (1994). Mammalian fertilization. In The Physiology of Reproduction, e.d.. Knobil, E. & Neill, J.D., 2nd edn, chapter 5. New York: Raven Press (in press).Google Scholar