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Signaling-Mediated Control of Cell Division pp 213–239Cite as

Oocyte Activation and Fertilisation: Crucial Contributors from the Sperm and Oocyte

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Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 59))

Abstract

This chapter intends to summarise the importance of sperm- and oocyte-derived factors in the processes of sperm–oocyte binding and oocyte activation. First, we describe the initial interaction between sperm and the zona pellucida, with particular regard to acrosome exocytosis. We then describe how sperm and oocyte membranes fuse, with special reference to the discovery of the sperm protein IZUMO1 and its interaction with the oocyte membrane receptor JUNO. We then focus specifically upon oocyte activation, the fundamental process by which the oocyte is alleviated from metaphase II arrest by a sperm-soluble factor. The identity of this sperm factor has been the source of much debate recently, although mounting evidence, from several different laboratories, provides strong support for phospholipase C ζ (PLCζ), a sperm-specific phospholipase. Herein, we discuss the evidence in support of PLCζ and evaluate the potential role of other candidate proteins, such as post-acrosomal WW-binding domain protein (PAWP/WBP2NL). Since the cascade of downstream events triggered by the sperm-borne oocyte activation factor heavily relies upon specialised cellular machinery within the oocyte, we also discuss the critical role of oocyte-borne factors, such as the inositol trisphosphate receptor (IP3R), protein kinase C (PKC), store-operated calcium entry (SOCE) and calcium/calmodulin-dependent protein kinase II (CaMKII), during the process of oocyte activation. In order to place the implications of these various factors and processes into a clinical context, we proceed to describe their potential association with oocyte activation failure and discuss how clinical techniques such as the in vitro maturation of oocytes may affect oocyte activation ability. Finally, we contemplate the role of artificial oocyte activating agents in the clinical rescue of oocyte activation deficiency and discuss options for more endogenous alternatives.

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References

  • Aarabi M, Balakier H, Bashar S, Moskovtsev SI, Sutovsky P, Librach CL, Oko R (2014a) Sperm-derived WW domain-binding protein, PAWP, elicits calcium oscillations and oocyte activation in humans and mice. FASEB J 28:4434–4440

    Article  CAS  PubMed  Google Scholar 

  • Aarabi M, Balakier H, Bashar S, Moskovtsev SI, Sutovsky P, Librach CL, Oko R (2014b) Sperm content of postacrosomal WW binding protein is related to fertilization outcomes in patients undergoing assisted reproductive technology. Fertil Steril 102:440–447

    Article  CAS  PubMed  Google Scholar 

  • Abi Nahed R, Martinez G, Escoffier J, Yassine S, Karaouzène T, Hograindleur JP, Turk J, Kokotos G, Ray PF, Bottari S, Lambeau G, Hennebicq S, Arnoult C (2016) Progesterone-induced acrosome exocytosis requires sequential involvement of calcium-independent phospholipase A2β (iPLA2β) and group X secreted phospholipase A2 (sPLA2). J Biol Chem 291:3076–3089

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Amdani SN, Yeste M, Jones C, Coward K (2015) Sperm factors and oocyte activation: current controversies and considerations. Biol Reprod 93:50. doi:10.1095/biolreprod.115.130609

    Article  PubMed  CAS  Google Scholar 

  • Amdani SN, Yeste M, Jones C, Coward K (2016) Phospholipase C zeta (PLCζ) and male infertility: clinical update and topical developments. Adv Biol Regul 61:58–67. doi:10.1016/j.jbior.2015.11.009

    Article  CAS  PubMed  Google Scholar 

  • Baluch DP, Koeneman BA, Hatch KR, McGaughey RW, Capco DG (2004) PKC isotypes in post-activated and fertilized mouse eggs: association with the meiotic spindle. Dev Biol 274:45–55

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Beck-Fruchter R, Lavee M, Weiss A, Geslevich Y, Shalev E (2014) Rescue intracytoplasmic sperm injection: a systematic review. Fertil Steril 101:690–698

    Article  PubMed  Google Scholar 

  • Bhanumathy C, da Fonseca PC, Morris EP, Joseph SK (2012) Identification of functionally critical residues in the channel domain of inositol trisphosphate receptors. J Biol Chem 287:43674–43684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhattacharya S, Maheshwari A, Mollison J (2013) Factors associated with failed treatment: an analysis of 121,744 women embarking on their first IVF cycles. PLoS One 8:e82249. doi:10.1371/journal.pone.0082249

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bianchi E, Wright GJ (2015) Cross-species fertilization: the hamster egg receptor, Juno, binds the human sperm ligand, Izumo1. Philos Trans R Soc Lond B Biol Sci 370:20140101. doi:10.1098/rstb.2014.0101

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bromfield E, Aitken RJ, Nixon B (2015) Novel characterization of the HSPA2-stabilizing protein BAG6 in human spermatozoa. Mol Hum Reprod 21:755–769

    Article  PubMed  Google Scholar 

  • Buffone MG, Hirohashi N, Gerton GL (2014) Unresolved questions concerning mammalian sperm acrosomal exocytosis. Biol Reprod 90:112. doi:10.1095/biolreprod.114.117911

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Busso D, Cohen DJ, Hayashi M, Kasahara M, Cuasnicú PS (2005) Human testicular protein TPX1/CRISP-2: localization in spermatozoa, fate after capacitation and relevance for gamete interaction. Mol Hum Reprod 11:299–305

    Article  CAS  PubMed  Google Scholar 

  • Busso D, Cohen DJ, Maldera JA, Dematteis A, Cuasnicu PS (2007) A novel function for CRISP1 in rodent fertilization: involvement in sperm-zona pellucida interaction. Biol Reprod 77:848–854

    Article  CAS  PubMed  Google Scholar 

  • Chen Q, Zhang W, Ran H, Feng L, Yan H, Mu X, Han Y, Liu W, Xia G, Wang C (2014) PKCδ and θ possibly mediate FSH-induced mouse oocyte maturation via NOX-ROS-TACE cascade signaling pathway. PLoS One 9:e111423. doi:10.1371/journal.pone.0111423

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cheon B, Lee HC, Wakai T, Fissore RA (2013) Ca2+ influx and the store-operated Ca2+ entry pathway undergo regulation during mouse oocyte maturation. Mol Biol Cell 24:1396–1410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chian RC, Uzelac PS, Nargund G (2013) In vitro maturation of human immature oocytes for fertility preservation. Fertil Steril 99:1173–1181

    Article  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 65:1000–1005

    Article  CAS  PubMed  Google Scholar 

  • Cohen DJ, Maldera JA, Vasen G, Ernesto JI, Muñoz MW, Battistone MA, Cuasnicú PS (2011) Epididymal protein CRISP1 plays different roles during the fertilization process. J Androl 32:672–678

    Article  CAS  PubMed  Google Scholar 

  • Combelles CM, Cekleniak NA, Racowsky C, Albertini DF (2002) Assessment of nuclear and cytoplasmic maturation in in-vitro matured human oocytes. Hum Reprod 17:1006–1016

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cooney MA, Malcuit C, Cheon B, Holland MK, Fissore RA, D’Cruz NT (2010) Species-specific differences in the activity and nuclear localization of murine and bovine phospholipase C zeta 1. Biol Reprod 83:92–101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cox LJ, Larman MG, Saunders CM, Hashimoto K, Swann K, Lai FA (2002) Sperm phospholipase Czeta from humans and cynomolgus monkeys triggers Ca2+ oscillations, activation and development of mouse oocytes. Reproduction 124:611–623

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Dale B, Wilding M, Coppola G, Tosti E (2010) How do spermatozoa activate oocytes? Reprod Biomed Online 21:1–3

    Article  PubMed  Google Scholar 

  • De Vincentiis S, De Martino E, Buffone MG, Brugo-Olmedo S (2013) Use of metaphase I oocytes matured in vitro is associated with embryo multinucleation. Fertil Steril 99:414–421

    Article  PubMed  Google Scholar 

  • Deemeh MR, Tavalaee M, Nasr-Esfahani MH (2014) Health of children born through artificial oocyte activation: a pilot study. Reprod Sci 22:322–328

    Article  PubMed  CAS  Google Scholar 

  • DeSouza N, Reiken S, Ondrias K, Yang YM, Matkovich S, Marks AR (2002) Protein kinase A and two phosphatases are components of the inositol 1,4,5-trisphosphate receptor macromolecular signaling complex. J Biol Chem 277:39397–39400

    Article  CAS  PubMed  Google Scholar 

  • Dietzel E, Wessling J, Floehr J, Schäfer C, Ensslen S, Denecke B, Rösing B, Neulen J, Veitinger T, Spehr M, Tropartz T, Tolba R, Renné T, Egert A, Schorle H, Gottenbusch Y, Hildebrand A, Yiallouros I, Stöcker W, Weiskirchen R, Jahnen-Dechent W (2013) Fetuin-B, a liver-derived plasma protein is essential for fertilization. Dev Cell 25:106–112

    Article  CAS  PubMed  Google Scholar 

  • Ducibella T, Schultz RM, Ozil JP (2006) Role of calcium signals in early development. Semin Cell Dev Biol 17:324–332

    Article  CAS  PubMed  Google Scholar 

  • Ebner T, Köster M, Shebl O, Moser M, Van der Ven H, Tews G, Montag M (2012) Application of a ready-to-use calcium ionophore increases rates of fertilization and pregnancy in severe male factor infertility. Fertil Steril 98:1432–1437

    Article  CAS  PubMed  Google Scholar 

  • Ebner T, Montag M, Oocyte Activation Study Group, Montag M, Van der Ven K, Van der Ven H, Ebner T, Shebl O, Oppelt P, Hirchenhain J, Krüssel J, Maxrath B, Gnoth C, Friol K, Tigges J, Wünsch E, Luckhaus J, Beerkotte A, Weiss D, Grunwald K, Struller D, Etien C (2015) Live birth after artificial oocyte activation using a ready-to-use ionophore: a prospective multicentre study. Reprod Biomed Online 30:359–365

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Eliyahu E, Tsaadon A, Shtraizent N, Shalgi R (2005) The involvement of protein kinase C and actin filaments in cortical granule exocytosis in the rat. Reproduction 129:161–170

    Article  CAS  PubMed  Google Scholar 

  • Eliyahu E, Shtraizent N, Tsaadon A, Shalgi R (2006) Association between myristoylated alanin-rich C kinase substrate (MARCKS) translocation and cortical granule exocytosis in rat eggs. Reproduction 131:221–231

    Article  CAS  PubMed  Google Scholar 

  • Escoffier J, Lee HC, Yassine S, Zouari R, Martinez G, Karaouzène T, Coutton C, Kherraf ZE, Halouani L, Triki C, Nef S, Thierry-Mieg N, Savinov SN, Fissore R, Ray PF, Arnoult C (2016) Homozygous mutation of PLCZ1 leads to defective human oocyte activation and infertility that is not rescued by the WW-binding protein PAWP. Hum Mol Genet 25:878–891

    Article  CAS  PubMed  Google Scholar 

  • Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel SH, Tanasa B, Hogan PG, Lewis RS, Daly M, Rao A (2006) A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441:179–185

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gallicano GI, McGaughey RW, Capco DG (1997) Activation of protein kinase C after fertilization is required for remodeling the mouse egg into the zygote. Mol Reprod Dev 46:587–601

    Article  CAS  PubMed  Google Scholar 

  • Gao Z, Garbers DL (1998) Species diversity in the structure of zonadhesin, a sperm-specific membrane protein containing multiple cell adhesion molecule-like domains. J Biol Chem 273:3415–3421

    Article  CAS  PubMed  Google Scholar 

  • Gasca S, Reyftmann L, Pellestor F, Rème T, Assou S, Anahory T, Dechaud H, Klein B, De Vos J, Hamamah S (2008) Total fertilization failure and molecular abnormalities in metaphase II oocytes. Reprod Biomed Online 17:772–781

    Article  CAS  PubMed  Google Scholar 

  • Goud PT, Goud AP, Van Oostveldt P, Dhont M (1999) Presence and dynamic redistribution of type I inositol 1,4,5-trisphosphate receptors in human oocytes and embryos during in-vitro maturation, fertilization and early cleavage divisions. Mol Hum Reprod 5:441–451

    Article  CAS  PubMed  Google Scholar 

  • Goudet G, Mugnier S, Callebaut I, Monget P (2008) Phylogenetic analysis and identification of pseudogenes reveal a progressive loss of zona pellucida genes during evolution of vertebrates. Biol Reprod 78:796–806

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Grøndahl ML, Borup R, Vikeså J, Ernst E, Andersen CY, Lykke-Hartmann K (2013) The dormant and the fully competent oocyte: comparing the transcriptome of human oocytes from primordial follicles and in metaphase II. Mol Hum Reprod 19:600–617

    Article  PubMed  CAS  Google Scholar 

  • Gudlur A, Quintana A, Zhou Y, Hirve N, Mahapatra S, Hogan PG (2014) STIM1 triggers a gating rearrangement at the extracellular mouth of the ORAI1 channel. Nat Commun 5:5164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta SK (2014) Unraveling the intricacies of mammalian fertilization. Asian J Androl 16:801–802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta SK (2015) Role of zona pellucida glycoproteins during fertilization in humans. J Reprod Immunol 108:90–97

    Article  CAS  PubMed  Google Scholar 

  • Gupta SK, Bhandari B, Shrestha A, Biswal BK, Palaniappan C, Malhotra SS, Gupta N (2012) Mammalian zona pellucida glycoproteins: structure and function during fertilization. Cell Tissue Res 349:665–678

    Article  CAS  PubMed  Google Scholar 

  • Halet G, Tunwell R, Parkinson SJ, Carroll J (2004) Conventional PKCs regulate the temporal pattern of Ca2+ oscillations at fertilization in mouse eggs. J Cell Biol 164:1033–1044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harada Y, Matsumoto T, Hirahara S, Nakashima A, Ueno S, Oda S, Miyazaki S, Iwao Y (2007) Characterization of a sperm factor for egg activation at fertilization of the newt Cynops pyrrhogaster. Dev Biol 306:797–808

    Article  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 4:361–393

    Article  CAS  PubMed  Google Scholar 

  • Heindryckx B, Van der Elst J, De Sutter P, Dhont M (2005) Treatment option for sperm- or oocyte-related fertilization failure: assisted oocyte activation following diagnostic heterologous ICSI. Hum Reprod 20:2237–2241

    Article  CAS  PubMed  Google Scholar 

  • Heindryckx B, De Gheselle S, Gerris J, Dhont M, De Sutter P (2008) Efficiency of assisted oocyte activation as a solution for failed intracytoplasmic sperm injection. Reprod Biomed Online 17:662–668

    Article  PubMed  Google Scholar 

  • Heytens E, Parrington J, Coward K, Young C, Lambrecht S, Yoon SY, Fissore RA, Hamer R, Deane CM, Ruas M, Grasa P, Soleimani R, Cuvelier CA, Gerris J, Dhont M, Deforce D, Leybaert L, De Sutter P (2009) Reduced amounts and abnormal forms of phospholipase C zeta (PLCzeta) in spermatozoa from infertile men. Hum Reprod 24:2417–2428

    Article  CAS  PubMed  Google Scholar 

  • Heytens E, Schmitt-John T, Moser JM, Jensen NM, Soleimani R, Young C, Coward K, Parrington J, De Sutter P (2010) Reduced fertilization after ICSI and abnormal phospholipase C zeta presence in spermatozoa from the wobbler mouse. Reprod Biomed Online 21:742–749

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Horner VL, Wolfner MF (2008) Transitioning from egg to embryo: triggers and mechanisms of egg activation. Dev Dyn 237:527–544

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Inoue N, Hamada D, Kamikubo H, Hirata K, Kataoka M, Yamamoto M, Ikawa M, Okabe M, Hagihara Y (2013) Molecular dissection of IZUMO1, a sperm protein essential for sperm-egg fusion. Development 140:3221–3229

    Article  CAS  PubMed  Google Scholar 

  • Inoue N, Hagihara Y, Wright D, Suzuki T, Wada I (2015) Oocyte-triggered dimerization of sperm IZUMO1 promotes sperm-egg fusion in mice. Nat Commun 6:8858. doi:10.1038/ncomms9858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Johnson MH (2011) Robert Edwards: the path to IVF. Reprod Biomed Online 23:245–262

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones KT (2007) Intracellular calcium in the fertilization and development of mammalian eggs. Clin Exp Pharmacol Physiol 34:1084–1089

    Article  CAS  PubMed  Google Scholar 

  • Jones KT, Soeller C, Cannell MB (1998) The passage of Ca2+ and fluorescent markers between the sperm and egg after fusion in the mouse. Development 125:4627–4635

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kashir J, Heindryckx B, Jones C, De Sutter P, Parrington J, Coward K (2010) Oocyte activation, phospholipase C zeta and human infertility. Hum Reprod Update 16:690–703

    Article  CAS  PubMed  Google Scholar 

  • Kashir J, Jones C, Lee HC, Rietdorf K, Nikiforaki D, Durrans C, Ruas M, Tee ST, Heindryckx B, Galione A, De Sutter P, Fissore RA, Parrington J, Coward K (2011) Loss of activity mutations in phospholipase C zeta (PLCζ) abolishes calcium oscillatory ability of human recombinant protein in mouse oocytes. Hum Reprod 26:3372–3387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kashir J, Konstantinidis M, Jones C, Heindryckx B, De Sutter P, Parrington J, Wells D, Coward K (2012a) Characterization of two heterozygous mutations of the oocyte activation factor phospholipase C zeta (PLCζ) from an infertile man by use of minisequencing of individual sperm and expression in somatic cells. Fertil Steril 98:423–431

    Article  CAS  PubMed  Google Scholar 

  • Kashir J, Konstantinidis M, Jones C, Lemmon B, Lee HC, Hamer R, Heindryckx B, Deane CM, De Sutter P, Fissore RA, Parrington J, Wells D, Coward K (2012b) A maternally inherited autosomal point mutation in human phospholipase C zeta (PLCζ) leads to male infertility. Hum Reprod 27:222–231

    Article  CAS  PubMed  Google Scholar 

  • Kashir J, Deguchi R, Jones C, Coward K, Stricker SA (2013) Comparative biology of sperm factors and fertilization-induced calcium signals across the animal kingdom. Mol Reprod Dev 80:787–815

    Article  CAS  PubMed  Google Scholar 

  • Kasri NN, Török K, Galione A, Garnham C, Callewaert G, Missiaen L, Parys JB, De Smedt H (2006) Endogenously bound calmodulin is essential for the function of the inositol 1,4,5-trisphosphate receptor. J Biol Chem 281:8332–8338

    Article  CAS  PubMed  Google Scholar 

  • Kennedy CE, Krieger KB, Sutovsky M, Xu W, Vargovič P, Didion BA, Ellersieck MR, Hennessy ME, Verstegen J, Oko R, Sutovsky P (2014) Protein expression pattern of PAWP in bull spermatozoa is associated with sperm quality and fertility following artificial insemination. Mol Reprod Dev 81:436–449

    Article  CAS  PubMed  Google Scholar 

  • Kilani S, Chapman MG (2014) Meiotic spindle normality predicts live birth in patients with recurrent in vitro fertilization failure. Fertil Steril 101:403–406

    Article  PubMed  Google Scholar 

  • Kim JW, Yang SH, Yoon SH, Kim SD, Jung JH, Lim JH (2015) Successful pregnancy and delivery after ICSI with artificial oocyte activation by calcium ionophore in in-vitro matured oocytes: a case report. Reprod Biomed Online 30:373–377

    Article  PubMed  Google Scholar 

  • Kline D, Kline JT (1992) Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg. Dev Biol 149:80–89

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Knott JG, Gardner AJ, Madgwick S, Jones KT, Williams CJ, Schultz RM (2006) Calmodulin-dependent protein kinase II triggers mouse egg activation and embryo development in the absence of Ca2+ oscillations. Dev Biol 296:388–395

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  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 411:172–182

    Article  PubMed  CAS  Google Scholar 

  • Lee B, Yoon SY, Malcuit C, Parys JB, Fissore RA (2010) Inositol 1,4,5-trisphosphate receptor 1 degradation in mouse eggs and impact on [Ca2+]i oscillations. J Cell Physiol 222:238–247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lefièvre L, Conner SJ, Salpekar A, Olufowobi O, Ashton P, Pavlovic B, Lenton W, Afnan M, Brewis IA, Monk M, Hughes DC, Barratt CL (2004) Four zona pellucida glycoproteins are expressed in the human. Hum Reprod 19:1580–1586

    Article  PubMed  Google Scholar 

  • Li Y, Li RQ, Ou SB, Zhang NF, Ren L, Wei LN, Zhang QX, Yang DZ (2014) Increased GDF9 and BMP15 mRNA levels in cumulus granulosa cells correlate with oocyte maturation, fertilization, and embryo quality in humans. Reprod Biol Endocrinol 12:81. doi:10.1186/1477-7827-12-81

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Louis JF, Thoma ME, Sørensen DN, McLain AC, King RB, Sundaram R, Keiding N, Buck Louis GM (2013) The prevalence of couple infertility in the United States from a male perspective: evidence from a nationally representative sample. Andrology 1:741–748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luria A, Tennenbaum T, Sun QY, Rubinstein S, Breitbart H (2000) Differential localization of conventional protein kinase C isoforms during mouse oocyte development. Biol Reprod 62:1564–1570

    Article  CAS  PubMed  Google Scholar 

  • Machaca K (2007) Ca2+ signaling differentiation during oocyte maturation. J Cell Physiol 213:331–340

    Article  CAS  PubMed  Google Scholar 

  • Madgwick S, Levasseur M, Jones KT (2005) Calmodulin-dependent protein kinase II, and not protein kinase C, is sufficient for triggering cell-cycle resumption in mammalian eggs. J Cell Sci 118:3849–3859

    Article  CAS  PubMed  Google Scholar 

  • Mahutte NG, Arici A (2003) Failed fertilization: is it predictable? Curr Opin Obstet Gynecol 15:211–218

    Article  PubMed  Google Scholar 

  • Malcuit C, Knott JG, He C, Wainwright T, Parys JB, Robl JM, Fissore RA (2005) Fertilization and inositol 1,4,5-trisphosphate (IP3)-induced calcium release in type-1 inositol 1,4,5-trisphosphate receptor down-regulated bovine eggs. Biol Reprod 73:2–13

    Article  CAS  PubMed  Google Scholar 

  • Maldera JA, Weigel Muñoz M, Chirinos M, Busso D, GE Raffo F, Battistone MA, Blaquier JA, Larrea F, Cuasnicu PS (2014) Human fertilization: epididymal hCRISP1 mediates sperm-zona pellucida binding through its interaction with ZP3. Mol Hum Reprod 20:341–349

    Google Scholar 

  • Mao HT, Yang WX (2013) Modes of acrosin functioning during fertilization. Gene 526:75–79

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Miyara F, Aubriot FX, Glissant A, Nathan C, Douard S, Stanovici A, Herve F, Dumont-Hassan M, LeMeur A, Cohen-Bacrie P, Debey P (2003) Multiparameter analysis of human oocytes at metaphase II stage after IVF failure in non-male infertility. Hum Reprod 18:1494–1503

    Article  PubMed  Google Scholar 

  • Montag M, Köster M, van der Ven K, Bohlen U, van der Ven H (2012) The benefit of artificial oocyte activation is dependent on the fertilization rate in a previous treatment cycle. Reprod Biomed Online 24:521–526

    Article  PubMed  Google Scholar 

  • Moor RM, Dai Y, Lee C, Fulka J Jr (1998) Oocyte maturation and embryonic failure. Hum Reprod Update 4:223–236

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Munuce MJ, Quintero I, Caille AM, Ghersevich S, Berta CL (2006) Comparative concentrations of steroid hormones and proteins in human peri-ovulatory peritoneal and follicular fluids. Reprod Biomed Online 13:202–207

    Article  CAS  PubMed  Google Scholar 

  • Nasr-Esfahani MH, Deemeh MR, Tavalaee M (2010) Artificial oocyte activation and intracytoplasmic sperm injection. Fertil Steril 94:520–526

    Article  PubMed  Google Scholar 

  • Neri QV, Lee B, Rosenwaks Z, Machaca K, Palermo GD (2014) Understanding fertilization through intracytoplasmic sperm injection (ICSI). Cell Calcium 55:24–37

    Article  CAS  PubMed  Google Scholar 

  • Nikiforaki D, Vanden Meerschaut F, Qian C, De Croo I, Lu Y, Deroo T, Van den Abbeel E, Heindryckx B, De Sutter P (2014) Oocyte cryopreservation and in vitro culture affect calcium signalling during human fertilization. Hum Reprod 29:29–40

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nomikos M, Elgmati K, Theodoridou M, Calver BL, Cumbes B, Nounesis G, Swann K, Lai FA (2011a) Male infertility-linked point mutation disrupts the Ca2+ oscillation-inducing and PIP2 hydrolysis activity of sperm PLCζ. Biochem J 434:211–217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nomikos M, Elgmati K, Theodoridou M, Georgilis A, Gonzalez-Garcia JR, Nounesis G, Swann K, Lai FA (2011b) Novel regulation of PLCζ activity via its XY-linker. Biochem J 438:427–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nomikos M, Sanders JR, Theodoridou M, Kashir J, Matthews E, Nounesis G, Lai FA, Swann K (2014) Sperm-specific post-acrosomal WW-domain binding protein (PAWP) does not cause Ca2+ release in mouse oocytes. Mol Hum Reprod 20:938–947

    Article  PubMed  PubMed Central  Google Scholar 

  • Nomikos M, Sanders JR, Kashir J, Sanusi R, Buntwal L, Love D, Ashley P, Sanders D, Knaggs P, Bunkheila A, Swann K, Lai FA (2015) Functional disparity between human PAWP and PLCζ in the generation of Ca2+ oscillations for oocyte activation. Mol Hum Reprod 21:702–710

    Article  PubMed  Google Scholar 

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

    Chapter  Google Scholar 

  • Ombelet W, Cooke I, Dyer S, Serour G, Devroey P (2008) Infertility and the provision of infertility medical services in developing countries. Hum Reprod Update 14:605–621

    Article  PubMed  PubMed Central  Google Scholar 

  • Ozil JP, Huneau D (2001) Activation of rabbit oocytes: the impact of the Ca2+ signal regime on development. Development 128:917–928

    CAS  PubMed  Google Scholar 

  • Pang PC, Chiu PC, Lee CL, Chang LY, Panico M, Morris HR, Haslam SM, Khoo KH, Clark GF, Yeung WS, Dell A (2011) Human sperm binding is mediated by the sialyl-Lewis(x) oligosaccharide on the zona pellucida. Science 333:1761–1764

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pesty A, Avazeri N, Lefèvre B (1998) Nuclear calcium release by InsP3-receptor channels plays a role in meiosis reinitiation in the mouse oocyte. Cell Calcium 24:239–251

    Article  CAS  PubMed  Google Scholar 

  • Petit FM, Serres C, Bourgeon F, Pineau C, Auer J (2013) Identification of sperm head proteins involved in zona pellucida binding. Hum Reprod 28:852–865

    Article  CAS  PubMed  Google Scholar 

  • Putney JW (2009) Capacitative calcium entry: from concept to molecules. Immunol Rev 231:10–22

    Article  CAS  PubMed  Google Scholar 

  • Putney JW (2011) Origins of the concept of store-operated calcium entry. Front Biosci 3:980–984

    Article  Google Scholar 

  • Roos J, DiGregorio PJ, Yeromin AV, Ohlsen K, Lioudyno M, Zhang S, Safrina O, Kozak JA, Wagner SL, Cahalan MD, Veliçelebi G, Stauderman KA (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol 169:435–445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ross PJ, Beyhan Z, Iager AE, Yoon SY, Malcuit C, Schellander K, Fissore RA, Cibelli JB (2008) Parthenogenetic activation of bovine oocytes using bovine and murine phospholipase C zeta. BMC Dev Biol 8:16. doi:10.1186/1471-213X-8-16

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sabetian S, Shamsir MS, Abu Naser M (2014) Functional features and protein network of human sperm-egg interaction. Syst Biol Reprod Med 60:329–337

    Article  CAS  PubMed  Google Scholar 

  • Saldívar-Hernández A, González-González ME, Sánchez-Tusié A, Maldonado-Rosas I, López P, Treviño CL, Larrea F, Chirinos M (2015) Human sperm degradation of zona pellucida proteins contributes to fertilization. Reprod Biol Endocrinol 13:99

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Satouh Y, Nozawa K, Ikawa M (2015) Sperm postacrosomal WW domain-binding protein is not required for mouse egg activation. Biol Reprod 93:94

    Article  PubMed  CAS  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 129:3533–3544

    CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sengoku K, Takuma N, Miyamoto T, Horikawa M, Ishikawa M (2004) Integrins are not involved in the process of human sperm-oolemmal fusion. Hum Reprod 19:639–644

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smyth JT, Hwang SY, Tomita T, DeHaven WI, Mercer JC, Putney JW (2010) Activation and regulation of store-operated calcium entry. J Cell Mol Med 14:2337–2349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Son WY, Chung JT, Demirtas E, Holzer H, Sylvestre C, Buckett W, Chian RC, Tan SL (2008) Comparison of in-vitro maturation cycles with and without in-vivo matured oocytes retrieved. Reprod Biomed Online 17:59–67

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Stetson I, Avilés M, Moros C, García-Vázquez FA, Gimeno L, Torrecillas A, Aliaga C, Bernardo-Pisa MV, Ballesta J, Izquierdo-Rico MJ (2015) Four glycoproteins are expressed in the cat zona pellucida. Theriogenology 83:1162–1173

    Article  CAS  PubMed  Google Scholar 

  • Suarez SS, Pacey AA (2006) Sperm transport in the female reproductive tract. Hum Reprod Update 12:23–37

    Article  CAS  PubMed  Google Scholar 

  • Sutovsky P, Manandhar G, Wu A, Oko R (2003) Interactions of sperm perinuclear theca with the oocyte: implications for oocyte activation, anti-polyspermy defense, and assisted reproduction. Microsc Res Tech 61:362–378

    Article  PubMed  Google Scholar 

  • Swann K (1990) A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs. Development 110:1295–1302

    CAS  PubMed  Google Scholar 

  • Swann K, Lai FA (2013) PLCζ and the initiation of Ca(2+) oscillations in fertilizing mammalian eggs. Cell Calcium 53:55–62

    Article  CAS  PubMed  Google Scholar 

  • Swann K, Lai FA (2016) Egg activation at fertilization by a soluble sperm protein. Physiol Rev 96:127–149

    Article  PubMed  Google Scholar 

  • Swann K, Yu Y (2008) The dynamics of calcium oscillations that activate mammalian eggs. Int J Dev Biol 52:585–594

    Article  CAS  PubMed  Google Scholar 

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

    Article  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 17:574–582

    Article  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 17:661–668

    Article  CAS  PubMed  Google Scholar 

  • Taylor SL, Yoon SY, Morshedi MS, Lacey DR, Jellerette T, Fissore RA, Oehninger S (2010) Complete globozoospermia associated with PLCζ deficiency treated with calcium ionophore and ICSI results in pregnancy. Reprod Biomed Online 20:559–564

    Article  CAS  PubMed  Google Scholar 

  • Taylor CW, Tovey SC, Rossi AM, Lopez Sanjurjo CI, Prole DL, Rahman T (2014) Structural organization of signalling to and from IP3 receptors. Biochem Soc Trans 42:63–70

    Article  CAS  PubMed  Google Scholar 

  • Theodoridou M, Nomikos M, Parthimos D, Gonzalez-Garcia JR, Elgmati K, Calver BL, Sideratou Z, Nounesis G, Swann K, Lai FA (2013) Chimeras of sperm PLCζ reveal disparate protein domain functions in the generation of intracellular Ca2+ oscillations in mammalian eggs at fertilization. Mol Hum Reprod 19:852–864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thoma ME, McLain AC, Louis JF, King RB, Trumble AC, Sundaram R, Buck Louis GM (2013) Prevalence of infertility in the United States as estimated by the current duration approach and a traditional constructed approach. Fertil Steril 99:1324–1331

    Article  PubMed  PubMed Central  Google Scholar 

  • Thompson P (2015) HFEA response to ‘A plea for caution and more research in the “experimental” use of ionophores in ICSI’. Reprod Biomed Online 31:829–830

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Toshimori K, Saxena DK, Tanii I, Yoshinaga K (1998) An MN9 antigenic molecule, equatorin, is required for successful sperm-oocyte fusion in mice. Biol Reprod 59:22–29

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Tsaadon L, Kaplan-Kraicer R, Shalgi R (2008) Myristoylated alanine-rich C kinase substrate, but not Ca2+/calmodulin-dependent protein kinase II, is the mediator in cortical granules exocytosis. Reproduction 135:613–624

    Article  CAS  PubMed  Google Scholar 

  • Ullah G, Jung P, Machaca K (2007) Modeling Ca2+ signaling differentiation during oocyte maturation. Cell Calcium 42:556–564

    Article  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 79:1129–1134

    Article  CAS  PubMed  Google Scholar 

  • Van Blerkom J, Cohen J, Johnson M (2015) A plea for caution and more research in the ‘experimental’ use of ionophores in ICSI. Reprod Biomed Online 30:323–324

    Article  PubMed  Google Scholar 

  • Vanden Meerschaut F, Leybaert L, Nikiforaki D, Qian C, Heindryckx B, De Sutter P (2013) Diagnostic and prognostic value of calcium oscillatory pattern analysis for patients with ICSI fertilization failure. Hum Reprod 28:87–98

    Article  CAS  PubMed  Google Scholar 

  • Vanden Meerschaut F, Nikiforaki D, Heindryckx B, De Sutter P (2014a) Assisted oocyte activation following ICSI fertilization failure. Reprod Biomed Online 28:560–571

    Article  PubMed  Google Scholar 

  • Vanden Meerschaut F, D’Haeseleer E, Gysels H, Thienpont Y, Dewitte G, Heindryckx B, Oostra A, Roeyers H, Van Lierde K, De Sutter P (2014b) Neonatal and neurodevelopmental outcome of children aged 3-10 years born following assisted oocyte activation. Reprod Biomed Online 28:54–63

    Article  PubMed  Google Scholar 

  • Vanderheyden V, Wakai T, Bultynck G, De Smedt H, Parys JB, Fissore RA (2009) Regulation of inositol 1,4,5-trisphosphate receptor type 1 function during oocyte maturation by MPM-2 phosphorylation. Cell Calcium 46:56–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verbert L, Lee B, Kocks SL, Assefa Z, Parys JB, Missiaen L, Callewaert G, Fissore RA, De Smedt H, Bultynck G (2008) Caspase-3-truncated type 1 inositol 1,4,5-trisphosphate receptor enhances intracellular Ca2+ leak and disturbs Ca2+ signalling. Biol Cell 100:39–49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Von Stetina JR, Orr-Weaver TL (2011) Developmental control of oocyte maturation and egg activation in metazoan models. Cold Spring Harb Perspect Biol 3:a005553

    Google Scholar 

  • Wakai T, Zhang N, Vangheluwe P, Fissore RA (2013) Regulation of endoplasmic reticulum Ca(2+) oscillations in mammalian eggs. J Cell Sci 126:5714–5724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, Machaty Z (2013) Calcium influx in mammalian eggs. Reproduction 145:97–105

    Article  CAS  Google Scholar 

  • Wang C, Lee K, Gajdócsi E, Papp AB, Machaty Z (2012) Orai1 mediates store-operated Ca2+ entry during fertilization in mammalian oocytes. Dev Biol 365:414–423

    Article  CAS  PubMed  Google Scholar 

  • Williams CJ, Mehlmann LM, Jaffe LA, Kopf GS, Schultz RM (1998) Evidence that Gq family G proteins do not function in mouse egg activation at fertilization. Dev Biol 198:116–127

    CAS  PubMed  Google Scholar 

  • Williams CJ (2002) Signaling mechanisms of mammalian oocyte activation. Hum Reprod Update 8:313–321

    Article  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 (2007a) PAWP, a sperm-specific WW domain-binding protein, promotes meiotic resumption and pronuclear development during fertilization. J Biol Chem 282:12164–12175

    Article  CAS  PubMed  Google Scholar 

  • Wu AT, Sutovsky P, Xu W, van der Spoel AC, Platt FM, Oko R (2007b) The postacrosomal assembly of sperm head protein, PAWP, is independent of acrosome formation and dependent on microtubular manchette transport. Dev Biol 312:471–483

    Article  CAS  PubMed  Google Scholar 

  • Yanagida K, Fujikura Y, Katayose H (2008) The present status of artificial oocyte activation in assisted reproductive technology. Reprod Med Biol 7:133–142

    Article  Google Scholar 

  • Yanagimachi R (1998) Intracytoplasmic sperm injection experiments using the mouse as a model. Hum Reprod 13(Suppl 1):87–98

    Article  PubMed  Google Scholar 

  • Yang YR, Follo MY, Cocco L, Suh PG (2013) The physiological roles of primary phospholipase C. Adv Biol Regul 53:232–241

    Article  CAS  PubMed  Google Scholar 

  • Yassine S, Escoffier J, Martinez G, Coutton C, Karaouzène T, Zouari R, Ravanat JL, Metzler-Guillemain C, Lee HC, Fissore R, Hennebicq S, Ray PF, Arnoult C (2015) Dpy19l2-deficient globozoospermic sperm display altered genome packaging and DNA damage that compromises the initiation of embryo development. Mol Hum Reprod 21:169–185

    Article  PubMed  Google Scholar 

  • Yelumalai S, Yeste M, Jones C, Amdani SN, Kashir J, Mounce G, Fatum M, Barratt C, McVeigh E, Coward K (2015) Total levels and proportions of sperm exhibiting phospholipase C Zeta (PLCζ) are significantly correlated with fertilization rates following intracytoplasmic sperm injection. Fertil Steril 104:561–568

    Article  CAS  PubMed  Google Scholar 

  • Yeste M (2013a) Boar spermatozoa within the oviductal environment (III): fertilisation. In: Bonet S, Casas I, Holt WV, Yeste M (eds) Boar reproduction: fundamentals and new biotechnological trends. Springer, Berlin, pp 343–406

    Google Scholar 

  • Yeste M (2013b) Boar spermatozoa within the oviductal environment (II): sperm capacitation. In: Bonet S, Casas I, Holt WV, Yeste M (eds) Boar reproduction: fundamentals and new biotechnological trends. Springer, Berlin, pp 281–342

    Google Scholar 

  • Yeste M, Jones C, Amdani SN, Patel S, Coward K (2016) Oocyte activation deficiency: a role for an oocyte contribution? Hum Reprod Update 22:23–47

    Article  PubMed  Google Scholar 

  • Yoneda A, Kashima M, Yoshida S, Terada K, Nakagawa S, Sakamoto A, Hayakawa K, Suzuki K, Ueda J, Watanabe T (2006) Molecular cloning, testicular postnatal expression, and oocyte-activating potential of porcine phospholipase Czeta. Reproduction 132:393–401

    Article  CAS  PubMed  Google Scholar 

  • Yoon SY, Jellerette T, Salicioni AM, Lee HC, Yoo MS, Coward K, Parrington J, Grow D, Cibelli JB, Visconti PE, Mager J, Fissore RA (2008) Human sperm devoid of PLC, zeta 1 fail to induce Ca(2+) release and are unable to initiate the first step of embryo development. J Clin Invest 118:3671–3681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon SY, Eum JH, Lee JE, Lee HC, Kim YS, Han JE, Won HJ, Park SH, Shim SH, Lee WS, Fissore RA, Lee DR, Yoon TK (2012) Recombinant human phospholipase C zeta 1 induces intracellular calcium oscillations and oocyte activation in mouse and human oocytes. Hum Reprod 27:1768–1780

    Article  CAS  PubMed  Google Scholar 

  • Young C, Grasa P, Coward K, Davis LC, Parrington J (2009) Phospholipase C zeta undergoes dynamic changes in its pattern of localization in sperm during capacitation and the acrosome reaction. Fertil Steril 91:2230–2242

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Halet G, Lai FA, Swann K (2008) Regulation of diacylglycerol production and protein kinase C stimulation during sperm- and PLCzeta-mediated mouse egg activation. Biol Cell 100:633–643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu Y, Nomikos M, Theodoridou M, Nounesis G, Lai FA, Swann K (2012) PLCζ causes Ca(2+) oscillations in mouse eggs by targeting intracellular and not plasma membrane PI(4,5)P(2). Mol Biol Cell 23:371–380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zhang SL, Yu Y, Roos J, Kozak JA, Deerinck TJ, Ellisman MH, Stauderman KA, Cahalan MD (2005) STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 437:902–905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors’ Contribution

M.Y. wrote the chapter. C.J., S.N.A. and K.C. critically revised the chapter and approved the final version.Funding M.Y. was funded by the European Commission, FP7-People Programme, Marie Curie-IEF (Grant Number: 626061). S.N.A. is funded by the Ministry of Education (Brunei Darussalam) and the Chancellor’s Scholarship, Universiti Brunei Darussalam.Conflict of Interest The authors declare that there is no conflict of interest in regards to the contents of this chapter.

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  1. Unit of Cell Biology, Department of Biology, Faculty of Sciences, University of Girona, C/ Maria Aurèlia Campany, 69, Campus Montilivi, E-17071, Girona, Spain

    Marc Yeste

  2. Nuffield Department of Obstetrics and Gynaecology, University of Oxford, Level 3, Women’s Centre, John Radcliffe Hospital, Headington, Oxford, UK

    Marc Yeste, Celine Jones, Siti Nornadhirah Amdani & Kevin Coward

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  1. Dept. of Genetics, Genes & Dev. Program, UT MD Anderson Cancer Center, Houston, Texas, USA

    Swathi Arur

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Yeste, M., Jones, C., Amdani, S.N., Coward, K. (2017). Oocyte Activation and Fertilisation: Crucial Contributors from the Sperm and Oocyte. In: Arur, S. (eds) Signaling-Mediated Control of Cell Division . Results and Problems in Cell Differentiation, vol 59. Springer, Cham. https://doi.org/10.1007/978-3-319-44820-6_8

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