Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 1988 Oct;54(4):643–654. doi: 10.1016/S0006-3495(88)83000-5

Mechanics of sperm-egg interaction at the zona pellucida.

J M Baltz 1, D F Katz 1, R A Cone 1
PMCID: PMC1330369  PMID: 3224150

Abstract

Mammalian sperm traverse several layers of egg vestments before fertilization can occur. The innermost vestment, the zona pellucida, is a glycoprotein shell, which captures and tethers the sperm before they penetrate it. We report here direct measurements of the force required to tether a motile human sperm as well as independent calculations of this force using flagellar beat parameters observed for sperm of several species on their homologous zonae. We have compared these sperm-generated forces with the calculated tensile strength of sperm-zona bonds, and found that a motile sperm can be tethered, at least temporarily, by a single bond. Therefore, sperm can be captured by the first bond formed and tethered permanently by a few. The sperm cannot subsequently penetrate the zona unless the bonds are first eliminated. However, premature elimination would simply allow the sperm to escape. Therefore, not only must the bonds be eliminated, but the timing of this must be regulated so that the sperm is already oriented toward the egg and beginning to penetrate as the bonds are broken.

Full text

PDF
644

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. AUSTIN C. R. Observations on the penetration of the sperm in the mammalian egg. Aust J Sci Res B. 1951 Nov;4(4):581–596. doi: 10.1071/bi9510581. [DOI] [PubMed] [Google Scholar]
  2. Bell G. I. Models for the specific adhesion of cells to cells. Science. 1978 May 12;200(4342):618–627. doi: 10.1126/science.347575. [DOI] [PubMed] [Google Scholar]
  3. Bleil J. D., Wassarman P. M. Mammalian sperm-egg interaction: identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm. Cell. 1980 Jul;20(3):873–882. doi: 10.1016/0092-8674(80)90334-7. [DOI] [PubMed] [Google Scholar]
  4. Bleil J. D., Wassarman P. M. Sperm-egg interactions in the mouse: sequence of events and induction of the acrosome reaction by a zona pellucida glycoprotein. Dev Biol. 1983 Feb;95(2):317–324. doi: 10.1016/0012-1606(83)90032-5. [DOI] [PubMed] [Google Scholar]
  5. Bleil J. D., Wassarman P. M. Structure and function of the zona pellucida: identification and characterization of the proteins of the mouse oocyte's zona pellucida. Dev Biol. 1980 Apr;76(1):185–202. doi: 10.1016/0012-1606(80)90371-1. [DOI] [PubMed] [Google Scholar]
  6. CHANG M. C. Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature. 1951 Oct 20;168(4277):697–698. doi: 10.1038/168697b0. [DOI] [PubMed] [Google Scholar]
  7. Cardullo R. A., Cone R. A. Mechanical immobilization of rat sperm does not change their oxygen consumption rate. Biol Reprod. 1986 Jun;34(5):820–830. doi: 10.1095/biolreprod34.5.820. [DOI] [PubMed] [Google Scholar]
  8. Cummins J. M., Woodall P. F. On mammalian sperm dimensions. J Reprod Fertil. 1985 Sep;75(1):153–175. doi: 10.1530/jrf.0.0750153. [DOI] [PubMed] [Google Scholar]
  9. Denehy M. A., Herbison-Evans D., Denehy B. V. Rotational and oscillatory components of the tailwave in ram spermatozoa. Biol Reprod. 1975 Oct;13(3):289–297. doi: 10.1093/biolreprod/13.3.289. [DOI] [PubMed] [Google Scholar]
  10. Dresdner R. D., Katz D. F. Relationships of mammalian sperm motility and morphology to hydrodynamic aspects of cell function. Biol Reprod. 1981 Dec;25(5):920–930. doi: 10.1095/biolreprod25.5.920. [DOI] [PubMed] [Google Scholar]
  11. Gould J. E., Overstreet J. W., Yanagimachi H., Yanagimachi R., Katz D. F., Hanson F. W. What functions of the sperm cell are measured by in vitro fertilization of zona-free hamster eggs? Fertil Steril. 1983 Sep;40(3):344–352. doi: 10.1016/s0015-0282(16)47298-5. [DOI] [PubMed] [Google Scholar]
  12. Green D. P. Mammalian sperm cannot penetrate the zona pellucida solely by force. Exp Cell Res. 1987 Mar;169(1):31–38. doi: 10.1016/0014-4827(87)90221-7. [DOI] [PubMed] [Google Scholar]
  13. Green D. P., Purves R. D. Mechanical hypothesis of sperm penetration. Biophys J. 1984 Apr;45(4):659–662. doi: 10.1016/S0006-3495(84)84207-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hartmann J. F., Gwatkin R. B., Hutchison C. F. Early contact interactions between mammalian gametes in vitro: evidence that the vitellus influences adherence between sperm and zona pellucida. Proc Natl Acad Sci U S A. 1972 Oct;69(10):2767–2769. doi: 10.1073/pnas.69.10.2767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ishijima S., Mohri H. A quantitative description of flagellar movement in golden hamster spermatozoa. J Exp Biol. 1985 Jan;114:463–475. doi: 10.1242/jeb.114.1.463. [DOI] [PubMed] [Google Scholar]
  16. Isojima S., Kameda K., Tsuji Y., Shigeta M., Ikeda Y., Koyama K. Establishment and characterization of a human hybridoma secreting monoclonal antibody with high titers of sperm immobilizing and agglutinating activities against human seminal plasma. J Reprod Immunol. 1987 Jan;10(1):67–78. doi: 10.1016/0165-0378(87)90051-9. [DOI] [PubMed] [Google Scholar]
  17. Katz D. F., Yanagimachi R., Dresdner R. D. Movement characteristics and power output of guinea-pig and hamster spermatozoa in relation to activation. J Reprod Fertil. 1978 Jan;52(1):167–172. doi: 10.1530/jrf.0.0520167. [DOI] [PubMed] [Google Scholar]
  18. Katz D. F., Yanagimachi R. Movement characteristics of hamster and guinea pig spermatozoa upon attachment to the zona pellucida. Biol Reprod. 1981 Nov;25(4):785–791. doi: 10.1095/biolreprod25.4.785. [DOI] [PubMed] [Google Scholar]
  19. Lillie F. R. THE MECHANISM OF FERTILIZATION. Science. 1913 Oct 10;38(980):524–528. doi: 10.1126/science.38.980.524. [DOI] [PubMed] [Google Scholar]
  20. Lopez L. C., Bayna E. M., Litoff D., Shaper N. L., Shaper J. H., Shur B. D. Receptor function of mouse sperm surface galactosyltransferase during fertilization. J Cell Biol. 1985 Oct;101(4):1501–1510. doi: 10.1083/jcb.101.4.1501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mahi C. A., Yanagimachi R. Maturation and sperm penetration of canine ovarian oocytes in vitro. J Exp Zool. 1976 May;196(2):189–196. doi: 10.1002/jez.1401960206. [DOI] [PubMed] [Google Scholar]
  22. O'Rand M. G., Matthews J. E., Welch J. E., Fisher S. J. Identification of zona binding proteins of rabbit, pig, human, and mouse spermatozoa on nitrocellulose blots. J Exp Zool. 1985 Sep;235(3):423–428. doi: 10.1002/jez.1402350314. [DOI] [PubMed] [Google Scholar]
  23. Peterson R. N., Russell L. D., Hunt W. P. Evidence for specific binding of uncapacitated boar spermatozoa to porcine zonae pellucidae in vitro. J Exp Zool. 1984 Jul;231(1):137–147. doi: 10.1002/jez.1402310118. [DOI] [PubMed] [Google Scholar]
  24. Phillips D. M. Comparative analysis of mammalian sperm motility. J Cell Biol. 1972 May;53(2):561–573. doi: 10.1083/jcb.53.2.561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rikmenspoel R. The tail movement of bull spermatozoa. Observations and model calculations. Biophys J. 1965 Jul;5(4):365–392. doi: 10.1016/S0006-3495(65)86723-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Schmell E. D., Gulyas B. J. Mammalian sperm-egg recognition and binding in vitro. I. Specificity of sperm interactions with live and fixed eggs in homologous and heterologous inseminations of hamster, mouse, and guinea pig oocytes. Biol Reprod. 1980 Dec;23(5):1075–1085. doi: 10.1095/biolreprod23.5.1075. [DOI] [PubMed] [Google Scholar]
  27. Suarez S. S., Katz D. F., Overstreet J. W. Movement characteristics and acrosomal status of rabbit spermatozoa recovered at the site and time of fertilization. Biol Reprod. 1983 Dec;29(5):1277–1287. doi: 10.1095/biolreprod29.5.1277. [DOI] [PubMed] [Google Scholar]
  28. Talbot P., DiCarlantonio G., Zao P., Penkala J., Haimo L. T. Motile cells lacking hyaluronidase can penetrate the hamster oocyte cumulus complex. Dev Biol. 1985 Apr;108(2):387–398. doi: 10.1016/0012-1606(85)90042-9. [DOI] [PubMed] [Google Scholar]
  29. Talbot P. Sperm penetration through oocyte investments in mammals. Am J Anat. 1985 Nov;174(3):331–346. doi: 10.1002/aja.1001740312. [DOI] [PubMed] [Google Scholar]
  30. Wassarman P. M. The biology and chemistry of fertilization. Science. 1987 Jan 30;235(4788):553–560. doi: 10.1126/science.3027891. [DOI] [PubMed] [Google Scholar]
  31. Yanagimachi R. The movement of golden hamster spermatozoa before and after capacitation. J Reprod Fertil. 1970 Oct;23(1):193–196. doi: 10.1530/jrf.0.0230193. [DOI] [PubMed] [Google Scholar]
  32. Yanagimachi R., Usui N. Calcium dependence of the acrosome reaction and activation of guinea pig spermatozoa. Exp Cell Res. 1974 Nov;89(1):161–174. doi: 10.1016/0014-4827(74)90199-2. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES