Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Dynamic regulation of sperm interactions with the zona pellucida prior to and after fertilisation

B. M. Gadella
+ Author Affiliations
- Author Affiliations

Department of Farm Animal Health and of Biochemistry and Cell Biology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 2, 3584 CM Utrecht, The Netherlands. Email: b.m.gadella@uu.nl

Reproduction, Fertility and Development 25(1) 26-37 https://doi.org/10.1071/RD12277
Published: 4 December 2012

Abstract

Recent findings have refined our thinking on sperm interactions with the cumulus–oocyte complex (COC) and our understanding of how, at the molecular level, the sperm cell fertilises the oocyte. Proteomic analyses has identified a capacitation-dependent sperm surface reordering that leads to the formation of functional multiprotein complexes involved in zona–cumulus interactions in several mammalian species. During this process, multiple docking of the acrosomal membrane to the plasma membrane takes place. In contrast with the dogma that the acrosome reaction is initiated when spermatozoa bind to the zona pellucida (ZP), it has been established recently that, in mice, the fertilising spermatozoon initiates its acrosome reaction during its voyage through the cumulus before it reaches the ZP. In fact, even acrosome-reacted mouse spermatozoa collected from the perivitelline space can fertilise another ZP-intact oocyte. The oviduct appears to influence the extracellular matrix properties of the spermatozoa as well as the COC. This may influence sperm binding and penetration of the cumulus and ZP, and, in doing so, increase monospermic while decreasing polyspermic fertilisation rates. Structural analysis of the ZP has shed new light on how spermatozoa bind and penetrate this structure and how the cortical reaction blocks sperm–ZP interactions. The current understanding of sperm interactions with the cumulus and ZP layers surrounding the oocyte is reviewed with a special emphasis on the lack of comparative knowledge on this topic in humans, as well as in most farm mammals.

Additional keywords: acrosome reaction, capacitation, cortical reaction, cumulus matrix, hypermotility, oocyte activation, oviduct, polyspermy block.


References

Abbott, A. L., and Ducibella, T. (2001). Calcium and the control of mammalian cortical granule exocytosis. Front. Biosci. 6, D792–D806.
Calcium and the control of mammalian cortical granule exocytosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlslKhu7k%3D&md5=33cace2758a6a8f0eec194a365de61cbCAS |

Austin, C. R., and Bishop, M. W. (1958). Role of the rodent acrosome and perforatorium in fertilization. Proc. R. Soc. Lond. B Biol. Sci. 149, 241–248.
Role of the rodent acrosome and perforatorium in fertilization.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG1M%2Fktl2itg%3D%3D&md5=bca8b12112620a2723ca81beb06ce07eCAS |

Avilés, M., Jaber, L., Castells, M. T., Kan, F. K., and Ballesta, J. (1996). Modifications of the lectin binding pattern in the rat zona pellucida after in vivo fertilization. Mol. Reprod. Dev. 44, 370–381.
Modifications of the lectin binding pattern in the rat zona pellucida after in vivo fertilization.Crossref | GoogleScholarGoogle Scholar |

Avilés, M., Jaber, L., Castells, M. T., Ballesta, J., and Kan, F. W. (1997). Modifications of carbohydrate residues and ZP2 and ZP3 glycoproteins in the mouse zona pellucida after fertilization. Biol. Reprod. 57, 1155–1163.
Modifications of carbohydrate residues and ZP2 and ZP3 glycoproteins in the mouse zona pellucida after fertilization.Crossref | GoogleScholarGoogle Scholar |

Avilés, M., Okinaga, T., Shur, B. D., and Ballesta, J. (2000). Differential expression of glycoside residues in the mammalian zona pellucida. Mol. Reprod. Dev. 57, 296–308.
Differential expression of glycoside residues in the mammalian zona pellucida.Crossref | GoogleScholarGoogle Scholar |

Avilés, M., Gutiérrez-Adán, A., and Coy, P. (2010). Oviduct secretions: will they be the key factors for the future ARTs? Mol. Hum. Reprod. 16, 896–906.
Oviduct secretions: will they be the key factors for the future ARTs?Crossref | GoogleScholarGoogle Scholar |

Baibakov, B., Boggs, N. A., Yauger, B., Baibakov, G., and Dean, J. (2012). Human sperm bind to the N-terminal domain of ZP2 in humanized zonae pellucidae in transgenic mice. J. Cell Biol. 197, 897–905.
Human sperm bind to the N-terminal domain of ZP2 in humanized zonae pellucidae in transgenic mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpvFOlsrw%3D&md5=7741f472e87ccb7fdedfb641d6ef1486CAS |

Baldi, E., Luconi, M., Krausz, C., and Forti, G. (2011). Progesterone and spermatozoa: a long-lasting liaison comes to definition. Hum. Reprod. 26, 2933–2934.
Progesterone and spermatozoa: a long-lasting liaison comes to definition.Crossref | GoogleScholarGoogle Scholar |

Barraud-Lange, V., Naud-Barriant, N., Bomsel, M., Wolf, J. P., and Ziyyat, A. (2007). Transfer of oocyte membrane fragments to fertilizing spermatozoa. FASEB J. 21, 3446–3449.
Transfer of oocyte membrane fragments to fertilizing spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht12jsbrI&md5=592261808e8d681285960d2958a92b60CAS |

Barraud-Lange, V., Chalas Boissonnas, C., Serres, C., Auer, J., Schmitt, A., Lefèvre, B., Wolf, J. P., and Ziyyat, A. (2012). Membrane transfer from oocyte to sperm occurs in two CD9-independent ways that do not supply the fertilising ability of Cd9-deleted oocytes. Reproduction 144, 53–66.
Membrane transfer from oocyte to sperm occurs in two CD9-independent ways that do not supply the fertilising ability of Cd9-deleted oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtV2ht7vM&md5=420df6600aa56326890d8afe64c21b2cCAS |

Bedford, J. M. (1966). Development of the fertilizing ability of spermatozoa in the epididymis of the rabbit. J. Exp. Zool. 163, 319–329.
Development of the fertilizing ability of spermatozoa in the epididymis of the rabbit.Crossref | GoogleScholarGoogle Scholar |

Bedford, J. M. (1968). Ultrastructural changes in the sperm head during fertilization in the rabbit. Am. J. Anat. 123, 329–358.
Ultrastructural changes in the sperm head during fertilization in the rabbit.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF1M%2FnslyltQ%3D%3D&md5=2844b0738b7e4a5b705ae719fcf39dbeCAS |

Bedford, J. M. (2011). Site of the mammalian sperm physiological acrosome reaction. Proc. Natl Acad. Sci. USA 108, 4703–4704.
Site of the mammalian sperm physiological acrosome reaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXktVOgtbc%3D&md5=230cbbbffeaa5b95b8daac39e28883c5CAS |

Bijttebier, J., Van Soom, A., Meyer, E., Mateusen, B., and Maes, D. (2008). Preovulatory follicular fluid during in vitro maturation decreases polyspermic fertilization of cumulus-intact porcine oocytes in vitro maturation of porcine oocytes. Theriogenology 70, 715–724.
Preovulatory follicular fluid during in vitro maturation decreases polyspermic fertilization of cumulus-intact porcine oocytes in vitro maturation of porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cvovVGhsw%3D%3D&md5=b73c63e5c3aa2069ee229f11f1bdca81CAS |

Bleil, J. D., and Wassarman, P. M. (1983). Oviduct-specific glycoprotein and heparin modulate sperm–zona pellucida interaction during fertilization and contribute to the control of polyspermy. Dev. Biol. 95, 317–324.
Oviduct-specific glycoprotein and heparin modulate sperm–zona pellucida interaction during fertilization and contribute to the control of polyspermy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXhtVGitL4%3D&md5=53ef384c6262ce1b7dcdcc67a4d91767CAS |

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.
Identification of a secondary sperm receptor in the mouse egg zona pellucida: role in maintenance of binding of acrosome-reacted sperm to eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXksFahurg%3D&md5=5c1d730d3df15245981bca85ebf88e00CAS |

Boatman, D. E., and Robbins, R. S. (1991). Detection of a soluble acrosome reaction-inducing factor, different from serum albumin, associated with the ovulated egg–cumulus complex. Mol. Reprod. Dev. 30, 396–401.
Detection of a soluble acrosome reaction-inducing factor, different from serum albumin, associated with the ovulated egg–cumulus complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhtVehurk%3D&md5=30e959416e1d0bdd67a1716339c24458CAS |

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, 34 189–34 202.
Structural characterization of native mouse zona pellucida proteins using mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvVCqs70%3D&md5=29512ea2496ab863b9ac00bd4569ead1CAS |

Buffone, M. G., Rodriguez-Miranda, E., Storey, B. T., and Gerton, G. L. (2009). Acrosomal exocytosis of mouse sperm progresses in a consistent direction in response to zona pellucida. J. Cell. Physiol. 220, 611–620.
Acrosomal exocytosis of mouse sperm progresses in a consistent direction in response to zona pellucida.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsV2ntLw%3D&md5=9919c1ef55f324224d4b832a3fde903fCAS |

Bureau, M., Bailey, J. L., and Sirard, M. A. (2000). Influence of oviductal cells and conditioned medium on porcine gametes. Zygote 8, 139–144.
Influence of oviductal cells and conditioned medium on porcine gametes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FhsVyisw%3D%3D&md5=38a56add812e1b63e91925bbc78ef515CAS |

Burkart, A. D., Xiong, B., Baibakov, B., Jiménez-Movilla, M., and Dean, J. (2012). Ovastacin, a cortical granule protease, cleaves ZP2 in the zona pellucida to prevent polyspermy. J. Cell Biol. 197, 37–44.
Ovastacin, a cortical granule protease, cleaves ZP2 in the zona pellucida to prevent polyspermy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlsVChur0%3D&md5=4cc0fa2106e3965fbe2809ea1259833bCAS |

Bustos, M. A., Lucchesi, O., Ruete, M. C., Mayorga, L. S., and Tomes, C. N. (2012). Rab27 and Rab3 sequentially regulate human sperm dense-core granule exocytosis. Proc. Natl Acad. Sci. USA , .
Rab27 and Rab3 sequentially regulate human sperm dense-core granule exocytosis.Crossref | GoogleScholarGoogle Scholar |

Canovas, S., Romar, R., Grullon, L. A., Aviles, M., and Coy, P. (2009). Pre-fertilization zona pellucida hardening by different cross-linkers affects IVF in pigs and cattle and improves embryo production in pigs. Reproduction 137, 803–812.
Pre-fertilization zona pellucida hardening by different cross-linkers affects IVF in pigs and cattle and improves embryo production in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovVKgtLc%3D&md5=99b98a5c72ddeef4c67bbc35fa0298c6CAS |

Carballada, R., and Esponda, P. (1992). Role of fluid from seminal vesicles and coagulating glands in sperm transport into the uterus and fertility in rats. J. Reprod. Fertil. 95, 639–648.
Role of fluid from seminal vesicles and coagulating glands in sperm transport into the uterus and fertility in rats.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s%2FitVOhtA%3D%3D&md5=16b199386340f3ee23423f76f5269d15CAS |

Chiu, P. C., Wong, B. S., Lee, C. L., Lam, K. K., Chung, M. K., Lee, K. F., Koistinen, R., Koistinen, H., Gupta, S. K., Seppälä, M., and Yeung, W. S. (2010). Zona pellucida-induced acrosome reaction in human spermatozoa is potentiated by glycodelin-A via down-regulation of extracellular signal-regulated kinases and up-regulation of zona pellucida-induced calcium influx. Hum. Reprod. 25, 2721–2733.
Zona pellucida-induced acrosome reaction in human spermatozoa is potentiated by glycodelin-A via down-regulation of extracellular signal-regulated kinases and up-regulation of zona pellucida-induced calcium influx.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlShtb7F&md5=bf6112fac053634dfd6932fc461d8940CAS |

Clark, G. F. (2011a). The molecular basis of mouse sperm-zona pellucida binding: a still unresolved issue in developmental biology. Reproduction 142, 377–381.
The molecular basis of mouse sperm-zona pellucida binding: a still unresolved issue in developmental biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Cjur3P&md5=84e3468c2757692cf71a7a7110db1c72CAS |

Clark, G. F. (2011b). Molecular models for mouse sperm–oocyte binding. Glycobiology 21, 3–5.
Molecular models for mouse sperm–oocyte binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFGru7rI&md5=ee8aa0c3ff2657c1a4523744f3142c50CAS |

Cooper, T. G. (2007). Sperm maturation in the epididymis: a new look at an old problem. Asian J. Androl. 9, 533–539.
Sperm maturation in the epididymis: a new look at an old problem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptVSltrc%3D&md5=b557d9e7eff8b3c056b6dff42612f02aCAS |

Cornwall, G. A. (2009). New insights into epididymal biology and function. Hum. Reprod. Update 15, 213–227.
New insights into epididymal biology and function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Ogurc%3D&md5=005ed51b8a6347767553a1cb21867524CAS |

Coy, P., Cánovas, S., Mondéjar, I., Saavedra, M. D., Romar, R., Grullón, L., Matás, C., and Avilés, M. (2008). Oviduct-specific glycoprotein and heparin modulate sperm–zona pellucida interaction during fertilization and contribute to the control of polyspermy. Proc. Natl Acad. Sci. USA 105, 15 809–15 814.
Oviduct-specific glycoprotein and heparin modulate sperm–zona pellucida interaction during fertilization and contribute to the control of polyspermy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1yitrjL&md5=9a84afefe6f0250c1f8ebfdc69e925fbCAS |

Coy, P., Lloyd, R., Romar, R., Satake, N., Matas, C., Gadea, J., and Holt, W. V. (2010). Effects of porcine pre-ovulatory oviductal fluid on boar sperm function. Theriogenology 74, 632–642.
Effects of porcine pre-ovulatory oviductal fluid on boar sperm function.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cjms1GntA%3D%3D&md5=420a46bb97ea303021aa5a1be683d23aCAS |

Darszon, A., Nishigaki, T., Beltran, C., and Treviño, C. L. (2011). Calcium channels in the development, maturation, and function of spermatozoa. Physiol. Rev. 91, 1305–1355.
Calcium channels in the development, maturation, and function of spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVOjsbrK&md5=fcac32c16a1784916a5efb00c8c54772CAS |

Ducibella, T., Duffy, P., and Buetow, J. (1994). Quantification and localization of cortical granules during oogenesis in the mouse. Biol. Reprod. 50, 467–473.
Quantification and localization of cortical granules during oogenesis in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c3itVGlsw%3D%3D&md5=51841cc189215323d8d081088518da02CAS |

Dun, M. D., Smith, N. D., Baker, M. A., Lin, M., Aitken, R. J., and Nixon, B. (2011). The chaperonin containing TCP1 complex (CCT/TRiC) is involved in mediating sperm–oocyte interaction. J. Biol. Chem. 286, 36 875–36 887.
The chaperonin containing TCP1 complex (CCT/TRiC) is involved in mediating sperm–oocyte interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlSqtLrJ&md5=317c140e1003009f685c004754e88adaCAS |

Evans, J. P. (2012). Sperm–egg interaction. Annu. Rev. Physiol. 74, 477–502.
Sperm–egg interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjvFynt78%3D&md5=6c9da03faa2630ced720b3ca92523d05CAS |

Fléchon, J. E., Degrouard, J., Kopecný, V., Pivko, J., Pavlok, A., and Motlik, J. (2003). The extracellular matrix of porcine mature oocytes: origin, composition and presumptive roles. Reprod. Biol. Endocrinol. 1, 124.
The extracellular matrix of porcine mature oocytes: origin, composition and presumptive roles.Crossref | GoogleScholarGoogle Scholar |

Florman, H. M., and Ducibella, T. (2006). Fertilization in mammals. In ‘Knobil and Neill’s Physiology of Reproduction’. 3rd edn. (Ed. J. D. Neill.) pp. 55–112. (Raven Press: New York.)

Fülöp, C., Szántó, S., Mukhopadhyay, D., Bárdos, T., Kamath, R. V., Rugg, M. S., Day, A. J., Salustri, A., Hascall, V. C., Glant, T. T., and Mikecz, K. (2003). Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice. Development 130, 2253–2261.
Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice.Crossref | GoogleScholarGoogle Scholar |

Gadella, B. M. (2010). Interaction of sperm with the zona pellucida during fertilization. Soc. Reprod. Fertil. Suppl. 67, 267–287.
| 1:STN:280:DC%2BC3MnosFenuw%3D%3D&md5=1fd09d14d2c2532aa5fc5ff3ee25970dCAS |

Gadella, B. M., and Evans, J. P. (2011). Membrane fusions during mammalian fertilization. Adv. Exp. Med. Biol. 713, 65–80.
Membrane fusions during mammalian fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVCltrvP&md5=d7a1a85081ca7cd5a4dbe476eea2a5f2CAS |

Gahlay, G., Gauthier, L., Baibakov, B., Epifano, O., and Dean, J. (2010). Gamete recognition in mice depends on the cleavage status of an egg’s zona pellucida protein. Science 329, 216–219.
Gamete recognition in mice depends on the cleavage status of an egg’s zona pellucida protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXosVWgurc%3D&md5=4e321713d7caf9fcb48c825157f27bd6CAS |

Ganguly, A., Bukovsky, A., Sharma, R. K., Bansal, P., Bhandari, B., and Gupta, S. K. (2010a). In humans, zona pellucida glycoprotein-1 binds to spermatozoa and induces acrosomal exocytosis. Hum. Reprod. 25, 1643–1656.
In humans, zona pellucida glycoprotein-1 binds to spermatozoa and induces acrosomal exocytosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVWmtb7O&md5=16ea5797fd103b411d1dad4fa889bf36CAS |

Ganguly, A., Bansal, P., Gupta, T., and Gupta, S. K. (2010b). ‘ZP domain’ of human zona pellucida glycoprotein-1 binds to human spermatozoa and induces acrosomal exocytosis. Reprod. Biol. Endocrinol. 8, 110.
‘ZP domain’ of human zona pellucida glycoprotein-1 binds to human spermatozoa and induces acrosomal exocytosis.Crossref | GoogleScholarGoogle Scholar |

Gardner, A. J., Williams, C. J., and Evans, J. P. (2007). Establishment of the mammalian membrane block to polyspermy: evidence for calcium-dependent and -independent regulation. Reproduction 133, 383–393.
Establishment of the mammalian membrane block to polyspermy: evidence for calcium-dependent and -independent regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvVOjtrg%3D&md5=7a3ae07b6904ae92293a71d1f544d27aCAS |

Ghosh, I., and Datta, K. (2003). Sperm surface hyaluronan binding protein (HABP1) interacts with zona pellucida of water buffalo (Bubalus bubalis) through its clustered mannose residues. Mol. Reprod. Dev. 64, 235–244.
Sperm surface hyaluronan binding protein (HABP1) interacts with zona pellucida of water buffalo (Bubalus bubalis) through its clustered mannose residues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXis1yltw%3D%3D&md5=78fb895b89d2fa6fa0bf82b62202594eCAS |

Gonçalves, R. F., Barnabe, V. H., and Killian, G. J. (2008). Pre-treatment of cattle sperm and/or oocyte with antibody to lipocalin type prostaglandin D synthase inhibits in vitro fertilization and increases sperm–oocyte binding. Anim. Reprod. Sci. 106, 188–193.
Pre-treatment of cattle sperm and/or oocyte with antibody to lipocalin type prostaglandin D synthase inhibits in vitro fertilization and increases sperm–oocyte binding.Crossref | GoogleScholarGoogle Scholar |

Gonzalez-Garcia, J. R., Machaty, Z., Lai, F. A., and Swann, K. (2012). The dynamics of PKC-induced phosphorylation triggered by Ca(2+) oscillations in mouse eggs. J. Cell. Physiol. , .
The dynamics of PKC-induced phosphorylation triggered by Ca(2+) oscillations in mouse eggs.Crossref | GoogleScholarGoogle Scholar |

Goudet, G., Mugnier, S., Callebaut, I., and Monget, P. (2008). Phylogenetic analysis and identification of pseudogenes reveal a progressive loss of zona pellucida genes during evolution of vertebrates. Biol. Reprod. 78, 796–806.
Phylogenetic analysis and identification of pseudogenes reveal a progressive loss of zona pellucida genes during evolution of vertebrates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltVOgu7s%3D&md5=46ed157c7de6674ed430b910837f26aaCAS |

Gupta, S. K., Bhandari, B., Shrestha, A., Biswal, B. K., Palaniappan, C., Malhotra, S. S., and Gupta, N. (2012). Mammalian zona pellucida glycoproteins: structure and function during fertilization. Cell Tissue Res. , .
Mammalian zona pellucida glycoproteins: structure and function during fertilization.Crossref | GoogleScholarGoogle Scholar |

Hanna, W. F., Kerr, C. L., Shaper, J. H., and Wright, W. W. (2004). Lewis X-containing neoglycoproteins mimic the intrinsic ability of zona pellucida glycoprotein ZP3 to induce the acrosome reaction in capacitated mouse sperm. Biol. Reprod. 71, 778–789.
Lewis X-containing neoglycoproteins mimic the intrinsic ability of zona pellucida glycoprotein ZP3 to induce the acrosome reaction in capacitated mouse sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntFejtb0%3D&md5=b55ae0eb5d5d25970159ade23b85f3b1CAS |

Hao, Y., Mathialagan, N., Walters, E., Mao, J., Lai, L., Becker, D., Li, W., Critser, J., and Prather, R. S. (2006). Osteopontin reduces polyspermy during in vitro fertilization of porcine oocytes. Biol. Reprod. 75, 726–733.
Osteopontin reduces polyspermy during in vitro fertilization of porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFCgt7nM&md5=ffa103a1fe451337b9fed7ac7a85a775CAS |

Hoodbhoy, T., and Dean, J. (2004). Insights into the molecular basis of sperm–egg recognition in mammals. Reproduction 127, 417–422.
Insights into the molecular basis of sperm–egg recognition in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjt1OlsbY%3D&md5=9475522a86fc1e11242131c50b5408f2CAS |

Howes, E., Pascall, J. C., Engel, W., and Jones, R. (2001). Interactions between mouse ZP2 glycoprotein and proacrosin; a mechanism for secondary binding of sperm to the zona pellucida during fertilization. J. Cell Sci. 114, 4127–4136.
| 1:CAS:528:DC%2BD3MXptVKlsLw%3D&md5=1cbc867ac4dd81ddc659aa595e18ae5fCAS |

Hunter, R. H., Petersen, H. H., and Greve, T. (1999). Ovarian follicular fluid, progesterone and Ca2+ ion influences on sperm release from the fallopian tube reservoir. Mol. Reprod. Dev. 54, 283–291.
Ovarian follicular fluid, progesterone and Ca2+ ion influences on sperm release from the fallopian tube reservoir.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmsVCjt7o%3D&md5=b83da60c59db100e519599ff4ce775c3CAS |

Inoue, N., Satouh, Y., Ikawa, M., Okabe, M., and Yanagimachi, R. (2011a). Acrosome-reacted mouse spermatozoa recovered from the perivitelline space can fertilize other eggs. Proc. Natl Acad. Sci. USA 108, 20 008–20 011.
Acrosome-reacted mouse spermatozoa recovered from the perivitelline space can fertilize other eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs12gtbnK&md5=4f7ab282154cce50fec9652786ba6f44CAS |

Inoue, N., Ikawa, M., and Okabe, M. (2011b). The mechanism of sperm–egg interaction and the involvement of IZUMO1 in fusion. Asian J. Androl. 13, 81–87.
The mechanism of sperm–egg interaction and the involvement of IZUMO1 in fusion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlejtw%3D%3D&md5=3304eeeef54031703fd7fdbb5f283c28CAS |

Izquierdo-Rico, M. J., Jimenez-Movilla, M., Llop, E., Perez-Oliva, A. B., Ballesta, J., Gutierrez-Gallego, R., Jimenez-Cervantes, C., and Aviles, M. (2009). Hamster zona pellucida is formed by four glycoproteins: ZP1, ZP2, ZP3, and ZP4. J. Proteome Res. 8, 926–941.
Hamster zona pellucida is formed by four glycoproteins: ZP1, ZP2, ZP3, and ZP4.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpt1akug%3D%3D&md5=ba85380761785a1a2798c212672aa658CAS |

Jin, M., Fujiwara, E., Kakiuchi, Y., Okabe, M., Satouh, Y., Baba, S. A., Chiba, K., and Hirohashi, N. (2011). Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization. Proc. Natl Acad. Sci. USA 108, 4892–4896.
Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXktValt7s%3D&md5=8a9ed79d4cf669976b2d0b87c0843fc7CAS |

Kaji, K., Oda, S., Shikano, T., Ohnuki, T., Uematsu, Y., Sakagami, J., Tada, N., Miyazaki, S., and Kudo, A. (2000). The gamete fusion process is defective in eggs of Cd9-deficient mice. Nat. Genet. 24, 279–282.
The gamete fusion process is defective in eggs of Cd9-deficient mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhvFaqt7s%3D&md5=dadf70be51b33c290fe111a5dc8e5a4cCAS |

Kalab, P., Kopf, G. S., and Schultz, R. M. (1991). Modifications of the mouse zona pellucida during oocyte maturation and egg activation: effects of newborn calf serum and fetuin. Biol. Reprod. 45, 783–787.
Modifications of the mouse zona pellucida during oocyte maturation and egg activation: effects of newborn calf serum and fetuin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmsFaqsbk%3D&md5=56768982ff9cea32dde273d1841e10d0CAS |

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.
Structural characterization of the N-linked carbohydrate chains of the zona pellucida glycoproteins from bovine ovarian and fertilized eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlsF2gtL8%3D&md5=c5fc99fd4c1e45024f3a811409d018d1CAS |

Kawano, N., Kang, W., Yamashita, M., Koga, Y., Yamazaki, T., Hata, T., Miyado, K., and Baba, T. (2010). Mice lacking two sperm serine proteases, ACR and PRSS21, are subfertile, but the mutant sperm are infertile in vitro. Biol. Reprod. 83, 359–369.
Mice lacking two sperm serine proteases, ACR and PRSS21, are subfertile, but the mutant sperm are infertile in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVyrsrrK&md5=b1c4b767b1347d38ba4087a5111abccbCAS |

Killian, G. (2011). Physiology and endocrinology symposium: evidence that oviduct secretions influence sperm function: a retrospective view for livestock. J. Anim. Sci. 89, 1315–1322.
Physiology and endocrinology symposium: evidence that oviduct secretions influence sperm function: a retrospective view for livestock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXls1Oitbs%3D&md5=504ccd6867147f2aa2f1e5a0ede1b242CAS |

Kim, K. S., Foster, J. A., Kvasnicka, K. W., and Gerton, G. L. (2011). Transitional states of acrosomal exocytosis and proteolytic processing of the acrosomal matrix in guinea pig sperm. Mol. Reprod. Dev. 78, 930–941.
Transitional states of acrosomal exocytosis and proteolytic processing of the acrosomal matrix in guinea pig sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVOisbzF&md5=0e7c1998cccbd779fcb56f9e6ae59c48CAS |

Kölle, S., Reese, S., and Kummer, W. (2010). New aspects of gamete transport, fertilization, and embryonic development in the oviduct gained by means of live cell imaging. Theriogenology 73, 786–795.
New aspects of gamete transport, fertilization, and embryonic development in the oviduct gained by means of live cell imaging.Crossref | GoogleScholarGoogle Scholar |

Leahy, T., and Gadella, B. M. (2011). Sperm surface changes and physiological consequences induced by sperm handling and storage. Reproduction 142, 759–778.
Sperm surface changes and physiological consequences induced by sperm handling and storage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1GqtLnL&md5=d6a4f0eb2b8ce1e77de217e4b1a8f8a7CAS |

Lefèvre, B., Wolf, J. P., and Ziyyat, A. (2010). Sperm–egg interaction: is there a link between tetraspanin(s) and GPI-anchored protein(s)? Bioessays 32, 143–152.
Sperm–egg interaction: is there a link between tetraspanin(s) and GPI-anchored protein(s)?Crossref | GoogleScholarGoogle Scholar |

Lefièvre, L., Conner, S. J., Salpekar, A., Olufowobi, O., Ashton, P., Pavlovic, B., Lenton, W., Afnan, M., Brewis, I. A., Monk, M., Hughes, D. C., and Barratt, C. L. (2004). Four zona pellucida glycoproteins are expressed in the human. Hum. Reprod. 19, 1580–1586.
Four zona pellucida glycoproteins are expressed in the human.Crossref | GoogleScholarGoogle Scholar |

Le Naour, F., Rubinstein, E., Jasmin, C., Prenant, M., and Boucheix, C. (2000). Severely reduced female fertility in CD9-deficient mice. Science 287, 319–321.
Severely reduced female fertility in CD9-deficient mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlvVOntA%3D%3D&md5=ea9fd4dabe84f7d6756d64af5373ca75CAS |

Lishko, P. V., Kirichok, Y., Ren, D., Navarro, B., Chung, J. J., and Clapham, D. E. (2012). The control of male fertility by spermatozoan ion channels. Annu. Rev. Physiol. 74, 453–475.
The control of male fertility by spermatozoan ion channels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjvFynt74%3D&md5=2e6b9738d9306e6ded405b620addde3aCAS |

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.
Characterization of mouse ZP3-derived glycopeptide, gp55, that exhibits sperm receptor and acrosome reaction-inducing activity in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhsFKqtr4%3D&md5=b6333e67f48527ae5ead9ab77d1ac830CAS |

Liu, M. (2011). The biology and dynamics of mammalian cortical granules. Reprod. Biol. Endocrinol. 9, 149.
The biology and dynamics of mammalian cortical granules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Gg&md5=5925309abc0aef3ed08b5e8ed9fe7125CAS |

Liu, D. Y., Garrett, C., and Baker, H. W. (2006). Acrosome-reacted human sperm in insemination medium do not bind to the zona pellucida of human oocytes. Int. J. Androl. 29, 475–481.
Acrosome-reacted human sperm in insemination medium do not bind to the zona pellucida of human oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xps1Cqurc%3D&md5=82e02d7e786c2c164d297f542426ffc6CAS |

Lyng, R., and Shur, B. D. (2009). Mouse oviduct-specific glycoprotein is an egg-associated ZP3-independent sperm-adhesion ligand. J. Cell Sci. 122, 3894–3906.
Mouse oviduct-specific glycoprotein is an egg-associated ZP3-independent sperm-adhesion ligand.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFWhurnF&md5=8ed92f5b3a9949cde364e6d6ed78428bCAS |

Marín-Briggiler, C. I., González-Echeverría, M. F., Munuce, M. J., Ghersevich, S., Caille, A. M., Hellman, U., Corrigall, V. M., and Vazquez-Levin, M. H. (2010). Glucose-regulated protein 78 (Grp78/BiP) is secreted by human oviduct epithelial cells and the recombinant protein modulates sperm–zona pellucida binding. Fertil. Steril. 93, 1574–1584.
Glucose-regulated protein 78 (Grp78/BiP) is secreted by human oviduct epithelial cells and the recombinant protein modulates sperm–zona pellucida binding.Crossref | GoogleScholarGoogle Scholar |

Martin-DeLeon, P. A. (2011). Germ-cell hyaluronidases: their roles in sperm function. Int. J. Androl. 34, e306–e318.
Germ-cell hyaluronidases: their roles in sperm function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlOksr7O&md5=6238355232de1b7796be8645f0744c6aCAS |

Mattioli, M., Lucidi, P., and Barboni, B. (1998). Expanded cumuli induce acrosome reaction in boar sperm. Mol. Reprod. Dev. 51, 445–453.
Expanded cumuli induce acrosome reaction in boar sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnt1Ort74%3D&md5=aed553fc2e86daccbc0299b5b08988b1CAS |

Maxwell, W. M., de Graaf, S. P., Ghaoui, R.-H., and Evans, G. (2007). Seminal plasma effects on sperm handling and female fertility. Soc. Reprod. Fertil. Suppl. 64, 13–38.
| 1:CAS:528:DC%2BD1cXpvVyku7c%3D&md5=83b9988277486e3e635e3deca6b890fdCAS |

Miyado, K., Yamada, G., Yamada, S., Hasuwa, H., Nakamura, Y., Ryu, F., Suzuki, K., Kosai, K., Inoue, K., Ogura, A., Okabe, M., and Mekada, E. (2000). Requirement of CD9 on the egg plasma membrane for fertilization. Science 287, 321–324.
Requirement of CD9 on the egg plasma membrane for fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlvVOmsw%3D%3D&md5=545e8e59ebe94f0b6f4c6e865b0089d3CAS |

Miyado, K., Yoshida, K., Yamagata, K., Sakakibara, K., Okabe, M., Wang, X., Miyamoto, K., Akutsu, H., Kondo, T., Takahashi, Y., Ban, T., Ito, C., Toshimori, K., Nakamura, A., Ito, M., Miyado, M., Mekada, E., and Umezawa, A. (2008). The fusing ability of sperm is bestowed by CD9-containing vesicles released from eggs in mice. Proc. Natl Acad. Sci. USA 105, 12 921–12 926.
The fusing ability of sperm is bestowed by CD9-containing vesicles released from eggs in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFSmtrjL&md5=230a9d2ed9733fc0ee0aaa6e5c463c90CAS |

Mondéjar, I., Grullón, L. A., García-Vázquez, F. A., Romar, R., and Coy, P. (2012). Fertilization outcome could be regulated by binding of oviductal plasminogen to oocytes and by releasing of plasminogen activators during interplay between gametes. Fertil. Steril. 97, 453–461.e3.
Fertilization outcome could be regulated by binding of oviductal plasminogen to oocytes and by releasing of plasminogen activators during interplay between gametes.Crossref | GoogleScholarGoogle Scholar |

Monné, M., and Jovine, L. (2011). A structural view of egg coat architecture and function in fertilization. Biol. Reprod. 85, 661–669.
A structural view of egg coat architecture and function in fertilization.Crossref | GoogleScholarGoogle Scholar |

Moreno, R. D., Hoshi, M., and Barros, C. (1999). Functional interactions between sulphated polysaccharides and proacrosin: implications in sperm binding and digestion of zona pellucida. Zygote 7, 105–111.
Functional interactions between sulphated polysaccharides and proacrosin: implications in sperm binding and digestion of zona pellucida.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkvV2kur0%3D&md5=3ede30af70e26dc87f752cff8016fb10CAS |

Muiño-Blanco, T., Pérez-Pé, R., and Cebrián-Pérez, J. A. (2008). Seminal plasma proteins and sperm resistance to stress. Reprod. Domest. Anim. 43, 18–31.
Seminal plasma proteins and sperm resistance to stress.Crossref | GoogleScholarGoogle Scholar |

Munuce, M. J., Serravalle, A., Caille, A. M., Zumoffen, C., Botti, G., Cabada, M., and Ghersevich, S. (2009). Human tubal secretion can modify the affinity of human spermatozoa for the zona pellucida. Fertil. Steril. 91, 407–413.
Human tubal secretion can modify the affinity of human spermatozoa for the zona pellucida.Crossref | GoogleScholarGoogle Scholar |

Nixon, B., Mitchell, L. A., Anderson, A. L., McLaughlin, E. A., O’Bryan, M. K., and Aitken, R. J. (2011). Proteomic and functional analysis of human sperm detergent resistant membranes. J. Cell. Physiol. 226, 2651–2665.
Proteomic and functional analysis of human sperm detergent resistant membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpt1CltLo%3D&md5=05c9fcb0650f5de90b36ed9ec088eee9CAS |

Nomikos, M., Swann, K., and Lai, F. A. (2012). Starting a new life: sperm PLC-zeta mobilizes the Ca2+ signal that induces egg activation and embryo development: an essential phospholipase C with implications for male infertility. Bioessays 34, 126–134.
Starting a new life: sperm PLC-zeta mobilizes the Ca2+ signal that induces egg activation and embryo development: an essential phospholipase C with implications for male infertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltVaguw%3D%3D&md5=eef2bef15c64af54c85c52b1f5981788CAS |

Pang, P. C., Chiu, P. C., Lee, C. L., Chang, L. Y., Panico, M., Morris, H. R., Haslam, S. M., Khoo, K. H., Clark, G. F., Yeung, W. S., and Dell, A. (2011). Human sperm binding is mediated by the sialyl-Lewis(x) oligosaccharide on the zona pellucida. Science 333, 1761–1764.
Human sperm binding is mediated by the sialyl-Lewis(x) oligosaccharide on the zona pellucida.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFyqurnE&md5=9dacee4ba1280e188ab58568653f579eCAS |

Patrat, C., Auer, J., Fauque, P., Leandri, R. L., Jouannet, P., and Serres, C. (2006). Zona pellucida from fertilised human oocytes induces a voltage-dependent calcium influx and the acrosome reaction in spermatozoa, but cannot be penetrated by sperm. BMC Dev. Biol. 6, 59.
Zona pellucida from fertilised human oocytes induces a voltage-dependent calcium influx and the acrosome reaction in spermatozoa, but cannot be penetrated by sperm.Crossref | GoogleScholarGoogle Scholar |

Redgrove, K. A., Anderson, A. L., Dun, M. D., McLaughlin, E. A., O’Bryan, M. K., Aitken, R. J., and Nixon, B. (2011). Involvement of multimeric protein complexes in mediating the capacitation-dependent binding of human spermatozoa to homologous zonae pellucidae. Dev. Biol. 356, 460–474.
Involvement of multimeric protein complexes in mediating the capacitation-dependent binding of human spermatozoa to homologous zonae pellucidae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptlCntro%3D&md5=2feff0458f9181c96fd737488b604ea9CAS |

Reid, A. T., Redgrove, K., Aitken, R. J., and Nixon, B. (2011). Cellular mechanisms regulating sperm–zona pellucida interaction. Asian J. Androl. 13, 88–96.
Cellular mechanisms regulating sperm–zona pellucida interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlejsw%3D%3D&md5=eaebfc7723517a04f0cc2b2b92605fe2CAS |

Robertson, S. A. (2007). Seminal fluid signaling in the female reproductive tract: lessons from rodents and pigs. J. Anim. Sci. 85, E36–E44.
Seminal fluid signaling in the female reproductive tract: lessons from rodents and pigs.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s7itlWkug%3D%3D&md5=616c619a0ccc73316a3a51e1d82c8366CAS |

Rodriguez-Martinez, H. (2007). Role of the oviduct in sperm capacitation. Theriogenology 68, S138–S146.
Role of the oviduct in sperm capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotlaitLY%3D&md5=6c0c90330fb105eb81682e33960dc18bCAS |

Roggero, C. M., De Blas, G. A., Dai, H., Tomes, C. N., Rizo, J., and Mayorga, L. S. (2007). Complexin/synaptotagmin interplay controls acrosomal exocytosis. J. Biol. Chem. 282, 26 335–26 343.
Complexin/synaptotagmin interplay controls acrosomal exocytosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpslGjt78%3D&md5=dc0c6e39f5805350c5dcfab0b71f8e00CAS |

Rubinstein, E., Ziyyat, A., Wolf, J. P., Le Naour, F., and Boucheix, C. (2006). The molecular players of sperm–egg fusion in mammals. Semin. Cell Dev. Biol. 17, 254–263.
The molecular players of sperm–egg fusion in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XntFSgsrk%3D&md5=a807f85574ceef46ec3a53d186970d91CAS |

Schroeder, A. C., Schultz, R. M., Kopf, G. S., Taylor, F. R., Becker, R. B., and Eppig, J. J. (1990). Fetuin inhibits zona pellucida hardening and conversion of ZP2 to ZP2f during spontaneous mouse oocyte maturation in vitro in the absence of serum. Biol. Reprod. 43, 891–897.
Fetuin inhibits zona pellucida hardening and conversion of ZP2 to ZP2f during spontaneous mouse oocyte maturation in vitro in the absence of serum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXmt1ymtbw%3D&md5=4b11fe6df7b3aed6014d2e792521cdfcCAS |

Selvaraj, V., Buttke, D. E., Asano, A., McElwee, J. L., Wolff, C. A., Nelson, J. L., Klaus, A. V., Hunnicutt, G. R., and Travis, A. J. (2007). GM1 dynamics as a marker for membrane changes associated with the process of capacitation in murine and bovine spermatozoa. J. Androl. 28, 588–599.
GM1 dynamics as a marker for membrane changes associated with the process of capacitation in murine and bovine spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosVymu7k%3D&md5=42498f97a611fe57494ff11136d5e241CAS |

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.
Reassessing the role of protein–carbohydrate complementarity during sperm–egg interactions in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht12qsL7L&md5=a3a94dd674060d0130fa57b2a4fa74a1CAS |

Somers, C. E., Battaglia, D. E., and Shapiro, B. M. (1989). Localization and developmental fate of ovoperoxidase and proteoliaisin, two proteins involved in fertilization envelope assembly. Dev. Biol. 131, 226–235.
Localization and developmental fate of ovoperoxidase and proteoliaisin, two proteins involved in fertilization envelope assembly.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXjslSqsQ%3D%3D&md5=30c6697fc7506f85256ad03bff2142ffCAS |

Stetson, I., Izquierdo-Rico, M. J., Moros, C., Chevret, P., Lorenzo, P. L., Ballesta, J., Rebollar, P. G., Gutiérrez-Gallego, R., and Avilés, M. (2012). Rabbit zona pellucida composition: a molecular, proteomic and phylogenetic approach. J. Proteomics , .
Rabbit zona pellucida composition: a molecular, proteomic and phylogenetic approach.Crossref | GoogleScholarGoogle Scholar |

Suarez, S. S. (2008). Regulation of sperm storage and movement in the mammalian oviduct. Int. J. Dev. Biol. 52, 455–462.
Regulation of sperm storage and movement in the mammalian oviduct.Crossref | GoogleScholarGoogle Scholar |

Sun, Q. Y. (2003). Cellular and molecular mechanisms leading to cortical reaction and polyspermy block in mammalian eggs. Microsc. Res. Tech. 61, 342–348.
Cellular and molecular mechanisms leading to cortical reaction and polyspermy block in mammalian eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXls1Gnu7k%3D&md5=34f54d9f34c570035f6f7a2e6d0c6ccaCAS |

Swann, K., and Yu, Y. (2008). The dynamics of calcium oscillations that activate mammalian eggs. Int. J. Dev. Biol. 52, 585–594.
The dynamics of calcium oscillations that activate mammalian eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht12qs7fJ&md5=18879d4f385d22342c21fd74969468c7CAS |

Tanii, I., Aradate, T., Matsuda, K., Komiya, A., and Fuse, H. (2011). PACAP-mediated sperm–cumulus cell interaction promotes fertilization. Reproduction 141, 163–171.
PACAP-mediated sperm–cumulus cell interaction promotes fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisVehsLw%3D&md5=14c00de236b28ed7cf7af3e177f281ceCAS |

Thaler, C. D., Thomas, M., and Ramalie, J. R. (2006). Reorganization of mouse sperm lipid rafts by capacitation. Mol. Reprod. Dev. 73, 1541–1549.
Reorganization of mouse sperm lipid rafts by capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFGhtr%2FP&md5=fc3799be2040f3323cbe72670c7d2508CAS |

Thérien, I., and Manjunath, P. (2003). Effect of progesterone on bovine sperm capacitation and acrosome reaction. Biol. Reprod. 69, 1408–1415.
Effect of progesterone on bovine sperm capacitation and acrosome reaction.Crossref | GoogleScholarGoogle Scholar |

Tollner, T. L., Yudin, A. I., Treece, C. A., Overstreet, J. W., and Cherr, G. N. (2008). Macaque sperm coating protein DEFB126 facilitates sperm penetration of cervical mucus. Hum. Reprod. 23, 2523–2534.
Macaque sperm coating protein DEFB126 facilitates sperm penetration of cervical mucus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Ois73E&md5=9a49b9e530296ed0c1c00c392a505b32CAS |

Troedsson, M. H., Desvousges, A., Alghamdi, A. S., Dahms, B., Dow, C. A., Hayna, J., Valesco, R., Collahan, P. T., Macpherson, M. L., Pozor, M., and Buhi, W. C. (2005). Components in seminal plasma regulating sperm transport and elimination. Anim. Reprod. Sci. 89, 171–186.
Components in seminal plasma regulating sperm transport and elimination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVart77F&md5=a2ae6287715003fa4a2228f7442232a3CAS |

Tsai, P. S., and Gadella, B. (2009). Molecular kinetics of proteins at the surface of porcine sperm before and during fertilization. Soc. Reprod. Fertil. Suppl. 66, 23–36.
| 1:CAS:528:DC%2BC3cXjslKjt7Y%3D&md5=4958bdd6e1979a34c3c837fcd19aa58dCAS |

Tsai, P. S., Garcia-Gil, N., van Haeften, T., and Gadella, B. M. (2010). How pig sperm prepares to fertilize: stable acrosome docking to the plasma membrane. PLoS One 5, e11204.
How pig sperm prepares to fertilize: stable acrosome docking to the plasma membrane.Crossref | GoogleScholarGoogle Scholar |

Tsai, P. S., van Haeften, T., and Gadella, B. M. (2011). Preparation of the cortical reaction: maturation-dependent migration of SNARE proteins, clathrin, and complexin to the porcine oocyte’s surface blocks membrane traffic until fertilization. Biol. Reprod. 84, 327–335.
Preparation of the cortical reaction: maturation-dependent migration of SNARE proteins, clathrin, and complexin to the porcine oocyte’s surface blocks membrane traffic until fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVeltrg%3D&md5=ff6a48c5950e15ac4010ad9b7bea4808CAS |

Tsai, P. S., Brewis, I. A., van Maaren, J., and Gadella, B. M. (2012). Involvement of complexin 2 in docking, locking and unlocking of different SNARE complexes during sperm capacitation and induced acrosomal exocytosis. PLoS One 7, e32603.
Involvement of complexin 2 in docking, locking and unlocking of different SNARE complexes during sperm capacitation and induced acrosomal exocytosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XktVOks7o%3D&md5=82ac166d367a3d2caeb9325bb66e177cCAS |

Tulsiani, D. R., Abou-Haila, A., Loeser, C. R., and Pereira, B. M. (1998). The biological and functional significance of the sperm acrosome and acrosomal enzymes in mammalian fertilization. Exp. Cell Res. 240, 151–164.
The biological and functional significance of the sperm acrosome and acrosomal enzymes in mammalian fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXivFOnsLw%3D&md5=dc8e1b44497b72cc2f3031721a4b8daaCAS |

Turunen, H. T., Sipilä, P., Krutskikh, A., Toivanen, J., Mankonen, H., Hämäläinen, V., Björkgren, I., Huhtaniemi, I., and Poutanen, M. (2012). Loss of cysteine-rich secretory protein 4 (Crisp4) leads to deficiency in sperm–zona pellucida interaction in mice. Biol. Reprod. 86, 1–8.
Loss of cysteine-rich secretory protein 4 (Crisp4) leads to deficiency in sperm–zona pellucida interaction in mice.Crossref | GoogleScholarGoogle Scholar |

van Gestel, R. A., Brewis, I. A., Ashton, P. R., Helms, J. B., Brouwers, J. F., and Gadella, B. M. (2005). Capacitation-dependent concentration of lipid rafts in the apical ridge head area of porcine sperm cells. Mol. Hum. Reprod. 11, 583–590.
Capacitation-dependent concentration of lipid rafts in the apical ridge head area of porcine sperm cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVelsbrP&md5=7ccda1bd843121e26a192adce2ee5772CAS |

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.
Multiple proteins present in purified porcine sperm apical plasma membranes interact with the zona pellucida of the oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotl2qurg%3D&md5=e1477b7a9fbc47bb6a99eb703fd8a6cfCAS |

Vatzias, G., and Hagen, D. R. (1999). Effects of porcine follicular fluid and oviduct-conditioned media on maturation and fertilization of porcine oocytes in vitro. Biol. Reprod. 60, 42–48.
Effects of porcine follicular fluid and oviduct-conditioned media on maturation and fertilization of porcine oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvFymtQ%3D%3D&md5=3dde8966905f3442e3cb4b6d1d500ab0CAS |

Velásquez, J. G., Canovas, S., Barajas, P., Marcos, J., Jiménez-Movilla, M., Gallego, R. G., Ballesta, J., Avilés, M., and Coy, P. (2007). Role of sialic acid in bovine sperm–zona pellucida binding. Mol. Reprod. Dev. 74, 617–628.
Role of sialic acid in bovine sperm–zona pellucida binding.Crossref | GoogleScholarGoogle Scholar |

Wassarman, P. M., and Albertini, D. F. (1994). The mammalian ovum. In ‘The Physiology of Reproduction’. (Eds E. Knobil and J. D. Neill.) pp. 79–122. (Raven Press: New York.)

Yanagimachi, R. (1994). Mammalian fertilization. In ‘The Physiology of Reproduction’. (Eds E. Knobil and J. D. Neill) pp. 189–317. (Raven Press: New York.)

Yeung, W. S., Lee, K. F., Koistinen, R., Koistinen, H., Seppälä, M., and Chiu, P. C. (2009). Effects of glycodelins on functional competence of spermatozoa. J. Reprod. Immunol. 83, 26–30.
Effects of glycodelins on functional competence of spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVyntr3O&md5=043a0bfbdb835a6447b6828be8e19835CAS |

Yonezawa, N., Amari, S., Takahashi, K., Ikeda, K., Imai, F. L., Kanai, S., Kikuchi, K., and Nakano, M. (2005). Participation of the nonreducing terminal beta-galactosyl residues of the neutral N-linked carbohydrate chains of porcine zona pellucida glycoproteins in sperm-egg binding. Mol. Reprod. Dev. 70, 222–227.
Participation of the nonreducing terminal beta-galactosyl residues of the neutral N-linked carbohydrate chains of porcine zona pellucida glycoproteins in sperm-egg binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltlSrsw%3D%3D&md5=97c9191e42a50da24a6820e26579863eCAS |

Yonezawa, N., Kanai-Kitayama, S., Kitayama, T., Hamano, A., and Nakano, M. (2011). Porcine zona pellucida glycoprotein ZP4 is responsible for the sperm-binding activity of the ZP3/ZP4 complex. Zygote 6, 1–9.
Porcine zona pellucida glycoprotein ZP4 is responsible for the sperm-binding activity of the ZP3/ZP4 complex.Crossref | GoogleScholarGoogle Scholar |

Yu, Y., Nomikos, M., Theodoridou, M., Nounesis, G., Lai, F. A., and Swann, K. (2012). PLCζ causes Ca(2+) oscillations in mouse eggs by targeting intracellular and not plasma membrane PI(4,5)P(2). Mol. Biol. Cell 23, 371–380.
PLCζ causes Ca(2+) oscillations in mouse eggs by targeting intracellular and not plasma membrane PI(4,5)P(2).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlWqtbg%3D&md5=4bedbbb0ed7c173ff762016a5b98c677CAS |

Zhao, L., Burkin, H. R., Shi, X., Li, L., Reim, K., and Miller, D. J. (2007). Complexin I is required for mammalian sperm acrosomal exocytosis. Dev. Biol. 309, 236–244.
Complexin I is required for mammalian sperm acrosomal exocytosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVWmt7rL&md5=501743303cf8b446bdd50ef3d8aaee25CAS |

Zhou, C., Kang, W., and Baba, T. (2012). Functional caharcetrization of double-knockout mouse lacking SPAM1 and ACR or SPAM1 and PRSS21 in fertilization. J. Reprod. Dev. 58, 330–337.
Functional caharcetrization of double-knockout mouse lacking SPAM1 and ACR or SPAM1 and PRSS21 in fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtF2jsr3L&md5=5d372caab76ea058046b45030abbdef3CAS |

Zhuo, L., Yoneda, M., Zhao, M., Yingsung, W., Yoshida, N., Kitagawa, Y., Kawamura, K., Suzuki, T., and Kimata, K. (2001). Defect in SHAP–hyaluronan complex causes severe female infertility. A study by inactivation of the bikunin gene in mice. J. Biol. Chem. 276, 7693–7696.
Defect in SHAP–hyaluronan complex causes severe female infertility. A study by inactivation of the bikunin gene in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXitFKht7g%3D&md5=d578428c3ee5303dec6160eb82f96516CAS |