Boar Spermatozoa Within the Oviductal Environment (III): Fertilisation

  • Marc YesteEmail author


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.


Sperm-ZP binding and interaction Acrosome exocytosis Sperm-oocyte fusion Sperm chromatin integrity Post-fertilisation events 


  1. 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 28:23–34PubMedGoogle Scholar
  2. Adham IM, Nayernia K, Engel W (1997) Spermatozoa lacking acrosin protein show delayed fertilization. Mol Reprod Dev 46:370–376PubMedGoogle Scholar
  3. Aitken RJ (1995) Free radicals, lipid peroxidation and sperm function. Reprod Fertil Dev 7:659–668PubMedGoogle Scholar
  4. Aitken RJ (2011) The capacitation-apoptosis highway: oxysterols and mammalian sperm function. Biol Reprod 85:9–12PubMedGoogle Scholar
  5. 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):7–14PubMedGoogle Scholar
  6. Ajduk A, Yamauchi Y, Ward MA (2006) Sperm chromatin remodeling after intra-cytoplasmic sperm injection differs from that of in vitro fertilization. Biol Reprod 75:442–451PubMedGoogle Scholar
  7. 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 45:797–809PubMedGoogle Scholar
  8. Alberts B, Johnson A, Walter P, Lewis J, Raff M, Roberts K (2008) Molecular biology of the cell, 5th edn. Garland Science, New YorkGoogle Scholar
  9. Allan V (1996) Role of motor proteins in organizing the endoplasmic reticulum and Golgi apparatus. Semi Cell Dev Biol 7:335–342Google Scholar
  10. 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 56:817–829PubMedGoogle Scholar
  11. Amanai M, Brahmajosyula M, Perry ACF (2006) A restricted role for sperm-borne microRNAs in mammalian fertilization. Biol Reprod 75:877–884PubMedGoogle Scholar
  12. 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 59:221–226PubMedGoogle Scholar
  13. Ankel-Simons F, Cummins JM (1996) Misconceptions about mitochondria and mammalian fertilization: implications for theories on human evolution. Proc Natl Acad Sci USA 93:13859–13863PubMedGoogle Scholar
  14. Arcelay E, Salicioni AM, Wertheimer E, Visconti PE (2008) Identification of proteins undergoing tyrosine phosphorylation during mouse sperm capacitation. Int J Dev Biol 52:463–472PubMedGoogle Scholar
  15. 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 10:1897–1906PubMedGoogle Scholar
  16. 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 24:270–277PubMedGoogle Scholar
  17. Avendaño C, Franchi A, Taylor S, Morshedi M, Bocca S, Oehninger S (2009) Fragmentation of DNA in morphologically normal human spermatozoa. Fertil Steril 91:1077–1084PubMedGoogle Scholar
  18. 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 207:322–333PubMedGoogle Scholar
  19. Baarends M, Roest P, Grootegoed A (1999b) The ubiquitin system in gametogenesis. Mol Cell Endocrinol 151:5–16PubMedGoogle Scholar
  20. 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 264:11920–11927PubMedGoogle Scholar
  21. 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 1:524–532PubMedGoogle Scholar
  22. 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 8:2312–2321PubMedGoogle Scholar
  23. 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 9:718–729Google Scholar
  24. Barroso G, Valdespin C, Vega E, Kershenovich R, Avila R, Avendaño C, Oehninger S (2009) Developmental sperm contributions: fertilization and beyond. Fertil Steril 92:835–848PubMedGoogle Scholar
  25. 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 215:684–696PubMedGoogle Scholar
  26. 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 3:23PubMedGoogle Scholar
  27. 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 375:477–488PubMedGoogle Scholar
  28. Blobel CP (2000) Functional processing of fertilin: evidence for a critical role of proteolysis in sperm maturation and activation. Rev Reprod 5:75–83PubMedGoogle Scholar
  29. 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 70:1188–1196PubMedGoogle Scholar
  30. 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 36:346–353PubMedGoogle Scholar
  31. Bookbinder H, Cheng A, Bleil D (1995) Tissue- and species-specific expression of SP56, a mouse sperm fertilization protein. Science 269:86–89PubMedGoogle Scholar
  32. Braude P, Bolton V, Moore S (1998) Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature 332:459–461Google Scholar
  33. 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 42:118–125Google Scholar
  34. Breitbart H (2002) Role and regulation of intracellular calcium in acrosomal exocytosis. J Reprod Immunol 53:151–159PubMedGoogle Scholar
  35. Breitbart H, Naor Z (1999) Protein kinases in mammalian sperm capacitation and the acrosome reaction. Rev Reprod 4:151–159PubMedGoogle Scholar
  36. 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 16:743–751PubMedGoogle Scholar
  37. 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) 8:241–251Google Scholar
  38. Brüssow KP (1985) Distribution of oocytes in oviducts of gilts, following synchronized ovulation. Mh Vet Med 40:264–268Google Scholar
  39. Brüssow KP, Rátky J, Rodríguez-Martínez H (2008) Fertilization and early embryonic development in the porcine fallopian tube. Reprod Domest Anim 43(Suppl 2):245–251PubMedGoogle Scholar
  40. 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 11:299–305PubMedGoogle Scholar
  41. 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 9:365–372PubMedGoogle Scholar
  42. Calvete JJ, Dostàlovà Z, Sanz L, Adermann K, Thole HH, Töpfer-Petersen E (1996) Mapping the heparin-binding domain of boar spermadhesins. FEBS Lett 379:207–211PubMedGoogle Scholar
  43. 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 407:201–206PubMedGoogle Scholar
  44. 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 13:65–75PubMedGoogle Scholar
  45. Cánovas S, Coy P, Gómez E (2007) First steps in the development of a functional assay for human sperm using pig oocytes. J Androl 28:273–281PubMedGoogle Scholar
  46. Castle E, Dean J (1999) Manipulating the genome to study reproduction. Mice with ‘‘humanized’’ zonae pellucidae. Hum Reprod 14:1927–1939PubMedGoogle Scholar
  47. 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 241:136–140PubMedGoogle Scholar
  48. Chapman R, Barratt L (1996) The role of carbohydrate in sperm-ZP3 adhesion. Mol Hum Reprod 2:767–774PubMedGoogle Scholar
  49. Chernomordik LV, Kozlov MM (2008) Mechanics of membrane fusion. Nat Struct Mol Biol 15:675–683PubMedGoogle Scholar
  50. 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 120:33–44PubMedGoogle Scholar
  51. 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 79:869–877PubMedGoogle Scholar
  52. 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 81:2080–2087PubMedGoogle Scholar
  53. 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 11:467–473PubMedGoogle Scholar
  54. 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 3:5–13PubMedGoogle Scholar
  55. 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 7:157–163PubMedGoogle Scholar
  56. Conner J, Lefievre L, Hughes C, Barratt L (2005) Cracking the egg: increased complexity in the zona pellucida. Hum Reprod 20:1148–1152PubMedGoogle Scholar
  57. 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 15:502–509Google Scholar
  58. 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 41:1621–1629Google Scholar
  59. 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 105:15809–15814PubMedGoogle Scholar
  60. Coy P, Avilés M (2010) What controls polyspermy in mammals, the oviduct or the oocyte? Biol Rev Camb Philos Soc 85:593–605PubMedGoogle Scholar
  61. Cross L, Morales P, Overstreet W, Hanson W (1988) Induction of acrosome reactions by the human zona pellucida. Biol Reprod 38:235–244PubMedGoogle Scholar
  62. Cummins J (1998) Mitochondrial DNA in mammalian reproduction. Rev Reprod 3:172–182PubMedGoogle Scholar
  63. Cummins J, Wakayama T, Yanagimachi R (1998) Fate of microinjected spermatid mitochondria in the mouse oocyte and embryo. Zygote 6:213–222PubMedGoogle Scholar
  64. 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 65:353–356PubMedGoogle Scholar
  65. 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 11:133–140PubMedGoogle Scholar
  66. Dale B, DeFelice LJ, Ehrenstein G (1985) Injection of a soluble sperm extract into sea urchin eggs triggers the cortical reaction. Experientia 41:1068–1070PubMedGoogle Scholar
  67. 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 65:229–244Google Scholar
  68. Day BN (2000) Reproductive biotechnologies: current status in porcine reproduction. Anim Reprod Sci 60:161–172PubMedGoogle Scholar
  69. 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 270:24116–24126PubMedGoogle Scholar
  70. 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 100:15631–15636PubMedGoogle Scholar
  71. Dell’Aquila ME, Fusco S, Lacalandra GM, Maritato F (1996) In vitro maturation and fertilization of equine oocytes recovered during the breeding season. Theriogenology 45:547–560PubMedGoogle Scholar
  72. 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 22:1420–1430PubMedGoogle Scholar
  73. Didion BA, Kasperson KM, Wixon RL, Evenson DP (2009) Boar fertility and sperm chromatin structure status: a retrospective report. J Androl 30:655–660PubMedGoogle Scholar
  74. 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 96:555–564PubMedGoogle Scholar
  75. 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 376:237–242PubMedGoogle Scholar
  76. Dostàlovà Z, Calvete JJ, Sanz L, Töpfer-Petersen E (1995b) Boar spermadhesin AWN-1: oligosaccharide and zona pellucida binding characteristics. Eur J Biochem 230:329–336PubMedGoogle Scholar
  77. Du Y, Liu ML, Jia MC (2008) Identification and characterization of a spermatogenesis-related gene Ube1 in rat testis. Sheng Li Xue Bao 60:382–390PubMedGoogle Scholar
  78. Dupont G (1998) Theoretical insights into the mechanism of spiral Ca2+ wave initiation in xenopus oocytes. Am J Physiol 275:C317–C322PubMedGoogle Scholar
  79. 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 13:1235–1239PubMedGoogle Scholar
  80. 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 98:795–800PubMedGoogle Scholar
  81. Edwards RG, Beard HK (1997) Oocyte polarity and cell determination in early mammalian embryos. Mol Hum Reprod 3:863–905PubMedGoogle Scholar
  82. 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 70:1197–1201PubMedGoogle Scholar
  83. 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 73:536–545PubMedGoogle Scholar
  84. 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 392:253–265PubMedGoogle Scholar
  85. Eliyahu E, Shalgi R (2002) A role for protein kinase C during rat egg activation. Biol Reprod 67:189–195PubMedGoogle Scholar
  86. 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 376:733–738PubMedGoogle Scholar
  87. 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 58:1057–1064PubMedGoogle Scholar
  88. Espey LL, Lipner H (1994) Ovulation. In: Knobil E, Neill JD (eds) The physiology of reproduction. Raven Press, New York, pp 725–780Google Scholar
  89. Esterhuizen D, Franken R, Becker J, Lourens G, Muller I, van Rooyen H (2002) Defective sperm decondensation: a cause for fertilization failure. Andrologia 34:1–7PubMedGoogle Scholar
  90. 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 9:96PubMedGoogle Scholar
  91. Familiari G, Heyn R, Relucenti M, Sathananthan H (2008) Structural changes of the zona pellucida during fertilization and embryo development. Front Biosci 13:6730–6751PubMedGoogle Scholar
  92. 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 32:51–61PubMedGoogle Scholar
  93. 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 278:11579–11589PubMedGoogle Scholar
  94. 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 130:213–222PubMedGoogle Scholar
  95. Fissore A, Reis M, Palermo D (1999) Isolation of the Ca2+ releasing component(s) of mammalian sperm extracts: the search continues. Mol Hum Reprod 5:189–192PubMedGoogle Scholar
  96. 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 44:207–218PubMedGoogle Scholar
  97. Flesch FM, Gadella BM (2000) Dynamics of the mammalian sperm plasma membrane in the process of fertilization. Biochim Biophys Acta 1469:197–235PubMedGoogle Scholar
  98. 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 76:1450–1464PubMedGoogle Scholar
  99. 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 152:304–314PubMedGoogle Scholar
  100. 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 135:133–146PubMedGoogle Scholar
  101. 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 118:1811–1820PubMedGoogle Scholar
  102. 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 66:1009–1011PubMedGoogle Scholar
  103. 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 86:297–303PubMedGoogle Scholar
  104. 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 63:1437–1442PubMedGoogle Scholar
  105. Funahashi H, Nagai T (2001) Regulation of in vitro penetration of frozen-thawed boar spermatozoa by caffeine and adenosine. Mol Reprod Dev 58:424–431PubMedGoogle Scholar
  106. 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 2:341–347PubMedGoogle Scholar
  107. 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 273:3415–3421PubMedGoogle Scholar
  108. 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 71:643–650PubMedGoogle Scholar
  109. 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 265:20662–20666PubMedGoogle Scholar
  110. Gilbert I, Bissonnette N, Boissonneault G, Vallée M, Robert C (2007) A molecular analysis of the population of mRNA in bovine spermatozoa. Reproduction 133:1073–1086PubMedGoogle Scholar
  111. 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 151:1591–1598PubMedGoogle Scholar
  112. 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 94:615–623PubMedGoogle Scholar
  113. Glickman MH, Ciechanover A (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82:373–428PubMedGoogle Scholar
  114. 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 207:202–205PubMedGoogle Scholar
  115. 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 78:951–961PubMedGoogle Scholar
  116. 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 78:796–806PubMedGoogle Scholar
  117. 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 20:226–230PubMedGoogle Scholar
  118. Green DPL (1987) Mammalian sperm can not penetrate the zona pellcuida soley by force. Exp Cell Res 169:31–38PubMedGoogle Scholar
  119. Greve JM, Wassarman PM (1985) Mouse egg extracellular coat is a matrix of interconnected filaments possessing a structural repeat. J Mol Biol 181:253–264PubMedGoogle Scholar
  120. 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 62:559–567PubMedGoogle Scholar
  121. Grunewald S, Paasch U, Glander HJ, Anderegg U (2005) Mature human spermatozoa do not transcribe novel RNA. Andrologia 37:69–71PubMedGoogle Scholar
  122. Hafez ESE (1993) Anatomy of female reproductive tract. In: Hafez ESE (ed) Reproduction in farm animals, 6th edn. Lea and Febiger, PhiladelphiaGoogle Scholar
  123. 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 55:585–595PubMedGoogle Scholar
  124. 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 4:361–393PubMedGoogle Scholar
  125. 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 69:1170–1176PubMedGoogle Scholar
  126. Hecht NB (1974) A DNA polymerase isolated from bovine spermatozoa. J Reprod Fertil 41:345–354PubMedGoogle Scholar
  127. 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 157:795–806PubMedGoogle Scholar
  128. 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 49:28PubMedGoogle Scholar
  129. Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425–479PubMedGoogle Scholar
  130. Hewitson L, Simerly C, Schatten G (2000) Cytoskeletal aspects of assisted fertilization. Semin Reprod Med 18:151–159PubMedGoogle Scholar
  131. Hewitson L, Simerly CR, Schatten G (2002) Fate of sperm components during assisted reproduction: implications for infertility. Hum Fertil (Camb) 5:110–116Google Scholar
  132. Hewitson L, Simerly CR, Schatten G (2003) ICSI, male pronuclear remodeling and cell cycle checkpoints. Adv Exp Med Biol 518:199–210PubMedGoogle Scholar
  133. 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 67:256–262PubMedGoogle Scholar
  134. 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 51:193–204PubMedGoogle Scholar
  135. Hochstrasser M (1996) Ubiquitin-dependent protein degradation. Annu Rev Genet 30:405–439PubMedGoogle Scholar
  136. 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 221:491–512PubMedGoogle Scholar
  137. Honda A, Siruntawinwti J, Baba T (2002) Role of acrosomal matrix proteinases in sperm-zona pellucida interactiosn. Hum Reprod Update 5:405–412Google Scholar
  138. Hoodbhoy T, Dean J (2004) Insights into the molecular basis of sperm-egg recognition in mammals. Reproduction 127:417–422PubMedGoogle Scholar
  139. 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 280:12721–12731PubMedGoogle Scholar
  140. Hughes DC (2007) ZP genes in the avian species illustrates the dynamic evolution of the vertebrate egg envelope. Cytogenet Genome Res 117:86–91PubMedGoogle Scholar
  141. Hunter RH (1984) Pre-ovulatory arrest and peri-ovulatory redistribution of competent spermatozoa in the isthmus of the pig oviduct. J Reprod Fertil 72:203–211PubMedGoogle Scholar
  142. 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 293:834–838PubMedGoogle Scholar
  143. Hutvagner G, Zamore PD (2002) A microRNA in a multiple-turnover RNAi enzyme complex. Science 297:2056–2060PubMedGoogle Scholar
  144. 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, (in press)
  145. Ingman M, Kaessmann H, Pääbo S, Gyllensten U (2000) Mitochondrial genome variation and the origin of modern humans. Nature 408:708–713PubMedGoogle Scholar
  146. Inoue N, Ikawa M, Isotani A, Okabe M (2005) The immunoglobulin superfamily protein Izumo is required for sperm to fuse with eggs. Nature 434:234–238PubMedGoogle Scholar
  147. Inoue N, Ikawa M, Okabe M (2008) Putative sperm fusion protein IZUMO and the role of N-glycosylation. Biochem Biophys Res Comm 377:910–914PubMedGoogle Scholar
  148. 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 117:395–402PubMedGoogle Scholar
  149. Iwao Y (2012) Egg activation in physiological polyspermy. Reproduction 144:11–12Google Scholar
  150. 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 8:926–941PubMedGoogle Scholar
  151. Jaffe F (1983) Sources of calcium in egg activation: a review and hypothesis. Dev Biol 99:265–276PubMedGoogle Scholar
  152. Jahn R, Scheller RH (2006) SNAREs-engines for membrane fusion. Nat Rev Mol Cell Biol 7:631–643PubMedGoogle Scholar
  153. 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 108:4892–4896PubMedGoogle Scholar
  154. 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 3:499–502PubMedGoogle Scholar
  155. 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 24:279–282PubMedGoogle Scholar
  156. 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 92:4542–4546PubMedGoogle Scholar
  157. Katayama M, Koshida M, Miyake M (2002) Fate of the acrosome in ooplasm in pigs after IVF and ICSI. Hum Reprod 17:2657–2664PubMedGoogle Scholar
  158. 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 15:2654–2659PubMedGoogle Scholar
  159. 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 53:84–91PubMedGoogle Scholar
  160. Klemm U, Müller-Esterl W, Engle W (1991) Acrosin, the peculiar sperm-specific serine protease. Hum Genet 87:635–641PubMedGoogle Scholar
  161. 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 241:464–467PubMedGoogle Scholar
  162. Knobil E, Neill JD (1994) The physiology of reproduction, 2nd edn. Raven Press, New YorkGoogle Scholar
  163. 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 80:1026–1035PubMedGoogle Scholar
  164. 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 436:687–698PubMedGoogle Scholar
  165. 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 65:1246–1251PubMedGoogle Scholar
  166. 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 279:10408–10412PubMedGoogle Scholar
  167. Kramer JA, Krawetz SA (1997) RNA in spermatozoa: implications for the alternative haploid genome. Mol Hum Reprod 3:473–478PubMedGoogle Scholar
  168. Krawetz A (2005) Paternal contribution: new insights and future challenges. Nat Rev Genet 6:633–642PubMedGoogle Scholar
  169. 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 252:492–499Google Scholar
  170. Kumar G, Patel D, Naz RK (1993) c-MYC mRNA is present in human sperm cells. Cell Mol Biol Res 39:111–117PubMedGoogle Scholar
  171. Kvist U (1980) Sperm nuclear chromatin decondensation ability. An in vitro study on ejaculated human spermatozoa. Acta Physiol Scand Suppl 486:1–24PubMedGoogle Scholar
  172. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T (2001) Identification of novel genes coding for small expressed RNAs. Science 294:853–858PubMedGoogle Scholar
  173. 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 10:535–541PubMedGoogle Scholar
  174. 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 56:937–953PubMedGoogle Scholar
  175. 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 15:1717–1722PubMedGoogle Scholar
  176. Lau NC, Lim LP, Weinstein EG, Bartel DP (2001) An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294:858–862PubMedGoogle Scholar
  177. 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 31:78–86PubMedGoogle Scholar
  178. Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854PubMedGoogle Scholar
  179. 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 19:1580–1586PubMedGoogle Scholar
  180. Leyton L, LeGuen P, Bunch D, Saling PM (1992) Regulation of mouse gamete interaction by a sperm tyrosine kinase. Proc Natl Acad Sci USA 89:11692–11695PubMedGoogle Scholar
  181. Li GP, Seidel GE, Squires EL (2003) Intracytoplasmic sperm injection of bovine oocytes with stallion spermatozoa. Theriogenology 59:1143–1155PubMedGoogle Scholar
  182. Lin SL, Kim H, Ying SY (2007) Intron-mediated RNA interference and microRNA (miRNA). Front Biosci 13:2216–2230Google Scholar
  183. Linfor J, Berger T (2000) Potential role of αv and β1 integrins as oocyte adhesion molecules during fertilization in pigs. J Reprod Fertil 120:65–72PubMedGoogle Scholar
  184. Litscher ES, Wassarman PM (2007) Egg extracellular coat proteins: from fish to mammals. Histol Histopathol 22:337–347PubMedGoogle Scholar
  185. Madej A, Lang A, Brandt Y, Kindahl H, Madsen MT, Einarsson S (2005) Factors regulating ovarian function in pigs. Domestic Anim Endocrinol 29:347–361Google Scholar
  186. Maleszewski M, Kline D, Yanagimachi R (1995) Activation of hamster zona-free oocytes by homologous and heterologous spermatozoa. J Reprod Fertil 105:99–107PubMedGoogle Scholar
  187. 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 13:621–631PubMedGoogle Scholar
  188. 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 5:5–13PubMedGoogle Scholar
  189. Martens S, McMahon HT (2008) Mechanisms of membrane fusion: disparate players and common principles. Nat Rev Mol Cell Biol 9:543–556PubMedGoogle Scholar
  190. Matsukawa K, Takahashi M, Hanada A (2002) Assay for penetrability of frozen-thawed stallion spermatozoa into zona-free hamster oocytes. J Reprod Dev 48:539–544Google Scholar
  191. Maximov A, Tang J, Yang X, Pang ZP, Sudhof TC (2009) Complexin controls the force transfer from SNARE complexes to membranes in fusion. Science 323:516–521PubMedGoogle Scholar
  192. 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 52:221–234PubMedGoogle Scholar
  193. McLay DW, Clarke HJ (2003) Remodelling the paternal chromatin at fertilization in mammals. Reproduction 125:625–633PubMedGoogle Scholar
  194. 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 97:9996–10001PubMedGoogle Scholar
  195. 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 42:594–602PubMedGoogle Scholar
  196. 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 9:864–869PubMedGoogle Scholar
  197. Miller J, Macek B, Shur D (1992) Complementarity between sperm surface beta -1,4-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding. Nature 357:589–593PubMedGoogle Scholar
  198. 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 287:321–324PubMedGoogle Scholar
  199. 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 5:836–844PubMedGoogle Scholar
  200. Morales P, Kong M, Pizarro E, Pasten C (2003) Participation of the sperm proteasome in human fertilization. Hum Reprod 18:1010–1017PubMedGoogle Scholar
  201. Morales P, Pizarro E, Kong M, Jara M (2004) Extracellular localization of proteasomes in human sperm. Mol Reprod Dev 68:115–124PubMedGoogle Scholar
  202. 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 65:269–273PubMedGoogle Scholar
  203. 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 62:1536–1542PubMedGoogle Scholar
  204. 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 168:575–593PubMedGoogle Scholar
  205. 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 15:447–456PubMedGoogle Scholar
  206. 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 16:720–728PubMedGoogle Scholar
  207. 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 81:856–870PubMedGoogle Scholar
  208. 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 59:185–199PubMedGoogle Scholar
  209. 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 54:1305–1316PubMedGoogle Scholar
  210. Mwanza AM, Razdan P, Hultén F, Einarsson S (2002a) Transport of fertilised and unfertilised ova in sows. Anim Reprod Sci 74:69–74PubMedGoogle Scholar
  211. 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 58:1111–1124PubMedGoogle Scholar
  212. Nagai T, Funahashi H, Yoshioka K, Kikuchi K (2006) Update of in vitro production of porcine embryos. Front Biosci 11:2565–2573PubMedGoogle Scholar
  213. 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 65:1359–1363PubMedGoogle Scholar
  214. 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 8:434–440PubMedGoogle Scholar
  215. Naz RK (1998) Effect of actinomycin D and cycloheximide on human sperm function. Arch Androl 41:135–142PubMedGoogle Scholar
  216. Nazarov IB, Shlyakhtenko LS, Lyubchenko YL, Zalenskaya IA, Zalensky AO (2008) Sperm chromatin released by nucleases. Syst Biol Reprod Med 54:37–46PubMedGoogle Scholar
  217. Niemann H, Rath D (2001) Progress in reproductive biotechnology in swine. Theriogenology 56:1291–1304PubMedGoogle Scholar
  218. 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):47–70PubMedGoogle Scholar
  219. 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 207:1130PubMedGoogle Scholar
  220. 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 209:883–894PubMedGoogle Scholar
  221. 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 1201:7–14PubMedGoogle Scholar
  222. Nonchev S, Tsanev R (1990) Protamine-histone replacement and DNA replication in the male mouse pronucleus. Mol Reprod Dev 25:72–76PubMedGoogle Scholar
  223. O’Brien J, Zini A (2005) Sperm DNA integrity and male infertility. Urology 65:16–22PubMedGoogle Scholar
  224. 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 131–144Google Scholar
  225. 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 180:336–343PubMedGoogle Scholar
  226. Oehninger S (2001) Molecular basis of human sperm-zona pellucida interaction. Cells Tissues Organs 168:58–64PubMedGoogle Scholar
  227. Oehninger S (2003) Biochemical and functional characterization of the human zona pellucida. Reprod Biomed Online 7:641–648PubMedGoogle Scholar
  228. 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 52:991–997PubMedGoogle Scholar
  229. 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 64:977–981PubMedGoogle Scholar
  230. 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 11:1086–1089PubMedGoogle Scholar
  231. 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 216:671–680PubMedGoogle Scholar
  232. Ostermeier C, Dix J, Millar D, Khatri P, Krawetz A (2002) Spermatozoal RNA profiles of normal fertile men. Lancet 360:772–777PubMedGoogle Scholar
  233. Ostermeier C, Miller D, Huntriss D, Diamond P, Krawetz A (2004) Reproductive biology: delivering spermatozoan RNA to the oocyte. Nature 429:154PubMedGoogle Scholar
  234. Ostermeier C, Goodrich J, Moldenhauer S, Diamond P, Krawetz A (2005) A suite of novel human spermatozoal RNAs. J Androl 26:70–74PubMedGoogle Scholar
  235. 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 4:318–324PubMedGoogle Scholar
  236. 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 282:36593–36602PubMedGoogle Scholar
  237. Parinaud J, Mieusset R, Vieitez G, Labal B, Richoilley G (1993) Influence of sperm parameters on embryo quality. Fertil Steril 60:888–892PubMedGoogle Scholar
  238. Parrington J, Swann K, Shevchenko VI, Sesay AK, Lai FA (1996) Calcium oscillations in mammalian eggs triggered by a soluble sperm protein. Nature 379:364–368PubMedGoogle Scholar
  239. Pasten C, Morales P, Kong M (2005) Role of the sperm proteasome during fertilization and gamete interaction in the mouse. Mol Reprod Dev 71:209–219PubMedGoogle Scholar
  240. 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 3:501–505PubMedGoogle Scholar
  241. 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 116:4727–4738PubMedGoogle Scholar
  242. Perreault SD (1992) Chromatin remodeling in mammalian zygotes. Mutat Res 296:43–55PubMedGoogle Scholar
  243. Perreault SD, Wolff RA, Zirkin BR (1984) The role of disulfide bond reduction during mammalian sperm nuclear decondensation in vivo. Dev Biol 101:160–167PubMedGoogle Scholar
  244. 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 125:181–186PubMedGoogle Scholar
  245. Pessot A, Brito M, Figueroa J, Concha I, Yanez A, Burzio O (1989) Presence of RNA in the sperm nucleus. Biochem Biophys Res Comm 158:272–278PubMedGoogle Scholar
  246. 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 125:377–387PubMedGoogle Scholar
  247. Philpott A, Leno GH (1992) Nucleoplasmin remodels sperm chromatin in Xenopus egg extracts. Cell 69:759–767PubMedGoogle Scholar
  248. Pizarro E, Pasten C, Kong M, Morales P (2004) Proteasomal activity in mammalian spermatozoa. Mol Reprod Dev 69:87–93PubMedGoogle Scholar
  249. Primakoff P, Myles DG (2000) The ADAM gene family: surface proteins with adhesion and protease activity. Trends Genet 16:83–87PubMedGoogle Scholar
  250. Provost P, Dishart D, Doucet J, Frendewey D, Samuelsson B, Radmark O (2002) Ribonuclease activity and RNA binding of recombinant human Dicer. EMBO J 21:5864–5874PubMedGoogle Scholar
  251. 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 23:837–845PubMedGoogle Scholar
  252. 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 68:3727–3735PubMedGoogle Scholar
  253. 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 5:33–43PubMedGoogle Scholar
  254. 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 125:2415–2424PubMedGoogle Scholar
  255. 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 63:352–362PubMedGoogle Scholar
  256. 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 62:317–330PubMedGoogle Scholar
  257. 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 6:510–516PubMedGoogle Scholar
  258. 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 23:573–580PubMedGoogle Scholar
  259. 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 42:45–55PubMedGoogle Scholar
  260. 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 70:127–137PubMedGoogle Scholar
  261. 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 403:901–906PubMedGoogle Scholar
  262. Richards JS, Russell DL, Ochsner S, Espey LL (2002) Ovulation: new dimensions and new regulators of the inflammatory-like response. Annu Rev Physiol 64:69–92PubMedGoogle Scholar
  263. 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 238:1851–1861PubMedGoogle Scholar
  264. 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 15:182–190Google Scholar
  265. Rodríguez CI, Stewart CL (2007) Disruption of the ubiquitin ligase HERC4 causes defects in spermatozoon maturation and impaired fertility. Dev Biol 312:501–508PubMedGoogle Scholar
  266. Rodríguez-Martínez H, Einarsson S, Larsson B (1982) Spontaneous motility of the oviduct in the anaesthetized pig. J Reprod Fertil 66:615–624PubMedGoogle Scholar
  267. 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 10:491–497PubMedGoogle Scholar
  268. 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 58:129–145Google Scholar
  269. 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 55:338–344PubMedGoogle Scholar
  270. 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 43:106–113PubMedGoogle Scholar
  271. Sakai N, Sawada MT, Sawada H (2004) Non-traditional roles of ubiquitin-proteasome system in fertilization and gametogenesis. Int J Biochem Cell Biol 36:776–784PubMedGoogle Scholar
  272. 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 65:245–259PubMedGoogle Scholar
  273. Samour J, Moore HD, Smith CA (1986) Avian spermatozoa penetrate zona-free hamster oocytes in vitro. J Exp Zool 239:295–298PubMedGoogle Scholar
  274. 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 43:114–120PubMedGoogle Scholar
  275. 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 43:685–689PubMedGoogle Scholar
  276. 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 35:37–43PubMedGoogle Scholar
  277. Sartini BL, Berger T (2000) Identification of homologous binding proteins in porcine and bovine gametes. Mol Reprod Dev 55:446–451PubMedGoogle Scholar
  278. 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 129:3533–3544PubMedGoogle Scholar
  279. Saunders CM, Swann K, Lai FA (2007) PLCzeta, a sperm-specific PLC and its potential role in fertilization. Biochem Soc Symp 74:23–36PubMedGoogle Scholar
  280. 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 99:1223–1228PubMedGoogle Scholar
  281. Schatten G (1994) The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization. Dev Biol 165:299–335PubMedGoogle Scholar
  282. 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 96:341–352PubMedGoogle Scholar
  283. 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 8:722–727PubMedGoogle Scholar
  284. Schwartz M, Vissing J (2002) Paternal inheritance of mitochondrial DNA. N Engl J Med 347:576–580PubMedGoogle Scholar
  285. 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 23:401–430PubMedGoogle Scholar
  286. 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 124:2267–2274PubMedGoogle Scholar
  287. 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 21:5386–5395PubMedGoogle Scholar
  288. Shadel S, Clayton A (1997) Mitochondrial DNA maintenance in vertebrates. Annu Rev Biochem 66:409–435PubMedGoogle Scholar
  289. 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 13:364–372PubMedGoogle Scholar
  290. 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 120:247–256PubMedGoogle Scholar
  291. Shur BD (1994) Glycobiology. The beginning of a sweet tale. Curr Biol 4:996–999PubMedGoogle Scholar
  292. Shur BD, Ensslin MA, Rodeheffer C. (2004) SED1 function during mammalian sperm-egg adhesion. Curr Opin Cell Biol 16: 477-485Google Scholar
  293. Short RV (1998) Difference between a testis and an ovary. J Exp Zool 281:359–361PubMedGoogle Scholar
  294. Signorelli J, Días ES, Morales P (2012) Kinases, phosphatases and proteases during sperm capacitation. Cell Tissue Res 349:765–782PubMedGoogle Scholar
  295. Silva PF, Gadella BM (2006) Detection of damage in mammalian sperm cells. Theriogenology 65:958–978PubMedGoogle Scholar
  296. 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 22:743–750PubMedGoogle Scholar
  297. Sinowatz F, Kölle S, Töpfer-Petersen E (2001) Biosynthesis and expression of zona pellcucida glycoproteins in mammals. Cell Tissues Organs 168:24–35Google Scholar
  298. 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 38:141–146PubMedGoogle Scholar
  299. Snell J, White M (1996) The molecules of mammalian fertilization. Cell 85:629–637PubMedGoogle Scholar
  300. 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 142:779–792PubMedGoogle Scholar
  301. 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 43:293–298PubMedGoogle Scholar
  302. Spargo SC, Hope RM (2003) Evolution and nomenclature of the zona pellucida gene family. Biol Reprod 68:358–362PubMedGoogle Scholar
  303. Stein KK, Primafoff P, Myles D (2004) Sperm-egg fusion: events at the plasma membrane. J Cell Sci 117:6269–6274PubMedGoogle Scholar
  304. Suarez SS (2008) Control of hyperactivation in sperm. Hum Reprod Update 14:647–657PubMedGoogle Scholar
  305. Sudhof TC, Rothman JE (2009) Membrane fusion: grappling with SNARE and SM proteins. Science 323:474–477PubMedGoogle Scholar
  306. Sutovsky P (2009) Sperm-egg adhesion and fusion in mammals. Expert Rev Mol Med 11:e11PubMedGoogle Scholar
  307. Sutovsky P (2011) Sperm proteasome and fertilization. Reproduction 142:1–14PubMedGoogle Scholar
  308. 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 56:1503–1512PubMedGoogle Scholar
  309. Sutovsky P, Moreno R, Ramalho-Santos J, Dominko T, Simerly C, Schatten G (1999) Ubiquitin tag for sperm mitochondria. Nature 402:371–372PubMedGoogle Scholar
  310. 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 63:582–590PubMedGoogle Scholar
  311. 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 114:1665–1675PubMedGoogle Scholar
  312. Sutovsky P, Terada Y, Schatten G (2001b) Ubiquitin-based sperm assay for the diagnosis of male factor infertility. Hum Reprod 16:250–258PubMedGoogle Scholar
  313. 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 61:406–413PubMedGoogle Scholar
  314. 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 71:1625–1637PubMedGoogle Scholar
  315. 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 19:628–638PubMedGoogle Scholar
  316. Sutton A, Jungnickel K, Ward J, Harris C, Florman M (2006) Functional characterization of PKDREJ, a male germ cell-restricted polycystin. J Cell Physiol 209:493–500PubMedGoogle Scholar
  317. Swain JE, Pool TB (2008) ART failure: oocyte contributions to unsuccessful fertilization. Hum Reprod Update 14:431–446PubMedGoogle Scholar
  318. 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 127:431–439PubMedGoogle Scholar
  319. 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 109:861–871PubMedGoogle Scholar
  320. 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 1473:206–215PubMedGoogle Scholar
  321. Talbot P, Geiske C, Knoll M (1999) Oocyte pickup by the mammalian oviduct. Mol Biol Cell 10:5–8PubMedGoogle Scholar
  322. 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 127:455–463PubMedGoogle Scholar
  323. 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 14:24–31PubMedGoogle Scholar
  324. 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 85:357–366PubMedGoogle Scholar
  325. 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 67:360–365PubMedGoogle Scholar
  326. Tesarik J (1998) Sperm-induced calcium oscillations. Oscillin-reopening the hunting season. Mol Hum Reprod 4:1007–1012PubMedGoogle Scholar
  327. Tesarik J (2005) Paternal effects on cell division in the human preimplantation embryo. Reprod Biomed Online 10:370–375PubMedGoogle Scholar
  328. Tesarik J, Mendoza C (1999) In vitro fertilization by intracytoplasmic sperm injection. BioEssays 21:791–801PubMedGoogle Scholar
  329. 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 19:611–615PubMedGoogle Scholar
  330. 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 69:254–260PubMedGoogle Scholar
  331. 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 3:1053–1060PubMedGoogle Scholar
  332. Töpfer-Petersen E (1999) Carbohydrate-based interactions on the route of a spermatozoon to fertilization. Hum Reprod Update 5:314–329PubMedGoogle Scholar
  333. Töpfer-Petersen E, Henschen A (1987) Acrosin shows zona and fucose- binding, novel properties for a serine proteinase. FEBS Lett 226:38–42PubMedGoogle Scholar
  334. 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 369:69–76PubMedGoogle Scholar
  335. Töpfer-Petersen E, Friess AE, Nguyen H, Schill WB (1985) Evidence for a fucose-bindng protein in boar spermatozoa. Histochemistry 83:139–145PubMedGoogle Scholar
  336. 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 265:51–54PubMedGoogle Scholar
  337. Töpfer-Petersen E, Calvete JJ, Schäfer W, Henschen A (1990b) Complete localization of disulfide bridges and glycosylation sites in boar sperm acrosin. FEBS Lett 275:139–142PubMedGoogle Scholar
  338. 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 30:217–224PubMedGoogle Scholar
  339. Töpfer-Petersen E, Ekhlasi-Hundrieser M, Tsolova M (2008) Glycobiology of fertilization in the pig. Int J Dev Biol 52:717–736PubMedGoogle Scholar
  340. 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 59:22–29PubMedGoogle Scholar
  341. Tranter R, Read JA, Jones R, Brady RL (2000) Effector sites in the three-dimensional structure of mammalian sperm β-acrosin. Structure 8:1179–1188PubMedGoogle Scholar
  342. 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 24:313–324PubMedGoogle Scholar
  343. 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:e11204PubMedGoogle Scholar
  344. Tyler JP, Pryor JP, Collins WP (1981) Heterologous ovum penetration by human spermatozoa. J Reprod Fertil 63:499–508PubMedGoogle Scholar
  345. Vadnais ML, Foster DN, Roberts KP (2008) Molecular cloning and expression of the CRISP family of proteins in the boar. Biol Reprod 79:1129–1134PubMedGoogle Scholar
  346. Van Blerkom J (2000) Intrafollicular influences on human oocyte developmental competence: perifollicular vascularity, oocyte metabolism and mitochondrial function. Hum Reprod 15(Suppl 2):173–188PubMedGoogle Scholar
  347. 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 122:1008–1022PubMedGoogle Scholar
  348. 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 13:445–454PubMedGoogle Scholar
  349. Verhage M (2009) Organelle docking: R-SNAREs are late. Proc Natl Acad Sci USA 106:19745–19746PubMedGoogle Scholar
  350. Verhage M, Toonen RF (2007) Regulated exocytosis: merging ideas on fusing membranes. Curr Opin Cell Biol 19:402–408PubMedGoogle Scholar
  351. Vjugina U, Evans JP (2008) New insights into the molecular basis of mammalian sperm-egg membrane interactions. Front Biosci 13:462–476PubMedGoogle Scholar
  352. Vo LH, Hedrick JL (2000) Independent and hetero-oligomeric-dependent sperm binding to egg envelope glycoprotein ZPC of Xenopus laevis. Biol Reprod 62:766–774PubMedGoogle Scholar
  353. Voges D, Zwickl P, Baumeister W (1999) The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu Rev Biochem 68:1015–1068PubMedGoogle Scholar
  354. 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 15:475–488Google Scholar
  355. 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 17:325–331PubMedGoogle Scholar
  356. 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 61:249–257PubMedGoogle Scholar
  357. Ward WS (1993) Deoxyribonucleic acid loop domain tertiary structure in mammalian spermatozoa. Biol Reprod 48:1193–1201PubMedGoogle Scholar
  358. Ward WS, Coffey DS (1991) DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol Reprod 44:569–574PubMedGoogle Scholar
  359. Wassarman PM (1995) Mammalian fertilization: egg and sperm (glyco)proteins that support gamete adhesion. Am J Reprod Immunol 33:253–258PubMedGoogle Scholar
  360. Wassarman PM (1999) Mammalian fertilization: molecular aspect of gamete adhesion exocytosis, and fusion. Cell 96:175–183PubMedGoogle Scholar
  361. Wassarman PM (2005) Contribution of mouse egg zona pellucida glycoproteins to gamete recognition during fertilization. J Cell Physiol 204:388–391PubMedGoogle Scholar
  362. Wassarman PM, Jovine L, Qi H, Williams Z, Darie C, Litscher ES (2005) Recent aspects of mammalian fertilization research. Mol Cell Endocrinol 234:95–103PubMedGoogle Scholar
  363. Wilkinson KD (1997) Regulation of ubiquitin-dependent processes by deubiquitinating enzymes. FASEB J 11:1245–1256PubMedGoogle Scholar
  364. 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 102:181–193PubMedGoogle Scholar
  365. Wojcik C, Benchaib M, Lornage J, Czyba JC, Guerin JF (2000) Proteasomes in human spermatozoa. Int J Androl 23:169–177PubMedGoogle Scholar
  366. 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 296:1104–1111PubMedGoogle Scholar
  367. 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 282:12164–12175PubMedGoogle Scholar
  368. Wykes SM, Krawetz SA (2003) The structural organization of sperm chromatin. J Biol Chem 278:29471–29477PubMedGoogle Scholar
  369. Wykes SM, Visscher DW, Krawetz SA (1997) Haploid transcripts persist in mature human spermatozoa. Mol Hum Reprod 3:15–19PubMedGoogle Scholar
  370. Yanagimachi R (1994a) Fertility of mammalian spermatozoa: its development and relativity. Zygote 2:371–372PubMedGoogle Scholar
  371. Yanagimachi R (1994b) Mammalian fertilization. In: Knobil E, Neill JD (eds) The physiology of reproduction, 2nd edn. Raven Press, New York, pp 189–317Google Scholar
  372. Yanagimachi R (1998) Intracytoplasmic sperm injection experiments using the mouse as a model. Hum Reprod 13:87–98PubMedGoogle Scholar
  373. 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 113:143–155PubMedGoogle Scholar
  374. 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, (in press)
  375. 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 77:780–793PubMedGoogle Scholar
  376. 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 84:154–163PubMedGoogle Scholar
  377. 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 341:325–340PubMedGoogle Scholar
  378. 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 35:196–210PubMedGoogle Scholar
  379. 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 308:222–231PubMedGoogle Scholar
  380. 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 260:57–63PubMedGoogle Scholar
  381. 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 70:222–227PubMedGoogle Scholar
  382. 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 118:3671–3681PubMedGoogle Scholar
  383. Yunes R, Michaut M, Tomes C, Mayorga LS (2000) Rab3A triggers the acrosome reaction in permeabilized human spermatozoa. Biol Reprod 62:1084–1089PubMedGoogle Scholar
  384. 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 273:7488–7494PubMedGoogle Scholar
  385. Zalenskaya A, Bradbury M, Zalensky O (2000) Chromatin structure of telomere domain in human sperm. Biochem Biophys Res Commun 279:213–218PubMedGoogle Scholar
  386. Zalensky A, Zalenskaya I (2007) Organization of chromosomes in spermatozoa: an additional layer of epigenetic information? Biochem Soc Trans 35:609–611PubMedGoogle Scholar
  387. 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 370:323–327PubMedGoogle Scholar
  388. Zhao XM, Song XX, Kawai Y, Niwa K (2002) Penetration in vitro of zona-free pig oocytes by homologous and heterologous spermatozoa. Theriogenology 58:995–1006PubMedGoogle Scholar
  389. 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 21:1583–1590PubMedGoogle Scholar
  390. 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) 36:227–234Google Scholar
  391. Zimmerman SW, Sutovsky P (2009) The sperm proteasome during sperm capacitation and fertilization. J Reprod Immunol 83:19–25PubMedGoogle Scholar
  392. 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:e17256PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Unit of Animal Reproduction, Department of Animal Medicine and Surgery, Faculty of Veterinary MedicineAutonomous University of BarcelonaBellaterra (Cerdanyola el Vallès, Barcelona)Spain

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