Advertisement

Species Variation in the Zona Pellucida

  • S. M. Skinner
  • B. S. Dunbar
Part of the Reproductive Biology book series (RBIO)

Abstract

The mammalian fertilization process is an intricate one which involves many aspects of species specificity. Before the fusion of gamete membranes occurs and fertilization is achieved, a number of closely synchronized events must take place. In order to monitor and ultimately to control this process, it is necessary to understand the fundamental nature as well as the timing of these events. Central to the success of fertilization is the ovulation of a mature ovum which is surrounded by a unique extracellular matrix, the zona pellucida (ZP). This glycoprotein matrix surrounds the mammalian oocyte at a time early in follicular development and remains intact until the eventual implantation of the fertilized ovum. After ovulation, the sperm must attach to and penetrate the ZP. Over the past decade, much attention has been brought to studies which have demonstrated that immunization with ZP glycoproteins results in a dramatic reduction in fertility. In order for us to appreciate the mechanisms by which this immunologically induced infertility occurs, it is essential to understand the biochemical and functional properties of the ZP throughout ovarian follicular development.

Keywords

Zona Pellucida Follicular Development Cortical Granule Dolichos Biflorus Agglutinin Zona Pellucida Protein 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aitken, R.J., and Richardson, D.W., 1980, Immunization against zona pellucida antigens, in “Immunological Aspects of Reproduction and Fertility Control,” J.P. Hearn, ed., Lancaster, U.K.: MTP Press Ltd.Google Scholar
  2. Aketa, K., 1973, Physiological studies on the egg surface components responsible for sperm-egg binding in sea urchin fertilization. I. Effect of sperm-binding protein on the fertilizing capacity of sperm, Exp. Cell Res., 70: 439.CrossRefGoogle Scholar
  3. Anderson, N.L., and Anderson, A.G., 1977, High-resolution two-dimensional electrophoresis of human plasma proteins, Proc. Natl. Acad. Sci. USA, 74: 5421.PubMedCrossRefGoogle Scholar
  4. Austin, C.R., and Braden, A.W.H., 1956, Early reactions of the rodent egg spermatozoan penetration, J. Exp. Biol., 33: 358.Google Scholar
  5. Baranska, W., Konwinski, M., and Kuwaja, 1975, Fine structure of the zona pellucida of unfertilized egg cells and embryos, J. Exp. Zool., 192: 193.PubMedCrossRefGoogle Scholar
  6. Barros, C., and Yanagimachi, R., 1971, Induction of zona reaction in golden hamster eggs by cortical granule material, Nature, 233: 258.CrossRefGoogle Scholar
  7. Barros, C., and Yanagimachi, R., 1972, Polyspermy-preventing mechanisms in the golden hamster egg, J. Exp. Zool., 180: 251.PubMedCrossRefGoogle Scholar
  8. Batnagar, P., Skinner, S.M., and Dunbar, B.S., 1985, Antigenicity and immunogenicity of anti-zona pellucida antibodies, (in preparation).Google Scholar
  9. Bedford, J.M., 1977, Sperm/egg interaction: The specificity of human spermatozoa, Anat. Rec., 188: 477.PubMedCrossRefGoogle Scholar
  10. Bleil, J.D., and Wassarman, P.M., 1980a, Synthesis of zona pellucida proteins by denuded and follicle-enclosed mouse oocytes during culture in vitro, Proc. Natl. Acad. Sci. USA, 77: 1029.PubMedCrossRefGoogle Scholar
  11. Bleil, J.D., and Wassarman, P.M., 1980b, Structure and function of the zona pellucida: Identification and characterization of the proteins of the mouse oocyte zona pellucida, Dev. Biol., 76: 185.PubMedCrossRefGoogle Scholar
  12. Braden, A.W.H., Austin, C.R., and David, H.A., 1954, The reaction of the zona pellucida to sperm penetration, Austral. J. Biol. Sci., 7: 391.Google Scholar
  13. Cinader, B., 1977, Enzyme-antibody interactions, in “Methods in Immunology and Immunochemistry,” Vol. 44, C.A. Williams and M.W. Chase, eds., New York: Academic Press, 313.Google Scholar
  14. Crozet, N., and Dumont, M., 1984, The site of the acrosome reaction during in vivo penetration of the sheep oocyte, Gam. Res., 10: 97.CrossRefGoogle Scholar
  15. Drell, D.W., and Dunbar, B.S., 1984, Monoclonal antibodies to rabbit and pig zonae pellucidae distinguish species specific as well as shared antigenic determinants, Biol. Reprod., 30: 435.PubMedCrossRefGoogle Scholar
  16. Drell, D.W., Wood, D.M., Bundman, D.S., and Dunbar, B.S., 1984, Immunological comparison of antibodies to porcine zonae pellucidae in rats and rabbits, Biol. Reprod., 30: 455.Google Scholar
  17. Dudkiewicz, A.B., Shivers, C.A., and Williams, W.L., 1976, Ultrastucture of hamster zona pellucida treated with zona-precipitating antibody, Biol. Reprod., 14: 175.PubMedCrossRefGoogle Scholar
  18. Dunbar, B.S., 1980, Model system to study the relationship between antibodies to zonae and infertility. Comparison of rabbit and porcine zonae pellucidae, Proc. Int. Cong. Anim. Reprod. Artif. Insem., 11: 191.Google Scholar
  19. Dunbar, B.S., and Raynor, B.D., 1980, Characterization of porcine zona pellucida antigens, Biol. Reprod., 22: 941.PubMedCrossRefGoogle Scholar
  20. Dunbar, B.S., Wardrip, N.J., and Hedrick, J.L., 1980, Isolation, physicochemical properties and the macromolecular composition of the zona pellucida from porcine oocytes, Biochemistry, 19: 356.PubMedCrossRefGoogle Scholar
  21. Dunbar, B.S., Liu, C., and Sammons, D.W., 1981), Identification of the three major proteins of porcine and rabbit zonae pellucidae by highresolution two-dimensional gel electrophoresis: Comparison with follicular fluid, sera, and ovarian cell proteins, Biol. Reprod., 24: 1111.PubMedGoogle Scholar
  22. Dunbar, B.S., 1983a, Antibodies to zonae pellucidae antigens and their role in fertility, in “International Congress on Reproductive Immunology,” T. Wegmann and T. Gills (eds.), London: Oxford University Press, 505.Google Scholar
  23. Dunbar, B.S., 1983b, Morphological, biochemical and immunochemical characterization of the mammalian zona pellucida, in “Mechanism and Control of Animal Fertilization,” J. Hartmann (ed.), Academic Press, New York, 139.Google Scholar
  24. Dunbar, B.S., and Wolgemuth, D.J., 1984), Structure and function of the mammalian zona pellucida, a unique extracellular matrix, in “Modern Cell Biology,” B. Satir (ed.), Alan R. Liss, Inc., New York, 3: 77.Google Scholar
  25. Dunbar, B.S., Dudkiewicz, A.B., and Bundman, D.S., 1985, Proteolysis of specific porcine zona pellucida glycoproteins by boar acrosin, Biol. Reprod., 32: 619.PubMedCrossRefGoogle Scholar
  26. East, I.J., and Dean, J., 1984, Monoclonal antibodies as probes of the distribution of ZP-2, the major sulfated glycoprotein of the murine zona pellucida, J. Cell Biol., 98: 795.PubMedCrossRefGoogle Scholar
  27. East, I.J., Mattison, D.R., and Dean, J., 1984a, Monoclonal antibodies to the major proteins of the murine zona pellucida: effects on fertilization and early development, Devel. Biol., 104: 49.CrossRefGoogle Scholar
  28. East, I.J., Keenan, A.M., Larson, S.M., and Dean, J., 1984b, Scintography of normal mouse ovaries with monoclonal antibodies to ZP-2, the major zona pellucida protein, Science, 225:(4665), 938.CrossRefGoogle Scholar
  29. East, I.J., Gulyas, B.J., and Dean, J., 1985, Monoclonal antibodies to the murine zona pellucida protein with sperm receptor activity: effects on fertilization and early development, Devel. Biol., 109: 268.CrossRefGoogle Scholar
  30. Elder, J.H., and Alexander, S., 1982, Endo-N-acetylglucoaminidase F: Endoglycosidase from flavobacterium meningosepticium that cleaves both high mannose and complex glycoproteins, Proc. Natl. Acad. Sci. USA, 79: 4540.PubMedCrossRefGoogle Scholar
  31. Florman, H.M., and Wassarman, P.M., 1985, O-linked oligosaccharides of mouse egg ZP3 account for its sperm receptor activity, Cell, 41: 313.PubMedCrossRefGoogle Scholar
  32. Gaddum-Rosse, P., Blandau, R.J., Langley, L.B., and Barraglia, D.E., 1984, In vitro fertilization in the rat: observations on living eggs, Fertil. Steril, 42(2): 285.PubMedGoogle Scholar
  33. Gerrity, M., Niu, E., and Dunbar, B.S., 1981, A specific radioimmunoassay for evaluation of serum antibodies to zona pellucida antigens, J. Reprod. Immunol., 3: 59.PubMedCrossRefGoogle Scholar
  34. Gianfortoni, J.G., and Gulyas, B.J., 1985, The effects of short-term incubation (aging) of mouse oocytes on in vitro fertilization, zona solubility, and embryonic development, Gam. Res., 11: 59.CrossRefGoogle Scholar
  35. Gibson, R.E., Spilman, C.H., Skinner, S., and Dunbar, B.S., 1985, Passive immunization with polyclonal and monoclonal (McAb) antibodies to zonae pellucidae, Biol. Repr., (submitted).Google Scholar
  36. Glabe, C.G., and Vacquier, V.D., 1977, Isolation and characterization of the vitelline layer of sea urchin eggs, J. Cell Biol., 75: 410.PubMedCrossRefGoogle Scholar
  37. Green, D.P.L., and Purves, R.D., 1984, Mechanical hypothesis of sperm penetration, Biophys. J., 45: 659.PubMedCrossRefGoogle Scholar
  38. Greve, J.M., Salzman, 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.PubMedCrossRefGoogle Scholar
  39. Gulyas, B.J., Gwatkin, R.B.L., and Yuan, L.C., 1983, Active immunization of cynomalgus monkeys (Macaca fascicularis) with porcine zona pellucida, Gam. Res., 7(4): 299.CrossRefGoogle Scholar
  40. Gwatkin, R.B.L., Williams, D.T., and Anderson, O.F., 1973, Zona reaction of mammalian eggs: properties of the cortical granule protease (Cortin) and its receptor substrate in hamster eggs, J. Cell Biol., 59: 128a.Google Scholar
  41. Gwatkin, R.B.L., Carter, H.W., and Patterson, H., 1976, Association of mammalian sperm with the cumulus cells and the zona pellucida studied by scanning electron microscopy. Part IV, “Proceedings of the Workshop on SEM in Reproductive Biology,” O. Johari and R.P. Becker, eds., Chicago: IITRES. Inst. Vd., 379.Google Scholar
  42. Gwatkin, R.B.L., Williams, D.T., and Carlo, D.J., 1977, Immunization of mice with heat-solubilized hamster zonae: production of anti-zona antibody and inhibition of fertility, Fertil. Steril., 28: 871.PubMedGoogle Scholar
  43. Gwatkin, R.B.L., Anderson, O.F., and Williams, D.T., 1980, Large scale isolation of bovine, and pig zonae pellucidae: chemical, immunological, and receptor properties, Gamete Res., 3: 217.CrossRefGoogle Scholar
  44. Habeeb, A.F.S.A., 1977, Influence of conformation on immunochemical properties of proteins, in: “Immunochemistry of Proteins,” Vol. 2, M.Z. Atassi, ed., New York: Plenum Press, 163.CrossRefGoogle Scholar
  45. Hartmann, J.F., and Gwatkin, R.B.L., 1971, Alteration of sites on the mammalian sperm surface following capacitation, Nature, 234: 479.PubMedCrossRefGoogle Scholar
  46. Hartmann, J.F., Gwatkin, R.B.L., and Hutchison, C.F., 1972, Early contact interactions between mammalian gametes in vitro: evidence that the vitellus influences adherence between sperm and zona pellucida, Proc. Natl. Acad. Sci. USA, 69: 2767.PubMedCrossRefGoogle Scholar
  47. Hartmann, J.F., and Hutchison, C.F., 1974, Nature of pre-penetration contact interaction between hamster gametes in vitro, J. Reprod. Fertil., 36: 49.PubMedCrossRefGoogle Scholar
  48. Hedrick, J.L., and Fry, G.N., 1980, Immunocytochemical studies on the porcine zona pellucida, J. Cell Biol., 87: 136a.Google Scholar
  49. Huang, T.T.F., and Yanagimachi, R., 1984, Fucoidin inhibits attachment of guinea pig spermatozoa to the zona pellucida through binding to the lunar acrosomal membrane and equatorial domains, Exp. Cell Res., 153: 363.PubMedCrossRefGoogle Scholar
  50. Isojima, S., Koyama, K., Hasegawa, A., Tsunoda, Y., and Hanadu, A., 1984, Monoclonal antibodies to porcine zona pellucida antigens and their inhibitory effects on fertilization, J. Reprod. Immun., 6 (2):77.CrossRefGoogle Scholar
  51. Jackowski, S., and Dumont, J.N., 1979, Surface alterations of the mouse zona pellucida and ovum following in vitro fertilization: correlation with cell cycle, Biol. Reprod., 20: 150.PubMedCrossRefGoogle Scholar
  52. Kamada, M., Hasebe, H., Milrahara, T., Kinoshita, T., Naka, O., and Mori, T., 1984, Detection of anti-zona pellucida activities in human sera by the passive hemagglutination reaction, Fertil. Steril., 41(6): 901.PubMedGoogle Scholar
  53. Karp, D.R., Atkinson, J.P., and Shreffler, D.C., 1982, Genetic variation in glycosylation of the fourth component of murine complement, J. Biol. Chem., 257 (13):7330.PubMedGoogle Scholar
  54. Kennett, R.H., McKearn, T.J., and Bechtol, K.B., 1980, “Monoclonal antibodies. Hybridomas: A new dimension in biological analyses,” Plenum Press, New York.Google Scholar
  55. Kinsey, W.H., and Lennarz, W.J., 1981, Isolation of a glycopeptide fraction from the surface of the sea urchin egg that inhibits sperm-egg binding and fertilization, J. Cell Biol., 91: 325.PubMedCrossRefGoogle Scholar
  56. Kohler, G., and Milstein, C., 1975, Continuous cultures of fused cells secreting antibody of predefined specificity, Nature, 256: 495.PubMedCrossRefGoogle Scholar
  57. Kuzan, F.B., Fleming, A.D., and Seidel, G.E., 1984, Successful fertilization in vitro of fresh, intact oocytes by perivitelline (acrosomereacted) spermatozoa of the rabbit, Fertil. Steril., 41 (5): 766.PubMedGoogle Scholar
  58. Mahi-Brown, C.A., and Yanagimachi, R., 1985, Effect of immunization with porcine zona pellucida on ovarian cycles in the bitch, In press (Biol. Reprod.).Google Scholar
  59. Mhasker, A., Buckshee, K., and Talwar, G.P., 1984, Autoantibodies to zona pellucida in tubectomized women, Contraception, 29(i):75.CrossRefGoogle Scholar
  60. Mintz, B., 1962, Experimental study of the developing mammalian egg: removal of the zona pellucida, Science, 138: 594.PubMedCrossRefGoogle Scholar
  61. Modlinski, J.A., 1970, The role of the zona pellucida in the development of mouse eggs in vivo, J. Embryol. Exp. Morph., 23: 539.PubMedGoogle Scholar
  62. Nayuda, P.L., Freeman, L.E., and Trounson, A.O., 1982a, Zona pellucida antibodies in human sera, J. Reprod. Fertil., 65: 77.CrossRefGoogle Scholar
  63. Nayuda, P.L., Freeman, L.E., and Trounson, A.O., 1982b, A quantitative indirect immunofluorescent assay for zona pellucida antibodies, J. Reprod. Fertil., 65: 67.CrossRefGoogle Scholar
  64. Nicholson, G.L., Yanagimachi, R., and Yanagimachi, H., 1975, Ultrastructural localization of lectin-binding sites on the zonae pellucidae and plasma membranes of mammalian eggs, J. Cell Biol., 66: 263.CrossRefGoogle Scholar
  65. Nishimoto, T., Mori, T., Yamada, I., and Nishimura, T., 1980, Autoantibodies to zona pellucida in infertile and aged women, Fertil. Steril., 34: 522.Google Scholar
  66. Oikawa, T., Nicholson, G.L., and Yanagimachi, R., 1975, Trypsin-mediated modification of the zona pellucida glycopeptide structure of hamster eggs, J. Reprod. Fertil., 43: 133.PubMedCrossRefGoogle Scholar
  67. O’Rand, M.G., Matthews, J.E., Welch, J.E., Fisher, S.J., 1985, Identification of zona binding proteins of rabbit, pig, human and mouse spermatozoa on nitrocellulose blots, J. Expl Zool., (in press).Google Scholar
  68. Overstreet, J.W., and Bedford, J.M., 1975, The penetrability of rabbit ova treated with enzymes or anti-progesterone antibodies: a probe into the nature of mammalian fertilization, J. Reprod. Fertil., 44: 273.PubMedCrossRefGoogle Scholar
  69. Phillips, D.M., and Shalgi, R.M., 1980, Surface properties of the zona pellucida, J. Exp. Zool., 213: 1.PubMedCrossRefGoogle Scholar
  70. Sacco, A.G., and Moghiss, K.S., 1979, Anti-zona pellucida activity in human sera, Fertil. Steril., 31: 503.PubMedGoogle Scholar
  71. Sacco, A.G., Subramanian, G., and Yurewicz, E.C., 1981, Application of a radioimmunoassay (RIA) for monitoring immune response to porcine zona pellucida, Proc. Soc. Expt. Biol. Mod., 167: 318.Google Scholar
  72. Sacco, A.G., Subramanian, M.G., and Yurewicz, E.C., 1981, Active immunization of mice with porcine zonae pellucidae: immune response and effect on fertility, J. Exp. Zool., 218: 405.PubMedCrossRefGoogle Scholar
  73. Sacco, A.G., Yurewicz, E.C., Subramanian, M.G., and DeMayo, F.J., 1982, Zona pellucida composition: Species crossreactivity and contraceptive potential of antiserum of a partially purified pig zona antigen, Biol. Reprod., 25: 997.CrossRefGoogle Scholar
  74. Sacco, A.G., Yurewicz, E.C., and Zhang, S., 1983a, Immunoelectrophoretic analysis of the porcine zona pellucida, J. Repr. Fertil., 68: 21.CrossRefGoogle Scholar
  75. Sacco, A.G., Subramanian, M.G., Yurewicz, E.C., DeMayo, F.J., and Dukelow, W.R., 1983b, Heteroimmunization of squirrel monkeys (Saineri sciureus) with a purified porcine zona antigen: Immune response and biological activity of antiserum, Fertil. Steril., 39: 350.PubMedGoogle Scholar
  76. Sacco, A.G., Subramanian, M.G., and Yurewicz, E.C., 1984, Association of sperm receptor activity with a purified pig zona antigen (PPZA), J. Rep. Immunol., 6: 89.CrossRefGoogle Scholar
  77. Saling, P.M., Storey, B.T., and Wolf, D.P., 1978, Calcium-dependent binding of mouse epididymal spermatozoa to the zona pellucida, Devel. Biol., 65: 515.CrossRefGoogle Scholar
  78. Sammons, D.W., Anderson, L.D., and Nishiawa, E.E., 1981, Ultrasensitive color-based silver staining of polypeptides in Polyacrylamide gels, Electrophor., 2: 135.CrossRefGoogle Scholar
  79. Sellens, M.H., and Jenkinson, E.J., 1975, Permeability of the mouse zona pellucida to immunoglobulin, J. Reprod. Fertil., 42: 153.PubMedCrossRefGoogle Scholar
  80. Shimizu, S., Masahiro, T., and Dean, J., 1983, In vitro biosynthesis of three sulfated glycoproteins of murine ZP by oocytes grown in follicle culture, J. Biol. Chem., 258 (9): 5858.PubMedGoogle Scholar
  81. Shur, B.D., and Hall, N.G., 1982, A role for mouse sperm galactosyltransferase in sperm binding to the egg zona pellucida, J. Cell Biol., 95 (2): 574.PubMedCrossRefGoogle Scholar
  82. Skinner, S.M., Mills, T., Kirchick, H.J., and Dunbar, B.S., 1984, Immunization with zona pellucida proteins results in abnormal ovarian follicular differentiation and inhibition of gonadotropin-induced steroid secretion, Endocrin., 115 (b): 2418.CrossRefGoogle Scholar
  83. Stambaugh, R.L., and Nicosia, S.V., 1984, Localization of tubulin and microtubules of in vitro fertilized rabbit oocytes, J. Androl., 5: 259.PubMedGoogle Scholar
  84. Surneva-Nakova, T., and Nakov, L.S., 1982, Immunoelectrophoretic characterization of antigens of porcine zona pellucida, Comptes rendus de l’Acadmie blugare des sciences, Tome 35(9): 1307.Google Scholar
  85. Surneva-Nakova, N., Nakov, L.S., Kyurkchiev, S.D., Gancheva, S.D., and Yalumov, O.I., 1984, Study on the specificity of pig zona pellucida by enzyme-linked immunoadsorbent assay (ELISA), Comptes rendus de l’Academi bulgare des Sciences, 37 (7): 975.Google Scholar
  86. Swenson, C.E., and Dunbar, B.S., 1982, Specificity of sperm-zona interaction, J. Exp. Zool., 219: 97.PubMedCrossRefGoogle Scholar
  87. Talbot, P., and DiCarlantonio, G., 1984a, The oocyte-cumulus complex: ultrastructure of the extracellular components in hamsters and mice, Gam. Res., 10: 127.CrossRefGoogle Scholar
  88. Talbot, P., and DiCarlantonio, G., 1984b, Ultrastructure of opossum oocyte investing coats and their senstivity to trypsin and hyaluronidase, Devel. Biol., 103: 159.CrossRefGoogle Scholar
  89. Urch, U.A., Wardrip, N.J., and Hedrick, J.L., 1985, Limited and specific proteolysis of the zona pellucida by acrosin, J. Exper. Zool., 233: 479.CrossRefGoogle Scholar
  90. Watanabe, M., Muramatsu, T., Shirne, H., and Ugai, K., 1981, Discrete distribution of binding sites for dolichos biflorus agglutinin (DBA) and for peanut agglutinin (PNA) in mouse organ tissues, J. Histochem. Cytochem., 29: 779.PubMedCrossRefGoogle Scholar
  91. Wolgemuth, D.J., and Gavin, B.J., 1981, Ultrastructural and biochemical characterization of gene expression on follicular oocytes in neonatal and prepubertal rats, in “Proceedings of the Fifth Workshop on Development and Function of the Reproductive Organs,” Byskov, A.G. (ed.), Amsterdam: Excerpta Medica, 289.Google Scholar
  92. Wolgemuth, D.J., Gavin, B.J., Wood, D.M., Celenza, J.L., and Dunbar, B.S., 1982, Differences in crossreactivity of zona pellucida antigens among mammals, J. Cell Biol., 95 (2): 8032.Google Scholar
  93. Wolgemuth, D.J., Celenza, J., Bundman, D.S., and Dunbar, B.S., 1984, Formation of the rabbit zona pellucida and its relationship to ovarian follicular development, Devel. Biol., 106: 1.CrossRefGoogle Scholar
  94. Wood, D.M., Liu, C., and Dunbar, B.S., 1981, The effect of alloimmunization and heteroimmunization with zonae pellucidae on fertility in rabbits, Biol. Reprod., 25: 439.PubMedCrossRefGoogle Scholar
  95. Yanagimachi, R., 1977, Specificity of sperm-egg interaction, in: “Immunobiology of Gametes,” M. Edidin and M.H. Johnson (eds.), Cambridge: Cambridge University Press, 187.Google Scholar
  96. Yanagimachi, R., and Phillips, D.M., 1984, The status of acrosomal caps of hamster spermatozoa immediately before fertilization in vivo, Gam. Res., 9: 1.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1986

Authors and Affiliations

  • S. M. Skinner
    • 1
  • B. S. Dunbar
    • 1
  1. 1.Department of Cell BiologyBaylor College of MedicineHoustonUSA

Personalised recommendations