1,821
Views
26
CrossRef citations to date
0
Altmetric
Review

The Mammalian Zona Pellucida: A Matrix That Mediates Both Gamete Binding and Immune Recognition?

Pages 349-364 | Received 08 Jul 2009, Accepted 18 Sep 2009, Published online: 21 Jul 2010

REFERENCES

  • Amari, S., Yonezawa, N., Mitsui, S., Katsumata, T., Hamano, S., Kuwayama, M., Hashimoto, Y., Suzuki, A., Takeda, Y. and Nakano, M. (2001) Essential role of the nonreducing terminal α-mannosyl residues of the N-linked carbohydrate chain of bovine zona pellucida glycoproteins in sperm-egg binding. Mol Reprod Dev 59:221–226.
  • Baba, T., Niida, Y., Michikawa, Y., Kashiwabara, S., Kodaira, K., Takenaka, et al. (1994) An acrosomal protein, sp32, in mammalian sperm is a binding protein specific for two proacrosins and an acrosin intermediate. J Biol Chem 269:10133–10140.
  • Bansal, P., Chakrabarti, K. and Gupta, S. K. (2009) Functional activity of human ZP3 primary sperm receptor resides toward its C-terminus. Biol Reprod 81:7–15.
  • Barber, L. D., Patel, T. K. Percival, L., Gumperz, J. E., Lanier, L. L., Phillips, J.?H., et al. (1996) Unusual uniformity of the N-linked oligosaccharides of HLA-A, -B, and –C glycoproteins. J Immunol 156:3275–3284.
  • Bauskin, A. R., Franken, D. R., Eberspaecher, U. and Donner, P. (1999) Characterization of human zona pellucida glycoproteins. Mol Hum Reprod 5:534–540.
  • Bedford, J. M. (1977) Sperm/egg interaction: the specificity of human spermatozoa. Anat Rec 188:477–487.
  • Berger, T., Davis, A., Wardrip, N. J. and Hedrick, J. L. (1989a) Sperm binding to the pig zona pellucida and inhibition of binding by solubilized components of the zona pellucida. J Reprod Fertil 86:559–565.
  • Berger, T., Turner, K. O., Meizel, S. and Hedrick, J. L. (1989b) Zona pellucida-induced acrosome reaction in boar sperm. Biol Reprod 40:525–530.
  • Bleil, J. D., Greve, J. M. and Wassarman, P. M. (1988) Identification of a secondary sperm receptor in the mouse egg zona pellucida: role in maintenance of binding of acrosome-reacted sperm to eggs. Dev Biol 128:376–385.
  • Bleil, J. D. and Wassarman, P. M. (1978) Identification and characterization of proteins of zona pellucida. J Cell Biol 79:A173.
  • Bleil, J. D. and Wassarman, P. M. (1980a) Structure and function of the zona pellucida: identification and characterization of the proteins of the mouse oocyte's zona pellucida. Dev Biol 76:185–202.
  • Bleil, J. D. and Wassarman, P. M. (1980b) Mammalian sperm-egg interaction: identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm. Cell 20:873–882.
  • 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. Dev Biol 95:317–324.
  • Bleil, J. D. and Wassarman, P. M. (1988) Galactose at the nonreducing terminus of O-linked oligosaccharides of mouse egg zona pellucida glycoprotein ZP3 is essential for the glycoprotein's sperm receptor activity. Proc Natl Acad Sci USA 85:6778–6782.
  • Boja, E. S., Hoodbhoy, T., Fales, H. M. and Dean, J. (2003) Structural characterization of native mouse zona pellucida proteins using mass spectrometry. J Biol Chem 278:34189–34202.
  • Breed, W. G., Hope, R. M., Wiebkin, O. W., Spargo, S. C. and Chapman, J. A. (2002) Structural organization and evolution of the marsupial zona pellucida. Reproduction 123:13–21.
  • Buffone, M. G., Foster, J. A. and Gerton, G. L. (2008a) The role of the acrosomal matrix in fertilization. Int J Dev Biol 52:511–522.
  • Buffone, M. G., Zhuang, T., Ord, T. S., Hui, L., Moss, S. B. and Gerton, G. L. (2008b) Recombinant mouse sperm ZP3-binding protein (ZP3R/sp56) forms a high order oligomer that binds eggs and inhibits mouse fertilization in vitro. J Biol Chem 283:12438–12445.
  • Burkman, L. J., Coddington, C. C., Franken, D. R., Krugen, T. F., Rosenwaks, Z. and Hogen, G. D. (1988) The hemizona assay (HZA): development of a diagnostic test for the binding of human spermatozoa to the human hemizona pellucida to predict fertilization potential. Fertil Steril 49:688–697.
  • Calvete, J. J., Carrera, E., Sanz, L. and Topfer-Petersen, E. (1996) Boar spermadhesins AQN-1 and AQN-3: oligosaccharide and zona pellucida binding characteristics. Biol Chem 377:521–527.
  • Chakravarty, S., Kadunganattil, S., Bansal, P., Sharma, R. K. and Gupta, S. K. (2008) Relevance of glycosylation of human zona pellucida glycoproteins for their binding to capacitated human spermatozoa and subsequent induction of acrosomal exocytosis. Mol Reprod Dev 75:75–88.
  • Chakravarty, S., Kadunganattil, S. and Gupta, S. K. (2005) Baculovirus expressed recombinant human zona pellucida glycoprotein-B induces acrosomal exocytosis in capacitated spermatozoa in addition to zona pellucida glycoprotein-C. Mol Hum Reprod 11:365–372.
  • Chamberlin, M. E. and Dean, J. (1989) Genomic organization of a sex specific gene: the primary sperm receptor of the mouse zona pellucida. Dev Biol 131:207–214.
  • Chamberlin, M. E. and Dean, J. (1990) Human homolog of the mouse sperm receptor. Proc Natl Acad Sci USA 87:6014–6018.
  • Chapman, N., Kessopoulou, E., Andrews, P., Hornby, D. and Barratt, C. R. (1998) The polypeptide backbone of recombinant human zona pellucida glycoprotein-3 initiates acrosomal exocytosis in human spermatozoa in vitro. Biochem J 330 (Pt 2):839–845.
  • Chen, J., Litscher, E. S. and Wassarman, P. M. (1998) Inactivation of the mouse sperm receptor, mZP3, by site-directed mutagenesis of individual serine residues located at the combining site for sperm. Proc Natl Acad Sci USA 95:6193–6197.
  • Chiu, P. C., Chung, M. K., Koistinen, R., Koistinen, H., Seppala, M., Ho, P. C., et al. (2007) Glycodelin-A interacts with fucosyltransferase on human sperm plasma membrane to inhibit spermatozoa-zona pellucida binding. J Cell Sci 120:33–44.
  • Chiu, P. C., Chung, M. K., Tsang, H. Y., Koistinen, R., Koistinen, H., Seppala, M., et al. (2005) Glycodelin-S in human seminal plasma reduces cholesterol efflux and inhibits capacitation of spermatozoa. J Biol Chem 280:25580–25589.
  • Chiu, P. C., Ho, P. C., Ng, E. H. and Yeung, W. S. (2002) Comparative study of the biological activity of spermatozoa-zona pellucida binding inhibitory factors from human follicular fluid on various sperm function parameters. Mol Reprod Dev 61:205–212.
  • Chiu, P. C., Wong, B. S., Chung, M. K., Lam, K. K., Pang, R. T., Lee, K. F., et al. (2008b) Effects of native human zona pellucida glycoproteins 3 and 4 on acrosome reaction and zona pellucida binding of human spermatozoa. Biol Reprod 79:869–877.
  • Chiu, P. C., Wong, B. S., Lee, C. L., Pang, R. T., Lee, K. F., Sumitro, S. B., Gupta, S. K. and Yeung, W. S. (2008a) Native human zona pellucida glycoproteins: purification and binding properties. Hum Reprod 23:1385–1393.
  • Clark, G. F. and Dell, A. (2006) Molecular models for murine sperm-egg binding. J Biol Chem 281:13853–13856.
  • Clark, G. F., Dell, A., Morris, H. R. and Patankar, M. S. (2006) The eutherian fetoembryonic defense system hypothesis: an update. In Immunology of Pregnancy ed. Mor, G. Landes Bioscience/Springer Science Business Media New York, NY pp. 179–194.
  • Clark, G. F., Dell, A., Morris, H. R., Patankar, M. S. and Easton, R. L. (2001) The species recognition system: a new corrolary for the human fetoembryonic defense system hypothesis. Cells Tissue Organs 168:113–121.
  • Clark, G. F., Oehninger, S. and Seppala, M. (1996) Role for glycoconjugates in cellular communication in the human reproductive system. Mol Hum Reprod 2:513–517.
  • Clark, G. F., Sutovsky, P., Zimmerman, S., and Lafrenz, D. E. (2009) Carbohydrate-mediated binding and induction of acrosomal exocytosis in a sperm-somatic cell adhesion model. Biol Reprod 81: 328 (abstr.).
  • Dell, A., Chalabi, S., Easton, R. L., Haslam, S. M., Sutton-Smith, M., Patankar, M. S., et al. (2003) Murine and human ZP3 derived from mouse eggs express identical O-glycans. Proc Natl Acad Sci USA 100:15631–15636.
  • Dell, A., Morris, H. R., Easton, R. L., Panico, M., Patankar, M., Oehniger, S., et al. (1995) Structural analysis of the oligosaccharides derived from glycodelin, a human glycoprotein with potent immunosuppressive and contraceptive activities. J Biol Chem 270:24116–24126.
  • Demetriou, M., Granovsky, M., Quaggin, S. and Dennis, J. W. (2001) Negative regulation of T-cell activation and autoimmunity by Mgat5 N-glycosylation. Nature 409:733–739.
  • Dunbar, B. S., Wardrip, N. J. and Hedrick, J. L. (1978) Isolation and physicochemical properties of porcine zona pellucida. J Cell Biol 79:A163.
  • Easton, R. L., Patankar, M. S., Lattanzio, F. A., Leaven, T. H., Morris, H. R., Clark, G. F. and Dell, A. (2000) Structural analysis of murine zona pellucida glycans. Evidence for the expression of core 2-type O-glycans and the Sda antigen. J Biol Chem 275:7731–7742.
  • el Ouagari, K., Teissie, J. and Benoist, H. (1995) Glycophorin A protects K562 cells from natural killer cell attack. Role of oligosaccharides. J Biol Chem 270:26970–26975.
  • Ensslin, M., Calvete, J. J., Thole, H. H., Sierralta, W. D., Adermann, K., Sanz, L. and Topfer-Petersen, E. (1995) Identification by affinity chromatography of boar sperm membrane-associated proteins bound to immobilized porcine zona pellucida. Mapping of the phosphorylethanolamine-binding region of spermadhesin AWN. Biol Chem Hoppe Seyler 376:733–738.
  • Ensslin, M. A. and Shur, B. D. (2003) Identification of mouse sperm SED1, a bimotif EGF repeat and discoidin-domain protein involved in sperm-egg binding. Cell 114:405–417.
  • Epifano, O., Liang, L. F. and Dean, J. (1995) Mouse Zp1 encodes a zona pellucida protein homologous to egg envelope proteins in mammals and fish. J Biol Chem 270:27254–27258.
  • Florman, H. M., Bechtol, K. B. and Wassarman, P. M. (1984) Enzymatic dissection of the functions of the mouse egg's receptor for sperm. Dev Biol 106:243–255.
  • Florman, H. M. and First, N. L. (1988) The regulation of acrosomal exocytosis. I. Sperm capacitation is required for the induction of acrosome reactions by the bovine zona pellucida in vitro. Dev Biol 128:453–463.
  • Florman, H. M., Jungnickel, M. K. and Sutton, K. A. (2008) Regulating the acrosome reaction. Int J Dev Biol 52:503–510.
  • Foster, J. A., Friday, B. B., Maulit, M. T., Blobel, C., Winfrey, V. P., Olson, G. E., et al. (1997) AM67, a secretory component of the guinea pig sperm acrosomal matrix, is related to mouse sperm protein sp56 and the complement component 4-binding proteins. J Biol Chem 272:12714–12722.
  • Franken, D. R., Henkel, R., Kaskar, K. and Habenicht, U. F. (1996) Defining bioassay conditions to evaluate sperm/zona interaction: inhibition of zona binding mediated by solubilized human zona pellucida. J Assist Reprod Genet 13:329–332.
  • Gupta, S. K., Chakravarty, S., Suraj, K., Bansal, P., Ganguly, A., Jain, M. K. and Bhandari, B. (2007) Structural and functional attributes of zona pellucida glycoproteins. Soc Reprod Fertil Suppl 63:203–216.
  • Hanfland, P., Kordowicz, M., Peter-Katalinic, J., Egge, H., Dabrowski, J. and Dabrowski, U. (1988) Structure elucidation of blood group B-like and I-active ceramide eicosa- and pentacosasaccharides from rabbit erythrocyte membranes by combined gas chromatography-mass spectrometry; electron-impact and fast-atom-bombardment mass spectrometry; and two-dimensional correlated, relayed-coherence transfer, and nuclear Overhauser effect 500-MHz 1H-n.m.r. spectroscopy. Carbohydr Res 178:1–21.
  • Harris, J. D., Hibler, D. W., Fontenot, G. K., Hsu, K. T., Yurewicz, E. C. and Sacco, A. G. (1994) Cloning and characterization of zona pellucida genes and cDNAs from a variety of mammalian species: the ZPA, ZPB and ZPC gene families. DNA Seq 4:361–393.
  • Hedrick, J. L. (2008) Anuran and pig egg zona pellucida glycoproteins in fertilization and early development. Int J Dev Biol 52:683–701.
  • Hirano, T., Takasaki, S., Hedrick, J. L., Wardrip, N. J., Amano, J. and Kobata, A. (1993) O-linked neutral sugar chains of porcine zona pellucida glycoproteins. Eur J Biochem 214:763–769.
  • Hokke, C. H., Damm, J. B., Kamerling, J. P. and Vliegenthart, J. F. (1993) Structure of three acidic O-linked carbohydrate chains of porcine zona pellucida glycoproteins. FEBS Lett 329:29–34.
  • Hokke, C. H., Damm, J. B., Penninkhof, B., Aitken, R. J., Kamerling, J. P. and Vliegenthart, J. F. (1994) Structure of the O-linked carbohydrate chains of porcine zona pellucida glycoproteins. Eur J Biochem 221:491–512.
  • Hoodbhoy, T., Joshi, S., Boja, E. S., Williams, S. A., Stanley, P. and Dean, J. (2005) Human sperm do not bind to rat zonae pellucidae despite the presence of four homologous glycoproteins. J Biol Chem 280:12721–12731.
  • Hughes, D. C. and Barratt, C. L. (1999) Identification of the true human orthologue of the mouse Zp1 gene: evidence for greater complexity in the mammalian zona pellucida? Biochim Biophys Acta 1447:303–306.
  • Johnston, D. S., Wright, W. W., Shaper, J. H., Hokke, C. H., Van den Eijnden, D. H. and Joziasse, D. H. (1998) Murine sperm-zona binding, a fucosyl residue is required for a high affinity sperm-binding ligand. A second site on sperm binds a nonfucosylated, β-galactosyl-capped oligosaccharide. J Biol Chem 273:1888–1895.
  • Kanai, S., Yonezawa, N., Ishii, Y., Tanokura, M. and Nakano, M. (2007) Recombinant bovine zona pellucida glycoproteins ZP3 and ZP4 coexpressed in Sf9 cells form a sperm-binding active hetero-complex. Febs J 274:5390–5405.
  • Karre, K. (2002) NK cells, MHC class I molecules and the missing self. Scand J Immunol 55:221–228.
  • Katsumata, T., Noguchi, S., Yonezawa, N., Tanokura, M. and Nakano, M. (1996) Structural characterization of the N-linked carbohydrate chains of the zona pellucida glycoproteins from bovine ovarian and fertilized eggs. Eur J Biochem 240:448–453.
  • Kerr, C. L., Hanna, W. F., Shaper, J. H. and Wright, W. W. (2004) Lewis X-containing glycans are specific and potent competitive inhibitors of the binding of ZP3 to complementary sites on capacitated, acrosome-intact mouse sperm. Biol Reprod 71:770–777.
  • Kinloch, R. A., Mortillo, S., Stewart, C. L. and Wassarman, P. M. (1991) Embryonal carcinoma cells transfected with ZP3 genes differentially glycosylate similar polypeptides and secrete active mouse sperm receptor. J Cell Biol 115:655–664.
  • Kinloch, R. A., Roller, R. J., Fimiani, C. M., Wassarman, D. A. and Wassarman, P. M. (1988) Primary structure of the mouse sperm receptor polypeptide determined by genomic cloning. Proc Natl Acad Sci USA 85:6409–6413.
  • Kudo, K., Yonezawa, N., Katsumata, T., Aoki, H. and Nakano, M. (1998) Localization of carbohydrate chains of pig sperm ligand in the glycoprotein ZPB of egg zona pellucida. Eur J Biochem 252:492–499.
  • Lefievre, L., Conner, S. J., Salpekar, A., Olufowobi, O., Ashton, P., Pavlovic, B., et al. (2004) Four zona pellucida glycoproteins are expressed in the human. Hum Reprod 19:1580–1586.
  • Li, D., Cao, S. and Xu, C. (2007) Polypeptide backbone derived from carboxyl terminal of mouse ZP3 inhibits sperm-zona binding. Mol Reprod Dev 74:1327–1336.
  • Liang, L. F., Chamow, S. M. and Dean, J. (1990) Oocyte-specific expression of mouse Zp-2: developmental regulation of the zona pellucida genes. Mol Cell Biol 10:1507–1515.
  • Liang, L. F. and Dean, J. (1993) Conservation of mammalian secondary sperm receptor genes enables the promoter of the human gene to function in mouse oocytes. Dev Biol 156:399–408.
  • Lin, Y. N., Roy, A., Yan, W., Burns, K. H. and Matzuk, M. M. (2007) Loss of zona pellucida binding proteins in the acrosomal matrix disrupts acrosome biogenesis and sperm morphogenesis. Mol Cell Biol 27:6794–6805.
  • Litscher, E. S., Juntunen, K., Seppo, A., Penttila, L., Niemela, R., Renkonen, O. and Wassarman, P. M. (1995) Oligosaccharide constructs with defined structures that inhibit binding of mouse sperm to unfertilized eggs in vitro. Biochemistry 34:4662–4669.
  • Litscher, E. S. and Wassarman, P. M. (1996) Characterization of mouse ZP3-derived glycopeptide, gp55, that exhibits sperm receptor and acrosome reaction-inducing activity in vitro. Biochemistry 35:3980–3985.
  • Liu, C., Litscher, E. S., Mortillo, S., Sakai, Y., Kinloch, R. A., Stewart, C. L. and Wassarman, P.M. (1996) Targeted disruption of the mZP3 gene results in production of eggs lacking a zona pellucida and infertility in female mice. Proc Natl Acad Sci USA 93:5431–5436.
  • Liu, D. Y., Baker, H. W., Pearse, M. J. and d'Apice, A. J. (1997) Normal sperm-zona pellucida interaction and fertilization in vitro in α1–3-galactosyltransferase gene knockout mice. Mol Hum Reprod 3:1015–1016.
  • Lopez, L. C., Bayna, E. M., Litoff, D., Shaper, N. L., Shaper, J. H. and Shur, B. D. (1985) Receptor function of mouse sperm surface galactosyltransferase during fertilization. J Cell Biol 101:1501–1510.
  • Lu, Q. and Shur, B. D. (1997) Sperm from β1,4-galactosyltransferase-null mice are refractory to ZP3-induced acrosome reactions and penetrate the zona pellucida poorly. Development 124:4121–4131.
  • Mengerink, K. J. and Vacquier, V. D. (2001) Glycobiology of sperm-egg interactions in deuterostomes. Glycobiology 11:37R–43R.
  • Miller, D. J., Macek, M. B. and Shur, B. D. (1992) Complementarity between sperm surface β-1,4-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding. Nature 357:589–593.
  • Monne, M., Han, L., Schwend, T., Burendahl, S. and Jovine, L. (2008) Crystal structure of the ZP-N domain of ZP3 reveals the core fold of animal egg coats. Nature 456:653–657.
  • Mori, E., Hedrick, J. L., Wardrip, N. J., Mori, T. and Takasaki, S. (1998) Occurrence of reducing terminal N-acetylglucosamine 3-sulfate and fucosylated outer chains in acidic N-glycans of porcine zona pellucida glycoproteins. Glycoconj J 15:447–456.
  • Mori, E., Mori, T. and Takasaki, S. (1997) Binding of mouse sperm to β-galactose residues on egg zona pellucida and asialofetuin-coupled beads. Biochem Biophys Res Commun 238:95–99.
  • Mori, E., Takasaki, S., Hedrick, J. L., Wardrip, N. J., Mori, T. and Kobata, A. (1991) Neutral oligosaccharide structures linked to asparagines of porcine zona pellucida glycoproteins. Biochemistry 30:2078–2087.
  • Morris, H. R., Dell, A., Easton, R. L., Panico, M., Koistinen, H., Koistinen, R., et al. (1996) Gender-specific glycosylation of human glycodelin affects its contraceptive activity. J Biol Chem 271:32159–32167.
  • Nakano, M., Yonezawa, N., Hatanaka, Y. and Noguchi, S. (1996) Structure and function of the N-linked carbohydrate chains of pig zona pellucida glycoproteins. J Reprod Fertil Suppl 50:25–34.
  • Nixon, B., Asquith, K. L. and Aitken, R. J. (2005) The role of molecular chaperones in mouse sperm-egg interactions. Mol Cell Endocrinol 240:1–10.
  • Nixon, B., Bielanowicz, A., McLaughlin, E. A., Tanphaichitr, N., Ensslin, M. A. and Aitken, R. J. (2009) Composition and significance of detergent resistant membranes in mouse spermatozoa. J Cell Physiol 218:122–134.
  • Noguchi, S., Hatanaka, Y., Tobita, T. and Nakano, M. (1992) Structural analysis of the N-linked carbohydrate chains of the 55-kDa glycoprotein family (pZP3) from porcine zona pellucida. Eur J Biochem 207:1130.
  • Noguchi, S. and Nakano, M. (1992) Structure of the acidic N-linked carbohydrate chains of the 55-kDa glycoprotein family (PZP3) from porcine zona pellucida. Eur J Biochem 209:883–894.
  • Noguchi, S. and Nakano, M. (1993) Structural characterization of the N-linked carbohydrate chains from mouse zona pellucida glycoproteins ZP2 and ZP3. Biochim Biophys Acta 1158:217–226.
  • Noguchi, S., Yonezawa, N., Katsumata, T., Hashizume, K., Kuwayama, M., Hamano, S., et al. (1994) Characterization of the zona pellucida glycoproteins from bovine ovarian and fertilized eggs. Biochim Biophys Acta 1201:7–14.
  • Oehninger, S., Acosta, A. and Hodgen, G. D. (1990) Antagonistic and agonistic properties of saccharide moieties in the hemizona assay. Fertil Steril 53:143–149.
  • Oehninger, S., Coddington, C. C., Hodgen, G. D. and Seppala, M. (1995) Factors affecting fertilization: endometrial placental protein 14 reduces the capacity of human spermatozoa to bind to the human zona pellucida. Fertil Steril 63:377–383.
  • Overstreet, J. W. and Hembree, W. C. (1976) Penetration of the zona pellucida of nonliving human oocytes by human spermatozoa in vitro. Fertil Steril 27:815–831.
  • Ozgur, K., Patankar, M. S., Oehninger, S. and Clark, G. F. (1998) Direct evidence for the involvement of carbohydrate sequences in human sperm-zona pellucida binding. Mol Hum Reprod 4:318–324.
  • Pang, P. C., Tissot, B., Drobnis, E. Z., Sutovsky, P., Morris, H. R., Clark, G. F. and Dell, A. (2007) Expression of bisecting type and Lewisx/Lewisy terminated N-glycans on human sperm. J Biol Chem 282:36593–36602.
  • Patankar, M. S., Oehninger, S., Barnett, T., Williams, R. L. and Clark, G. F. (1993) A revised structure for fucoidan may explain some of its biological activities. J Biol Chem 268:21770–21776.
  • Patankar, M. S., Ozgur, K., Oehninger, S., Dell, A., Morris, H., Seppala, M. and Clark, G. F. (1997) Expression of glycans linked to natural killer cell inhibition on the human zona pellucida. Mol Hum Reprod 3:501–505.
  • Rankin, T., Familari, M., Lee, E., Ginsberg, A., Dwyer, N., Blanchette-Mackie, J., et al. (1996) Mice homozygous for an insertional mutation in the ZP3 gene lack a zona pellucida and are infertile. Development 122:2903–2910.
  • Rankin, T., Talbot, P., Lee, E. and Dean, J. (1999) Abnormal zonae pellucidae in mice lacking ZP1 result in early embryonic loss. Development 126:3847–3855.
  • Rankin, T. L., Coleman, J. S., Epifano, O., Hoodbhoy, T., Turner, S. G., Castle, P. E., et al. (2003) Fertility and taxon-specific sperm binding persist after replacement of mouse sperm receptors with human homologs. Dev Cell 5:33–43.
  • Rankin, T. L., Tong, Z. B., Castle, P. E., Lee, E., Gore-Langton, R., Nelson, L. M. and Dean, J. (1998) Human ZP3 restores fertility in ZP3 null mice without affecting order-specific sperm binding. Development 125:2415–2424.
  • Sacco, A. G., Yurewicz, E. C., Subramanian, M. G. and Matzat, P. D. (1989) Porcine zona pellucida: association of sperm receptor activity with the α-glycoprotein component of the Mr=55,000 family. Biol Reprod 41:523–532.
  • Sandow, B. A. and Clark, G. F. (1993) Terminal α-galactose sequences contribute to mouse sperm binding in a cell adhesion model. Biol. Reprod 48:A166.
  • Shi, S., Williams, S. A., Seppo, A., Kurniawan, H., Chen, W., Ye, Z., et al. (2004) Inactivation of the Mgat1 gene in oocytes impairs oogenesis, but embryos lacking complex and hybrid N-glycans develop and implant. Mol Cell Biol 24:9920–9929.
  • Shur, B. D. (2008) Reassessing the role of protein-carbohydrate complementarity during sperm-egg interactions in the mouse. Int J Dev Biol 52:703–715.
  • Sutton-Smith, M., Wong, N. K., Khoo, K. H., Wu, S. W., Yu, S. Y., Patankar, M. S., et al. (2007) Analysis of protein-linked glycosylation in a sperm-somatic cell adhesion system. Glycobiology 17:553–567.
  • Taya, T., Yamasaki, N., Tsubamoto, H., Hasegawa, A. and Koyama, K. (1995) Cloning of a cDNA coding for porcine zona pellucida glycoprotein ZP1 and its genomic organization. Biochem Biophys Res Commun 207:790–799.
  • Thaler, C. D. and Cardullo, R. A. (1996) The initial molecular interaction between mouse sperm and the zona pellucida is a complex binding event. J Biol Chem 271:23289–23297.
  • Thall, A. D., Maly, P. and Lowe, J. B. (1995) Oocyte Galα1–3Gal epitopes implicated in sperm adhesion to the zona pellucida glycoprotein ZP3 are not required for fertilization in the mouse. J Biol Chem 270:21437–21440.
  • Topfer-Petersen, E., Ekhlasi-Hundrieser, M. and Tsolova, M. (2008) Glycobiology of fertilization in the pig. Int J Dev Biol 52:717–736.
  • van Duin, M., Polman, J., De Breet, I. T., van Ginneken, K., Bunschoten, H., Grootenhuis, A., et al. (1994) Recombinant human zona pellucida protein ZP3 produced by Chinese hamster ovary cells induces the human sperm acrosome reaction and promotes sperm–egg interaction. Biol Reprod 51:607–617.
  • van Gestel, R. A., Brewis, I. A., Ashton, P. R., Brouwers, J. F. and Gadella, B. M. (2007) Multiple proteins present in purified porcine sperm apical plasma membranes interact with the zona pellucida of the oocyte. Mol Hum Reprod 13:445–454.
  • Varki, A. (1993) Biological roles of oligosaccharides: all of the theories are correct. Glycobiology 3:97–130.
  • von Witzendorff, D., Ekhlasi-Hundrieser, M., Dostalova, Z., Resch, M., Rath, D., Michelmann, H. W. and Topfer-Petersen, E. (2005) Analysis of N-linked glycans of porcine zona pellucida glycoprotein ZPA by MALDI-TOF MS: a contribution to understanding zona pellucida structure. Glycobiology 15:475–488.
  • Wassarman, P. M. (1990) Profile of a mammalian sperm receptor. Development 108:1–17.
  • Wassarman, P. M. and Litscher, E. S. (2008) Mammalian fertilization: the egg's multifunctional zona pellucida. Int J Dev Biol 52:665–676.
  • Wassarman, P. M., Qi, H. and Litscher, E. S. (1997) Mutant female mice carrying a single mZP3 allele produce eggs with a thin zona pellucida, but reproduce normally. Proc Roy Soc London B 264:323–328.
  • Williams, S. A. and Stanley, P. (2008) Mouse fertility is enhanced by oocyte-specific loss of core 1-derived O-glycans. Faseb J 22:2273–2284.
  • Williams, S. A., Xia, L., Cummings, R. D., McEver, R. P. and Stanley, P. (2007) Fertilization in mouse does not require terminal galactose or N-acetylglucosamine on the zona pellucida glycans. J Cell Sci 120:1341–1349.
  • Yamagata, T. (1985) The role of saccharides in fertilization in the mouse. Dev Growth Differ 27:176–177.
  • Yamagata, T., Ito, M. and Takahashi, K. (1983) The involvement of a saccharide-mediated recognition mechanism in the interactions between sperm and the zona pellucida of the egg cells of the mouse. In Glycoconjugates. eds Chester, M. A., Heinegard, A., Svensson, S., Rhams, New York, NY pp. 623–624.
  • Yao, Y. Q., Chiu, C. N., Ip, S. M., Ho, P. C. and Yeung, W. S. (1998) Glycoproteins present in human follicular fluid that inhibit the zona-binding capacity of spermatozoa. Hum Reprod 13:2541–2547.
  • Yonezawa, N., Amari, S., Takahashi, K., Ikeda, K., Imai, F.L., Kanai, S., et al. (2005) Participation of the nonreducing terminal β-galactosyl residues of the neutral N-linked carbohydrate chains of porcine zona pellucida glycoproteins in sperm-egg binding. Mol Reprod Dev 70:222–227.
  • Yonezawa, N., Fukui, N., Kuno, M., Shinoda, M., Goko, S., Mitsui, S. and Nakano, M. (2001) Molecular cloning of bovine zona pellucida glycoproteins ZPA and ZPB and analysis for sperm-binding component of the zona. Eur J Biochem 268:3587–3594.
  • Yonezawa, N., Kanai, S. and Nakano, M. (2007) Structural significance of N-glycans of the zona pellucida on species-selective recognition of spermatozoa between pig and cattle. Soc Reprod Fertil Suppl 63:217–228.
  • Yonezawa, N., Kudo, K., Terauchi, H., Kanai, S., Yoda, N., Tanokura, M., et al. (2005) Recombinant porcine zona pellucida glycoproteins expressed in Sf9 cells bind to bovine sperm but not to porcine sperm. J Biol Chem 280:20189–20196.
  • Yoshimura, M., Ihara, Y., Ohnishi, A., Ijuhin, N., Nishiura, T., Kanakura, Y., et al. (1996) Bisecting N-acetylglucosamine on K562 cells suppresses natural killer cytotoxicity and promotes spleen colonization. Cancer Res 56:412–418.
  • Yu, Y., Xu, W., Yi, Y. J., Sutovsky, P. and Oko, R. (2006) The extracellular protein coat of the inner acrosomal membrane is involved in zona pellucida binding and penetration during fertilization: characterization of its most prominent polypeptide (IAM38). Dev Biol 290: 32–43.
  • Yurewicz, E. C., Hibler, D., Fontenot, G. K., Sacco, A. G. and Harris, J. (1993) Nucleotide sequence of cDNA encoding ZP3α, a sperm-binding glycoprotein from zona pellucida of pig oocyte. Biochim Biophys Acta 1174:211–214.
  • Yurewicz, E. C., Pack, B. A. and Sacco, A. G. (1991) Isolation, composition, and biological activity of sugar chains of porcine oocyte zona pellucida 55K glycoproteins. Mol Reprod Dev 30:126–134.
  • Yurewicz, E. C., Sacco, A. G. and Subramanian, M. G. (1987) Structural characterization of the Mr=55,000 antigen (ZP3) of porcine oocyte zona pellucida. Purification and characterization of α- and β-glycoproteins following digestion of lactosaminoglycan with endo-β-galactosidase. J Biol Chem 262:564–571.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.