Perfect date-the review of current research into molecular bases of mammalian fertilization

. 2020 Feb ; 37 (2) : 243-256. [epub] 20200106

Jazyk angličtina Země Nizozemsko Médium print-electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid31909446

Grantová podpora
19-14990Y Grantová Agentura České Republiky
Medicine 2017 Neuron Fund for Support of Science

Odkazy

PubMed 31909446
PubMed Central PMC7056734
DOI 10.1007/s10815-019-01679-4
PII: 10.1007/s10815-019-01679-4
Knihovny.cz E-zdroje

Fertilization is a multistep process during which two terminally differentiated haploid cells, an egg and a sperm, combine to produce a totipotent diploid zygote. In the early 1950s, it became possible to fertilize mammalian eggs in vitro and study the sequence of cellular and molecular events leading to embryo development. Despite all the achievements of assisted reproduction in the last four decades, remarkably little is known about the molecular aspects of human conception. Current fertility research in animal models is casting more light on the complexity of the process all our lives start with. This review article provides an update on the investigation of mammalian fertilization and highlights the practical implications of scientific discoveries in the context of human reproduction and reproductive medicine.

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Sakkas D, Ramalingam M, Garrido N, Barratt CL. Sperm selection in natural conception: what can we learn from Mother Nature to improve assisted reproduction outcomes? Hum Reprod Update. 2015;21(6):711–726. PubMed PMC

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

Puga Molina LC, Luque GM, Balestrini PA, Marin-Briggiler CI, Romarowski A, Buffone MG. Molecular basis of human sperm capacitation. Front Cell Dev Biol. 2018;6:72. PubMed PMC

Suarez SS. Formation of a Reservoir of Sperm in the Oviduct. Reproduction in Domestic Animals. 2002;37(3):140–143. PubMed

Wang Shang, Larina Irina V. In vivo three-dimensional tracking of sperm behaviors in the mouse oviduct. Development. 2018;145(6):dev157685. PubMed PMC

Bannai H, Yoshimura M, Takahashi K, Shingyoji C. Calcium regulation of microtubule sliding in reactivated sea urchin sperm flagella. J Cell Sci. 2000;113(Pt 5):831–839. PubMed

Ho HC, Granish KA, Suarez SS. Hyperactivated motility of bull sperm is triggered at the axoneme by Ca2+ and not cAMP. Dev Biol. 2002;250(1):208–217. PubMed

Carlson AE, Westenbroek RE, Quill T, et al. CatSper1 required for evoked Ca2+ entry and control of flagellar function in sperm. Proc Natl Acad Sci U S A. 2003;100(25):14864–14868. PubMed PMC

Kirichok Y, Navarro B, Clapham DE. Whole-cell patch-clamp measurements of spermatozoa reveal an alkaline-activated Ca2+ channel. Nature. 2006;439(7077):737–740. PubMed

Chung JJ, Miki K, Kim D, et al. CatSperzeta regulates the structural continuity of sperm Ca(2+) signaling domains and is required for normal fertility. elife. 2017;6:e23082.https://elifesciences.org/articles/23082 PubMed PMC

Qi H, Moran MM, Navarro B, Chong JA, Krapivinsky G, Krapivinsky L, Kirichok Y, Ramsey IS, Quill TA, Clapham DE. All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility. Proc Natl Acad Sci U S A. 2007;104(4):1219–1223. PubMed PMC

Ren D, Navarro B, Perez G, Jackson AC, Hsu S, Shi Q, Tilly JL, Clapham DE. A sperm ion channel required for sperm motility and male fertility. Nature. 2001;413(6856):603–609. PubMed PMC

Bystroff C. Intramembranal disulfide cross-linking elucidates the super-quaternary structure of mammalian CatSpers. Reprod Biol. 2018;18(1):76–82. PubMed PMC

Singh AP, Rajender S. CatSper channel, sperm function and male fertility. Reprod BioMed Online. 2015;30(1):28–38. PubMed

Hildebrand MS, Avenarius MR, Fellous M, Zhang Y, Meyer NC, Auer J, Serres C, Kahrizi K, Najmabadi H, Beckmann JS, Smith RJ. Genetic male infertility and mutation of CATSPER ion channels. Eur J Hum Genet. 2010;18(11):1178–1184. PubMed PMC

Visser L, Westerveld GH, Xie F, et al. A comprehensive gene mutation screen in men with asthenozoospermia. Fertil Steril. 2011;95(3):1020–1024. PubMed

Bhilawadikar R, Zaveri K, Mukadam L, Naik S, Kamble K, Modi D, Hinduja I. Levels of Tektin 2 and CatSper 2 in normozoospermic and oligoasthenozoospermic men and its association with motility, fertilization rate, embryo quality and pregnancy rate. J Assist Reprod Genet. 2013;30(4):513–523. PubMed PMC

Smith JF, Syritsyna O, Fellous M, Serres C, Mannowetz N, Kirichok Y, Lishko PV. Disruption of the principal, progesterone-activated sperm Ca2+ channel in a CatSper2-deficient infertile patient. Proc Natl Acad Sci U S A. 2013;110(17):6823–6828. PubMed PMC

Williams HL, Mansell S, Alasmari W, Brown SG, Wilson SM, Sutton KA, Miller MR, Lishko PV, Barratt CL, Publicover SJ, Martins da Silva S. Specific loss of CatSper function is sufficient to compromise fertilizing capacity of human spermatozoa. Hum Reprod. 2015;30(12):2737–2746. PubMed PMC

Suarez SS. Control of hyperactivation in sperm. Hum Reprod Update. 2008;14(6):647–657. PubMed

Windler F, Bonigk W, Korschen HG, et al. The solute carrier SLC9C1 is a Na(+)/H(+)-exchanger gated by an S4-type voltage-sensor and cyclic-nucleotide binding. Nat Commun. 2018;9(1):2809. PubMed PMC

Hwang JY, Mannowetz N, Zhang Y, Everley RA, Gygi SP, Bewersdorf J, Lishko PV, Chung JJ. Dual sensing of physiologic pH and calcium by EFCAB9 regulates sperm motility. Cell. 2019;177(6):1480–1494. PubMed PMC

Maas DH, Storey BT, Mastroianni L., Jr Hydrogen ion and carbon dioxide content of the oviductal fluid of the rhesus monkey (Macaca mulatta) Fertil Steril. 1977;28(9):981–985. PubMed

Lishko PV, Botchkina IL, Kirichok Y. Progesterone activates the principal Ca2+ channel of human sperm. Nature. 2011;471(7338):387–391. PubMed

Strunker T, Goodwin N, Brenker C, et al. The CatSper channel mediates progesterone-induced Ca2+ influx in human sperm. Nature. 2011;471(7338):382–386. PubMed

Teves ME, Barbano F, Guidobaldi HA, Sanchez R, Miska W, Giojalas LC. Progesterone at the picomolar range is a chemoattractant for mammalian spermatozoa. Fertil Steril. 2006;86(3):745–749. PubMed

Miller MR, Mannowetz N, Iavarone AT, Safavi R, Gracheva EO, Smith JF, Hill RZ, Bautista DM, Kirichok Y, Lishko PV. Unconventional endocannabinoid signaling governs sperm activation via the sex hormone progesterone. Science. 2016;352(6285):555–559. PubMed PMC

Cai X, Clapham DE. Evolutionary genomics reveals lineage-specific gene loss and rapid evolution of a sperm-specific ion channel complex: CatSpers and CatSperbeta. PLoS One. 2008;3(10):e3569. PubMed PMC

Rahman MS, Kwon WS, Pang MG. Calcium influx and male fertility in the context of the sperm proteome: an update. Biomed Res Int. 2014;2014:841615. PubMed PMC

Brenker C, Goodwin N, Weyand I, Kashikar ND, Naruse M, Krähling M, Müller A, Kaupp UB, Strünker T. The CatSper channel: a polymodal chemosensor in human sperm. EMBO J. 2012;31(7):1654–1665. PubMed PMC

Li H, Ding X, Guan H, Xiong C. Inhibition of human sperm function and mouse fertilization in vitro by an antibody against cation channel of sperm 1: the contraceptive potential of its transmembrane domains and pore region. Fertil Steril. 2009;92(3):1141–1146. PubMed

Li H, Ding X, Guo C, Guan H, Xiong C. Immunization of male mice with B-cell epitopes in transmembrane domains of CatSper1 inhibits fertility. Fertil Steril. 2012;97(2):445–452. PubMed

Carlson AE, Burnett LA, del Camino D, et al. Pharmacological targeting of native CatSper channels reveals a required role in maintenance of sperm hyperactivation. PLoS One. 2009;4(8):e6844. PubMed PMC

Mannowetz N, Miller MR, Lishko PV. Regulation of the sperm calcium channel CatSper by endogenous steroids and plant triterpenoids. Proc Natl Acad Sci U S A. 2017;114(22):5743–5748. PubMed PMC

Tavares RS, Mansell S, Barratt CL, Wilson SM, Publicover SJ, Ramalho-Santos J. p,p'-DDE activates CatSper and compromises human sperm function at environmentally relevant concentrations. Hum Reprod. 2013;28(12):3167–3177. PubMed PMC

Schiffer C, Muller A, Egeberg DL, et al. Direct action of endocrine disrupting chemicals on human sperm. EMBO Rep. 2014;15(7):758–765. PubMed PMC

Rehfeld A, Dissing S, Skakkebaek NE. Chemical UV filters mimic the effect of progesterone on Ca(2+) signaling in human sperm cells. Endocrinology. 2016;157(11):4297–4308. PubMed

He Y, Zou Q, Li B, Chen H, du X, Weng S, Luo T, Zeng X. Ketamine inhibits human sperm function by Ca(2+)-related mechanism. Biochem Biophys Res Commun. 2016;478(1):501–506. PubMed

Shannon M, Rehfeld A, Frizzell C, et al. In vitro bioassay investigations of the endocrine disrupting potential of steviol glycosides and their metabolite steviol, components of the natural sweetener Stevia. Mol Cell Endocrinol. 2016;427:65–72. PubMed

Zou QX, Peng Z, Zhao Q, Chen HY, Cheng YM, Liu Q, He YQ, Weng SQ, Wang HF, Wang T, Zheng LP, Luo T. Diethylstilbestrol activates CatSper and disturbs progesterone actions in human spermatozoa. Hum Reprod. 2017;32(2):290–298. PubMed

Brenker C, Schiffer C, Wagner IV, et al. Action of steroids and plant triterpenoids on CatSper Ca(2+) channels in human sperm. Proc Natl Acad Sci U S A. 2018;115(3):E344–E346. PubMed PMC

Costello S, Michelangeli F, Nash K, Lefievre L, Morris J, Machado-Oliveira G, Barratt C, Kirkman-Brown J, Publicover S. Ca2+-stores in sperm: their identities and functions. Reproduction. 2009;138(3):425–437. PubMed PMC

Correia J, Michelangeli F, Publicover S. Regulation and roles of Ca2+ stores in human sperm. Reproduction. 2015;150(2):R65–R76. PubMed PMC

Alasmari W, Costello S, Correia J, Oxenham SK, Morris J, Fernandes L, Ramalho-Santos J, Kirkman-Brown J, Michelangeli F, Publicover S, Barratt CL. Ca2+ signals generated by CatSper and Ca2+ stores regulate different behaviors in human sperm. J Biol Chem. 2013;288(9):6248–6258. PubMed PMC

Stein KK, Primakoff P, Myles D. Sperm-egg fusion: events at the plasma membrane. J Cell Sci. 2004;117(Pt 26):6269–6274. PubMed

Sutovsky P. Sperm-egg adhesion and fusion in mammals. Expert Rev Mol Med. 2009;11:e11. PubMed

Ikawa M, Inoue N, Benham AM, Okabe M. Fertilization: a sperm’s journey to and interaction with the oocyte. J Clin Invest. 2010;120(4):984–994. PubMed PMC

Bianchi E, Wright GJ. Sperm meets egg: the genetics of mammalian fertilization. Annu Rev Genet. 2016;50:93–111. PubMed

Wilson NF, Snell WJ. Microvilli and cell-cell fusion during fertilization. Trends Cell Biol. 1998;8(3):93–96. PubMed

Speksnijder JE, Jaffe LF, Sardet C. Polarity of sperm entry in the ascidian egg. Dev Biol. 1989;133(1):180–184. PubMed

Motosugi N, Dietrich JE, Polanski Z, Solter D, Hiiragi T. Space asymmetry directs preferential sperm entry in the absence of polarity in the mouse oocyte. PLoS Biol. 2006;4(5):e135. PubMed PMC

Hosseini SM, Moulavi F, Tanhaie-Vash N, Asgari V, Ghanaei HR, Abedi-Dorche M, Jafarzadeh N, Gourabi H, Shahverdi AH, Dizaj AV, Shirazi A, Nasr-Esfahani MH. The principal forces of oocyte polarity are evolutionary conserved but may not affect the contribution of the first two blastomeres to the blastocyst development in mammals. PLoS One. 2016;11(3):e0148382. PubMed PMC

Phillips DM, Shalgi R. Surface architecture of the mouse and hamster zona pellucida and oocyte. J Ultrastruct Res. 1980;72(1):1–12. PubMed

Talansky BE, Malter HE, Cohen J. A preferential site for sperm-egg fusion in mammals. Mol Reprod Dev. 1991;28(2):183–188. PubMed

Santella L, Alikani M, Talansky BE, Cohen J, Dale B. Is the human oocyte plasma membrane polarized? Hum Reprod. 1992;7(7):999–1003. PubMed

Van Blerkom J, Caltrider K. Sperm attachment and penetration competence in the human oocyte: a possible aetiology of fertilization failure involving the organization of oolemmal lipid raft microdomains influenced by the DeltaPsim of subplasmalemmal mitochondria. Reprod BioMed Online. 2013;27(6):690–701. PubMed

Okabe M. The cell biology of mammalian fertilization. Development. 2013;140(22):4471–4479. PubMed

Runge KE, Evans JE, He ZY, Gupta S, McDonald K, Stahlberg H, Primakoff P, Myles DG. Oocyte CD9 is enriched on the microvillar membrane and required for normal microvillar shape and distribution. Dev Biol. 2007;304(1):317–325. PubMed

Chen MS, Tung KS, Coonrod SA, Takahashi Y, Bigler D, Chang A, Yamashita Y, Kincade PW, Herr JC, White JM. Role of the integrin-associated protein CD9 in binding between sperm ADAM 2 and the egg integrin alpha6beta1: implications for murine fertilization. Proc Natl Acad Sci U S A. 1999;96(21):11830–11835. PubMed PMC

Kaji K, Oda S, Shikano T, Ohnuki T, Uematsu Y, Sakagami J, Tada N, Miyazaki S, Kudo A. The gamete fusion process is defective in eggs of Cd9-deficient mice. Nat Genet. 2000;24(3):279–282. PubMed

Le Naour F, Rubinstein E, Jasmin C, Prenant M, Boucheix C. Severely reduced female fertility in CD9-deficient mice. Science. 2000;287(5451):319–321. PubMed

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

Jegou A, Ziyyat A, Barraud-Lange V, et al. CD9 tetraspanin generates fusion competent sites on the egg membrane for mammalian fertilization. Proc Natl Acad Sci U S A. 2011;108(27):10946–10951. PubMed PMC

Barraud-Lange V, Naud-Barriant N, Bomsel M, Wolf JP, Ziyyat A. Transfer of oocyte membrane fragments to fertilizing spermatozoa. FASEB J. 2007;21(13):3446–3449. PubMed

Miyado K, Yoshida K, Yamagata K, Sakakibara K, Okabe M, Wang X, Miyamoto K, Akutsu H, Kondo T, Takahashi Y, Ban T, Ito C, Toshimori K, Nakamura A, Ito M, Miyado M, Mekada E, Umezawa A. The fusing ability of sperm is bestowed by CD9-containing vesicles released from eggs in mice. Proc Natl Acad Sci U S A. 2008;105(35):12921–12926. PubMed PMC

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

Satouh Y, Inoue N, Ikawa M, Okabe M. Visualization of the moment of mouse sperm-egg fusion and dynamic localization of IZUMO1. J Cell Sci. 2012;125(Pt 21):4985–4990. PubMed

Spiridonov NA, Wong L, Zerfas PM, Starost MF, Pack SD, Paweletz CP, Johnson GR. Identification and characterization of SSTK, a serine/threonine protein kinase essential for male fertility. Mol Cell Biol. 2005;25(10):4250–4261. PubMed PMC

Sosnik J, Miranda PV, Spiridonov NA, Yoon SY, Fissore RA, Johnson GR, Visconti PE. Tssk6 is required for Izumo relocalization and gamete fusion in the mouse. J Cell Sci. 2009;122(Pt 15):2741–2749. PubMed PMC

Clark S, Naz RK. Presence and incidence of izumo antibodies in sera of immunoinfertile women and men. Am J Reprod Immunol. 2013;69(3):256–263. PubMed

Granados-Gonzalez V, Aknin-Seifer I, Touraine RL, Chouteau J, Wolf JP, Levy R. Preliminary study on the role of the human IZUMO gene in oocyte-spermatozoa fusion failure. Fertil Steril. 2008;90(4):1246–1248. PubMed

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

Naz RK. Immunocontraceptive effect of Izumo and enhancement by combination vaccination. Mol Reprod Dev. 2008;75(2):336–344. PubMed

Wang M, Lv Z, Shi J, Hu Y, Xu C. Immunocontraceptive potential of the Ig-like domain of Izumo. Mol Reprod Dev. 2009;76(8):794–801. PubMed

Naz RK. Vaccine for human contraception targeting sperm Izumo protein and YLP12 dodecamer peptide. Protein Sci. 2014;23(7):857–868. PubMed PMC

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. 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. 2014;141(19):3732–3739. PubMed

Inoue N, Hamada D, Kamikubo H, Hirata K, Kataoka M, Yamamoto M, Ikawa M, Okabe M, Hagihara Y. Molecular dissection of IZUMO1, a sperm protein essential for sperm-egg fusion. Development. 2013;140(15):3221–3229. PubMed

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

Yu M, Zhao H, Chen T, Tian Y, Li M, Wu K, Bian Y, Su S, Cao Y, Ning Y, Liu H, Chen ZJ. Mutational analysis of IZUMO1R in women with fertilization failure and polyspermy after in vitro fertilization. J Assist Reprod Genet. 2018;35(3):539–544. PubMed PMC

Suzuki B, Sugano Y, Ito J, Saito H, Niimura S, Yamashiro H. Location and expression of Juno in mice oocytes during maturation. JBRA Assist Reprod. 2017;21(4):321–326. PubMed PMC

Jean C, Haghighirad F, Zhu Y, Chalbi M, Ziyyat A, Rubinstein E, Gourier C, Yip P, Wolf JP, Lee JE, Boucheix C, Barraud-Lange V. JUNO, the receptor of sperm IZUMO1, is expressed by the human oocyte and is essential for human fertilisation. Hum Reprod. 2019;34(1):118–126. PubMed

Dai X, Zhang M, Lu Y, Miao Y, Zhou C, Sun S, Xiong B. Melamine impairs female fertility via suppressing protein level of Juno in mouse eggs. PLoS One. 2015;10(12):e0144248. PubMed PMC

Zhang M, Miao Y, Chen Q, et al. BaP exposure causes oocyte meiotic arrest and fertilization failure to weaken female fertility. FASEB J. 2018;32(1):342–352. PubMed

Bianchi E, Wright GJ. Cross-species fertilization: the hamster egg receptor, Juno, binds the human sperm ligand, Izumo1. Philos Trans R Soc Lond Ser B Biol Sci. 2015;370(1661):20140101. PubMed PMC

Yanagimachi R, Yanagimachi H, Rogers BJ. The use of zona-free animal ova as a test-system for the assessment of the fertilizing capacity of human spermatozoa. Biol Reprod. 1976;15(4):471–476. PubMed

Stricker SA. Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev Biol. 1999;211(2):157–176. PubMed

Ramadan WM, Kashir J, Jones C, Coward K. Oocyte activation and phospholipase C zeta (PLCzeta): diagnostic and therapeutic implications for assisted reproductive technology. Cell Commun Signal. 2012;10(1):12. PubMed PMC

Yeste M, Jones C, Amdani SN, Patel S, Coward K. Oocyte activation deficiency: a role for an oocyte contribution? Hum Reprod Update. 2016;22(1):23–47. PubMed

Whitaker M. Calcium at fertilization and in early development. Physiol Rev. 2006;86(1):25–88. PubMed PMC

Swann K. A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs. Development. 1990;110(4):1295–1302. PubMed

Stice SL, Robl JM. Activation of mammalian oocytes by a factor obtained from rabbit sperm. Mol Reprod Dev. 1990;25(3):272–280. PubMed

Homa ST, Swann K. A cytosolic sperm factor triggers calcium oscillations and membrane hyperpolarizations in human oocytes. Hum Reprod. 1994;9(12):2356–2361. PubMed

Sutovsky P, Manandhar G, Wu A, Oko R. Interactions of sperm perinuclear theca with the oocyte: implications for oocyte activation, anti-polyspermy defense, and assisted reproduction. Microsc Res Tech. 2003;61(4):362–378. PubMed

Parrington J, Swann K, Shevchenko VI, Sesay AK, Lai FA. Calcium oscillations in mammalian eggs triggered by a soluble sperm protein. Nature. 1996;379(6563):364–368. PubMed

Sette C, Bevilacqua A, Bianchini A, Mangia F, Geremia R, Rossi P. Parthenogenetic activation of mouse eggs by microinjection of a truncated c-kit tyrosine kinase present in spermatozoa. Development. 1997;124(11):2267–2274. PubMed

Harada Y, Matsumoto T, Hirahara S, Nakashima A, Ueno S, Oda S, Miyazaki S, Iwao Y. Characterization of a sperm factor for egg activation at fertilization of the newt Cynops pyrrhogaster. Dev Biol. 2007;306(2):797–808. PubMed

Aarabi M, Balakier H, Bashar S, et al. Sperm-derived WW domain-binding protein, PAWP, elicits calcium oscillations and oocyte activation in humans and mice. FASEB J. 2014;28(10):4434–4440. PubMed

Tavalaee M, Kiani-Esfahani A, Nasr-Esfahani MH. Relationship between potential sperm factors involved in oocyte activation and sperm DNA fragmentation with intra-cytoplasmic sperm injection clinical outcomes. Cell J. 2017;18(4):588–596. PubMed PMC

Saunders CM, Larman MG, Parrington J, et al. PLC zeta: a sperm-specific trigger of Ca(2+) oscillations in eggs and embryo development. Development. 2002;129(15):3533–3544. PubMed

Cox LJ, Larman MG, Saunders CM, Hashimoto K, Swann K, Lai FA. Sperm phospholipase Czeta from humans and cynomolgus monkeys triggers Ca2+ oscillations, activation and development of mouse oocytes. Reproduction. 2002;124(5):611–623. PubMed

Amdani SN, Yeste M, Jones C, Coward K. Phospholipase C zeta (PLCzeta) and male infertility: clinical update and topical developments. Adv Biol Regul. 2016;61:58–67. PubMed

Knott JG, Kurokawa M, Fissore RA, Schultz RM, Williams CJ. Transgenic RNA interference reveals role for mouse sperm phospholipase Czeta in triggering Ca2+ oscillations during fertilization. Biol Reprod. 2005;72(4):992–996. PubMed

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. PLCzeta is the physiological trigger of the Ca(2+) oscillations that induce embryogenesis in mammals but conception can occur in its absence. Development. 2017;144(16):2914–2924. PubMed PMC

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

Yoon SY, Jellerette T, Salicioni AM, Lee HC, Yoo MS, Coward K, Parrington J, Grow D, Cibelli JB, Visconti PE, Mager J, Fissore RA. 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. 2008;118(11):3671–3681. PubMed PMC

Yamaguchi T, Ito M, Kuroda K, Takeda S, Tanaka A. The establishment of appropriate methods for egg-activation by human PLCZ1 RNA injection into human oocyte. Cell Calcium. 2017;65:22–30. PubMed

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. Reduced amounts and abnormal forms of phospholipase C zeta (PLCzeta) in spermatozoa from infertile men. Hum Reprod. 2009;24(10):2417–2428. PubMed

Kashir J, Konstantinidis M, Jones C, Heindryckx B, de Sutter P, Parrington J, Wells D, Coward K. Characterization of two heterozygous mutations of the oocyte activation factor phospholipase C zeta (PLCzeta) from an infertile man by use of minisequencing of individual sperm and expression in somatic cells. Fertil Steril. 2012;98(2):423–431. PubMed

Heindryckx B, Van der Elst J, De Sutter P, Dhont M. Treatment option for sperm- or oocyte-related fertilization failure: assisted oocyte activation following diagnostic heterologous ICSI. Hum Reprod. 2005;20(8):2237–2241. PubMed

Heindryckx B, De Gheselle S, Gerris J, Dhont M, De Sutter P. Efficiency of assisted oocyte activation as a solution for failed intracytoplasmic sperm injection. Reprod BioMed Online. 2008;17(5):662–668. PubMed

Nomikos M, Theodoridou M, Elgmati K, Parthimos D, Calver BL, Buntwal L, Nounesis G, Swann K, Lai FA. Human PLCzeta exhibits superior fertilization potency over mouse PLCzeta in triggering the Ca(2+) oscillations required for mammalian oocyte activation. Mol Hum Reprod. 2014;20(6):489–498. PubMed PMC

Ebner T, Montag M. Artificial oocyte activation: evidence for clinical readiness. Reprod BioMed Online. 2016;32(3):271–273. PubMed

Rogers NT, Hobson E, Pickering S, Lai FA, Braude P, Swann K. Phospholipase Czeta causes Ca2+ oscillations and parthenogenetic activation of human oocytes. Reproduction. 2004;128(6):697–702. PubMed

Gardner AJ, Evans JP. Mammalian membrane block to polyspermy: new insights into how mammalian eggs prevent fertilisation by multiple sperm. Reprod Fertil Dev. 2006;18(1–2):53–61. PubMed

Jaffe LA. Fast block to polyspermy in sea urchin eggs is electrically mediated. Nature. 1976;261(5555):68–71. PubMed

Wozniak KL, Carlson AE. Ion channels and signaling pathways used in the fast polyspermy block. Mol Reprod Dev. 2019;1-8. PubMed PMC

Dale B, DeFelice L. Polyspermy prevention: facts and artifacts? J Assist Reprod Genet. 2011;28(3):199–207. PubMed PMC

Maleszewski M, Kimura Y, Yanagimachi R. Sperm membrane incorporation into oolemma contributes to the oolemma block to sperm penetration: evidence based on intracytoplasmic sperm injection experiments in the mouse. Mol Reprod Dev. 1996;44(2):256–259. PubMed

Sengoku K, Tamate K, Takaoka Y, Horikawa M, Goishi K, Okada R, Tsuchiya K, Ishikawa M. Requirement of sperm-oocyte plasma membrane fusion for establishment of the plasma membrane block to polyspermy in human pronuclear oocytes. Mol Reprod Dev. 1999;52(2):183–188. PubMed

Gulyas BJ. Cortical granules of mammalian eggs. Int Rev Cytol. 1980;63:357–392. PubMed

Cheeseman LP, Boulanger J, Bond LM, Schuh M. Two pathways regulate cortical granule translocation to prevent polyspermy in mouse oocytes. Nat Commun. 2016;7:13726. PubMed PMC

Vogt EJ, Tokuhiro K, Guo M, Dale R, Yang G, Shin SW, Movilla MJ, Shroff H, Dean J. Anchoring cortical granules in the cortex ensures trafficking to the plasma membrane for post-fertilization exocytosis. Nat Commun. 2019;10(1):2271. PubMed PMC

Liu M. The biology and dynamics of mammalian cortical granules. Reprod Biol Endocrinol. 2011;9:149. PubMed PMC

Miao YL, Kikuchi K, Sun QY, Schatten H. Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility. Hum Reprod Update. 2009;15(5):573–585. PubMed

Gahlay G, Gauthier L, Baibakov B, Epifano O, Dean J. Gamete recognition in mice depends on the cleavage status of an egg’s zona pellucida protein. Science. 2010;329(5988):216–219. PubMed PMC

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

Schroeder AC, Schultz RM, Kopf GS, Taylor FR, Becker RB, Eppig JJ. Fetuin inhibits zona pellucida hardening and conversion of ZP2 to ZP2f during spontaneous mouse oocyte maturation in vitro in the absence of serum. Biol Reprod. 1990;43(5):891–897. PubMed

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. Fetuin-B, a liver-derived plasma protein is essential for fertilization. Dev Cell. 2013;25(1):106–112. PubMed

Dietzel E, Floehr J, Van de Leur E, Weiskirchen R, Jahnen-Dechent W. Recombinant fetuin-B protein maintains high fertilization rate in cumulus cell-free mouse oocytes. Mol Hum Reprod. 2017;23(1):25–33. PubMed

Floehr J, Dietzel E, Neulen J, Rosing B, Weissenborn U, Jahnen-Dechent W. Association of high fetuin-B concentrations in serum with fertilization rate in IVF: a cross-sectional pilot study. Hum Reprod. 2016;31(3):630–637. PubMed

Fang L, Hu X, Cui L, Lv P, Ma X, Ye Y. Serum and follicular fluid fetuin-B levels are correlated with fertilization rates in conventional IVF cycles. J Assist Reprod Genet. 2019;36(6):1101–1107. PubMed PMC

Floehr J, Dietzel E, Schmitz C, Chappell A, Jahnen-Dechent W. Down-regulation of the liver-derived plasma protein fetuin-B mediates reversible female infertility. Mol Hum Reprod. 2017;23(1):34–44. PubMed

Kim AM, Bernhardt ML, Kong BY, Ahn RW, Vogt S, Woodruff TK, O'Halloran TV. Zinc sparks are triggered by fertilization and facilitate cell cycle resumption in mammalian eggs. ACS Chem Biol. 2011;6(7):716–723. PubMed PMC

Bernhardt ML, Kong BY, Kim AM, O’Halloran TV, Woodruff TK. A zinc-dependent mechanism regulates meiotic progression in mammalian oocytes. Biol Reprod. 2012;86(4):114. PubMed PMC

Que EL, Bleher R, Duncan FE, Kong BY, Gleber SC, Vogt S, Chen S, Garwin SA, Bayer AR, Dravid VP, Woodruff TK, O'Halloran TV. Quantitative mapping of zinc fluxes in the mammalian egg reveals the origin of fertilization-induced zinc sparks. Nat Chem. 2015;7(2):130–139. PubMed PMC

Zhang N, Duncan FE, Que EL, O'Halloran TV, Woodruff TK. The fertilization-induced zinc spark is a novel biomarker of mouse embryo quality and early development. Sci Rep. 2016;6:22772. PubMed PMC

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

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

Que EL, Duncan FE, Lee HC, Hornick JE, Vogt S, Fissore RA, O’Halloran TV, Woodruff TK. Bovine eggs release zinc in response to parthenogenetic and sperm-induced egg activation. Theriogenology. 2019;127:41–48. PubMed PMC

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

Lee K, Davis A, Zhang L, Ryu J, Spate LD, Park KW, Samuel MS, Walters EM, Murphy CN, Machaty Z, Prather RS. Pig oocyte activation using a Zn(2)(+) chelator, TPEN. Theriogenology. 2015;84(6):1024–1032. PubMed PMC

de Macedo MP, Glanzner WG, Rissi VB, Gutierrez K, Currin L, Baldassarre H, Bordignon V. A fast and reliable protocol for activation of porcine oocytes. Theriogenology. 2019;123:22–29. PubMed

Jeon Y, Yoon JD, Cai L, Hwang SU, Kim E, Zheng Z, Lee E, Kim DY, Hyun SH. Supplementation of zinc on oocyte in vitro maturation improves preimplatation embryonic development in pigs. Theriogenology. 2014;82(6):866–874. PubMed

Ho PC, Yeung WS, Chan YF, So WW, Chan ST. Factors affecting the incidence of polyploidy in a human in vitro fertilization program. Int J Fertil Menopausal Stud. 1994;39(1):14–19. PubMed

Hassold T, Chen N, Funkhouser J, Jooss T, Manuel B, Matsuura J, Matsuyama A, Wilson C, Yamane JA, Jacobs PA. A cytogenetic study of 1000 spontaneous abortions. Ann Hum Genet. 1980;44(2):151–178. PubMed

Byrne J, Warburton D, Kline J, Blanc W, Stein Z. Morphology of early fetal deaths and their chromosomal characteristics. Teratology. 1985;32(2):297–315. PubMed

Menten B, Swerts K, Delle Chiaie B, et al. Array comparative genomic hybridization and flow cytometry analysis of spontaneous abortions and mors in utero samples. BMC Med Genet. 2009;10:89. PubMed PMC

Jacobs PA, Angell RR, Buchanan IM, Hassold TJ, Matsuyama AM, Manuel B. The origin of human triploids. Ann Hum Genet. 1978;42(1):49–57. PubMed

Bieber FR, Nance WE, Morton CC, Brown JA, Redwine FO, Jordan RL, Mohanakumar T. Genetic studies of an acardiac monster: evidence of polar body twinning in man. Science. 1981;213(4509):775–777. PubMed

McNamara HC, Kane SC, Craig JM, Short RV, Umstad MP. A review of the mechanisms and evidence for typical and atypical twinning. Am J Obstet Gynecol. 2016;214(2):172–191. PubMed

Gabbett MT, Laporte J, Sekar R, Nandini A, McGrath P, Sapkota Y, Jiang P, Zhang H, Burgess T, Montgomery GW, Chiu R, Fisk NM. Molecular support for heterogonesis resulting in sesquizygotic twinning. N Engl J Med. 2019;380(9):842–849. PubMed

Hendriks S, Dancet EA, van Pelt AM, Hamer G, Repping S. Artificial gametes: a systematic review of biological progress towards clinical application. Hum Reprod Update. 2015;21(3):285–296. PubMed

Vassena R, Heindryckx B, Peco R, et al. Genome engineering through CRISPR/Cas9 technology in the human germline and pluripotent stem cells. Hum Reprod Update. 2016;22(4):411–419. PubMed

Clift D, McEwan WA, Labzin LI, Konieczny V, Mogessie B, James LC, Schuh M. A method for the acute and rapid degradation of endogenous proteins. Cell. 2017;171(7):1692–1706. PubMed PMC

Clift D, So C, McEwan WA, James LC, Schuh M. Acute and rapid degradation of endogenous proteins by Trim-Away. Nat Protoc. 2018;13(10):2149–2175. PubMed

Jones S, Lukanowska M, Suhorutsenko J, Oxenham S, Barratt C, Publicover S, Copolovici DM, Langel Ü, Howl J. Intracellular translocation and differential accumulation of cell-penetrating peptides in bovine spermatozoa: evaluation of efficient delivery vectors that do not compromise human sperm motility. Hum Reprod. 2013;28(7):1874–1889. PubMed PMC

Morris J, Jones S, Howl J, Lukanowska M, Lefievre L, Publicover S. Cell-penetrating peptides, targeting the regulation of store-operated channels, slow decay of the progesterone-induced [Ca2+]i signal in human sperm. Mol Hum Reprod. 2015;21(7):563–570. PubMed PMC

Ohto U, Ishida H, Krayukhina E, Uchiyama S, Inoue N, Shimizu T. Structure of IZUMO1-JUNO reveals sperm-oocyte recognition during mammalian fertilization. Nature. 2016;534(7608):566–569. PubMed

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