Abstract
Fertilization of an egg by a spermatozoon sets the stage for mammalian development. Viable sperm are a prerequisite for successful fertilization and beyond. Spermatozoa have a unique cell structure where haploid genomic DNA is located in a tiny cytoplasmic space in the head, mitochondria in the midpiece and then the tail, all enclosed by several layers of membrane. Proteins in sperm play vital roles in motility, capacitation, fertilization, egg activation and embryo development. Molecular defects in these proteins are associated with low fertility or in some cases, infertility. This review will first summarize genesis, molecular anatomy and physiology of spermatozoa, fertilization, embryogenesis and then those proteins playing important roles in various aspects of sperm physiology.
Similar content being viewed by others
References
Abbott AL, Ducibella T (2001) Calcium and the control of mammalian cortical granule exocytosis. Front Biosci 6:D792–D806
Aul RB, Oko RJ (2002) The major subacrosomal occupant of bull spermatozoa is a novel histone H2B. Dev Biol 242:376–387
Austin CR (1951) Observations on the penetration of the sperm in the mammalian egg. Aust J Sci Res B 4:581–596
Awda BJ, Buhr MM (2010) Extracellular signal-regulated kinases (ERKs) pathway and reactive oxygen species regulate tyrosine phosphorylation in capacitating boar spermatozoa. Biol Reprod 83(5):750–758
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
Baker MA, Reeves G, Hetherington L, Muller J, Baur I, Aitken RJ (2007) Identification of gene products present in the Triton X soluble and insoluble fractions of human spermatozoa lysates using LC-MS/MS analysis. Proteomics Clin Appl 1:524–532
Bartholomew RA, Parks JE (2007) Identification, localization, and sequencing of fetal bovine VASA homolog. Anim Reprod Sci 101:241–251
Brener E, Rubinstein S, Cohen G, Shternall K, Rivlin J, Breitbart H (2003) Remodeling of the actin cytoskeleton during mammalian sperm capacitation and acrosome reaction. Biol Reprod 68:837–845
Buaas FW, Kirsh AL, Sharma M, McLean DJ, Morris JL, Griswold MD, de Rooij DG, Braun RE (2004) Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet 36:647–652
Chang MC (1951) Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature 168:697–698
Chao HC, Chung CL, Pan HA, Liao PC, Kuo PL, Hsu CC (2011) Protein tyrosine phosphatase non-receptor type 14 is a novel sperm-motility biomarker. J Assist Reprod Genet 28:851–861
Chen L, Wang D, Wu Z, Ma L, Daley GQ (2010) Molecular basis of the first cell fate determination in mouse embryogenesis. Cell Res 20:982–993
Cho C, Bunch DO, Faure JE, Goulding EH, Eddy EM, Primakoff P, Myles DG (1998) Fertilization defects in sperm from mice lacking fertilin beta. Science 281:1857–1859
Cockburn K, Rossant J (2010) Making the blastocyst: lessons from the mouse. J Clin Invest 120:995–1003
Conner SJ, Lefievre L, Hughes DC, Barratt CL (2005) Cracking the egg: increased complexity in the zona pellucida. Hum Reprod 20:1148–1152
Cooney MA, Malcuit C, Cheon B, Holland MK, Fissore RA, D’Cruz NT (2010) Species-specific differences in the activity and nuclear localization of murine and bovine phospholipase C zeta 1. Biol Reprod 83:92–101
Coward K, Ponting CP, Zhang N, Young C, Huang CJ, Chou CM, Kashir J, Fissore RA, Parrington J (2011) Identification and functional analysis of an ovarian form of the egg activation factor phospholipase C Zeta (PLCζ) in pufferfish. Mol Reprod Dev 134:3941–3952
Cox LJ, Larman MG, Saunders CM, Hashimoto K, Swann K, Lai FA (2002) Sperm phospholipase Cf from humans and cynomolgus monkeys triggers Ca2+ oscillations, activation and development of mouse oocytes. Reproduction 124:611–623
Da Ros VG, Maldera JA, Willis WD, Cohen DJ, Goulding EH, Gelman DM, Rubinstein M, Eddy EM, Cuasnicu PS (2008) Impaired sperm fertilizing ability in mice lacking cysteine-rIch secretory protein 1 (CRISP1). Dev Biol 320:12–18
D’Amours O, Frenette G, Fortier M, Leclerc P, Sullivan R (2010) Proteomic comparison of detergent-extracted sperm proteins from bulls with different fertility indexes. Reproduction 139:545–556
de Rooij DG, Grootegoed JA (1998) Spermatogonial stem cells. Curr Opin Cell Biol 10(6):694–701
de Rooij DG, Russell LD (2000) All you wanted to know about spermatogonia but were afraid to ask. J Androl 21:776–798
Dorus S, Wasbrough ER, Busby J, Wilkin EC, Karr TL (2010) Sperm proteomics reveals intensified selection on mouse sperm membrane and acrosome genes. Mol Biol Evol 27:1235–1246
Engvall E, Perlmann P (1971) Enzyme-linked immunosorbent assay (ELISA). Quantitative assay of immunoglobulin G. Immunochemistry 8:871–874
Erikson DW, Way AL, Chapman DA, Killian GJ (2007) Detection of osteopontin on Holstein bull spermatozoa, in cauda epididymal fluid and testis homogenates, and its potential role in bovine fertilization. Reproduction 133:909–917
Evans JP (2002) The molecular basis of sperm–oocyte membrane interactions during mammalian fertilization. Hum Reprod Update 8:297–311
Flesch FM, Wijnand E, van de Lest CH, Colenbrander B, van Golde LM, Gadella BM (2001) Capacitation dependent activation of tyrosine phosphorylation generates two sperm head plasma membrane proteins with high primary binding affinity for the zona pellucida. Mol Reprod Dev 60:107–115
Frapsauce C, Pionneau C, Bouley J, de Larouziere V, Berthaut I, Ravel C, Antoine JM, Soubrier F, Mandelbaum J (2009) Unexpected in vitro fertilization failure in patients with normal sperm: a proteomic analysis. Gynecol Obstet Fertil 37:796–802
Galantino-Homer HL, Visconti PE, Kopf GS (1997) Regulation of protein tyrosine phosphorylation during bovine sperm capacitation by a cyclic adenosine 3′5′-monophosphate-dependent pathway. Biol Reprod 56:707–719
Galantino-Homer HL, Florman HM, Storey BT, Dobrinski I, Kopf GS (2004) Bovine sperm capacitation: assessment of phosphodiesterase activity and intracellular alkalinization on capacitation-associated protein tyrosine phosphorylation. Mol Reprod Dev 67:487–500
Gardner AJ, Evans JP (2006) Mammalian membrane block to polyspermy: new insights into how mammalian eggs prevent fertilisation by multiple sperm. Reprod Fertil Dev 18:53–61
Gardner RL, Rossant J (1979) Investigation of the fate of 4-5 day post-coitum mouse inner cell mass cells by blastocyst injection. J Embryol Exp Morphol 52:141–152
Gardner AJ, Williams CJ, Evans JP (2007) Establishment of the mammalian membrane block to polyspermy: evidence for calcium-dependent and -independent regulation. Reproduction 133:383–393
Gatewood JM, Cook GR, Balhorn R, Schmid CW, Bradbury EM (1990) Isolation of four core histones from human sperm chromatin representing a minor subset of somatic histones. J Biol Chem 265:20662–20666
Gauci VJ, Wright EP, Coorssen JR (2011) Quantitative proteomics: assessing the spectrum of in-gel protein detection methods. J Chem Biol 4:3–29
Goossens K, Van Soom A, Van Poucke M, Vandaele L, Vandesompele J, Van Zeveren A, Peelman LJ (2007) Identification and expression analysis of genes associated with bovine blastocyst formation. BMC Dev Biol 7:64
Goto M, O’Brien DA, Eddy EM (2010) Speriolin is a novel human and mouse sperm centrosome protein. Hum Reprod 25:1884–1894
Goudet G, Mugnier S, Callebaut I, Monget P (2008) Phylogenetic analysis and identification of pseudogenes reveal a progressive loss of zona pellucida genes during evolution of vertebrates. Biol Reprod 78:796–806
Graham JK, Moce E (2005) Fertility evaluation of frozen/thawed semen. Theriogenology 64:492–504
Gupta SK, Bhandari B (2011) Acrosome reaction: relevance of zona pellucida glycoproteins. Asian J Androl 13:97–105
Hahnel AC, Eddy EM (1986) Cell surface markers of mouse primordial germ cells defined by two monoclonal antibodies. Gamete Research 15:10
Hamatani T, Carter MG, Sharov AA, Ko MS (2004) Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell 6:117–131
Han C, Park I, Lee B, Jin S, Choi H, Kwon JT, Kwon YI, Kim do H, Park ZY, Cho C (2011) Identification of heat shock protein 5, calnexin and integral membrane protein 2B as Adam7-interacting membrane proteins in mouse sperm. J Cell Physiol 226:1186–1195
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
Hermann BP, Sukhwani M, Lin CC, Sheng Y, Tomko J, Rodriguez M, Shuttleworth JJ, McFarland D, Hobbs RM, Pandolfi PP et al (2007) Characterization, cryopreservation, and ablation of spermatogonial stem cells in adult rhesus macaques. Stem Cells 25:2330–2338
Hernandez P, Muller M, Appel RD (2006) Automated protein identification by tandem mass spectrometry: issues and strategies. Mass Spectrom Rev 25:235–254
Herrid M, Davey RJ, Hill JR (2007) Characterization of germ cells from pre-pubertal bull calves in preparation for germ cell transplantation. Cell Tissue Res 330:321–329
Ignotz GG, Cho MY, Suarez SS (2007) Annexins are candidate oviductal receptors for bovine sperm surface proteins and thus may serve to hold bovine sperm in the oviductal reservoir. Biol Reprod 77:906–913
Ikawa M, Inoue N, Okabe M (2008) Mechanisms of sperm–egg interactions emerging from gene- manipulated animals. Int J Dev Biol 52:657–664
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, Ikawa M, Okabe M (2011) The mechanism of sperm–egg interaction and the involvement of IZUMO1 in fusion. Asian J Androl 13:81–87
Itach SB, Finklestein M, Etkovitz N, Breitbart H (2012) Hyper-activated motility in sperm capacitation is mediated by phospholipase D-dependent actin polymerization. Dev Biol 362(2):154–161
Ito M, Nagaoka K, Kuroda K, Kawano N, Yoshida K, Harada Y, Shikano T, Miyado M, Oda S, Toshimori K, Mizukami Y, Murata T, Umezawa A, Miyazaki S, Miyado K. (2010) Arrest of spermatogenesis at round spermatids in PLCZ1-deficient mice. 11th Int Symp. On Spermatology (abstract).
Ito J, Parrington J, Fissore RA (2011) PLCzeta and its role as a trigger of development in vertebrates. Mol Reprod Dev 78: 846–853. doi:10.1002/mrd.21359
Januskauskas A, Johannisson A, Rodriguez-Martinez H (2001) Assessment of sperm quality through fluorometry and sperm chromatin structure assay in relation to field fertility of frozen-thawed semen from Swedish AI bulls. Theriogenology 55:947–961
Jones R, James PS, Oxley D, Coadwell J, Suzuki-Toyota F, Howes EA (2008) The equatorial subsegment in mammalian spermatozoa is enriched in tyrosine phosphorylated proteins. Biol Reprod 79:421–431
Kaewmala K, Uddin M, Cinar M, Große-Brinkhaus C, Jonas E, Tesfaye D, Phatsara C, Tholen E, Looft C, Schellander K (2012) Investigation into association and expression of PLCz and COX-2 as candidate genes for boar sperm quality and fertility. Reprod Domest Anim 47:213–223. doi:10.1111/j.1439-0531.2011.01831.x
Kashir J, Heindryckx B, Jones C, De Sutter P, Parrington J, Coward K (2010) Oocyte activation, phospholipase C zeta and human infertility. Human Reprod Update 16:690–703
Kim E, Yamashita M, Kimura M, Honda A, Kashiwabara S, Baba T (2008) Sperm penetration through cumulus mass and zona pellucida. Int J Dev Biol 52(5–6):677–682
Kimura Y, Tateno H, Handel MA, Yanagimachi R (1998a) Factors affecting meiotic and developmental competence of primary spermatocyte nuclei injected into mouse oocytes. Biol Reprod 59:871–877
Kimura Y, Yanagimachi R, Kuretake S, Bortkiewicz H, Perry AC, Yanagimachi H (1998b) Analysis of mouse oocyte activation suggests the involvement of sperm perinuclear material. Biol Reprod 58:1407–1415
Klemm U, Muller-Esterl W, Engel W (1991) Acrosin, the peculiar sperm-specific serine protease. Hum Genet 87:635–641
Kline D, Kline JT (1992) Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg. Dev Biol 149:80–89
Lalancette C, Faure RL, Leclerc P (2006) Identification of the proteins present in the bull sperm cytosolic fraction enriched in tyrosine kinase activity: a proteomic approach. Proteomics 6:4523–4540
Lavon U, Volgani R, Danon D (1971) The proteins of bovine spermatozoa from the caput and cauda epididymidis. J Reprod Fertil 24(2):219–232
Lee GS, Kim HS, Lee SH, Kang MS, Kim DY, Lee CK, Kang SK, Lee BC, Hwang WS (2005) Characterization of pig VASA homolog gene and specific expression in germ-cell lineage. Mol Reprod Dev 72:320–328
Lefievre L, Conner SJ, Salpekar A, Olufowobi O, Ashton P, Pavlovic B, Lenton W, Afnan M, Brewis IA, Monk M, Hughes DC, Barratt CL (2004) Four zona pellucida glycoproteins are expressed in the human. Hum Reprod 19:1580–1586
Lequarre AS, Marchandise J, Moreau B, Massip A, Donnay I (2003) Cell cycle duration at the time of maternal zygotic transition for in vitro produced bovine embryos: effect of oxygen tension and transcription inhibition. Biol Reprod 69:1707–1713
Lie PP, Cheng CY, Mruk DD (2009) Coordinating cellular events during spermatogenesis: a biochemical model. Trends Biochem Sci 34:366–373
Litscher ES, Williams Z, Wassarman PM (2009) Zona pellucida glycoprotein ZP3 and fertilization in mammals. Mol Reprod Dev 76:933–941
Luo J, Megee S, Rathi R, Dobrinski I (2006) Protein gene product 9.5 is a spermatogonia-specific marker in the pig testis: application to enrichment and culture of porcine spermatogonia. Mol Reprod Dev 73:1531–1540
Luo J, Megee S, Dobrinski I (2009) Asymmetric distribution of UCH-L1 in spermatogonia is associated with maintenance and differentiation of spermatogonial stem cells. J Cell Physiol 220:460–468
Luo J, Gupta V, Kern B, Tash JS, Sanchez G, Blanco G, Kinsey WH (2012) Role of FYN kinase in spermatogenesis: defects characteristic of Fyn-null sperm in mice. Biol Reprod 86(1):1–8
Mandal A, Klotz KL, Shetty J, Jayes FL, Wolkowicz MJ, Bolling LC, Coonrod SA, Black MB, Diekman AB, Haystead TA, Flickinger CJ, Herr JC (2003) SLLP1, a unique, intra-acrosomal, non-bacteriolytic, c lysozyme-like protein of human spermatozoa. Biol Reprod 68:1525–1537
Marcello MR, Evans JP (2010) Multivariate analysis of male reproductive function in Inpp 5b-/- mice reveals heterogeneity in defects in fertility, sperm-egg membrane interaction and proteolytic cleavage of sperm ADAMs. Mol Hum Reprod 16:492–505
Margalit I, Rubinstein S, Breitbart H (1997) A novel method for evaluating the acrosomal status of mammalian spermatozoa. Arch Androl 39:87–99
Martinez-Heredia J, Estanyol JM, Ballesca JL, Oliva R (2006) Proteomic identification of human sperm proteins. Proteomics 6:4356–4369
Matwee C, Kamaruddin M, Betts DH, Basrur PK, King WA (2001) The effects of antibodies to heat shock protein 70 in fertilization and embryo development. Mol Hum Reprod 7:829–837
McLaren A, Lawson KA (2005) How is the mouse germ-cell lineage established? Differentiation 73:435–437
Memili E, First NL (2000) Zygotic and embryonic gene expression in cow: a review of timing and mechanisms of early gene expression as compared with other species. Zygote 8:87–96
Naaby-Hansen S, Mandal A, Wolkowicz MJ, Sen B, Westbrook VA, Shetty J, Coonrod SA, Klotz KL, Kim YH, Bush LA, Flickinger CJ, Herr JC (2002) CABYR, a novel calcium-binding tyrosine phosphorylation-regulated fibrous sheath protein involved in capacitation. Dev Biol 242:236–254
Nakagawa T, Nabeshima Y, Yoshida S (2007) Functional identification of the actual and potential stem cell compartments in mouse spermatogenesis. Dev Cell 12:195–206
Novak S, Smith TA, Paradis F, Burwash L, Dyck MK, Foxcroft GR, Dixon WT (2010) Biomarkers of in vivo fertility in sperm and seminal plasma of fertile stallions. Theriogenology 74:956–967
O’Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007–4021
Palmer DK, O’Day K, Margolis RL (1990) The centromere specific histone CENP-A is selectively retained in discrete foci in mammalian sperm nuclei. Chromosoma 100:32–36
Peddinti D, Nanduri B, Kaya A, Feugang JM, Burgess SC, Memili E (2008) Comprehensive proteomic analysis of bovine spermatozoa of varying fertility rates and identification of biomarkers associated with fertility. BMC Syst Biol 2:19. doi:10.1186/1752-0509-2-19
Perl A, Qian Y, Chohan KR, Shirley CR, Amidon W, Banerjee S, Middleton FA, Conkrite KL, Barcza M, Gonchoroff N, Suarez SS, Banki K (2006) Transaldolase is essential for maintenance of the mitochondrial transmembrane potential and fertility of spermatozoa. Proc Natl Acad Sci U S A 103:14813–14818
Phillips BT, Gassei K, Orwig KE (2010) Spermatogonial stem cell regulation and spermatogenesis. Philos Trans R Soc Lond B Biol Sci 365:1663–1678
Primakoff P, Myles DG (2000) The ADAM gene family: surface proteins with adhesion and protease activity. Trends Genet 16:83–87
Primakoff P, Myles DG (2007) Cell–cell membrane fusion during mammalian fertilization. FEBS Lett 581:2174–2180
Ren D, Navarro B, Perez G, Jackson AC, Hsu S, Shi Q, Tilly JL, Clapham DE (2001) A sperm ion channel required for sperm motility and male fertility. Nature 413:603–609
Renart J, Reiser J, Stark GR (1979) Transfer of proteins from gels to diazobenzyloxymethyl-paper and detection with antisera: a method for studying antibody specificity and antigen structure. Proc Natl Acad Sci U S A 76:3116–3120
Rodriquez-Martinez H (2003) Laboratory semen assessment and prediction of fertility: still Utopia. Reprod Dom Anim 38:312–318
Saunders CM, Larman MG, Parrington J, Cox LJ, Royse J, Blayney LM, Swann K, Lai FA (2002) PLC zeta: a sperm-specific trigger of Ca(2+) oscillations in eggs and embryo development. Development 129:3533–3544
Schultz RM (1993) Regulation of zygotic gene activation in the mouse. Bioessays 15:531–538
Schultz RM (2002) The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum Reprod Update 8:323–331
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
Shao M, Ghosh A, Cooke VG, Naik UP, Martin-DeLeon PA (2008) JAM-A is present in mammalian spermatozoa where it is essential for normal motility. Dev Biol 313:246–255
Shetty J, Wolkowicz MJ, Digilio LC, Klotz KL, Jayes FL, Diekman AB, Westbrook VA, Farris EM, Hao Z, Coonrod SA, Flickinger CJ, Herr JC (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
Suarez SS (2008) Regulation of sperm storage and movement in the mammalian oviduct. Int J Dev Biol 52:455–462
Swann K, Yu Y (2008) The dynamics of calcium oscillations that activate mammalian eggs. Int J Dev Biol 52:585–594
Tam PP, Snow MH (1981) Proliferation and migration of primordial germ cells during compensatory growth in mouse embryos. J Embryol Exp Morphol 64:133–147
Tarnasky H, Cheng M, Ou Y, Thundathil JC, Oko R, van der Hoorn FA (2010) Gene trap mutation of murine outer dense fiber protein-2 gene can result in sperm tail abnormalities in mice with high percentage chimaerism. BMC Dev Biol 10:67
Tegelenbosch RA, de Rooij DG (1993) A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H ⁄ 101 F1 hybrid mouse. Mutat Res 290:193–200
Telford NA, Watson AJ, Schultz GA (1990) Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol Reprod Dev 26:90–100
Tovich PR, Oko RJ (2003) Somatic histones are components of the perinuclear theca in bovine spermatozoa. J Biol Chem 278:32431–32438
Toyooka Y, Tsunekawa N, Takahashi Y, Matsui Y, Satoh M, Noce T (2000) Expression and intracellular localization of mouse VASA-homologue protein during germ cell development. Mech Dev 93:139–149
Unlu M, Morgan ME, Minden JS (1997) Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis 18:2071–2077
Van der Heijden GW, Ramos L, Esther B, Baart EB, Van den Berg IM, Derijck AA (2008) Sperm-derived histones contribute to zygotic chromatin in humans. BMC Dev Biol 8:34
Visconti PE, Moore GD, Bailey JL, Leclerc P, Connors SA, Pan D, Olds-Clarke P, Kopf GS (1995) Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development 121:1139–1150
Waheeb R, Hofmann MC (2011) Human spermatogonial stem cells: a possible origin for spermatocytic seminoma. Int J Androl 34:296–305
Wassarman PM (1988) Zona pellucida glycoproteins. Annu Rev Biochem 57:415–442
White KL, Pate BJ, Sessions BR (2010) Oolemma receptors and oocyte activation. Syst Biol Reprod Med 56:365–375
Wilkins MR, Gasteiger E, Gooley AA, Herbert BR, Molloy MP, Binz PA, Ou K, Sanchez JC, Bairoch A, Williams KL, Hochstrasser DF (1999) High-throughput mass spectrometric discovery of protein post-translational modifications. J Mol Biol 289:645–657
Wu AT, Sutovsky P, Manandhar G, Xu W, Katayama M, Day BN, Park KW, Yi YJ, Xi YW, Prather RS, Oko R (2007) PAWP, a sperm-specific WW domain-binding protein, promotes meiotic resumption and pronuclear development during fertilization. J Biol Chem 282:12164–12175
Yamaguchi R, Muro Y, Isotani A, Tokuhiro K, Takumi K, Adham I, Ikawa M, Okabe M (2009) Disruption of ADAM3 impairs the migration of sperm into oviduct in mouse. Biol Reprod 81:142–146
Yin L, Chung CM, Huo R, Liu H, Zhou C, Xu W, Zhu H, Zhang J, Shi Q, Wong HY, Chen J, Lu Y, Bi Y, Zhao C, Du Y, Ma M, Cai Y, Chen WY, Fok KL, Tsang LL, Li K, Ni Y, Chung YW, Zhou Z, Sha J, Chan HC (2009) A sperm GPI-anchored protein elicits sperm–cumulus cross-talk leading to the acrosome reaction. Cell Mol Life Sci 66:900–908
Yoshida N, Amanai M, Fukui T, Kajikawa E, Brahmajosyula M, Iwahori A, Nakano Y, Shoji S, Diebold J, Hessel H et al (2007) Broad, ectopic expression of the sperm protein PLCZ1 induces parthenogenesis and ovarian tumours in mice. Development 134:3941–3952
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Govindaraju, A., Dogan, S., Rodriguez-Osorio, N. et al. Delivering value from sperm proteomics for fertility. Cell Tissue Res 349, 783–793 (2012). https://doi.org/10.1007/s00441-012-1452-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-012-1452-2