Human Sperm-Oocyte Recognition and Infertility

ABSTRACT

The incidence of infertility related to both male and female factors continues to rise despite many advances in reproductive technologies. Some abnormalities in human gamete interaction have been shown to be due to defects in the sperm, and others have been attributed to defects in the zona pellucida (ZP). Our lack of understanding of molecular mechanisms involved in the interaction of human sperm with the ZP in fertile as compared with infertile females and males has been limited because of the unavailability of human oocytes and ethical restraints on experimental studies. It is becoming increasingly apparent that improved clinical assays are necessary for evaluating sperm-ZP interaction in order to assess the optimal procedures for successful fertilization and pregnancy. With advances in molecular biology, the genes encoding the three major human ZP proteins have been identified and complementary DNAs are available to begin to better evaluate the molecular basis of sperm-ZP interaction.

KEYWORD

Pellucida - infertility - fertilization

REFERENCES

• 1 Clark G F, Patankar M S, Hinsch K D, Oehninger S. New concepts in human sperm-zona pellucida interaction.  Hum Reprod . 1995;  10 31-37
• 2 Liu D Y, Clarke G N, Lopata A, Jonston W I, Baker H W. A sperm-zona pellucida binding test and in vitro fertilization.  Fertil Steril . 1989;  52 281-287
• 3 Liu D Y, Baker H W. Relationship between the zona pellucida (ZP) and ionophore A23187-induced acrosome reaction and the ability of sperm to penetrate the ZP in men with normal sperm-ZP binding.  Fertil Steril . 1996;  66 312-315
• 4 Liu D Y, Baker H W. Disordered acrosome reaction of spermatozoa bound to the zona pellucida: a newly discovered sperm defect causing infertility with reduced sperm-zona pellucida penetration and reduced fertilization in vitro.  Hum Reprod . 1994;  9 1694-1700
• 5 Calvo L, Dennison-Lagos L, Banks S M. Acrosome reaction inducibility predicts fertilization success at in-vitro fertilization.  Hum Reprod . 1994;  9 1880-1886
• 6 Coetzee K, Olmedo J, Lombard C J. Induced acrosome reactions as fertility predictor.  J Assist Reprod Genet . 1994;  11 470-473
• 7 de Kretser M D. The potential of intracytoplasmic sperm injection (ICSI) to transmit genetic defects causing male infertility.  Reprod Fertil Dev . 1995;  7 137-141
• 8 Martin R H. The risk of chromosomal abnormalities following ICSI.  Hum Reprod . 1996;  11 924-925
• 9 Tesarik J, Mendoza C. Genomic imprinting abnormalities: a new potential risk of assisted reproduction.  Mol Hum Reprod . 1996;  2 295-298
• 10 Benoff S. Human sperm-zona interaction. Investigations into the molecular basis of human sperm-egg interactions: what's next?.  Mol Hum Reprod . 1998;  4 925-928
• 11 Cooke H J, Hargreave T, Elliot D J. Understanding the genes involved in spermatogenesis: a progress report.  Fertil Steril . 1998;  69 989-995
• 12 Bedford J M, Kim H H. Sperm/egg binding patterns and oocyte cytology in retrospective analysis of fertilization failure in vitro.  Hum Reprod . 1993;  8 453-463
• 13 Van Blerkom J, Davis P W, Merriam J. A retrospective analysis of unfertilized and presumed parthenogentically activated human oocytes demonstrates a high frequency of sperm penetration.  Hum Reprod . 1994;  9 2381-2388
• 14 Windt M L, Franken D R, Kruger T F, Oehninger S C. In vitro fertilization failure: identification of gamete defects by investigation of sperm-zona pellucida binding capacity of unfertilized oocytes.  Andrologia . 1996;  28 211-215
• 15 Shivers C A, Dunbar B S. Autoantibodies to zona pellucida: a possible cause of infertility in women.  Science . 1977;  197 1082-1084
• 16 Caudle M R, Shivers C A, Wild R A. Clinical significance of naturally occurring anti-zona pellucida antibodies in infertile women.  Am J Reprod Immunol Microbiol . 1987;  15 119-121
• 17 Ezra Y, Simon A, Laufer N. Defective oocytes: a new subgroup of unexplained infertility.  Fertil Steril . 1992;  58 24-27
• 18 Oehninger S, Veeck L L, Lanzendorf S, Maloney M, Toner J, Muasher S. Intracytoplasmic sperm injection: achievement of high pregnancy rates in couples with severe male factor infertility is dependent primarily upon female and not male factors.  Fertil Steril . 1995;  64 977-981
• 19 Ducibella T, Dubey A, Gross V. Zona biochemical change and spontaneous cortical granule loss in eggs that fail to fertilize in in vitro fertilization.  Fertil Steril . 1995;  64 1154-1161
• 20 Oehninger S, Hinsch E, Pfisterer S. Use of a specific zona pellucida (ZP) protein 3 antiserum as a clinical marker for human ZP integrity and function.  Fertil Steril . 1996;  65 139-145
• 21 Kamada M, Yamamoto S, Takikawa M. Identification of human sperm protein that interacts with sperm-immobilizing antibodies in the sera of infertile women.  Fertil Steril . 1999;  72 691-695
• 22 Yanagimachi R. Mammalian fertilization In: Knobil E, Neill JD, eds. The Physiology of Reproduction.  New York: Raven Press 1994: 189-317
• 23 Liu D Y, Baker H WG. Defective sperm-zona pellucida interaction: a major cause of failure of fertilization in clinical in-vitro fertilization.  Hum Reprod . 2000;  15 702-708
• 24 Oehninger S, Acosta A, Veeck L. Recurrent failure of in vitro fertilization: role of the hemizona assay in the sequential diagnosis of specific sperm-oocyte defects.  Am J Obstet Gynecol . 1991;  164 1210-1215
• 25 Franken D R, Kruger T F, Lombard C, Oehninger S C, Acosta A A, Hodgen G D. The ability of hemizona assay to predict human fertilization in vitro in different IVF/GIFT cycles.  Hum Reprod . 1993;  8 1240-1244
• 26 Liu Y, Bourne H, Baker H WG. High fertilization and pregnancy rates after intracytoplasmic sperm injection in patients with disordered zona pellucida-induced acrosome reaction.  Fertil Steril . 1997;  67 955-958
• 27 Dunbar B S. Morphological, Biochemical and immunochemical characterization of the mammalian zonae pellucidae. In: Hartmann J, ed. Mechanisms and Control of Animal Fertilization New York: Academic Press 1983: 140-167
• 28 Wassarman P M. Zona pellucida glycoproteins.  Annu Rev Biochem . 1988;  57 415-442
• 29 Dunbar B S, Prasad S V, Timmons T. Comparative structure and function of the mammalian zonae pellucidae. In: Dunbar BS, O'Rand MG, eds. A Comparative Overview of Mammalian Fertilization New York: Plenum Press 1991: 97-116
• 30 Dunbar B S, Avery S, Lee V. The mammalian zona pellucida: its biochemistry, immunochemistry, molecular biology and developmental expression.  Reprod Fertil Dev . 1994;  6 59-76
• 31 Epifano O, Dean J. Biology and structure of the zona pellucida: a target for immunocontraception.  Reprod Fertil Dev . 1994;  6 319-330
• 32 Prasad S V, Wilkins B, Dunbar B S. Molecular biology approaches to evaluate species variation in immunogenicity and antigenicity of zona pellucida proteins.  J Reprod Fertil . 1996;  50(Suppl) 143-149
• 33 McLeskey S B, Dowds C, Carballada R, White R R, Saling P M. Molecules involved in mammalian sperm-egg interaction.  Int Rev Cytol . 1998;  177 57-113
• 34 Prasad S V, Skinner S M, Cariño C, Wang N, Cartwright J, Dunbar B S. Structure and function of the proteins of the mammalian zona pelllucida.  Cells Tissues Organs . 2000;  166 148-164
• 35 Bork P, Sander C. A large domain common to sperm receptors (ZP2 and ZP3) and TGF-β type III receptor.  Fed Eur Biochem Soc . 1992;  300 237-240
• 36 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;  95 317-324
• 37 Yurewicz E C, Pack B A, Armant D R, Sacco A G. Porcine zona pellucida ZP3a glycoprotein mediates binding of the biotin-labeled M_r 55,000 family (ZP3) to boar sperm membrane vesicles.  Mol Reprod Dev . 1993;  36 382-389
• 38 Yurewicz E C, Sacco A G, Gupta S K, Xu N, Gage D A. 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
• 39 Yamasaki N, Richardson R T, O'Rand M G. Expression of the rabbit sperm protein Sp17 in COS cells and interaction of recombinant Sp17 with the rabbit zona pellucida.  Mol Reprod Dev . 1995;  40 48-55
• 40 Prasad S V, Wilkins B, Skinner S M, Dunbar B S. Evaluating zona pellucida structure and function using antibodies to 55kDa ZP protein expressed in baculovirus expression system.  Mol Reprod Dev . 1996;  43 519-529
• 41 Gupta S K, Chadha K, Harris J D. Mapping of epitopes on porcine zona pellucida-3a by monoclonal antibodies inhibiting oocyte-sperm interaction.  Biol Reprod . 1996;  55 410-415
• 42 Greve J, Wassarman P. Mouse extracellular coat is a matrix of interconnected filaments possessing a structural repeat.  J Mol Biol . 1985;  181 253-266
• 43 Hughes D C, Barratt C LR. Identification of the true human orthologue of the mouse ZP1 gene: evidence for greater complexity in the mammalian zona pellucida?.  Biochim Biophys Acta . 1999;  1447 303-306
• 44 Morales P, Vigil P, Franken D R, Kaskar K, Coetzee K, Kruger T F. Sperm-oocyte interaction: studies on the kinetics of zona pellucida binding and acrosome reaction of human spermatozoa.  Andrologia . 1994;  26 131-137
• 45 Fraser L R. Cellular biology of capacitation and the acrosome reaction.  Hum Reprod . 1995;  10 22-30
• 46 Franken D R, Bastiaan H S, Kidson A, Wranz P, Habenicht U-F. Zona pellucida mediated acrosome reaction and sperm morphology.  Andrologia . 1997;  29 311-317
• 47 Henkel R, Franken D R, Habenicht U-F. Zona pellucida as physiological trigger for the induction of acrosome reaction.  Andrologia . 1998;  30 275-280
• 48 van Duin M, Polman J, De Breet I. 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 . 1994;  51 607-617
• 49 Chapman N R, Kessopoulou E, Andrews P D, Hornby D P, Barratt L R. The polypeptide backbone of recombinant human zona pellucida glycoprotein-3 initiates acrosomal exocytosis in human spermatozoa in vitro.  Biochem J . 1998;  330 839-845
• 50 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
• 51 Govind C K, Hasegawa A, Koyama K, Gupta S K. Delineation of a conserved B cell epitope on bonnet monkey (Macaca radiata) and human zona pellucida glycoprotein-B by monoclonal antibodies demonstrating inhibition of sperm-egg binding.  Biol Reprod . 2000;  62 67-75
• 52 VandeVoort C A, Schwoebel E D, Dunbar B S. Immunization of monkeys with recombinant cDNA expressed zona pellucida proteins.  Fertil Steril . 1995;  64 838-847
• 53 Hartman J. Mammalian fertilization: gamete surface interactions in vitro In: Hartman J, ed. Mechanism and Control of Animal Fertilization.  New York: Academic Press 1983: 325-359
• 54 Snell W J, White J M. The molecules of mammalian fertilization.  Cell . 1996;  85 629-637
• 55 Benoff S. Carbohydrates and fertilization: an overview.  Mol Hum Reprod . 1997;  3 599-637
• 56 Sinowatz F, Plendl J, Kolle S. Protein-carbohydrate interactions during fertilization.  Acta Anat . 1998;  161 196-205
• 57 Brewis I A, Wong C H. Gamete recognition: sperm proteins that interact with the egg zona pellucida.  Rev Reprod . 1999;  4 135-142
• 58 Dell A, Morris H R, Easton R L, Patankar M, Clark G F. The glycobiology of gametes and fertilization.  Biochim Biophys Acta . 1999;  1473 196-205
• 59 Oehninger S, Acosta A, Hodgen G D. Antagonistic and agonistic properties of saccharide moieties in the hemizona assay.  Fertil Steril . 1990;  53 143-149
• 60 Tesarik J, Mendoza C, Ramirez J P, Moos J. Solubilized human zona pellucida competes with a fucosylated neoglycoprotein for binding sites on the human sperm surface.  Fertil Steril . 1993;  60 344-350
• 61 Oehninger S, Patankar M, Seppala M, Clark G F. Involvement of selectin-like carbohydrate binding specificity in gamete interaction.  Andrologia . 1998;  30 269-274
• 62 Tulsiani D R, Skudlarek M D, Orgebin-Crist M C. Human sperm plasma membranes possess alpha-D-mannosidase activity but no galactosyltransferase activity.  Biol Reprod . 1990;  42 843-858
• 63 Benoff S, Cooper G W, Hurley I. Human sperm fertilizing potential in vitro is correlated with differential expression of a head-specific mannose-ligand receptor.  Fertil Steril . 1993;  59 854-862
• 64 Benoff S, Barcia M, Hurley I R. Classification of male factor infertility relevant to in-vitro fertilization insemination strategies using mannose ligands, acrosome status and anti-cytoskeletal antibodies.  Hum Reprod . 1996;  11 1905-1918
• 65 Goluboff E T, Mertz J R, Tres L L, Kierszenbaum A L. Galactosyl receptor in human testis and sperm is antigenically related to the minor C-type (Ca²⁺-dependent) lectin variant of human and rat liver.  Mol Reprod Dev . 1995;  40 460-466
• 66 Lassalle B, Testart J. Human zona pellucida recognition associated with removal of sialic acid from human sperm surface.  J Reprod Fertil . 1994;  101 703-711
• 67 Ozgur K, Patankar M S, Oehninger S, Clark G F. Direct evidence for the involvement of carbohydrate sequences in human sperm-zona pellucida binding.  Mol Hum Reprod . 1998;  4 318-324
• 68 Banerjee M, Chowdhury M. Localization of a 25 kDa human sperm surface protein: its role in in-vitro human sperm capacitation.  Mol Hum Reprod . 1997;  3 109-114
• 69 Burks D J, Carballada R, Moore H D, Saling P M. Interaction of a tyrosine kinase from human sperm with the zona pellucida at fertilization.  Science . 1995;  269 83-86
• 70 Naz R K, Ahmed K. Molecular identities of human sperm proteins that bind human zona pellucida: nature of sperm-zona interaction, tyrosine kinase activity, and involvement of FA-1.  Mol Reprod Dev . 1994;  39 397-408
• 71 Naz R K, Zhu X, Kadam A L. Identification of human sperm peptide sequence involved in egg binding for immunocontraception.  Biol Reprod . 2000;  62 318-324
• 72 Kopf G S, Gerton G L. The mammalian sperm acrosome and the acrosome reaction. In: Wassarman P, ed. Elements of Mammalian Fertilization 1 Boca Raton, FL: CRC Press 1991: 153-206
• 73 Zaneveld L JD, De Jonge J C, Anderson R A, Mack S R. Human sperm capacitation and the acrosome reaction.  Hum Reprod . 1991;  6 1265-1274
• 74 Cross N L, Morales P, Overstreet J W, Hanson F W. Induction of the acrosome reaction by the human zona pellucida.  Biol Reprod . 1988;  38 235-244
• 75 Sueldo C E, Oehninger S C, Subias E. Effect of progesterone on human zona pellucida sperm binding and oocyte penetrating capacity.  Fertil Steril . 1993;  60 137-140
• 76 Meizel S, Turner K O, Nuccitelli R. Progesterone triggers a wave of increased free calcium during the human sperm acrosome reaction.  Dev Biol . 1997;  182 67-75
• 77 Revelli A, Modotti M, Piffaretti-Yanez A, Massobrio M, Balerna M. Steroid receptors in human spermatozoa.  Hum Reprod . 1994;  9 760-766
• 78 Falkenstein E, Heck M, Gerdes D. Specific progesterone binding to a membrane protein and related nongenomic effects on Ca²⁺-fluxes in sperm.  Endocrinology . 1999;  140 5999-6002
• 79 Tesarik J, Carreras A, Mendoza C. Differential sensitivity of progesterone- and zona pellucida-induced acrosome reactions to pertussis toxin.  Mol Reprod Dev . 1993;  34 183-189
• 80 Jacob A, Hurley I, Mandel F S, Hershlag A, Cooper G W, Benoff S. Human sperm non-nuclear progesterone receptor expression is a novel marker for fertilization outcome.  Mol Hum Reprod . 1998;  4 533-542
• 81 Baldi E, Luconi M, Muratori M, Forti G. A novel functional estrogen receptor on human sperm membrane interferes with progesterone effects.  Mol Cell Endocrinol . 2000;  161 31-35
• 82 Breitbart H, Spungin B. The biochemistry of the acrosome reaction.  Mol Hum Reprod . 1997;  3 195-202
• 83 Brewis I A, Moore H DM. Molecular mechanisms of gamete recognition and fusion at fertilization.  Hum Reprod . 1997;  12(Suppl 2) 156-165
• 84 Benoff S. Modelling human sperm-egg interaction in vitro: signal transduction pathways regulating the acrosome reaction.  Mol Hum Reprod . 1998;  4 453-471
• 85 Carrera A, Moos J, Ning X P. Regulation of protein tyrosine phosphorylation in human sperm by a calcium/calmodulin-dependent mechanism: identification of A kinase anchor proteins as major substrates for tyrosine phosphorylation.  Dev Biol . 1996;  180 284-296
• 86 Bastiaan H, Franken D, Wranz P. G-protein regulation of the solubilized human zona pellucida mediated acrosome reaction and zona pellucida binding.  J Assist Reprod Genet . 1999;  16 332-336
• 87 Bielfeld P, Faridi A, Zaneveld L J, De Jonge J C. The zona pellucida-induced acrosome reaction of human spermatozoa is mediated by protein kinases.  Fertil Steril . 1994;  61 536-541
• 88 Epifano O, Liang L, Familari M, Moos M C, Dean J. Coordinate expression of the three zona pellucida genes during mouse oogenesis.  Development . 1995;  121 1947-1956
• 89 Dunbar B S, Liu C, Sammons D W. Identification of the three major proteins of porcine and rabbit zonae pellucidae by two-dimensional gel electrophoresis: comparison with follicular fluid, sera and ovarian cell proteins.  Biol Reprod . 1981;  24 1111-1124
• 90 Schwoebel E, Prasad S, Timmons T. Isolation and characterization of a full length cDNA encoding the 55 kDa rabbit zona pellucida protein.  J Biol Chem . 1991;  266 7214-7219
• 91 Yurewicz E D, Sacco A G, Subramanian M G. Structural characterization of Mr = 55,000 antigen (ZP3) of porcine oocyte zona pellucida.  J Biol Chem . 1987;  262 564-571
• 92 Yurewicz E C, Hibler D, Fontenot G K, Sacco A G, Harris J. Nucleotide sequence of cDNA encoding ZP3a, a sperm-binding glycoprotein from zona pellucida of pig oocyte.  Biochim Biophys Acta . 1993;  1174 211-214
• 93 Gupta S K, Sharma M, Behera A K, Bisht R, Kaul R. Sequence of complementary deoxyribonucleic acid encoding bonnet monkey zona pellucida glycoprotein-ZP1 and its high level expression in Escherichia coli Biol Reprod .  1997;  57 532-538
• 94 Harris J D, Hibler D W, Fontenot G K, Hsu K T, Yurewicz E C, Sacco A G. Cloning and characterization of zona pellucida genes and cDNAs from a variety of mammalian species: the ZPA, ZPB and ZPC gene families.  DNA Sequence . 1994;  4 361-393
• 95 Moos J, Faundes D, Kopf G S, Shultz R M. Composition of the human zona pellucida and modifications following fertilization.  Mol Hum Reprod . 1995;  1 2467-2471
• 96 Gupta S K, Yurewicz E C, Sacco A G, Kaul R, Jethanandani P, Govind C K. Human zona pellucid glycoproteins: characterization using antibodies against recombinant non-human primate ZP1, ZP2 and ZP3.  Mol Hum Reprod . 1998;  4 1058-1064
• 97 Liang L, Chamow S, Dean J. Oocyte-specific expression of mouse ZP-2: developmental regulation of the zona pellucida genes.  Mol Cell Biol . 1990;  10 1507-1515
• 98 Lee V, Schwoebel E, Prasad S, Timmons T, Cook R, Dunbar B. Isolation and characterization of a cDNA encoding the rabbit 75-kDa zona pellucida protein.  J Biol Chem . 1993;  268 12412-12417
• 99 Dunbar B S, Wardrip N J, Hedrick J L. Isolation, physicochemical properties and macromolecular composition of the zona pellucida from porcine oocytes.  Biochemistry . 1980;  19 356-365
• 100 Taya T, Yamasaki N, Tsubamoto H, Hasegawa A, Koyama K. Cloning of a cDNA coding for the porcine zona pellucida glycoprotein ZP1 and its genomic organization.  Biochem Biophy Res Commun . 1995;  207 790-799
• 101 Jethanandani P, Santhanam R, Gupta S K. Molecular cloning and expression in Escherichia coli of cDNA encoding bonnet monkey (Macaca radiata) zona pellucida glycoprotein-ZP2.  Mol Reprod Dev . 1998;  50 229-239
• 102 Liang L, Dean J. Conservation of mammalian secondary sperm receptor genes enables the promoter of the human gene to function in mouse oocytes.  Dev Biol . 1993;  156 399-408
• 103 Ringuette M J, Chamberlin M, Baur A, Sobieski D, Dean J. Molecular analysis of cDNA coding for ZP3, a sperm binding protein of the mouse zona pellucida.  Dev Biol . 1988;  127 287-295
• 104 Chamberlin M E, Dean J. Human homolog of the mouse sperm receptor.  Proc Natl Acad Sci U S A . 1990;  87 6014-6018
• 105 Thillai-Koothan P, van Duin M, Aitken R J. Cloning, sequencing and oocyte specific expression of the marmoset sperm receptor protein ZP3.  Zygote . 1993;  1 93-101
• 106 Kolluri S, Kaul R, Banerjee K, Gupta S K. Nucleotide sequence of cDNA encoding bonnet monkey (Macaca radiata) zona pellucida glycoprotein-ZP3.  Reprod Fertil Dev . 1995;  7 1209-1212
• 107 Sacco A G, Yurewicz E C, Subramanian M G, Matzat P D. Porcine zona pellucida: association of sperm receptor activity with the α-glycoprotein component (ZP3α) of the Mr = 55,000 family (ZP3).  Biol Reprod . 1989;  41 523-532
• 108 Bleil J D, Greve J, Wassarman P M. 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 . 1988;  128 376-385
• 109 Tsubamoto H, Hasegawa A, Inoue M, Yamasaki N, Koyama K. Binding of recombinant pig zona pellucida protein 1 (ZP1) to acrosome -reacted spermatozoa.  J Reprod Fertil . 1996;  50(Suppl) 63-67
• 110 Kinloch R A, Mortillo S, Stewart C L, Wassarman P M. Embryonal carcinoma cells transfected with ZP3 genes differentially glycosylate similar polypeptides and secrete active mouse sperm receptor.  J Cell Biol . 1991;  115 655-664
• 111 Beebe S, Leyton L, Burks D. Recombinant mouse ZP3 inhibits sperm binding and induces the acrosome reaction.  Dev Biol . 1992;  151 48-54
• 112 Miller D J, Macek M B, Shur B D. Complementarity between sperm surface β-1,4-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding.  Nature . 1992;  357 589-593
• 113 Leyton L, Sailing P M. 95kDa sperm proteins bind ZP3 and serve as tyrosine kinase substrates in response to zona binding.  Cell . 1989;  57 1123-1130
• 114 Cheng A, Le T, Palacios M. Sperm-egg recognition in the mouse: characterization of sp56, a sperm protein having specific affinity for ZP3.  J Cell Biol . 1994;  125 867-878
• 115 Robinson R, Richardson R, Hinds K, Clayton D, Poirier G R. Features of a seminal plasma proteinase inhibitor-zona pellucida binding component on murine spermatozoa.  Gamete Res . 1987;  16 217-288
• 116 Tulsiani D R, Skudlarek M D, Orgebin-Crist M C. Novel alpha-D-mannosidase of rat sperm plasme membranes: characterization amd potential role in sperm-egg interactions.  J Cell Biol . 1989;  109 1257-1267
• 117 Tanphaichitr N, Tayabali A, Gradil C, Juneja S, Leveille M C, Lingwood C A. Role for a germ cell-specific sulfolipid-immobilizing protein (SLIP1) in mouse in vivo fertilization.  Mol Reprod Dev . 1992;  32 17-22
• 118 Thaler C D, Cardullo R A. Defining oligosaccharide specificity for the initial sperm-zona pellucida adhesion in the mouse.  Mol Reprod Dev . 1998;  45 535-546
• 119 Primakoff P, Cowan A, Hyatt H, Tredick-Kline J, Myles D G. Purification of the guinea pig sperm PH-20 antigen and detection of a site specific endoproteolytic cleavage activity in sperm preperations that cleaves PH-20 into two disulfide-linked fragments.  Biol Reprod . 1988;  38 921-934
• 120 Huang T TF, Ohzu E, Yanagimachi R. Evidence suggesting that L-fucose is part of the recognition signal for sperm-zona pellucida attachment in mammals.  Gamete Res . 1982;  5 355-361
• 121 Richardson R T, Yamasaki N, O'Rand M G. Sequence of a rabbit sperm zona pellucida binding protein and localization during the acrosome reaction.  Dev Biol . 1994;  165 688-701
• 122 O'Rand M G, Widgreen E E, Fisher S J. Characterization of the rabbit sperm membrane autoantigen, RSA, as a lectin-like zona binding protein.  Dev Biol . 1988;  129 231-240
• 123 Dostolova Z, Calvette J J, Sanz L, Topfer-Petersen E. Boar sperm adhesion AWN-1: oligosaccharide and zona pellucida binding characteristics.  Eur J Biochem . 1995;  230 329-336
• 124 Topfer-Petersen E, Romero A, Verela P F. Spermadhesins: a new protein family. Facts, hypotheses and perspectives.  Andrologia . 1998;  30 217-224
• 125 Peterson R N, Hunat W P. Identification, isolation and properties of a plasme membrane protein involved in the adhesion of boar sperm to the porcine zona pellucida.  Gamete Res . 1989;  23 103-118
• 126 Hardy D M, Garbers D L. A sperm membrane protein that binds in a species-specific manner to the egg extracellular matrix is homologous to von Willebrand factor.  J Biol Chem . 1995;  270 26025-26028