Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-22T17:42:29.276Z Has data issue: false hasContentIssue false

Recombinant hamster sperm receptors that exhibit species-specific binding to sperm

Published online by Cambridge University Press:  26 September 2008

Eveline S. Litscher
Affiliation:
Department of Cell Biology and Anatomy, Mount Sinai School of Medicine, New York, NY 10029, USA.
Paul M. Wassarman*
Affiliation:
Department of Cell Biology and Anatomy, Mount Sinai School of Medicine, New York, NY 10029, USA.
*
P.M. Wassarman, Mount Sinai School of Medicine, One Gustave L. Levy Place, New York, NY 10029-6574, USA. Telephone: +1(212) 241-8616. Fax: +1(212) 427-7532. e-mail: [email protected].

Summary

Previous studies have shown that mouse sperm bind to hamster eggs and hamster sperm bind to mouse eggs in vitro. Furthermore, sperm receptor glycoprotein isolated from the zona pellucida of unfertilised hamster (hZP3) and mouse (mZP3) eggs binds to sperm from the heterologous species. Here, we expressed the hZP3 gene, under control of a constitutive promoter (pgk-1), in mouse embryonal carcinoma (EC) cells and Chinese hamster ovary (CHO) cells stably transfected with the hZP3 gene. In both cases, recombinant hZP3 (EC-hZP3 and CHO-hZP3) secreted into the culture medium was partially purified by high-performance liquid chromatography on a size-exclusion column and assayed for bioactivity using mouse and hamster gametes. Unlike hamster egg hZP3, which binds to both mouse and hamster sperm, EC-hZP3 and CHO-hZP3 exhibits species-specific binding to hamster sperm and induce hamster sperm, but not mouse sperm, to undergo the acrosome reaction in vitro. These results provide further evidence that species-specific binding of sperm to eggs in mammals is carbohydrate-mediated. Furthermore, the results suggest that recombinant forms of mammalian sperm receptors may be useful in assessing the molecular basis of species-specific fertilisation in mammals.

Type
Article
Copyright
Copyright © Cambridge University Press 1996

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.)

References

Bedford, J.M.. (1982). Fertilization, In Reproduction in Mammals, ed. Austin, C.R. & Short, R.V., vol. 1, pp. 128–63. Cambridge: Cambridge University Press.Google Scholar
Beebe, S.L., Leyton, L., Burks, D., Ishikawa, M., Fuerst, T., Dean, J. & Saling, P.. (1992). Recombinant mouse ZP3 inhibits sperm binding and induces the acrosome reaction. Dev. Biol. 151, 4854.Google Scholar
Bleil, J.D. & Wassarman, P.M.. (1980). Mammalian sperm-egg interaction: identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm. Cell 20, 873–82.Google Scholar
Bookbinder, L.H., Cheng, A. & Bleil, J.D.. (1995). Tissue- and species-specific expression of sp56, a mouse sperm fertilization protein. Science 269, 86–9.Google Scholar
Cherr, G.N., Lambert, H., Meizel, S. & Katz, D.F.. (1986). In vitro studies of the golden hamster sperm acrosome reaction: completion on the zona pellucida and induction by homologous soluble zonae pellucidae. Dev. Biol. 114, 119–31.CrossRefGoogle Scholar
Elhammer, A.P., Poorman, K.A., Brown, F., Maggiora, L.L., Hoogerheide, J.G. & Kézdy, F.J.. (1993). The specificity of UDP-GalNAc:polypeptide N-acetylgalactosaminyltrans-ferase as inferred from a database of in vivo substrates and from the in vitro glycosylation of proteins and peptides. J. Biol. Chem. 268, 10029–38.Google Scholar
Florman, H.M. & Wassarman, P.M.. (1985). O-linked oligo-saccharides of mouse egg ZP3 account for its sperm receptor activity. Cell 41, 313–24.Google Scholar
Florman, H.M., Bechtol, K.B. & Wassarman, P.M.. (1984). Enzymatic dissection of the functions of the mouse egg's receptor for sperm. Dev. Biol 106, 243–55.Google Scholar
Goelz, S., Kumar, R., Potvin, B., Sundaram, S., Brickelmaier, M. & Stanley, P.. (1994). Differential expression of an E-selectin ligand (Sle×) by two Chinese hamster ovary cell lines transfected with the same α(1,3)-fucosyltransferase gene (ELFT). J. Biol. Chem. 269, 1033–40.Google Scholar
Gooley, A.A. & Williams, K.L.. (1994). Towards characterizing O-glycans: the relative merits of in vivo and in vitro approaches in seeking peptide motifs specifying O-glyco-sylation sites. Glycobiology 4, 413–17.Google Scholar
Gwatkin, R.B.L.. (1977). Fertilisation Mechanisms in Man and Mammals. New York: Plenum Press.Google Scholar
Kinloch, R.A., Roller, R.J., Fimiani, C., Wassarman, D.A. & Wassarman, P.M.. (1988). Primary structure of the mouse sperm receptor's polypeptide chain determined by genomic cloning. Proc. Natl. Acad. Sci. USA 85, 6409–13.Google Scholar
Kinloch, R.A., Ruiz-Seiler, B & Wassarman, P.M.. (1990). Genomic organization and polypeptide primary struture of zona pellucida glycoprotein hZP3, the hamster sperm receptor. Dev. Biol 142, 414–21.Google Scholar
Kinloch, R.A., Mortillo, S., Stewart, C.L. & Wassarman, P.M.. (1991). Embryonal carcinoma cells transfected with ZP3 genes differentially glycosylate similar polypeptides and secrete active mouse sperm receptor. J. Cell Biol 115, 655–64.Google Scholar
Kinloch, R.A., Mortillo, S. & Wassarman, P.M.. (1992). Transgenic mouse eggs with functional hamster sperm receptors in their zona pellucida. Development 115, 937–46.Google Scholar
Kinloch, R.A., Lire, S.A., Mortillo, S., Schickler, M., Roller, R.J. & Wassarman, P.M.. (1993). Regulation of expression of mZP3, the sperm receptor gene, during mouse development. In Molecular Basis of Morphogenesis, ed. Bernfield, M., pp. 1933. New York: Wiley-Liss.Google Scholar
Kinloch, R.A., Sakai, Y. & Wassarman, P.M.. (1995). Mapping the mouse ZP3 combining site for sperm by exon swapping and site-directed mutagenesis. Proc. Natl. Acad. Sci. USA., 92, 263–7.Google Scholar
Litscher, E.S. & Wassarman, P.M.. (1993). Carbohydrate-mediated adhesion of eggs and sperm during mammalian fertilization. Trends Glycosci. Glycotech 5, 369–88.Google Scholar
Litscher, E.S. & Wassarman, P.M.. (1996). Characterization of a mouse ZP3-derived glycopeptide, gp55, that exhibits sperm receptor and acrosome reaction-inducing activity in vitro. Biochemistry 35, 3980–5.Google Scholar
Litscher, E.S., Juntunen, K., Seppo, A., Penttilä, R., Renkonen, O. & Wassarman, P.M.. (1995). Oligosaccharide constructs with defined structures that inhibit binding of mouse sperm to unfertilized eggs in vitro. Biochemistry 34, 4662–9.Google Scholar
Miller, D.J., Macek, M.B. & Shur, B.D.. (1992). Complementarity between sperm surface β-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding. Nature 357, 589–93.Google Scholar
Moller, C.C., Bleil, J.D., Kinloch, R.A. & Wassarman, P.M.. (1990). Structural and functional relationships between mouse and hamster zona pellucida glycoproteins. Dev. Biol 137, 276–86.Google Scholar
Mortillo, S., Litscher, E.S., Joziasse, D.H., Shaper, J.H. & Wassarman, P.M.. (1994). Synthesis of an active mZP3 by CV-1 cells stably transfected with expression vectors encoding mZP3 and α1,3-galactosyltransferase. Mol. Biol. Cell 5, 223a (abstr.).Google Scholar
Nehrke, K., Hagen, F.K. & Tabak, L.A.. (1996). Charge distribution of flanking amino acids influences O-glycan acquisition in vivo. J. Biol. Chem. 271, 7061–5.Google Scholar
Rosiere, T.G. & Wassarman, P.M.. (1992). Identification of a region of mouse zona pellucida glycoprotein mZP3 that possesses sperm receptor activity. Dev. Biol 154, 309–17.Google Scholar
Schmell, E.D. & Gulyas, B.J.. (1980). Mammalian sperm–egg recognition and binding in vitro. I. Specificity of sperm interaction with live and fixed eggs in homologous and heterologous insemination of hamster, mouse, and guinea pig oocytes. Biol. Reprod. 23, 1075–85.Google Scholar
Sharon, N. & Lis, H.. (1993). Carbohydrates in cell recognition. Sci. Am. 261 (Jan), 82–9.Google Scholar
Smith, D.F., Larsen, R.D., Mattox, S., Lowe, J.B. & Cummings, R.D.. (1990). Transfer and expression of a murine UDP-Gal:β-D-Gal-αl,3-galactosyltransferase gene in transfected Chinese hamster ovary cells. J. Biol. Chem. 265, 6225–34.Google Scholar
Snell, W.J. & White, J.M.. (1996). The molecules of mammalian fertilization. Cell 85, 629–37.Google Scholar
Stanley, P.. (1992). Glycosylation engineering. Glycobiology 2, 99107.CrossRefGoogle Scholar
van Duin, M., Polman, J.E.M., de Breet, I.T.M., van Ginneken, K., Bunschoten, H., Grootenhuis, A., Brindle, J. & Aitken, R.J.. (1994). Recombinant human zona pellucida protein ZP3 produced by Chinese hamster ovary cells induces the human sperm acrosome reaction and promotes sperm-egg fusion. Biol. Reprod. 51. 607–17.Google Scholar
Wassarman, P.M.. (1988). Zona pellucida glycoproteins. Annu. Rev. Biochem 57, 415–42.Google Scholar
Wassarman, P.M.. (1990). Profile of a mammalian sperm receptor. Development 108, 117.Google Scholar
Wassarman, P.M.. (1995). Towards molecular mechanisms for gamete adhesion and fusion during mammalian fertilization. Curr. Opin. Cell Biol. 7, 658–64.Google Scholar
Wassarman, P.M. & Litscher, E.S.. (1995). Sperm-egg recognition mechanisms in mammals. Curr. Top. Dev. Biol 30, 119.Google Scholar
Weetall, M.L., Litscher, E.S. & Wassarman, P.M.. (1993). Structure–function relationships between mouse and hamster sperm receptors. Mol. Biol. Cell 4, 248a (abstr.).Google Scholar
Wilson, I.B.H., Gavel, Y. & von Heijne, G.. (1991). Amino acid distributions around O-linked glycosylation sites. Biochem. J. 275, 529–34.Google Scholar
Yanagimachi, R.. (1994). Mammalian fertilization. In The Physiology of Reproduction, ed. Knobil, E. & Neil, J.D. pp. 189317. New York: Raven Press.Google Scholar