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Summary

The zona pellucida is an extracellular coat that surrounds all mammalian eggs. Sperm must penetrate the zona pellucida in order to reach and fuse with the plasma membrane of unfertilized eggs. Penetration is accomplished by a sequence of events involving both egg and sperm. First, sperm must bind to the outer margin of the zona pellucida. Such binding is mediated in a relatively species-specific manner by “sperm receptors” in the zona pellucida. Second, sperm must undergo the “acrosome reaction”, a membrane fusion event, in order to traverse the zona pellucida.

Here we review results from our own laboratory which demonstrate that, during the course of sperm-egg interaction in mice, zona pellucida glycoprotein ZP3 serves as both receptor for sperm and inducer of the acrosome reaction. Furthermore, we review evidence from our laboratory indicating that the sperm receptor activity of ZP3 is dependent only on its 0-linked carbohydrate components, whereas acrosome reaction-inducing activity is dependent on the polypeptide portion of ZP3 as well.

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REFERENCES

  1. Adair, W.S., Monk, B.C., Cohen, R., Hwang, C., and Goodenough, U. W. 1982. Sexual agglutinins from the Chlamydomonas flagellar membrane. Partial purification and characterization. J. Biol. Chem. 257: 4593–4602.

    Google Scholar 

  2. Austin, C.R. 1965.,,Fertilization,,, Prentice-Hall, New Jersey.

    Google Scholar 

  3. Barros, C., and Yanagimachi, R. 1971. Induction of the zona reaction in golden hamster eggs by cortical granule material. Nature 233: 268–269.

    Article  ADS  Google Scholar 

  4. Bleil, J.D., and Wassarman, P.M. 1978. Identification and characterization of the proteins of the zona pellucida. J. Cell Biol. 79: 173a.

    Google Scholar 

  5. Bleil, J.D., and Wassarman, P.M. 1980. Structure and function of the zona pellucida: identification and characterization of the proteins of the mouse oocyte’s zona pellucida. Devel. Biol. 76: 185–203.

    Article  Google Scholar 

  6. Bleil, J.D., and Wassarman, P.M. 1980. Synthesis of zona pellucida proteins by denuded and follicle-enclosed mouse oocytes during culture in vitro. Proc. Nat. Acad. Sci. USA 77: 1029–1033.

    Article  ADS  Google Scholar 

  7. Bleil, J.D., and Wassarman, P.M. 1980. Mamalian sperm-egg interaction: identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm. Cell 20: 873–882.

    Article  Google Scholar 

  8. Bleil, J.D., Beall, C.F., and Wassarman, P.M. 1981. Mammalian sperm-egg interaction: fertilization of mouse eggs triggers modification of the major zona pellucida glycoprotein. Devel. Biol. 86: 189–197.

    Article  Google Scholar 

  9. Bleil, J.D., and Wassarman, P.M. 1983. Sperm-egg interactions in the mouse: sequence of events and induction of the acrosome reaction by a zona pellucida glycoprotein. Devel. Biol. 95: 317–324.

    Article  Google Scholar 

  10. Christiensen, J.R. 1975. The kinetics of reversible and irreversible attachment of bacteriophage Tl. Virol. 26: 727–737.

    Google Scholar 

  11. Culp, L.A. 1978. Biochemical determinants of cell adhesion. Curr. Topics Memb. Trans. 11: 327–396.

    Article  Google Scholar 

  12. Edge, A.S.B., Faltynek, C.R., Hof, L., Reichert, L.E., and Weber, P. 1981. Deglycosylation of glycoproteins by trifluoromethane-sulfonic acid. Anal. Biochem. 118: 131–137.

    Article  Google Scholar 

  13. Elder, J.H., and Alexander, S. 1982. Endo-beta-N-acetyl-glucosaminidase F: endoglycosidase from Flavobacterium meningosepticum that cleaves both high-mannose and complex glycoproteins. Proc. Nat. Acad. Sci. USA 79: 4540–4544.

    Article  ADS  Google Scholar 

  14. Epel, D., and Vacquier, V.C. 1978. Membrane fusion events during invertebrate fertilization. In “Cell Surface Reviews” ( G. Poste and G. L. Nicolson, eds.), 5: 1–63, Elsevier: North Holland, Amsterdam.

    Google Scholar 

  15. Florman, H.M., and Storey, B.T. 1982. Mouse gamete interactions: the zona pellucida is the site of the acrosome reaction leading to fertilization in vitro. Devel. Biol. 91: 121–130.

    Article  Google Scholar 

  16. Florman, H.M., and Wassarman, P.M. 1985. 0-linked oligosaccharides of mouse egg ZP3 account for its sperm receptor activity. Cell 41: 313–324.

    Google Scholar 

  17. Florman, H.M., Bechtol, K.B., and Wassarman, P.M. 1984. Enzymatic dissection of the functions of the mouse egg’s receptor for sperm. Devel. Biol. 106: 243–255.

    Article  Google Scholar 

  18. Frazier, W.A., and Glaser, L. 1979. Surfact components and cell recognition. Ann. Rev. Biochem. 48: 491–523.

    Article  Google Scholar 

  19. Glabe, C.G., and Vacquier, V.D. 1978. Egg surface glycoprotein receptor for sea urchin sperm bindin. Proc. Nat. Acad. Sci. USA 75: 881–885.

    Article  ADS  Google Scholar 

  20. Glabe, C.G. 1979. A supramolecular theory for specificity in intercellular adhesion. J. Theoret. Biol. 78: 417–432.

    Article  Google Scholar 

  21. Glabe, C.G., and Lennarz, W.J. 1979. Species-specific sperm adhesion in sea urchins: a quantitative investigation of bindin mediated egg agglutination. J. Cell Biol. 83:595– 604.

    Google Scholar 

  22. Glabe, C.G., and Lennarz, W.J. 1981. Isolation of a high molecular weight glycoconjugate derived from the surface of Strongylocentrotus purpuratus eggs that is implicated in cell adhesion. J. Supramol. Struc. Cell Biochem. 15: 387–394.

    Article  Google Scholar 

  23. Glabe, C.G., Grabel, L.B., Vacquier, V.D., and Rosen, S.D. 1982. Carbohydrate specificity of sea urchin sperm bindin: a cell surface lectin mediating sperm-egg adhesion. J. Cell Biol. 94: 123–128.

    Article  Google Scholar 

  24. Greve, J.M., Salzmann, G.S., Roller, R.J., and Wassarman, P.M. 1982. Biosynthesis of the major zona pellucida glycoprotein secreted by oocytes during mammalian oogenesis. Cell 31: 749–759.

    Article  Google Scholar 

  25. Grinnel, F. 1978. Cellular adhesiveness and extracellular substrata. Inter. Rev. Cytol. 53: 65–144.

    Article  Google Scholar 

  26. Gulyas, B.J. 1980. Cortical granules of mammalian eggs. Inter. Rev. Cytol. 63: 357–392.

    Article  Google Scholar 

  27. Gwatkin, R.B.L., Williams, D.T., Hartman, J.F., and Kniazuk, M. 1973. The zona reaction of hamster and mouse eggs: production in vitro by a trypsin-like protease from cortical granules. J. Reprod. Fert. 32: 259–265.

    Article  Google Scholar 

  28. Gwatkin, R.B.L. 1976. Fertilization. In “Cell Surface Reviews” ( G. Poste and G. L. Nicholson, eds.), 1: 1 - 52, Elsevier: North Holland, Amsterdam.

    Google Scholar 

  29. Gwatkin, R.B.L., and Williams, D.T. 1976. Receptor activity of the solubilized hamster and mouse zona pellucida before ani after the zona reaction. J. Reprod. Fert. 49: 55–59.

    Article  Google Scholar 

  30. Gwatkin, R.B.L. 1977. “Fertilization Mechanisms in Man and Mammals”, Plenum Press, New York.

    Google Scholar 

  31. Hartmann, J.F., Gwatkin, R.B.L., and Hutchinson, C.F. 1972. Early contact interactions between mammalian gametes in vitro: evidence that the vitellus influences adherence between sperm and zona pellucida. Proc. Nat. Acad. Sci. USA 69: 2767–2769.

    Article  ADS  Google Scholar 

  32. Hoffmann, K., Wingender, W., and Finn, F.M. 1970. Correlations of adrenocorticotropic activity with ACTH analogs with degree of binding to an adrenal gland particulate preparation. Proc. Nat. Acad. Sci. USA 67: 820–833.

    ADS  Google Scholar 

  33. Huang, T.T.F., Ohzu, E., and Yanagimachi, R. 1982. Evidence suggesting that L-fucose is part of the recognition signal for sperm-zona pellucida attachment in mammals. Gamete Res. 5: 355–361.

    Article  Google Scholar 

  34. Hubbard, S.C., and Ivatt, R.J. 1981. Synthesis and processing of asparagine-linked oligosaccharides. Ann. Rev. Biochem. 50: 555–583.

    Article  Google Scholar 

  35. Huesgen, A., and Gerisch, G. 1975. Solubilized contact sites A from cell membranes of Dictyostelium discoideum. FEBS Lett. 56: 46–49.

    Article  Google Scholar 

  36. Inoue, M., and Wolf, D.P. 1975. Sperm binding characteristics of the murine zona pellucida. Biol. Reprod. 13: 340–346.

    Article  Google Scholar 

  37. Jones, H.P., Lenz, R.W., Palevitz, B.A., and Cormier, M.J. 1980. Calmodulin localization in mammalian spermatozoa. Proc. Natl. Acad. Sci. USA 77: 2772–2776.

    Article  ADS  Google Scholar 

  38. Kalyan, N.K., and Bahl, O.P. 1983. Role of carbohydrate in human chorionic gonadotropin. Effect of deglycosylation on the subunit interaction and on its in vitro and in vivo biological properties. J. Biol. Chem. 258: 67–74.

    Google Scholar 

  39. Kinsey, W.J., and Lennarz, W.J. 1981. Isolation of a glycopep-tide fraction from the surface of the sea urchin egg that inhibits sperm-egg binding and fertilization. J. Cell Biol. 91: 325–331.

    Article  Google Scholar 

  40. Linberg, A.A. 1973. Bacteriophage receptors. Ann. Rev. Microbiol. 27: 205–239.

    Article  Google Scholar 

  41. Lovett, P.S., and Shockman, G.D. 1970. Interaction of bacteriophage N1 with cell walls of Micrococcus lysodeikticus. J. Virol. 6: 135–144.

    Google Scholar 

  42. Lunney, J., and Ashwell, G. 1976. A hepatic receptor of avian origin capable of binding specifically modified glycoproteins. Proc. Nat. Acad. Sci. USA 73: 341–343.

    Article  ADS  Google Scholar 

  43. Mesland, D.A.M., Hoffman, J.L., Caligor, E., and Goodenough, U.W. 1980. Flagellar tip activation stimulated by membrane adhesions in Chlamydomonas gametes. J. Cell Biol. 84: 599–617.

    Article  Google Scholar 

  44. Metz, C.B., and Monroy, A. 1985. “Biology of Fertilization”, Academic Press, New York.

    Google Scholar 

  45. Michael, J.G. 1968. The surface antigens and phage receptors on Escherichia coli B. Proc. Soc. Exp. Biol. Med. 128: 434–438.

    Google Scholar 

  46. Oikawa, T., Nicolson, G.L., and Yanagimachi, R. 1973. Wheat germ agglutinin blocks mammalian fertilization. Nature 241: 256–259.

    Article  ADS  Google Scholar 

  47. Oikawa, T., and Yanagimachi, R. 1975. Block of hamster fertilization by anti-ovary antibody. J. Reprod. Fert. 45: 487–494.

    Article  Google Scholar 

  48. Robbins, P.W., Hubbard, S.C., Turco, S.J., and Wirth, D.F. 1977. Proposal for a common oligosaccharide intermediate in the synthesis of membrane glycoproteins. Cell 12: 893–900.

    Article  Google Scholar 

  49. Rodbell, M., Birnbaumer, L., Pohl, S.L., and Sunby, F. 1971. The reaction of glucagon with its receptor: evidence for discrete regions of activity and binding in the glucagon molecule. Proc. Nat. Acad. Sci. USA 68: 909–913.

    Article  ADS  Google Scholar 

  50. Roller, R.J., and Wassarman, P.M. 1983. Role of asparagine-linked oligosaccharides in secretion of glycoproteins of the mouse egg’s extracellular coat. J. Biol. Chem. 258: 13243–13249.

    Google Scholar 

  51. Rossignol, D.P., Roschelle, A.J., and Lennarz, W.J. 1981. Sperm-egg binding: identification of specific sperm receptor from eggs of Strongylocentrotus purpuratus. J. Supramol. Struct. Cell. Biochem. 15: 347–358.

    Article  Google Scholar 

  52. Saling, P.M., Wosinski, J., and Storey, B.T. 1979. An ultra-structural study of epididymal mouse spermatozoa binding to zonae pellucidae in vitro: sequential relationship to the acrosome reaction. J. Exp. Zool. 109: 229–238.

    Article  Google Scholar 

  53. Saling, P.M., and Storey, B.T. 1979. Mouse gamete interactions during fertilization in vitro. Chlortetracycline as a fluorescent probe for the mouse acrosome reaction. J. Cell Biol. 83: 544–555.

    Article  Google Scholar 

  54. Salzmann, G.S., Greve, J.M., Roller, R.J., and Wassarman, P.M. 1983. Biosynthesis of the sperm receptor during oogenesis in the mouse. EMBO J. 2: 1451–1456.

    Google Scholar 

  55. Schmell, E., Earles, B.J., Breaux, C., and Lennarz, W.J. 1977. Identification of a sperm receptor on the surface of eggs of the sea urchin, Arbacia punctulata. J. Cell Biol. 72: 35–46.

    Article  Google Scholar 

  56. SeGall, G.K., and Lennarz, W.J. 1979. Chemical characterization of the component of the jelly coat from sea urchin eggs responsible for induction of the acrosome reaction. Devel. Biol. 71: 33–48.

    Article  Google Scholar 

  57. SeGall, G.K., and Lennarz, W.J. 1981. Jelly coat and induction of the acrosome reaction in echinoderm sperm. Devel. Biol. 86: 87–93.

    Article  Google Scholar 

  58. Shapiro, B.D., Schackmann, R.W., and Gabel, C.A. 1981. Molecular approaches to the study of fertilization. Ann. Rev. Biochem. 50: 815–843.

    Article  Google Scholar 

  59. Shur, B.D., and Hall, N.G. 1982. Sperm surface glycosyltransferase activities during in vitro capacitation. J. Cell Biol. 95: 567–573.

    Article  Google Scholar 

  60. Shur, B.D., and Hall, N.G. 1982. A role for mouse sperm surface galactosyltransferase in sperm binding to the egg zona pellucida. J. Cell Biol. 95: 574–579.

    Article  Google Scholar 

  61. Takatsuki, A., Fukui, Y., and Tamura, A. 1975. Inhibition of biosynthesis of polyisoprenol sugars in chick embryo microsomes of tunicamycin. Agric. Biol. Chem. 39: 2089–2091.

    Article  Google Scholar 

  62. Tarentino, A.L., and Maley, F. 1974. Purification and properties of an endo-beta-N-acetylgucosaminidase from Streptomyces griseus. J. Biol. Chem. 249: 811–817.

    Google Scholar 

  63. Tarentino, A.L., Plummer, T.H., and Maley, F. 1974. The release of intact oligosaccharides from specific glycoproteins by endo-beta-N-acetylglucosaminidase H. J. Biol. Chem. 249: 818–824.

    Google Scholar 

  64. Tkacz, J.S., and Lampen, J.O. 1975. Tunicamycin inhibition of polyisoprenyl N-acetylglucosaminyl pyrophosphate formation in calf liver microsomes. Biochem. Biophys. Res. Commun. 65: 248–257.

    Article  Google Scholar 

  65. Tsuzuki, H., Yoshida, M., Onitake, K., and Aketa, K. 1977. Purification of the sperm-binding factor from the egg of the sea urchin Hemicentrotus pulcherrimus. Biochem. Biophys. Res. Commun. 76: 502–511.

    Article  Google Scholar 

  66. Vacquier, V.D., and Moy, G. 1977. Isolation of bindin: the protein responsible for adhesion of sperm to sea urchin eggs. Proc. Nat. Acad. Sci. USA 74: 2456–2460.

    Article  ADS  Google Scholar 

  67. Wassarman, P.M., and Bleil, J.D. 1982. The role of zona pellucida glycoproteins as regulators of sperm-egg interaction in the mouse. In “Cellular Recognition” ( W.A. Frazier, L. Glaser, and D.I. Gottlieb, eds.), pp. 845–863, Alan R. Liss, New York.

    Google Scholar 

  68. Wassarman, P.M. 1983. Fertilization. In “Cell Interactions and Development: Molecular Mechanisms” ( K. Yamada, ed.) pp. 1–27, John Wiley and Sons, New York.

    Google Scholar 

  69. Wassarman, P.M. 1983. Oogenesis: synthetic events in the developing mammalian egg. In “Mechanism and Control of Animal Fertilization”, ( J. F. Hartmann, ed.), pp. 1–54, Academic Press, New York.

    Google Scholar 

  70. Wassarman, P.M., Florman, H.M., and Greve, J.M. 1985. Receptor mediated sperm-egg interactions in mammals. In “Biology of Fertilization” ( C.B. Metz and A. Monroy, eds.), 2: 341 - 360, Academic Press, New York.

    Google Scholar 

  71. Wassarman, P.M., Greve, J.M., Perona, R.M., Roller, R.J., and Salzmann, G.S. 1984. How mouse eggs put on and take off their extracellular coat. In “Molecular Biology of Development” ( E.H. Davidson and R. A. Firtel, eds.), pp. 213–225, Alan R. Liss, New York.

    Google Scholar 

  72. Wolf, D.P., and Hamada, M. 1977. Induction of zonal and oolemmal blocks to sperm penetration in mouse eggs with cortical granule exudate. Biol. Reprod. 21: 205–211.

    Article  Google Scholar 

  73. Yanagimachi, R. 1978. Sperm-egg association in mammals. In “Current Topics in Developmental Biology” ( A. A. Moscona and A. Monroy, eds.), 12: 83–105, Academic Press, New York.

    Google Scholar 

  74. Yanagimachi, R. 1981. Mechanisms of fertilization in mammals. In “Fertilization and Embryonic Development In Vitro” ( L. Mastroianni and J. D. Biggers, eds.) pp. 81–182, Plenum Press, New York.

    Google Scholar 

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Wassarman, P.M., Bleil, J.D., Florman, H.M., Greve, J.M., Roller, R.J., Salzmann, G.S. (1986). Nature of the Mouse Egg’s Receptor for Sperm. In: Hedrick, J.L. (eds) The Molecular and Cellular Biology of Fertilization. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-2255-9_5

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