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Porcine model for the study of sperm capacitation, fertilization and male fertility

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Abstract

Mammalian fertilization remains a poorly understood event with the vast majority of studies done in the mouse model. The purpose of this review is to revise the current knowledge about semen deposition, sperm transport, sperm capacitation, gamete interactions and early embryonic development with a focus on the porcine model as a relevant, alternative model organism to humans. The review provides a thorough overview of post-ejaculation events inside the sow’s reproductive tract including comparisons with humans and implications for human fertilization and assisted reproductive therapy (ART). Porcine methodology for sperm handling, preservation, in vitro capacitation, oocyte in vitro maturation, in vitro fertilization and intra-cytoplasmic sperm injection that are routinely used in pig research laboratories can be successfully translated into ART to treat human infertility. Last, but not least, new knowledge about mitochondrial inheritance in the pig can provide an insight into human mitochondrial diseases and new knowledge on polyspermy defense mechanisms could contribute to the development of new male contraceptives.

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References

  • Adenot PG, Szollosi MS, Geze M, Renard JP, Debey P (1991) Dynamics of paternal chromatin changes in live one-cell mouse embryo after natural fertilization. Mol Reprod Dev 28(1):23–34

    CAS  PubMed  Google Scholar 

  • Aitken RJ, Nixon B (2013) Sperm capacitation: a distant landscape glimpsed but unexplored. Mol Hum Reprod 19(12):785–793

    CAS  PubMed  Google Scholar 

  • Alvarez-Rodriguez M, Atikuzzaman M, Venhoranta H, Wright D, Rodriguez-Martinez H (2019) Expression of immune regulatory genes in the porcine internal genital tract is differentially triggered by spermatozoa and seminal plasma. Int J Mol Sci 20(3):513

  • Archibald AL, Bolund L, Churcher C, Fredholm M, Groenen MA, Harlizius B, Lee KT, Milan D, Rogers J, Rothschild MF, Uenishi H, Wang J, Schook LB, Swine Genome Sequencing C (2010) Pig genome sequence--analysis and publication strategy. BMC Genomics 11:438

    PubMed  PubMed Central  Google Scholar 

  • Ash K, Berger T, Horner CM, Calvert CC (1995) Identification of porcine sperm plasma membrane proteins that may play a role in sperm-egg fusion. Zygote 3(2):163–170

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  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(5):750–758

    CAS  PubMed  Google Scholar 

  • Aydin H, Sultana A, Li S, Thavalingam A, Lee JE (2016) Molecular architecture of the human sperm IZUMO1 and egg JUNO fertilization complex. Nature 534(7608):562–565

    CAS  PubMed  PubMed Central  Google Scholar 

  • Azad N, Nazarian H, Nazari L, Ghaffari Novin M, Piryaei A, Heidari MH, Masteri Farahani R, Sadjadpour SS (2018) Evaluation of PAWP and PLC? Expression in infertile men with previous ICSI fertilization failure. Urol J 15(3):116–121

    PubMed  Google Scholar 

  • Bailey JL (2010) Factors regulating sperm capacitation. Syst Biol Reprod Med 56(5):334–348

    CAS  PubMed  Google Scholar 

  • Balhorn R (2007) The protamine family of sperm nuclear proteins. Genome Biol 8(9):227

    PubMed  PubMed Central  Google Scholar 

  • Berger T, Nitta BJ, Ducolomb Y, Betancourt M (2011) Interaction of potential porcine sperm ligands with the oocyte plasma membrane. Reprod Domest Anim 46(1):15–20

    CAS  PubMed  Google Scholar 

  • Bi M, Hickox JR, Winfrey VP, Olson GE, Hardy DM (2003) Processing, localization and binding activity of zonadhesin suggest a function in sperm adhesion to the zona pellucida during exocytosis of the acrosome. Biochem J 375(Pt 2):477–488

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bianchi E, Doe B, Goulding D, Wright GJ (2014) Juno is the egg Izumo receptor and is essential for mammalian fertilization. Nature 508(7497):483–487

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bieniek JM, Drabovich AP, Lo KC (2016) Seminal biomarkers for the evaluation of male infertility. Asian J Androl 18(3):426–433

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bigler D, Chen M, Waters S, White JM (1997) A model for sperm-egg binding and fusion based on ADAMs and integrins. Trends Cell Biol 7(6):220–225

    CAS  PubMed  Google Scholar 

  • Bjorndahl L, Kvist U (2003) Sequence of ejaculation affects the spermatozoon as a carrier and its message. Reprod BioMed Online 7(4):440–448

    PubMed  Google Scholar 

  • Bjorndahl L, Kvist U (2010) Human sperm chromatin stabilization: a proposed model including zinc bridges. Mol Hum Reprod 16(1):23–29

    PubMed  Google Scholar 

  • Bleil JD, Wassarman PM (1980) Structure and function of the zona pellucida: identification and characterization of the proteins of the mouse oocyte’s zona pellucida. Dev Biol 76(1):185–202

    CAS  PubMed  Google Scholar 

  • Blobel CP (1999) Roles of metalloprotease-disintegrins in cell-cell interactions, in neurogenesis, and in the cleavage of TNFα. Adv Dev Biochem 5:165–198

    CAS  Google Scholar 

  • Boe-Hansen GB, Christensen P, Vibjerg D, Nielsen MB, Hedeboe AM (2008) Sperm chromatin structure integrity in liquid stored boar semen and its relationships with field fertility. Theriogenology 69(6):728–736

    CAS  PubMed  Google Scholar 

  • Boerke A, Tsai PS, Garcia-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(8):1188–1196

    CAS  PubMed  Google Scholar 

  • Borsuk E, Manka R (1988) Behavior of sperm nuclei in intact and bisected metaphase II mouse oocytes fertilized in the presence of colcemid. Gamete Res 20(3):365–376

    CAS  PubMed  Google Scholar 

  • Buffone MG, Wertheimer EV, Visconti PE, Krapf D (2014) Central role of soluble adenylyl cyclase and cAMP in sperm physiology. Biochim Biophys Acta 1842(12 Pt B):2610–2620

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burkart AD, Xiong B, Baibakov B, Jimenez-Movilla M, Dean J (2012) Ovastacin, a cortical granule protease, cleaves ZP2 in the zona pellucida to prevent polyspermy. J Cell Biol 197(1):37–44

    CAS  PubMed  PubMed Central  Google Scholar 

  • Calvete JJ, Mann K, Schafer W, Raida M, Sanz L, Topfer-Petersen E (1995) Boar spermadhesin PSP-II: location of posttranslational modifications, heterodimer formation with PSP-I glycoforms and effect of dimerization on the ligand-binding capabilities of the subunits. FEBS Lett 365(2–3):179–182

    CAS  PubMed  Google Scholar 

  • Calvete JJ, Raida M, Gentzel M, Urbanke C, Sanz L, Topfer-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(2):201–206

    CAS  PubMed  Google Scholar 

  • Carmona E, Weerachatyanukul W, Soboloff T, Fluharty AL, White D, Promdee L, Ekker M, Berger T, Buhr M, Tanphaichitr N (2002) Arylsulfatase a is present on the pig sperm surface and is involved in sperm-zona pellucida binding. Dev Biol 247(1):182–196

    CAS  PubMed  Google Scholar 

  • Carrasco LC, Romar R, Aviles M, Gadea J, Coy P (2008) Determination of glycosidase activity in porcine oviductal fluid at the different phases of the estrous cycle. Reproduction 136(6):833–842

    CAS  PubMed  Google Scholar 

  • Centurion F, Vazquez JM, Calvete JJ, Roca J, Sanz L, Parrilla I, Garcia EM, Martinez EA (2003) Influence of porcine spermadhesins on the susceptibility of boar spermatozoa to high dilution. Biol Reprod 69(2):640–646

    CAS  PubMed  Google Scholar 

  • Chalbi M, Barraud-Lange V, Ravaux B, Howan K, Rodriguez N, Soule P, Ndzoudi A, Boucheix C, Rubinstein E, Wolf JP, Ziyyat A, Perez E, Pincet F, Gourier C (2014) Binding of sperm protein Izumo1 and its egg receptor Juno drives Cd9 accumulation in the intercellular contact area prior to fusion during mammalian fertilization. Development 141(19):3732–3739

    CAS  PubMed  Google Scholar 

  • Chang MC (1951) Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature 168(4277):697–698

    CAS  PubMed  Google Scholar 

  • Chang H, Suarez SS (2011) Two distinct Ca(2+) signaling pathways modulate sperm flagellar beating patterns in mice. Biol Reprod 85(2):296–305

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cohen DJ, Ellerman DA, Cuasnicu PS (2000) Mammalian sperm-egg fusion: evidence that epididymal protein DE plays a role in mouse gamete fusion. Biol Reprod 63(2):462–468

    CAS  PubMed  Google Scholar 

  • Cohen DJ, Ellerman DA, Busso D, Morgenfeld MM, Piazza AD, Hayashi M, Young ET, Kasahara M, Cuasnicu PS (2001) Evidence that human epididymal protein ARP plays a role in gamete fusion through complementary sites on the surface of the human egg. Biol Reprod 65(4):1000–1005

    CAS  PubMed  Google Scholar 

  • Coonrod SA, Herr JC, Westhusin ME (1996) Inhibition of bovine fertilization in vitro by antibodies to SP-10. J Reprod Fertil 107(2):287–297

    CAS  PubMed  Google Scholar 

  • Cornwall GA, Tulsiani DR, Orgebin-Crist MC (1991) Inhibition of the mouse sperm surface alpha-D-mannosidase inhibits sperm-egg binding in vitro. Biol Reprod 44(5):913–921

    CAS  PubMed  Google Scholar 

  • Cross NL (1998) Role of cholesterol in sperm capacitation. Biol Reprod 59(1):7–11

    CAS  PubMed  Google Scholar 

  • Davidova N, Jonakova V, Manaskova-Postlerova P (2009) Expression and localization of acrosin inhibitor in boar reproductive tract. Cell Tissue Res 338(2):303–311

    CAS  PubMed  Google Scholar 

  • Davis BK (1981) Timing of fertilization in mammals: sperm cholesterol/phospholipid ratio as a determinant of the capacitation interval. Proc Natl Acad Sci U S A 78(12):7560–7564

    CAS  PubMed  PubMed Central  Google Scholar 

  • Day BN (2000) Reproductive biotechnologies: current status in porcine reproduction. Anim Reprod Sci 60–61:161–172

    PubMed  Google Scholar 

  • Day AE, Quilter CR, Sargent CA, Mileham AJ (2003) Chromosomal mapping, sequence and transcription analysis of the porcine fertilin beta gene (ADAM2). Anim Genet 34(5):375–378

    CAS  PubMed  Google Scholar 

  • De Lazari FL, Sontag ER, Schneider A, Moura AAA, Vasconcelos FR, Nagano CS, Mattos RC, Jobim MIM, Bustamante-Filho IC (2019) Seminal plasma proteins and their relationship with sperm motility and morphology in boars. Andrologia 51(4):e13222

    PubMed  Google Scholar 

  • Didion BA, Kasperson KM, Wixon RL, Evenson DP (2009) Boar fertility and sperm chromatin structure status: a retrospective report. J Androl 30(6):655–660

    PubMed  Google Scholar 

  • Dostalova Z, Calvete JJ, Sanz L, Topfer-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(1):48–54

    CAS  PubMed  Google Scholar 

  • Dostalova Z, Calvete JJ, Topfer-Petersen E (1995) 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(4):237–242

    CAS  PubMed  Google Scholar 

  • Drabovich AP, Saraon P, Jarvi K, Diamandis EP (2014) Seminal plasma as a diagnostic fluid for male reproductive system disorders. Nat Rev Urol 11(5):278–288

    CAS  PubMed  Google Scholar 

  • Druart X, Rickard JP, Mactier S, Kohnke PL, Kershaw-Young CM, Bathgate R, Gibb Z, Crossett B, Tsikis G, Labas V, Harichaux G, Grupen CG, de Graaf SP (2013) Proteomic characterization and cross species comparison of mammalian seminal plasma. J Proteome 91:13–22

    CAS  Google Scholar 

  • Dube C, Leclerc P, Baba T, Reyes-Moreno C, Bailey JL (2005) The proacrosin binding protein, sp32, is tyrosine phosphorylated during capacitation of pig sperm. J Androl 26(4):519–528

    CAS  PubMed  Google Scholar 

  • Duncan FE, Que EL, Zhang N, Feinberg EC, O'Halloran TV, Woodruff TK (2016) The zinc spark is an inorganic signature of human egg activation. Sci Rep 6:24737

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ekhlasi-Hundrieser M, Gohr K, Wagner A, Tsolova M, Petrunkina A, Topfer-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(3):536–545

    CAS  PubMed  Google Scholar 

  • Ellerman DA, Da Ros VG, Cohen DJ, Busso D, Morgenfeld MM, Cuasnicu PS (2002) Expression and structure-function analysis of de, a sperm cysteine-rich secretory protein that mediates gamete fusion. Biol Reprod 67(4):1225–1231

    CAS  PubMed  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(2):191–203

    CAS  PubMed  Google Scholar 

  • Ensslin M, Calvete JJ, Thole HH, Sierralta WD, Adermann K, Sanz L, Topfer-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(12):733–738

    CAS  PubMed  Google Scholar 

  • Ensslin M, Vogel T, Calvete JJ, Thole HH, Schmidtke J, Matsuda T, Topfer-Petersen E (1998) Molecular cloning and characterization of P47, a novel boar sperm-associated zona pellucida-binding protein homologous to a family of mammalian secretory proteins. Biol Reprod 58(4):1057–1064

    CAS  PubMed  Google Scholar 

  • Evans JP (2012) Sperm-egg interaction. Annu Rev Physiol 74:477–502

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  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(4):879–886

    CAS  PubMed  Google Scholar 

  • Fazeli A, Elliott RM, Duncan AE, Moore A, Watson PF, Holt WV (2003) In vitro maintenance of boar sperm viability by a soluble fraction obtained from oviductal apical plasma membrane preparations. Reproduction 125(4):509–517

    CAS  PubMed  Google Scholar 

  • Ferrer M, Rodriguez H, Zara L, Yu Y, Xu W, Oko R (2012) MMP2 and acrosin are major proteinases associated with the inner acrosomal membrane and may cooperate in sperm penetration of the zona pellucida during fertilization. Cell Tissue Res 349(3):881–895

    CAS  PubMed  PubMed Central  Google Scholar 

  • Flesch FM, Gadella BM (2000) Dynamics of the mammalian sperm plasma membrane in the process of fertilization. Biochim Biophys Acta 1469(3):197–235

    CAS  PubMed  Google Scholar 

  • Flesch FM, Colenbrander B, van Golde LM, Gadella BM (1999) Capacitation induces tyrosine phosphorylation of proteins in the boar sperm plasma membrane. Biochem Biophys Res Commun 262(3):787–792

    CAS  PubMed  Google Scholar 

  • Florman HM, Ducibella T (2006) Fertilization in mammals. In: Neill JD (ed) Knobil and Neill’s physiology of reproduction, vol. 1. Elsevier Academic Press, Inc., New York, pp 55–112

    Google Scholar 

  • Florman HM, Fissore RA (2015) Fertilization in mammals. In: Plant TM, Zeleznik AJ (eds) Knobil and Neill’s physiology of reproduction, vol. 1. Academic Press, New York, pp 149–196

    Google Scholar 

  • Fraser LR (1984) Mouse sperm capacitation in vitro involves loss of a surface-associated inhibitory component. J Reprod Fertil 72(2):373–384

    CAS  PubMed  Google Scholar 

  • Fraser LR (2008) The role of small molecules in sperm capacitation. Theriogenology 70(8):1356–1359

    CAS  PubMed  Google Scholar 

  • Fraser LR, Harrison RA, Herod JE (1990) Characterization of a decapacitation factor associated with epididymal mouse spermatozoa. J Reprod Fertil 89(1):135–148

    CAS  PubMed  Google Scholar 

  • Frayne J, Hall L (1999) Mammalian sperm-egg recognition: does fertilin beta have a major role to play? Bioessays 21(3):183–187

    CAS  PubMed  Google Scholar 

  • Gadella BM, Boerke A (2016) An update on post-ejaculatory remodeling of the sperm surface before mammalian fertilization. Theriogenology 85(1):113–124

    CAS  PubMed  Google Scholar 

  • Gadella BM, Harrison RA (2000) The capacitating agent bicarbonate induces protein kinase A-dependent changes in phospholipid transbilayer behavior in the sperm plasma membrane. Development 127(11):2407–2420

    CAS  PubMed  Google Scholar 

  • Gadella BM, Harrison RA (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(1):340–350

    CAS  PubMed  Google Scholar 

  • Gadella BM, Tsai PS, Boerke A, Brewis IA (2008) Sperm head membrane reorganisation during capacitation. Int J Dev Biol 52(5–6):473–480

    CAS  PubMed  Google Scholar 

  • Gangwar DK, Atreja SK (2015) Signalling events and associated pathways related to the mammalian sperm capacitation. Reprod Domest Anim 50(5):705–711

    CAS  PubMed  Google Scholar 

  • Geisert RD, Sutovsky P, Lucy M, Bartol FF, Meyer AE (2019) Reproductive physiology of swine. In: Bazer FW, Lamb GC, Wu G (eds) Animal agriculture 1st edition: challenges, innovations, and sustainability. Academic Press, Cambridge, pp 263–282

  • Gervasi MG, Visconti PE (2016) Chang’s meaning of capacitation: a molecular perspective. Mol Reprod Dev 83(10):860–874

    CAS  PubMed  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(8):583–590

    PubMed  Google Scholar 

  • van Gestel RA, Brewis IA, Ashton PR, Brouwers JF, Gadella BM (2007) Multiple proteins present in purified porcine sperm apical plasma membranes interact with the zona pellucida of the oocyte. Mol Hum Reprod 13(7):445–454

    PubMed  Google Scholar 

  • Ghersevich S, Massa E, Zumoffen C (2015) Oviductal secretion and gamete interaction. Reproduction 149(1):R1–r14

    PubMed  Google Scholar 

  • Gilany K, Minai-Tehrani A, Savadi-Shiraz E, Rezadoost H, Lakpour N (2015) Exploring the human seminal plasma proteome: an unexplored gold mine of biomarker for male infertility and male reproduction disorder. J Reprod Infertil 16(2):61–71

    PubMed  PubMed Central  Google Scholar 

  • Glotzer M, Murray AW, Kirschner MW (1991) Cyclin is degraded by the ubiquitin pathway. Nature 349(6305):132–138

    CAS  PubMed  Google Scholar 

  • Gonzalez-Cadavid V, Martins JA, Moreno FB, Andrade TS, Santos AC, Monteiro-Moreira AC, Moreira RA, Moura AA (2014) Seminal plasma proteins of adult boars and correlations with sperm parameters. Theriogenology 82(5):697–707

    CAS  PubMed  Google Scholar 

  • Green CE, Bredl J, Holt WV, Watson PF, Fazeli A (2001) Carbohydrate mediation of boar sperm binding to oviductal epithelial cells in vitro. Reproduction 122(2):305–315

    CAS  PubMed  Google Scholar 

  • Gualtieri R, Talevi R (2000) In vitro-cultured bovine oviductal cells bind acrosome-intact sperm and retain this ability upon sperm release. Biol Reprod 62(6):1754–1762

    CAS  PubMed  Google Scholar 

  • Hachem A, Godwin J, Ruas M, Lee HC, Ferrer Buitrago M, Ardestani G, Bassett A, Fox S, Navarrete F, de Sutter P, Heindryckx B, Fissore R, Parrington J (2017) PLCzeta is the physiological trigger of the Ca(2+) oscillations that induce embryogenesis in mammals but conception can occur in its absence. Development 144(16):2914–2924

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hamilton LE, Suzuki J, Acteau G, Shi M, Xu W, Meinsohn MC, Sutovsky P, Oko R (2018) WBP2 shares a common location in mouse spermatozoa with WBP2NL/PAWP and like its descendent is a candidate mouse oocyte-activating factor. Biol Reprod 99(6):1171–1183

    PubMed  PubMed Central  Google Scholar 

  • Hamilton LE, Suzuki J, Aguila L, Meinsohn MC, Smith OE, Protopapas N, Xu W, Sutovsky P, Oko R (2019) Sperm-borne glutathione-s-transferase omega 2 accelerates the nuclear decondensation of spermatozoa during fertilization in mice. Biol Reprod 101(2):368–376

  • Hao Y, Mathialagan N, Walters E, Mao J, Lai L, Becker D, Li W, Critser J, Prather RS (2006) Osteopontin reduces polyspermy during in vitro fertilization of porcine oocytes. Biol Reprod 75(5):726–733

    CAS  PubMed  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(6):831–842

    CAS  PubMed  Google Scholar 

  • Harayama H (2013) Roles of intracellular cyclic AMP signal transduction in the capacitation and subsequent hyperactivation of mouse and boar spermatozoa. J Reprod Dev 59(5):421–430

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harayama H (2018) Flagellar hyperactivation of bull and boar spermatozoa. Reprod Med Biol 17(4):442–448

    CAS  PubMed  PubMed Central  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(9):1396–1407

    CAS  PubMed  Google Scholar 

  • Harayama H, Muroga M, Miyake M (2004) A cyclic adenosine 3′,5′-monophosphate-induced tyrosine phosphorylation of Syk protein tyrosine kinase in the flagella of boar spermatozoa. Mol Reprod Dev 69(4):436–447

    CAS  PubMed  Google Scholar 

  • Harayama H, Noda T, Ishikawa S, Shidara O (2012) Relationship between cyclic AMP-dependent protein tyrosine phosphorylation and extracellular calcium during hyperactivation of boar spermatozoa. Mol Reprod Dev 79(10):727–739

    CAS  PubMed  Google Scholar 

  • Hardy DM, Garbers DL (1995) A sperm membrane protein that binds in a species-specific manner to the egg extracellular matrix is homologous to von Willebrand factor. J Biol Chem 270(44):26025–26028

    CAS  PubMed  Google Scholar 

  • Harris JD, Hibler DW, Fontenot GK, Hsu KT, Yurewicz EC, Sacco AG (1994) Cloning and characterization of zona pellucida genes and cDNAs from a variety of mammalian species: the ZPA, ZPB and ZPC gene families. DNA Seq 4(6):361–393

    CAS  PubMed  Google Scholar 

  • Hayasaka S, Terada Y, Inoue N, Okabe M, Yaegashi N, Okamura K (2007) Positive expression of the immunoglobulin superfamily protein IZUMO on human sperm of severely infertile male patients. Fertil Steril 88(1):214–216

    PubMed  Google Scholar 

  • Hedrick JL, Wardrip NJ (1986) Isolation of the zona pellucida and purification of its glycoprotein families from pig oocytes. Anal Biochem 157(1):63–70

    CAS  PubMed  Google Scholar 

  • Hedrick JL, Wardrip NJ (1987) On the macromolecular composition of the zona pellucida from porcine oocytes. Dev Biol 121(2):478–488

    CAS  PubMed  Google Scholar 

  • Hemler ME (1998) Integrin associated proteins. Curr Opin Cell Biol 10(5):578–585

    CAS  PubMed  Google Scholar 

  • Herr JC, Wright RM, John E, Foster J, Kays T, Flickinger CJ (1990) Identification of human acrosomal antigen SP-10 in primates and pigs. Biol Reprod 42(2):377–382

    CAS  PubMed  Google Scholar 

  • Hickox JR, Bi M, Hardy DM (2001) Heterogeneous processing and zona pellucida binding activity of pig zonadhesin. J Biol Chem 276(44):41502–41509

    CAS  PubMed  Google Scholar 

  • Hino T, Muro Y, Tamura-Nakano M, Okabe M, Tateno H, Yanagimachi R (2016) The behavior and acrosomal status of mouse spermatozoa in vitro, and within the oviduct during fertilization after natural mating. Biol Reprod 95(3):50

    PubMed  Google Scholar 

  • Huang TT Jr, Yanagimachi R (1985) Inner acrosomal membrane of mammalian spermatozoa: its properties and possible functions in fertilization. Am J Anat 174(3):249–268

    PubMed  Google Scholar 

  • Hughes DC, Barratt CL (1999) Identification of the true human orthologue of the mouse Zp1 gene: evidence for greater complexity in the mammalian zona pellucida? Biochim Biophys Acta 1447(2–3):303–306

    CAS  PubMed  Google Scholar 

  • Hunter RH (1996) Ovarian control of very low sperm/egg ratios at the commencement of mammalian fertilisation to avoid polyspermy. Mol Reprod Dev 44(3):417–422

    CAS  PubMed  Google Scholar 

  • Hunter RH, Rodriguez-Martinez H (2004) Capacitation of mammalian spermatozoa in vivo, with a specific focus on events in the Fallopian tubes. Mol Reprod Dev 67(2):243–250

    CAS  PubMed  Google Scholar 

  • Huovila AP, Almeida EA, White JM (1996) ADAMs and cell fusion. Curr Opin Cell Biol 8(5):692–699

    CAS  PubMed  Google Scholar 

  • Hurtado de Llera A, Martin-Hidalgo D, Gil MC, Garcia-Marin LJ, Bragado MJ (2014) The calcium/CaMKKalpha/beta and the cAMP/PKA pathways are essential upstream regulators of AMPK activity in boar spermatozoa. Biol Reprod 90(2):29

    PubMed  Google Scholar 

  • Hurtado de Llera A, Martin-Hidalgo D, Gil MC, Garcia-Marin LJ, Bragado MJ (2016) New insights into transduction pathways that regulate boar sperm function. Theriogenology 85(1):12–20

    CAS  PubMed  Google Scholar 

  • Ickowicz D, Finkelstein M, Breitbart H (2012) Mechanism of sperm capacitation and the acrosome reaction: role of protein kinases. Asian J Androl 14(6):816–821

    CAS  PubMed  PubMed Central  Google Scholar 

  • Inoue N, Ikawa M, Isotani A, Okabe M (2005) The immunoglobulin superfamily protein Izumo is required for sperm to fuse with eggs. Nature 434(7030):234–238

    CAS  PubMed  Google Scholar 

  • Inoue N, Satouh Y, Ikawa M, Okabe M, Yanagimachi R (2011) Acrosome-reacted mouse spermatozoa recovered from the perivitelline space can fertilize other eggs. Proc Natl Acad Sci U S A 108(50):20008–20011

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jaffe LA, Gould M (1985) Polyspermy-preventing mechanisms. In: Metz CB, Monroy A (eds) Biology of Fertilization. Academic Press, New York, pp 223–250

    Google Scholar 

  • Jankovicova J, Secova P, Manaskova-Postlerova P, Simonik O, Frolikova M, Chmelikova E, Horovska L, Michalkova K, Dvorakova-Hortova K, Antalikova J (2019) Detection of CD9 and CD81 tetraspanins in bovine and porcine oocytes and embryos. Int J Biol Macromol 123:931–938

    CAS  PubMed  Google Scholar 

  • Jansen RP (1980) Cyclic changes in the human fallopian tube isthmus and their functional importance. Am J Obstet Gynecol 136(3):292–308

    CAS  PubMed  Google Scholar 

  • Jelinkova P, Manaskova P, Ticha M, Jonakova V (2003) Proteinase inhibitors in aggregated forms of boar seminal plasma proteins. Int J Biol Macromol 32(3–5):99–107

    CAS  PubMed  Google Scholar 

  • Jelinkova P, Liberda J, Manaskova P, Ryslava H, Jonakova V, Ticha M (2004) Mannan-binding proteins from boar seminal plasma. J Reprod Immunol 62(1–2):167–182

    CAS  PubMed  Google Scholar 

  • Jin YZ, Dacheux F, Dacheux JL, Bannai S, Sugita Y, Okamura N (1999) Purification and properties of major alpha-D-mannosidase in the luminal fluid of porcine epididymis. Biochim Biophys Acta 1432(2):382–392

    CAS  PubMed  Google Scholar 

  • Jin M, Fujiwara E, Kakiuchi Y, Okabe M, Satouh Y, Baba SA, Chiba K, Hirohashi N (2011) Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization. Proc Natl Acad Sci U S A 108(12):4892–4896

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jodar M, Soler-Ventura A, Oliva R (2017) Semen proteomics and male infertility. J Proteome 162:125–134

    CAS  Google Scholar 

  • Johansson M, Tienthai P, Rodriguez-Martinez H (2000) Histochemistry and ultrastructure of the intraluminal mucus in the sperm reservoir of the pig oviduct. J Reprod Dev 46(3):10

    Google Scholar 

  • Jonakova V, Ticha M (2004) Boar seminal plasma proteins and their binding properties. Collect Czechoslov Chem Commun 69:461–475

    CAS  Google Scholar 

  • Jonakova V, Sanz L, Calvete JJ, Henschen A, Cechova D, Topfer-Petersen E (1991) Isolation and biochemical characterization of a zona pellucida-binding glycoprotein of boar spermatozoa. FEBS Lett 280(1):183–186

    CAS  PubMed  Google Scholar 

  • Jonakova V, Calvete JJ, Mann K, Schafer W, Schmid ER, Topfer-Petersen E (1992) The complete primary structure of three isoforms of a boar sperm-associated acrosin inhibitor. FEBS Lett 297(1–2):147–150

    CAS  PubMed  Google Scholar 

  • Jonakova V, Kraus M, Veselsky L, Cechova D, Bezouska K, Ticha M (1998) Spermadhesins of the AQN and AWN families, DQH sperm surface protein and HNK protein in the heparin-binding fraction of boar seminal plasma. J Reprod Fertil 114(1):25–34

    CAS  PubMed  Google Scholar 

  • Jonakova V, Manaskova P, Kraus M, Liberda J, Ticha M (2000) Sperm surface proteins in mammalian fertilization. Mol Reprod Dev 56(2 Suppl):275–277

    CAS  PubMed  Google Scholar 

  • Jonakova V, Manaskova P, Ticha M (2007) Separation, characterization and identification of boar seminal plasma proteins. J Chromatogr B Anal Technol Biomed Life Sci 849(1–2):307–314

    CAS  Google Scholar 

  • Jonakova V, Jonak J, Ticha M (2010) Proteomics of male seminal plasma. In: Jiang Z, Ott TL (eds) Reproductive genomics in domestic animals. Blackwell Publishing, Oxford, UK, pp 339–368

    Google Scholar 

  • Kadirvel G, Machado SA, Korneli C, Collins E, Miller P, Bess KN, Aoki K, Tiemeyer M, Bovin N, Miller DJ (2012) Porcine sperm bind to specific 6-sialylated biantennary glycans to form the oviduct reservoir. Biol Reprod 87(6):147

    PubMed  PubMed Central  Google Scholar 

  • Katayama M, Sutovsky P, Yang BS, Cantley T, Rieke A, Farwell R, Oko R, Day BN (2005) Increased disruption of sperm plasma membrane at sperm immobilization promotes dissociation of perinuclear theca from sperm chromatin after intracytoplasmic sperm injection in pigs. Reproduction 130(6):907–916

    CAS  PubMed  Google Scholar 

  • Katayama M, Rieke A, Cantley T, Murphy C, Dowell L, Sutovsky P, Day BN (2007) Improved fertilization and embryo development resulting in birth of live piglets after intracytoplasmic sperm injection and in vitro culture in a cysteine-supplemented medium. Theriogenology 67(4):835–847

    CAS  PubMed  Google Scholar 

  • Katoh Y, Takebayashi K, Kikuchi A, Iki A, Kikuchi K, Tamba M, Kawashima A, Matsuda M, Okamura N (2014) Porcine sperm capacitation involves tyrosine phosphorylation and activation of aldose reductase. Reproduction 148(4):389–401

    CAS  PubMed  Google Scholar 

  • Kelly RW, Critchley HO (1997) Immunomodulation by human seminal plasma: a benefit for spermatozoon and pathogen? Hum Reprod 12(10):2200–2207

    CAS  PubMed  Google Scholar 

  • Kerns K, Morales P, Sutovsky P (2016) Regulation of sperm capacitation by the 26S proteasome: an emerging new paradigm in spermatology. Biol Reprod 94(5):117

    PubMed  Google Scholar 

  • Kerns K, Zigo M, Drobnis EZ, Sutovsky M, Sutovsky P (2018a) Zinc ion flux during mammalian sperm capacitation. Nat Commun 9(1):2061

    PubMed  PubMed Central  Google Scholar 

  • Kerns K, Zigo M, Sutovsky P (2018b) Zinc: a necessary ion for mammalian sperm fertilization competency. Int J Mol Sci 19(12)

  • Kervancioglu ME, Djahanbakhch O, Aitken RJ (1994) Epithelial cell coculture and the induction of sperm capacitation. Fertil Steril 61(6):1103–1108

    CAS  PubMed  Google Scholar 

  • Kim E, Yamashita M, Nakanishi T, Park KE, Kimura M, Kashiwabara S, Baba T (2006) Mouse sperm lacking ADAM1b/ADAM2 fertilin can fuse with the egg plasma membrane and effect fertilization. J Biol Chem 281(9):5634–5639

    CAS  PubMed  Google Scholar 

  • Kim E, Park KE, Kim JS, Baek DC, Lee JW, Lee SR, Kim MS, Kim SH, Kim CS, Koo DB, Kang HS, Ryoo ZY, Chang KT (2009) Importance of the porcine ADAM3 disintegrin domain in sperm-egg interaction. J Reprod Dev 55(2):156–162

    CAS  PubMed  Google Scholar 

  • Kim E, Kim JS, Lee Y, Song BS, Sim BW, Kim SU, Saitoh T, Yazawa H, Nunoya T, Chang KT (2013) Molecular cloning, characterization of porcine IZUMO1, an IgSF family member. Reprod Domest Anim 48(1):90–97

    CAS  PubMed  Google Scholar 

  • Knox RV (2015) Recent advancements in the hormonal stimulation of ovulation in swine. Vet Med (Auckl) 6:309–320

    Google Scholar 

  • Kongmanas K, Kruevaisayawan H, Saewu A, Sugeng C, Fernandes J, Souda P, Angel JB, Faull KF, Aitken RJ, Whitelegge J, Hardy D, Berger T, Baker MA, Tanphaichitr N (2015) Proteomic characterization of pig sperm anterior head plasma membrane reveals roles of acrosomal proteins in ZP3 binding. J Cell Physiol 230(2):449–463

    CAS  PubMed  Google Scholar 

  • Kopecny V, Pavlok A (1975) Incorporation of Arginine-3H into chromatin of mouse eggs shortly after sperm penetration. Histochemistry 45(4):341–345

    CAS  PubMed  Google Scholar 

  • Kudo K, Yonezawa 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 Biochem 252(3):492–499

    CAS  PubMed  Google Scholar 

  • Kuno M, Yonezawa N, Amari S, Hayashi M, Ono Y, Kiss L, Sonohara K, Nakano M (2000) The presence of a glycosyl phosphatidylinositol-anchored alpha-mannosidase in boar sperm. IUBMB Life 49(6):485–489

    CAS  PubMed  Google Scholar 

  • La Spina FA, Puga Molina LC, Romarowski A, Vitale AM, Falzone TL, Krapf D, Hirohashi N, Buffone MG (2016) Mouse sperm begin to undergo acrosomal exocytosis in the upper isthmus of the oviduct. Dev Biol 411(2):172–182

    PubMed  PubMed Central  Google Scholar 

  • Larson JL, Miller DJ (1997) Sperm from a variety of mammalian species express beta1,4-galactosyltransferase on their surface. Biol Reprod 57(2):442–453

    CAS  PubMed  Google Scholar 

  • Lay KM, Oshiro R, Arasaki C, Ashizawa K, Tatemoto H (2011) Role of acidification elicited by sialylation and sulfation of zona glycoproteins during oocyte maturation in porcine sperm-zona pellucida interactions. J Reprod Dev 57(6):744–751

  • Lea IA, Sivashanmugam P, O'Rand MG (2001) Zonadhesin: characterization, localization, and zona pellucida binding. Biol Reprod 65(6):1691–1700

    CAS  PubMed  Google Scholar 

  • Lee JW, Tian XC, Yang X (2003) Failure of male pronucleus formation is the major cause of lack of fertilization and embryo development in pig oocytes subjected to intracytoplasmic sperm injection. Biol Reprod 68(4):1341–1347

    CAS  PubMed  Google Scholar 

  • Leemans B, Stout TAE, De Schauwer C, Heras S, Nelis H, Hoogewijs M, Van Soom A, Gadella BM (2019) Update on mammalian sperm capacitation: How much does the horse differ from other species? Reproduction 157(5):R181–R197

    CAS  PubMed  Google Scholar 

  • Li YH, Hou Y, Ma W, Yuan JX, Zhang D, Sun QY, Wang WH (2004) Localization of CD9 in pig oocytes and its effects on sperm-egg interaction. Reproduction 127(2):151–157

    CAS  PubMed  Google Scholar 

  • Li H, Hung PH, Suarez SS (2015) Ejaculated mouse sperm enter cumulus-oocyte complexes more efficiently in vitro than epididymal sperm. PLoS One 10(5):e0127753

    PubMed  PubMed Central  Google Scholar 

  • Liberda J, Manaskova P, Prelovska L, Ticha M, Jonakova V (2006) Saccharide-mediated interactions of boar sperm surface proteins with components of the porcine oviduct. J Reprod Immunol 71(2):112–125

    CAS  PubMed  Google Scholar 

  • Linfor J, Berger T (2000) Potential role of alphav and beta1 integrins as oocyte adhesion molecules during fertilization in pigs. J Reprod Fertil 120(1):65–72

    CAS  PubMed  Google Scholar 

  • Litvin TN, Kamenetsky M, Zarifyan A, Buck J, Levin LR (2003) Kinetic properties of “soluble” adenylyl cyclase. Synergism between calcium and bicarbonate. J Biol Chem 278(18):15922–15926

    CAS  PubMed  Google Scholar 

  • Lorenzetti D, Poirier C, Zhao M, Overbeek PA, Harrison W, Bishop CE (2014) A transgenic insertion on mouse chromosome 17 inactivates a novel immunoglobulin superfamily gene potentially involved in sperm-egg fusion. Mamm Genome 25(3–4):141–148

    CAS  PubMed  Google Scholar 

  • Luo S, Valencia CA, Zhang J, Lee NC, Slone J, Gui B, Wang X, Li Z, Dell S, Brown J, Chen SM, Chien YH, Hwu WL, Fan PC, Wong LJ, Atwal PS, Huang T (2018) Biparental inheritance of mitochondrial DNA in humans. Proc Natl Acad Sci U S A 115(51):13039–13044

    CAS  PubMed  PubMed Central  Google Scholar 

  • Machado SA, Kadirvel G, Daigneault BW, Korneli C, Miller P, Bovin N, Miller DJ (2014) LewisX-containing glycans on the porcine oviductal epithelium contribute to formation of the sperm reservoir. Biol Reprod 91(6):140

    PubMed  Google Scholar 

  • Manaskova P, Jonakova V (2008) Localization of porcine seminal plasma (PSP) proteins in the boar reproductive tract and spermatozoa. J Reprod Immunol 78(1):40–48

    CAS  PubMed  Google Scholar 

  • Manaskova P, Liberda J, Ticha M, Jonakova V (2000) Aggregated and monomeric forms of proteins in boar seminal plasma: characterization and binding properties. Folia Biol (Praha) 46(4):143–151

    CAS  Google Scholar 

  • Manaskova P, Balinova P, Kraus M, Ticha M, Jonakova V (2003) Mutual interactions of boar seminal plasma proteins studied by immunological and chromatographic methods. Am J Reprod Immunol 50(5):399–410

    PubMed  Google Scholar 

  • Manaskova P, Peknicova J, Elzeinova F, Ticha M, Jonakova V (2007) Origin, localization and binding abilities of boar DQH sperm surface protein tested by specific monoclonal antibodies. J Reprod Immunol 74(1–2):103–113

    CAS  PubMed  Google Scholar 

  • Mao J, O'Gorman C, Sutovsky M, Zigo M, Wells KD, Sutovsky P (2018) Ubiquitin A-52 residue ribosomal protein fusion product 1 (Uba52) is essential for preimplantation embryo development. Biol Open 7(10):bio035717

  • Marini PE, Cabada MO (2003) One step purification and biochemical characterization of a spermatozoa-binding protein from porcine oviductal epithelial cells. Mol Reprod Dev 66(4):383–390

    CAS  PubMed  Google Scholar 

  • Martinez FA (2005) Studies on the interaction of chromatin-unstable boar sperm with the female reproductive tract. In: Institute of Reproductive Medicine. University of Veterinary Medicine Hannover, Hannover, Germany, p 119

    Google Scholar 

  • Mattioli M, Lucidi P, Barboni B (1998) Expanded cumuli induce acrosome reaction in boar sperm. Mol Reprod Dev 51(4):445–453

    CAS  PubMed  Google Scholar 

  • McLay DW, Clarke HJ (2003) Remodelling the paternal chromatin at fertilization in mammals. Reproduction 125(5):625–633

    CAS  PubMed  PubMed Central  Google Scholar 

  • McLeskey SB, Dowds C, Carballada R, White RR, Saling PM (1998) Molecules involved in mammalian sperm-egg interaction. Int Rev Cytol 177:57–113

    CAS  PubMed  Google Scholar 

  • Menino AR Jr, Wright RW Jr (1979) Characterization of porcine oocyte zonae pellucidae by polyacrylamide gel electrophoresis. Proc Soc Exp Biol Med 160(4):449–452

    CAS  PubMed  Google Scholar 

  • Miles EL, O'Gorman C, Zhao J, Samuel M, Walters E, Yi YJ, Sutovsky M, Prather RS, Wells KD, Sutovsky P (2013) Transgenic pig carrying green fluorescent proteasomes. Proc Natl Acad Sci U S A 110(16):6334–6339

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miyado K, Yamada G, Yamada S, Hasuwa H, Nakamura Y, Ryu F, Suzuki K, Kosai K, Inoue K, Ogura A, Okabe M, Mekada E (2000) Requirement of CD9 on the egg plasma membrane for fertilization. Science 287(5451):321–324

    CAS  PubMed  Google Scholar 

  • Moore HD, Bedford JM (1983) The interaction of mammalian gametes in the female. In: Hartmann JF (ed) Mechanism and control of animal fertilization. Academic Press, New York, pp 453–497

    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

    CAS  PubMed  Google Scholar 

  • Mori E, Baba T, Iwamatsu A, Mori T (1993) Purification and characterization of a 38-kDa protein, sp38, with zona pellucida-binding property from porcine epididymal sperm. Biochem Biophys Res Commun 196(1):196–202

    CAS  PubMed  Google Scholar 

  • Mori E, Kashiwabara S, Baba T, Inagaki Y, Mori T (1995) Amino acid sequences of porcine Sp38 and proacrosin required for binding to the zona pellucida. Dev Biol 168(2):575–583

    CAS  PubMed  Google Scholar 

  • Mori E, Fukuda H, Imajoh-Ohmi S, Mori T, Takasaki S (2012) Purification of N-acetyllactosamine-binding activity from the porcine sperm membrane: possible involvement of an ADAM complex in the carbohydrate-binding activity of sperm. J Reprod Dev 58(1):117–125

    CAS  PubMed  Google Scholar 

  • Mtango NR, Sutovsky M, Susor A, Zhong Z, Latham KE, Sutovsky P (2011) Essential role of maternal UCHL1 and UCHL3 in fertilization and preimplantation embryo development. J Cell Physiol 227(4):1592–1603

    Google Scholar 

  • Muro Y, Hasuwa H, Isotani A, Miyata H, Yamagata K, Ikawa M, Yanagimachi R, Okabe M (2016) Behavior of mouse spermatozoa in the female reproductive tract from soon after mating to the beginning of fertilization. Biol Reprod 94(4):80

    PubMed  Google Scholar 

  • Murray SC, Smith TT (1997) Sperm interaction with fallopian tube apical membrane enhances sperm motility and delays capacitation. Fertil Steril 68(2):351–357

    PubMed  Google Scholar 

  • Myles DG, Hyatt H, Primakoff P (1987) Binding of both acrosome-intact and acrosome-reacted guinea pig sperm to the zona pellucida during in vitro fertilization. Dev Biol 121(2):559–567

    CAS  PubMed  Google Scholar 

  • Nakano M, Hatanaka Y, Sawai T, Kobayashi N, Tobita T (1987) Fractionation of glycoproteins from porcine zonae pellucidae into three families by high-performance liquid chromatography. Biochem Int 14(3):417–423

    CAS  PubMed  Google Scholar 

  • Nozawa K, Satouh Y, Fujimoto T, Oji A, Ikawa M (2018) Sperm-borne phospholipase C zeta-1 ensures monospermic fertilization in mice. Sci Rep 8(1):1315

    PubMed  PubMed Central  Google Scholar 

  • Okamura N, Tajima Y, Soejima A, Masuda H, Sugita Y (1985) Sodium bicarbonate in seminal plasma stimulates the motility of mammalian spermatozoa through direct activation of adenylate cyclase. J Biol Chem 260(17):9699–9705

    CAS  PubMed  Google Scholar 

  • Okamura N, Tamba M, Liao HJ, Onoe S, Sugita Y, Dacheux F, Dacheux JL (1995) Cloning of complementary DNA encoding a 135-kilodalton protein secreted from porcine corpus epididymis and its identification as an epididymis-specific alpha-mannosidase. Mol Reprod Dev 42(2):141–148

    CAS  PubMed  Google Scholar 

  • Oko R, Aarabi M, Mao J, Balakier H, Sutovsky P (2017) Sperm specific WW-domain binding proteins. In: DeJonge C, Barratt C (eds) The sperm cell: production, maturation, fertilization, regeneration. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • O'Leary S, Jasper MJ, Warnes GM, Armstrong DT, Robertson SA (2004) Seminal plasma regulates endometrial cytokine expression, leukocyte recruitment and embryo development in the pig. Reproduction 128(2):237–247

    CAS  PubMed  Google Scholar 

  • Pacey AA, Davies N, Warren MA, Barratt CL, Cooke ID (1995a) Hyperactivation may assist human spermatozoa to detach from intimate association with the endosalpinx. Hum Reprod 10(10):2603–2609

    CAS  PubMed  Google Scholar 

  • Pacey AA, Hill CJ, Scudamore IW, Warren MA, Barratt CL, Cooke ID (1995b) The interaction in vitro of human spermatozoa with epithelial cells from the human uterine (fallopian) tube. Hum Reprod 10(2):360–366

    CAS  PubMed  Google Scholar 

  • Peng L, Wen M, Liu Q, Peng J, Tang S, Hong Y, Liu S, Xiao Y (2018) Persistence and transcription of paternal mtDNA dependent on the delivery strategy rather than mitochondria source in fish embryos. Cell Physiol Biochem 47(5):1898–1908

    CAS  PubMed  Google Scholar 

  • Perez-Patino C, Barranco I, Parrilla I, Martinez EA, Rodriguez-Martinez H, Roca J (2016a) Extensive dataset of boar seminal plasma proteome displaying putative reproductive functions of identified proteins. Data Brief 8:1370–1373

    PubMed  PubMed Central  Google Scholar 

  • Perez-Patino C, Barranco I, Parrilla I, Valero ML, Martinez EA, Rodriguez-Martinez H, Roca J (2016b) Characterization of the porcine seminal plasma proteome comparing ejaculate portions. J Proteome 142:15–23

    CAS  Google Scholar 

  • Perreault SD, Wolff RA, Zirkin BR (1984) The role of disulfide bond reduction during mammalian sperm nuclear decondensation in vivo. Dev Biol 101(1):160–167

    CAS  PubMed  Google Scholar 

  • Peterson RN, Hunt WP (1989) Identification, isolation, and properties of a plasma membrane protein involved in the adhesion of boar sperm to the porcine zona pellucida. Gamete Res 23(1):103–118

    CAS  PubMed  Google Scholar 

  • Petrunkina AM, Harrison RA, Topfer-Petersen E (2000) Only low levels of spermadhesin AWN are detectable on the surface of live ejaculated boar spermatozoa. Reprod Fertil Dev 12(7–8):361–371

    CAS  PubMed  Google Scholar 

  • Petrunkina AM, Gehlhaar R, Drommer W, Waberski D, Topfer-Petersen E (2001) Selective sperm binding to pig oviductal epithelium in vitro. Reproduction 121(6):889–896

    CAS  PubMed  Google Scholar 

  • Petrunkina AM, Lakamp A, Gentzel M, Ekhlasi-Hundrieser M, Topfer-Petersen E (2003) Fate of lactadherin P47 during post-testicular maturation and capacitation of boar spermatozoa. Reproduction 125(3):377–387

    CAS  PubMed  Google Scholar 

  • Pilch B, Mann M (2006) Large-scale and high-confidence proteomic analysis of human seminal plasma. Genome Biol 7(5):R40

    PubMed  PubMed Central  Google Scholar 

  • Plante G, Therien I, Lachance C, Leclerc P, Fan J, Manjunath P (2014) Implication of the human Binder of SPerm Homolog 1 (BSPH1) protein in capacitation. Mol Hum Reprod 20(5):409–421

    CAS  PubMed  Google Scholar 

  • Plante G, Prud'homme B, Fan J, Lafleur M, Manjunath P (2016) Evolution and function of mammalian binder of sperm proteins. Cell Tissue Res 363(1):105–127

    CAS  PubMed  Google Scholar 

  • Politi Y, Gal L, Kalifa Y, Ravid L, Elazar Z, Arama E (2014) Paternal mitochondrial destruction after fertilization is mediated by a common endocytic and autophagic pathway in Drosophila. Dev Cell 29(3):305–320

    CAS  PubMed  Google Scholar 

  • Porter JC, Hogg N (1998) Integrins take partners: cross-talk between integrins and other membrane receptors. Trends Cell Biol 8(10):390–396

    CAS  PubMed  Google Scholar 

  • Primakoff P, Myles DG (2000) The ADAM gene family: surface proteins with adhesion and protease activity. Trends Genet 16(2):83–87

    CAS  PubMed  Google Scholar 

  • Puga Molina L, Luque G, Balestrini P, Marín-Briggiler C, Romarowski A, Romarowski A (2018) Molecular basis of human sperm capacitation. Front Cell Dev Biol 6(72)

  • Que EL, Duncan FE, Bayer AR, Philips SJ, Roth EW, Bleher R, Gleber SC, Vogt S, Woodruff TK, O'Halloran TV (2017) Zinc sparks induce physiochemical changes in the egg zona pellucida that prevent polyspermy. Integr Biol (Camb) 9(2):135–144

    CAS  Google Scholar 

  • Rebeiz M, Miller DJ (1999) Porcine sperm surface beta1,4galactosyltransferase binds to the zona pellucida but is not necessary or sufficient to mediate sperm-zona pellucida binding. Mol Reprod Dev 54(4):379–387

    CAS  PubMed  Google Scholar 

  • Redgrove KA, Anderson AL, Dun MD, McLaughlin EA, O'Bryan MK, Aitken RJ, Nixon B (2011) Involvement of multimeric protein complexes in mediating the capacitation-dependent binding of human spermatozoa to homologous zonae pellucidae. Dev Biol 356(2):460–474

    CAS  PubMed  Google Scholar 

  • Reid AT, Redgrove K, Aitken RJ, Nixon B (2011) Cellular mechanisms regulating sperm-zona pellucida interaction. Asian J Androl 13(1):88–96

    CAS  PubMed  Google Scholar 

  • Rodríguez-Martínez H, Peña Vega FJ (2013) Semen technologies in domestic animal species. Anim Front 3(4):8

    Google Scholar 

  • Rodriguez-Martinez H, Iborra A, Martinez P, Calvete JJ (1998) Immunoelectronmicroscopic imaging of spermadhesin AWN epitopes on boar spermatozoa bound in vivo to the zona pellucida. Reprod Fertil Dev 10(6):491–497

    CAS  PubMed  Google Scholar 

  • Rodriguez-Martinez H, Kvist U, Saravia F, Wallgren M, Johannisson A, Sanz L, Pena FJ, Martinez EA, Roca J, Vazquez JM, Calvete JJ (2009) The physiological roles of the boar ejaculate. Soc Reprod Fertil Suppl 66:1–21

    CAS  PubMed  Google Scholar 

  • Rodriguez-Martinez H, Saravia F, Wallgren M, Martinez EA, Sanz L, Roca J, Vazquez JM, Calvete JJ (2010) Spermadhesin PSP-I/PSP-II heterodimer induces migration of polymorphonuclear neutrophils into the uterine cavity of the sow. J Reprod Immunol 84(1):57–65

    CAS  PubMed  Google Scholar 

  • Rojansky R, Cha MY, Chan DC (2016) Elimination of paternal mitochondria in mouse embryos occurs through autophagic degradation dependent on PARKIN and MUL1. eLife 5:e17896

  • Roldan ML, Teijeiro JM, Ruiz Alvarez J, Marini PE (2018) Sperm binding to porcine oviductal cells is mediated by SRCR domains contained in DMBT1. J Cell Biochem 119(4):3755–3762

    CAS  PubMed  Google Scholar 

  • Rozeboom KJ, Troedsson MH, Molitor TW, Crabo BG (1999) The effect of spermatozoa and seminal plasma on leukocyte migration into the uterus of gilts. J Anim Sci 77(8):2201–2206

    CAS  PubMed  Google Scholar 

  • Rubinstein E, Ziyyat A, Prenant M, Wrobel E, Wolf JP, Levy S, Le Naour F, Boucheix C (2006) Reduced fertility of female mice lacking CD81. Dev Biol 290(2):351–358

    CAS  PubMed  Google Scholar 

  • Rybar R, Fladikova L, Faldyna M, Machatkova M, Rubes J (2004) Bull and boar sperm DNA integrity evaluated by sperm chromatin structure assay in the Czech Republic. Vet Med Czech 49:1–8

    CAS  Google Scholar 

  • Ryu J, Lee K (2017) CRISPR/Cas9-mediated gene targeting during embryogenesis in swine. Methods Mol Biol 1605:231–244

    CAS  PubMed  PubMed Central  Google Scholar 

  • Santi CM, Orta G, Salkoff L, Visconti PE, Darszon A, Trevino CL (2013) K+ and Cl- channels and transporters in sperm function. Curr Top Dev Biol 102:385–421

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sanz L, Calvete JJ, Jonakova V, Topfer-Petersen E (1992) Boar spermadhesins AQN-1 and AWN are sperm-associated acrosin inhibitor acceptor proteins. FEBS Lett 300(1):63–66

    CAS  PubMed  Google Scholar 

  • Sartini BL, Berger T (2000) Identification of homologous binding proteins in porcine and bovine gametes. Mol Reprod Dev 55(4):446–451

    CAS  PubMed  Google Scholar 

  • Sato M, Sato K (2011) Degradation of paternal mitochondria by fertilization-triggered autophagy in C. elegans embryos. Science 334(6059):1141–1144

    CAS  PubMed  Google Scholar 

  • Saunders CM, Larman MG, Parrington J, Cox LJ, Royse J, Blayney LM, Swann K, Lai FA (2002) PLC zeta: a sperm-specific trigger of Ca(2+) oscillations in eggs and embryo development. Development 129(15):3533–3544

    CAS  PubMed  Google Scholar 

  • Schjenken JE, Robertson SA (2014) Seminal fluid and immune adaptation for pregnancy--comparative biology in mammalian species. Reprod Domest Anim 49(Suppl 3):27–36

    PubMed  Google Scholar 

  • Schlondorff J, Blobel CP (1999) Metalloprotease-disintegrins: modular proteins capable of promoting cell-cell interactions and triggering signals by protein-ectodomain shedding. J Cell Sci 112(Pt 21):3603–3617

    CAS  PubMed  Google Scholar 

  • Schuberth HJ, Taylor U, Zerbe H, Waberski D, Hunter R, Rath D (2008) Immunological responses to semen in the female genital tract. Theriogenology 70(8):1174–1181

    CAS  PubMed  Google Scholar 

  • Schwartz M, Vissing J (2002) Paternal inheritance of mitochondrial DNA. N Engl J Med 347(8):576–580

    PubMed  Google Scholar 

  • Shalgi R, Phillips D (1980) Mechanics of sperm entry in cycling hamsters. J Ultrastruct Res 71(2):154–161

    CAS  PubMed  Google Scholar 

  • Sharkey DJ, Tremellen KP, Jasper MJ, Gemzell-Danielsson K, Robertson SA (2012) Seminal fluid induces leukocyte recruitment and cytokine and chemokine mRNA expression in the human cervix after coitus. J Immunol 188(5):2445–2454

    CAS  PubMed  Google Scholar 

  • Shitara H, Kaneda H, Sato A, Inoue K, Ogura A, Yonekawa H, Hayashi JI (2000) Selective and continuous elimination of mitochondria microinjected into mouse eggs from spermatids, but not from liver cells, occurs throughout embryogenesis. Genetics 156(3):1277–1284

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shitara H, Kaneda H, Sato A, Iwasaki K, Hayashi J, Taya C, Yonekawa H (2001) Non-invasive visualization of sperm mitochondria behavior in transgenic mice with introduced green fluorescent protein (GFP). FEBS Lett 500(1–2):7–11

    CAS  PubMed  Google Scholar 

  • Silva E, Frost D, Li L, Bovin N, Miller DJ (2017) Lactadherin is a candidate oviduct Lewis X trisaccharide receptor on porcine spermatozoa. Andrology 5(3):589–597

    CAS  PubMed  PubMed Central  Google Scholar 

  • Snell WJ, White JM (1996) The molecules of mammalian fertilization. Cell 85(5):629–637

    CAS  PubMed  Google Scholar 

  • Soede NM, Helmond FA, Kemp B (1994) Periovulatory profiles of oestradiol, LH and progesterone in relation to oestrus and embryo mortality in multiparous sows using transrectal ultrasonography to detect ovulation. J Reprod Fertil 101(3):633–641

    CAS  PubMed  Google Scholar 

  • Song X, Li F, Cao G, Zhang J, Han Y (2007) Distribution of alpha-D-mannose residues on zona pellucida and their role(s) in fertilization in pigs. Sci China C Life Sci 50(2):170–177

    CAS  PubMed  Google Scholar 

  • Song WH, Yi YJ, Sutovsky M, Meyers S, Sutovsky P (2016) Autophagy and ubiquitin-proteasome system contribute to sperm mitophagy after mammalian fertilization. Proc Natl Acad Sci U S A 113(36):E5261–E5270

    CAS  PubMed  PubMed Central  Google Scholar 

  • Spargo SC, Hope RM (2003) Evolution and nomenclature of the zona pellucida gene family. Biol Reprod 68(2):358–362

    CAS  PubMed  Google Scholar 

  • Suarez SS (1987) Sperm transport and motility in the mouse oviduct: observations in situ. Biol Reprod 36(1):203–210

    CAS  PubMed  Google Scholar 

  • Suarez SS (1996) Hyperactivated motility in sperm. J Androl 17(4):331–335

    CAS  PubMed  Google Scholar 

  • Suarez SS (1998) The oviductal sperm reservoir in mammals: mechanisms of formation. Biol Reprod 58(5):1105–1107

    CAS  PubMed  Google Scholar 

  • Suarez SS (2008) Regulation of sperm storage and movement in the mammalian oviduct. Int J Dev Biol 52(5–6):455–462

    PubMed  Google Scholar 

  • Suarez SS (2015) Gamete and Zygote Transport. In: Plant TM, Zeleznik AJ (eds) Knobil and Neill’s physiology of reproduction, vol. 1. Academic Press, Cambridge, pp 197–232

  • Suarez SS (2016) Mammalian sperm interactions with the female reproductive tract. Cell Tissue Res 363(1):185–194

    PubMed  Google Scholar 

  • Suarez S, 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(6):998–1004

    CAS  PubMed  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(1):75–80

    CAS  PubMed  Google Scholar 

  • Suarez SS, Varosi SM, Dai X (1993) Intracellular calcium increases with hyperactivation in intact, moving hamster sperm and oscillates with the flagellar beat cycle. Proc Natl Acad Sci U S A 90(10):4660–4664

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun QY, Nagai T (2003) Molecular mechanisms underlying pig oocyte maturation and fertilization. J Reprod Dev 49(5):347–359

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Sutovsky P, Schatten G (1997) Depletion of glutathione during bovine oocyte maturation reversibly blocks the decondensation of the male pronucleus and pronuclear apposition during fertilization. Biol Reprod 56(6):1503–1512

    CAS  PubMed  Google Scholar 

  • Sutovsky P, Navara CS, Schatten G (1996) Fate of the sperm mitochondria, and the incorporation, conversion, and disassembly of the sperm tail structures during bovine fertilization. Biol Reprod 55(6):1195–1205

    CAS  PubMed  Google Scholar 

  • Sutovsky P, McCauley TC, Sutovsky M, Day BN (2003) Early degradation of paternal mitochondria in domestic pig (Sus scrofa) is prevented by selective proteasomal inhibitors lactacystin and MG132. Biol Reprod 68(5):1793–1800

    CAS  PubMed  Google Scholar 

  • Sutovsky P, Van Leyen K, McCauley T, Day BN, Sutovsky M (2004) Degradation of paternal mitochondria after fertilization: implications for heteroplasmy, assisted reproductive technologies and mtDNA inheritance. Reprod BioMed Online 8(1):24–33

    CAS  PubMed  Google Scholar 

  • Sutovsky P, Kerns K, Zigo M, Zuidema D (2019) Boar semen improvement through sperm capacitation management, with emphasis on zinc ion homeostasis. Theriogenology 137:50–55

    CAS  PubMed  Google Scholar 

  • Suzuki T, Fujinoki M, Shibahara H, Suzuki M (2010) Regulation of hyperactivation by PPP2 in hamster spermatozoa. Reproduction 139(5):847–856

    CAS  PubMed  Google Scholar 

  • Talevi R, Gualtieri R (2010) Molecules involved in sperm-oviduct adhesion and release. Theriogenology 73(6):796–801

    CAS  PubMed  Google Scholar 

  • Tanihara F, Nakai M, Men NT, Kato N, Kaneko H, Noguchi J, Otoi T, Kikuchi K (2014) Roles of the zona pellucida and functional exposure of the sperm-egg fusion factor 'IZUMO' during in vitro fertilization in pigs. Anim Sci J 85(4):395–404

    PubMed  Google Scholar 

  • Tanphaichitr N, Moase C, Taylor T, Surewicz K, Hansen C, Namking M, Berube B, Kamolvarin N, Lingwood CA, Sullivan R, Rattanachaiyanont M, White D (1998) Isolation of antiSLIP1-reactive boar sperm P68/62 and its binding to mammalian zona pellucida. Mol Reprod Dev 49(2):203–216

    CAS  PubMed  Google Scholar 

  • Tanphaichitr N, Carmona E, Bou Khalil M, Xu H, Berger T, Gerton GL (2007) New insights into sperm-zona pellucida interaction: involvement of sperm lipid rafts. Front Biosci 12:1748–1766

    CAS  PubMed  Google Scholar 

  • Tanphaichitr N, Kongmanas K, Kruevaisayawan H, Saewu A, Sugeng C, Fernandes J, Souda P, Angel JB, Faull KF, Aitken RJ, Whitelegge J, Hardy D, Berger T, Baker M (2015) Remodeling of the plasma membrane in preparation for sperm-egg recognition: roles of acrosomal proteins. Asian J Androl 17(4):574–582

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tardif S, Cormier N (2011) Role of zonadhesin during sperm-egg interaction: a species-specific acrosomal molecule with multiple functions. Mol Hum Reprod 17(11):661–668

    CAS  PubMed  Google Scholar 

  • Tardif S, Dube C, Chevalier S, Bailey JL (2001) Capacitation is associated with tyrosine phosphorylation and tyrosine kinase-like activity of pig sperm proteins. Biol Reprod 65(3):784–792

    CAS  PubMed  Google Scholar 

  • Tardif S, Dube 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(1):207–213

    CAS  PubMed  Google Scholar 

  • Tardif S, Wilson MD, Wagner R, Hunt P, Gertsenstein M, Nagy A, Lobe C, Koop BF, Hardy DM (2010) Zonadhesin is essential for species specificity of sperm adhesion to the egg zona pellucida. J Biol Chem 285(32):24863–24870

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tateno H, Krapf D, Hino T, Sanchez-Cardenas C, Darszon A, Yanagimachi R, Visconti PE (2013) Ca2+ ionophore A23187 can make mouse spermatozoa capable of fertilizing in vitro without activation of cAMP-dependent phosphorylation pathways. Proc Natl Acad Sci U S A 110(46):18543–18548

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tavalaee M, Parivar K, Shahverdi AH, Ghaedi K, Nasr-Esfahani MH (2017) Status of sperm-born oocyte activating factors (PAWP, PLCzeta) and sperm chromatin in uncapacitated, capacitated and acrosome-reacted conditions. Hum Fertil (Camb) 20(2):96–103

    CAS  Google Scholar 

  • Teijeiro JM, Cabada MO, Marini PE (2008) Sperm binding glycoprotein (SBG) produces calcium and bicarbonate dependent alteration of acrosome morphology and protein tyrosine phosphorylation on boar sperm. J Cell Biochem 103(5):1413–1423

    CAS  PubMed  Google Scholar 

  • Teijeiro JM, Ignotz GG, Marini PE (2009) Annexin A2 is involved in pig (Sus scrofa)sperm-oviduct interaction. Mol Reprod Dev 76(4):334–341

    CAS  PubMed  Google Scholar 

  • Teijeiro JM, Roldan ML, Marini PE (2016) Annexin A2 and S100A10 in the mammalian oviduct. Cell Tissue Res 363(2):567–577

    CAS  PubMed  Google Scholar 

  • Tesarik J, Drahorad J, Peknicova J (1988) Subcellular immunochemical localization of acrosin in human spermatozoa during the acrosome reaction and zona pellucida penetration. Fertil Steril 50(1):133–141

    CAS  PubMed  Google Scholar 

  • Topfer-Petersen E (1999) Carbohydrate-based interactions on the route of a spermatozoon to fertilization. Hum Reprod Update 5(4):314–329

    CAS  PubMed  Google Scholar 

  • Topfer-Petersen E, Calvete JJ (1995) Molecular mechanisms of the interaction between sperm and the zona pellucida in mammals: studies on the pig. Int J Androl 18(Suppl 2):20–26

    PubMed  Google Scholar 

  • Topfer-Petersen E, Henschen A (1987) Acrosin shows zona and fucose binding, novel properties for a serine proteinase. FEBS Lett 226(1):38–42

    CAS  PubMed  Google Scholar 

  • Topfer-Petersen E, Friess AE, Nguyen H, Schill WB (1985) Evidence for a fucose-binding protein in boar spermatozoa. Histochemistry 83(2):139–145

    CAS  PubMed  Google Scholar 

  • Topfer-Petersen E, Mann K, Calvete JJ (1993) Identification of porcine oocyte 55 kDa alpha and beta proteins within the zona pellucida glycoprotein families indicates that oocyte sperm receptor activity is associated with different zone pellucida proteins in different mammalian species. Biol Chem Hoppe Seyler 374(7):411–417

    CAS  PubMed  Google Scholar 

  • Topfer-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(4–5):217–224

    CAS  PubMed  Google Scholar 

  • Topfer-Petersen E, Ekhlasi-Hundrieser M, Tsolova M (2008) Glycobiology of fertilization in the pig. Int J Dev Biol 52(5–6):717–736

    PubMed  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(6):e11204

    PubMed  PubMed Central  Google Scholar 

  • Tsai PS, Brewis IA, van Maaren J, Gadella BM (2012) Involvement of complexin 2 in docking, locking and unlocking of different SNARE complexes during sperm capacitation and induced acrosomal exocytosis. PLoS One 7(3):e32603

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vadnais ML, Althouse GC (2011) Characterization of capacitation, cryoinjury, and the role of seminal plasma in porcine sperm. Theriogenology 76(8):1508–1516

    CAS  PubMed  Google Scholar 

  • Vadnais ML, Roberts KP (2007) Effects of seminal plasma on cooling-induced capacitative changes in boar sperm. J Androl 28(3):416–422

    CAS  PubMed  Google Scholar 

  • Vadnais ML, Kirkwood RN, Tempelman RJ, Sprecher DJ, Chou K (2005) Effect of cooling and seminal plasma on the capacitation status of fresh boar sperm as determined using chlortetracycline assay. Anim Reprod Sci 87(1–2):121–132

    CAS  PubMed  Google Scholar 

  • Vadnais ML, Foster DN, Roberts KP (2008) Molecular cloning and expression of the CRISP family of proteins in the boar. Biol Reprod 79(6):1129–1134

    CAS  PubMed  Google Scholar 

  • Veselsky L, Jonakova V, Sanz ML, Topfer-Petersen E, Cechova D (1992) Binding of a 15 kDa glycoprotein from spermatozoa of boars to surface of zona pellucida and cumulus oophorus cells. J Reprod Fertil 96(2):593–602

    CAS  PubMed  Google Scholar 

  • Veselsky L, Peknicova J, Cechova D, Kraus M, Geussova G, Jonakova V (1999) Characterization of boar spermadhesins by monoclonal and polyclonal antibodies and their role in binding to oocytes. Am J Reprod Immunol 42(3):187–197

    CAS  PubMed  Google Scholar 

  • Veselsky L, Jonakova V, Dostal J, Holan V, Voburka Z, Drahorad J, Manaskova P, Zelezna B (2000) Inhibition of the antibody responses to rat blood transfusion antigens in mice by boar seminal immunosuppressive fraction. Am J Reprod Immunol 44(6):325–335

    CAS  PubMed  Google Scholar 

  • Visconti PE, Florman HM (2010) Mechanisms of sperm-egg interactions: between sugars and broken bonds. Sci Signal 3(142):e35

    Google Scholar 

  • Visconti PE, Moore GD, Bailey JL, Leclerc P, Connors SA, Pan D, Olds-Clarke P, Kopf GS (1995) Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development 121(4):1139–1150

    CAS  PubMed  Google Scholar 

  • Visconti PE, Krapf D, de la Vega-Beltran JL, Acevedo JJ, Darszon A (2011) Ion channels, phosphorylation and mammalian sperm capacitation. Asian J Androl 13(3):395–405

    CAS  PubMed  PubMed Central  Google Scholar 

  • Waberski D, Helms D, Beyerbach M, Weitze KF, Bollwein H, Bluemig P, Willeke H, Acevedo N, Saacke RG (2002) Sperm chromatin structure in boars used in artificial insemination. Reprod Domest Anim 37(4):257

    Google Scholar 

  • Wagner A, Ekhlasi-Hundrieser M, Hettel C, Petrunkina A, Waberski D, Nimtz M, Topfer-Petersen E (2002) Carbohydrate-based interactions of oviductal sperm reservoir formation-studies in the pig. Mol Reprod Dev 61(2):249–257

    CAS  PubMed  Google Scholar 

  • Wardrip NJ, Hedrick JL (1985) Pig zona pellucida 25K and 65K glycoproteins are derived from Hydrolysis and reduction of the 90K family. J Cell Biol 101:378a

    Google Scholar 

  • Wassarman PM (1999) Mammalian fertilization: molecular aspects of gamete adhesion, exocytosis, and fusion. Cell 96(2):175–183

    CAS  PubMed  Google Scholar 

  • Wassarman PM (2009) Mammalian fertilization: the strange case of sperm protein 56. Bioessays 31(2):153–158

    CAS  PubMed  Google Scholar 

  • Whitworth KM, Lee K, Benne JA, Beaton BP, Spate LD, Murphy SL, Samuel MS, Mao J, O'Gorman C, Walters EM, Murphy CN, Driver J, Mileham A, McLaren D, Wells KD, Prather RS (2014) Use of the CRISPR/Cas9 system to produce genetically engineered pigs from in vitro-derived oocytes and embryos. Biol Reprod 91(3):78

    PubMed  PubMed Central  Google Scholar 

  • Williams TA, Barnes K, Kenny AJ, Turner AJ, Hooper NM (1992) A comparison of the zinc contents and substrate specificities of the endothelial and testicular forms of porcine angiotensin converting enzyme and the preparation of isoenzyme-specific antisera. Biochem J 288(Pt 3):875–881

    CAS  PubMed  PubMed Central  Google Scholar 

  • Williams M, Hill CJ, Scudamore I, Dunphy B, Cooke ID, Barratt CL (1993) Sperm numbers and distribution within the human fallopian tube around ovulation. Hum Reprod 8(12):2019–2026

    CAS  PubMed  Google Scholar 

  • Wolff JN, Gemmell NJ (2013) Mitochondria, maternal inheritance, and asymmetric fitness: why males die younger. Bioessays 35(2):93–99

    CAS  PubMed  Google Scholar 

  • Wright SJ, Longo FJ (1988) Sperm nuclear enlargement in fertilized hamster eggs is related to meiotic maturation of the maternal chromatin. J Exp Zool 247(2):155–165

    CAS  PubMed  Google Scholar 

  • Wu AT, Sutovsky P, Manandhar G, Xu W, Katayama M, Day BN, Park KW, Yi YJ, Xi YW, Prather RS, Oko R (2007) PAWP, a sperm-specific WW domain-binding protein, promotes meiotic resumption and pronuclear development during fertilization. J Biol Chem 282(16):12164–12175

    CAS  PubMed  Google Scholar 

  • Yamasaki K, Yoshida K, Yoshiike M, Shimada K, Nishiyama H, Takamizawa S, Yanagida K, Iwamoto T (2017) Relationship between Semenogelins bound to human sperm and other semen parameters and pregnancy outcomes. Basic Clin Androl 27:15

    PubMed  PubMed Central  Google Scholar 

  • Yanagimachi R (1994) Mammalian fertilization. In: Knobil E, Neill JD (eds) The Physiology of Reproduction, vol. 1. Raven Press, New York, pp 189–317

    Google Scholar 

  • Yefimova M, Bourmeyster N, Becq F, Burel A, Lavault MT, Jouve G, Veau S, Pimentel C, Jegou B, Ravel C (2019) Update on the cellular and molecular aspects of cystic fibrosis transmembrane conductance regulator (CFTR) and male fertility. Morphologie 103(341):4–10

    CAS  PubMed  Google Scholar 

  • Yi YJ, Manandhar G, Sutovsky M, Li R, Jonakova 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(5):780–793

    CAS  PubMed  Google Scholar 

  • Yi YJ, Manandhar G, Sutovsky M, Jonakova 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(2):154–163

    CAS  PubMed  Google Scholar 

  • Yi YJ, Manandhar G, Sutovsky M, Zimmerman SW, Jonakova 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(2):325–340

    CAS  PubMed  Google Scholar 

  • Yonezawa N, Hatanaka Y, Takeyama H, Nakano M (1995) Binding of pig sperm receptor in the zona pellucida to the boar sperm acrosome. J Reprod Fertil 103(1):1–8

    CAS  PubMed  Google Scholar 

  • Yonezawa N, Fukui N, Kudo K, Nakano M (1999) Localization of neutral N-linked carbohydrate chains in pig zona pellucida glycoprotein ZPC. Eur J Biochem 260(1):57–63

    CAS  PubMed  Google Scholar 

  • Yonezawa N, Amari S, Takahashi K, Ikeda K, Imai FL, Kanai S, Kikuchi K, Nakano M (2005) Participation of the nonreducing terminal beta-galactosyl residues of the neutral N-linked carbohydrate chains of porcine zona pellucida glycoproteins in sperm-egg binding. Mol Reprod Dev 70(2):222–227

    CAS  PubMed  Google Scholar 

  • Yoon S, Chang KT, Cho H, Moon J, Kim JS, Min SH, Koo DB, Lee SR, Kim SH, Park KE, Park YI, Kim E (2014) Characterization of pig sperm hyaluronidase and improvement of the digestibility of cumulus cell mass by recombinant pSPAM1 hyaluronidase in an in vitro fertilization assay. Anim Reprod Sci 150(3–4):107–114

    CAS  PubMed  Google Scholar 

  • Yu Y, Xu W, Yi YJ, Sutovsky P, Oko R (2006) The extracellular protein coat of the inner acrosomal membrane is involved in zona pellucida binding and penetration during fertilization: characterization of its most prominent polypeptide (IAM38). Dev Biol 290(1):32–43

    CAS  PubMed  Google Scholar 

  • Yuan Y, Spate LD, Redel BK, Tian Y, Zhou J, Prather RS, Roberts RM (2017) Quadrupling efficiency in production of genetically modified pigs through improved oocyte maturation. Proc Natl Acad Sci U S A 114(29):E5796–e5804

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yurewicz EC, Sacco AG, Subramanian MG (1987) Structural characterization of the Mr = 55,000 antigen (ZP3) of porcine oocyte zona pellucida. Purification and characterization of alpha- and beta-glycoproteins following digestion of lactosaminoglycan with endo-beta-galactosidase. J Biol Chem 262(2):564–571

    CAS  PubMed  Google Scholar 

  • Yurewicz EC, Pack BA, Sacco AG (1991) Isolation, composition, and biological activity of sugar chains of porcine oocyte zona pellucida 55K glycoproteins. Mol Reprod Dev 30(2):126–134

    CAS  PubMed  Google Scholar 

  • Zapata-Carmona H, Baron L, Zuniga LM, Diaz ES, Kong M, Drobnis EZ, Sutovsky P, Morales P (2019) The activation of the chymotrypsin-like activity of the proteasome is regulated by soluble adenyl cyclase / cAMP / protein kinase a pathway and required for human sperm capacitation. Mol Hum Reprod 25(10):587–600

  • Zayas-Perez H, Casas E, Bonilla E, Betancourt M (2005) Inhibition of sperm-zona pellucida binding by a 55 kDa pig sperm protein in vitro. Arch Androl 51(3):195–206

    CAS  PubMed  Google Scholar 

  • Zhu J, Massey JB, Mitchell-Leef D, Elsner CW, Kort HI, Roudebush WE (2006) Platelet-activating factor acetylhydrolase activity affects sperm motility and serves as a decapacitation factor. Fertil Steril 85(2):391–394

    CAS  PubMed  Google Scholar 

  • Zigo M, Jonakova V, Sulc M, Manaskova-Postlerova P (2013) Characterization of sperm surface protein patterns of ejaculated and capacitated boar sperm, with the detection of ZP binding candidates. Int J Biol Macromol 61:322–328

    CAS  PubMed  Google Scholar 

  • Zigo M, Dorosh A, Pohlova A, Jonakova V, Sulc M, Manaskova-Postlerova P (2015) Panel of monoclonal antibodies to sperm surface proteins as a tool for monitoring localization and identification of sperm-zona pellucida receptors. Cell Tissue Res 359(3):895–908

    CAS  PubMed  Google Scholar 

  • Zigo M, Kerns K, Sutovsky M, Sutovsky P (2018) Modifications of the 26S proteasome during boar sperm capacitation. Cell Tissue Res 372(3):591–601

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zigo M, Jonakova V, Manaskova-Postlerova P, Kerns K, Sutovsky P (2019a) Ubiquitin-proteasome system participates in the de-aggregation of spermadhesin and DQH protein during boar sperm capacitation. Reproduction 157(3):283–295

    CAS  PubMed  Google Scholar 

  • Zigo M, Manaskova-Postlerova P, Jonakova V, Kerns K, Sutovsky P (2019b) Compartmentalization of the proteasome-interacting proteins during sperm capacitation. Sci Rep 9(1):12583

    PubMed  PubMed Central  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(2):e17256

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zuidema D, Sutovsky P (2019) The domestic pig as a model for the study of mitochondrial inheritance. Cell Tissue Research. https://doi.org/10.1007/s00441-019-03100-z

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Acknowledgments

We would like to thank to our past and present colleagues, trainees, associates and collaborators who inspired and facilitated our studies reviewed in this article. In particular, we appreciate the support from Dr. Richard Oko (Queen’s University, Kingston, ON) and Dr. Randall Prather (National Swine Research Resource Center, University of Missouri). Logistic, technical and clerical support by Ms. Miriam Sutovsky and Ms. Kathy Craighead is gratefully acknowledged.

Funding

This review is supported by the National Institute of Food and Agriculture (NIFA), U.S. Department of Agriculture (USDA) grant number 2015-67015-23231 (P.S.); the USDA NIFA Agriculture and Food Research Initiative’s Post-Doctoral Fellowships program, grant number 2019-67012-29714 (K.K.); grant number 5 R01 HD084353-02 from National Institutes of Health (NIH) National Institute of Child and Human Development (P.S.); and seed funding from the Food for the twenty-first Century Program of the University of Missouri (P.S.); and by the project BIOCEV (CZ.1.05/1.1.00/02.0109) from the European Regional Development Fund (P.M.-P., V.J.), by the Grant Agency of the Czech Republic No. GA-18-11275S (P.M.-P.), by the Institutional support of the Institute of Biotechnology, Czech Academy of Sciences RVO: 86652036 (P.M.-P., V.J.), CellFit COST Action CA16119, Ministry of Education, Youth and Sports, Czech Republic INTER-COST LTC 18059 (P.M.-P., L.T.), Internal Grant Agency of Czech University of Life Sciences in Prague (SV18-08-21230) (P.M.-P., L.T., F.B.).

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Authors and Affiliations

  1. Division of Animal Sciences, University of Missouri, Columbia, MO, 65211, USA

    Michal Zigo, Dalen Zuidema, Karl Kerns & Peter Sutovsky

  2. Laboratory of Reproductive Biology, Institute of Biotechnology of the Czech Academy of Sciences, 25250, Vestec, Czech Republic

    Pavla Maňásková-Postlerová & Věra Jonáková

  3. Department of Veterinary Sciences, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences, 16521, Prague, Czech Republic

    Pavla Maňásková-Postlerová, Lucie Tůmová & Filipa Bubeníčková

  4. Department of Obstetrics, Gynecology & Women’s Health, University of Missouri, Columbia, MO, 65211, USA

    Peter Sutovsky

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Zigo, M., Maňásková-Postlerová, P., Zuidema, D. et al. Porcine model for the study of sperm capacitation, fertilization and male fertility. Cell Tissue Res 380, 237–262 (2020). https://doi.org/10.1007/s00441-020-03181-1

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