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Boar Reproduction pp 347–405Cite as

Boar Spermatozoa Within the Oviductal Environment (II): Sperm Capacitation

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Abstract

Around ovulation, a set of changes leads to a destabilisation of the sperm membrane that results in the release of spermatozoa from the oviductal reservoir (see Chap. 6). This destabilisation of the sperm membrane is an early step of the capacitation process, is mediated by bicarbonate, and allows AQN-1 to be shed from the surface. After being released from sperm reservoir, spermatozoa freely swim from the isthmus towards the ampulla/ampullary–isthmic junction where, amongst others, the following crucial and sequential events take place: (1) completion of sperm capacitation, (2) binding of spermatozoa to the ZP of the oocyte, (3) acrosome exocytosis and (4) further membrane fusion. The present chapter deals with the first issue, and thus focuses on the changes that the spermatozoon undergoes during capacitation. These changes, which can be separated between early/fast and late/slow, entail the activation of several signalling pathways, the increase of certain intracellular messengers, such as Ca2+ and cAMP, the reorganisation of proteins and lipids of sperm plasmalemma, and changes in motility patterns. Finally, destabilisation of the acrosomal sperm head membrane increases the sperm’s ability to bind the zona pellucida of the oocyte.

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References

  • Ackermann F, Zitranski N, Heydecke D, Wilhelm B, Gudermann T, Boekhoff I (2008) The multi-PDZ domain protein MUPP1 as a lipid raft-associated scaffolding protein controlling the acrosome reaction in mammalian spermatozoa. J Cell Physiol 214:757–768

    Article  PubMed  CAS  Google Scholar 

  • Adachi J, Tate S, Miyake M, Harayama H (2008) Effects of protein phosphatase inhibitor calyculin A on the postacrosomal protein serine/threonine phosphorylation state and acrosome reaction in boar spermatozoa incubated with a cAMP analog. J Reprod Dev 54:171–176

    Article  PubMed  CAS  Google Scholar 

  • Adeoya-Osiguwa SA, Fraser LR (1996) Evidence for Ca2+-dependent ATPase activity, stimulated by decapacitation factor and calmodulin, in mouse sperm. Mol Reprod Dev 44:111–120

    Article  PubMed  CAS  Google Scholar 

  • Adeoya-Osiguwa SA, Fraser LR (2002) Capacitation state-dependent changes in adenosine receptors and their regulation of adenylyl cyclase/cAMP. Mol Reprod Dev 63:245–255

    Article  PubMed  CAS  Google Scholar 

  • Adeoya-Osiguwa SA, Fraser LR (2003) Calcitonin acts as a first messenger to regulate adenylyl cyclase/cAMP and mammalian sperm function. Mol Reprod Dev 65:228–236

    Article  PubMed  CAS  Google Scholar 

  • Adeoya-Osiguwa SA, Fraser LR (2005) Cathine and norephedrine, both phenylpropanolamines, accelerate capacitation and then inhibit spontaneous acrosome loss. Hum Reprod 20:198–207

    Article  PubMed  CAS  Google Scholar 

  • Adeoya-Osiguwa SA, Gibbons R, Fraser LR (2006) Identification of functional alpha2- and beta-adrenergic receptors in mammalian spermatozoa. Hum Reprod 21:1555–1563

    Article  PubMed  CAS  Google Scholar 

  • Alnagar FA, Brennan P, Brewis IA (2010) Bicarbonate-dependent serine/threonine protein dephosphorylation in capacitating boar spermatozoa. J Androl 31:393–405

    Article  PubMed  CAS  Google Scholar 

  • Alonso A, Sasin J, Bottini N, Friedberg I, Friedberg I, Osterman A, Godzik A, Hunter T, Dixon J, Mustelin T (2004) Protein tyrosine phosphatases in the human genome. Cell 117:699–711

    Article  PubMed  CAS  Google Scholar 

  • Anderson RG (1998) The caveolae membrane system. Annu Rev Biochem 67:199–225

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Arnoult C, Zeng Y, Florman HM (1996) ZP3-dependent activation of sperm cation channels regulates acrosomal secretion during mammalian fertilization. J Cell Biol 134:637–645

    Article  PubMed  CAS  Google Scholar 

  • Asano A, Selvaraj V, Buttke DE, Nelson JL, Green KM, Evans JE, Travis AJ (2009) Biochemical characterization of membrane fractions in murine sperm: identification of three distinct sub-types of membrane rafts. J Cell Physiol 218:537–548

    Article  PubMed  CAS  Google Scholar 

  • Ashizawa K, Wishart GJ, Katayama S, Takano D, Ranasinghe AR, Narumi K, Tsuzuki Y (2006) Regulation of acrosome reaction of fowl spermatozoa: evidence for the involvement of protein kinase C and protein phosphatase-type 1 and/or -type 2A. Reproduction 131:1017–1024

    Article  PubMed  CAS  Google Scholar 

  • Aumann T, Horne M (2012) Activity-dependent regulation of the dopamine phenotype in substantia nigra neurons. J Neurochem 121:497–515

    Article  PubMed  CAS  Google Scholar 

  • Austin CR (1951) Observations on the penetration of the sperm in the mammalian egg. Aust J Sci Res 4:581–596

    CAS  Google Scholar 

  • Awda BJ, Buhr MM (2010) Extracellular signal-regulated kinases (ERKs) pathway and reactive oxygen species regulate tyrosine phosphorylation in capacitating boar spermatozoa. Biol Reprod 83:750–758

    Article  PubMed  CAS  Google Scholar 

  • Bailey JL (2010) Factors regulating sperm capacitation. Syst Biol Reprod Med 56:334–348

    Article  PubMed  CAS  Google Scholar 

  • Bajpai M, Doncel GF (2003) Involvement of tyrosine kinase and cAMPdependent kinase cross-talk in the regulation of human sperm motility. Reproduction 126:183–195

    Article  PubMed  CAS  Google Scholar 

  • Baker MA, Hetherington L, Aitken RJ (2006) Identification of SRC as a key PKA-stimulated tyrosine kinase involved in the capacitation-associated hyperactivation of murine spermatozoa. J Cell Sci 119:3182–3192

    Article  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 Proteome Res 9:718–729

    Article  PubMed  CAS  Google Scholar 

  • Baldi E, Luconi L, Bonaccorsi L, Krausz C, Forti G (1996) Human sperm activation during capacitation and acrosome reaction: role of calcium, protein phosphorylation and lipid remodelling pathways. Front Biosci 1:189–205

    Google Scholar 

  • Barford D, Das AK, Egloff MP (1998) The structure and mechanism of protein phosphatases: insights into catalysis and regulation. Annu Rev Biophys Biomol Struct 27:133–164

    Article  PubMed  CAS  Google Scholar 

  • Bastians H, Ponstingl H (1996) The novel human protein serine/threonine phosphatase 6 is a functional homologue of budding yeast Sit4p and fission yeast pp e1, which are involved in cell cycle regulation. J Cell Sci 109:2865–2874

    PubMed  CAS  Google Scholar 

  • Baxendale RW, Fraser LR (2003) Immunolocalization of multiple Ga subunits in mammalian spermatozoa and additional evidence for Gαs. Mol Reprod Dev 65:104–113

    Article  PubMed  CAS  Google Scholar 

  • Bedford JM, Chang MC (1962) Removal of decapacitation factor from seminal plasma by high-speed centrifugation. Am J Physiol 202:179–181

    PubMed  CAS  Google Scholar 

  • Bedford L, Paine S, Sheppard PW, Mayer RJ, Roelofs J (2010) Assembly, structure, and function of the 26S proteasome. Trends Cell Biol 20:391–401

    Article  PubMed  CAS  Google Scholar 

  • Bedu-Addo K, Lefievre L, Moseley FL, Barratt CL, Publicover SJ (2005) Bicarbonate and bovine serum albumin reversibly “switch” capacitation-induced events in human spermatozoa. Mol Hum Reprod 11:683–691

    Article  PubMed  CAS  Google Scholar 

  • Bennett MK, Scheller RH (1994) Molecular correlates of synaptic vesicle docking and fusion. Curr Opin Neurobiol 4:324–329

    Article  PubMed  CAS  Google Scholar 

  • Bentley JK, Garbers DL, Domino SE, Noland TD, Van Dop C (1986) Spermatozoa contain a guanine nucleotide-binding protein ADP-ribosylated by pertussis toxin. Biochem Biophys Res Commun 138:728–734

    Article  PubMed  CAS  Google Scholar 

  • Bergqvist AS, Ballester J, Johannisson A, Hernández M, Lundeheim N, Rodríguez-Martínez H (2006) In vitro capacitation of bull spermatozoa by oviductal fluid and its components. Zygote 14:259–273

    Google Scholar 

  • Bergqvist AS, Ballester J, Johannisson A, Lundeheim N, Rodríguez-Martínez H (2007) Heparin and dermatan sulphate induced capacitation of frozen-thawed bull spermatozoa measured by merocyanine-540. Zygote 15:225–232

    Google Scholar 

  • Bernabò N, Pistilli MG, Mattioli M, Barboni B (2010a) Role of TRPV1 channels in boar spermatozoa acquisition of fertilizing ability. Mol Cell Endocrinol 323:224–231

    Article  PubMed  CAS  Google Scholar 

  • Bernabò N, Mattioli M, Barboni B (2010b) The spermatozoa caught in the net: the biological networks to study the male gametes post-ejaculatory life. BMC Syst Biol 4:87

    Article  PubMed  CAS  Google Scholar 

  • Bernabò N, Berardinelli P, Mauro A, Russo V, Lucidi P, Mattioli M, Barboni B (2011) The role of actin in capacitation-related signaling: an in silico and in vitro study. BMC Syst Biol 5:47

    Article  PubMed  CAS  Google Scholar 

  • Bose S, Mason GG, Rivett AJ (1999) Phosphorylation of proteasomes in mammalian cells. Mol Biol Rep 26:11–14

    Article  PubMed  CAS  Google Scholar 

  • Botto L, Beretta E, Bulbarelli A, Rivolta I, Lettiero B, Leone BE, Miserocchi G, Palestini P (2008) Hypoxia-induced modifications in plasma membranes and lipid microdomains in A549 cells and primary human alveolar cells. J Cell Biochem 105:503–513

    Article  PubMed  CAS  Google Scholar 

  • Botto L, Bernabò N, Palestini P, Barboni B (2010) Bicarbonate induces membrane reorganization and CBR1 and TRPV1 endocannabinoid receptor migration in lipid microdomains in capacitating boar spermatozoa. J Membr Biol 238:33–41

    Article  PubMed  CAS  Google Scholar 

  • Brami-Cherrier K, Valjent E, Garcia M, Pages C, Hipskind RA, Caboche J (2002) Dopamine induces a PI3-kinase-independent activation of Akt in striatal neurons: a new route to camp response element-binding protein phosphorylation. J Neurosci 22:8911–8921

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Breitbart H, Cohen G, Rubinstein S (2005) Role of actin cytoskeleton in mammalian sperm capacitation and the acrosome reaction. Reproduction 129:263–268

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Brown DA (2006) Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiol (Bethesda) 21:430–439

    Article  CAS  Google Scholar 

  • Brush MH, Shenolikar S (2008) Control of cellular GADD34 levels by the 26S proteasome. Mol Cell Biol 28:6989–7000

    Article  PubMed  CAS  Google Scholar 

  • Buffone MG, Verstraeten SV, Calamera JC, Doncel GF (2009) High cholesterol content and decreased membrane fluidity in human spermatozoa are associated with protein tyrosine phosphorylation and functional deficiencies. J Androl 30:552–558

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Cancel AM, Lobdell D, Mendola P, Perreault SD (2000) Objective evaluation of hyperactivated motility in rat spermatozoa using computer-assisted sperm analysis. Hum Reprod 15:1322–1328

    Article  PubMed  CAS  Google Scholar 

  • Carrera A, Moos J, Ning XP, Gerton GL, Tesarik J, Kopf GS, Moss SB (1996) Regulation of protein tyrosine phosphorylation in human sperm by a calcium/calmodulin-dependent mechanism: identification of A kinase anchor proteins as major substrates for tyrosine phosphorylation. Dev Biol 180:284–296

    Article  PubMed  CAS  Google Scholar 

  • Chakrabarti R, Cheng L, Puri P, Soler D, Vijayaraghavan S (2007a) Protein phosphatase PP1 gamma 2 in sperm morphogenesis and epididymal initiation of sperm motility. Asian J Androl 9:445–452

    Article  PubMed  CAS  Google Scholar 

  • Chakrabarti R, Kline D, Lu J, Orth J, Pilder S, Vijayaraghavan S (2007b) Analysis of Ppp1cc-null mice suggests a role for PP1gamma2 in sperm morphogenesis. Biol Reprod 76:992–1001

    Article  PubMed  CAS  Google Scholar 

  • Chang MC (1951) Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature 168:697–698

    Article  PubMed  CAS  Google Scholar 

  • Chang MC (1959) Fertilization of rabbit ova in vitro. Nature 184:466–467

    Article  PubMed  Google Scholar 

  • Chaud M, Fernández J, Viggiano M, Gimeno MF, Gimeno AL (1983) Is there a role for dopamine in the regulation of motility of sow oviducts? Pharmacol Res Commun 15:923–936

    Article  PubMed  CAS  Google Scholar 

  • Chen Y, Cann MJ, Litvin TN, Iourgenko V, Sinclair ML, Levin LR, Buck J (2000) Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Sci 289:625–628

    Google Scholar 

  • Chen YA, Scheller RH (2001) SNARE-mediated membrane fusion. Nat Rev Mol Cell Biol 2:98–106

    Article  PubMed  CAS  Google Scholar 

  • Choi BH, Hur EM, Lee JH, Jun DJ, Kim KT (2006) Protein kinase Cdelta-mediated proteasomal degradation of MAP kinase phosphatase-1 contributes to glutamate-induced neuronal cell death. J Cell Sci 119:1329–1340

    Article  PubMed  CAS  Google Scholar 

  • Choi YH, Toyoda Y (1998) Cyclodextrin removes cholesterol from mouse sperm and induces capacitation in a protein-free medium. Biol Reprod 59:1328–1333

    Article  PubMed  CAS  Google Scholar 

  • Choi YJ, Uhm SJ, Song SJ, Song H, Park JK, Kim T, Park C, Kim JH (2008) Cytochrome c upregulation during capacitation and spontaneous acrosome reaction determines the fate of pig sperm cells: linking proteome analysis. J Reprod Dev 54:68–83

    Article  PubMed  CAS  Google Scholar 

  • Ciechanover A (1998) The ubiquitin-proteasome pathway: on protein death and cell life. EMBO J 17:7151–7160

    Article  PubMed  CAS  Google Scholar 

  • Ciechanover A (2005a) Intracellular protein degradation: from a vague idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Cell Death Differ 12:1178–1190

    Article  PubMed  CAS  Google Scholar 

  • Ciechanover A (2005b) Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat Rev Mol Cell Biol 6:79–87

    Article  PubMed  CAS  Google Scholar 

  • Ciechanover A (2006) The ubiquitin proteolytic system: from a vague idea, through basic mechanisms, and onto human diseases and drug targeting. Neurology 66:S7–S19

    Article  PubMed  Google Scholar 

  • Ciechanover A, Schwartz AL (1998) The ubiquitin-proteasome pathway: the complexity and myriad functions of proteins death. Proc Natl Acad Sci USA 95:2727–2730

    Article  PubMed  CAS  Google Scholar 

  • Cohen PT (1989) The structure and regulation of protein phosphatases. Annu Rev Biochem 58:453–508

    Article  PubMed  CAS  Google Scholar 

  • Cohen PT (2002) Protein phosphatase 1-targeted in many directions. J Cell Sci 115:241–256

    PubMed  CAS  Google Scholar 

  • Cornett LE, Meizel S (1978) Stimulation of in vitro activation and the acrosome reaction of hamster spermatozoa by catecholamines. Proc Natl Acad Sci USA 75:4954–4958

    Article  PubMed  CAS  Google Scholar 

  • Cross NL (2004) Reorganization of lipid rafts during capacitation of human sperm. Biol Reprod 71:1367–1373

    Article  PubMed  CAS  Google Scholar 

  • Cummerson JA, Flanagan BF, Spiller DG, Johnson PM (2006) The complement regulatory proteins CD55 (decay accelerating factor) and CD59 are expressed on the inner acrosomal membrane of human spermatozoa as well as CD46 (membrane cofactor protein). Immunology 118:333–342

    Article  PubMed  CAS  Google Scholar 

  • Das SK, Yano S, Wang J, Edwards DR, Nagase H, Dey SK (1997) Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in the mouse uterus during the peri-implantation period. Dev Genet 21:44–54

    Article  PubMed  CAS  Google Scholar 

  • DasGupta S, Mills CL, Fraser LR (1994) A possible role for Ca2+-ATPase in human sperm capacitation. J Reprod Fertil 102:107–116

    Article  PubMed  CAS  Google Scholar 

  • De Blas GA, Roggero CM, Tomes CN, Mayorga LS (2005) Dynamics of SNARE assembly and disassembly during sperm acrosomal exocytosis. PLoS Biol 3:1801–1812

    Article  CAS  Google Scholar 

  • De Lamirande E, Leclerc P, Gagnon C (1997) Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol Hum Reprod 3:175–194

    Article  PubMed  Google Scholar 

  • Demarco IA, Espinosa F, Edwards J, Sosnik J, de la Vega-Beltran JL, Hockensmith JW, Kopf GS, Darszon A, Visconti PE (2003) Involvement of a Na+/HCO-3 cotransporter in mouse sperm capacitation. J Biol Chem 278:7001–7009

    Article  PubMed  CAS  Google Scholar 

  • Dostàlovà Z, Calvete JJ, Sanz L, Töpfer-Petersen E (1994) Quantitation of boar spermadhesins in accessory sex gland fluids and on the surface of epididymal, ejaculated and capacitated spermatozoa. Biochim Biophys Acta 1200:48–54

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Elliott RM, Lloyd RE, Fazeli A, Sostaric E, Georgiou AS, Satake N, Watson PF, Holt WV (2009) Effects of HSPA8, an evolutionarily conserved oviductal protein, on boar and bull spermatozoa. Reproduction 137:191–203

    Article  PubMed  CAS  Google Scholar 

  • Esposito G, Jaiswal BS, Xie F, Krajnc-Franken MA, Robben TJ, Strik AM, Kuil C, Philipsen RL, van Duin M, Conti M, Gossen JA (2004) Mice deficient for soluble adenylyl cyclase are infertile because of a severe sperm-motility defect. Proc Natl Acad Sci USA 101:2993–2998

    Article  PubMed  CAS  Google Scholar 

  • Fait G, Vered Y, Yogev L, Gamzu R, Lessing JB, Paz G, Yavetz H (2001) High levels of catecholamines in human semen: a preliminary study. Andrologia 33:347–350

    Article  PubMed  CAS  Google Scholar 

  • Fardilha M, Esteves SL, Korrodi-Gregório L, Pelech S, Da Cruz e Silva OA, Da Cruz e Silva E (2011) Protein phosphatase 1 complexes modulate sperm motility and present novel targets for male infertility. Mol Hum Reprod 17:466–477

    Article  PubMed  CAS  Google Scholar 

  • Fazeli A, Duncan AE, Watson PF, Holt WV (1999) Sperm-oviduct interaction: induction of capacitation and preferential binding of uncapacitated spermatozoa to oviductal epithelial cells in porcine species. Biol Reprod 60:879–886

    Article  PubMed  CAS  Google Scholar 

  • Fernández I, Ying Y, Albanesi J, Anderson RG (2002) Mechanism of caveolin filament assembly. Proc Natl Acad Sci USA 99:11193–11198

    Article  PubMed  Google Scholar 

  • Fernández-Novell JM, Ballester J, Altirriba J, Ramió-Lluch L, Barberà A, Gomis R, Guinovart JJ, Rodríguez-Gil JE (2011) Glucose and fructose as functional modulators of overall dog, but not boar sperm function. Reprod Fertil Develop 23:468–480

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Fisher HM, Brewis IA, Barratt CL, Cooke ID, Moore HD (1998) Phosphoinositide 3-kinase is involved in the induction of the human sperm acrosome reaction downstream of tyrosine phosphorylation. Mol Hum Reprod 4:849–855

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Flesch FM, Voorhout WF, Colenbrander B, van Golde LM, Gadella BM (1998) Use of lectins to characterize plasma membrane preparations from boar spermatozoa: a novel technique for monitoring membrane purity and quantity. Biol Reprod 1998:1530–1539

    Article  Google Scholar 

  • Flesch FM, Wijnand E, van de Lest CH, Colenbrander B, van Golde LM, Gadella BM (2001a) Capacitation dependent activation of tyrosine phosphorylation generates two sperm head plasma membrane proteins with high primary binding affinity for the zona pellucida. Mol Reprod Dev 60:107–115

    Article  PubMed  CAS  Google Scholar 

  • Flesch FM, Brouwers JF, Nievelstein PF, Verkleij AJ, van Golde LM, Colenbrander B, Gadella BM (2001b) Bicarbonate stimulated phospholipid scrambling induces cholesterol redistribution and enables cholesterol depletion in the sperm plasma membrane. J Cell Sci 114:3543–3555

    PubMed  CAS  Google Scholar 

  • Florman HM (1995) Sequential focal and global elevations of sperm intracellular Ca2+ are initiated by the zona pellucida during acrosomal exocytosis. Dev Biol 165:152–164

    Article  Google Scholar 

  • Florman HM, Jungnickel MK, Sutton KA (2008) Regulating the acrosome reaction. Int J Dev Biol 52:503–510

    Article  PubMed  CAS  Google Scholar 

  • Forgacs G, Yook SH, Janmey PA, Jeong H, Burd CG (2004) Role of the cytoskeleton in signaling networks. J Cell Sci 117:2769–2775

    Google Scholar 

  • Fraser LR (1984) Mouse sperm capacitation in vitro involves the loss of a surface-associated inhibitory component. J Reprod Fertil 72:373–384

    Article  PubMed  CAS  Google Scholar 

  • Fraser LR (1998a) Interactions between a decapacitation factor and mouse spermatozoa appear to involve fucose residues and a GPI-anchored receptor. Mol Reprod Dev 51:193–202

    Article  PubMed  CAS  Google Scholar 

  • Fraser LR (1998b) Fertilization promoting peptide: an important regulator of sperm function in vivo? Rev Reprod 3:151–154

    Article  PubMed  CAS  Google Scholar 

  • Fraser LR (2008) The role of small molecules in sperm capacitation. Theriogenology 70:1356–1359

    Article  PubMed  CAS  Google Scholar 

  • Fraser LJ (2010) The “switching on” of mammalian spermatozoa: molecular events involved in promotion and regulation of capacitation. Mol Reprod Dev 77:197–208

    PubMed  CAS  Google Scholar 

  • Fraser LR, Osiguwa OO (2004) Human sperm responses to calcitonin, angiotensin II and fertilization-promoting peptide in prepared semen samples from normal donors and infertility patients. Hum Reprod 19:596–606

    Article  PubMed  CAS  Google Scholar 

  • Fraser LR, Harrison RAP, Herod JE (1990) Characterization of a decapacitation factor associated with epididymal mouse spermatozoa. J Reprod Fertil 89:135–148

    Article  PubMed  CAS  Google Scholar 

  • Fraser LR, Hosseini R, Hanyaloglu A, Talmor A, Dudley RK (1997) TCP-11, the product of a mouse t-complex gene, plays a role in stimulation of capacitation and inhibition of the spontaneous acrosome reaction. Mol Reprod Dev 48:375–382

    Article  PubMed  CAS  Google Scholar 

  • Fraser LR, Adeoya-Osiguwa SA (1999) Modulation of adenylyl cyclase by FPP and adenosine involves stimulatory and inhibitory adenosine receptors and G proteins. Mol Reprod Dev 53:459–471

    Article  PubMed  CAS  Google Scholar 

  • Fraser LR, Adeoya-Osiguwa SA, Baxendale R (2003) First messenger regulation of capacitation via G protein-coupled mechanisms: a tale of serendipity and discovery. Mol Hum Reprod 9:739–748

    Article  PubMed  CAS  Google Scholar 

  • Fraser LR, Adeoya-Osiguwa SA, Baxendale RW, Gibbons R (2006) Regulation of mammalian sperm capacitation by endogenous molecules. Front Biosci 11:1636–1645

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Funahashi H, Romar R (2004) Reduction of the incidence of polyspermic penetration into porcine oocytes by pre-treatment of fresh spermatozoa with adenosine and a transient co-incubation of the gametes with caffeine. Reproduction 128:789–800

    Article  PubMed  CAS  Google Scholar 

  • Funahashi H, Asano A, Fujiwara T, Nagai T, Niwa K, Fraser LR (2000a) Both fertilization promoting peptide and adenosine stimulate capacitation but inhibit spontaneous acrosome loss in ejaculated boar spermatozoa in vitro. Mol Reprod Dev 55:117–124

    Article  PubMed  CAS  Google Scholar 

  • Funahashi H, Fujiwara T, Nagai T (2000b) Modulation of the function of boar spermatozoa via adenosine and fertilization promoting peptide receptors reduces the incidence of polyspermic penetration into porcine oocytes. Biol Reprod 63:1157–1163

    Article  PubMed  CAS  Google Scholar 

  • Gadella BM (2008a) Sperm membrane physiology and relevance for fertilization. Anim Reprod Sci 107:229–236

    Article  PubMed  CAS  Google Scholar 

  • Gadella BM (2008b) The assembly of a zona pellucida binding protein complex in sperm. Reprod Domest Anim 43(Suppl 5):12–19

    Article  PubMed  Google Scholar 

  • Gadella BM, Harrison RAP (2000) The capacitating agent bicarbonate induces protein kinase A-dependent changes in phospholipid transbilayer behaviour in the sperm plasma membrane. Development 127:2407–2420

    PubMed  CAS  Google Scholar 

  • Gadella BM, Harrison RAP (2002) Capacitation induces cyclic adenosine 3′, 5′-monophosphate-dependent, but apoptosis-unrelated, exposure of aminophospholipids at the apical head plasma membrane of boar sperm cells. Biol Reprod 67:340–350

    Article  PubMed  CAS  Google Scholar 

  • Gadella BM, Van Gestel RA (2004) Bicarbonate and its role in mammalian sperm function. Anim Reprod Sci 82:307–319

    Article  PubMed  CAS  Google Scholar 

  • Gadella BM, Lopes-Cardozo M, van Golde LMG, Colenbrander B, Gadella TW Jr (1995) Glycolipid migration from the apical to the equatorial subdomains of the sperm head plasma membrane precedes the acrosome reaction. Evidence for a primary capacitation event in boar spermatozoa. J Cell Biol 108:935–946

    CAS  Google Scholar 

  • Gadella BM, Tsai PS, Boerke A, Brewis IA (2008) Sperm head membrane reorganisation during capacitation. Int J Dev Biol 52:473–480

    Article  PubMed  CAS  Google Scholar 

  • Gallastegui N, Groll M (2010) The 26S proteasome: assembly and function of a destructive machine. Trends Biochem Sci 35:634–642

    Article  PubMed  CAS  Google Scholar 

  • Gallego M, Virshup DM (2005) Protein serine/threonine phosphatases: life, death, and sleeping. Curr Opin Cell Biol 17:197–202

    Article  PubMed  CAS  Google Scholar 

  • García-Herreros M, Aparicio IM, Núñez I, García-Marín LJ, Gil MC, Peña Vega FJ (2005) Boar sperm velocity and motility patterns under capacitating and non-capacitating incubation conditions. Theriogenology 63:795–805

    Article  PubMed  CAS  Google Scholar 

  • Geussova G, Kalab P, Peknicova J (2002) Valosine containing protein is a substrate of cAMP-activated boar sperm tyrosine kinase. Mol Reprod Dev 63:366–375

    Article  PubMed  CAS  Google Scholar 

  • Gibbons R, Adeoya-Osiguwa SA, Fraser LR (2005) A mouse sperm decapacitation factor receptor is phosphatidylethanolaminebinding protein 1. Reproduction 130:497–508

    Article  PubMed  CAS  Google Scholar 

  • Glenney JR Jr, Soppet D (1992) Sequence and expression of caveolin, a protein component of caveolae plasma membrane domains phosphorylated on tyrosine in Rous sarcoma virus-transformed fibroblasts. Proc Natl Acad Sci USA 89:10517–10521

    Article  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 

  • Goldberg AL (2003) Protein degradation and protection against misfolded or damaged proteins. Nature 426:895–899

    Article  PubMed  CAS  Google Scholar 

  • Green CM, Cockle SM, Watson PF, Fraser LR (1996) A possible mechanism of action for fertilization promoting peptide, a TRH-related tripeptide that promotes capacitation and fertilizing ability in mammalian spermatozoa. Mol Reprod Dev 45:244–252

    Article  PubMed  CAS  Google Scholar 

  • Groll M, Koguchi Y, Huber R, Kohno J (2001) Crystal structure of the 20 S proteasome: TMC-95A complex, a non-covalent proteasome inhibitor. J Mol Biol 311:543–548

    Article  PubMed  CAS  Google Scholar 

  • Gur Y, Breitbart H (2006) Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes. Genes Dev 20:411–416

    Google Scholar 

  • Hall DA, Strange PG (1999) Comparison of the ability of dopamine receptor agonists to inhibit forskolin-stimulated adenosine 3′ 5′-cyclic monophosphate (cAMP) accumulation via D2L (long isoform) and D3 receptors expressed in Chinese hamster ovary (CHO) cells. Biochem Pharmacol 58:285–289

    Article  PubMed  CAS  Google Scholar 

  • Han Y, Haines CJ, Feng HL (2007) Role(s) of the serine/threonine protein phosphatase 1 on mammalian sperm motility. Arch Androl 53:169–177

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Harayama H (2003) Viability and protein phosphorylation patterns of boar spermatozoa agglutinated by treatment with a cell-permeable cyclic adenosine 3′, 5′-monophosphate analog. J Androl 24:831–842

    PubMed  CAS  Google Scholar 

  • Harayama H, Nakamura K (2008) Changes of PKA and PDK1 in the principal piece of boar spermatozoa treated with a cell-permeable cAMP analog to induce flagellar hyperactivation. Mol Reprod Dev 75:1396–1407

    Article  PubMed  CAS  Google Scholar 

  • Harrison RAP (1996) Capacitation mechanisms and the role of capacitation as seen in eutherian mammals. Reprod Fertil Dev 8:581–594

    Article  PubMed  CAS  Google Scholar 

  • Harrison RAP (2004) Rapid PKA-catalysed phosphorylation of boar sperm proteins induced by the capacitating agent bicarbonate. Mol Reprod Dev 67:337–352

    Article  PubMed  CAS  Google Scholar 

  • Harrison RAP, Gadella BM (2005) Bicarbonate-induced membrane processing in sperm capacitation. Theriogenology 63:346–360

    Google Scholar 

  • Harrison RAP, Miller NG (2000) cAMP-dependent protein kinase control of plasma membrane lipid architecture in boar sperm. Mol Reprod Dev 55:220–228

    Article  PubMed  CAS  Google Scholar 

  • Harrison RAP, Ashworth PJC, Miller NGA (1996) Bicarbonate/CO2, an effector of capacitation, induces a rapid and reversible change in the lipid architecture of boar sperm plasma membranes. Mol Reprod Dev 145:378–391

    Article  Google Scholar 

  • Helm G, Owman C, Rosengres E, Sjoberg NO (1982) Regional and cyclic variations in catecholamine concentration of the human fallopian tube. Biol Reprod 26:553–558

    Article  PubMed  CAS  Google Scholar 

  • Hess KC, Jones BH, Marquez B, Chen Y, Ord TS, Kamenetsky M, Miyamoto C, Zippin JH, Kopf GS, Suarez SS, Levin LR, Williams CJ, Buck J, Moss SB (2005) The “soluble” adenylyl cyclase in sperm mediates multiple signaling events required for fertilization. Dev Cell 9:249–259

    Article  PubMed  CAS  Google Scholar 

  • Heydecke D, Meyer D, Ackermann F, Wilhelm B, Gudermann T, Boekhoff I (2006) The multi PDZ domain protein MUPP1 as a putative scaffolding protein for organizing signaling complexes in the acrosome of mammalian spermatozoa. J Androl 27:390–404

    Article  PubMed  CAS  Google Scholar 

  • Hicke L, Dunn R (2003) Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 19:141–172

    Article  PubMed  CAS  Google Scholar 

  • Himmler A, Stratowa C, Czernilofsky AP (1993) Functional testing of human dopamine D1 and D5 receptors expressed in stable cAMP-responsive luciferase reporter cell lines. J Recept Res 13:79–84

    PubMed  CAS  Google Scholar 

  • Ho K, Wolff CA, Suarez SS (2009) CatSper-null spermatozoa are unable to ascend beyond the oviductal reservoir. Reprod Fertil Dev 21:345–350

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Holt WV, Harrison RAP (2002) Bicarbonate stimulation of boar sperm motility via a protein kinase A-dependent pathway between cell and between ejaculate differences are not due to deficiencies in protein kinase A activation. J Androl 23:557–565

    PubMed  CAS  Google Scholar 

  • Hunter RH, Hall JP (1974) Capacitation of boar spermatozoa: synergism between uterine and tubal environments. J Exp Zool 188:203–214

    Article  PubMed  CAS  Google Scholar 

  • Hunter RH, Huang WT, Holtz W (1998) Regional influences of the fallopian tubes on the role of boar sperm capacitation in surgically inseminated gilts. J Reprod Fertil 114:17–23

    Article  PubMed  CAS  Google Scholar 

  • Hunter RH, Rodríguez-Martínez H (2004) Capacitation of mammalian spermatozoa in vivo, with a specific focus on events in the fallopian tubes. Mol Reprod Dev 67:243–250

    Article  PubMed  CAS  Google Scholar 

  • Jahn R, Sudhof TC (1994) Synaptic vesicles and exocytosis. Annu Rev Neurosci 17:219–246

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Janmey PA (1998) The cytoskeleton and cell signaling: component localization and mechanical coupling. Physiol Rev 78:763–778

    PubMed  CAS  Google Scholar 

  • Janssens V, Goris J (2001) Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 353:417–439

    Article  PubMed  CAS  Google Scholar 

  • Jarrahian A, Watts VJ, Barker EL (2004) D2 dopamine receptors modulate Gs-subunit coupling of the CB1 cannabinoid receptor. J Pharmacol Exp Ther 308:880–886

    Article  PubMed  CAS  Google Scholar 

  • Jin J, Jin N, Zheng H, Ro S, Tafolla D, Sanders KM, Yan W (2007) Catsper3 and Catsper4 are essential for sperm hyperactivated motility and male fertility. Biol Reprod 77:37–44

    Article  PubMed  CAS  Google Scholar 

  • Kalab P, Peknicová J, Geussová G, Moos J (1998) Regulation of protein tyrosine phosphorylation in boar sperm through a cAMP-dependent pathway. Mol Reprod Dev 51:304–314

    Article  PubMed  CAS  Google Scholar 

  • Khatchadourian C, Menezo Y, Gerard M, Thibault C (1987) Catecholamines within the rabbit oviduct at fertilization time. Hum Reprod 2:1–5

    Article  PubMed  CAS  Google Scholar 

  • Kihara T, Shimohama S, Sawada H, Honda K, Nakamizo T, Kanki R, Yamashita H, Akaike A (2002) Protective effect of dopamine D2 agonists in cortical neurons via the phosphatidylinositol l3 kinase cascade. J Neurosci Res 70:274–282

    Article  PubMed  CAS  Google Scholar 

  • Killian JG (2004) Evidence for the role of oviduct secretions in sperm function, fertilization and embryo development. Anim Reprod Sci 82:141–153

    Article  PubMed  CAS  Google Scholar 

  • Kirichok Y, Navarro B, Clapham DE (2006) Whole-cell patch-clamp measurements of spermatozoa reveal an alkaline-activated Ca2+ channel. Nature 439:737–740

    Article  PubMed  CAS  Google Scholar 

  • Kondoh K, Nishida E (2007) Regulation of MAP kinases by MAP kinase phosphatases. Biochim Biophys Acta 1773:1227–1237

    Article  PubMed  CAS  Google Scholar 

  • Kong M, Diaz 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

    Article  PubMed  CAS  Google Scholar 

  • Kopf GS, Woolkalis MJ, Gerton GL (1986) Evidence for a guanine nucleotide-binding regulatory protein in invertebrate and mammalian sperm. Identification by islet-activating protein-catalyzed ADP-ribosylation and immunochemical methods. J Biol Chem 261:7327–7331

    PubMed  CAS  Google Scholar 

  • Kotwica G, Kurowicka B, Franczak A, Grzegorzewski W, Wrobel M, Mlynarczuk J, Kotwica J (2003) The concentrations of catecholamines and oxytocin receptors in the oviduct and its contractile activity in cows during the estrous cycle. Theriogenology 60:953–964

    Article  PubMed  CAS  Google Scholar 

  • Krapf D, Arcelay E, Wertheimer EV, Sanjay A, Pilder SH, Salicioni AM, Visconti PE (2010) Inhibition of Ser/Thr phosphatases induces capacitation-associated signaling in the presence of Src kinase inhibitors. J Biol Chem 285:7977–7985

    Article  PubMed  CAS  Google Scholar 

  • Lai EC (2003) Lipid rafts make for slippery platforms. J Cell Biol 162:365–370

    Article  PubMed  CAS  Google Scholar 

  • Leahy T, Gadella BM (2011) Capacitation and capacitation-like sperm surface changes induced by handling boar semen. Reprod Domest Anim 46(Suppl 2):7–13

    Article  PubMed  Google Scholar 

  • Leclerc P, Goupil S (2002) Regulation of the human sperm tyrosine kinase c-yes. Activation by cyclic adenosine 3′, 5′-monophosphate and inhibition by Ca2+. Biol Reprod 67:301–307

    Article  PubMed  CAS  Google Scholar 

  • Liberda J, Manaskova P, Prelovska L, Ticha M, Jonáková V (2006) Saccharide-mediated interactions of boar sperm surface proteins with components of the porcine oviduct. J Reprod Immunol 71:112–125

    Article  PubMed  CAS  Google Scholar 

  • Lindner R, Naim HY (2009) Domains in biological membranes. Exp Cell Res 315:2871–2878

    Article  PubMed  CAS  Google Scholar 

  • Litvin TN, Kamenetsky M, Zarifyan A, Buck J, Levin LR (2003) Linetic properties of “soluble” adenylyl cyclase. Synergism between calcium and bicarbonate. J Biol Chem 278:15922–15926

    Article  PubMed  CAS  Google Scholar 

  • Liu DY, Clarke GN, Baker HW (2006) Tyrosine phosphorylation on capacitated human sperm tail detected by immunofluorescence correlates strongly with sperm-zona pellucida (ZP) binding but not with the ZP-induced acrosome reaction. Hum Reprod 21:1002–1008

    Article  PubMed  CAS  Google Scholar 

  • Lloyd RE, Elliott RM, Fazeli A, Watson PF, Holt WV (2009) Effects of oviductal proteins, including heat shock 70 kDa protein 8, on survival of ram spermatozoa over 48 h in vitro. Reprod Fertil Dev 21:408–418

    Article  PubMed  CAS  Google Scholar 

  • Lloyd RE, Fazeli A, Watson PF, Holt WV (2012) The oviducal protein, heat-shock 70 kDa protein 8, improves the long-term survival of ram spermatozoa during storage at 17 °C in a commercial extender. Reprod Fertil Dev 24:543–549

    Article  PubMed  CAS  Google Scholar 

  • Luconi M, Barni T, Vannelli GB, Krausz C, Marra F, Benedetti PA, Evangelista V, Francavilla S, Properzi G, Forti G, Baldi E (1998a) Extracellular signal-regulated kinases modulate capacitation of human spermatozoa. Biol Reprod 58:1476–1489

    Article  PubMed  CAS  Google Scholar 

  • Luconi M, Krausz C, Barni T, Vannelli GB, Forti G, Baldi E (1998b) Progesterone stimulates p42 extracellular signal-regulated kinase (p42erk) in human spermatozoa. Mol Hum Reprod 4:251–258

    Article  PubMed  CAS  Google Scholar 

  • Maccarrone M, Barboni B, Paradisi A, Bernabò N, Gasperi V, Pistilli MG, Fezza F, Lucidi P, Mattioli M (2005) Characterization of the endocannabinoid system in boar spermatozoa and implications for sperm capacitation and acrosome reaction. J Cell Sci 118:4393–4404

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Heredia J, de Mateo S, Vidal-Taboada JM, Ballesca JL, Oliva R (2008) Identification of proteomic differences in asthenozoospermic sperm samples. Hum Reprod 23:783–791

    Article  PubMed  CAS  Google Scholar 

  • Matveev S, Li X, Everson W, Smart EJ (2001) The role of caveolae and caveolin in vesicle-dependent and vesicle-independent trafficking. Adv Drug Deliv Rev 49:237–250

    Article  PubMed  CAS  Google Scholar 

  • Mayor S, Riezman H (2004) Sorting GPI-anchored proteins. Nat Rev Mol Cell Biol 5:110–120

    Article  PubMed  CAS  Google Scholar 

  • Meizel S (2004) The sperm, a neuron with a tail: ‘neuronal’ receptors in mammalian sperm. Biol Rev Camb Philos Soc 79:713–732

    Article  PubMed  Google Scholar 

  • Millward TA, Zolnierowicz S, Hemmings BA (1999) Regulation of protein kinase cascades by protein phosphatase 2A. Trends Biochem Sci 24:186–191

    Article  PubMed  CAS  Google Scholar 

  • Mishra S, Somanath PR, Huang Z, Vijayaraghavan S (2003) Binding and inactivation of the germ cell-specific protein phosphatase PP1gamma2 by sds22 during epididymal sperm maturation. Biol Reprod 69:1572–1579

    Article  PubMed  CAS  Google Scholar 

  • Missale C, Nash SR, Robinson SW, Jaber M, Caron MG (1998) Dopamine receptors: from structure to function. Physiol Rev 78:189–225

    PubMed  CAS  Google Scholar 

  • Mitchell LA, Nixon B, Baker MA, Aitken RJ (2008) Investigation of the role of SRC in capacitation-associated tyrosine phosphorylation of human spermatozoa. Mol Hum Reprod 14:235–243

    Article  PubMed  CAS  Google Scholar 

  • Morales P, Diaz 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 

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

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Morgan DJ, Weisenhaus M, Shum S, Su T, Zheng R, Zhang C, Shokat KM, Hille B, Babcock DF, McKnight GS (2008) Tissue-specific PKA inhibition using a chemical genetic approach and its application to studies on sperm capacitation. Proc Natl Acad Sci USA 105:20740–20745

    Article  PubMed  CAS  Google Scholar 

  • Murata M, Peränen J, Schreiner R, Wieland F, Kurzchalia TV, Simons K (1996) VIP21/caveolin is a cholesterol-binding protein. Proc Natl Acad Sci USA 92:10339–10343

    Article  Google Scholar 

  • Muratori M, Marchiani S, Tamburrino L, Forti G, Luconi M, Baldi E (2011) Markers of human sperm functions in the ICSI era. Front Biosci 16:1344–1363

    Article  PubMed  CAS  Google Scholar 

  • Murray SC, Smith TT (1997) Sperm interaction with the fallopian tube apical membrane enhances sperm motility and delays capacitation. Fertil Steril 68:351–357

    Article  PubMed  Google Scholar 

  • Naaby-Hansen S, Mandal A, Wolkowicz MJ, Sen B, Westbrook VA, Shetty J, Coonrod SA, Klotz KL, Kim YH, Bush LA, Flickinger CJ, Herr JC (2002) CABYR, a novel calcium-binding tyrosine phosphorylation-regulated fibrous sheath protein involved in capacitation. Dev Biol 242:236–254

    Article  PubMed  CAS  Google Scholar 

  • Nair VD, Sealfon SC (2003) Agonist-specific transactivation of phosphoinositide 3-kinase signaling pathway mediated by the dopamine D2 receptor. J Biol Chem 278:47053–47061

    Article  PubMed  CAS  Google Scholar 

  • Naz RK (1999) Involvement of protein serine and threonine phosphorylation in human sperm capacitation. Biol Reprod 60:1402–1409

    Article  PubMed  CAS  Google Scholar 

  • Naz RK, Rajesh PB (2004) Role of tyrosine phosphorylation in sperm capacitation/acrosome reaction. Reprod Biol Endocrinol 2:75

    Article  PubMed  CAS  Google Scholar 

  • Nichol R, Hunter RH, de Lamirande E, Gagnon C, Cooke GM (1997) Motility of spermatozoa in hydrosalpingeal and follicular fluid of pigs. J Reprod Fertil 110:79–86

    Article  PubMed  CAS  Google Scholar 

  • Nolan MA, Babcock DF, Wennemuth G, Brown W, Burton KA, McKnight GS (2004) Sperm-specific protein kinase A catalytic subunit C-alpha2 orchestrates cAMP signaling for male fertility. Proc Natl Acad Sci USA 101:13483–13488

    Article  PubMed  CAS  Google Scholar 

  • Otth C, Torres M, Ramírez A, Fernandez C, Castro M, Rauch MC, Brito M, Yañez A, Rodríguez-Gil JE, Slebe JC, Concha II (2007) Identification of peripheral dopaminergic D2 receptor in rat male germ cells. J Cell Biochem 100:141–150

    Article  PubMed  CAS  Google Scholar 

  • Pardo PS, Murray PF, Walz K, Franco L, Passeron S (1998) In vivo and in vitro phosphorylation of the alpha 7/PRS1 subunit of Saccharomyces cerevisiae 20 S proteasome: in vitro phosphorylation by protein kinase CK2 is absolutely dependent on polylysine. Arch Biochem Biophys 349:397–401

    Article  PubMed  CAS  Google Scholar 

  • Pariset C, Weinman S (1994) Differential localization of two isoforms of the regulatory subunit RII alpha of cAMP-dependent protein kinase in human sperm: biochemical and cytochemical study. Mol Reprod Dev 39:415–422

    Article  PubMed  CAS  Google Scholar 

  • Parton RG, Richards AA (2003) Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic 4:724–738

    Article  PubMed  CAS  Google Scholar 

  • Parton RG, Simons K (2007) The multiple faces of caveolae. Nat Rev Mol Cell Biol 8:185–194

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Petrunkina AM, Simon K, Günzel-Apel AR, Töpfer-Petersen E (2003) Regulation of capacitation of canine spermatozoa during co-culture with heterologous oviductal epithelial cells. Reprod Domest Anim 38:455–463

    Article  PubMed  CAS  Google Scholar 

  • Petrunkina AM, Simon K, Günzel-Apel AR, Töpfer-Petersen E (2004) Kinetics of protein tyrosine phosphorylation in sperm selected by binding to homologous and heterologous oviductal explants: how specific is the regulation by the oviduct? Theriogenology 61:1617–1634

    Article  PubMed  CAS  Google Scholar 

  • Picconi B, Piccoli G, Calabresi P (2012) Synaptic dysfunction in Parkinson’s disease. Adv Exp Med Biol 970:553–572

    Article  PubMed  CAS  Google Scholar 

  • Pike LJ (2009) The challenge of lipid rafts. J Lipid Res 50:S323–S328

    Article  PubMed  CAS  Google Scholar 

  • Pollard JW, Plante C, King WA, Hansen PJ, Betteridge KJ, Suarez SS (1991) Fertilizing capacity of bovine sperm may be maintained by the binding of oviductal epithelial cells. Biol Reprod 44:102–107

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Qi H, Moran MM, Navarro B, Chong JA, Krapivinsky G, Krapivinsky L, Kirichok Y, Ramsey IS, Quill TA, Clapham DE (2007) All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility. Proc Natl Acad Sci USA 104:1219–1223

    Article  PubMed  CAS  Google Scholar 

  • Quill TA, Sugden SA, Rossi KL, Doolittle LK, Hammer RE, Garbers DL (2003) Hyperactivated sperm motility driven by CatSper2 is required for fertilization. Proc Natl Acad Sci USA 100:14869–14874

    Article  PubMed  CAS  Google Scholar 

  • Ramalho-Santos J, Moreno RD, Sutovsky P, Chan AW, Hewitson L, Wessel GM, Simerly CR, Schatten G (2000) SNAREs in mammalian sperm: possible implications for fertilization. Dev Biol 223:54–69

    Article  PubMed  CAS  Google Scholar 

  • Ramió-Lluch L, Fernández-Novell JM, Peña A, Bucci D, Rigau T, Rodríguez-Gil JE (2012) “In vitro” capacitation and subsequent acrosome reaction are related to changes in the expression and location of midpiece actin and mitofusin-2 in boar spermatozoa. Theriogenology 77:979–988

    Article  PubMed  CAS  Google Scholar 

  • Ramírez AR, Castro MA, Angulo C, Ramió L, Rivera MM, Torres M, Rigau T, Rodríguez-Gil JE, Concha II (2009) The presence and function of dopamine type 2 receptors in boar sperm: a possible role for dopamine in viability, capacitation, and modulation of sperm motility. Biol Reprod 80:753–761

    Article  PubMed  CAS  Google Scholar 

  • Ren D, Navarro B, Perez G, Jackson AC, Hsu S, Shi Q, Tilly JL, Clapham DE (2001) A sperm ion channel required for sperm motility and male fertility. Nature 413:603–609

    Article  PubMed  CAS  Google Scholar 

  • Rivett AJ, Bose S, Brooks P, Broadfoot KI (2001) Regulation of proteasome complexes by gamma-interferon and phosphorylation. Biochimie 83:363–366

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez-Martínez H (2007) Role of the oviduct in sperm capacitation. Theriogenology 68(1):S138–S146

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez-Martínez H, Ekstedt E, Einarsson S (1990) Acidification of the epididymal fluid in the boar. Int J Androl 13:238–243

    Article  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 58:129–145

    Google Scholar 

  • Rodríguez-Martínez H, Saravia F, Wallgren M, Tienthai P, Johannisson A, Vázquez JM, Martínez E, Roca J, Sanz L, Calvete JJ (2005) Boar spermatozoa in the oviduct. Theriogenology 63:514–535

    Article  PubMed  CAS  Google Scholar 

  • Roggero CM, De Blas GA, Dai H, Tomes CN, Rizo J, Mayorga LS (2007) Complexin/synaptotagmin interplay controls acrosomal exocytosis. J Biol Chem 282:26335–26343

    Article  PubMed  CAS  Google Scholar 

  • Rossato M, Ion Popa F, Ferigo M, Clarim G, Foresta C (2005) Human sperm express cannabinoid receptor CB1, the activation of which inhibits motility, acrosome reaction, and mitochondrial function. J Clin Endocrinol Metab 90:984–991

    Article  PubMed  CAS  Google Scholar 

  • Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, Anderson RG (1992) Caveolin, a protein component of caveolae membrane coats. Cell 68:673–682

    Article  PubMed  CAS  Google Scholar 

  • Salaun C, Gould GW, Chamberlain LH (2005) The SNARE proteins SNAP-25 and SNAP-23 display different affinities for lipid rafts in PC12 cells. Regulation by distinct cysteine-rich domains. J Biol Chem 280:1236–1240

    Article  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 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Satake N, Elliott RM, Watson PF, Holt WV (2006) Sperm selection and competition in pigs may be mediated by the differential motility activation and suppression of sperm subpopulations within the oviduct. J Exp Biol 209:1560–1572

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Schuh S, Hille B, Babcock D (2007) Adenosine and catecholamine agonists speed the flagellar beat of mammalian sperm by a non-receptor-mediated mechanism. Biol Reprod 77:960–969

    Article  PubMed  CAS  Google Scholar 

  • Shadan S, James PS, Howes EA, Jones R (2004) Cholesterol efflux alters lipid raft stability and distribution during capacitation of boar spermatozoa. Biol Reprod 71:253–265

    Article  PubMed  CAS  Google Scholar 

  • Shafrir Y, Ben-Avraham D, Forgacs G (2000) Trafficking and signaling through the cytoskeleton: a specific mechanism. J Cell Sci 113:2747–2757

    PubMed  CAS  Google Scholar 

  • Signorelli J, Díaz ES, Morales P (2011) Human sperm capacitation requires the inhibition of the activity of the serine/threonine phosphatase PP2A. In: 44th annual meeting of the socitey for the study of reproduction, Portland, Oregon

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Siva AB, Kameshwari DB, Singh V, Pavani K, Sundaram CS, Rangaraj N, Deenadayal M, Shivaji S (2010) Proteomics-based study on asthenozoospermia: differential expression of proteasome alpha complex. Mol Hum Reprod 16:452–462

    Article  PubMed  CAS  Google Scholar 

  • Smith GD, Wolf DP, Trautman KC, da Cruz e Silva EF, Greengard P, Vijayaraghavan S (1996) Primate sperm contain protein phosphatase 1, a biochemical mediator of motility. Biol Reprod 54:719–727

    Article  PubMed  CAS  Google Scholar 

  • Smith TT, Nothnick WB (1997) Role of direct contact between spermatozoa and oviductal epithelial cells in maintaining rabbit sperm viability. Biol Reprod 56:83–89

    Article  PubMed  CAS  Google Scholar 

  • Spehr M, Schwane K, Riffell JA, Barbour J, Zimmer RK, Neuhaus EM, Hatt H (2004) Particulate adenylate cyclase plays a key role in human sperm olfactory receptor-mediated chemotaxis. J Biol Chem 279:40194–40203

    Article  PubMed  CAS  Google Scholar 

  • Spungin B, Breitbart H (1996) Calcium mobilization and influx during sperm exocytosis. J Cell Sci 109:1947–1955

    PubMed  CAS  Google Scholar 

  • Stoker AW (2005) Protein tyrosine phosphatases and signalling. J Endocrinol 185:19–33

    Article  PubMed  CAS  Google Scholar 

  • Storey BT (2008) Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int J Dev Biol 52:427–437

    Article  PubMed  CAS  Google Scholar 

  • Suarez SS (2007) Sperm interactions with the female tract: inspiration for assisted reproduction. Reprod Fertil Dev 19:104–110

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Suarez SS, Redfern K, Raynor P, Martin F, Phillips DM (1991) Attachment of boar sperm to mucosal explants of oviduct in vitro: possible role in formation of a sperm reservoir. Biol Reprod 44:998–1004

    Article  PubMed  CAS  Google Scholar 

  • Suarez SS, Dai XB, DeMott RP, Redfern K, Mirando MA (1992) Movement characteristics of boar sperm obtained from the oviduct or hyperactivated in vitro. J Androl 13:75–80

    PubMed  CAS  Google Scholar 

  • Sumiyoshi E, Sugimoto A, Yamamoto M (2002) Protein phosphatase 4 is required for centrosome maturation in mitosis and sperm meiosis in C. elegans. J Cell Sci 115:1403–1410

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Sutovsky P, Moreno R, Ramalho-Santos J, Dominko T, Thompson WE, Schatten G (2001) 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, 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Suzuki C, Yoshioka K, Itol S, Kawarasaki T, Kikuchi K (2005) In vitro fertilization and subsequent development of porcine oocytes using cryopreserved and liquid-stored spermatozoa from various boars. Theriogenology 64:1287–1296

    Article  PubMed  Google Scholar 

  • Tanaka K, Chiba T (1998) The proteasome: a protein-destroying machine. Genes Cells 3:499–510

    Article  PubMed  CAS  Google Scholar 

  • Tardif S, Dubé C, Chevalier S, Bailey JL (2001) Capacitation is associated with tyrosine phosphorylation and tyrosine-like activity of pig sperm proteins. Biol Reprod 65:784–792

    Article  PubMed  CAS  Google Scholar 

  • Tardif S, Dubé C, Bailey JL (2003) Porcine sperm capacitation and tyrosine kinase activity are dependent on bicarbonate and calcium but protein tyrosine phosphorylation is only associated with calcium. Biol Reprod 68:207–213

    Article  PubMed  CAS  Google Scholar 

  • Tash JS, Bracho GE (1994) Regulation of sperm motility: emerging evidence for a major role for protein phosphatases. J Androl 15:505–509

    PubMed  CAS  Google Scholar 

  • Tash JS, Krinks M, Patel J, Means RL, Klee CB, Means AR (1988) Identification, characterization, and functional correlation of calmodulin-dependent protein phosphatase in sperm. J Cell Biol 106:1625–1633

    Article  PubMed  CAS  Google Scholar 

  • Tengowski MW, Feng D, Sutovsky M, Sutovsky P (2007) Differential expression of genes encoding constitutive and inducible 20S proteasomal core subunits in the testis and epididymis of theophylline- or 1,3-dinitrobenzene-exposed rats. Biol Reprod 76:149–163

    Article  PubMed  CAS  Google Scholar 

  • Tienthai P, Johannisson A, Rodríguez-Martínez H (2004) Sperm capacitation in the porcine oviduct. Anim Reprod Sci 80:131–146

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Tomes CN, Michaut M, De Blas G, Visconti P, Matti U, Mayorga LS (2002) SNARE complex assembly is required for human sperm acrosome reaction. Dev Biol 243:326–338

    Article  PubMed  CAS  Google Scholar 

  • Tonks NK (2006) Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol 7:833–846

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Töpfer-Petersen E, Wagner A, Friedrich J, Petrunkina AM, Ekhlasi-Hundrieser M, Waberski D, Drommer W (2002) Function of the mammalian oviductal sperm reservoir. J Exp Zool 292:210–215

    Article  PubMed  Google Scholar 

  • Travis AJ, Merdiushev T, Vargas LA, Jones BH, Purdon MA, Nipper RW, Galatioto J, Moss SB, Hunnicutt GR, Kopf GS (2001) Expression and localization of caveolin-1, and the presence of membrane rafts, in mouse and guinea pig spermatozoa. Dev Biol 240:599–610

    Article  PubMed  CAS  Google Scholar 

  • Trockenbacher A, Suckow V, Foerster J, Winter J, Krauss S, Ropers HH, Schneider R, Schweiger S (2001) MID1, mutated in Opitz syndrome, encodes an ubiquitin ligase that targets phosphatase 2A for degradation. Nat Genet 29:287–294

    Article  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

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Tulsiani DR, Zeng HT, Abou-Haila A (2007) Biology of sperm capacitation: evidence for multiple signalling pathways. Soc Reprod Fertil Suppl 63:257–272

    PubMed  CAS  Google Scholar 

  • Urner F, Sakkas D (2003) Protein phosphorylation in mammalian spermatozoa. Reproduction 125:17–26

    Article  PubMed  CAS  Google Scholar 

  • Van Gestel RA, Brewis IA, Ashton PR, Helms JB, Brouwers JF, Gadella BM (2005) Capacitation-dependent concentration of lipid rafts in the apical ridge head area of porcine sperm cells. Mol Hum Reprod 11:583–590

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Varano G, Lombardi A, Cantini G, Forti G, Baldi E, Luconi M (2008) Src activation triggers capacitation and acrosome reaction but not motility in human spermatozoa. Hum Reprod 23:2652–2662

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Vijayaraghavan S, Stephens DT, Trautman K, Smith GD, Khatra B, da Cruz e Silva EF, Greengard P (1996) Sperm motility development in the epididymis is associated with decreased glycogen synthase kinase-3 and protein phosphatase 1 activity. Biol Reprod 54:709–718

    Article  PubMed  CAS  Google Scholar 

  • Visconti PE (2009) Understanding the molecular basis of sperm capacitation through kinase design. Proc Natl Acad Sci USA 106:667–668

    Article  PubMed  CAS  Google Scholar 

  • Visconti PE, Bailey JL, Moore GD, Pan D, Olds-Clarke P, Kopf GS (1995a) Capacitation of mouse spermatozoa (I): correlation between the capacitation state and protein tyrosine phosphorylation. Development 121:1129–1137

    PubMed  CAS  Google Scholar 

  • Visconti PE, Moore GD, Bailey JL, Leclerc P, Connors SA, Pan D, Olds-Clarke P, Kopf GS (1995b) Capacitation of mouse spermatozoa (II): protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development 121:1139–1150

    PubMed  CAS  Google Scholar 

  • Visconti PE, Stewart-Savage J, Blasco A, Battaglia L, Miranda P, Kopf GS, Tezón JG (1999a) Roles of bicarbonate, cAMP, and protein tyrosine phosphorylation on capacitation and the spontaneous acrosome reaction of hamster sperm. Biol Reprod 61:76–84

    Article  PubMed  CAS  Google Scholar 

  • Visconti PE, Galantino-Homer H, Ning X, Moore GD, Valenzuela JP, Jorgez CJ, Alvarez JG, Kopf GS (1999b) Cholesterol efflux-mediated signal transduction in mammalian sperm. Beta-cyclodextrins initiate transmembrane signaling leading to an increase in protein tyrosine phosphorylation and capacitation. J Biol Chem 274:3235–3242

    Article  PubMed  CAS  Google Scholar 

  • Visconti PE, Ning X, Fornés MW, Alvarez JG, Stein P, Connors SA, Kopf GS (1999c) Cholesterol efflux-mediated signal transduction in mammalian sperm: cholesterol release signals an increase in protein tyrosine phosphorylation during mouse sperm capacitation. Dev Biol 214:429–443

    Article  PubMed  CAS  Google Scholar 

  • Visconti PE, Westbrook VA, Chertihin O, Demarco I, Sleight S, Diekman AB (2002) Novel signaling pathways involved in sperm acquisition of fertilizing capacity. J Reprod Immunol 53:133–150

    Article  PubMed  CAS  Google Scholar 

  • Way AL, Killian GL (2002) Capacitation and induction of acrosome reaction in bull spermatozoa with norepinephrine. J Androl 23:352–357

    PubMed  CAS  Google Scholar 

  • Wennemuth G, Carlson AE, Harper AJ, Babcock DF (2003) Bicarbonate actions on flagellar and Ca2+−channel responses: initial events in sperm activation. Development 130:1317–1326

    Article  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

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Yanagimachi R (1970) The movement of golden hamster spermatozoa before and after capacitation. J Reprod Fertil 23:193–196

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Yeste M, Briz M, Pinart E, Sancho S, García-Gil N, Badia E, Bassols J, Pruneda A, Bussalleu E, Casas I, Bonet S (2008) Hyaluronic acid delays boar sperm capacitation after 3 days of storage at 15 °C. Anim Reprod Sci 109:236–250

    Article  PubMed  CAS  Google Scholar 

  • Yeste M, Lloyd RE, Briz M, Badia E, Bonet S, Holt WV (2009) Direct contact between boar spermatozoa and porcine oviductal epithelial cell (OEC) cultures is needed for optimal sperm survival in vitro. Anim Reprod Sci 113:263–278

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Yin DM, Chen YJ, Sathyamurthy A, Xiong WC, Mei L (2012) Synaptic dysfunction in schizophrenia. Adv Exp Med Biol 970:493–516

    Article  PubMed  CAS  Google Scholar 

  • Zhang F, Paterson AJ, Huang P, Wang K, Kudlow JE (2007a) Metabolic control of proteasome function. Physiology (Bethesda) 22:373–379

    Article  CAS  Google Scholar 

  • Zhang F, Hu Y, Huang P, Toleman CA, Paterson AJ, Kudlow JE (2007b) Proteasome function is regulated by cyclic AMP-dependent protein kinase through phosphorylation of Rpt6. J Biol Chem 282:22460–22471

    Article  PubMed  CAS  Google Scholar 

  • Zhang SQ, Yang W, Kontaridis MI, Bivona TG, Wen G, Araki T, Luo J, Thompson JA, Schraven BL, Philips MR, Neel BG (2004) Shp2 regulates SRC family kinase activity and Ras/Erk activation by controlling Csk recruitment. Mol Cell 13:341–355

    Article  PubMed  Google Scholar 

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

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Zong C, Gomes AV, Drews O, Li X, Young GW, Berhane B, Qiao X, French SW, Bardag-Gorce F, Ping P (2006) Regulation of murine cardiac 20S proteasomes: role of associating partners. Circ Res 99:372–380

    Article  PubMed  CAS  Google Scholar 

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  1. Unit of Animal Reproduction, Department of Animal Medicine and Surgery, Faculty of Veterinary Medicine, Autonomous University of Barcelona, 08193, Bellaterra (Cerdanyola del Vallès, Barcelona), Spain

    Marc Yeste

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  1. , Faculty of Sciences, University of Girona, Campus Montilivi s/n, Girona, 17071, Spain

    Sergi Bonet

  2. University of Girona, Institute of Food and Agricultural Techn, Campus Montilivi, Girona, 17071, Spain

    Isabel Casas

  3. , Department of Human Metabolism, The University of Sheffield, Sheffield, NW1 4RY, United Kingdom

    William V. Holt

  4. , Department of Animal Medicine and Surger, Autonomous University of Barcelona, Cerdanyola del Vallès, Bellaterra, 08193, Spain

    Marc Yeste

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Yeste, M. (2013). Boar Spermatozoa Within the Oviductal Environment (II): Sperm Capacitation. 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_7

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