Skip to main content

Boar Spermatozoa Within the Oviductal Environment (III): Fertilisation

  • Chapter
  • First Online:
Boar Reproduction

Abstract

This chapter is the last of a series of four chapters about the transit of boar spermatozoa within the female reproductive tract and deals with the fertilisation events that take place during and after a capacitated spermatozoon interacts with the ZP of the oocyte. Thus, we will focus on the mechanisms of gamete binding and interaction, including acrosome exocytosis, ZP-penetration and fusion between sperm and oocyte plasma membranes. In addition, subsequent events that take place after sperm-oocyte fusion, such as sperm chromatin remodelling and sperm-mediated oocyte activation will also be dealt with. To conclude, other novel aspects about the role played by sperm in post-fertilisation and early embryo development events will also be discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adenot PG, Szollosi MS, Geze M, Renard JP, Debey P (1991) Dynamics of paternal chromatin changes in live one-cell mouse embryo after natural fertilization. Mol Reprod Dev 28:23–34

    PubMed  CAS  Google Scholar 

  • Adham IM, Nayernia K, Engel W (1997) Spermatozoa lacking acrosin protein show delayed fertilization. Mol Reprod Dev 46:370–376

    PubMed  CAS  Google Scholar 

  • Aitken RJ (1995) Free radicals, lipid peroxidation and sperm function. Reprod Fertil Dev 7:659–668

    PubMed  CAS  Google Scholar 

  • Aitken RJ (2011) The capacitation-apoptosis highway: oxysterols and mammalian sperm function. Biol Reprod 85:9–12

    PubMed  CAS  Google Scholar 

  • Aitken RJ, De Iuliis GN, Gibb Z, Baker MA (2012) The Simmet lecture: new horizons on an old landscape—oxidative stress, DNA damage and apoptosis in the male germ line. Reprod Domest Anim 47(Suppl. 4):7–14

    PubMed  Google Scholar 

  • Ajduk A, Yamauchi Y, Ward MA (2006) Sperm chromatin remodeling after intra-cytoplasmic sperm injection differs from that of in vitro fertilization. Biol Reprod 75:442–451

    PubMed  CAS  Google Scholar 

  • Alberio R, Zakhartchenko V, Motlik J, Wolf E (2001) Mammalian oocyte activation: lessons from the sperm and implications for nuclear transfer. Int J Dev Biol 45:797–809

    PubMed  CAS  Google Scholar 

  • Alberts B, Johnson A, Walter P, Lewis J, Raff M, Roberts K (2008) Molecular biology of the cell, 5th edn. Garland Science, New York

    Google Scholar 

  • Allan V (1996) Role of motor proteins in organizing the endoplasmic reticulum and Golgi apparatus. Semi Cell Dev Biol 7:335–342

    CAS  Google Scholar 

  • Alm H, Torner H, Blottner S, Nurnberg G, Kanitz W (2001) Effect of sperm cryopreservation and treatment with calcium ionophore or heparin on in vitro fertilization of horse oocytes. Theriogenology 56:817–829

    PubMed  CAS  Google Scholar 

  • Amanai M, Brahmajosyula M, Perry ACF (2006) A restricted role for sperm-borne microRNAs in mammalian fertilization. Biol Reprod 75:877–884

    PubMed  CAS  Google Scholar 

  • Amari S, Yonezawa N, Mitsui S, Katsmata T, Hamano S, Kuwyama M, Hasimoto Y, Suzuki A, Takeda Y, Nakano M (2001) Essential role of the nonreducing terminal α-mannosyl residues of the N-linked carbohydrate chain of bovine zona pellucida glycoproteins in sperm-egg binding. Mol Reprod Dev 59:221–226

    PubMed  CAS  Google Scholar 

  • Ankel-Simons F, Cummins JM (1996) Misconceptions about mitochondria and mammalian fertilization: implications for theories on human evolution. Proc Natl Acad Sci USA 93:13859–13863

    PubMed  CAS  Google Scholar 

  • Arcelay E, Salicioni AM, Wertheimer E, Visconti PE (2008) Identification of proteins undergoing tyrosine phosphorylation during mouse sperm capacitation. Int J Dev Biol 52:463–472

    PubMed  CAS  Google Scholar 

  • Asch R, Simerly C, Ord T, Ord VA (1995) Schatten G (the stages at which human fertilization arrests: microtubule and chromosome configurations in inseminated oocytes which failed to complete fertilization and development in humans. Hum Reprod 10:1897–1906

    PubMed  CAS  Google Scholar 

  • Avendaño C, Franchi A, Jones E, Oehninger S (2008) Pregnancy-specific β-1-glycoprotein 1 and human leukocyte antigen-E mRNA in human sperm: differential expression in fertile and infertile men and evidence of a possible functional role during early development. Hum Reprod 24:270–277

    PubMed  Google Scholar 

  • Avendaño C, Franchi A, Taylor S, Morshedi M, Bocca S, Oehninger S (2009) Fragmentation of DNA in morphologically normal human spermatozoa. Fertil Steril 91:1077–1084

    PubMed  Google Scholar 

  • Baarends WM, Hoogerbrugge JW, Roest HP, Ooms M, Vreeburg J, Hoeijmakers JH, Grootegoed JA (1999a) Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. Dev Biol 207:322–333

    PubMed  CAS  Google Scholar 

  • Baarends M, Roest P, Grootegoed A (1999b) The ubiquitin system in gametogenesis. Mol Cell Endocrinol 151:5–16

    PubMed  CAS  Google Scholar 

  • Baba T, Kashiwabara S, Watanabe K, Itoh H, Michikawa Y, Kimura K, Takada M, Fukamizu A, Arai Y (1989) Activation and maturation mechanisms of boar acrosin zymogen based on the deduced primary structure. J Biol Chem 264:11920–11927

    PubMed  CAS  Google Scholar 

  • Baker MA, Reeves G, Hetherington L, Muller J, Baur I, Aitken RJ (2007) Identification of gene products present in triton X-100 soluble and insoluble fractions of human spermatozoa lysates using LC-MS/MS analysis. Proteomics Clin Appl 1:524–532

    PubMed  CAS  Google Scholar 

  • Baker MA, Hetherington L, Reeves G, Muller J, Aitken RJ (2008) The rat sperm proteome characterized via IPG strip prefractionation and LC-MS/MS identification. Proteomics 8:2312–2321

    PubMed  CAS  Google Scholar 

  • Baker MA, Smith ND, Hetherington L, Taubman K, Graham ME, Robinson PJ, Aitken RJ (2010) Label-free quantitation of phosphopeptide changes during rat sperm capacitation. J Proteom Res 9:718–729

    CAS  Google Scholar 

  • Barroso G, Valdespin C, Vega E, Kershenovich R, Avila R, Avendaño C, Oehninger S (2009) Developmental sperm contributions: fertilization and beyond. Fertil Steril 92:835–848

    PubMed  CAS  Google Scholar 

  • Baska KM, Manandhar G, Feng D, Agca Y, Tengowski MW, Sutovsky M, Yi YJ, Sutovsky P (2008) Mechanism of extracellular ubiquitination in the mammalian epididymis. J Cell Physiol 215:684–696

    PubMed  CAS  Google Scholar 

  • Bazer FW, Song G, Kim J, Dunlap KA, Satterfield MC, Johnson GA, Burghardt RC, Wu G (2012) Uterine biology in pigs and sheep. J Anim Sci Biotechnol 3:23

    PubMed  Google Scholar 

  • Bi M, Hickox R, Winfrey P, Olson E, Hardy M (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

    PubMed  CAS  Google Scholar 

  • Blobel CP (2000) Functional processing of fertilin: evidence for a critical role of proteolysis in sperm maturation and activation. Rev Reprod 5:75–83

    PubMed  CAS  Google Scholar 

  • Boerke A, Tsai PS, García-Gil N, Brewis IA, Gadella BM (2008) Capacitation-dependent reorganization of microdomains in the apical sperm head plasma membrane: functional relationship with zona binding and the zona-induced acrosome reaction. Theriogenology 70:1188–1196

    PubMed  CAS  Google Scholar 

  • Boettger-Tong L, Aarons J, Biegler E, George B, Poirier R (1993) Binding of a murine proteinase inhibitor to the acrosome region of the human sperm head. Mol Reprod Dev 36:346–353

    PubMed  CAS  Google Scholar 

  • Bookbinder H, Cheng A, Bleil D (1995) Tissue- and species-specific expression of SP56, a mouse sperm fertilization protein. Science 269:86–89

    PubMed  CAS  Google Scholar 

  • Braude P, Bolton V, Moore S (1998) Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature 332:459–461

    Google Scholar 

  • Brandt Y, Madej A, Rodríguez-Martínez H, Einarsson S (2007) Effects of exogenous ACTH during oestrus on early embryo development and oviductal transport in the sow. Reprod Domest Anim 42:118–125

    Google Scholar 

  • Breitbart H (2002) Role and regulation of intracellular calcium in acrosomal exocytosis. J Reprod Immunol 53:151–159

    PubMed  CAS  Google Scholar 

  • Breitbart H, Naor Z (1999) Protein kinases in mammalian sperm capacitation and the acrosome reaction. Rev Reprod 4:151–159

    PubMed  CAS  Google Scholar 

  • Brenner A, Kubisch M, Pierce E (2004) Role of the mitochondrial genome in assisted reproductive technologies and embryonic stem cell-based therapeutic cloning. Reprod Fertil Dev 16:743–751

    PubMed  CAS  Google Scholar 

  • Brewis IA, Van Gestel RA, Gadella BM, Jones R, Publicover SJ, Roldan ER, Frayne J, Barratt CL (2005) The spermatozoon at fertilisation: current understanding and future research directions. Hum Fertil (Camb) 8:241–251

    CAS  Google Scholar 

  • Brüssow KP (1985) Distribution of oocytes in oviducts of gilts, following synchronized ovulation. Mh Vet Med 40:264–268

    Google Scholar 

  • Brüssow KP, Rátky J, Rodríguez-Martínez H (2008) Fertilization and early embryonic development in the porcine fallopian tube. Reprod Domest Anim 43(Suppl 2):245–251

    PubMed  Google Scholar 

  • Busso D, Cohen DJ, Hayashi M, Kasahara M, Cuasnicú 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

    PubMed  CAS  Google Scholar 

  • Calafell JM, Nogués C, Ponsà M, Santaló J, Egozcue J (1992) Zona pellucida surface of immature and in vitro matured mouse oocytes: analysis by scanning electron microscopy. J Assist Reprod Genet 9:365–372

    PubMed  CAS  Google Scholar 

  • Calvete JJ, Dostàlovà Z, Sanz L, Adermann K, Thole HH, Töpfer-Petersen E (1996) Mapping the heparin-binding domain of boar spermadhesins. FEBS Lett 379:207–211

    PubMed  CAS  Google Scholar 

  • Calvete JJ, Raida M, Gentzel M, Urbanke C, Sanz L, Töpfer-Petersen E (1997) Isolation and characterization of heparin- and phosphorylcholine-binding proteins of boar and stallion seminal plasma. Primary structure of porcine pB1. FEBS Lett 407:201–206

    PubMed  CAS  Google Scholar 

  • Calvin HI, Bedford JM (1971) Formation of disulphide bonds in the nucleus and accessory structures of mammalian spermatozoa during maturation in the epididymis. J Reprod Fertil Suppl 13:65–75

    PubMed  Google Scholar 

  • Cánovas S, Coy P, Gómez E (2007) First steps in the development of a functional assay for human sperm using pig oocytes. J Androl 28:273–281

    PubMed  Google Scholar 

  • Castle E, Dean J (1999) Manipulating the genome to study reproduction. Mice with ‘‘humanized’’ zonae pellucidae. Hum Reprod 14:1927–1939

    PubMed  CAS  Google Scholar 

  • Cechova D, Töpfer-Petersen E, Henschen E (1988) Boar proacrosin is a single chain molecule which ahs the N-terminus of the acrosin-A chain (light chain). FEBS Lett 241:136–140

    PubMed  CAS  Google Scholar 

  • Chapman R, Barratt L (1996) The role of carbohydrate in sperm-ZP3 adhesion. Mol Hum Reprod 2:767–774

    PubMed  CAS  Google Scholar 

  • Chernomordik LV, Kozlov MM (2008) Mechanics of membrane fusion. Nat Struct Mol Biol 15:675–683

    PubMed  CAS  Google Scholar 

  • Chiu PC, Chung MK, Koistinen R, Koistinen H, Seppala M, Ho PC, Ng EH, Lee KF, Yeung WS (2007) Glycodelin-A interacts with fucosyltransferase on human sperm plasma membrane to inhibit spermatozoa-zona pellucida binding. J Cell Sci 120:33–44

    PubMed  CAS  Google Scholar 

  • Chiu PC, Wong BS, Chung MK, Lam KK, Pang RT, Lee KF, Sumitro SB, Gupta SK, Yeung WS (2008) Effects of native human zona pellucida glycoproteins 3 and 4 on acrosome reaction and zona pellucida binding of human spermatozoa. Biol Reprod 79:869–877

    PubMed  CAS  Google Scholar 

  • Choi YH, Landim-Alvarenga FC, Seidel GE, Squires EL (2003) Effect of capacitation of stallion sperm with polyvinylalcohol or bovine serum albumin on penetration of bovine zona-free or partially zona-removed equine oocytes. J Anim Sci 81:2080–2087

    PubMed  CAS  Google Scholar 

  • Clark F, Oehninger S, Patankar S, Koistinen R, Dell A, Morris HR, Koistinen H, Seppälä M (1996) A role for glycoconjugates in human development: the human feto-embryonic defence system hypothesis. Hum Reprod 11:467–473

    PubMed  CAS  Google Scholar 

  • Clark F, Dell A, Morris R, Patankar M, Oehninger S, Seppälä M (1997) Viewing AIDS from a glycobiological perspective: potential linkages to the human fetoembryonic defence system hypothesis. Mol Hum Reprod 3:5–13

    PubMed  CAS  Google Scholar 

  • Colombero T, Moomjy M, Silis S, Rosenwaks Z, Palermo D (1999) The role of structural integrity of the fertilizing spermatozoon in early human embryogenesis. Zygote 7:157–163

    PubMed  CAS  Google Scholar 

  • Conner J, Lefievre L, Hughes C, Barratt L (2005) Cracking the egg: increased complexity in the zona pellucida. Hum Reprod 20:1148–1152

    PubMed  CAS  Google Scholar 

  • Cowan E, Koppel E, Vargas A, Hunnicutt R (2001) Guinea pig fertilin exhibits restricted lateral mobility in epididymal sperm and becomes freely diffusing during capacitation. Dev Biol 15:502–509

    Google Scholar 

  • Cox JF, Avila J, Saravia F, Santa Maria A (1994) Assessment of fertilizing ability of goat spermatozoa by in vitro fertilization of cattle and sheep intact oocytes. Theriogenology 41:1621–1629

    Google Scholar 

  • Coy P, Cánovas S, Mondéjar I, Saavedra MD, Romar R, Grullón L, Matás C, Avilés M (2008) Oviduct-specific glycoprotein and heparin modulate sperm-zona pellucida interaction during fertilization and contribute to the control of polyspermy. Proc Natl Acad Sci USA 105:15809–15814

    PubMed  CAS  Google Scholar 

  • Coy P, Avilés M (2010) What controls polyspermy in mammals, the oviduct or the oocyte? Biol Rev Camb Philos Soc 85:593–605

    PubMed  Google Scholar 

  • Cross L, Morales P, Overstreet W, Hanson W (1988) Induction of acrosome reactions by the human zona pellucida. Biol Reprod 38:235–244

    PubMed  CAS  Google Scholar 

  • Cummins J (1998) Mitochondrial DNA in mammalian reproduction. Rev Reprod 3:172–182

    PubMed  CAS  Google Scholar 

  • Cummins J, Wakayama T, Yanagimachi R (1998) Fate of microinjected spermatid mitochondria in the mouse oocyte and embryo. Zygote 6:213–222

    PubMed  CAS  Google Scholar 

  • Da Ros V, Busso D, Cohen DJ, Maldera J, Goldweic N, Cuasnicu PS (2007) Molecular mechanisms involved in gamete interaction: evidence for the participation of cysteine-rich secretory proteins (CRISP) in sperm-egg fusion. Soc Reprod Fertil Suppl 65:353–356

    PubMed  Google Scholar 

  • Dadoune JP, Pawlak A, Alfonso MF, Siffro JP, Beebe S (2005) Identification of transcripts by macroarrays, RT-PCR and in situ hybridization in human ejaculate spermatozoa. Mol Hum Reprod 11:133–140

    PubMed  CAS  Google Scholar 

  • Dale B, DeFelice LJ, Ehrenstein G (1985) Injection of a soluble sperm extract into sea urchin eggs triggers the cortical reaction. Experientia 41:1068–1070

    PubMed  CAS  Google Scholar 

  • Darson A, Treviño CL, Wood C, Galindo B, Rodríguez-Miranda E, Acevedo JJ, Hernández-González EO, Beltrán C, Martínez-López P, Nishigaki T (2007) Ion channels in sperm motility and capacitation. Soc Reprod Fertil Suppl 65:229–244

    Google Scholar 

  • Day BN (2000) Reproductive biotechnologies: current status in porcine reproduction. Anim Reprod Sci 60:161–172

    PubMed  Google Scholar 

  • Dell A, Morris HR, Easton RL, Panico M, Patankar M, Oehniger S, Koistinen R, Koistinen H, Seppala M, Clark GF (1995) Structural analysis of the oligosaccharides derived from glycodelin, a human glycoprotein with potent immunosuppressive and contraceptive activities. J Biol Chem 270:24116–24126

    PubMed  CAS  Google Scholar 

  • Dell A, Chalabi S, Easton RL, Haslam SM, Sutton-Smith M, Patankar MS, Lattanzio F, Panico M, Morris HR, Clark GF (2003) Murine and human zona pellucida 3 derived from mouse eggs express identical O-glycans. Proc Natl Acad Sci USA 100:15631–15636

    PubMed  CAS  Google Scholar 

  • Dell’Aquila ME, Fusco S, Lacalandra GM, Maritato F (1996) In vitro maturation and fertilization of equine oocytes recovered during the breeding season. Theriogenology 45:547–560

    PubMed  Google Scholar 

  • Díaz ES, Kong M, Morales P (2007) Effect of fibronectin on proteasome activity, acrosome reaction, tyrosine phosphorylation and intracellular calcium concentrations of human sperm. Hum Reprod 22:1420–1430

    PubMed  Google Scholar 

  • Didion BA, Kasperson KM, Wixon RL, Evenson DP (2009) Boar fertility and sperm chromatin structure status: a retrospective report. J Androl 30:655–660

    PubMed  Google Scholar 

  • Donoghue AM, Johnston LA, Seal US, Armstrong DL, Simmons LG, Gross T, Tilson RL, Wildt DE (1992) Ability of thawed tiger (Panthera tigris) spermatozoa to fertilize conspecific eggs and bind and penetrate domestic cat eggs in vitro. J Reprod Fertil 96:555–564

    PubMed  CAS  Google Scholar 

  • Dostàlovà Z, Calvete JJ, Töpfer-Petersen E (1995a) 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 Hoppe Seyler 376:237–242

    PubMed  Google Scholar 

  • Dostàlovà Z, Calvete JJ, Sanz L, Töpfer-Petersen E (1995b) Boar spermadhesin AWN-1: oligosaccharide and zona pellucida binding characteristics. Eur J Biochem 230:329–336

    PubMed  Google Scholar 

  • Du Y, Liu ML, Jia MC (2008) Identification and characterization of a spermatogenesis-related gene Ube1 in rat testis. Sheng Li Xue Bao 60:382–390

    PubMed  CAS  Google Scholar 

  • Dupont G (1998) Theoretical insights into the mechanism of spiral Ca2+ wave initiation in xenopus oocytes. Am J Physiol 275:C317–C322

    PubMed  CAS  Google Scholar 

  • Duran EH, Gürgan T, Günalp S, Enginsu ME, Yarali H, Ayhan A (1998) A logistic regression model including DNA status and morphology of spermatozoa for prediction of fertilization in vitro. Hum Reprod 13:1235–1239

    PubMed  CAS  Google Scholar 

  • East IJ, Dean J (1984) Monoclonal antibodies as probes of the distribution of ZP2, the major sulfated glycoprotein of the murine zona pellucida. J Cell Biol 98:795–800

    PubMed  CAS  Google Scholar 

  • Edwards RG, Beard HK (1997) Oocyte polarity and cell determination in early mammalian embryos. Mol Hum Reprod 3:863–905

    PubMed  CAS  Google Scholar 

  • Einarsson S, Brandt Y, Rodríguez-Martínez H, Madej A (2008) Conference lecture: influence of stress on estrus, gametes and early embryo development in the sow. Theriogenology 70:1197–1201

    PubMed  CAS  Google Scholar 

  • Ekhlasi-Hundrieser M, Gohr K, Wagner A, Tsolova M, Petrunkina AM, Töpfer-Petersen E (2005) Spermadhesin AQN1 is a candidate receptor molecule involved in the formation of the oviductal sperm reservoir in the pig. Biol Reprod 73:536–545

    PubMed  CAS  Google Scholar 

  • Ekhlasi-Hundrieser M, Schäfer B, Philipp U, Kuiper H, Leeb T, Mehta M, Kirchhoff C, Töpfer-Petersen E (2007) Sperm-binding fibronectin type II-module proteins are genetically linked and functionally related. Gene 392:253–265

    PubMed  CAS  Google Scholar 

  • Eliyahu E, Shalgi R (2002) A role for protein kinase C during rat egg activation. Biol Reprod 67:189–195

    PubMed  CAS  Google Scholar 

  • Ensslin M, Calvete JJ, Thole HH, Sierralta WD, Adermann K, Sanz L, Töpfer-Petersen E (1995) 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 Hoppe Seyler 376:733–738

    PubMed  CAS  Google Scholar 

  • Ensslin M, Vogel T, Calvete JJ, Thole HH, Schmidtke J, Matsuda T, Töpfer-Petersen E (1998) Molecular cloning an characterization of P47: a novel boar sperm-associated zona pellucida-bninding protein homologous to a family of mammalian secretory proteins. Biol Reprod 58:1057–1064

    PubMed  CAS  Google Scholar 

  • Espey LL, Lipner H (1994) Ovulation. In: Knobil E, Neill JD (eds) The physiology of reproduction. Raven Press, New York, pp 725–780

    Google Scholar 

  • Esterhuizen D, Franken R, Becker J, Lourens G, Muller I, van Rooyen H (2002) Defective sperm decondensation: a cause for fertilization failure. Andrologia 34:1–7

    PubMed  CAS  Google Scholar 

  • Fàbrega A, Guyonnet B, Dacheux JL, Gatti JL, Puigmulé M, Bonet S, Pinart E (2011) Expression, immunolocalization and processing of fertilins ADAM-1 and ADAM-2 in the boar (sus domesticus) spermatozoa during epididymal maturation. Reprod Biol Endocrinol 9:96

    PubMed  Google Scholar 

  • Familiari G, Heyn R, Relucenti M, Sathananthan H (2008) Structural changes of the zona pellucida during fertilization and embryo development. Front Biosci 13:6730–6751

    PubMed  Google Scholar 

  • Familiari G, Nottola SA, Macchiarelli G, Micara G, Aragona C, Motta PM (1992) Human zona pellucida during in vitro fertilization: an ultrastructural study using saponin, ruthenium red and osmium-thiocarbohydrazide. Mol Reprod Dev 32:51–61

    PubMed  CAS  Google Scholar 

  • Ficarro S, Chertihin O, Westbrook VA, White F, Jayes F, Kalab P, Marto JA, Shabanowitz J, Herr JC, Hunt DF, Visconti PE (2003) Phosphoproteome analysis of capacitated human sperm. Evidence of tyrosine phosphorylation of a kinase-anchoring protein 3 and valosin-containing protein/p97 during capacitation. J Biol Chem 278:11579–11589

    PubMed  CAS  Google Scholar 

  • Fischer KA, van Leyen K, Lovercamp KW, Manandhar G, Sutovsky M, Feng D, Safranski T, Sutovsky P (2005) 15-lipoxygenase is a component of the mammalian sperm cytoplasmic droplet. Reproduction 130:213–222

    PubMed  CAS  Google Scholar 

  • Fissore A, Reis M, Palermo D (1999) Isolation of the Ca2+ releasing component(s) of mammalian sperm extracts: the search continues. Mol Hum Reprod 5:189–192

    PubMed  CAS  Google Scholar 

  • Fléchon JE, Kopecny V, Pivko J, Pavlok A, Motlik J (2004) Texture of the zona pellucida of the mature pig oocyte: the mammalian egg envelope revisited. Reprod Nutr Dev 44:207–218

    PubMed  Google Scholar 

  • Flesch FM, Gadella BM (2000) Dynamics of the mammalian sperm plasma membrane in the process of fertilization. Biochim Biophys Acta 1469:197–235

    PubMed  CAS  Google Scholar 

  • Flores E, Ramió-Lluch L, Bucci D, Fernández-Novell JM, Peña A, Rodríguez-Gil JE (2011) Freezing-thawing induces alterations in histone H1-DNA binding and the breaking of protein-DNA disulfide bonds in boar sperm. Theriogenology 76:1450–1464

    PubMed  CAS  Google Scholar 

  • Florman M, Corron E, Kim D, Babcock F (1992) Activation of voltage-dependent calcium channels of mammalian sperm is required for zona pellucida-induced acrosomal exocytosis. Dev Biol 152:304–314

    PubMed  CAS  Google Scholar 

  • Florman M, Tombes M, First L, Babcock F (1989) An adhesion-associated agonist from the zona pellucida activates G protein-promoted elevations of internal Ca2+ and pH that mediate mammalian sperm acrosomal exocytosis. Dev Biol 135:133–146

    PubMed  CAS  Google Scholar 

  • Foster HA, Abeydeera LR, Griffin DK, Bridger JM (2005) Non-random chromosome positioning in mammalian sperm nuclei, with migration of the sex chromosomes during late spermatogenesis. J Cell Sci 118:1811–1820

    PubMed  CAS  Google Scholar 

  • Franken DR, Morales J, Habenicht F (1996) Inhibition of G protein in human sperm and its influence on acrosome reaction and zona pellucida binding. Fertil Steril 66:1009–1011

    PubMed  CAS  Google Scholar 

  • Friess AE, Töpfer-Petersen E, Nguyen H, Schill WB (1987) Electron micorscopic localization of a fucose-binding protein in acrosomereacted boar spermatozoa by the fucosyl-peroxidase-gold method. Histochemistry 86:297–303

    PubMed  CAS  Google Scholar 

  • Funahashi H, Ekwall H, Rodríguez-Martínez H (2000) The zona reaction in porcine oocytes fertilized in vivo and in vitro as seen with scanning electron microscopy. Biol Reprod 63:1437–1442

    PubMed  CAS  Google Scholar 

  • Funahashi H, Nagai T (2001) Regulation of in vitro penetration of frozen-thawed boar spermatozoa by caffeine and adenosine. Mol Reprod Dev 58:424–431

    PubMed  CAS  Google Scholar 

  • Fusi F, Montesano M, Bernocchi N, Panzeri C, Ferrara F, Villa A, Bronson R (1996) P-selectin is expressed on the oolemma of human and hamster oocytes following sperm adhesion and is also detected on the equatorial region of acrosome-reacted human spermatozoa. Mol Hum Reprod 2:341–347

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • García-Álvarez O, Maroto-Morales A, Martínez-Pastor F, Fernández-Santos MR, Esteso MC, Pérez-Guzman MD, Soler AJ (2008) Heterologous in vitro fertilization is a good procedure to assess the fertility of thawed ram spermatozoa. Theriogenology 71:643–650

    PubMed  Google Scholar 

  • Gatewood M, Cook R, Balhorn R, Schmid W, Bradbury M (1990) Isolation of four core histones from human sperm chromatin representing a minor subset of somatic histones. J Biol Chem 265:20662–20666

    PubMed  CAS  Google Scholar 

  • Gilbert I, Bissonnette N, Boissonneault G, Vallée M, Robert C (2007) A molecular analysis of the population of mRNA in bovine spermatozoa. Reproduction 133:1073–1086

    PubMed  CAS  Google Scholar 

  • Gineitis A, Zalenskaya A, Yau M, Bradbury M, Zalensky O (2000) Human sperm telomere-binding complex involves histone H2B and secures telomere membrane attachment. J Cell Biol 151:1591–1598

    PubMed  CAS  Google Scholar 

  • Glickman MH, Rubin DM, Coux O, Wefes I, Pfeifer G, Cjeka Z, Baumeister W, Fried VA, Finley D (1998) A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 94:615–623

    PubMed  CAS  Google Scholar 

  • Glickman MH, Ciechanover A (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82:373–428

    PubMed  CAS  Google Scholar 

  • Gorczyca W, Traganos F, Jesionowska H, Darzynkiewicz Z (1993) Presence of DNA strand breaks and increased sensitivity of DNA in situ to denaturation in abnormal human sperm cells: analogy to apoptosis of somatic cells. Exp Cell Res 207:202–205

    PubMed  CAS  Google Scholar 

  • Gosálvez J, López-Fernández C, Fernández JL, Gouraud A, Holt WV (2011) Relationships between the dynamics of iatrogenic DNA damage and genomic design in mammalian spermatozoa from eleven species. Mol Reprod Dev 78:951–961

    PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Greco E, Scarselli F, Iacobelli M, Rienzi L, Ubaldi F, Ferrero S, Franco G, Anniballo N, Mendoza C, Tesarik J (2005) Efficient treatment of infertility due to sperm DNA damage by ICSI with testicular spermatozoa. Hum Reprod 20:226–230

    PubMed  Google Scholar 

  • Green DPL (1987) Mammalian sperm can not penetrate the zona pellcuida soley by force. Exp Cell Res 169:31–38

    PubMed  CAS  Google Scholar 

  • Greve JM, Wassarman PM (1985) Mouse egg extracellular coat is a matrix of interconnected filaments possessing a structural repeat. J Mol Biol 181:253–264

    PubMed  CAS  Google Scholar 

  • Grow DR, Oehninger S, Seltman HJ, Toner JP, Swanson RJ, Kruger TF, Muasher SJ (1994) Sperm morphology as diagnosed by strict criteria: probing the impact of teratozoospermia on fertilization rate and pregnancy outcome in a large in vitro fertilization population. Fertil Steril 62:559–567

    PubMed  CAS  Google Scholar 

  • Grunewald S, Paasch U, Glander HJ, Anderegg U (2005) Mature human spermatozoa do not transcribe novel RNA. Andrologia 37:69–71

    PubMed  CAS  Google Scholar 

  • Hafez ESE (1993) Anatomy of female reproductive tract. In: Hafez ESE (ed) Reproduction in farm animals, 6th edn. Lea and Febiger, Philadelphia

    Google Scholar 

  • Haraguchi CM, Mabuchi T, Hirata S, Shoda T, Tokumoto T, Hoshi K, Yokota S (2007) Possible function of caudal nuclear pocket: degradation of nucleoproteins by ubiquitin-proteasome system in rat spermatids and human sperm. J Histochem Cytochem 55:585–595

    PubMed  CAS  Google Scholar 

  • Harris JD, Hibler DW, Fontenot GK, Hsu KT, Yurewicz EC, Sacco AG (1994) Cloning and characterization of zona pellucida genes and cDNAs from a variety of mammalian species: the ZPA, ZPB and ZPC gene families. DNA Seq 4:361–393

    PubMed  CAS  Google Scholar 

  • Hayashi S, Yang J, Christenson L, Yanagimachi R, Hecht NB (2003) Mouse preimplantation embryos developed from oocytes injected with round spermatids or spermatozoa have similar but distinct patterns of early messenger RNA expression. Biol Reprod 69:1170–1176

    PubMed  CAS  Google Scholar 

  • Hecht NB (1974) A DNA polymerase isolated from bovine spermatozoa. J Reprod Fertil 41:345–354

    PubMed  CAS  Google Scholar 

  • Helfand T, Mikami A, Vallee B, Goldman D (2002) A requirement for cytoplasmic dynein and dynactin in intermediate filament network assembly and organization. J Cell Biol 157:795–806

    PubMed  CAS  Google Scholar 

  • Hermansson U, Axnér E, Holst SB (2007) Application of a zona pellucida binding assay (ZBA) in the domestic cat benefits from the use of in vitro matured oocytes. Acta Vet Scand 49:28

    PubMed  Google Scholar 

  • Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425–479

    PubMed  CAS  Google Scholar 

  • Hewitson L, Simerly C, Schatten G (2000) Cytoskeletal aspects of assisted fertilization. Semin Reprod Med 18:151–159

    PubMed  CAS  Google Scholar 

  • Hewitson L, Simerly CR, Schatten G (2002) Fate of sperm components during assisted reproduction: implications for infertility. Hum Fertil (Camb) 5:110–116

    Google Scholar 

  • Hewitson L, Simerly CR, Schatten G (2003) ICSI, male pronuclear remodeling and cell cycle checkpoints. Adv Exp Med Biol 518:199–210

    PubMed  Google Scholar 

  • Hinrichs K, Love CC, Brinsko SP, Choi YH, Varner DD (2002) In vitro fertilization of in vitro-matured equine oocytes: effect of maturation medium, duration of maturation, and sperm calcium ionophore treatment, and comparison with rates of fertilization in vitro after oviductal transfer. Biol Reprod 67:256–262

    PubMed  CAS  Google Scholar 

  • Hinsch KD, Hinsch E, Meinecke B, Töpfer-Petersen E, Pfisterer S, Schill WB (1994) Identification of mouse ZP3 protein in mammalian oocytes with antisera against synthetic ZP3 peptides. Biol Reprod 51:193–204

    PubMed  CAS  Google Scholar 

  • Hochstrasser M (1996) Ubiquitin-dependent protein degradation. Annu Rev Genet 30:405–439

    PubMed  CAS  Google Scholar 

  • Hokke CH, Damm JB, Penninkhof B, Aitken RJ, Kamerling JP, Vliegenthart JF (1994) Structure of the O-linked carbohydrate chains of porcine zona pellucida glycoproteins. Eur J Biochem 221:491–512

    PubMed  CAS  Google Scholar 

  • Honda A, Siruntawinwti J, Baba T (2002) Role of acrosomal matrix proteinases in sperm-zona pellucida interactiosn. Hum Reprod Update 5:405–412

    Google Scholar 

  • Hoodbhoy T, Dean J (2004) Insights into the molecular basis of sperm-egg recognition in mammals. Reproduction 127:417–422

    PubMed  CAS  Google Scholar 

  • Hoodbhoy T, Joshi S, Boja ES, Williams SA, Stanley P, Dean J (2005) Human sperm do not bind to rat zonae pellucidae despite the presence of four homologous glycoproteins. J Biol Chem 280:12721–12731

    PubMed  CAS  Google Scholar 

  • Hughes DC (2007) ZP genes in the avian species illustrates the dynamic evolution of the vertebrate egg envelope. Cytogenet Genome Res 117:86–91

    PubMed  CAS  Google Scholar 

  • Hunter RH (1984) Pre-ovulatory arrest and peri-ovulatory redistribution of competent spermatozoa in the isthmus of the pig oviduct. J Reprod Fertil 72:203–211

    PubMed  CAS  Google Scholar 

  • Hutvagner G, McLachlan J, Pasquinelli AE, Balint E, Tuschl T, Zamore PD (2001) A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293:834–838

    PubMed  CAS  Google Scholar 

  • Hutvagner G, Zamore PD (2002) A microRNA in a multiple-turnover RNAi enzyme complex. Science 297:2056–2060

    PubMed  CAS  Google Scholar 

  • Hwang JY, Mulligan BP, Kim, HM, Y BC, Lee CK (2012) Quantitative analysis of sperm mRNA in the pig: relationship with early embryo development and capacitation. Reprod Fertil Dev, http://dx.doi.org/10.1071/RD12160 (in press)

  • Ingman M, Kaessmann H, Pääbo S, Gyllensten U (2000) Mitochondrial genome variation and the origin of modern humans. Nature 408:708–713

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Inoue N, Ikawa M, Okabe M (2008) Putative sperm fusion protein IZUMO and the role of N-glycosylation. Biochem Biophys Res Comm 377:910–914

    PubMed  CAS  Google Scholar 

  • Iwamoto K, Ikeda K, Yonezawa N, Noguchi S, Kudo K, Hamano S, Kuwayama M, Nakano M (1999) Disulfide formation in bovine zona pellucida glycoproteins during fertilization: evidence for the involvement of cystine cross-linkages in hardening of the zona pellucida. J Reprod Fertil 117:395–402

    PubMed  CAS  Google Scholar 

  • Iwao Y (2012) Egg activation in physiological polyspermy. Reproduction 144:11–12

    Google Scholar 

  • Izquierdo-Rico MJ, Jiménez-Movilla M, Llop E, Pérez-Oliva AB, Ballesta J, Gutiérrez-Gallego R, Jiménez-Cervantes C, Avilés M (2009) Hamster zona pellucida is formed by four glycoproteins: ZP1, ZP2, ZP3, and ZP4. J Proteome Res 8:926–941

    PubMed  CAS  Google Scholar 

  • Jaffe F (1983) Sources of calcium in egg activation: a review and hypothesis. Dev Biol 99:265–276

    PubMed  CAS  Google Scholar 

  • Jahn R, Scheller RH (2006) SNAREs-engines for membrane fusion. Nat Rev Mol Cell Biol 7:631–643

    PubMed  CAS  Google Scholar 

  • Jin M, Fujiwara E, Kakiuchi Y, Okabe M, Satouh Y, Baba SA, Chiba K, Hirohashi N (2011) Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization. Proc Natl Acad Sci USA 108:4892–4896

    PubMed  CAS  Google Scholar 

  • Jungnickel MK, Marrero H, Birnbaumer L, Lemos JR, Florman HM (2001) Trp2 regulates entry of Ca2+ into mouse sperm triggered by egg ZP3. Nat Cell Biol 3:499–502

    PubMed  CAS  Google Scholar 

  • Kaji K, Oda S, Shikano T, Ohnuki T, Uematsu Y, Sakagami J, Tada N, Miyazaki S, Kudo A (2000) The gamete fusion process is defective in eggs of CD9-deficient mice. Nat Genet 24:279–282

    PubMed  CAS  Google Scholar 

  • Kaneda H, Hayashi J, Takahama S, Taya C, Lindahl KF, Yonekawa H (1995) Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proc Natl Acad Sci USA 92:4542–4546

    PubMed  CAS  Google Scholar 

  • Katayama M, Koshida M, Miyake M (2002) Fate of the acrosome in ooplasm in pigs after IVF and ICSI. Hum Reprod 17:2657–2664

    PubMed  CAS  Google Scholar 

  • Ketting RF, Fischer SE, Bernstein E, Sijen T, Hannon GJ, Plasterk RH (2001) Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev 15:2654–2659

    PubMed  CAS  Google Scholar 

  • Kim NH, Jun SH, Do JT, Uhm SJ, Lee HT, Chung KS (1999) Intracytoplasmic injection of porcine, bovine, mouse, or human spermatozoon into porcine oocytes. Mol Reprod Dev 53:84–91

    PubMed  CAS  Google Scholar 

  • Klemm U, Müller-Esterl W, Engle W (1991) Acrosin, the peculiar sperm-specific serine protease. Hum Genet 87:635–641

    PubMed  CAS  Google Scholar 

  • Kline D, Simoncini L, Mandel G, Maue RA, Kado RT, Jaffe LA (1988) Fertilization events induced by neurotransmitters after injection of mRNA in xenopus eggs. Science 241:464–467

    PubMed  CAS  Google Scholar 

  • Knobil E, Neill JD (1994) The physiology of reproduction, 2nd edn. Raven Press, New York

    Google Scholar 

  • Kong M, Días ES, Morales P (2009) Participation of the human sperm proteasome in the capacitation process and its regulation by protein kinase A and tyrosine kinase. Biol Reprod 80:1026–1035

    PubMed  CAS  Google Scholar 

  • Koppers AJ, Mitchell LA, Wang P, Lin M, Aitken RJ (2011) Phosphoinositide 3-kinase signalling pathway involvement in a truncated apoptotic cascade associated with motility loss and oxidative DNA damage in human spermatozoa. Biochem J 436:687–698

    PubMed  CAS  Google Scholar 

  • Kouba AJ, Atkinson MW, Gandolf AR, Roth TL (2001) Species-specific sperm-egg interaction affects the utility of a heterologous bovine in vitro fertilization system for evaluating antelope sperm. Biol Reprod 65:1246–1251

    PubMed  CAS  Google Scholar 

  • Kouchi Z, Fukami K, Shikano T, Oda S, Nakamura Y, Takenawa T, Miyazaki S (2004) Recombinant phospholipase Cζ has high Ca2+ sensitivity and induces Ca2+ oscillations in mouse eggs. J Biol Chem 279:10408–10412

    PubMed  CAS  Google Scholar 

  • Kramer JA, Krawetz SA (1997) RNA in spermatozoa: implications for the alternative haploid genome. Mol Hum Reprod 3:473–478

    PubMed  CAS  Google Scholar 

  • Krawetz A (2005) Paternal contribution: new insights and future challenges. Nat Rev Genet 6:633–642

    PubMed  CAS  Google Scholar 

  • Kudo K, Yonezawy N, Katsumata T, Aoki H, Nakano M (1998) Localization of carbohydrate chains of pig sperm ligand in the glycoprotein ZPB of egg zona pellucida Eur. J Biol 252:492–499

    CAS  Google Scholar 

  • Kumar G, Patel D, Naz RK (1993) c-MYC mRNA is present in human sperm cells. Cell Mol Biol Res 39:111–117

    PubMed  CAS  Google Scholar 

  • Kvist U (1980) Sperm nuclear chromatin decondensation ability. An in vitro study on ejaculated human spermatozoa. Acta Physiol Scand Suppl 486:1–24

    PubMed  CAS  Google Scholar 

  • Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T (2001) Identification of novel genes coding for small expressed RNAs. Science 294:853–858

    PubMed  CAS  Google Scholar 

  • Lambard S, Galeraud-Denis I, Martin G, Levy R, Chocat A, Carreau S (2004) Analysis and significance of mRNA in human ejaculated sperm from normozoospermic donors: relationship to sperm motility and capacitation. Mol Hum Reprod 10:535–541

    PubMed  CAS  Google Scholar 

  • Landim-Alvarenga FC, Alvarenga MA, Seidel GE Jr, Squires EL, Graham JK (2001) Penetration of zona-free hamster, ovine and equine oocytes by stallion and bull spermatozoa pretreated with equine follicular fluid, dilauroylphosphatidylcholine or calcium ionophore A23187. Theriogenology 56:937–953

    PubMed  CAS  Google Scholar 

  • Larson L, DeJonge J, Barnes M, Jost K, Evenson P (2000) Sperm chromatin structure assay parameters as predictors of failed pregnancy following assisted reproductive techniques. Hum Reprod 15:1717–1722

    PubMed  CAS  Google Scholar 

  • Lau NC, Lim LP, Weinstein EG, Bartel DP (2001) An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294:858–862

    PubMed  CAS  Google Scholar 

  • Lee A, Check H, Kopf A (1992) Guanine nucleotide-binding regulatory protein in human sperm mediates acrosomal exocytosis induced by the human zona pellucida. Mol Reprod Dev 31:78–86

    PubMed  CAS  Google Scholar 

  • Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854

    PubMed  CAS  Google Scholar 

  • Lefièvre 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

    PubMed  Google Scholar 

  • Leyton L, LeGuen P, Bunch D, Saling PM (1992) Regulation of mouse gamete interaction by a sperm tyrosine kinase. Proc Natl Acad Sci USA 89:11692–11695

    PubMed  CAS  Google Scholar 

  • Li GP, Seidel GE, Squires EL (2003) Intracytoplasmic sperm injection of bovine oocytes with stallion spermatozoa. Theriogenology 59:1143–1155

    PubMed  Google Scholar 

  • Lin SL, Kim H, Ying SY (2007) Intron-mediated RNA interference and microRNA (miRNA). Front Biosci 13:2216–2230

    Google Scholar 

  • Linfor J, Berger T (2000) Potential role of αv and β1 integrins as oocyte adhesion molecules during fertilization in pigs. J Reprod Fertil 120:65–72

    PubMed  CAS  Google Scholar 

  • Litscher ES, Wassarman PM (2007) Egg extracellular coat proteins: from fish to mammals. Histol Histopathol 22:337–347

    PubMed  CAS  Google Scholar 

  • Madej A, Lang A, Brandt Y, Kindahl H, Madsen MT, Einarsson S (2005) Factors regulating ovarian function in pigs. Domestic Anim Endocrinol 29:347–361

    CAS  Google Scholar 

  • Maleszewski M, Kline D, Yanagimachi R (1995) Activation of hamster zona-free oocytes by homologous and heterologous spermatozoa. J Reprod Fertil 105:99–107

    PubMed  CAS  Google Scholar 

  • Marchiani S, Tamburrino L, Maoggi A, Vannelli GB, Forti G, Baldi E, Muratori M (2007) Characterization of M540 bodies in human semen: evidence that they are apoptotic bodies. Mol Hum Reprod 13:621–631

    PubMed  CAS  Google Scholar 

  • Matson PL, Vaid P, Parsons JH, Goswamy R, Collins WP, Pryor JP (1987) Use of the heterologous ovum penetration test to predict the fertilising capacity of human spermatozoa. Clin Reprod Fertil 5:5–13

    PubMed  CAS  Google Scholar 

  • Martens S, McMahon HT (2008) Mechanisms of membrane fusion: disparate players and common principles. Nat Rev Mol Cell Biol 9:543–556

    PubMed  CAS  Google Scholar 

  • Matsukawa K, Takahashi M, Hanada A (2002) Assay for penetrability of frozen-thawed stallion spermatozoa into zona-free hamster oocytes. J Reprod Dev 48:539–544

    Google Scholar 

  • Maximov A, Tang J, Yang X, Pang ZP, Sudhof TC (2009) Complexin controls the force transfer from SNARE complexes to membranes in fusion. Science 323:516–521

    PubMed  CAS  Google Scholar 

  • Mburu JN, Einarsson S, Kindahl H, Madej A, Rodríguez-Martínez H (1998) Effects of post-ovulatory food deprivation on oviductal sperm concentration, embryo development and hormonal profiles in the pig. Anim Reprod Sci 52:221–234

    PubMed  CAS  Google Scholar 

  • McLay DW, Clarke HJ (2003) Remodelling the paternal chromatin at fertilization in mammals. Reproduction 125:625–633

    PubMed  CAS  Google Scholar 

  • Michaut M, Tomes CN, De BG, Yunes R, Mayorga LS (2000) Calcium triggered acrosomal exocytosis in human spermatozoa requires the coordinated activation of Rab3A and N-ethylmaleimide-sensitive factor. Proc Natl Acad Sci USA 97:9996–10001

    PubMed  CAS  Google Scholar 

  • Michelmann HW, Rath D, Töpfer-Petersen E, Schwartz P (2007) Structural and functional events on the porcine zona pellucida during maturation, fertilization and embryonic development: a scanning electron microscopy analysis. Reprod Domest Anim 42:594–602

    PubMed  CAS  Google Scholar 

  • Miller D, Tang PZ, Skinner C, Lilford R (1994) Differential RNA finger printing as a tool in the analysis of spermatozoal gene expression. Hum Reprod 9:864–869

    PubMed  CAS  Google Scholar 

  • Miller J, Macek B, Shur D (1992) Complementarity between sperm surface beta -1,4-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding. Nature 357:589–593

    PubMed  CAS  Google Scholar 

  • Miyado K, Yamada G, Yamada S, Hasuwa H, Nakamura Y, Ryu F, Suzuki K, Kosai K, Inoue K, Ogura A, Okabe M, Mekada E (2000) Requirement of CD9 on the egg plasma membrane for fertilization. Science 287:321–324

    PubMed  CAS  Google Scholar 

  • Moomjy M, Colombero LT, Veeck L, Rosenwaks Z, Palermo D (1999) Sperm integrity is critical for normal mitotic division and early embryonic development. Mol Hum Reprod 5:836–844

    PubMed  CAS  Google Scholar 

  • Morales P, Kong M, Pizarro E, Pasten C (2003) Participation of the sperm proteasome in human fertilization. Hum Reprod 18:1010–1017

    PubMed  CAS  Google Scholar 

  • Morales P, Pizarro E, Kong M, Jara M (2004) Extracellular localization of proteasomes in human sperm. Mol Reprod Dev 68:115–124

    PubMed  CAS  Google Scholar 

  • Morales P, Díaz ES, Kong M (2007) Proteasome activity and its relationship with protein phosphorylation during capacitation and acrosome reaction in human spermatozoa. Soc Reprod Fertil Suppl 65:269–273

    PubMed  CAS  Google Scholar 

  • Moreno RD, Barros C (2000) A basic 18-amino acid peptide contains the polysulfate-binding domain responsible for activation of the boar proacrosin/acrosin system. Biol Reprod 62:1536–1542

    PubMed  CAS  Google Scholar 

  • Mori E, Kashiwabara S, Baba T, Inagaki AY, Mori T (1995) Amino acid sequences of porcine Sp38 and proacrosin required for binding to the zona pellucida. Dev Biol 168:575–593

    PubMed  CAS  Google Scholar 

  • Mori E, Hedrick JL, Wardrip NJ, Mori T, Takasaki S (1998) Occurrence of reducing terminal N-acetylglucosamine 3-sulfate and fucosylated outer chains in acidic N-glycans of porcine zona pellucida glycoproteins. Glycoconj J 15:447–456

    PubMed  CAS  Google Scholar 

  • Mourelatos Z, Dostie J, Paushkin S, Sharma A, Charroux B, Abel L, Rappsilber J, Mann M, Dreyfuss G (2002) miRNPs: a novel class of ribonucleoproteins containing numerous microRNAs. Genes Dev 16:720–728

    PubMed  CAS  Google Scholar 

  • Mugnier S, Dell’Aquila ME, Pelaez J, Douet C, Ambruosi B, De Santis T, Lacalandra GM, Lebos C, Sizaret PY, Delaleu B, Monget P, Mermillod P, Magistrini M, Meyers SA, Goudet G (2009) New insights into the mechanisms of fertilization: comparison of the fertilization steps, composition, and structure of the zona pellucida between horses and pigs. Biol Reprod 81:856–870

    PubMed  CAS  Google Scholar 

  • Mwanza AM, Englund P, Kindahl H, Lundeheim N, Einarsson S (2000a) Effects of post-ovulatory food deprivation on the hormonal profiles, activity of the oviduct and ova transport in sows. Anim Reprod Sci 59:185–199

    PubMed  CAS  Google Scholar 

  • Mwanza AM, Madej A, Kindahl H, Lundeheim N, Einarsson S (2000b) Postovulatory effect of repeated administration of ACTH on the contractile activity of the oviduct, ova transport and endocrine status of recently ovulated and unrestrained sows. Theriogenology 54:1305–1316

    PubMed  CAS  Google Scholar 

  • Mwanza AM, Razdan P, Hultén F, Einarsson S (2002a) Transport of fertilised and unfertilised ova in sows. Anim Reprod Sci 74:69–74

    PubMed  CAS  Google Scholar 

  • Mwanza AM, Einarsson S, Madej A, Lundeheim N, Rodríguez-Martínez H, Kindahl H (2002b) Postovulatory effect of repeated administration of prostaglandin F on the endocrine status, ova transport, binding of accessory spermatozoa to the zona pellucida and embryo development of recently ovulated sows. Theriogenology 58:1111–1124

    PubMed  CAS  Google Scholar 

  • Nagai T, Funahashi H, Yoshioka K, Kikuchi K (2006) Update of in vitro production of porcine embryos. Front Biosci 11:2565–2573

    PubMed  CAS  Google Scholar 

  • Nakamura S, Terada Y, Horiuchi T, Emuta C, Murakami T, Yaegashi N, Okamura K (2001) Human sperm aster formation and pronuclear decondensation in bovine eggs following intracytoplasmic sperm injection using a piezo-driven pipette: a novel assay for human sperm centrosomol function. Biol Reprod 65:1359–1363

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Naz RK (1998) Effect of actinomycin D and cycloheximide on human sperm function. Arch Androl 41:135–142

    PubMed  CAS  Google Scholar 

  • Nazarov IB, Shlyakhtenko LS, Lyubchenko YL, Zalenskaya IA, Zalensky AO (2008) Sperm chromatin released by nucleases. Syst Biol Reprod Med 54:37–46

    PubMed  CAS  Google Scholar 

  • Niemann H, Rath D (2001) Progress in reproductive biotechnology in swine. Theriogenology 56:1291–1304

    PubMed  CAS  Google Scholar 

  • Nikolettos N, Küpker W, Demirel C, Schöpper B, Blasig C, Sturm R, Felberbaum R, Bauer O, Diedrich K, Al-Hasani S (1999) Fertilization potential of spermatozoa with abnormal morphology. Hum Reprod 14(Suppl 1):47–70

    PubMed  Google Scholar 

  • Noguchi S, Hatanaka Y, Tobita T, Nakano M (1992) Structural analysis of the N-linked carbohydrate chains of the 55-kDa glycoprotein family (PZP3) from porcine zona pellucida. Eur J Biochem 207:1130

    PubMed  CAS  Google Scholar 

  • Noguchi S, Nakano M (1992) Structure of the acidic N-linked carbohydrate chains of the 55-kDa glycoprotein family (PZP3) from porcine zona pellucida. Eur J Biochem 209:883–894

    PubMed  CAS  Google Scholar 

  • Noguchi S, Yonezawa N, Katsumata T, Hashizume K, Kuwayama M, Hamano S, Watanabe S, Nakano M (1994) Characterization of the zona pellucida glycoproteins from bovine ovarian and fertilized eggs. Biochim Biophys Acta 1201:7–14

    PubMed  CAS  Google Scholar 

  • Nonchev S, Tsanev R (1990) Protamine-histone replacement and DNA replication in the male mouse pronucleus. Mol Reprod Dev 25:72–76

    PubMed  CAS  Google Scholar 

  • O’Brien J, Zini A (2005) Sperm DNA integrity and male infertility. Urology 65:16–22

    PubMed  Google Scholar 

  • O’Rand M, Welch JE, Fisher SJ (1986) Sperm membrane and zona pellucida interaction during fertilization. In: Dhinsa DS, Bahl O (eds) Molecular and cellular aspects of reproduction. Plenum Press, New York, pp 131–144

    Google Scholar 

  • Odorisio T, Mahadevaiah SK, McCarrey JR, Burgoyne PS (1996) Transcriptional analysis of the candidate spermatogenesis gene Ube1y and of the closely related Ube1x shows that they are coexpressed in spermatogonia and spermatids but are repressed in pachytene spermatocytes. Dev Biol 180:336–343

    PubMed  CAS  Google Scholar 

  • Oehninger S (2001) Molecular basis of human sperm-zona pellucida interaction. Cells Tissues Organs 168:58–64

    PubMed  CAS  Google Scholar 

  • Oehninger S (2003) Biochemical and functional characterization of the human zona pellucida. Reprod Biomed Online 7:641–648

    PubMed  CAS  Google Scholar 

  • Oehninger S, Acosta A, Veeck L, Simonetti S, Muasher J (1989) Delayed fertilization during in vitro fertilization and embryo transfer cycles: analysis of causes and impact on overall results. Fertil Steril 52:991–997

    PubMed  CAS  Google Scholar 

  • Oehninger S, Veeck L, Lanzendorf S, Maloney M, Toner J, Muasher S (1995) Intracytoplasmic sperm injection: achievement of high pregnancy rates in couples with severe male factor infertility is dependent primarily upon female and not male factors. Fertil Steril 64:977–981

    PubMed  CAS  Google Scholar 

  • Oehninger S, Kruger TF, Simon T, Jones D, Mayer J, Lanzendorf S, Toner JP, Muasher SJ (1996) A comparative analysis of embryo implantation potential in patients with severe teratozoospermia undergoing in vitro fertilization with a high insemination concentration or intracytoplasmic sperm injection. Hum Reprod 11:1086–1089

    PubMed  CAS  Google Scholar 

  • Olsen PH, Ambros V (1999) The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev Biol 216:671–680

    PubMed  CAS  Google Scholar 

  • Ostermeier C, Dix J, Millar D, Khatri P, Krawetz A (2002) Spermatozoal RNA profiles of normal fertile men. Lancet 360:772–777

    PubMed  CAS  Google Scholar 

  • Ostermeier C, Miller D, Huntriss D, Diamond P, Krawetz A (2004) Reproductive biology: delivering spermatozoan RNA to the oocyte. Nature 429:154

    PubMed  CAS  Google Scholar 

  • Ostermeier C, Goodrich J, Moldenhauer S, Diamond P, Krawetz A (2005) A suite of novel human spermatozoal RNAs. J Androl 26:70–74

    PubMed  CAS  Google Scholar 

  • Ozgur K, Patankar MS, Oehninger S, Clark GF (1998) Direct evidence for the involvement of carbohydrate sequences in human sperm-zona pellucida binding. Mol Hum Reprod 4:318–324

    PubMed  CAS  Google Scholar 

  • Pang PC, Tissot B, Drobnis EZ, Sutovsky P, Morris HR, Clark GF, Dell A (2007) Expression of bisecting type and Lewisx/Lewisy terminated N-glycans on human sperm. J Biol Chem 282:36593–36602

    PubMed  CAS  Google Scholar 

  • Parinaud J, Mieusset R, Vieitez G, Labal B, Richoilley G (1993) Influence of sperm parameters on embryo quality. Fertil Steril 60:888–892

    PubMed  CAS  Google Scholar 

  • Parrington J, Swann K, Shevchenko VI, Sesay AK, Lai FA (1996) Calcium oscillations in mammalian eggs triggered by a soluble sperm protein. Nature 379:364–368

    PubMed  CAS  Google Scholar 

  • Pasten C, Morales P, Kong M (2005) Role of the sperm proteasome during fertilization and gamete interaction in the mouse. Mol Reprod Dev 71:209–219

    PubMed  CAS  Google Scholar 

  • Patankar MS, Ozgur K, Oehninger S, Dell A, Morris H, Seppala M, Clark GF (1997) Expression of glycans linked to natural killer cell inhibition on the human zona pellucida. Mol Hum Reprod 3:501–505

    PubMed  CAS  Google Scholar 

  • Payne C, Rawe V, Ramalho-Santos J, Simerly C, Schatten G (2003) Preferentially localized dynein and perinuclear dynactin associate with nuclear pore complex proteins to mediate genomic union during mammalian fertilization. J Cell Sci 116:4727–4738

    PubMed  CAS  Google Scholar 

  • Perreault SD (1992) Chromatin remodeling in mammalian zygotes. Mutat Res 296:43–55

    PubMed  CAS  Google Scholar 

  • Perreault SD, Wolff RA, Zirkin BR (1984) The role of disulfide bond reduction during mammalian sperm nuclear decondensation in vivo. Dev Biol 101:160–167

    PubMed  CAS  Google Scholar 

  • Perreault SD, Barbee RR, Slott VL (1988) Importance of glutathione in the acquisition and maintenance of sperm nuclear decondensing activity in maturing hamster oocytes. Dev Biol 125:181–186

    PubMed  CAS  Google Scholar 

  • Pessot A, Brito M, Figueroa J, Concha I, Yanez A, Burzio O (1989) Presence of RNA in the sperm nucleus. Biochem Biophys Res Comm 158:272–278

    PubMed  CAS  Google Scholar 

  • Petrunkina AM, Läkamp A, Gentzel M, Eklhasi-Hundrieser M, Töpfer-Petersen E (2003) Fate of lactadherin P47 during post-testicular maturation and capacitation of boar spermatozoa. Reproduction 125:377–387

    PubMed  CAS  Google Scholar 

  • Philpott A, Leno GH (1992) Nucleoplasmin remodels sperm chromatin in Xenopus egg extracts. Cell 69:759–767

    PubMed  CAS  Google Scholar 

  • Pizarro E, Pasten C, Kong M, Morales P (2004) Proteasomal activity in mammalian spermatozoa. Mol Reprod Dev 69:87–93

    PubMed  CAS  Google Scholar 

  • Primakoff P, Myles DG (2000) The ADAM gene family: surface proteins with adhesion and protease activity. Trends Genet 16:83–87

    PubMed  CAS  Google Scholar 

  • Provost P, Dishart D, Doucet J, Frendewey D, Samuelsson B, Radmark O (2002) Ribonuclease activity and RNA binding of recombinant human Dicer. EMBO J 21:5864–5874

    PubMed  CAS  Google Scholar 

  • Puigmulé M, Fàbrega A, Yeste M, Bonet S, Pinart E (2011) Study of the proacrosin-acrosin system in epididymal, ejaculated and in vitro capacitated boar spermatozoa. Reprod Fertil Dev 23:837–845

    PubMed  Google Scholar 

  • Pusateri AE, Rothschild MF, Warner CM, Ford SP (1990) Changes in morphology, cell number, cell size and cellular estrogen content of individual littermate pig conceptuses on days 9 to 13 of gestation. J Anim Sci 68:3727–3735

    PubMed  CAS  Google Scholar 

  • Rankin TL, Coleman JS, Epifano O, Hoodbhoy T, Turner SG, Castle PE, Lee E, Gore-Langton R, Dean J (2003) Fertility and taxon-specific sperm binding persist after replacement of mouse “sperm receptors” with human homologs. Dev Cell 5:33–43

    PubMed  CAS  Google Scholar 

  • Rankin TL, Tong ZB, Castle PE, Lee E, Gore-Langton R, Nelson LM, Dean J (1998) Human ZP3 restores fertility in Zp3 null mice without affecting order-specific sperm binding. Development 125:2415–2424

    PubMed  CAS  Google Scholar 

  • Rath D, Töpfer-Petersen E, Michelmann HW, Schwartz P, Ebeling S (2005) Zona pellucida characteristics and sperm binding patterns of in vivo and in vitro produced porcine oocytes inseminated with differently prepared spermatozoa. Theriogenology 63:352–362

    PubMed  Google Scholar 

  • Rath D, Töpfer-Petersen E, Michelmann HW, Schwartz P, Von Witzendorff D, Ebeling S, Ekhlasi-Hundrieser M, Piehler E, Petrunkina A, Romar R (2006) Structural, biochemical and functional aspects of sperm-oocyte interactions in pigs. Soc Reprod Fertil Suppl 62:317–330

    PubMed  CAS  Google Scholar 

  • Rawe Y, Olmedo B, Nodar N, Doncel D, Acosta A, Vitullo D (2000) Cytoskeletal organization defects and abortive activation in human oocytes after IVF and ICSI failure. Mol Hum Reprod 6:510–516

    PubMed  CAS  Google Scholar 

  • Rawe VY, Días ES, Abdelmassih R, Wojcik C, Morales P, Sutovsky P, Chemes HE (2008) The role of sperm proteasomes during sperm aster formation and early zygote development: implications for fertilization failure in humans. Hum Reprod 23:573–580

    PubMed  CAS  Google Scholar 

  • Razdan P, Mwanza A, Kindahl H, Hultén F, Einarsson S (2001) Effects of post-ovulatory food deprivation on ova transport, hormonal profiles and metabolic changes in sows. Acta Vet Scand 42:45–55

    PubMed  CAS  Google Scholar 

  • Razdan P, Mwanza A, Kindahl H, Rodríguez-Martínez H, Hultén F, Einarsson S (2002) Effect of repeated ACTH-stimulation on early embryonic development and hormonal profiles in sows. Anim Reprod Sci 70:127–137

    PubMed  CAS  Google Scholar 

  • Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403:901–906

    PubMed  CAS  Google Scholar 

  • Richards JS, Russell DL, Ochsner S, Espey LL (2002) Ovulation: new dimensions and new regulators of the inflammatory-like response. Annu Rev Physiol 64:69–92

    PubMed  CAS  Google Scholar 

  • Rivkin E, Kierszenbaum AL, Gil M, Tres LL (2009) Rnf19a, a ubiquitin protein ligase, and Psmc3, a component of the 26S proteasome, tether to the acrosome membranes and the head-tail coupling apparatus during rat spermatid development. Dev Dyn 238:1851–1861

    PubMed  CAS  Google Scholar 

  • Rosano G, Caille AM, Gallardo-Ríos M, Munuce MJ (2007) D-Mannose-binding sites are putative sperm determinants of human oocyte recognition and fertilization. Reprod Biomed Online 15:182–190

    Google Scholar 

  • Rodríguez CI, Stewart CL (2007) Disruption of the ubiquitin ligase HERC4 causes defects in spermatozoon maturation and impaired fertility. Dev Biol 312:501–508

    PubMed  Google Scholar 

  • Rodríguez-Martínez H, Einarsson S, Larsson B (1982) Spontaneous motility of the oviduct in the anaesthetized pig. J Reprod Fertil 66:615–624

    PubMed  Google Scholar 

  • Rodríguez-Martínez H, Iborra A, Martínez P, Calvete JJ (1998) Immunoelectronmicroscopic imaging of spermadhesin AWN epitopes on boar spermatozoa bound in vivo to the zona pellucida. Reprod Fertil Dev 10:491–497

    PubMed  Google Scholar 

  • Rodríguez-Martínez H, Tienthai P, Suzuki K, Funahashi H, Ekwall H, Johannisson A (2001) Involvement of oviduct in sperm capacitation and oocyte development in pigs. Reproduction Suppl 58:129–145

    Google Scholar 

  • Ron-el R, Nachum H, Herman A, Golan A, Caspi E, Soifer Y (1991) Delayed fertilization and poor embryonic development associated with impaired semen quality. Fertil Steril 55:338–344

    PubMed  CAS  Google Scholar 

  • Rosales O, Opazo C, Días ES, Villegas JV, Sanchez R, Morales P (2011) Proteasome activity and proteasome subunit transcripts in human spermatozoa separated by a discontinuous percoll gradient. Andrologia 43:106–113

    PubMed  CAS  Google Scholar 

  • Sakai N, Sawada MT, Sawada H (2004) Non-traditional roles of ubiquitin-proteasome system in fertilization and gametogenesis. Int J Biochem Cell Biol 36:776–784

    PubMed  CAS  Google Scholar 

  • Salicioni AM, Platt MD, Wertheimer EV, Arcelay E, Allaire A, Sosnik J, Visconti PE (2007) Signalling pathways involved in sperm capacitation. Soc Reprod Fertil Suppl 65:245–259

    PubMed  CAS  Google Scholar 

  • Samour J, Moore HD, Smith CA (1986) Avian spermatozoa penetrate zona-free hamster oocytes in vitro. J Exp Zool 239:295–298

    PubMed  CAS  Google Scholar 

  • Sánchez R, Deppe M, Schulz M, Bravo P, Villegas J, Morales P, Risopatron J (2011) Participation of the sperm proteasome during in vitro fertilisation and the acrosome reaction in cattle. Andrologia 43:114–120

    PubMed  Google Scholar 

  • Santos P, Chaveiro A, Simoes N, Moreira da Silva F (2008) Bovine oocyte quality in relation to ultrastructural characteristics of zona pellucida, polyspermic penetration and developmental competence. Reprod Domest Anim 43:685–689

    PubMed  CAS  Google Scholar 

  • Sanz L, Calvete JJ, Mann K, Gabius HJ, Töpfer-Petersen E (1993) Isolation and biochemical of heparin-binding proteins from boar seminal plasma: a dual role for spermadhesins in fertilization. Mol Reprod Dev 35:37–43

    PubMed  CAS  Google Scholar 

  • Sartini BL, Berger T (2000) Identification of homologous binding proteins in porcine and bovine gametes. Mol Reprod Dev 55:446–451

    PubMed  CAS  Google Scholar 

  • Saunders CM, Larman MG, Parrington J, Cox LJ, Royse J, Blayney LM, Swann K, Lai FA (2002) PLCζ: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development. Development 129:3533–3544

    PubMed  CAS  Google Scholar 

  • Saunders CM, Swann K, Lai FA (2007) PLCzeta, a sperm-specific PLC and its potential role in fertilization. Biochem Soc Symp 74:23–36

    PubMed  CAS  Google Scholar 

  • Sawada H, Sakai N, Abe Y, Tanaka E, Takahashi Y, Fujino J, Kodama E, Takizawa S, Yokosawa H (2002) Extracellular ubiquitination and proteasome-mediated degradation of the ascidian sperm receptor. Proc Natl Acad Sci USA 99:1223–1228

    PubMed  CAS  Google Scholar 

  • Schatten G (1994) The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization. Dev Biol 165:299–335

    PubMed  CAS  Google Scholar 

  • Schatten G, Simerly C, Palmer DK, Margolis RL, Maul G, Andrews BS, Schatten H (1988) Kinetochore appearance during meiosis, fertilization and mitosis in mouse oocytes and zygotes. Chromosoma 96:341–352

    PubMed  CAS  Google Scholar 

  • Schuffner AA, Bastiaan HS, Duran HE, Lin ZY, Morshedi M, Franken DR, Oehninger S (2002) Zona pellucida-induced acrosome reaction in human sperm: dependency on activation of pertussis toxin-sensitive Gi protein and extracellular calcium, and priming effect of progesterone and follicular fluid. Mol Hum Reprod 8:722–727

    PubMed  CAS  Google Scholar 

  • Schwartz M, Vissing J (2002) Paternal inheritance of mitochondrial DNA. N Engl J Med 347:576–580

    PubMed  Google Scholar 

  • Seppälä M, Taylor N, Koistinen H, Koistinen R, Milgrom E (2002) Glycodelin: a major lipocalin protein of the reproductive axis with diverse actions in cell recognition and differentiation. Endocr Rev 23:401–430

    PubMed  Google Scholar 

  • Sette C, Bevilacqua A, Bianchini A, Mangia F, Geremia R, Rossi P (1997) Parthenogenetic activation of mouse eggs by microinjection of a truncated c-kit tyrosine kinase present in spermatozoa. Development 124:2267–2274

    PubMed  CAS  Google Scholar 

  • Sette C, Paronetto MP, Barchi M, Bevilacqua A, Geremia R, Rossi P (2002) Tr-kit-induced resumption of the cell cycle in mouse eggs requires activation of a Src-like kinase. EMBO J 21:5386–5395

    PubMed  CAS  Google Scholar 

  • Shadel S, Clayton A (1997) Mitochondrial DNA maintenance in vertebrates. Annu Rev Biochem 66:409–435

    PubMed  CAS  Google Scholar 

  • Sheeman B, Carvalho P, Sagot I, Geiser J, Kho D, Hoyt MA, Pellman D (2003) Determinants of S. cerevisiae dynein localization and activation: implications for the mechanism of spindle positioning. Curr Biol 13:364–372

    PubMed  CAS  Google Scholar 

  • Shimada A, Kikuchi K, Noguchi J, Akama K, Nakano M, Kaneko H (2000) Protamine dissociation before decondensation of sperm nuclei during in vitro fertilization of pig oocytes. J Reprod Fertil 120:247–256

    PubMed  CAS  Google Scholar 

  • Shur BD (1994) Glycobiology. The beginning of a sweet tale. Curr Biol 4:996–999

    PubMed  CAS  Google Scholar 

  • Shur BD, Ensslin MA, Rodeheffer C. (2004) SED1 function during mammalian sperm-egg adhesion. Curr Opin Cell Biol 16: 477-485

    Google Scholar 

  • Short RV (1998) Difference between a testis and an ovary. J Exp Zool 281:359–361

    PubMed  CAS  Google Scholar 

  • Signorelli J, Días ES, Morales P (2012) Kinases, phosphatases and proteases during sperm capacitation. Cell Tissue Res 349:765–782

    PubMed  CAS  Google Scholar 

  • Silva PF, Gadella BM (2006) Detection of damage in mammalian sperm cells. Theriogenology 65:958–978

    PubMed  CAS  Google Scholar 

  • Singleton S, Zalensky A, Doncel GF, Morshedi M, Zalenskaya IA (2007) Testis/sperm-specific histone 2B in the sperm of donors and subfertile patients: variability and relation to chromatin packaging. Hum Reprod 22:743–750

    PubMed  CAS  Google Scholar 

  • Sinowatz F, Kölle S, Töpfer-Petersen E (2001) Biosynthesis and expression of zona pellcucida glycoproteins in mammals. Cell Tissues Organs 168:24–35

    CAS  Google Scholar 

  • Sinowatz F, Wessa E, Neumüller C, Palma G (2003) On the species specificity of sperm binding and sperm penetration of the zona pellucida. Reprod Domest Anim 38:141–146

    PubMed  CAS  Google Scholar 

  • Snell J, White M (1996) The molecules of mammalian fertilization. Cell 85:629–637

    PubMed  CAS  Google Scholar 

  • Snook RR, Hosken DJ, Karr TL (2011) The biology and evolution of polyspermy: insights from cellular and functional studies of sperm and centrosomal behavior in the fertilized egg. Reproduction 142:779–792

    PubMed  Google Scholar 

  • Soler AJ, Poulin N, Fernández-Santos MR, Cognie Y, Esteso MC, Garde JJ, Mermillod P (2008) Heterologous in vitro fertility evaluation of cryopreserved Iberian red deer epididymal spermatozoa with zona-intact sheep oocytes and its relationship with the characteristics of thawed spermatozoa. Reprod Domest Anim 43:293–298

    PubMed  CAS  Google Scholar 

  • Spargo SC, Hope RM (2003) Evolution and nomenclature of the zona pellucida gene family. Biol Reprod 68:358–362

    PubMed  CAS  Google Scholar 

  • Stein KK, Primafoff P, Myles D (2004) Sperm-egg fusion: events at the plasma membrane. J Cell Sci 117:6269–6274

    PubMed  CAS  Google Scholar 

  • Suarez SS (2008) Control of hyperactivation in sperm. Hum Reprod Update 14:647–657

    PubMed  CAS  Google Scholar 

  • Sudhof TC, Rothman JE (2009) Membrane fusion: grappling with SNARE and SM proteins. Science 323:474–477

    PubMed  Google Scholar 

  • Sutovsky P (2009) Sperm-egg adhesion and fusion in mammals. Expert Rev Mol Med 11:e11

    PubMed  Google Scholar 

  • Sutovsky P (2011) Sperm proteasome and fertilization. Reproduction 142:1–14

    PubMed  CAS  Google Scholar 

  • Sutovsky P, Schatten G (1997) Depletion of glutathione during bovine oocyte maturation reversibly blocks the decondensation of the male pronucleus and pronuclear apposition during fertilization. Biol Reprod 56:1503–1512

    PubMed  CAS  Google Scholar 

  • Sutovsky P, Moreno R, Ramalho-Santos J, Dominko T, Simerly C, Schatten G (1999) Ubiquitin tag for sperm mitochondria. Nature 402:371–372

    PubMed  CAS  Google Scholar 

  • Sutovsky P, Moreno RD, Ramalho-Santos J, Dominko T, Simerly C, Schatten G (2000) Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos. Biol Reprod 63:582–590

    PubMed  CAS  Google Scholar 

  • Sutovsky P, Moreno R, Ramalho-Santos J, Dominko T, Thompson WE, Schatten G (2001a) A putative, ubiquitin-dependent mechanism for the recognition and elimination of defective spermatozoa in the mammalian epididymis. J Cell Sci 114:1665–1675

    PubMed  CAS  Google Scholar 

  • Sutovsky P, Terada Y, Schatten G (2001b) Ubiquitin-based sperm assay for the diagnosis of male factor infertility. Hum Reprod 16:250–258

    PubMed  CAS  Google Scholar 

  • Sutovsky P, Neuber E, Schatten G (2002) Ubiquitin-dependent sperm quality control mechanism recognizes spermatozoa with DNA defects as revealed by dual ubiquitin-TUNEL assay. Mol Reprod Dev 61:406–413

    PubMed  CAS  Google Scholar 

  • Sutovsky P, Manandhar G, McCauley TC, Caamano JN, Sutovsky M, Thompson WE, Day BN (2004a) Proteasomal interference prevents zona pellucida penetration and fertilization in mammals. Biol Reprod 71:1625–1637

    PubMed  CAS  Google Scholar 

  • Sutovsky P, Hauser R, Sutovsky M (2004b) Increased levels of sperm ubiquitin correlate with semen quality in men from an andrology laboratory clinic population. Hum Reprod 19:628–638

    PubMed  CAS  Google Scholar 

  • Sutton A, Jungnickel K, Ward J, Harris C, Florman M (2006) Functional characterization of PKDREJ, a male germ cell-restricted polycystin. J Cell Physiol 209:493–500

    PubMed  CAS  Google Scholar 

  • Swain JE, Pool TB (2008) ART failure: oocyte contributions to unsuccessful fertilization. Hum Reprod Update 14:431–446

    PubMed  Google Scholar 

  • Swann K, Larman G, Saunders M, Lai A (2004) The cytosolic sperm factor that triggers Ca2+ oscillations and egg activation in mammals is a novel phospholipase C: PLCzeta. Reproduction 127:431–439

    PubMed  CAS  Google Scholar 

  • Tabara H, Yigit E, Siomi H, Mello CC (2002) The dsRNA binding protein RDE-4 interacts with RDE-1, DCR-1, and a DExH-box helicase to direct RNAi in C. elegans. Cell 109:861–871

    PubMed  CAS  Google Scholar 

  • Takasaki S, Mori E, Mori T (1999) Structures of sugar chains included in mammalian zona pellucida glycoproteins and their potential roles in sperm-egg interaction. Biochim Biophys Acta 1473:206–215

    PubMed  CAS  Google Scholar 

  • Talbot P, Geiske C, Knoll M (1999) Oocyte pickup by the mammalian oviduct. Mol Biol Cell 10:5–8

    PubMed  CAS  Google Scholar 

  • Talmor-Cohen A, Tomashov-Matar R, Eliyahu E, Shapiro R, Shalgi R (2004) Are Src family kinases involved in cell cycle resumption in rat eggs? Reproduction 127:455–463

    PubMed  CAS  Google Scholar 

  • Tamburrino L, Marchiani S, Montoya M, Elia Marino F, Natali I, Cambi M, Forti G, Baldi E, Muratori M (2012) Mechanisms and clinical correlates of sperm DNA damage. Asian J Androl 14:24–31

    PubMed  CAS  Google Scholar 

  • Tapia S, Rojas M, Morales P, Ramírez MA, Díaz ES (2011) The laminin-induced acrosome reaction in human sperm is mediated by Src kinases and the proteasome. Biol Reprod 85:357–366

    PubMed  CAS  Google Scholar 

  • Terada Y, Nakamura S, Simerly C, Hewitson L, Murakami T, Yaegashi N, Okamura K, Schatten G (2004) Centrosomal function assessment in human sperm using heterologous ICSI with rabbit eggs: a new male factor infertility assay. Mol Reprod Dev 67:360–365

    PubMed  CAS  Google Scholar 

  • Tesarik J (1998) Sperm-induced calcium oscillations. Oscillin-reopening the hunting season. Mol Hum Reprod 4:1007–1012

    PubMed  CAS  Google Scholar 

  • Tesarik J (2005) Paternal effects on cell division in the human preimplantation embryo. Reprod Biomed Online 10:370–375

    PubMed  Google Scholar 

  • Tesarik J, Mendoza C (1999) In vitro fertilization by intracytoplasmic sperm injection. BioEssays 21:791–801

    PubMed  CAS  Google Scholar 

  • Tesarik J, Greco E, Mendoza C (2004) Late, but not early, paternal effect on human embryo development is related to sperm DNA fragmentation. Hum Reprod 19:611–615

    PubMed  CAS  Google Scholar 

  • Thompson WE, Ramalho-Santos J, Sutovsky P (2003) Ubiquitination of prohibitin in mammalian sperm mitochondria: possible roles in the regulation of mitochondrial inheritance and sperm quality control. Biol Reprod 69:254–260

    PubMed  CAS  Google Scholar 

  • Tipler CP, Hutchon SP, Hendil K, Tanaka K, Fishel S, Mayer RJ (1997) Purification and characterization of 26S proteasomes from human and mouse spermatozoa. Mol Hum Reprod 3:1053–1060

    PubMed  CAS  Google Scholar 

  • Töpfer-Petersen E (1999) Carbohydrate-based interactions on the route of a spermatozoon to fertilization. Hum Reprod Update 5:314–329

    PubMed  Google Scholar 

  • Töpfer-Petersen E, Henschen A (1987) Acrosin shows zona and fucose- binding, novel properties for a serine proteinase. FEBS Lett 226:38–42

    PubMed  Google Scholar 

  • Töpfer-Petersen E, Henschen A (1988) Zona pellucida-binding and fucose-binding of boar sperm acrosin is not correlated to proteolytic activity. Biol Chem Hoppe Seyler 369:69–76

    PubMed  Google Scholar 

  • Töpfer-Petersen E, Friess AE, Nguyen H, Schill WB (1985) Evidence for a fucose-bindng protein in boar spermatozoa. Histochemistry 83:139–145

    PubMed  Google Scholar 

  • Töpfer-Petersen E, Steinberger M, Von Eschenbach CE, Zucker A (1990a) Zona pellucida-binding of boar sperm acrosin is associated with the N-terminal peptide of the acrosin B-chain (heavy chain). FEBS Lett 265:51–54

    PubMed  Google Scholar 

  • Töpfer-Petersen E, Calvete JJ, Schäfer W, Henschen A (1990b) Complete localization of disulfide bridges and glycosylation sites in boar sperm acrosin. FEBS Lett 275:139–142

    PubMed  Google Scholar 

  • Töpfer-Petersen E, Romero A, Varela PF, Ekhlasi-Hundrieser M, Dostalova Z, Sanz L, Calvete JJ (1998) Spermadhesins: a new protein family. Facts, hypotheses and perspectives. Andrologia 30:217–224

    PubMed  Google Scholar 

  • Töpfer-Petersen E, Ekhlasi-Hundrieser M, Tsolova M (2008) Glycobiology of fertilization in the pig. Int J Dev Biol 52:717–736

    PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Tranter R, Read JA, Jones R, Brady RL (2000) Effector sites in the three-dimensional structure of mammalian sperm β-acrosin. Structure 8:1179–1188

    PubMed  CAS  Google Scholar 

  • Tsai PS, De Vries KJ, De Boer-Brouwer M, Garcia-Gil N, Van Gestel RA, Colenbrander B, Gadella BM, Van Haeften T (2007) Syntaxin and VAMP association with lipid rafts depends on cholesterol depletion in capacitating sperm cells. Mol Membr Biol 24:313–324

    PubMed  CAS  Google Scholar 

  • Tsai PS, Garcia-Gil N, van Haeften T, Gadella BM (2010) How pig sperm prepares to fertilize: stable acrosome docking to the plasma membrane. PLoS ONE 5:e11204

    PubMed  Google Scholar 

  • Tyler JP, Pryor JP, Collins WP (1981) Heterologous ovum penetration by human spermatozoa. J Reprod Fertil 63:499–508

    PubMed  CAS  Google Scholar 

  • Vadnais ML, Foster DN, Roberts KP (2008) Molecular cloning and expression of the CRISP family of proteins in the boar. Biol Reprod 79:1129–1134

    PubMed  CAS  Google Scholar 

  • Van Blerkom J (2000) Intrafollicular influences on human oocyte developmental competence: perifollicular vascularity, oocyte metabolism and mitochondrial function. Hum Reprod 15(Suppl 2):173–188

    PubMed  Google Scholar 

  • Van der Heijden GW, Dieker JW, Derijck AA, Muller S, Berden JH, Braat DD, van der Vlag J, de Boer P (2005) Asymmetry in histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote. Mech Dev 122:1008–1022

    PubMed  Google Scholar 

  • Van Gestel RA, Brewis IA, Ashton PR, Brouwers JF, Gadella BM (2007) Multiple proteins present in purified porcine sperm apical plasma membranes interact with the zona pellucida of the oocyte. Mol Hum Reprod 13:445–454

    PubMed  Google Scholar 

  • Verhage M (2009) Organelle docking: R-SNAREs are late. Proc Natl Acad Sci USA 106:19745–19746

    PubMed  CAS  Google Scholar 

  • Verhage M, Toonen RF (2007) Regulated exocytosis: merging ideas on fusing membranes. Curr Opin Cell Biol 19:402–408

    PubMed  CAS  Google Scholar 

  • Vjugina U, Evans JP (2008) New insights into the molecular basis of mammalian sperm-egg membrane interactions. Front Biosci 13:462–476

    PubMed  CAS  Google Scholar 

  • Vo LH, Hedrick JL (2000) Independent and hetero-oligomeric-dependent sperm binding to egg envelope glycoprotein ZPC of Xenopus laevis. Biol Reprod 62:766–774

    PubMed  CAS  Google Scholar 

  • Voges D, Zwickl P, Baumeister W (1999) The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu Rev Biochem 68:1015–1068

    PubMed  CAS  Google Scholar 

  • Von Witzendorff D, Ekhlasi-Hundrieser M, Dostàlovà Z, Resch M, Rath D, Michelmann HW, Töpfer-Petersen E (2005) Analysis of N-linked glycans of porcine zona pellucida glycoprotein, ZPA by MALDITOF MS: a contribution to understanding zona pellucida structure. Glycobiology 15:475–488

    Google Scholar 

  • Vrljic M, Strop P, Ernst JA, Sutton RB, Chu S, Brunger AT (2010) Molecular mechanism of the synaptotagmin-SNARE interaction in Ca2 + -triggered vesicle fusion. Nat Struct Mol Biol 17:325–331

    PubMed  CAS  Google Scholar 

  • Wagner A, Ekhlasi-Hundrieser M, Hettel C, Petrunkina A, Waberski D, Nimtz M, Töpfer-Petersen E (2002) Carbohydrate-based interactions of oviductal sperm reservoir formation-studies in the pig. Mol Reprod Dev 61:249–257

    PubMed  CAS  Google Scholar 

  • Ward WS (1993) Deoxyribonucleic acid loop domain tertiary structure in mammalian spermatozoa. Biol Reprod 48:1193–1201

    PubMed  CAS  Google Scholar 

  • Ward WS, Coffey DS (1991) DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol Reprod 44:569–574

    PubMed  CAS  Google Scholar 

  • Wassarman PM (1995) Mammalian fertilization: egg and sperm (glyco)proteins that support gamete adhesion. Am J Reprod Immunol 33:253–258

    PubMed  CAS  Google Scholar 

  • Wassarman PM (1999) Mammalian fertilization: molecular aspect of gamete adhesion exocytosis, and fusion. Cell 96:175–183

    PubMed  CAS  Google Scholar 

  • Wassarman PM (2005) Contribution of mouse egg zona pellucida glycoproteins to gamete recognition during fertilization. J Cell Physiol 204:388–391

    PubMed  CAS  Google Scholar 

  • Wassarman PM, Jovine L, Qi H, Williams Z, Darie C, Litscher ES (2005) Recent aspects of mammalian fertilization research. Mol Cell Endocrinol 234:95–103

    PubMed  CAS  Google Scholar 

  • Wilkinson KD (1997) Regulation of ubiquitin-dependent processes by deubiquitinating enzymes. FASEB J 11:1245–1256

    PubMed  CAS  Google Scholar 

  • Witte TS, Schäfer-Somi S (2007) Involvement of cholesterol, calcium and progesterone in the induction of capacitation and acrosome reaction of mammalian spermatozoa. Anim Reprod Sci 102:181–193

    PubMed  CAS  Google Scholar 

  • Wojcik C, Benchaib M, Lornage J, Czyba JC, Guerin JF (2000) Proteasomes in human spermatozoa. Int J Androl 23:169–177

    PubMed  CAS  Google Scholar 

  • Wong EY, Tse JY, Yao KM, Tam PC, Yeung WS (2002) VCY2 protein interacts with the HECT domain of ubiquitin-protein ligase E3A. Biochem Biophys Res Commun 296:1104–1111

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Wykes SM, Krawetz SA (2003) The structural organization of sperm chromatin. J Biol Chem 278:29471–29477

    PubMed  CAS  Google Scholar 

  • Wykes SM, Visscher DW, Krawetz SA (1997) Haploid transcripts persist in mature human spermatozoa. Mol Hum Reprod 3:15–19

    PubMed  CAS  Google Scholar 

  • Yanagimachi R (1994a) Fertility of mammalian spermatozoa: its development and relativity. Zygote 2:371–372

    PubMed  CAS  Google Scholar 

  • Yanagimachi R (1994b) Mammalian fertilization. In: Knobil E, Neill JD (eds) The physiology of reproduction, 2nd edn. Raven Press, New York, pp 189–317

    Google Scholar 

  • Yanagimachi R (1998) Intracytoplasmic sperm injection experiments using the mouse as a model. Hum Reprod 13:87–98

    PubMed  Google Scholar 

  • Yang CC, Lin YS, Hsu CC, Wu SC, Lin EC, Cheng WT (2009) Identification and sequencing of remnant messenger RNAs found in domestic swine (Sus scrofa) fresh ejaculated spermatozoa. Anim Reprod Sci 113:143–155

    PubMed  CAS  Google Scholar 

  • Yeste M, Flores E, Estrada E, Bonet S, Rigau T, Rodríguez-Gil JE (2012) Reduced glutathione and procaine hydrochloride protect the nucleoprotein structure of boar spermatozoa during freezing/thawing through stabilisation of disulphide bonds. Reprod Fertil Dev, http://dx.doi.org/10.1071/RD12230 (in press)

  • Yi YJ, Manandhar G, Sutovsky M, Li R, Jonáková V, Oko R, Park CS, Prather RS, Sutovsky P (2007) Ubiquitin C-terminal hydrolase-activity is involved in sperm acrosomal function and anti-polyspermy defense during porcine fertilization. Biol Reprod 77:780–793

    PubMed  CAS  Google Scholar 

  • Yi YJ, Manandhar G, Sutovsky M, Jonáková V, Park CS, Sutovsky P (2010a) Inhibition of 19S proteasomal regulatory complex subunit PSMD8 increases polyspermy during porcine fertilization in vitro. J Reprod Immunol 84:154–163

    PubMed  CAS  Google Scholar 

  • Yi YJ, Manandhar G, Sutovsky M, Zimmerman SW, Jonáková V, van Leeuwen FW, Oko R, Park CS, Sutovsky P (2010b) Interference with the 19S proteasomal regulatory complex subunit PSMD4 on the sperm surface inhibits sperm-zona pellucida penetration during porcine fertilization. Cell Tissue Res 341:325–340

    PubMed  CAS  Google Scholar 

  • Yi YJ, Zimmerman SW, Manandhar G, Odhiambo JF, Kennedy C, Jonáková V, Maňásková-Postlerová P, Sutovsky M, Park CS, Sutovsky P (2012) Ubiquitin-activating enzyme (UBA1) is required for sperm capacitation, acrosomal exocytosis and sperm–egg coat penetration during porcine fertilization. Int J Androl 35:196–210

    PubMed  CAS  Google Scholar 

  • Yokota N, Sawada H (2007) Sperm proteasomes are responsible for the acrosome reaction and sperm penetration of the vitelline envelope during fertilization of the sea urchin Pseudocentrotus depressus. Dev Biol 308:222–231

    PubMed  CAS  Google Scholar 

  • Yonezawa N, Fukui N, Kudo K, Nakano M (1999) Localization of neutral N-linked carbohydrate chains in pig zona pellucida glycoprotein ZPC. Eur J Biochem 260:57–63

    PubMed  CAS  Google Scholar 

  • Yonezawa N, Amari S, Takahashi K, Ikeda K, Imai FL, Kanai S, Kikuchi K, Nakano M (2005) Participation of the non-reducing terminal β-galactosyl residues of the neutral N-linked carbohydrate chains of porcine zona pellucida glycoproteins in sperm-egg binding. Mol Reprod Dev 70:222–227

    PubMed  CAS  Google Scholar 

  • Yoon SY, Jellerette T, Salicioni AM, Lee HC, Yoo MS, Coward K, Parrington J, Grow D, Cibelli JB, Visconti PE, Mager J, Fissore RA (2008) Human sperm devoid of PLC, zeta-1 fail to induce Ca2+ release and are unable to initiate the first step of embryo development. J Clin Invest 118:3671–3681

    PubMed  CAS  Google Scholar 

  • Yunes R, Michaut M, Tomes C, Mayorga LS (2000) Rab3A triggers the acrosome reaction in permeabilized human spermatozoa. Biol Reprod 62:1084–1089

    PubMed  CAS  Google Scholar 

  • Yurewicz EC, Sacco AG, Ghupta SK, Xu N, Gage DA (1998) Heterooligomerisation dependent binding of pig oocyte zona pellucida glycoproteins ZPB and ZPC to boar sperm membrane vesicles. J Biol Chem 273:7488–7494

    PubMed  CAS  Google Scholar 

  • Zalenskaya A, Bradbury M, Zalensky O (2000) Chromatin structure of telomere domain in human sperm. Biochem Biophys Res Commun 279:213–218

    PubMed  CAS  Google Scholar 

  • Zalensky A, Zalenskaya I (2007) Organization of chromosomes in spermatozoa: an additional layer of epigenetic information? Biochem Soc Trans 35:609–611

    PubMed  CAS  Google Scholar 

  • Zelezna B, Cechova D, Henschen A (1989) Isolation of boar sperm acrosin peptide released during conversion of α-form to β-form. Biol Chem Hoppe Seyler 370:323–327

    PubMed  CAS  Google Scholar 

  • Zhao XM, Song XX, Kawai Y, Niwa K (2002) Penetration in vitro of zona-free pig oocytes by homologous and heterologous spermatozoa. Theriogenology 58:995–1006

    PubMed  Google Scholar 

  • Zhao Y, Li Q, Yao C, Wang Z, Zhou Y, Wang Y, Liu L, Wang Y, Wang L, Qiao Z (2006) Characterization and quantification of mRNAtranscripts in ejaculated spermatozoa of fertilemenby serial analysis of gene expression. Hum Reprod 21:1583–1590

    PubMed  CAS  Google Scholar 

  • Zhu H, Zhou ZM, Huo R, Huang XY, Lu L, Lin M, Wang LR, Zhou YD, Li JM, Sha JH (2004) Identification and characteristics of a novel E1 like gene nUBE1L in human testis. Acta Biochim Biophys Sin (Shanghai) 36:227–234

    CAS  Google Scholar 

  • Zimmerman SW, Sutovsky P (2009) The sperm proteasome during sperm capacitation and fertilization. J Reprod Immunol 83:19–25

    PubMed  CAS  Google Scholar 

  • Zimmerman SW, Manandhar G, Yi YJ, Gupta SK, Sutovsky M, Odhiambo JF, Powell MD, Miller DJ, Sutovsky P (2011) Sperm proteasomes degrade sperm receptor on the egg zona pellucida during mammalian fertilization. PLoS ONE 6:e17256

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marc Yeste .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Yeste, M. (2013). Boar Spermatozoa Within the Oviductal Environment (III): Fertilisation. In: Bonet, S., Casas, I., Holt, W., Yeste, M. (eds) Boar Reproduction. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-35049-8_8

Download citation

Publish with us

Policies and ethics