Sperm-zona pellucida (ZP) interaction, involving the binding of sperm surface ligands to complementary carbohydrates of ZP, is the first direct gamete contact event crucial for subsequent gamete fusion and successful fertilization in mammals. It is a complex process mediated by the coordinated engagement of multiple ZP receptors forming high-molecular-weight (HMW) protein complexes at the acrosomal region of the sperm surface. The present article aims to review the current understanding of sperm-ZP binding in the four most studied mammalian models, i.e., murine, porcine, bovine, and human, and summarizes the candidate ZP receptors with established ZP affinity, including their origins and the mechanisms of ZP binding. Further, it compares and contrasts the ZP structure and carbohydrate composition in the aforementioned model organisms. The comprehensive understanding of sperm-ZP interaction mechanisms is critical for the diagnosis of infertility and thus becomes an integral part of assisted reproductive therapies/technologies.

Department of Obstetrics Gynecology and Women's Health University of Missouri Columbia MO 65211 USA

Department of Veterinary Sciences Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamycka 129 165 00 Prague Czech Republic

Division of Animal Sciences University of Missouri Columbia MO 65211 USA

Laboratory of Reproductive Biology Institute of Biotechnology of the Czech Academy of Sciences BIOCEV Prumyslova 595 252 50 Vestec Czech Republic

Zobrazit více v PubMed

Brewis I.A., Gadella B.M. Sperm surface proteomics: From protein lists to biological function. Mol. Hum. Reprod. 2010;16:68–79. doi: 10.1093/molehr/gap077. PubMed DOI

Byrne K., Leahy T., McCulloch R., Colgrave M.L., Holland M.K. Comprehensive mapping of the bull sperm surface proteome. Proteomics. 2012;12:3559–3579. doi: 10.1002/pmic.201200133. PubMed DOI

Kasvandik S., Sillaste G., Velthut-Meikas A., Mikelsaar A.V., Hallap T., Padrik P., Tenson T., Jaakma U., Koks S., Salumets A. Bovine sperm plasma membrane proteomics through biotinylation and subcellular enrichment. Proteomics. 2015;15:1906–1920. doi: 10.1002/pmic.201400297. PubMed DOI

Rickard J.P., de Graaf S.P. Sperm surface changes and their consequences for sperm transit through the female reproductive tract. Theriogenology. 2020 doi: 10.1016/j.theriogenology.2020.02.018. PubMed DOI

Yanagimachi R. Mammalian fertilization. In: Knobil E., Neill J.D., editors. The Physiology of Reproduction. Volume 1. Raven Press; New York, NY, USA: 1994. pp. 189–317.

Gadella B.M., Boerke A. An update on post-ejaculatory remodeling of the sperm surface before mammalian fertilization. Theriogenology. 2016;85:113–124. doi: 10.1016/j.theriogenology.2015.07.018. PubMed DOI

Clark G.F. A role for carbohydrate recognition in mammalian sperm-egg binding. Biochem. Biophys. Res. Commun. 2014;450:1195–1203. doi: 10.1016/j.bbrc.2014.06.051. PubMed DOI

Wassarman P.M. Contribution of mouse egg zona pellucida glycoproteins to gamete recognition during fertilization. J. Cell. Physiol. 2005;204:388–391. doi: 10.1002/jcp.20389. PubMed DOI

Rosano G., Caille A.M., Gallardo-Rios M., Munuce M.J. D-Mannose-binding sites are putative sperm determinants of human oocyte recognition and fertilization. Reprod. Biomed. Online. 2007;15:182–190. doi: 10.1016/S1472-6483(10)60707-9. PubMed DOI

Sinowatz F., Wessa E., Neumüller C., Palma G. On the species specificity of sperm binding and sperm penetration of the zona pellucida. Reprod. Domest. Anim. 2003;38:141–146. doi: 10.1046/j.1439-0531.2003.00401.x. PubMed DOI

Topfer-Petersen E., Ekhlasi-Hundrieser M., Tsolova M. Glycobiology of fertilization in the pig. Int. J. Dev. Biol. 2008;52:717–736. doi: 10.1387/ijdb.072536et. PubMed DOI

Takahashi K., Kikuchi K., Uchida Y., Kanai-Kitayama S., Suzuki R., Sato R., Toma K., Geshi M., Akagi S., Nakano M., et al. Binding of Sperm to the Zona Pellucida Mediated by Sperm Carbohydrate-Binding Proteins is not Species-Specific in Vitro between Pigs and Cattle. Biomolecules. 2013;3:85–107. doi: 10.3390/biom3010085. PubMed DOI PMC

Wassarman P.M., Litscher E.S. The mouse egg’s zona pellucida. In: Litscher E.S., Wassarman P.M., editors. Current Topics in Developmental Biology. Volume 130. Academic Press; Cambridge, MA, USA: 2018. pp. 331–356. PubMed

Evans J.P. Preventing polyspermy in mammalian eggs-Contributions of the membrane block and other mechanisms. Mol. Reprod. Dev. 2020;87:341–349. doi: 10.1002/mrd.23331. PubMed DOI

Fahrenkamp E., Algarra B., Jovine L. Mammalian egg coat modifications and the block to polyspermy. Mol. Reprod. Dev. 2020;87:326–340. doi: 10.1002/mrd.23320. PubMed DOI PMC

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 Seq. 1994;4:361–393. doi: 10.3109/10425179409010186. PubMed DOI

Spargo S.C., Hope R.M. Evolution and nomenclature of the zona pellucida gene family. Biol. Reprod. 2003;68:358–362. doi: 10.1095/biolreprod.102.008086. PubMed DOI

Goudet G., Mugnier S., Callebaut I., Monget P. Phylogenetic analysis and identification of pseudogenes reveal a progressive loss of zona pellucida genes during evolution of vertebrates. Biol. Reprod. 2008;78:796–806. doi: 10.1095/biolreprod.107.064568. PubMed DOI

Smith J., Paton I.R., Hughes D.C., Burt D.W. Isolation and mapping the chicken zona pellucida genes: An insight into the evolution of orthologous genes in different species. Mol. Reprod. Dev. 2005;70:133–145. doi: 10.1002/mrd.20197. PubMed DOI

Gupta S.K. The human egg’s zona pellucida. In: Litscher E.S., Wassarman P.M., editors. Current Topics in Developmental Biology. Volume 130. Academic Press; Cambridge, MA, USA: 2018. pp. 379–411. PubMed

Bokhove M., Jovine L. Structure of Zona Pellucida Module Proteins. Curr. Top. Dev. Biol. 2018;130:413–442. doi: 10.1016/bs.ctdb.2018.02.007. PubMed DOI

Conner S.J., Lefievre L., Hughes D.C., Barratt C.L. Cracking the egg: Increased complexity in the zona pellucida. Hum. Reprod. 2005;20:1148–1152. doi: 10.1093/humrep/deh835. PubMed DOI

Greve J.M., Wassarman P.M. Mouse egg extracellular coat is a matrix of interconnected filaments possessing a structural repeat. J. Mol. Biol. 1985;181:253–264. doi: 10.1016/0022-2836(85)90089-0. PubMed DOI

Hughes D.C., Barratt C.L. Identification of the true human orthologue of the mouse Zp1 gene: Evidence for greater complexity in the mammalian zona pellucida? Biochim. Biophys. Acta (BBA) Gene Struct. Expr. 1999;1447:303–306. doi: 10.1016/S0167-4781(99)00181-5. PubMed DOI

Wassarman P.M. Zona pellucida glycoproteins. Annu. Rev. Biochem. 1988;57:415–442. doi: 10.1146/annurev.bi.57.070188.002215. PubMed DOI

Chiu P.C., Wong B.S., Lee C.L., Pang R.T., Lee K.F., Sumitro S.B., Gupta S.K., Yeung W.S. Native human zona pellucida glycoproteins: Purification and binding properties. Hum. Reprod. 2008;23:1385–1393. doi: 10.1093/humrep/den047. PubMed DOI

Gupta S.K., Bhandari B., Shrestha A., Biswal B.K., Palaniappan C., Malhotra S.S., Gupta N. Mammalian zona pellucida glycoproteins: Structure and function during fertilization. Cell Tissue Res. 2012;349:665–678. doi: 10.1007/s00441-011-1319-y. PubMed DOI

Lefièvre L., Conner S.J., Salpekar A., Olufowobi O., Ashton P., Pavlovic B., Lenton W., Afnan M., Brewis I.A., Monk M., et al. Four zona pellucida glycoproteins are expressed in the human. Hum. Reprod. 2004;19:1580–1586. doi: 10.1093/humrep/deh301. PubMed DOI

Nishimura K., Dioguardi E., Nishio S., Villa A., Han L., Matsuda T., Jovine L. Molecular basis of egg coat cross-linking sheds light on ZP1-associated female infertility. Nat. Commun. 2019;10:3086. doi: 10.1038/s41467-019-10931-5. PubMed DOI PMC

Hasegawa A., Koyama K., Okazaki Y., Sugimoto M., Isojima S. Amino acid sequence of a porcine zona pellucida glycoprotein ZP4 determined by peptide mapping and cDNA cloning. J. Reprod. Fertil. 1994;100:245–255. doi: 10.1530/jrf.0.1000245. PubMed DOI

Hedrick J.L., Wardrip N.J. Isolation of the zona pellucida and purification of its glycoprotein families from pig oocytes. Anal. Biochem. 1986;157:63–70. doi: 10.1016/0003-2697(86)90196-X. PubMed DOI

Hedrick J.L., Wardrip N.J. On the macromolecular composition of the zona pellucida from porcine oocytes. Dev. Biol. 1987;121:478–488. doi: 10.1016/0012-1606(87)90184-9. PubMed DOI

Nakano M., Hatanaka Y., Sawai T., Kobayashi N., Tobita T. Fractionation of glycoproteins from porcine zonae pellucidae into three families by high-performance liquid chromatography. Biochem. Int. 1987;14:417–423. PubMed

Nakano M., Yonezawa N., Hatanaka Y., Noguchi S. Structure and function of the N-linked carbohydrate chains of pig zona pellucida glycoproteins. J. Reprod. Fertil. Suppl. 1996;50:25–34. PubMed

Topfer-Petersen E., Mann K., Calvete J.J. Identification of porcine oocyte 55 kDa alpha and beta proteins within the zona pellucida glycoprotein families indicates that oocyte sperm receptor activity is associated with different zone pellucida proteins in different mammalian species. Biol. Chem. 1993;374:411–417. PubMed

Wardrip N.J., Hedrick J.L. Pig zona pellucida 25K and 65K glycoproteins are derived from Hydrolysis and reduction of the 90K family. J. Cell Biol. 1985;101:378a.

Yurewicz E.C., Pack B.A., Sacco A.G. Isolation, composition, and biological activity of sugar chains of porcine oocyte zona pellucida 55K glycoproteins. Mol. Reprod. Dev. 1991;30:126–134. doi: 10.1002/mrd.1080300209. PubMed DOI

Yurewicz E.C., Sacco A.G., Subramanian M.G. Structural characterization of the Mr = 55,000 antigen (ZP3) of porcine oocyte zona pellucida. Purification and characterization of alpha- and beta-glycoproteins following digestion of lactosaminoglycan with endo-beta-galactosidase. J. Biol. Chem. 1987;262:564–571. doi: 10.1016/S0021-9258(19)75820-7. PubMed DOI

Noguchi S., Yonezawa N., Katsumata T., Hashizume K., Kuwayama M., Hamano S., Watanabe S., Nakano M. Characterization of the zona pellucida glycoproteins from bovine ovarian and fertilized eggs. Biochim. Biophys. Acta (BBA) Gene Struct. Expr. 1994;1201:7–14. doi: 10.1016/0304-4165(94)90143-0. PubMed DOI

Yonezawa N., Fukui N., Kuno M., Shinoda M., Goko S., Mitsui S., Nakano M. Molecular cloning of bovine zona pellucida glycoproteins ZPA and ZPB and analysis for sperm-binding component of the zona. Eur. J. Biochem. 2001;268:3587–3594. doi: 10.1046/j.1432-1327.2001.02269.x. PubMed DOI

Yonezawa N., Kanai S., Nakano M. Structural significance of N-glycans of the zona pellucida on species-selective recognition of spermatozoa between pig and cattle. Soc. Reprod. Fertil. Suppl. 2007;63:217–228. PubMed

Abou-Haila A., Bendahmane M., Tulsiani D.R. Significance of egg’s zona pellucida glycoproteins in sperm-egg interaction and fertilization. Minerva Ginecol. 2014;66:409–419. PubMed

Yonezawa N. Posttranslational modifications of zona pellucida proteins. Adv. Exp. Med. Biol. 2014;759:111–140. doi: 10.1007/978-1-4939-0817-2_6. PubMed DOI

Yonezawa N. Involvement of Carbohydrate Residues of the Zona Pellucida in In Vitro Sperm Recognition in Pigs and Cattle. In: Sawada H., Inoue N., Iwano M., editors. Sexual Reproduction in Animals and Plants. Springer; Tokyo, Japan: 2014. pp. 409–415.

Topfer-Petersen E. Carbohydrate-based interactions on the route of a spermatozoon to fertilization. Hum. Reprod. Update. 1999;5:314–329. doi: 10.1093/humupd/5.4.314. PubMed DOI

Wassarman P.M., Litscher E.S. Towards the molecular basis of sperm and egg interaction during mammalian fertilization. Cells Tissues Organs. 2001;168:36–45. doi: 10.1159/000016804. PubMed DOI

Hoodbhoy T., Dean J. Insights into the molecular basis of sperm-egg recognition in mammals. Reproduction. 2004;127:417–422. doi: 10.1530/rep.1.00181. PubMed DOI

Shalgi R., Maymon R., Bar-Shira B., Amihai D., Skutelsky E. Distribution of lectin receptors sites in the zona pellucida of follicular and ovulated rat oocytes. Mol. Reprod. Dev. 1991;29:365–372. doi: 10.1002/mrd.1080290408. PubMed DOI

Maymon B.B., Maymon R., Ben-Nun I., Ghetler Y., Shalgi R., Skutelsky E. Distribution of carbohydrates in the zona pellucida of human oocytes. J. Reprod. Fertil. 1994;102:81–86. doi: 10.1530/jrf.0.1020081. PubMed DOI

Parillo F., Stradaioli G., Dall’Aglio C., Verini-Supplizi A. Characterization of the complex carbohydrates in the zona pellucida of mammalian oocytes using lectin histochemistry. Vet. Res. Commun. 1996;20:225–236. doi: 10.1007/BF00366920. PubMed DOI

Katsumata T., Noguchi S., Yonezawa N., Tanokura M., Nakano M. Structural characterization of the N-linked carbohydrate chains of the zona pellucida glycoproteins from bovine ovarian and fertilized eggs. Eur. J. Biochem. 1996;240:448–453. doi: 10.1111/j.1432-1033.1996.0448h.x. PubMed DOI

Lucas H., Bercegeay S., Le Pendu J., Jean M., Mirallie S., Barriere P. A fucose-containing epitope potentially involved in gamete interaction on the human zona pellucida. Hum. Reprod. 1994;9:1532–1538. doi: 10.1093/oxfordjournals.humrep.a138744. PubMed DOI

Noguchi S., Hatanaka Y., Tobita T., Nakano M. Structural analysis of the N-linked carbohydrate chains of the 55-kDa glycoprotein family (PZP3) from porcine zona pellucida. Eur. J. Biochem. 1992;204:1089–1100. doi: 10.1111/j.1432-1033.1992.tb16733.x. PubMed DOI

Noguchi S., Nakano M. Structure of the acidic N-linked carbohydrate chains of the 55-kDa glycoprotein family (PZP3) from porcine zona pellucida. Eur. J. Biochem. 1992;209:883–894. doi: 10.1111/j.1432-1033.1992.tb17361.x. PubMed DOI

Mori E., Hedrick J.L., Wardrip N.J., Mori T., Takasaki S. Occurrence of reducing terminal N-acetylglucosamine 3-sulfate and fucosylated outer chains in acidic N-glycans of porcine zona pellucida glycoproteins. Glycoconj. J. 1998;15:447–456. doi: 10.1023/A:1006926801717. PubMed DOI

Töpfer-Petersen E., Petrounkina A.M., Ekhlasi-Hundrieser M. Oocyte-sperm interactions. Anim. Reprod. Sci. 2000;60–61 doi: 10.1016/S0378-4320(00)00128-7. PubMed DOI

Kudo K., Yonezawa N., Katsumata T., Aoki H., Nakano M. Localization of carbohydrate chains of pig sperm ligand in the glycoprotein ZPB of egg zona pellucida. Eur. J. Biochem. 1998;252:492–499. doi: 10.1046/j.1432-1327.1998.2520492.x. PubMed DOI

Easton R.L., Patankar M.S., Lattanzio F.A., Leaven T.H., Morris H.R., Clark G.F., Dell A. Structural analysis of murine zona pellucida glycans. Evidence for the expression of core 2-type O-glycans and the Sd(a) antigen. J. Biol. Chem. 2000;275:7731–7742. doi: 10.1074/jbc.275.11.7731. PubMed DOI

Noguchi S., Nakano M. Structural characterization of the N-linked carbohydrate chains from mouse zona pellucida glycoproteins ZP2 and ZP3. Biochim. Biophys. Acta (BBA) Gene Struct. Expr. 1993;1158:217–226. doi: 10.1016/0304-4165(93)90018-4. PubMed DOI

Dell A., Chalabi S., Easton R.L., Haslam S.M., Sutton-Smith M., Patankar M.S., Lattanzio F., Panico M., Morris H.R., Clark G.F. Murine and human zona pellucida 3 derived from mouse eggs express identical O-glycans. Proc. Natl. Acad. Sci. USA. 2003;100:15631–15636. doi: 10.1073/pnas.2635507100. PubMed DOI PMC

Boja E.S., Hoodbhoy T., Fales H.M., Dean J. Structural characterization of native mouse zona pellucida proteins using mass spectrometry. J. Biol. Chem. 2003;278:34189–34202. doi: 10.1074/jbc.M304026200. PubMed DOI

Jimenez-Movilla M., Aviles M., Gomez-Torres M.J., Fernandez-Colom P.J., Castells M.T., de Juan J., Romeu A., Ballesta J. Carbohydrate analysis of the zona pellucida and cortical granules of human oocytes by means of ultrastructural cytochemistry. Hum. Reprod. 2004;19:1842–1855. doi: 10.1093/humrep/deh311. PubMed DOI

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., et al. Human sperm binding is mediated by the sialyl-Lewis(x) oligosaccharide on the zona pellucida. Science. 2011;333:1761–1764. doi: 10.1126/science.1207438. PubMed DOI

Yonezawa N., Mitsui S., Kudo K., Nakano M. Identification of an N-glycosylated region of pig zona pellucida glycoprotein ZPB that is involved in sperm binding. Eur. J. Biochem. 1997;248:86–92. doi: 10.1111/j.1432-1033.1997.00086.x. PubMed DOI

Nakano M., Yonezawa N. Localization of sperm ligand carbohydrate chains in pig zona pellucida glycoproteins. Cells Tissues Organs. 2001;168:65–75. doi: 10.1159/000016807. PubMed DOI

Von Witzendorff D., Maass K., Pich A., Ebeling S., Kölle S., Kochel C., Ekhlasi-Hundrieser M., Geyer H., Geyer R., Töpfer-Petersen E. Characterization of the acidic N-linked glycans of the zona pellucida of prepuberal pigs by a mass spectrometric approach. Carbohydr. Res. 2009;344:1541–1549. doi: 10.1016/j.carres.2009.05.002. PubMed DOI

Hokke C.H., Damm J.B., Penninkhof B., Aitken R.J., Kamerling J.P., Vliegenthart J.F. Structure of the O-linked carbohydrate chains of porcine zona pellucida glycoproteins. Eur. J. Biochem. 1994;221:491–512. doi: 10.1111/j.1432-1033.1994.tb18762.x. PubMed DOI

Lay K.M., Nakada T., Tatemoto H. Involvement of N-glycosylation of zona glycoproteins during meiotic maturation in sperm-zona pellucida interactions of porcine denuded oocytes. Anim. Sci. J. 2013;84:8–14. doi: 10.1111/j.1740-0929.2012.01027.x. PubMed DOI

Clark G.F., Zimmerman S., Lafrenz D.E., Yi Y.J., Sutovsky P. Carbohydrate-mediated binding and induction of acrosomal exocytosis in a boar sperm-somatic cell adhesion model. Biol. Reprod. 2010;83:623–634. doi: 10.1095/biolreprod.110.084319. PubMed DOI

Suzuki K., Tatebe N., Kojima S., Hamano A., Orita M., Yonezawa N. The Hinge Region of Bovine Zona Pellucida Glycoprotein ZP3 Is Involved in the Formation of the Sperm-Binding Active ZP3/ZP4 Complex. Biomolecules. 2015;5:3339–3353. doi: 10.3390/biom5043339. PubMed DOI PMC

Ikeda K., Yonezawa N., Naoi K., Katsumata T., Hamano S., Nakano M. Localization of N-linked carbohydrate chains in glycoprotein ZPA of the bovine egg zona pellucida. Eur. J. Biochem. 2002;269:4257–4266. doi: 10.1046/j.1432-1033.2002.03111.x. PubMed DOI

Florman H.M., Fissore R.A. Fertilization in Mammals. In: Plant T.M., Zeleznik A.J., editors. Knobil and Neill’s Physiology of Reproduction. 4th ed. Volume 1. Academic Press; New York, NY, USA: 2015. pp. 149–196.

Georgadaki K., Khoury N., Spandidos D.A., Zoumpourlis V. The molecular basis of fertilization (Review) Int. J. Mol. Med. 2016;38:979–986. doi: 10.3892/ijmm.2016.2723. PubMed DOI PMC

Okabe M. Sperm-egg interaction and fertilization: Past, present, and future. Biol. Reprod. 2018;99:134–146. doi: 10.1093/biolre/ioy028. PubMed DOI

Zigo M., Manaskova-Postlerova P., Zuidema D., Kerns K., Jonakova V., Tumova L., Bubenickova F., Sutovsky P. Porcine model for the study of sperm capacitation, fertilization and male fertility. Cell Tissue Res. 2020;380:237–262. doi: 10.1007/s00441-020-03181-1. PubMed DOI

Tanphaichitr N., Carmona E., Bou Khalil M., Xu H., Berger T., Gerton G.L. New insights into sperm-zona pellucida interaction: Involvement of sperm lipid rafts. Front. Biosci. 2007;12:1748–1766. doi: 10.2741/2186. PubMed DOI

Fraser L.R. Minimum and maximum extracellular Ca2+ requirements during mouse sperm capacitation and fertilization in vitro. J. Reprod. Fertil. 1987;81:77–89. doi: 10.1530/jrf.0.0810077. PubMed DOI

Kim K.S., Gerton G.L. Differential release of soluble and matrix components: Evidence for intermediate states of secretion during spontaneous acrosomal exocytosis in mouse sperm. Dev. Biol. 2003;264:141–152. doi: 10.1016/j.ydbio.2003.08.006. PubMed DOI

Wassarman P.M. Mammalian fertilization: The strange case of sperm protein 56. Bioessays. 2009;31:153–158. doi: 10.1002/bies.200800152. PubMed DOI

Tanphaichitr N., Kongmanas K., Kruevaisayawan H., Saewu A., Sugeng C., Fernandes J., Souda P., Angel J.B., Faull K.F., Aitken R.J., et al. Remodeling of the plasma membrane in preparation for sperm-egg recognition: Roles of acrosomal proteins. Asian J. Androl. 2015;17:574–582. doi: 10.4103/1008-682X.152817. PubMed DOI PMC

López-Salguero J.B., Fierro R., Michalski J.C., Jiménez-Morales I., Lefebvre T., Mondragón-Payne O., Baldini S.F., Vercoutter-Edouart A.S., González-Márquez H. Identification of lipid raft glycoproteins obtained from boar spermatozoa. Glycoconj. J. 2020;37:499–509. doi: 10.1007/s10719-020-09924-0. PubMed DOI

Bleil J.D., Wassarman P.M. Mammalian sperm-egg interaction: Identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm. Cell. 1980;20:873–882. doi: 10.1016/0092-8674(80)90334-7. PubMed DOI

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. doi: 10.1016/0012-1606(83)90032-5. PubMed DOI

Beebe S.J., Leyton L., Burks D., Ishikawa M., Fuerst T., Dean J., Saling P. Recombinant mouse ZP3 inhibits sperm binding and induces the acrosome reaction. Dev. Biol. 1992;151:48–54. doi: 10.1016/0012-1606(92)90212-Y. PubMed DOI

Bleil J.D., Wassarman P.M. 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. 1988;85:6778–6782. doi: 10.1073/pnas.85.18.6778. PubMed DOI PMC

Litscher E.S., Wassarman P.M. Characterization of mouse ZP3-derived glycopeptide, gp55, that exhibits sperm receptor and acrosome reaction-inducing activity in vitro. Biochemistry. 1996;35:3980–3985. doi: 10.1021/bi952722m. PubMed DOI

Kinloch R.A., Sakai Y., Wassarman P.M. Mapping the mouse ZP3 combining site for sperm by exon swapping and site-directed mutagenesis. Proc. Natl. Acad. Sci. USA. 1995;92:263–267. doi: 10.1073/pnas.92.1.263. PubMed DOI PMC

Thall A.D., Malý P., Lowe J.B. Oocyte Gal alpha 1,3Gal epitopes implicated in sperm adhesion to the zona pellucida glycoprotein ZP3 are not required for fertilization in the mouse. J. Biol. Chem. 1995;270:21437–21440. doi: 10.1074/jbc.270.37.21437. PubMed DOI

Litscher E.S., Juntunen K., Seppo A., Penttilä L., Niemelä R., Renkonen O., Wassarman P.M. Oligosaccharide constructs with defined structures that inhibit binding of mouse sperm to unfertilized eggs in vitro. Biochemistry. 1995;34:4662–4669. doi: 10.1021/bi00014a020. PubMed DOI

Mori E., Mori T., Takasaki S. Binding of mouse sperm to beta-galactose residues on egg zona pellucida and asialofetuin-coupled beads. Biochem. Biophys. Res. Commun. 1997;238:95–99. doi: 10.1006/bbrc.1997.7249. PubMed DOI

Johnston D.S., Wright W.W., Shaper J.H., Hokke C.H., Van den Eijnden D.H., Joziasse D.H. Murine sperm-zona binding, a fucosyl residue is required for a high affinity sperm-binding ligand. A second site on sperm binds a nonfucosylated, beta-galactosyl-capped oligosaccharide. J. Biol. Chem. 1998;273:1888–1895. doi: 10.1074/jbc.273.4.1888. PubMed DOI

Bleil J.D., Greve J.M., 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. doi: 10.1016/0012-1606(88)90299-0. PubMed DOI

Avella M.A., Baibakov B., Dean J. A single domain of the ZP2 zona pellucida protein mediates gamete recognition in mice and humans. J. Cell Biol. 2014;205:801–809. doi: 10.1083/jcb.201404025. PubMed DOI PMC

Saling P.M., Sowinski J., Storey B.T. An ultrastructural study of epididymal mouse spermatozoa binding to zonae pellucidae in vitro: Sequential relationship to the acrosome reaction. J. Exp. Zool. 1979;209:229–238. doi: 10.1002/jez.1402090205. PubMed DOI

Saling P.M., Storey B.T. Mouse gamete interactions during fertilization in vitro. Chlortetracycline as a fluorescent probe for the mouse sperm acrosome reaction. J. Cell Biol. 1979;83:544–555. doi: 10.1083/jcb.83.3.544. PubMed DOI PMC

Baibakov B., Gauthier L., Talbot P., Rankin T.L., Dean J. Sperm binding to the zona pellucida is not sufficient to induce acrosome exocytosis. Development. 2007;134:933–943. doi: 10.1242/dev.02752. PubMed DOI

Jin M., Fujiwara E., Kakiuchi Y., Okabe M., Satouh Y., Baba S.A., Chiba K., Hirohashi N. Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization. Proc. Natl. Acad. Sci. USA. 2011;108:4892–4896. doi: 10.1073/pnas.1018202108. PubMed DOI PMC

Inoue N., Satouh Y., Ikawa M., Okabe M., Yanagimachi R. Acrosome-reacted mouse spermatozoa recovered from the perivitelline space can fertilize other eggs. Proc. Natl. Acad. Sci. USA. 2011;108:20008–20011. doi: 10.1073/pnas.1116965108. PubMed DOI PMC

Buffone M.G., Hirohashi N., Gerton G.L. Unresolved questions concerning mammalian sperm acrosomal exocytosis. Biol. Reprod. 2014;90:112. doi: 10.1095/biolreprod.114.117911. PubMed DOI PMC

Foster J.A., Gerton G.L. The Acrosomal Matrix. Adv. Anat. Embryol. Cell Biol. 2016;220:15–33. doi: 10.1007/978-3-319-30567-7_2. PubMed DOI PMC

Hirohashi N., Yanagimachi R. Sperm acrosome reaction: Its site and role in fertilization. Biol. Reprod. 2018;99:127–133. doi: 10.1093/biolre/ioy045. PubMed DOI

Clark G.F., Dell A. Molecular models for murine sperm-egg binding. J. Biol. Chem. 2006;281:13853–13856. doi: 10.1074/jbc.R600001200. PubMed DOI

Clark G.F. Molecular models for mouse sperm-oocyte binding. Glycobiology. 2011;21:3–5. doi: 10.1093/glycob/cwq159. PubMed DOI

Chakravarty S., Kadunganattil S., Bansal P., Sharma R.K., Gupta S.K. Relevance of glycosylation of human zona pellucida glycoproteins for their binding to capacitated human spermatozoa and subsequent induction of acrosomal exocytosis. Mol. Reprod. Dev. 2008;75:75–88. doi: 10.1002/mrd.20726. PubMed DOI

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. doi: 10.1093/molehr/4.4.318. PubMed DOI

Baibakov B., Boggs N.A., Yauger B., Baibakov G., Dean J. Human sperm bind to the N-terminal domain of ZP2 in humanized zonae pellucidae in transgenic mice. J. Cell Biol. 2012;197:897–905. doi: 10.1083/jcb.201203062. PubMed DOI PMC

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. doi: 10.1074/jbc.273.13.7488. PubMed DOI

Yonezawa N., Kudo K., Terauchi H., Kanai S., Yoda N., Tanokura M., Ito K., Miura K., Katsumata T., Nakano M. Recombinant porcine zona pellucida glycoproteins expressed in Sf9 cells bind to bovine sperm but not to porcine sperm. J. Biol. Chem. 2005;280:20189–20196. doi: 10.1074/jbc.M414242200. PubMed DOI

Yonezawa N., Amari S., Takahashi K., Ikeda K., Imai F.L., Kanai S., Kikuchi K., Nakano M. 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. 2005;70:222–227. doi: 10.1002/mrd.20195. PubMed DOI

Sutton-Smith M., Wong N.K., Khoo K.H., Wu S.W., Yu S.Y., Patankar M.S., Easton R., Lattanzio F.A., Morris H.R., Dell A., et al. Analysis of protein-linked glycosylation in a sperm-somatic cell adhesion system. Glycobiology. 2007;17:553–567. doi: 10.1093/glycob/cwm025. PubMed DOI

Berger T., Turner K.O., Meizel S., Hedrick J.L. Zona pellucida-induced acrosome reaction in boar sperm. Biol. Reprod. 1989;40:525–530. doi: 10.1095/biolreprod40.3.525. PubMed DOI

Mattioli M., Lucidi P., Barboni B. Expanded cumuli induce acrosome reaction in boar sperm. Mol. Reprod. Dev. 1998;51:445–453. doi: 10.1002/(SICI)1098-2795(199812)51:4<445::AID-MRD12>3.0.CO;2-L. PubMed DOI

Kanai S., Yonezawa N., Ishii Y., Tanokura M., Nakano M. Recombinant bovine zona pellucida glycoproteins ZP3 and ZP4 coexpressed in Sf9 cells form a sperm-binding active hetero-complex. FEBS J. 2007;274:5390–5405. doi: 10.1111/j.1742-4658.2007.06065.x. PubMed DOI

Amari S., Yonezawa N., Mitsui S., Katsumata T., Hamano S., Kuwayama M., Hashimoto Y., Suzuki A., Takeda Y., Nakano M. Essential role of the nonreducing terminal alpha-mannosyl residues of the N-linked carbohydrate chain of bovine zona pellucida glycoproteins in sperm-egg binding. Mol. Reprod. Dev. 2001;59:221–226. doi: 10.1002/mrd.1026. PubMed DOI

Velásquez J.G., Canovas S., Barajas P., Marcos J., Jiménez-Movilla M., Gallego R.G., Ballesta J., Avilés M., Coy P. Role of sialic acid in bovine sperm-zona pellucida binding. Mol. Reprod. Dev. 2007;74:617–628. doi: 10.1002/mrd.20619. PubMed DOI

Florman H.M., First N.L. 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. 1988;128:453–463. doi: 10.1016/0012-1606(88)90307-7. PubMed DOI

Herz Z., Northey D., Lawyer M., First N.L. Acrosome reaction of bovine spermatozoa in vivo: Sites and effects of stages of the estrous cycle. Biol. Reprod. 1985;32:1163–1168. doi: 10.1095/biolreprod32.5.1163. PubMed DOI

Didion B.A., Graves C.N. In vivo capacitation and acrosome reaction of bovine sperm in estrous and diestrous cows. J. Anim. Sci. 1986;62:1029–1033. doi: 10.2527/jas1986.6241029x. PubMed DOI

Shur B.D., Hall N.G. A role for mouse sperm surface galactosyltransferase in sperm binding to the egg zona pellucida. J. Cell Biol. 1982;95:574–579. doi: 10.1083/jcb.95.2.574. PubMed DOI PMC

Scully N.F., Shaper J.H., Shur B.D. Spatial and temporal expression of cell surface galactosyltransferase during mouse spermatogenesis and epididymal maturation. Dev. Biol. 1987;124:111–124. doi: 10.1016/0012-1606(87)90464-7. PubMed DOI

Miller D.J., Macek M.B., Shur B.D. Complementarity between sperm surface beta-1,4-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding. Nature. 1992;357:589–593. doi: 10.1038/357589a0. PubMed DOI

Shur B.D. Glycosyltransferases as cell adhesion molecules. Curr. Opin. Cell Biol. 1993;5:854–863. doi: 10.1016/0955-0674(93)90035-O. PubMed DOI

Gong X., Dubois D.H., Miller D.J., Shur B.D. Activation of a G protein complex by aggregation of beta-1,4-galactosyltransferase on the surface of sperm. Science. 1995;269:1718–1721. doi: 10.1126/science.7569899. PubMed DOI

Shi X., Amindari S., Paruchuru K., Skalla D., Burkin H., Shur B.D., Miller D.J. Cell surface beta-1,4-galactosyltransferase-I activates G protein-dependent exocytotic signaling. Development. 2001;128:645–654. PubMed

Huszar G., Sbracia M., Vigue L., Miller D.J., Shur B.D. Sperm plasma membrane remodeling during spermiogenetic maturation in men: Relationship among plasma membrane beta 1,4-galactosyltransferase, cytoplasmic creatine phosphokinase, and creatine phosphokinase isoform ratios. Biol. Reprod. 1997;56:1020–1024. doi: 10.1095/biolreprod56.4.1020. PubMed DOI

Larson J.L., Miller D.J. Sperm from a variety of mammalian species express beta1,4-galactosyltransferase on their surface. Biol. Reprod. 1997;57:442–453. doi: 10.1095/biolreprod57.2.442. PubMed DOI

Rebeiz M., Miller D.J. Porcine sperm surface beta1,4galactosyltransferase binds to the zona pellucida but is not necessary or sufficient to mediate sperm-zona pellucida binding. Mol. Reprod. Dev. 1999;54:379–387. doi: 10.1002/(SICI)1098-2795(199912)54:4<379::AID-MRD8>3.0.CO;2-8. PubMed DOI

Tengowski M.W., Wassler M.J., Shur B.D., Schatten G. Subcellular localization of beta1,4-galactosyltransferase on bull sperm and its function during sperm-egg interactions. Mol. Reprod. Dev. 2001;58:236–244. doi: 10.1002/1098-2795(200102)58:2<236::AID-MRD13>3.0.CO;2-0. PubMed DOI

Kallajoki M., Parvinen M., Suominen J.J. Expression of acrosin during mouse spermatogenesis: A biochemical and immunocytochemical analysis by a monoclonal antibody C 11 H. Biol. Reprod. 1986;35:157–165. doi: 10.1095/biolreprod35.1.157. PubMed DOI

Kashiwabara S., Baba T., Takada M., Watanabe K., Yano Y., Arai Y. Primary structure of mouse proacrosin deduced from the cDNA sequence and its gene expression during spermatogenesis. J. Biochem. 1990;108:785–791. doi: 10.1093/oxfordjournals.jbchem.a123281. PubMed DOI

Klemm U., Maier W.M., Tsaousidou S., Adham I.M., Willison K., Engel W. Mouse preproacrosin: cDNA sequence, primary structure and postmeiotic expression in spermatogenesis. Differentiation. 1990;42:160–166. doi: 10.1111/j.1432-0436.1990.tb00757.x. PubMed DOI

Kremling H., Keime S., Wilhelm K., Adham I.M., Hameister H., Engel W. Mouse proacrosin gene: Nucleotide sequence, diploid expression, and chromosomal localization. Genomics. 1991;11:828–834. doi: 10.1016/0888-7543(91)90005-Y. PubMed DOI

Watanabe K., Baba T., Kashiwabara S., Okamoto A., Arai Y. Structure and organization of the mouse acrosin gene. J. Biochem. 1991;109:828–833. doi: 10.1093/oxfordjournals.jbchem.a123466. PubMed DOI

Gilboa E., Elkana Y., Rigbi M. Purification and properties of human acrosin. Eur. J. Biochem. 1973;39:85–92. doi: 10.1111/j.1432-1033.1973.tb03106.x. PubMed DOI

Schleuning W.D., Hell R., Fritz H. Multiple forms of human acrosin: Isolation and properties. Hoppe-Seyler’s Z. Physiol. Chem. 1976;357:855–865. doi: 10.1515/bchm2.1976.357.1.855. PubMed DOI

Anderson R.A., Jr., Beyler S.A., Mack S.R., Zaneveld L.J. Characterization of a high-molecular-weight form of human acrosin. Comparison with human pancreatic trypsin. Biochem. J. 1981;199:307–316. doi: 10.1042/bj1990307. PubMed DOI PMC

Tesarik J., Drahorad J., Peknicova J. Subcellular immunochemical localization of acrosin in human spermatozoa during the acrosome reaction and zona pellucida penetration. Fertil. Steril. 1988;50:133–141. doi: 10.1016/S0015-0282(16)60021-3. PubMed DOI

Kobayashi T., Matsuda Y., Oshio S., Kaneko S., Nozawa S., Mhori H., Akihama S., Fujimoto Y. Human acrosin: Purification and some properties. Arch. Androl. 1991;27:9–16. doi: 10.3109/01485019108987646. PubMed DOI

Moreno R.D., Sepúlveda M.S., de Ioannes A., Barros C. The polysulphate binding domain of human proacrosin/acrosin is involved in both the enzyme activation and spermatozoa-zona pellucida interaction. Zygote. 1998;6:75–83. doi: 10.1017/S0967199400005104. PubMed DOI

Furlong L.I., Hellman U., Krimer A., Tezón J.G., Charreau E.H., Vazquez-Levin M.H. Expression of human proacrosin in Escherichia coli and binding to zona pellucida. Biol. Reprod. 2000;62:606–615. doi: 10.1095/biolreprod62.3.606. PubMed DOI

Furlong L.I., Veaute C., Vazquez-Levin M.H. Binding of recombinant human proacrosin/acrosin to zona pellucida glycoproteins. II. Participation of mannose residues in the interaction. Fertil. Steril. 2005;83:1791–1796. doi: 10.1016/j.fertnstert.2004.12.043. PubMed DOI

Schill W.B. Immunofluorescent localization of acrosin in spermatozoa by boar acrosin antibodies. Naturwissenschaften. 1975;62:540–541. doi: 10.1007/BF00609082. PubMed DOI

Jones R., Brown C.R. Identification of a zona-binding protein from boar spermatozoa as proacrosin. Exp. Cell Res. 1987;171:503–508. doi: 10.1016/0014-4827(87)90182-0. PubMed DOI

Jones R., Brown C.R., Lancaster R.T. Carbohydrate-binding properties of boar sperm proacrosin and assessment of its role in sperm-egg recognition and adhesion during fertilization. Development. 1988;102:781–792.

Baba T., Kashiwabara S., Watanabe K., Itoh H., Michikawa Y., Kimura K., Takada M., Fukamizu A., Arai Y. Activation and maturation mechanisms of boar acrosin zymogen based on the deduced primary structure. J. Biol. Chem. 1989;264:11920–11927. doi: 10.1016/S0021-9258(18)80154-5. PubMed DOI

Baba T., Michikawa Y., Kawakura K., Arai Y. Activation of boar proacrosin is effected by processing at both N- and C-terminal portions of the zymogen molecule. FEBS Lett. 1989;244:132–136. doi: 10.1016/0014-5793(89)81178-0. PubMed DOI

Jones R. Interaction of zona pellucida glycoproteins, sulphated carbohydrates and synthetic polymers with proacrosin, the putative egg-binding protein from mammalian spermatozoa. Development. 1991;111:1155–1163. PubMed

Puigmulé M., Fàbrega A., Yeste M., Bonet S., Pinart E. Study of the proacrosin-acrosin system in epididymal, ejaculated and in vitro capacitated boar spermatozoa. Reprod. Fertil. Dev. 2011;23:837–845. doi: 10.1071/RD10345. PubMed DOI

Zigo M., Dorosh A., Pohlova A., Jonakova V., Sulc M., Manaskova-Postlerova P. Panel of monoclonal antibodies to sperm surface proteins as a tool for monitoring localization and identification of sperm-zona pellucida receptors. Cell Tissue Res. 2015;359:895–908. doi: 10.1007/s00441-014-2072-9. PubMed DOI

Garner D.L., Easton M.P., Munson M.E., Doane M.A. Immunofluorescent localization of bovine acrosin. J. Exp. Zool. 1975;191:127–131. doi: 10.1002/jez.1401910113. PubMed DOI

Mansouri A., Phi-van L., Geithe H.P., Engel W. Proacrosin/acrosin activity during spermiohistogenesis of the bull. Differentiation. 1983;24:149–152. doi: 10.1111/j.1432-0436.1983.tb01315.x. PubMed DOI

De los Reyes M., Barros C. Immunolocalization of proacrosin/acrosin in bovine sperm and sperm penetration through the zona pellucida. Anim. Reprod. Sci. 2000;58:215–228. doi: 10.1016/S0378-4320(99)00077-9. PubMed DOI

Gao Z., Garbers D.L. Species diversity in the structure of zonadhesin, a sperm-specific membrane protein containing multiple cell adhesion molecule-like domains. J. Biol. Chem. 1998;273:3415–3421. doi: 10.1074/jbc.273.6.3415. PubMed DOI

Tardif S., Wilson M.D., Wagner R., Hunt P., Gertsenstein M., Nagy A., Lobe C., Koop B.F., Hardy D.M. Zonadhesin is essential for species specificity of sperm adhesion to the egg zona pellucida. J. Biol. Chem. 2010;285:24863–24870. doi: 10.1074/jbc.M110.123125. PubMed DOI PMC

Gao Z., Harumi T., Garbers D.L. Chromosome localization of the mouse zonadhesin gene and the human zonadhesin gene (ZAN) Genomics. 1997;41:119–122. doi: 10.1006/geno.1997.4620. PubMed DOI

Wilson M.D., Riemer C., Martindale D.W., Schnupf P., Boright A.P., Cheung T.L., Hardy D.M., Schwartz S., Scherer S.W., Tsui L.C., et al. Comparative analysis of the gene-dense ACHE/TFR2 region on human chromosome 7q22 with the orthologous region on mouse chromosome 5. Nucleic Acids Res. 2001;29:1352–1365. doi: 10.1093/nar/29.6.1352. PubMed DOI PMC

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. doi: 10.1074/jbc.270.44.26025. PubMed DOI

Bi M., Hickox J.R., Winfrey V.P., Olson G.E., Hardy D.M. Processing, localization and binding activity of zonadhesin suggest a function in sperm adhesion to the zona pellucida during exocytosis of the acrosome. Biochem. J. 2003;375:477–488. doi: 10.1042/bj20030753. PubMed DOI PMC

Bi M. Ph.D. Thesis. Texas Tech University; Lubbock, TX, USA: 2002. Biochemical and Functional Characterization of Zonadhesin: A Sperm Protein Potentially Mediating Species-Specific Sperm-Egg Adhesion during Fertilization.

Tanphaichitr N., Smith J., Mongkolsirikieart S., Gradil C., Lingwood C.A. Role of a gamete-specific sulfoglycolipid immobilizing protein on mouse sperm-egg binding. Dev. Biol. 1993;156:164–175. doi: 10.1006/dbio.1993.1067. PubMed DOI

Moase C.E., Kamolvarin N., Kan F.W., Tanphaichitr N. Localization and role of sulfoglycolipid immobilizing protein 1 on the mouse sperm head. Mol. Reprod. Dev. 1997;48:518–528. doi: 10.1002/(SICI)1098-2795(199712)48:4<518::AID-MRD13>3.0.CO;2-P. PubMed DOI

Tantibhedhyangkul J., Weerachatyanukul W., Carmona E., Xu H., Anupriwan A., Michaud D., Tanphaichitr N. Role of sperm surface arylsulfatase A in mouse sperm-zona pellucida binding. Biol. Reprod. 2002;67:212–219. doi: 10.1095/biolreprod67.1.212. PubMed DOI

Ngernsoungnern A., Weerachatyanukul W., Saewu A., Thitilertdecha S., Sobhon P., Sretarugsa P. Rat sperm AS-A: Subcellular localization in testis and epididymis and surface distribution in epididymal sperm. Cell Tissue Res. 2004;318:353–363. doi: 10.1007/s00441-004-0985-4. PubMed DOI

Redgrove K.A., Nixon B., Baker M.A., Hetherington L., Baker G., Liu D.Y., Aitken R.J. The molecular chaperone HSPA2 plays a key role in regulating the expression of sperm surface receptors that mediate sperm-egg recognition. PLoS ONE. 2012;7:e50851. doi: 10.1371/journal.pone.0050851. PubMed DOI PMC

Bromfield E.G., Aitken R.J., Anderson A.L., McLaughlin E.A., Nixon B. The impact of oxidative stress on chaperone-mediated human sperm-egg interaction. Hum. Reprod. 2015;30:2597–2613. doi: 10.1093/humrep/dev214. PubMed DOI

Carmona E., Weerachatyanukul W., Soboloff T., Fluharty A.L., White D., Promdee L., Ekker M., Berger T., Buhr M., Tanphaichitr N. Arylsulfatase a is present on the pig sperm surface and is involved in sperm-zona pellucida binding. Dev. Biol. 2002;247:182–196. doi: 10.1006/dbio.2002.0690. PubMed DOI

Kelsey K.M., Zigo M., Thompson W.E., Kerns K., Manandhar G., Sutovsky M., Sutovsky P. Reciprocal surface expression of arylsulfatase A and ubiquitin in normal and defective mammalian spermatozoa. Cell Tissue Res. 2020;379:561–576. doi: 10.1007/s00441-019-03144-1. PubMed DOI

Cardullo R.A., Armant D.R., Millette C.F. Characterization of fucosyltransferase activity during mouse spermatogenesis: Evidence for a cell surface fucosyltransferase. Biochemistry. 1989;28:1611–1617. doi: 10.1021/bi00430a028. PubMed DOI

Ram P.A., Cardullo R.A., Millette C.F. Expression and topographical localization of cell surface fucosyltransferase activity during epididymal sperm maturation in the mouse. Gamete Res. 1989;22:321–332. doi: 10.1002/mrd.1120220309. PubMed DOI

Chiu P.C., Chung M.K., Koistinen R., Koistinen H., Seppala M., Ho P.C., Ng E.H., Lee K.F., Yeung W.S. Glycodelin-A interacts with fucosyltransferase on human sperm plasma membrane to inhibit spermatozoa-zona pellucida binding. J. Cell Sci. 2007;120:33–44. doi: 10.1242/jcs.03258. PubMed DOI

Cornwall G.A., Tulsiani D.R., Orgebin-Crist M.C. Inhibition of the mouse sperm surface alpha-D-mannosidase inhibits sperm-egg binding in vitro. Biol. Reprod. 1991;44:913–921. doi: 10.1095/biolreprod44.5.913. PubMed DOI

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. doi: 10.1095/biolreprod42.5.843. PubMed DOI

Tesarik J., Mendoza C., Carreras A. Expression of D-mannose binding sites on human spermatozoa: Comparison of fertile donors and infertile patients. Fertil. Steril. 1991;56:113–118. doi: 10.1016/S0015-0282(16)54428-8. PubMed DOI

Eberspaecher U., Roosterman D., Krätzschmar J., Haendler B., Habenicht U.F., Becker A., Quensel C., Petri T., Schleuning W.D., Donner P. Mouse androgen-dependent epididymal glycoprotein CRISP-1 (DE/AEG): Isolation, biochemical characterization, and expression in recombinant form. Mol. Reprod. Dev. 1995;42:157–172. doi: 10.1002/mrd.1080420205. PubMed DOI

Cohen D.J., Ellerman D.A., Cuasnicu P.S. Mammalian sperm-egg fusion: Evidence that epididymal protein DE plays a role in mouse gamete fusion. Biol. Reprod. 2000;63:462–468. doi: 10.1095/biolreprod63.2.462. PubMed DOI

Busso D., Cohen D.J., Maldera J.A., Dematteis A., Cuasnicu P.S. A novel function for CRISP1 in rodent fertilization: Involvement in sperm-zona pellucida interaction. Biol. Reprod. 2007;77:848–854. doi: 10.1095/biolreprod.107.061788. PubMed DOI

Cohen D.J., Maldera J.A., Vasen G., Ernesto J.I., Muñoz M.W., Battistone M.A., Cuasnicú P.S. Epididymal protein CRISP1 plays different roles during the fertilization process. J. Androl. 2011;32:672–678. doi: 10.2164/jandrol.110.012922. PubMed DOI

Hayashi M., Fujimoto S., Takano H., Ushiki T., Abe K., Ishikura H., Yoshida M.C., Kirchhoff C., Ishibashi T., Kasahara M. Characterization of a human glycoprotein with a potential role in sperm-egg fusion: cDNA cloning, immunohistochemical localization, and chromosomal assignment of the gene (AEGL1) Genomics. 1996;32:367–374. doi: 10.1006/geno.1996.0131. PubMed DOI

Maldera J.A., Weigel Muñoz M., Chirinos M., Busso D., Ge Raffo F., Battistone M.A., Blaquier J.A., Larrea F., Cuasnicu P.S. Human fertilization: Epididymal hCRISP1 mediates sperm-zona pellucida binding through its interaction with ZP3. Mol. Hum. Reprod. 2014;20:341–349. doi: 10.1093/molehr/gat092. PubMed DOI

Leyton L., Saling P. 95 kd sperm proteins bind ZP3 and serve as tyrosine kinase substrates in response to zona binding. Cell. 1989;57:1123–1130. doi: 10.1016/0092-8674(89)90049-4. PubMed DOI

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. doi: 10.1126/science.7541556. PubMed DOI

Naz R.K., Alexander N.J., Isahakia M., Hamilton M.S. Monoclonal antibody to a human germ cell membrane glycoprotein that inhibits fertilization. Science. 1984;225:342–344. doi: 10.1126/science.6539947. PubMed DOI

Naz R.K., Phillips T.M., Rosenblum B.B. Characterization of the fertilization antigen 1 for the development of a contraceptive vaccine. Proc. Natl. Acad. Sci. USA. 1986;83:5713–5717. doi: 10.1073/pnas.83.15.5713. PubMed DOI PMC

Naz R.K., Sacco A.G., Yurewicz E.C. Human spermatozoal FA-1 binds with ZP3 of porcine zona pellucida. J. Reprod. Immunol. 1991;20:43–58. doi: 10.1016/0165-0378(91)90022-I. PubMed DOI

Naz R.K., Brazil C., Overstreet J.W. Effects of antibodies to sperm surface fertilization antigen-1 on human sperm-zona pellucida interaction. Fertil. Steril. 1992;57:1304–1310. doi: 10.1016/S0015-0282(16)55092-4. PubMed DOI

Kadam A.L., Fateh M., Naz R.K. Fertilization antigen (FA-1) completely blocks human sperm binding to human zona pellucida: FA-1 antigen may be a sperm receptor for zona pellucida in humans. J. Reprod. Immunol. 1995;29:19–30. doi: 10.1016/0165-0378(95)00928-E. PubMed DOI

Zhu X., Naz R.K. Fertilization antigen-1: cDNA cloning, testis-specific expression, and immunocontraceptive effects. Proc. Natl. Acad. Sci. USA. 1997;94:4704–4709. doi: 10.1073/pnas.94.9.4704. PubMed DOI PMC

Naz R.K., Zhu X. Molecular cloning and sequencing of cDNA encoding for human FA-1 antigen. Mol. Reprod. Dev. 2002;63:256–268. doi: 10.1002/mrd.90010. PubMed DOI

Ensslin M.A., Shur B.D. Identification of mouse sperm SED1, a bimotif EGF repeat and discoidin-domain protein involved in sperm-egg binding. Cell. 2003;114:405–417. doi: 10.1016/S0092-8674(03)00643-3. PubMed DOI

Shur B.D., Ensslin M.A., Rodeheffer C. SED1 function during mammalian sperm-egg adhesion. Curr. Opin. Cell Biol. 2004;16:477–485. doi: 10.1016/j.ceb.2004.07.005. PubMed DOI

Copland S.D., Murphy A.A., Shur B.D. The mouse gamete adhesin, SED1, is expressed on the surface of acrosome-intact human sperm. Fertil. Steril. 2009;92:2014–2019. doi: 10.1016/j.fertnstert.2008.09.004. PubMed DOI PMC

Ensslin M., Vogel T., Calvete J.J., Thole H.H., Schmidtke J., Matsuda T., Topfer-Petersen E. Molecular cloning and characterization of P47, a novel boar sperm-associated zona pellucida-binding protein homologous to a family of mammalian secretory proteins. Biol. Reprod. 1998;58:1057–1064. doi: 10.1095/biolreprod58.4.1057. PubMed DOI

Petrunkina A.M., Lakamp A., Gentzel M., Ekhlasi-Hundrieser M., Topfer-Petersen E. Fate of lactadherin P47 during post-testicular maturation and capacitation of boar spermatozoa. Reproduction. 2003;125:377–387. doi: 10.1530/rep.0.1250377. PubMed DOI

Hagaman J.R., Moyer J.S., Bachman E.S., Sibony M., Magyar P.L., Welch J.E., Smithies O., Krege J.H., O’Brien D.A. Angiotensin-converting enzyme and male fertility. Proc. Natl. Acad. Sci. USA. 1998;95:2552–2557. doi: 10.1073/pnas.95.5.2552. PubMed DOI PMC

Ramaraj P., Kessler S.P., Colmenares C., Sen G.C. Selective restoration of male fertility in mice lacking angiotensin-converting enzymes by sperm-specific expression of the testicular isozyme. J. Clin. Investig. 1998;102:371–378. doi: 10.1172/JCI3545. PubMed DOI PMC

Foresta C., Indino M., Manoni F., Scandellari C. Angiotensin-converting enzyme content of human spermatozoa and its release during capacitation. Fertil. Steril. 1987;47:1000–1003. doi: 10.1016/S0015-0282(16)59236-X. PubMed DOI

Köhn F.M., Miska W., Schill W.B. Release of angiotensin-converting enzyme (ACE) from human spermatozoa during capacitation and acrosome reaction. J. Androl. 1995;16:259–265. PubMed

Köhn F.M., Dammshäuser I., Neukamm C., Renneberg H., Siems W.E., Schill W.B., Aumüller G. Ultrastructural localization of angiotensin-converting enzyme in ejaculated human spermatozoa. Hum. Reprod. 1998;13:604–610. doi: 10.1093/humrep/13.3.604. PubMed DOI

Pilch B., Mann M. Large-scale and high-confidence proteomic analysis of human seminal plasma. Genome Biol. 2006;7:R40. doi: 10.1186/gb-2006-7-5-r40. PubMed DOI PMC

Yotsumoto H., Sato S., Shibuya M. Localization of angiotensin converting enzyme (dipeptidyl carboxypeptidase) in swine sperm by immunofluorescence. Life Sci. 1984;35:1257–1261. doi: 10.1016/0024-3205(84)90096-1. PubMed DOI

Gatti J.L., Druart X., Guerin Y., Dacheux F., Dacheux J.L. A 105- to 94-kilodalton protein in the epididymal fluids of domestic mammals is angiotensin I-converting enzyme (ACE); evidence that sperm are the source of this ACE. Biol. Reprod. 1999;60:937–945. doi: 10.1095/biolreprod60.4.937. PubMed DOI

Druart X., Rickard J.P., Mactier S., Kohnke P.L., Kershaw-Young C.M., Bathgate R., Gibb Z., Crossett B., Tsikis G., Labas V., et al. Proteomic characterization and cross species comparison of mammalian seminal plasma. J. Proteom. 2013;91:13–22. doi: 10.1016/j.jprot.2013.05.029. PubMed DOI

Zigo M., Jonakova V., Sulc M., Manaskova-Postlerova P. Characterization of sperm surface protein patterns of ejaculated and capacitated boar sperm, with the detection of ZP binding candidates. Int. J. Biol. Macromol. 2013;61:322–328. doi: 10.1016/j.ijbiomac.2013.07.014. PubMed DOI

Costa D.S., Thundathil J.C. Characterization and activity of angiotensin-converting enzyme in Holstein semen. Anim. Reprod. Sci. 2012;133:35–42. doi: 10.1016/j.anireprosci.2012.06.009. PubMed DOI

Ojaghi M., Kastelic J., Thundathil J. Testis-specific isoform of angiotensin-converting enzyme (tACE) is involved in the regulation of bovine sperm capacitation. Mol. Reprod. Dev. 2017;84:376–388. doi: 10.1002/mrd.22790. PubMed DOI

Ojaghi M., Kastelic J., Thundathil J.C. Testis-specific isoform of angiotensin-converting enzyme (tACE) as a candidate marker for bull fertility. Reprod. Fertil. Dev. 2018;30:1584–1593. doi: 10.1071/RD17300. PubMed DOI

Bleil J.D., Wassarman P.M. Identification of a ZP3-binding protein on acrosome-intact mouse sperm by photoaffinity crosslinking. Proc. Natl. Acad. Sci. USA. 1990;87:5563–5567. doi: 10.1073/pnas.87.14.5563. PubMed DOI PMC

Cheng A., Le T., Palacios M., Bookbinder L.H., Wassarman P.M., Suzuki F., Bleil J.D. Sperm-egg recognition in the mouse: Characterization of sp56, a sperm protein having specific affinity for ZP3. J. Cell Biol. 1994;125:867–878. doi: 10.1083/jcb.125.4.867. PubMed DOI PMC

Kim K.S., Cha M.C., Gerton G.L. Mouse sperm protein sp56 is a component of the acrosomal matrix. Biol. Reprod. 2001;64:36–43. doi: 10.1095/biolreprod64.1.36. PubMed DOI

Muro Y., Buffone M.G., Okabe M., Gerton G.L. Function of the acrosomal matrix: Zona pellucida 3 receptor (ZP3R/sp56) is not essential for mouse fertilization. Biol. Reprod. 2012;86:1–6. doi: 10.1095/biolreprod.111.095877. PubMed DOI PMC

Sullivan R., Bleau G. Interaction between isolated components from mammalian sperm and egg. Gamete Res. 1985;12:101–116. doi: 10.1002/mrd.1120120112. DOI

Sullivan R., Robitaille G. Heterogeneity of epididymal spermatozoa of the hamster. Gamete Res. 1989;24:229–236. doi: 10.1002/mrd.1120240210. PubMed DOI

Bérubé B., Sullivan R. Inhibition of in vivo fertilization by active immunization of male hamsters against a 26-kDa sperm glycoprotein. Biol. Reprod. 1994;51:1255–1263. doi: 10.1095/biolreprod51.6.1255. PubMed DOI

Bégin S., Bérubé B., Boué F., Sullivan R. Comparative immunoreactivity of mouse and hamster sperm proteins recognized by an anti-P26h hamster sperm protein. Mol. Reprod. Dev. 1995;41:249–256. doi: 10.1002/mrd.1080410216. PubMed DOI

Boué F., Bérubé B., De Lamirande E., Gagnon C., Sullivan R. Human sperm-zona pellucida interaction is inhibited by an antiserum against a hamster sperm protein. Biol. Reprod. 1994;51:577–587. doi: 10.1095/biolreprod51.4.577. PubMed DOI

Boué F., Blais J., Sullivan R. Surface localization of P34H an epididymal protein, during maturation, capacitation, and acrosome reaction of human spermatozoa. Biol. Reprod. 1996;54:1009–1017. doi: 10.1095/biolreprod54.5.1009. PubMed DOI

Van Gestel R.A., Brewis I.A., Ashton P.R., Brouwers J.F., Gadella B.M. Multiple proteins present in purified porcine sperm apical plasma membranes interact with the zona pellucida of the oocyte. Mol. Hum. Reprod. 2007;13:445–454. doi: 10.1093/molehr/gam030. PubMed DOI

Parent S., Lefievre L., Brindle Y., Sullivan R. Bull subfertility is associated with low levels of a sperm membrane antigen. Mol. Reprod. Dev. 1998;52:57–65. doi: 10.1002/(SICI)1098-2795(199901)52:1<57::AID-MRD8>3.0.CO;2-U. DOI

Lessard C., Parent S., Leclerc P., Bailey J.L., Sullivan R. Cryopreservation alters the levels of the bull sperm surface protein P25b. J. Androl. 2000;21:700–707. PubMed

Frenette G., Sullivan R. Prostasome-like particles are involved in the transfer of P25b from the bovine epididymal fluid to the sperm surface. Mol. Reprod. Dev. 2001;59:115–121. doi: 10.1002/mrd.1013. PubMed DOI

Sanz L., Calvete J.J., Jonakova V., Topfer-Petersen E. Boar spermadhesins AQN-1 and AWN are sperm-associated acrosin inhibitor acceptor proteins. FEBS Lett. 1992;300:63–66. doi: 10.1016/0014-5793(92)80164-C. PubMed DOI

Sanz L., Calvete J.J., Schäfer W., Mann K., Töpfer-Petersen E. Isolation and biochemical characterization of two isoforms of a boar sperm zona pellucida-binding protein. Biochim. Biophys. Acta (BBA) Gene Struct. Expr. 1992;1119:127–132. doi: 10.1016/0167-4838(92)90382-N. PubMed DOI

Veselsky L., Jonakova V., Sanz M.L., Topfer-Petersen E., Cechova D. Binding of a 15 kDa glycoprotein from spermatozoa of boars to surface of zona pellucida and cumulus oophorus cells. J. Reprod. Fertil. 1992;96:593–602. doi: 10.1530/jrf.0.0960593. PubMed DOI

Dostalova Z., Calvete J.J., Topfer-Petersen E. Interaction of non-aggregated boar AWN-1 and AQN-3 with phospholipid matrices. A model for coating of spermadhesins to the sperm surface. Biol. Chem. 1995;376:237–242. doi: 10.1515/bchm3.1995.376.4.237. PubMed DOI

Ensslin M., Calvete J.J., Thole H.H., Sierralta W.D., Adermann K., Sanz L., Topfer-Petersen E. 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. 1995;376:733–738. PubMed

Calvete J.J., Carrera E., Sanz L., Töpfer-Petersen E. Boar spermadhesins AQN-1 and AQN-3: Oligosaccharide and zona pellucida binding characteristics. Biol. Chem. 1996;377:521–527. doi: 10.1515/bchm3.1996.377.7-8.521. PubMed DOI

Jonakova V., Kraus M., Veselsky L., Cechova D., Bezouska K., Ticha M. Spermadhesins of the AQN and AWN families, DQH sperm surface protein and HNK protein in the heparin-binding fraction of boar seminal plasma. J. Reprod. Fertil. 1998;114:25–34. doi: 10.1530/jrf.0.1140025. PubMed DOI

Veselsky L., Peknicova J., Cechova D., Kraus M., Geussova G., Jonakova V. Characterization of boar spermadhesins by monoclonal and polyclonal antibodies and their role in binding to oocytes. Am. J. Reprod. Immunol. 1999;42:187–197. doi: 10.1111/j.1600-0897.1999.tb00483.x. PubMed DOI

Petrunkina A.M., Harrison R.A., Topfer-Petersen E. Only low levels of spermadhesin AWN are detectable on the surface of live ejaculated boar spermatozoa. Reprod. Fertil. Dev. 2000;12:361–371. doi: 10.1071/RD00117. PubMed DOI

Tichá M., Kraus M., Cechová D., Jonáková V. Saccharide-binding properties of boar AQN spermadhesins and DQH sperm surface protein. Folia Biol. 1998;44:15–21. PubMed

Jonakova V., Manaskova P., Kraus M., Liberda J., Ticha M. Sperm surface proteins in mammalian fertilization. Mol. Reprod. Dev. 2000;56:275–277. doi: 10.1002/(SICI)1098-2795(200006)56:2+<275::AID-MRD13>3.0.CO;2-G. PubMed DOI

Manaskova P., Peknicova J., Elzeinova F., Ticha M., Jonakova V. Origin, localization and binding abilities of boar DQH sperm surface protein tested by specific monoclonal antibodies. J. Reprod. Immunol. 2007;74:103–113. doi: 10.1016/j.jri.2006.11.003. PubMed DOI

Liberda J., Ryslavá H., Jelínková P., Jonáková V., Tichá M. Affinity chromatography of bull seminal proteins on mannan-Sepharose. J. Chromatogr. B. 2002;780:231–239. doi: 10.1016/S1570-0232(02)00521-4. PubMed DOI

Lin Y.N., Roy A., Yan W., Burns K.H., Matzuk M.M. Loss of zona pellucida binding proteins in the acrosomal matrix disrupts acrosome biogenesis and sperm morphogenesis. Mol. Cell. Biol. 2007;27:6794–6805. doi: 10.1128/MCB.01029-07. PubMed DOI PMC

Yu Y., Vanhorne J., Oko R. The origin and assembly of a zona pellucida binding protein, IAM38, during spermiogenesis. Microsc. Res. Tech. 2009;72:558–565. doi: 10.1002/jemt.20696. PubMed DOI

Yatsenko A.N., O’Neil D.S., Roy A., Arias-Mendoza P.A., Chen R., Murthy L.J., Lamb D.J., Matzuk M.M. Association of mutations in the zona pellucida binding protein 1 (ZPBP1) gene with abnormal sperm head morphology in infertile men. Mol. Hum. Reprod. 2012;18:14–21. doi: 10.1093/molehr/gar057. PubMed DOI PMC

Guo Y., Jiang J., Zhang H., Wen Y., Zhang H., Cui Y., Tian J., Jiang M., Liu X., Wang G., et al. Proteomic Analysis of Dpy19l2-Deficient Human Globozoospermia Reveals Multiple Molecular Defects. Proteom. Clin. Appl. 2019;13:e1900007. doi: 10.1002/prca.201900007. PubMed DOI

Mori E., Baba T., Iwamatsu A., Mori T. Purification and characterization of a 38-kDa protein, sp38, with zona pellucida-binding property from porcine epididymal sperm. Biochem. Biophys. Res. Commun. 1993;196:196–202. doi: 10.1006/bbrc.1993.2234. PubMed DOI

Mori E., Kashiwabara S., Baba T., Inagaki Y., Mori T. Amino acid sequences of porcine Sp38 and proacrosin required for binding to the zona pellucida. Dev. Biol. 1995;168:575–583. doi: 10.1006/dbio.1995.1103. PubMed DOI

Yu Y., Xu W., Yi Y.J., Sutovsky P., Oko R. 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. 2006;290:32–43. doi: 10.1016/j.ydbio.2005.11.003. PubMed DOI

Dubova-Mihailova M., Mollova M., Ivanova M., Kehayov I., Kyurkchiev S. Identification and characterization of human acrosomal antigen defined by a monoclonal antibody with blocking effect on in vitro fertilization. J. Reprod. Immunol. 1991;19:251–268. doi: 10.1016/0165-0378(91)90039-S. PubMed DOI

Foster J.A., Klotz K.L., Flickinger C.J., Thomas T.S., Wright R.M., Castillo J.R., Herr J.C. Human SP-10: Acrosomal distribution, processing, and fate after the acrosome reaction. Biol. Reprod. 1994;51:1222–1231. doi: 10.1095/biolreprod51.6.1222. PubMed DOI

Hamatani T., Tanabe K., Kamei K., Sakai N., Yamamoto Y., Yoshimura Y. A monoclonal antibody to human SP-10 inhibits in vitro the binding of human sperm to hamster oolemma but not to human Zona pellucida. Biol. Reprod. 2000;62:1201–1208. doi: 10.1095/biolreprod62.5.1201. PubMed DOI

Coonrod S.A., Herr J.C., Westhusin M.E. Inhibition of bovine fertilization in vitro by antibodies to SP-10. J. Reprod. Fertil. 1996;107:287–297. doi: 10.1530/jrf.0.1070287. PubMed DOI

Avilés M., Abascal I., Martínez-Menárguez J.A., Castells M.T., Skalaban S.R., Ballesta J., Alhadeff J.A. Immunocytochemical localization and biochemical characterization of a novel plasma membrane-associated, neutral pH optimum alpha-L-fucosidase from rat testis and epididymal spermatozoa. Pt 3Biochem. J. 1996;318:821–831. doi: 10.1042/bj3180821. PubMed DOI PMC

Phopin K., Nimlamool W., Bartlett M.J., Bean B.S. Distribution, crypticity, stability, and localization of α-L-fucosidase of mouse cauda epididymal sperm. Mol. Reprod. Dev. 2012;79:208–217. doi: 10.1002/mrd.22016. PubMed DOI

Phopin K., Nimlamool W., Lowe-Krentz L.J., Douglass E.W., Taroni J.N., Bean B.S. Roles of mouse sperm-associated alpha-L-fucosidases in fertilization. Mol. Reprod. Dev. 2013;80:273–285. doi: 10.1002/mrd.22164. PubMed DOI

Venditti J.J., Donigan K.A., Bean B.S. Crypticity and functional distribution of the membrane associated alpha-L-fucosidase of human sperm. Mol. Reprod. Dev. 2007;74:758–766. doi: 10.1002/mrd.20666. PubMed DOI

Venditti J.J., Bean B.S. Stabilization of membrane-associated alpha-L-fucosidase by the human sperm equatorial segment. Int. J. Androl. 2009;32:556–562. doi: 10.1111/j.1365-2605.2008.00897.x. PubMed DOI

Jauhiainen A., Vanha-Perttula T. alpha-L-Fucosidase in the reproductive organs and seminal plasma of the bull. Biochim. Biophys. Acta (BBA) Gene Struct. Expr. 1986;880:91–95. doi: 10.1016/0304-4165(86)90123-6. PubMed DOI

Peterson R.N., Hunt W.P. Identification, isolation, and properties of a plasma membrane protein involved in the adhesion of boar sperm to the porcine zona pellucida. Gamete Res. 1989;23:103–118. doi: 10.1002/mrd.1120230110. PubMed DOI

Zayas-Perez H., Casas E., Bonilla E., Betancourt M. Inhibition of sperm-zona pellucida binding by a 55 kDa pig sperm protein in vitro. Arch. Androl. 2005;51:195–206. doi: 10.1080/014850190884372. PubMed DOI

Redgrove K.A., Anderson A.L., Dun M.D., McLaughlin E.A., O’Bryan M.K., Aitken R.J., Nixon B. Involvement of multimeric protein complexes in mediating the capacitation-dependent binding of human spermatozoa to homologous zonae pellucidae. Dev. Biol. 2011;356:460–474. doi: 10.1016/j.ydbio.2011.05.674. PubMed DOI

Kongmanas K., Kruevaisayawan H., Saewu A., Sugeng C., Fernandes J., Souda P., Angel J.B., Faull K.F., Aitken R.J., Whitelegge J., et al. Proteomic Characterization of Pig Sperm Anterior Head Plasma Membrane Reveals Roles of Acrosomal Proteins in ZP3 Binding. J. Cell. Physiol. 2015;230:449–463. doi: 10.1002/jcp.24728. PubMed DOI

Shur B.D., Bennett D. A specific defect in galactosyltransferase regulation on sperm bearing mutant alleles of the T/t locus. Dev. Biol. 1979;71:243–259. doi: 10.1016/0012-1606(79)90167-2. PubMed DOI

Lopez L.C., Bayna E.M., Litoff D., Shaper N.L., Shaper J.H., Shur B.D. Receptor function of mouse sperm surface galactosyltransferase during fertilization. J. Cell Biol. 1985;101:1501–1510. doi: 10.1083/jcb.101.4.1501. PubMed DOI PMC

Nixon B., Lu Q., Wassler M.J., Foote C.I., Ensslin M.A., Shur B.D. Galactosyltransferase function during mammalian fertilization. Cells Tissues Organs. 2001;168:46–57. doi: 10.1159/000016805. PubMed DOI

Fayrer-Hosken R.A., Caudle A.B., Shur B.D. Galactosyltransferase activity is restricted to the plasma membranes of equine and bovine sperm. Mol. Reprod. Dev. 1991;28:74–78. doi: 10.1002/mrd.1080280112. PubMed DOI

Lu Q., Shur B.D. Sperm from beta 1,4-galactosyltransferase-null mice are refractory to ZP3-induced acrosome reactions and penetrate the zona pellucida poorly. Development. 1997;124:4121–4131. PubMed

Lyng R., Shur B.D. Sperm-egg binding requires a multiplicity of receptor-ligand interactions: New insights into the nature of gamete receptors derived from reproductive tract secretions. Soc. Reprod. Fertil. Suppl. 2007;65:335–351. PubMed

Topfer-Petersen E., Friess A.E., Nguyen H., Schill W.B. Evidence for a fucose-binding protein in boar spermatozoa. Histochemistry. 1985;83:139–145. doi: 10.1007/BF00495144. PubMed DOI

Topfer-Petersen E., Henschen A. Acrosin shows zona and fucose binding, novel properties for a serine proteinase. FEBS Lett. 1987;226:38–42. doi: 10.1016/0014-5793(87)80546-X. PubMed DOI

Baba T., Azuma S., Kashiwabara S., Toyoda Y. Sperm from mice carrying a targeted mutation of the acrosin gene can penetrate the oocyte zona pellucida and effect fertilization. J. Biol. Chem. 1994;269:31845–31849. doi: 10.1016/S0021-9258(18)31772-1. PubMed DOI

Isotani A., Matsumura T., Ogawa M., Tanaka T., Yamagata K., Ikawa M., Okabe M. A delayed sperm penetration of cumulus layers by disruption of acrosin gene in rats. Biol. Reprod. 2017;97:61–68. doi: 10.1093/biolre/iox066. PubMed DOI

Adham I.M., Nayernia K., Engel W. Spermatozoa lacking acrosin protein show delayed fertilization. Mol. Reprod. Dev. 1997;46:370–376. doi: 10.1002/(SICI)1098-2795(199703)46:3<370::AID-MRD16>3.0.CO;2-2. PubMed DOI

Dudkiewicz A.B. Inhibition of fertilization in the rabbit by anti-acrosin antibodies. Mol. Reprod. Dev. 1983;8:183–197. doi: 10.1002/mrd.1120080207. DOI

Liu D.Y., Baker H.W. Inhibition of acrosin activity with a trypsin inhibitor blocks human sperm penetration of the zona pellucida. Biol. Reprod. 1993;48:340–348. doi: 10.1095/biolreprod48.2.340. PubMed DOI

Hirose M., Honda A., Fulka H., Tamura-Nakano M., Matoba S., Tomishima T., Mochida K., Hasegawa A., Nagashima K., Inoue K., et al. Acrosin is essential for sperm penetration through the zona pellucida in hamsters. Proc. Natl. Acad. Sci. USA. 2020;117:2513–2518. doi: 10.1073/pnas.1917595117. PubMed DOI PMC

Yamagata K., Honda A., Kashiwabara S.I., Baba T. Difference of acrosomal serine protease system between mouse and other rodent sperm. Dev. Genet. 1999;25:115–122. doi: 10.1002/(SICI)1520-6408(1999)25:2<115::AID-DVG5>3.0.CO;2-1. PubMed DOI

Wassarman P.M. Zona pellucida glycoproteins. J. Biol. Chem. 2008;283:24285–24289. doi: 10.1074/jbc.R800027200. PubMed DOI PMC

Marco-Jiménez F., Naturil-Alfonso C., Jiménez-Trigos E., Lavara R., Vicente J.S. Influence of zona pellucida thickness on fertilization, embryo implantation and birth. Anim. Reprod. Sci. 2012;132:96–100. doi: 10.1016/j.anireprosci.2012.04.008. PubMed DOI

Lamas-Toranzo I., Fonseca Balvís N., Querejeta-Fernández A., Izquierdo-Rico M.J., González-Brusi L., Lorenzo P.L., García-Rebollar P., Avilés M., Bermejo-Álvarez P. ZP4 confers structural properties to the zona pellucida essential for embryo development. Elife. 2019;8 doi: 10.7554/eLife.48904. PubMed DOI PMC

Abe H., Oikawa T. Ultrastructural evidence for an association between an oviductal glycoprotein and the zona pellucida of the golden hamster egg. J. Exp. Zool. 1990;256:210–221. doi: 10.1002/jez.1402560211. PubMed DOI

Wiesak T., Wasielak M., Złotkowska A., Milewski R. Effect of vitrification on the zona pellucida hardening and follistatin and cathepsin B genes expression and developmental competence of in vitro matured bovine oocytes. Cryobiology. 2017;76:18–23. doi: 10.1016/j.cryobiol.2017.05.001. PubMed DOI

Balakier H., Sojecki A., Motamedi G., Bashar S., Mandel R., Librach C. Is the zona pellucida thickness of human embryos influenced by women’s age and hormonal levels? Fertil. Steril. 2012;98:77–83. doi: 10.1016/j.fertnstert.2012.04.015. PubMed DOI

Herlyn H., Zischler H. The molecular evolution of sperm zonadhesin. Int. J. Dev. Biol. 2008;52:781–790. doi: 10.1387/ijdb.082626hh. PubMed DOI

Tardif S., Cormier N. Role of zonadhesin during sperm-egg interaction: A species-specific acrosomal molecule with multiple functions. Mol. Hum. Reprod. 2011;17:661–668. doi: 10.1093/molehr/gar039. PubMed DOI

Hardy D.M., Garbers D.L. Species-specific binding of sperm proteins to the extracellular matrix (zona pellucida) of the egg. J. Biol. Chem. 1994;269:19000–19004. PubMed

Hickox J.R., Bi M., Hardy D.M. Heterogeneous processing and zona pellucida binding activity of pig zonadhesin. J. Biol. Chem. 2001;276:41502–41509. doi: 10.1074/jbc.M106795200. PubMed DOI

Dudkiewicz A.B. Purification of boar acrosomal arylsulfatase A and possible role in the penetration of cumulus cells. Biol. Reprod. 1984;30:1005–1014. doi: 10.1095/biolreprod30.4.1005. PubMed DOI

White D., Weerchatyanukul W., Gadella B.M., Kamolvarin N., Attar M., Tanphaichitr N. Role of sperm sulfogalactosylglycerolipid in mouse sperm-zona pellucida binding. Biol. Reprod. 2000;63:147–155. doi: 10.1095/biolreprod63.1.147. PubMed DOI

Rattanachaiyanont M., Weerachatyanukul W., Leveille M.-C., Taylor T., D’Amours D., Rivers D., Leader A., Tanphaichitr N. Anti-SLIP1-reactive proteins exist on human sperm and are involved in zona-pellucida binding. Mol. Hum. Reprod. 2001;7:633–640. doi: 10.1093/molehr/7.7.633. PubMed DOI

Weerachatyanukul W., Xu H., Anupriwan A., Carmona E., Wade M., Hermo L., da Silva S.M., Rippstein P., Sobhon P., Sretarugsa P., et al. Acquisition of arylsulfatase A onto the mouse sperm surface during epididymal transit. Biol. Reprod. 2003;69:1183–1192. doi: 10.1095/biolreprod.102.010231. PubMed DOI

Schenk M., Koppisetty C.A., Santos D.C., Carmona E., Bhatia S., Nyholm P.G., Tanphaichitr N. Interaction of arylsulfatase-A (ASA) with its natural sulfoglycolipid substrates: A computational and site-directed mutagenesis study. Glycoconj. J. 2009;26:1029–1045. doi: 10.1007/s10719-008-9222-9. PubMed DOI

Gadella B.M., Colenbrander B., Golde L.M.v., Lopes-Cardozo M. Boar seminal vesicles secrete arylsulfatases into seminal plasma: Evidence that desulfation of seminolipid occurs only after ejaculation. Biol. Reprod. 1993;48:483–489. doi: 10.1095/biolreprod48.3.483. PubMed DOI

Carmona E., Weerachatyanukul W., Xu H., Fluharty A., Anupriwan A., Shoushtarian A., Chakrabandhu K., Tanphaichitr N. Binding of arylsulfatase A to mouse sperm inhibits gamete interaction and induces the acrosome reaction. Biol. Reprod. 2002;66:1820–1827. doi: 10.1095/biolreprod66.6.1820. PubMed DOI

Gonzalez-Cadavid V., Martins J.A., Moreno F.B., Andrade T.S., Santos A.C., Monteiro-Moreira A.C., Moreira R.A., Moura A.A. Seminal plasma proteins of adult boars and correlations with sperm parameters. Theriogenology. 2014;82:697–707. doi: 10.1016/j.theriogenology.2014.05.024. PubMed DOI

Silva E., Frost D., Li L., Bovin N., Miller D.J. Lactadherin is a candidate oviduct Lewis X trisaccharide receptor on porcine spermatozoa. Andrology. 2017;5:589–597. doi: 10.1111/andr.12340. PubMed DOI PMC

Zigo M., Manaskova-Postlerova P., Jonakova V., Kerns K., Sutovsky P. Compartmentalization of the proteasome-interacting proteins during sperm capacitation. Sci. Rep. 2019;9:12583. doi: 10.1038/s41598-019-49024-0. PubMed DOI PMC

Miles E.L., O’Gorman C., Zhao J., Samuel M., Walters E., Yi Y.J., Sutovsky M., Prather R.S., Wells K.D., Sutovsky P. Transgenic pig carrying green fluorescent proteasomes. Proc. Natl. Acad. Sci. USA. 2013;110:6334–6339. doi: 10.1073/pnas.1220910110. PubMed DOI PMC

Zimmerman S.W., Manandhar G., Yi Y.J., Gupta S.K., Sutovsky M., Odhiambo J.F., Powell M.D., Miller D.J., Sutovsky P. Sperm proteasomes degrade sperm receptor on the egg zona pellucida during mammalian fertilization. PLoS ONE. 2011;6:e17256. doi: 10.1371/journal.pone.0017256. PubMed DOI PMC

Zigo M., Jonakova V., Manaskova-Postlerova P., Kerns K., Sutovsky P. Ubiquitin-proteasome system participates in the de-aggregation of spermadhesin and DQH protein during boar sperm capacitation. Reproduction. 2019;157:283–295. doi: 10.1530/REP-18-0413. PubMed DOI

Wassarman P.M., Jovine L., Litscher E.S. A profile of fertilization in mammals. Nat. Cell Biol. 2001;3:E59–E64. doi: 10.1038/35055178. PubMed DOI

Foster J.A., Friday B.B., Maulit M.T., Blobel C., Winfrey V.P., Olson G.E., Kim K.S., Gerton G.L. 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. 1997;272:12714–12722. doi: 10.1074/jbc.272.19.12714. PubMed DOI

Kim K.S., Foster J.A., Gerton G.L. Differential release of guinea pig sperm acrosomal components during exocytosis. Biol. Reprod. 2001;64:148–156. doi: 10.1095/biolreprod64.1.148. PubMed DOI

Buffone M.G., Zhuang T., Ord T.S., Hui L., Moss S.B., Gerton G.L. 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. 2008;283:12438–12445. doi: 10.1074/jbc.M706421200. PubMed DOI PMC

Da Ros V.G., Maldera J.A., Willis W.D., Cohen D.J., Goulding E.H., Gelman D.M., Rubinstein M., Eddy E.M., Cuasnicu P.S. Impaired sperm fertilizing ability in mice lacking Cysteine-RIch Secretory Protein 1 (CRISP1) Dev. Biol. 2008;320:12–18. doi: 10.1016/j.ydbio.2008.03.015. PubMed DOI PMC

Naz R.K., Ahmad 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. doi: 10.1002/mrd.1080390408. PubMed DOI

Naz R.K., Bhargava K.K. Antibodies to sperm surface fertilization antigen (FA-1): Their specificities and site of interaction with sperm in male genital tract. Mol. Reprod. Dev. 1990;26:175–183. doi: 10.1002/mrd.1080260212. PubMed DOI

Pan P.P., Zhan Q.T., Le F., Zheng Y.M., Jin F. Angiotensin-converting enzymes play a dominant role in fertility. Int. J. Mol. Sci. 2013;14:21071–21086. doi: 10.3390/ijms141021071. PubMed DOI PMC

Castilho C.S., Fontes P.K., Franchi F.F., Santos P.H., Razza E.M. Renin-Angiotensin System on Reproductive Biology. In: Tolekova A., editor. Renin-Angiotensin System Past, Present and Future. InTech; Rijeka, Croatia: 2017. p. 258.

Reis A.B., Araújo F.C., Pereira V.M., Dos Reis A.M., Santos R.A., Reis F.M. Angiotensin (1–7) and its receptor Mas are expressed in the human testis: Implications for male infertility. J. Mol. Histol. 2010;41:75–80. doi: 10.1007/s10735-010-9264-8. PubMed DOI

Wang Z., Xu X. scRNA-seq Profiling of Human Testes Reveals the Presence of the ACE2 Receptor, A Target for SARS-CoV-2 Infection in Spermatogonia, Leydig and Sertoli Cells. Cells. 2020;9:920. doi: 10.3390/cells9040920. PubMed DOI PMC

Shang J., Ye G., Shi K., Wan Y., Luo C., Aihara H., Geng Q., Auerbach A., Li F. Structural basis of receptor recognition by SARS-CoV-2. Nature. 2020;581:221–224. doi: 10.1038/s41586-020-2179-y. PubMed DOI PMC

Sullivan R., Saez F., Girouard J., Frenette G. Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood Cells Mol. Dis. 2005;35:1–10. doi: 10.1016/j.bcmd.2005.03.005. PubMed DOI

Petit F.M., Serres C., Bourgeon F., Pineau C., Auer J. Identification of sperm head proteins involved in zona pellucida binding. Hum. Reprod. 2013;28:852–865. doi: 10.1093/humrep/des452. PubMed DOI

Feiden S., Wolfrum U., Wegener G., Kamp G. Expression and compartmentalisation of the glycolytic enzymes GAPDH and pyruvate kinase in boar spermatogenesis. Reprod. Fertil. Dev. 2008;20:713–723. doi: 10.1071/RD08004. PubMed DOI

Topfer-Petersen E., Romero A., Varela P.F., Ekhlasi-Hundrieser M., Dostalova Z., Sanz L., Calvete J.J. Spermadhesins: A new protein family. Facts, hypotheses and perspectives. Andrologia. 1998;30:217–224. doi: 10.1111/j.1439-0272.1998.tb01163.x. PubMed DOI

Jonakova V., Ticha M. Boar seminal plasma proteins and their binding properties. Collect. Czechoslov. Chem. Commun. 2004;69:461–475. doi: 10.1135/cccc20040461. DOI

Jonakova V., Manaskova P., Ticha M. Separation, characterization and identification of boar seminal plasma proteins. J. Chromatogr. B. 2007;849:307–314. doi: 10.1016/j.jchromb.2006.10.054. PubMed DOI

Jonakova V., Jonak J., Ticha M. Proteomics of Male Seminal Plasma. In: Jiang Z., Ott T.L., editors. Reproductive Genomics in Domestic Animals. Blackwell Publishing; Oxford, UK: 2010. pp. 339–368.

Ekhlasi-Hundrieser M., Gohr K., Wagner A., Tsolova M., Petrunkina A., Topfer-Petersen E. Spermadhesin AQN1 is a candidate receptor molecule involved in the formation of the oviductal sperm reservoir in the pig. Biol. Reprod. 2005;73:536–545. doi: 10.1095/biolreprod.105.040824. PubMed DOI

Calvete J.J., Raida M., Gentzel M., Urbanke C., Sanz L., Topfer-Petersen E. Isolation and characterization of heparin- and phosphorylcholine-binding proteins of boar and stallion seminal plasma. Primary structure of porcine pB1. FEBS Lett. 1997;407:201–206. doi: 10.1016/S0014-5793(97)00344-X. PubMed DOI

Bezouska K., Sklenár J., Novák P., Halada P., Havlícek V., Kraus M., Tichá M., Jonáková V. Determination of the complete covalent structure of the major glycoform of DQH sperm surface protein, a novel trypsin-resistant boar seminal plasma O-glycoprotein related to pB1 protein. Protein Sci. 1999;8:1551–1556. doi: 10.1110/ps.8.7.1551. PubMed DOI PMC

Fan J., Lefebvre J., Manjunath P. Bovine seminal plasma proteins and their relatives: A new expanding superfamily in mammals. Gene. 2006;375:63–74. doi: 10.1016/j.gene.2006.02.025. PubMed DOI

Plante G., Prud’homme B., Fan J., Lafleur M., Manjunath P. Evolution and function of mammalian binder of sperm proteins. Cell Tissue Res. 2016;363:105–127. doi: 10.1007/s00441-015-2289-2. PubMed DOI

Kim E., Park K.E., Kim J.S., Baek D.C., Lee J.W., Lee S.R., Kim M.S., Kim S.H., Kim C.S., Koo D.B., et al. Importance of the porcine ADAM3 disintegrin domain in sperm-egg interaction. J. Reprod. Dev. 2009;55:156–162. doi: 10.1262/jrd.20134. PubMed DOI

Mori E., Fukuda H., Imajoh-Ohmi S., Mori T., Takasaki S. Purification of N-acetyllactosamine-binding activity from the porcine sperm membrane: Possible involvement of an ADAM complex in the carbohydrate-binding activity of sperm. J. Reprod. Dev. 2012;58:117–125. doi: 10.1262/jrd.11-108N. PubMed DOI

Srivastava N., Jerome A., Srivastava S.K., Ghosh S.K., Kumar A. Bovine seminal PDC-109 protein: An overview of biochemical and functional properties. Anim. Reprod. Sci. 2013;138:1–13. doi: 10.1016/j.anireprosci.2013.02.008. PubMed DOI

Gwathmey T.M., Ignotz G.G., Suarez S.S. PDC-109 (BSP-A1/A2) promotes bull sperm binding to oviductal epithelium in vitro and may be involved in forming the oviductal sperm reservoir. Biol. Reprod. 2003;69:809–815. doi: 10.1095/biolreprod.102.010827. PubMed DOI

Somashekar L., Selvaraju S., Parthipan S., Ravindra J.P. Profiling of sperm proteins and association of sperm PDC-109 with bull fertility. Syst. Biol. Reprod. Med. 2015;61:376–387. doi: 10.3109/19396368.2015.1094837. PubMed DOI

Kumar P., Kumar D., Singh I., Yadav P.S. Seminal Plasma Proteome: Promising Biomarkers for Bull Fertility. Agric. Res. 2012;1:78–86. doi: 10.1007/s40003-011-0006-2. DOI

Kelly V.C., Kuy S., Palmer D.J., Xu Z., Davis S.R., Cooper G.J. Characterization of bovine seminal plasma by proteomics. Proteomics. 2006;6:5826–5833. doi: 10.1002/pmic.200500830. PubMed DOI

Redgrove K.A., Aitken R.J., Nixon B. More Than a Simple Lock and Key Mechanism: Unraveling the Intricacies of Sperm-Zona Pellucida Binding. In: Abdelmohsen K., editor. Binding Protein. IntechOpen; Rijeka, Croatia: 2012. p. 206.

van Gestel R.A., Brewis I.A., Ashton P.R., Helms J.B., Brouwers J.F., Gadella B.M. Capacitation-dependent concentration of lipid rafts in the apical ridge head area of porcine sperm cells. Mol. Hum. Reprod. 2005;11:583–590. doi: 10.1093/molehr/gah200. PubMed DOI

Bou Khalil M., Chakrabandhu K., Xu H., Weerachatyanukul W., Buhr M., Berger T., Carmona E., Vuong N., Kumarathasan P., Wong P.T., et al. Sperm capacitation induces an increase in lipid rafts having zona pellucida binding ability and containing sulfogalactosylglycerolipid. Dev. Biol. 2006;290:220–235. doi: 10.1016/j.ydbio.2005.11.030. PubMed DOI

Gadella B.M., Tsai P.S., Boerke A., Brewis I.A. Sperm head membrane reorganisation during capacitation. Int. J. Dev. Biol. 2008;52:473–480. doi: 10.1387/ijdb.082583bg. PubMed DOI

Simons K., Sampaio J.L. Membrane organization and lipid rafts. Cold Spring Harb. Perspect. Biol. 2011;3:a004697. doi: 10.1101/cshperspect.a004697. PubMed DOI PMC

Pike L.J. Rafts defined: A report on the Keystone Symposium on Lipid Rafts and Cell Function. J. Lipid Res. 2006;47:1597–1598. doi: 10.1194/jlr.E600002-JLR200. PubMed DOI

Tanphaichitr N., Bou Khalil M., Weerachatyanukul W., Kates M., Xu H., Carmona E., Attar M., Carrier D. Physiological and Biophysical Properties of Male Germ Cell Sulfogalactosylglycerolipid. In: De Vriese S.R., Christophe A.B., editors. Male Fertility and Lipid Metabolsim. AOCS Press; Champaign, IL, USA: 2003. p. 279.

Tanphaichitr N., Kongmanas K., Faull K.F., Whitelegge J., Compostella F., Goto-Inoue N., Linton J.J., Doyle B., Oko R., Xu H., et al. Properties, metabolism and roles of sulfogalactosylglycerolipid in male reproduction. Prog. Lipid Res. 2018;72:18–41. doi: 10.1016/j.plipres.2018.08.002. PubMed DOI PMC

Attar M., Kates M., Bou Khalil M., Carrier D., Wong P.T., Tanphaichitr N. A Fourier-transform infrared study of the interaction between germ-cell specific sulfogalactosylglycerolipid and dimyristoylglycerophosphocholine. Chem. Phys. Lipids. 2000;106:101–114. doi: 10.1016/S0009-3084(00)00147-X. PubMed DOI

Weerachatyanukul W., Probodh I., Kongmanas K., Tanphaichitr N., Johnston L.J. Visualizing the localization of sulfoglycolipids in lipid raft domains in model membranes and sperm membrane extracts. Biochim. Biophys. Acta (BBA) Gene Struct. Expr. 2007;1768:299–310. doi: 10.1016/j.bbamem.2006.08.022. PubMed DOI

Weerachatyanukul W., Rattanachaiyanont M., Carmona E., Furimsky A., Mai A., Shoushtarian A., Sirichotiyakul S., Ballakier H., Leader A., Tanphaichitr N. Sulfogalactosylglycerolipid is involved in human gamete interaction. Mol. Reprod. Dev. 2001;60:569–578. doi: 10.1002/mrd.1122. PubMed DOI

Hartl F.U., Bracher A., Hayer-Hartl M. Molecular chaperones in protein folding and proteostasis. Nature. 2011;475:324–332. doi: 10.1038/nature10317. PubMed DOI

Kim Y.E., Hipp M.S., Bracher A., Hayer-Hartl M., Hartl F.U. Molecular chaperone functions in protein folding and proteostasis. Annu. Rev. Biochem. 2013;82:323–355. doi: 10.1146/annurev-biochem-060208-092442. PubMed DOI

Asquith K.L., Baleato R.M., McLaughlin E.A., Nixon B., Aitken R.J. Tyrosine phosphorylation activates surface chaperones facilitating sperm-zona recognition. J. Cell Sci. 2004;117:3645–3657. doi: 10.1242/jcs.01214. PubMed DOI

Kamaruddin M., Kroetsch T., Basrur P.K., Hansen P.J., King W.A. Immunolocalization of heat shock protein 70 in bovine spermatozoa. Andrologia. 2004;36:327–334. doi: 10.1111/j.1439-0272.2004.00629.x. PubMed DOI

Spinaci M., Volpe S., Bernardini C., De Ambrogi M., Tamanini C., Seren E., Galeati G. Immunolocalization of heat shock protein 70 (Hsp 70) in boar spermatozoa and its role during fertilization. Mol. Reprod. Dev. 2005;72:534–541. doi: 10.1002/mrd.20367. PubMed DOI

Nixon B., Aitken R.J. The biological significance of detergent-resistant membranes in spermatozoa. J. Reprod. Immunol. 2009;83:8–13. doi: 10.1016/j.jri.2009.06.258. PubMed DOI

Nixon B., Bielanowicz A., McLaughlin E.A., Tanphaichitr N., Ensslin M.A., Aitken R.J. Composition and significance of detergent resistant membranes in mouse spermatozoa. J. Cell. Physiol. 2009;218:122–134. doi: 10.1002/jcp.21575. PubMed DOI

Naaby-Hansen S., Herr J.C. Heat shock proteins on the human sperm surface. J. Reprod. Immunol. 2010;84:32–40. doi: 10.1016/j.jri.2009.09.006. PubMed DOI PMC

Asquith K.L., Harman A.J., McLaughlin E.A., Nixon B., Aitken R.J. Localization and significance of molecular chaperones, heat shock protein 1, and tumor rejection antigen gp96 in the male reproductive tract and during capacitation and acrosome reaction. Biol. Reprod. 2005;72:328–337. doi: 10.1095/biolreprod.104.034470. PubMed DOI

Walsh A., Whelan D., Bielanowicz A., Skinner B., Aitken R.J., O’Bryan M.K., Nixon B. Identification of the molecular chaperone, heat shock protein 1 (chaperonin 10), in the reproductive tract and in capacitating spermatozoa in the male mouse. Biol. Reprod. 2008;78:983–993. doi: 10.1095/biolreprod.107.066860. PubMed DOI

Dun M.D., Smith N.D., Baker M.A., Lin M., Aitken R.J., Nixon B. The chaperonin containing TCP1 complex (CCT/TRiC) is involved in mediating sperm-oocyte interaction. J. Biol. Chem. 2011;286:36875–36887. doi: 10.1074/jbc.M110.188888. PubMed DOI PMC

Bernabò N., Palestini P., Botto L., Mattioli M., Barboni B. Membrane Dynamics Occuring during Capacitation of Mammalian Spermatozoa. In: Erickson B.T., editor. Spermatozoa. Biology, Motility and Function and Chromosomal Abnormalities. Nova Science Publishers, Inc.; New York, NY, USA: 2014. pp. 99–122.

Sutovsky P. Sperm proteasome and fertilization. Reproduction. 2011;142:1–14. doi: 10.1530/REP-11-0041. PubMed DOI

Kerns K., Morales P., Sutovsky P. Regulation of Sperm Capacitation by the 26S Proteasome: An Emerging New Paradigm in Spermatology. Biol. Reprod. 2016;94:117. doi: 10.1095/biolreprod.115.136622. PubMed DOI

Sasanami T., Sugiura K., Tokumoto T., Yoshizaki N., Dohra H., Nishio S., Mizushima S., Hiyama G., Matsuda T. Sperm proteasome degrades egg envelope glycoprotein ZP1 during fertilization of Japanese quail (Coturnix japonica) Reproduction. 2012;144:423–431. doi: 10.1530/REP-12-0165. PubMed DOI

Sawada H., Mino M., Akasaka M. Sperm proteases and extracellular ubiquitin-proteasome system involved in fertilization of ascidians and sea urchins. Adv. Exp. Med. Biol. 2014;759:1–11. doi: 10.1007/978-1-4939-0817-2_1. PubMed DOI

Bottom-up approach to deciphering the targets of the ubiquitin-proteasome system in porcine sperm capacitation