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Structure and Function of Mammalian Zonae Pellucidae

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Introduction to Mammalian Reproduction

Abstract

The zona pellucida (ZP) is the unique extracellular matrix surrounding the mammalian oocyte. During the fertilization process, sperm must first bind to and penetrate the zona before it comes into contact with its plasma membrane and fuses with the oocyte. While the association of the sperm with the ZP is thought to be a species-specific event in some species, this specificity has been shown to be limited in other mammalian species. After binding, the sperm must penetrate the ZP matrix through limited proteolytic digestion by sperm enzymes. The ZP of some species has also been shown to be modified following fertilization resulting in a block to polyspermy, a process referred to as the “zona reaction”. The zona reaction has been attributed to chemical modifications of the ZP presumably due to the release of components from cortical granules initiated by fertilization (1). The ZP matrix remains intact after fertilization in order to support the cleaving cells of the blastocyst. It has also been thought to aid in the movement of embryo in the oviduct, and to ensure proper embryonic development as well as to prevent embryo fusion in the oviduct.

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References

  1. Yanagimachi R Mammalian fertilization. The physiology of reproduction. Knobil E, Neill JD Editors, Raven Press, New York, 1994.

    Google Scholar 

  2. Prasad SV, Skinner SM, Carino C, Wang N, Cartwright J, Dunbar BS. Structure and Function of the Proteins of the Mammalian Zona pellucida.Cells Tissues Organs 2000; 166: 148–164

    Article  PubMed  CAS  Google Scholar 

  3. Dunbar BS, Wolgemuth DJ. Structure and function of the mammalian zona pellucida, a unique extracellular matrix. Mod Cell Biol 1984; 3:77–111.

    CAS  Google Scholar 

  4. Liang LF, Dean J. Oocyte development: molecular biology of the zona pellucida. Vitam Horm 1992;47: 115–159.

    Google Scholar 

  5. Eppig JJ, Chesnel F, Hirao Y, O’Brien MJ, Pendola FL, Watanabe S, Wigglesworth K Oocyte control of granulosa cell development: how and why. Hum. Reprod 1997; 12: 127–132.

    PubMed  CAS  Google Scholar 

  6. Rankin T, Soyal S, Dean J. The mouse zona pellucida: folliculogenesis, fertility and pre-implantation development. Mol Cell Endocrinol 2000; 25: 21–5.

    Article  Google Scholar 

  7. Dunbar BS, Avery S, Lee V, Prasad SV, Schwann D, Schwoebel E, Skinner S, Wilkins B. The mammalian zona pellucida: Its biochemistry, immunochemistry, molecular biology and developmental expression. Reprod Fertil Dev 1994; 6: 59–76.

    Article  Google Scholar 

  8. Elvin JA, Matzuk MM. Mouse models of ovarian failure. Rev Reprod 1998; 3:183–195.

    Article  PubMed  CAS  Google Scholar 

  9. Dunbar BS, Prasad S, Carino C, Skinner SM. The ovary as an immune target. J Soc Gynecol Investig 2001; 8: S43–8.

    Article  Google Scholar 

  10. Dunbar BS, Prasad SV, Timmons T. Comparative mammalian zonae pellucidae; in Dunbar, B.S., M. O’Rand (eds): Comparative Overview of Mammalian Fertilization. New York, Plenum Press, 1991.

    Google Scholar 

  11. Palmstierna M, Murkes D, Csemiczky G, Andersson O, Wramsby. Zona pellucida thickness variation and occurrence of visible mononucleated blastomers in preembryos are associated with a high pregnancy rate in IVF treatment. J Assist Reprod Genet 1998; 15: 70–75.

    Article  PubMed  CAS  Google Scholar 

  12. Magerkurth C, Topfer-Petersen E, Schwartz P, Michelmann HW. Scanning electron microscopy analysis of the human zona pellucida: influence of maturity and fertilization on morphology and sperm binding pattern. Hum Reprod 1998; 14: 1057–1066.

    Article  Google Scholar 

  13. Maymon BB, Maymon R, Ben-Nun I, Ghetler Y, Shalgi R, Skutelsky E. Distribution of carbohydrates in the zona pellucida of human oocytes. J Reprod Fertil. 1994; 102: 81–86.

    Article  PubMed  CAS  Google Scholar 

  14. Dunbar BS, Timmons TM, Skinner SM, Prasad SV. Molecular analysis of a carbohydrate antigen involved in the structure and function of zona pellucida glycoproteins. Biol Reprod 2001; 65:951–60.

    Article  PubMed  CAS  Google Scholar 

  15. Turner K, Horobin RW. Permeability of the mouse zona pellucida: a structure-staining-correlation model using coloured probes. J Reprod Fertil 1997; 111: 259–265.

    Article  PubMed  CAS  Google Scholar 

  16. Kawana T. Sexually transmitted diseases of alpha herpes virus in women. Nippon Rinsho. 2000; 58: 883–889.

    PubMed  CAS  Google Scholar 

  17. Horgan M, Bersoff-Matcha S. Sexually transmitted diseases and HIV. A female perspective. Dermatol Clin 1998; 16: 847–51.

    Article  PubMed  Google Scholar 

  18. Wassarman PM. Zona pellucida glycoproteins. Annu Rev Biochem 1988; 57: 415–442.

    Article  PubMed  CAS  Google Scholar 

  19. McLeskey SB, Dowds C, Carballada R, White RR, Saling PM.(Molecules involved in mammalian sperm-egg interaction. Int Rev Cytol 1998; 177: 57–113.

    Article  PubMed  CAS  Google Scholar 

  20. Lira S, Schickler M, Wassarman PM. Cis-Acting DNA elements involved in oocyte-specific expression of mouse sperm receptor gene mZP3 are located close to the gene’s transcription start site. Mol. Reprod. Develop 1993; 36: 494–499.

    Article  CAS  Google Scholar 

  21. Liang L, Soyal SM, Dean J. FIGalpha, a germ cell specific transcription factor involved in the coordinate expression of the zona pellucida genes. Development 1997; 124: 4939–4947.

    PubMed  CAS  Google Scholar 

  22. Iwamoto K, Ikeda K, Yonezawa N, Noguchi S, Kudo K, Hamano S, Kuwayama M, Nakano.M Disulfide formation in bovine zona pellucida glycoproteins during fertilization: evidence for the involvement of cystine cross-linkages in hardening of the zona pellucida. J Reprod Fertil 1999; 117: 395–402.

    Article  PubMed  CAS  Google Scholar 

  23. Hughes DC, Barratt CL. Identification of the true human orthologue of the mouse Zpl gene: evidence for greater complexity in the mammalian zona pellucida? Biochim Biophys Acta 1999; 1447: 303–306.

    Article  PubMed  CAS  Google Scholar 

  24. Litscher ES, Qi H, Wassarman PM. Mouse zona pellucida glycoproteins mZP2 and mZP3 undergo carboxy-terminal proteolytic processing in growing oocytes. Biochemistry 1999; 38: 12280–12287.

    Article  PubMed  CAS  Google Scholar 

  25. van Duin M, Polman JE, Suikerbuijk RF, Geurts-van Kessel AH, Olijve W. The human gene for the zona pellucida glycoprotein ZP3 and a second polymorphic locus are located on chromosome 7. Cytogenet Cell Genet 1993; 63: 111–113.

    Article  PubMed  Google Scholar 

  26. Kipersztok S, Osawa GA, Liang LF, Modi WS, Dean J. POM-ZP3, a bipartite transcript derived from human ZP3 and aPOM121 homologue. Genomics 1995; 25: 354–359.

    Article  PubMed  CAS  Google Scholar 

  27. Tulsiani DR, Yoshida-Komiya H, Araki Y. Mammalian fertilization: a carbohydrate-mediated event. Biol Reprod 1997; 57: 487–494.

    Article  PubMed  CAS  Google Scholar 

  28. Takasaki S, Mori E, Mori T. Structures of sugar chains included in mammalian zona pellucida glycoproteins and their potential roles in sperm-egg interaction. Biochim Biophys Acta 1999; 1473: 206–215.

    Article  PubMed  CAS  Google Scholar 

  29. Easton RL, Patankar MS, Lattanzio FA, Leaven TH, Morris HR, Clark GF, Dell A. Structural analysis of murine zona pellucida glycans. Evidence for the expression of core 2-type O-glycans and the Sd(a) antigen., J Biol Chem 2000; 275: 7731–7742.

    Article  PubMed  CAS  Google Scholar 

  30. Tulsiani DR Structural analysis of the asparagine-linked glycan units of the ZP2 and ZP3 glycoproteins from mouse zona pellucida. Arch Biochem Biophys 2000;382: 275–283.

    Article  PubMed  CAS  Google Scholar 

  31. Aviles M, El-Mestrah M, Jaber L, Castells MT, Ballesta J, Kan FW. Cytochemical demonstration of modification of carbohydrates in the mouse zona pellucida during folliculogenesis. Histochem Cell Biol 2000; 113: 207–19.

    Article  PubMed  CAS  Google Scholar 

  32. Talevi R, Gualtieri R, Tartaglione G, Fortunato A. Heterogeneity of the zona pellucida carbohydrate distribution in human oocytes failing to fertilize in vitro. Hum Reprod 1997; 12: 2773–2780.

    Article  PubMed  CAS  Google Scholar 

  33. Nakano M, Yonezawa N. Localization of sperm ligand carbohydrate chains in pig zona pellucida glycoproteins. Cells Tissues Organs 2001; 168: 65–75.

    Article  PubMed  CAS  Google Scholar 

  34. Sinowatz F, Kolle S, Topfer-Petersen E. Biosynthesis and expression of zona pellucida glycoproteins in mammals. Cells Tissues Organs 2001; 168: 24–35.

    Article  PubMed  CAS  Google Scholar 

  35. Carino C, Prasad SV, Skinner SM, Dunbar BD, Larrea F, Dunbar BS. Localization of species conserved zona pellucida antigens in mammalian ovaries. Reproductive Biomedicine Online 2002 (in press).

    Google Scholar 

  36. Takeuchi Y, Nishimura K, Aoki N, Adachi T, Sato C, Kitajima K, Matsuda T. A 42-kDa glycoprotein from chicken egg-envelope, an avian homolog of the ZPC family glycoproteins in mammalian Zona pellucida. Its first identification, cDNA cloning and granulosa cell-specific expression. Eur J Biochem 1999; 260: 736–742.

    Article  PubMed  CAS  Google Scholar 

  37. Prasad SV, Dunbar BS. Human sperm-oocyte recognition and infertility. Semin Reprod Med 2000;18: 141–149.

    Article  PubMed  CAS  Google Scholar 

  38. Yurewicz EC, Sacco AG, Gupta SK, Xu N, Gage DA. Hetero-oligomerization-dependent binding of pig oocyte zona pellucida glycoproteins ZPB and ZPC to boar sperm membrane vesicles. J Biol Chem 1998; 273:7488–7494.

    Article  PubMed  CAS  Google Scholar 

  39. Yamasaki, N, Richardson RT, O’Rand MG. Expression of the rabbit sperm protein Spl7 in COS cells and interaction of recombinant Spl7 with the rabbit zona pellucida. Mol Reprod Dev 1995; 40: 48–55.

    Article  PubMed  CAS  Google Scholar 

  40. Oehinger S. Molecular basis of human sperm-zona pellucida interaction. Cells Tissues Organs 2001; 168: 58–64.

    Article  Google Scholar 

  41. Hinsch, KD, Schill WB, Hinsch E. Induction of acrosome reaction through a synthetic ZP3 peptide. J Reprod Fertil Abstr Ser 1998; 22: 17.

    Google Scholar 

  42. Tsubamoto H, Hasegawa A, Nakata Y, Naito S, Yamasaki N, Koyama K. Expression of recombinant human zona pellucida protein 2 and its binding capacity to spermatozoa. Biol Reprod 1999; 61: 1649–1654.

    Article  PubMed  CAS  Google Scholar 

  43. Govind CK, Gahlay GK, Choudhury S, Gupta SK. Purified and refolded recombinant bonnet monkey (Macaca radiata) zona pellucida glycoprotein-B expressed in Escherichia coli binds to spermatozoa. Biol Reprod 2001; 64: 1147–52.

    Article  PubMed  CAS  Google Scholar 

  44. VandeVoort CA, Schwoebel ED, Dunbar BS. Immunization of monkeys with recombinant cDNA expressed zona pellucida proteins. Fertil Steril 1995; 64: 838–847.

    PubMed  CAS  Google Scholar 

  45. Benoff S. Carbohydrates and fertilization: an overview. Mol Human Reprod 1997; 3: 599–637.

    Article  CAS  Google Scholar 

  46. Litscher ES, Juntunen K, Seppo A, Penttila L, Niemela R, Renkonen O, Wassarman PM. Oligosaccharide constructs with defined structures that inhibit binding of mouse sperm to unfertilized eggs in vitro. Biochemistry 1995; 34: 4662–4669.

    Article  PubMed  CAS  Google Scholar 

  47. Nixon B, Lu Q, Wassler MJ, Foote CI, Ensslin MA, Shur BD. Galactosyltransferase function during mammalian fertilization. Cells Tissues Organs 2001; 168: 46–57.

    Article  PubMed  CAS  Google Scholar 

  48. Loeser CR, Tulsiani DR. The role of carbohydrates in the induction of the acrosome reaction in mouse spermatozoa. Biol Reprod 1999; 60: 94–101.

    Article  PubMed  CAS  Google Scholar 

  49. Green DP. Three-dimensional structure of the zona pellucida. Rev Reprod 1997; 2: 147–56.

    Article  PubMed  CAS  Google Scholar 

  50. Rankin T, O’Brien M, Lee E, Wigglesworth K, Eppig J, Dean J. Defective zonae pellucidae in Zp2-null mice disrupt folliculogenesis, fertility and development. Develop 2001; 128: 1119–1126.

    CAS  Google Scholar 

  51. Paterson M, Jennings ZA, van Duin M, Aitken RJ. Immunocontraception with zona pellucida proteins. Cells Tissues Organs 2000; 166: 228–232.

    Article  PubMed  CAS  Google Scholar 

  52. Lou Y, Tung KSK. T cell peptide of a self-protein elicits autoantibody to the protein antigen. Implications for specificity and pathogenetic role of antibody in autoimmunity. J Immunol 1993; 151: 5790–5799.

    PubMed  CAS  Google Scholar 

  53. Afzalpurkar A, Shibahara H, Hasegawa A, Koyama K, Gupta SK. Immunoreactivity and in-vitro effect on human sperm-egg binding of antibodies against peptides corresponding to bonnet monkey zona pellucida-3 glycoprotein. Hum Reprod 1997; 12: 2664–2670.

    Article  PubMed  CAS  Google Scholar 

  54. Zhang X, Lou YH, Koopman M, Doggett T, Tung KS, Curtiss R Antibody responses and infertility in mice following oral immunization with attenuated Salmonella typhimurium expressing recombinant murine ZP3. Biol Reprod 1997; 56: 33–41.

    Article  PubMed  CAS  Google Scholar 

  55. Jackson RJ, Maguire DJ, Hinds LA, Ramshaw I A. Infertility in mice induced by a recombinant ectromelia virus expressing mouse zona pellucida glycoprotein 3. Biol Reprod 1998; 58: 152–9.

    Article  PubMed  CAS  Google Scholar 

  56. Lou Y, Ang J, Thai H, McElveen F, Tung KS. A zona pellucida 3 peptide vaccine induces antibodies and reversible infertility without ovarian pathology. J. Immunol 1995;155: 2715–2720.

    PubMed  CAS  Google Scholar 

  57. Sun W, Lou YH, Dean J, Tung KS. A contraceptive peptide vaccine targeting sulfated glycoprotein ZP2 of the mouse zona pellucida. Biol Reprod 1999; 60: 900–907

    Article  PubMed  CAS  Google Scholar 

  58. Govind CK, Gupta SK. Failure of female baboons (Papio anubis) to conceive following immunization with recombinant non-human primate zona pellucida glycoprotein-B expressed in Escherichia coll. Vaccine 2000; 18: 2970–2978.

    Article  PubMed  CAS  Google Scholar 

  59. Kerr PJ, Jackson RJ, Robinson AJ, Swan J, Silvers L, French N, Clarke H, Hall DF, Holland MK. Infertility in female rabbits (Oryctolagus cuniculus) alloimmunized with the rabbit zona pellucida protein ZPB either as a purified recombinant protein or expressed by recombinant myxoma virus. Biol Reprod 1999; 61: 606–613.

    Article  PubMed  CAS  Google Scholar 

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Prasad, S.V., Kaul, G., Dunbar, B.S. (2003). Structure and Function of Mammalian Zonae Pellucidae. In: Tulsiani, D.R.P. (eds) Introduction to Mammalian Reproduction. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0273-9_12

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  • DOI: https://doi.org/10.1007/978-1-4615-0273-9_12

  • Publisher Name: Springer, Boston, MA

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