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Complementarity between sperm surface β-l,4-galactosyl-transferase and egg-coat ZP3 mediates sperm–egg binding

Nature volume 357, pages 589–593 (1992)Cite this article

Abstract

DESPITE its importance, the molecular basis of mammalian gamete recognition has remained unclear. The enzyme β-1,4-galactosyltransferase (Gal-transferase) has been viewed traditionally as a biosynthetic component of the Golgi complex, but is also found on the surface of many cells where it can bind its specific glycoside substrate on adjacent cell surfaces or in the extracellular matrix1–3. In mouse it has been suggested that Gal-transferase on the sperm head mediates fertilization by binding oligosaccharide residues in the egg coat, or zona pellucida4–9, and that the ability of the zona pellucida to bind sperm is conferred by oligosaccharides of the ZP3 glycoprotein10,13. However, it has not been confirmed that Gal-transferase and ZP3 are in fact complementary gamete receptors whose interaction mediates sperm–egg binding. Here we show that mouse sperm Gal-transferase specifically recognizes those oligosaccharides on ZP3 that have sperm-binding activity, but does not interact with other zona pellucida glycoproteins. In contrast, all zona pellucida glyco-proteins are recognized by non-sperm Gal-transferase, demonstrating a more stringent substrate specificity for the sperm enzyme. This interaction is required for sperm–egg binding because blocking or removing the binding site for Gal-transferase on ZP3 inhibits its ability to bind sperm. After the release of the sperm acrosome, the transferase relocalizes to a new membrane domain where it can no longer bind to ZP3, which is consistent with the inability of acrosome-reacted sperm to bind ZP3 or to initiate binding to the zona pellucida. Following fertilization, ZP3 is modified by egg cortical granule secretions so that it loses sperm receptor activity, which can be accounted for by a selective loss of its binding site for sperm Gal-transferase. These results show that sperm surface β-1,4-galactosyltransferase and the egg-coat glycoprotein ZP3 are complementary adhesion molecules that mediate primary gamete binding in the mouse.

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References

  1. Shur, B. D. Glycobiology 1, 563–575 (1991).

    Article  CAS  Google Scholar 

  2. Roth, S. Q. Rev. Biol. 48, 541–563 (1973).

    Article  CAS  Google Scholar 

  3. Roseman, S. Chem. Phys. Lipids 5, 270–297 (1970).

    Article  CAS  Google Scholar 

  4. Lopez, L. C. & Shur, B. D. J. Cell Biol. 105, 1663–1670 (1987).

    Article  CAS  Google Scholar 

  5. Shur, B. D. & Neely, C. A. J. biol. Chem. 263, 17706–17714 (1988).

    CAS  PubMed  Google Scholar 

  6. Fayrer-Hosken, R. A., Caudle, A. B. & Shur, B. D. Molec. Reprod. Dev. 28, 74–78 (1991).

    Article  CAS  Google Scholar 

  7. Benau, D. A. & Storey, B. T. Biol. Reprod. 39, 235–244 (1988).

    Article  CAS  Google Scholar 

  8. Shur, B. D. & Hall, N. G. J. Cell Biol. 95, 574–579 (1982).

    Article  CAS  Google Scholar 

  9. Lopez, L. C. et al. J. Cell Biol. 101, 1501–1510 (1985).

    Article  CAS  Google Scholar 

  10. Florman, H. M., Bechtol, K. B. & Wassarman, P. M. Devl Biol. 106, 243–255 (1984).

    Article  CAS  Google Scholar 

  11. Leyton, L. & Saling, P. J. Cell Biol. 108, 2163–2168 (1989).

    Article  CAS  Google Scholar 

  12. Macek, M. B., Lopez, L. C. & Shur, B. D. Devl Biol. 147, 440–444 (1991).

    Article  CAS  Google Scholar 

  13. Florman, H. M. & Wassarman, P. M. Cell 41, 313–324 (1985).

    Article  CAS  Google Scholar 

  14. Bleil, J. D. & Wassarman, P. M. Proc. natn. Acad. Sci. U.S.A. 85, 6778–6782 (1988).

    Article  ADS  CAS  Google Scholar 

  15. Bleil, J. D. & Wassarman, P. M. J. Cell Biol. 102, 1363–1371 (1986).

    Article  CAS  Google Scholar 

  16. Bleil, J. D., Greve, J. M. & Wassarman, P. M. Devl Biol. 128, 376–385 (1988).

    Article  CAS  Google Scholar 

  17. Blobel, C. P. et al. Nature 356, 248–252 (1992).

    Article  ADS  CAS  Google Scholar 

  18. Jones, R., Brown, C. R. & Lancaster, R. T. Development 102, 781–792 (1988).

    CAS  Google Scholar 

  19. Bleil, J. D. & Wassarman, P. M. Cell 20, 873–882 (1980).

    Article  CAS  Google Scholar 

  20. Wassarman, P. A. Rev. Biochem. 57, 415–442 (1988).

    Article  CAS  Google Scholar 

  21. Lambert, C. C. Development 105, 415–420 (1989).

    CAS  PubMed  Google Scholar 

  22. Prody, G. A., Greva, L. C. & Hedrick, J. L. J. exp. Zool. 235, 335–340 (1985).

    Article  CAS  Google Scholar 

  23. Bleil, J. D. & Wassarman, P. M. Proc. natn. Acad. Sci. U.S.A. 87, 5563–5567 (1990).

    Article  ADS  CAS  Google Scholar 

  24. Leyton, L. & Saling, P. Cell 57, 1123–1130 (1989).

    Article  CAS  Google Scholar 

  25. Humphreys-Beher, M. G., Garrison, P. W. & Blackwell, R. E. Fertil. Steril. 54, 133–137 (1990).

    Article  CAS  Google Scholar 

  26. Miller, D. J., Cross, N. L., Vazquez-Levin, M. & Shur, B. D. in Comparative Spermatology—20 Years After (eds Baccetti, B.) 569–574 (Serono Symp., Raven, New York, 1992).

    Google Scholar 

  27. Sullivan, R., Ross, P. & Berube, B. Biochem. biophys. Res. Commun. 162, 184–188 (1989).

    Article  CAS  Google Scholar 

  28. Berger, T., Davis, A., Wardrip, N. J. & Hedrick, J. L. J. Reprod. Fertil. 86, 559–565 (1989).

    Article  CAS  Google Scholar 

  29. Fayrer-Hosken, R. A., McBride, C. E. & Brackett, B. G. Biol. Reprod. 36, 53 (1987).

    Article  Google Scholar 

  30. Mori, E. et al. Biochemistry 30, 2078–2087 (1991).

    Article  CAS  Google Scholar 

  31. Ruiz-Bravo, N. & Lennarz, W. J. Devl Biol. 118, 202–208 (1986).

    Article  CAS  Google Scholar 

  32. Baranski, T. J., Faust, P. L. & Kornfeld, S. Cell 63, 281–291 (1990).

    Article  CAS  Google Scholar 

  33. Begovac, P. C., Hall, D. E. & Shur, B. D. J. Cell Biol. 113, 637–644 (1991).

    Article  CAS  Google Scholar 

  34. Passaniti, A. & Hart, G. W. Cancer Res. 50, 7261–7271 (1990).

    CAS  PubMed  Google Scholar 

  35. Schachter, H. Biochem. Cell. Biol. 64, 163–181 (1986).

    Article  CAS  Google Scholar 

  36. Neill, J. M. & Olds-Clarke, P. Gamete Res. 20, 459–473 (1988).

    Article  CAS  Google Scholar 

  37. Endo, Y., Lee, M. A. & Kopf, G. S. Devl Biol. 119, 210–216 (1987).

    Article  CAS  Google Scholar 

  38. Beer, D. & Vasella, A. Helv. chim. Acta 68, 2254–2274 (1985).

    Article  CAS  Google Scholar 

  39. Neter, J. & Wasserman, W. Applied Linear Statistical Models (Irwin, Homewood, Illinois, 1974).

    Google Scholar 

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  1. Barry D. Shur: To whom correspondence should be addressed.

Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, The University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Boulevard, Box 117, Houston, Texas, 77030, USA

    David J. Miller, Mary B. Macek & Barry D. Shur

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  1. David J. Miller
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  2. Mary B. Macek
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  3. Barry D. Shur
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Miller, D., Macek, M. & Shur, B. Complementarity between sperm surface β-l,4-galactosyl-transferase and egg-coat ZP3 mediates sperm–egg binding. Nature 357, 589–593 (1992). https://doi.org/10.1038/357589a0

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