Abstract
Molecular biomarkers that can assess sperm acrosome status are very useful for evaluating sperm quality in the field of assisted reproductive technology. In this review, we introduce and discuss the localization and function of acrosomal proteins that have been well studied. Journal databases were searched using keywords, including “human acrosome”, “localization”, “fertilization-related protein”, “acrosomal membrane”, “acrosomal matrix”, “acrosome reaction”, “knockout mouse”, and “acrosome marker”.



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References
Adekunle AO, Arboleda CE, Zervos PH, Gerton GL, Teuscher C (1987) Purification and initial characterization of guinea pig testicular acrosin. Biol Reprod 37:201–210
Adham IM, Nayernia K, Engel W (1997) Spermatozoa lacking acrosin protein show delayed fertilization. Mol Reprod Dev 46:370–376
Anakwe OO, Gerton GL (1990) Acrosome biogenesis begins during meiosis: evidence from the synthesis and distribution of an acrosomal glycoprotein, acrogranin, during guinea pig spermatogenesis. Biol Reprod 42:317–328
Anderson DJ, Michaelson JS, Johnson PM (1989) Trophoblast/leukocyte-common antigen is expressed by human testicular germ cells and appears on the surface of acrosome-reacted sperm. Biol Reprod 41:285–293
Baba T, Kashiwabara S, Watanabe K et al (1989) Activation and maturation mechanisms of boar acrosin zymogen based on the deduced primary structure. J Biol Chem 264:11920–11927
Baba T, Azuma S, Kashiwabara S, Toyoda Y (1994) Sperm from mice carrying a targeted mutation of the acrosin gene can penetrate the oocyte zona pellucida and effect fertilization. J Biol Chem 269:31845–31849
Baba D, Kashiwabara S, Honda A et al (2002) Mouse sperm lacking cell surface hyaluronidase PH-20 can pass through the layer of cumulus cells and fertilize the egg. J Biol Chem 277:30310–30314
Bi M, Hickox JR, Winfrey VP, Olson GE, Hardy DM (2003) Processing, localization and binding activity of zonadhesin suggest a function in sperm adhesion to the zona pellucida during exocytosis of the acrosome. Biochem J 375:477–488
Bianchi E, Doe B, Goulding D, Wright GJ (2014) Juno is the egg Izumo receptor and is essential for mammalian fertilization. Nature 508:483–487
Bleil JD, Wassarman PM (1990) Identification of a ZP3-binding protein on acrosome-intact mouse sperm by photoaffinity crosslinking. Proc Natl Acad Sci USA 87:5563–5567
Brandon CI Jr, Srivastava PN, Heusner GL, Fayrer-Hosken RA (1997) Extraction and quantification of acrosin, beta-N-acetylglucosaminidase, and arylsulfatase-A from equine ejaculated spermatozoa. J Exp Zool 279:301–308
Busso D, Cohen DJ, Hayashi M, Kasahara M, Cuasnicu PS (2005) Human testicular protein TPX1/CRISP-2: localization in spermatozoa, fate after capacitation and relevance for gamete interaction. Mol Hum Reprod 11:299–305
Busso D, Goldweic NM, Hayashi M, Kasahara M, Cuasnicu PS (2007) Evidence for the involvement of testicular protein CRISP2 in mouse sperm–egg fusion. Biol Reprod 76:701–708
Chalbi M, Barraud-Lange V, Ravaux B et al (2014) Binding of sperm protein Izumo1 and its egg receptor Juno drives Cd9 accumulation in the intercellular contact area prior to fusion during mammalian fertilization. Development 141:3732–3739
Cheng A, Le T, Palacios M et al (1994) sperm–egg recognition in the mouse: characterization of sp56, a sperm protein having specific affinity for ZP3. J Cell Biol 125:867–878
Dörig RE, Marcil A, Chopra A, Richardson CD (1993) The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell 75:295–305
Fénichel P, Dohr G, Grivaux C, Cervoni F, Donzeau M, Hsi BL (1990) Localization and characterization of the acrosomal antigen recognized by GB24 on human spermatozoa. Mol Reprod Dev 27:173–178
Ferrer M, Xu W, Oko R (2012a) The composition, protein genesis and significance of the inner acrosomal membrane of eutherian sperm. Cell Tissue Res 349:733–748
Ferrer M, Rodriguez H, Zara L, Yu Y, Xu W, Oko R (2012b) MMP2 and acrosin are major proteinases associated with the inner acrosomal membrane and may cooperate in sperm penetration of the zona pellucida during fertilization. Cell Tissue Res 349:881–895
Florman HM, Fissore RA (2014) Fertilization in mammals. In: Plant TM, Zeleznik A (eds) Knobil and Neill’s physiology of reproduction, vol 1, 4th edn. Acaemic Press, New York, pp 149–196
Forsbach A, Heinlein UA (1998) Intratesticular distribution of cyritestin, a protein involved in gamete interaction. J Exp Biol 201:861–867
Foster JA, Klotz KL, Flickinger CJ et al (1994) Human SP-10: acrosomal distribution, processing, and fate after the acrosome reaction. Biol Reprod 51:1222–1231
Foster JA, Friday BB, Maulit MT et al (1997) AM67, a secretory component of the guinea pig sperm acrosomal matrix, is related to mouse sperm protein sp56 and the complement component 4-binding proteins. J Biol Chem 272:12714–12722
Freemerman AJ, Wright RM, Flickinger CJ, Herr JC (1993) Cloning and sequencing of baboon and cynomolgus monkey intra-acrosomal protein SP-10: homology with human SP-10 and a mouse sperm antigen (MSA-63). Mol Reprod Dev 34:140–148
Fujihara Y, Murakami M, Inoue N et al (2010) Sperm equatorial segment protein 1, SPESP1, is required for fully fertile sperm in mouse. J Cell Sci 123:1531–1536
Fujihara Y, Satouh Y, Inoue N, Isotani A, Ikawa M, Okabe M (2012) SPACA1-deficient male mice are infertile with abnormally shaped sperm heads reminiscent of globozoospermia. Development 139:3583–3589
Fujihara Y, Okabe M, Ikawa M (2014) GPI-anchored protein complex, LY6K/TEX101, is required for sperm migration into the oviduct and male fertility in mice. Biol Reprod 90:1–6
Gao Z, Garbers DL (1998) Species diversity in the structure of zonadhesin, a sperm-specific membrane protein containing multiple cell adhesion molecule-like domains. J Biol Chem 273:3415–3421
Gao Z, Harumi T, Garbers DL (1997) Chromosome localization of the mouse zonadhesin gene and the human zonadhesin gene (ZAN). Genomics 41:119–122
Gibbs GM, Scanlon MJ, Swarbrick J et al (2006) The cysteine-rich secretory protein domain of Tpx-1 is related to ion channel toxins and regulates ryanodine receptor Ca2+ signaling. J Biol Chem 281:4156–4163
Greenstone HL, Santoro F, Lusso P, Berger EA (2002) Human herpesvirus 6 and measles virus employ distinct CD46 domains for receptor function. J Biol Chem 277:39112–39118
Griffiths GS, Galileo DS, Reese K, Martin-Deleon PA (2008a) Investigating the role of murine epididymosomes and uterosomes in GPI-linked protein transfer to sperm using SPAM1 as a model. Mol Reprod Dev 75:1627–1636
Griffiths GS, Miller KA, Galileo DS, Martin-DeLeon PA (2008b) Murine SPAM1 is secreted by the estrous uterus and oviduct in a form that can bind to sperm during capacitation: acquisition enhances hyaluronic acid-binding ability and cumulus dispersal efficiency. Reproduction 135:293–301
Grzmil P, Kim Y, Shamsadin R et al (2001) Human cyritestin genes (CYRN1 and CYRN2) are non-functional. Biochem J 357:551–556
Hamatani T, Tanabe K, Kamei K, Sakai N, Yamamoto Y, Yoshimura Y (2000) 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 62:1201–1208
Hao Z, Wolkowicz MJ, Shetty J et al (2002) SAMP32, a testis-specific, isoantigenic sperm acrosomal membrane-associated protein. Biol Reprod 66:735–744
Hao J, Chen M, Ji S et al (2014) Equatorin is not essential for acrosome biogenesis but is required for the acrosome reaction. Biochem Biophys Res Commun 444:537–542
Hardy DM, Garbers DL (1994) Species-specific binding of sperm proteins to the extracellular matrix (zona pellucida) of the egg. J Biol Chem 269:19000–19004
Hardy DM, Garbers DL (1995) 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 270:26025–26028
Hardy DM, Wild GC, Tung KS (1987) Purification and initial characterization of proacrosins from guinea pig testes and epididymal spermatozoa. Biol Reprod 37:189–199
Hardy DM, Oda MN, Friend DS, Huang TT Jr (1991) A mechanism for differential release of acrosomal enzymes during the acrosome reaction. Biochem J 275(Pt 3):759–766
He XB, Yan YC, Li YP, Koide SS (2003) Cloning of rat sp56, the homologue of mouse sperm ZP3 receptor-sp56. Cell Res 13:121–129
Herlyn H, Zischler H (2008) The molecular evolution of sperm zonadhesin. Int J Dev Biol 52:781–790
Herr JC, Flickinger CJ, Homyk M, Klotz K, John E (1990a) Biochemical and morphological characterization of the intra-acrosomal antigen SP-10 from human sperm. Biol Reprod 42:181–193
Herr JC, Wright RM, John E, Foster J, Kays T, Flickinger CJ (1990b) Identification of human acrosomal antigen SP-10 in primates and pigs. Biol Reprod 42:377–382
Herrero MB, Mandal A, Digilio LC, Coonrod SA, Maier B, Herr JC (2005) Mouse SLLP1, a sperm lysozyme-like protein involved in sperm–egg binding and fertilization. Dev Biol 284:126–142
Honda A, Siruntawineti J, Baba T (2002) Role of acrosomal matrix proteases in sperm–zona pellucida interactions. Hum Reprod Update 8:405–412
Hsu YC, Perin MS (1995) Human neuronal pentraxin II (NPTX2): conservation, genomic structure, and chromosomal localization. Genomics 28:220–227
Inoue N, Ikawa M, Nakanishi T et al (2003) Disruption of mouse CD46 causes an accelerated spontaneous acrosome reaction in sperm. Mol Cell Biol 23:2614–2622
Inoue N, Ikawa M, Isotani A, Okabe M (2005) The immunoglobulin superfamily protein Izumo is required for sperm to fuse with eggs. Nature 434:234–238
Inoue N, Hamada D, Kamikubo H et al (2013) Molecular dissection of IZUMO1, a sperm protein essential for sperm–egg fusion. Development 140:3221–3229
Ito M, Yamatoya K, Yoshida K et al (2010) Appearance of an oocyte activation-related substance during spermatogenesis in mouse and human. Hum Reprod 25:2734–2744
Ito C, Yamatoya K, Yoshida K et al (2013) Integration of the mouse sperm fertilization-related protein equatorin into the acrosome during spermatogenesis as revealed by super-resolution and immunoelectron microscopy. Cell Tissue Res 352:739–750
Ito C, Yamatoya K, Toshimori K (2015) Analysis of the complexity of the sperm acrosomal membrane by super-resolution stimulated emission depletion microscopy compared with transmission electron microscopy. Microscopy 64:279–287
Jin M, Fujiwara E, Kakiuchi Y et al (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
Kawano N, Kang W, Yamashita M et al (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
Kemper C, Chan AC, Green JM et al (2003) Activation of human CD4+ cells with CD3 and CD46 induces a T-regulatory cell 1 phenotype. Nature 421:388–392
Kierszenbaum AL, Tres LL (2004) The acrosome–acroplaxome–manchette complex and the shaping of the spermatid head. Arch Histol Cytol 67:271–284
Kim KS, Gerton GL (2003) Differential release of soluble and matrix components: evidence for intermediate states of secretion during spontaneous acrosomal exocytosis in mouse sperm. Dev Biol 264:141–152
Kim KS, Cha MC, Gerton GL (2001) Mouse sperm protein sp56 is a component of the acrosomal matrix. Biol Reprod 64:36–43
Kim E, Nishimura H, Iwase S, Yamagata K, Kashiwabara S, Baba T (2004) Synthesis, processing, and subcellular localization of mouse ADAM3 during spermatogenesis and epididymal sperm transport. J Reprod Dev 50:571–578
Kim KS, Foster JA, Kvasnicka KW, Gerton GL (2011) Transitional states of acrosomal exocytosis and proteolytic processing of the acrosomal matrix in guinea pig sperm. Mol Reprod Dev 78:930–941
Klemm U, Muller-Esterl W, Engel W (1991) Acrosin, the peculiar sperm-specific serine protease. Hum Genet 87:635–641
Kurth BE, Klotz K, Flickinger CJ, Herr JC (1991) Localization of sperm antigen SP-10 during the six stages of the cycle of the seminiferous epithelium in man. Biol Reprod 44:814–821
Lea IA, Sivashanmugam P, O’Rand MG (2001) Zonadhesin: characterization, localization, and zona pellucida binding. Biol Reprod 65:1691–1700
Lin YN, Roy A, Yan W, Burns KH, Matzuk MM (2007) Loss of zona pellucida binding proteins in the acrosomal matrix disrupts acrosome biogenesis and sperm morphogenesis. Mol Cell Biol 27:6794–6805
Linder B, Bammer S, Heinlein UA (1995) Delayed translation and posttranslational processing of cyritestin, an integral transmembrane protein of the mouse acrosome. Exp Cell Res 221:66–72
Liu MS, Aebersold R, Fann CH, Lee CY (1992) Molecular and developmental studies of a sperm acrosome antigen recognized by HS-63 monoclonal antibody. Biol Reprod 46:937–948
Maeda T, Sakashita M, Ohba Y, Nakanishi Y (1998) Molecular cloning of the rat Tpx-1 responsible for the interaction between spermatogenic and sertoli cells. Biochem Biophys Res Commun 248:140–146
Maeda T, Nishida J, Nakanishi Y (1999) Expression pattern, subcellular localization and structure–function relationship of rat Tpx-1, a spermatogenic cell adhesion molecule responsible for association with sertoli cells. Dev Growth Differ 41:715–722
Manandhar G, Toshimori K (2001) Exposure of sperm head equatorin after acrosome reaction and its fate after fertilization in mice. Biol Reprod 65:1425–1436
Mandal A, Klotz KL, Shetty J et al (2003) SLLP1, a unique, intra-acrosomal, non-bacteriolytic, c lysozyme-like protein of human spermatozoa. Biol Reprod 68:1525–1537
Marie JC, Astier AL, Rivailler P, Rabourdin-Combe C, Wild TF, Horvat B (2002) Linking innate and acquired immunity: divergent role of CD46 cytoplasmic domains in T cell induced inflammation. Nat Immunol 3:659–666
Mizuno M, Harris CL, Johnson PM, Morgan BP (2004) Rat membrane cofactor protein (MCP; CD46) is expressed only in the acrosome of developing and mature spermatozoa and mediates binding to immobilized activated C3. Biol Reprod 71:1374–1383
Mizuno M, Harris CL, Suzuki N, Matsuo S, Morgan BP (2005) Expression of CD46 in developing rat spermatozoa: ultrastructural localization and utility as a marker of the various stages of the seminiferous tubuli. Biol Reprod 72:908–915
Mori E, Baba T, Iwamatsu A, Mori T (1993) Purification and characterization of a 38-kDa protein, sp38, with zona pellucida-binding property from porcine epididymal sperm. Biochem Biophys Res Commun 196:196–202
Mori E, Kashiwabara S, Baba T, Inagaki Y, Mori T (1995) Amino acid sequences of porcine Sp38 and proacrosin required for binding to the zona pellucida. Dev Biol 168:575–583
Morin G, Lalancette C, Sullivan R, Leclerc P (2005) Identification of the bull sperm p80 protein as a PH-20 ortholog and its modification during the epididymal transit. Mol Reprod Dev 71:523–534
Morin G, Sullivan R, Laflamme I, Robert C, Leclerc P (2010) SPAM1 isoforms from two tissue origins are differentially localized within ejaculated bull sperm membranes and have different roles during fertilization. Biol Reprod 82:271–281
Muro Y, Buffone MG, Okabe M, Gerton GL (2012) Function of the acrosomal matrix: zona pellucida 3 receptor (ZP3R/sp56) is not essential for mouse fertilization. Biol Reprod 86:1–6
Nakanishi T, Ikawa M, Yamada S et al (1999) Real-time observation of acrosomal dispersal from mouse sperm using GFP as a marker protein. FEBS Lett 449:277–283
Nayernia K, Adham IM, Shamsadin R, Müller C, Sancken U, Engel W (2002) Proacrosin-deficient mice and zona pellucida modifications in an experimental model of multifactorial infertility. Mol Hum Reprod 8:434–440
Nimlamool W, Bean BS, Lowe-Krentz LJ (2013) Human sperm CRISP2 is released from the acrosome during the acrosome reaction and re-associates at the equatorial segment. Mol Reprod Dev 80:488–502
Nishimura H, Cho C, Branciforte DR, Myles DG, Primakoff P (2001) Analysis of loss of adhesive function in sperm lacking cyritestin or fertilin beta. Dev Biol 233:204–213
Nishimura H, Gupta S, Myles DG, Primakoff P (2011) Characterization of mouse sperm TMEM190, a small transmembrane protein with the trefoil domain: evidence for co-localization with IZUMO1 and complex formation with other sperm proteins. Reproduction 141:437–451
Noland TD, Friday BB, Maulit MT, Gerton GL (1994) The sperm acrosomal matrix contains a novel member of the pentaxin family of calcium-dependent binding proteins. J Biol Chem 269:32607–32614
O’Bryan MK, Loveland KL, Herszfeld D, McFarlane JR, Hearn MT, de Kretser DM (1998) Identification of a rat testis-specific gene encoding a potential rat outer dense fibre protein. Mol Reprod Dev 50:313–322
O’Bryan MK, Sebire K, Meinhardt A et al (2001) Tpx-1 is a component of the outer dense fibers and acrosome of rat spermatozoa. Mol Reprod Dev 58:116–125
Oh-Oka T, Tanii I, Wakayama T, Yoshinaga K, Watanabe K, Toshimori K (2001) Partial characterization of an intra-acrosomal protein, human acrin1 (MN7). J Androl 22:17–24
Okabe M, Yagasaki M, Oda H, Matzno S, Kohama Y, Mimura T (1988) Effect of a monoclonal anti-mouse sperm antibody (OBF13) on the interaction of mouse sperm with zona-free mouse and hamster eggs. J Reprod Immunol 13:211–219
Okada N, Liszewski MK, Atkinson JP, Caparon M (1995) Membrane cofactor protein (CD46) is a keratinocyte receptor for the M protein of the group A streptococcus. Proc Natl Acad Sci USA 92:2489–2493
Olson GE, Winfrey VP, Bi M, Hardy DM, NagDas SK (2004) Zonadhesin assembly into the hamster sperm acrosomal matrix occurs by distinct targeting strategies during spermiogenesis and maturation in the epididymis. Biol Reprod 71:1128–1134
Overstreet JW, Lin Y, Yudin AI et al (1995) Location of the PH-20 protein on acrosome-intact and acrosome-reacted spermatozoa of cynomolgus macaques. Biol Reprod 52:105–114
Phelps BM, Primakoff P, Koppel DE, Low MG, Myles DG (1988) Restricted lateral diffusion of PH-20, a PI-anchored sperm membrane protein. Science 240:1780–1782
Polakoski KL, Parrish RF (1977) Boar proacrosin. Purification and preliminary activation studies of proacrosin isolated from ejaculated boar sperm. J Biol Chem 252:1888–1894
Post TW, Liszewski MK, Adams EM, Tedja I, Miller EA, Atkinson JP (1991) Membrane cofactor protein of the complement system: alternative splicing of serine/threonine/proline-rich exons and cytoplasmic tails produces multiple isoforms that correlate with protein phenotype. J Exp Med 174:93–102
Primakoff P, Hyatt H, Myles DG (1985) A role for the migrating sperm surface antigen PH-20 in guinea pig sperm binding to the egg zona pellucida. J Cell Biol 101:2239–2244
Ramalho-Santos J, Terada Y, Schatten G (2002) VAMP/synaptobrevin as an acrosomal marker for human sperm. Fertil Steril 77:159–161
Reddi PP, Naaby-Hansen S, Aguolnik I et al (1995) Complementary deoxyribonucleic acid cloning and characterization of mSP-10: the mouse homologue of human acrosomal protein SP-10. Biol Reprod 53:873–881
Reddi PP, Shore AN, Acharya KK, Herr JC (2002) Transcriptional regulation of spermiogenesis: insights from the study of the gene encoding the acrosomal protein SP-10. J Reprod Immunol 53:25–36
Reid MS, Blobel CP (1994) Apexin, an acrosomal pentaxin. J Biol Chem 269:32615–32620
Russell LD, Ettlin RA, Sinha-Hikim A, Clegg E (1990) Hitological and histopathological evaluation of the testis. Cache River Press, USA
Sabeur K, Cherr GN, Yudin AI, Primakoff P, Li MW, Overstreet JW (1997) The PH-20 protein in human spermatozoa. J Androl 18:151–158
Sachdev M, Mandal A, Mulders S et al (2012) Oocyte specific oolemmal SAS1B involved in sperm binding through intra-acrosomal SLLP1 during fertilization. Dev Biol 363:40–51
Satouh Y, Inoue N, Ikawa M, Okabe M (2012) Visualization of the moment of mouse sperm–egg fusion and dynamic localization of IZUMO1. J Cell Sci 125:4985–4990
Saxena DK, Tanii I, Yoshinaga K, Toshimori K (1999) Role of intra-acrosomal antigenic molecules acrin 1 (MN7) and acrin 2 (MC41) in penetration of the zona pellucida in fertilization in mice. J Reprod Fertil 117:17–25
Shamsadin R, Adham IM, Nayernia K, Heinlein UA, Oberwinkler H, Engel W (1999) Male mice deficient for germ-cell cyritestin are infertile. Biol Reprod 61:1445–1451
Shetty J, Wolkowicz MJ, Digilio LC et al (2003) SAMP14, a novel, acrosomal membrane-associated, glycosylphosphatidylinositol-anchored member of the Ly-6/urokinase-type plasminogen activator receptor superfamily with a role in sperm–egg interaction. J Biol Chem 278:30506–30515
Siegel MS, Bechtold DS, Kopta CI, Polakoski KL (1986) The rapid purification and partial characterization of human sperm proacrosin using an automated fast protein liquid chromatography (FPLC) system. Biochim Biophys Acta 883:567–573
Sosnik J, Miranda PV, Spiridonov NA et al (2009) Tssk6 is required for Izumo relocalization and gamete fusion in the mouse. J Cell Sci 122:2741–2749
Suryavathi V, Panneerdoss S, Wolkowicz MJ et al (2015) Dynamic changes in equatorial segment protein 1 (SPESP1) glycosylation during mouse spermiogenesis. Biol Reprod 92:1–16
Tanii I, Araki S, Toshimori K (1994) Intra-acrosomal organization of a 90-kilodalton antigen during spermiogenesis in the rat. Cell Tissue Res 277:61–67
Tardif S, Cormier N (2011) Role of zonadhesin during sperm–egg interaction: a species-specific acrosomal molecule with multiple functions. Mol Hum Reprod 17:661–668
Tardif S, Wilson MD, Wagner R et al (2010) Zonadhesin is essential for species specificity of sperm adhesion to the egg zona pellucida. J Biol Chem 285:24863–24870
Thaler CD, Cardullo RA (1995) Biochemical characterization of a glycosylphosphatidylinositol-linked hyaluronidase on mouse sperm. Biochemistry 34:7788–7795
Tokuhiro K, Ikawa M, Benham AM, Okabe M (2012) Protein disulfide isomerase homolog PDILT is required for quality control of sperm membrane protein ADAM3 and male fertility. Proc Natl Acad Sci USA 109:3850–3855
Toshimori K (2009) Dynamics of the mammalian sperm head: modifications and maturation events from spermatogenesis to egg activation. Adv Anat Embryol Cell Biol 204:5–94
Toshimori K (2011) Dynamics of the mammalian sperm membrane modification leading to fertilization: a cytological study. J Electron Microsc (Tokyo) 60[Suppl 1]:S31–S42
Toshimori K, Eddy EM (2014) The Spermatozoon. In: Plant TM, Zeleznik A (eds) Knobil and Neill’s physiology of reproduction, vol 1, 4th edn. Acaemic Press, New York, pp 99–148
Toshimori K, Ito C (2003) Formation and organization of the mammalian sperm head. Arch Histol Cytol 66:383–396
Toshimori K, Tanii I, Araki S, Oura C (1992) Characterization of the antigen recognized by a monoclonal antibody MN9: unique transport pathway to the equatorial segment of sperm head during spermiogenesis. Cell Tissue Res 270:459–468
Toshimori K, Saxena DK, Tanii I, Yoshinaga K (1998) An MN9 antigenic molecule, equatorin, is required for successful sperm–oocyte fusion in mice. Biol Reprod 59:22–29
Tulsiani DR, Abou-Haila A, Loeser CR, Pereira BM (1998) The biological and functional significance of the sperm acrosome and acrosomal enzymes in mammalian fertilization. Exp Cell Res 240:151–164
Wassarman PM (2009) Mammalian fertilization: the strange case of sperm protein 56. BioEssays 31:153–158
Westbrook-Case VA, Winfrey VP, Olson GE (1994) A domain-specific 50-kilodalton structural protein of the acrosomal matrix is processed and released during the acrosome reaction in the guinea pig. Biol Reprod 51:1–13
Westbrook-Case VA, Winfrey VP, Olson GE (1995) Sorting of the domain-specific acrosomal matrix protein AM50 during spermiogenesis in the guinea pig. Dev Biol 167:338–349
Wolkowicz MJ, Shetty J, Westbrook A et al (2003) Equatorial segment protein defines a discrete acrosomal subcompartment persisting throughout acrosomal biogenesis. Biol Reprod 69:735–745
Wolkowicz MJ, Digilio L, Klotz K, Flickinger CJ, Herr JC (2008) Equatorial segment protein (ESP) is a human alloantigen involved in sperm–egg binding and fusion. J Androl 29:272–282
Wright RM, Suri AK, Kornreich B, Flickinger CJ, Herr JC (1993) Cloning and characterization of the gene coding for the human acrosomal protein SP-10. Biol Reprod 49:316–325
Yamagata K, Murayama K, Okabe M et al (1998) Acrosin accelerates the dispersal of sperm acrosomal proteins during acrosome reaction. J Biol Chem 273:10470–10474
Yamaguchi R, Muro Y, Isotani A et al (2009) Disruption of ADAM3 impairs the migration of sperm into oviduct in mouse. Biol Reprod 81:142–146
Yamatoya K, Yoshida K, Ito C et al (2009) Equatorin: identification and characterization of the epitope of the MN9 antibody in the mouse. Biol Reprod 81:889–897
Yanagimachi R (1994) Fertilization. In: Knobil E, Neill JD (eds) The physiology of reproduction, vol 1. Raven Press, New York, pp 189–317
Yatsenko AN, O’Neil DS, Roy A et al (2012) Association of mutations in the zona pellucida binding protein 1 (ZPBP1) gene with abnormal sperm head morphology in infertile men. Mol Hum Reprod 18:14–21
Yoshida K, Ito C, Yamatoya K et al (2010) A model of the acrosome reaction progression via the acrosomal membrane-anchored protein equatorin. Reproduction 139:533–544
Yoshinaga K, Tanii I, Saxena DK, Toshimori K (1998) Immunocytochemical alterations in the intra-acrosomal antigen MN7 during epididymal maturation of guinea pig spermatozoa. Cell Tissue Res 292:427–433
Yoshinaga K, Tanii I, Oh-Oka T, Toshimori K (2000) Transport and rearrangement of the intra-acrosomal protein acrin1 (MN7) during spermiogenesis in the guinea pig testis. Anat Rec 259:131–140
Yoshinaga K, Saxena DK, Oh-oka T, Tanii I, Toshimori K (2001) Inhibition of mouse fertilization in vivo by intra-oviductal injection of an anti-equatorin monoclonal antibody. Reproduction 122:649–655
Yu Y, Xu W, Yi YJ, Sutovsky P, Oko R (2006) The extracellular protein coat of the inner acrosomal membrane is involved in zona pellucida binding and penetration during fertilization: characterization of its most prominent polypeptide (IAM38). Dev Biol 290:32–43
Yu Y, Vanhorne J, Oko R (2009) The origin and assembly of a zona pellucida binding protein, IAM38, during spermiogenesis. Microsc Res Tech 72:558–565
Yuan R, Primakoff P, Myles DG (1997) A role for the disintegrin domain of cyritestin, a sperm surface protein belonging to the ADAM family, in mouse sperm–egg plasma membrane adhesion and fusion. J Cell Biol 137:105–112
Zaneveld LJ, De Jonge CJ (1991) Mammalian sperm acrosomal enzymes and the acrosome reaction. In: Dunbar B, O’Rand M (eds) A comparative overview of mammalian fertilization. Plenum, New York
Zhang H, Martin-DeLeon PA (2003) Mouse Spam1 (PH-20) is a multifunctional protein: evidence for its expression in the female reproductive tract. Biol Reprod 69:446–454
Zhang H, Morales CR, Badran H, El-Alfy M, Martin-DeLeon PA (2004) Spam1 (PH-20) expression in the extratesticular duct and accessory organs of the mouse: a possible role in sperm fluid reabsorption. Biol Reprod 71:1101–1107
Zhou C, Kang W, Baba T (2012) Functional characterization of double-knockout mouse sperm lacking SPAM1 and ACR or SPAM1 and PRSS21 in fertilization. J Reprod Dev 58:330–337
Acknowledgments
The authors would like to thank T. Mutoh, K Ushikoshi, A Tajima, and T Kanamori for their excellent technical assistance. This work is supported by a Grant from the Japan Society for the Promotion of Science in part to C. I. (15K10638), K. T. (25293041) and CREST, Japan Science and Technology Agency.
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Ito, C., Toshimori, K. Acrosome markers of human sperm. Anat Sci Int 91, 128–142 (2016). https://doi.org/10.1007/s12565-015-0323-9
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DOI: https://doi.org/10.1007/s12565-015-0323-9
