Skip to main content
Hauptrubriken
CME Facharzt-Training Webinare Zeitschriften Bücher e.Medpedia Podcast
Service
Jobbörse Info & Hilfe
Fachgebiete
Anästhesiologie Allgemeinmedizin Arbeitsmedizin Augenheilkunde Chirurgie Dermatologie Gynäkologie und Geburtshilfe HNO Innere Medizin Kardiologie Neurologie Onkologie und Hämatologie Orthopädie und Unfallchirurgie Pädiatrie Pathologie Psychiatrie Radiologie Rechtsmedizin Urologie Zahnmedizin
Themen
Klimawandel und Gesundheit Neues aus dem Markt COVID-19 Praxis und Beruf Seltene Erkrankungen GOÄ & EBM Panorama
Sammlungen
Kasuistiken Algorithmen & Infografiken Blickdiagnosen Arthropedia FlapFinder (für Dermatochirurgen) Videos Kongressberichterstattung Medizin für Apothekerinnen und Apotheker Für Ärztinnen und Ärzte in Weiterbildung Für Medizinstudierende
Erweiterte Suche
Anmelden
nach oben
Journal of Assisted Reproduction and Genetics
Erschienen in: Journal of Assisted Reproduction and Genetics 6/2020

14.04.2020 | Review

Increasing associations between defects in phospholipase C zeta and conditions of male infertility: not just ICSI failure?

verfasst von: Junaid Kashir

Erschienen in: Journal of Assisted Reproduction and Genetics | Ausgabe 6/2020

Einloggen, um Zugang zu erhalten

Abstract

Purpose

Oocyte activation is a fundamental event at mammalian fertilization. In mammals, this process is initiated by a series of characteristic calcium (Ca2+) oscillations, induced by a sperm-specific phospholipase C (PLC) termed PLCzeta (PLCζ). Dysfunction/reduction/deletion of PLCζ is associated with forms of male infertility where the sperm is unable to initiate Ca2+ oscillations and oocyte activation, specifically in cases of fertilization failure. This review article aims to systematically summarize recent advancements and controversies in the field to update expanding clinical associations between PLCζ and various male factor conditions. This article also discusses how such associations may potentially underlie defective embryogenesis and recurrent implantation failure following fertility treatments, alongside potential diagnostic and therapeutic PLCζ approaches, aiming to direct future research efforts to utilize such knowledge clinically.

Methods

An extensive literature search was performed using literature databases (PubMed/MEDLINE/Web of Knowledge) focusing on phospholipase C zeta (PLCzeta; PLCζ), oocyte activation, and calcium oscillations, as well as specific male factor conditions.

Results and discussion

Defective PLCζ or PLCζ-induced Ca2+ release can be linked to multiple forms of male infertility including abnormal sperm parameters and morphology, sperm DNA fragmentation and oxidation, and abnormal embryogenesis/pregnancies. Such sperm exhibit absent/reduced levels, and abnormal localization patterns of PLCζ within the sperm head.

Conclusions

Defective PLCζ and abnormal patterns of Ca2+ release are increasingly suspected a significant causative factor underlying abnormalities or insufficiencies in Ca2+ oscillation-driven early embryogenic events. Such cases could potentially strongly benefit from relevant therapeutic and diagnostic applications of PLCζ, or even alternative mechanisms, following further focused research efforts.
Literatur
1.
European IVF-Monitoring Consortium (EIM) for the European Society of Human Reproduction and Embryology (ESHRE), Calhaz-Jorge C, de Geyter C, Kupka MS, de Mouzon J, Erb K, et al. Assisted reproductive technology in Europe, 2012: results generated from European registers by ESHRE. Hum Reprod. 2016;31(8):1638–52.
2.
Jungwirth A, Giwercman A, Tournaye H, Diemer T, Kopa Z, Dohle G, et al. European Association of Urology guidelines on male infertility: the 2012 update. Eur Urol. 2012;62(2):324–32.
3.
Hotaling JM. Genetics of male infertility. Urol Clin North Am. 2014;41:1–17.PubMed
4.
Gunes S, Arslan MA, Hekim GNT, Asci R. The role of epigenetics in idiopathic male infertility. J Assist Reprod Genet. 2016;33:553–69.PubMedPubMedCentral
5.
Kashir J, Heindryckx B, Jones C, De Sutter P, Parrington J, Coward K. Oocyte activation, phospholipase C zeta and human infertility. Hum Reprod Update. 2010;16:690–703.PubMed
6.
Botezatu A, Socolov R, Socolov D, Iancu IV, Anton G. Methylation pattern of methylene tetrahydrofolate reductase and small nuclear ribonucleoprotein polypeptide N promoters in oligoasthenospermia: a case-control study. Reprod BioMed Online. 2014;28(2):225–31.PubMed
7.
Sousa M, Tesarik J. Fertiliza1tion and early embryology: ultrastructural analysis of fertilization failure after intracytoplasmic sperm injection. Hum Reprod. 1994;9:2374–80.PubMed
8.
Mahutte NG, Arici A. Failed fertilization: is it predictable? Curr Opin Obstet Gynecol. 2003;15(3):211–8.PubMed
9.
Amdani SN, Yeste M, Jones C, Coward K. Phospholipase C zeta (PLCζ) and male infertility: clinical update and topical developments. Adv Biol Regul. 2016;61:58–67.PubMed
10.
Polanski LT, Baumgarten MN, Quenby S, Brosens J, Campbell BK, Raine-Fenning NJ. What exactly do we mean by ‘recurrent implantation failure’? A systematic review and opinion. Reprod BioMed Online. 2014;28(4):409–23.PubMed
11.
Dyer S, Chambers GM, de Mouzon J, Nygren KG, Zegers-Hochschild F, Mansour R, et al. International committee for monitoring assisted reproductive technologies world report: assisted reproductive technology 2008, 2009 and 2010. Hum Reprod. 2016;31(7):1588–609.
12.
Fauque P, Léandri R, Merlet F, Juillard JC, Epelboin S, Guibert J, et al. Pregnancy outcome and live birth after IVF and ICSI according to embryo quality. J Assist Reprod Genet. 2007;24(5):159–65.
13.
Pelinck MJ, Hoek A, Simons AH, Heineman MJ, van Echten-Arends J, Arts EG. Embryo quality and impact of specific embryo characteristics on ongoing implantation in unselected embryos derived from modified natural cycle in vitro fertilization. Fertil Steril. 2010;94:527–34.PubMed
14.
Loutradi KE, Tarlatzis BC, Goulis DG, Zepiridis L, Pagou T, Chatziioannou E, et al. The effects of sperm quality on embryo development after intracytoplasmic sperm injection. J Assist Reprod Genet. 2006;23(2):69–74.
15.
Oseguera-López I, Ruiz-Díaz S, Ramos-Ibeas P, Pérez-Cerezales S. Novel techniques of sperm selection for improving IVF and ICSI outcomes. Front Cell Dev Biol. 2019;7:298.PubMedPubMedCentral
16.
Gannon JR, Emery BR, Jenkins TG, Carrell DT. The sperm epigenome: implications for the embryo. Adv Exp Med Biol. 2014;791:53–66.PubMed
17.
Jenkins TG, Aston KI, James ER, Carrell DT. Sperm epigenetics in the study of male fertility, offspring health, and potential clinical applications. Syst Biol Reprod Med. 2017;63(2):69–76.PubMed
18.
Denomme MM, McCallie BR, Parks JC, Schoolcraft WB, Katz-Jaffe MG. Alterations in the sperm histone-retained epigenome are associated with unexplained male factor infertility and poor blastocyst development in donor oocyte IVF cycles. Hum Reprod. 2017;32(12):2443–55.PubMed
19.
Carrell DT, Salas-Huetos A, Hotaling J. Increasing evidence of the role of the sperm epigenome in embryogenesis: oligoasthenoteratozoospermia, altered embryo DNA methylation, and miscarriage. Fertil Steril. 2018;110(3):401–2.PubMed
20.
Alvarez Sedó C, Bilinski M, Lorenzi D, Uriondo H, Noblía F, Longobucco V, et al. Effect of sperm DNA fragmentation on embryo development: clinical and biological aspects. JBRA Assist Reprod. 2017;21(4):343–50.
21.
Esbert M, Pacheco A, Soares SR, Amorós D, Florensa M, Ballesteros A, et al. High sperm DNA fragmentation delays human embryo kinetics when oocytes from young and healthy donors are microinjected. Andrology. 2018;6(5):697–706.
22.
Borges E Jr, Zanetti BF, Setti AS, Braga DPAF, Provenza RR, Iaconelli A Jr. Sperm DNA fragmentation is correlated with poor embryo development, lower implantation rate, and higher miscarriage rate in reproductive cycles of non-male factor infertility. Fertil Steril. 2019;112(3):483–90.PubMed
23.
Kim ST, Moley KH. Paternal effect on embryo quality in diabetic mice is related to poor sperm quality and associated with decreased glucose transporter expression. Reproduction. 2008;136(3):313–22.PubMed
24.
Binder NK, Mitchell M, Gardner DK. Parental diet-induced obesity leads to retarded early mouse embryo development and altered carbohydrate utilisation by the blastocyst. Reprod Fertil Dev. 2012;24(6):804–12.PubMed
25.
Braga DP, Halpern G, Setti AS, Figueira RC, Iaconelli A Jr, Borges E Jr. The impact of food intake and social habits on embryo quality and the likelihood of blastocyst formation. Reprod BioMed Online. 2015;31(1):30–8.PubMed
26.
Chen Q, Yan M, Cao Z, Li X, Zhang Y, Shi J, et al. Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science. 2016;351(6271):397–400.
27.
Sharma U, Conine CC, Shea JM, Boskovic A, Derr AG, Bing XY, et al. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science. 2016;351(6271):391–6.
28.
Watkins AJ, Sirovica S, Stokes B, Isaacs M, Addison O, Martin RA. Paternal low protein diet programs preimplantation embryo gene expression, fetal growth and skeletal development in mice. Biochim Biophys Acta Mol basis Dis. 2017;1863(6):1371–81.PubMed
29.
Kashir J, Nomikos M, Lai FA. Phospholipase C zeta and calcium oscillations at fertilization: the evidence, applications, and further questions. Adv Biol Regul. 2018;67:148–62.PubMed
30.
Kline D, Kline T. Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg. Dev Biol. 1992;149:80–9.PubMed
31.
Swann K, Ozil JP. Dynamics of the calcium signal that triggers mammalian egg activation. Int Rev Cytol. 1994;152:183–222.PubMed
32.
Stricker SA. Comparative biology of calcium signalling during fertilization and egg activation in mammals. Dev Biol. 1999;211:57–176.
33.
Miyazaki S, Ito M. Calcium signals for egg activation in mammals. J Pharmacol Sci. 2006;100:545–52.PubMed
34.
Horner VL, Wolfner MF. Transitioning from egg to embryo: triggers and mechanisms of egg activation. Dev Dyn. 2008;237(3):527–44.PubMed
35.
Swann K, Yu Y. The dynamics of calcium oscillations that activate mammalian eggs. Int J Dev Biol. 2008;52:585–94.PubMed
36.
Ito J, Parrington J, Fissore RA. PLCζ and its role as a trigger of development in vertebrates. Mol Reprod Dev. 2011;78(10–11):846–53.PubMed
37.
Parrington J. Does a soluble sperm factor trigger calcium release in the egg at fertilization? J Androl. 2001;22:1–11.PubMed
38.
Swann K, Saunders CM, Rogers NT, Lai FA. PLCzeta (zeta): a sperm protein that triggers Ca2+ oscillations and egg activation in mammals. Semin Cell Dev Biol. 2006;17:264–73.PubMed
39.
40.
Parrington J, Davis LC, Galione A, Wessel G. Flipping the switch: how a sperm activates the egg at fertilization. Dev Dyn. 2007;236:2027–38.PubMed
41.
Saunders CM, Swann K, Lai FA. PLCzeta, a sperm-specific PLC and its potential role in fertilization. Biochem Soc Symp. 2007;74:23–36.
42.
Miyazaki S, Shirakawa H, Nakada K, Honda Y. Essential role of the inositol 1,4,5-trisphosphate receptor/Ca2+ release channel in Ca2+ waves and Ca2+ oscillations at fertilization of mammalian eggs. Dev Biol. 1993;158:62–78.PubMed
43.
Ducibella T, Huneau D, Angelichio E, Xu Z, Schultz RM, Kopf GS, et al. Egg-to-embryo transition is driven by differential responses to Ca(2+) oscillation number. Dev Biol. 2002;250:280–91.
44.
Ducibella T, Schultz RM, Ozil JP. Role of calcium signals in early development. Semin Cel Dev Biol. 2006;17:324–32.
45.
Kashir J, Nomikos M, Lai FA, Swann K. Sperm-induced Ca2+ release during egg activation in mammals. Biochem Biophys Res Commun. 2014;450:1204–11.PubMed
46.
Kashir J, Deguchi R, Jones C, Coward K, Stricker SA. Comparative biology of sperm factors and fertilization-induced calcium signals across the animal kingdom. Mol Reprod Dev. 2013;80(10):787–815.PubMed
47.
Fulton BP, Whittingham DG. Activation of mammalian oocytes by intracellular injection of calcium. Nature. 1978;273:149–51.PubMed
48.
Miyazaki S, Yuzaki M, Nakada K, Shirakawa H, Nakanishi S, Nakade S, et al. Block of Ca2+ wave and Ca2+ oscillation by antibody to the inositol 1,4,5-trisphosphate receptor in fertilized hamster eggs. Science. 1992;257:251–5.
49.
Brind S, Swann K, Carroll J. Inositol 1,4,5-trisphosphate receptors are downregulated in mouse oocytes in response to sperm or adenophostin A but not to increases in intracellular Ca(2+) or egg activation. Dev Biol. 2000;223:251–65.PubMed
50.
Jellerette T, He CL, Wu H, Parys JB, Fissore RA. Down-regulation of the inositol 1,4,5-trisphosphate receptor in mouse eggs following fertilization or parthenogenetic activation. Dev Biol. 2000;223:238–50.PubMed
51.
Xu Z, Williams CJ, Kopf GS, Schultz RM. Maturation-associated increase in IP3 receptor type 1: role in conferring increased IP3 sensitivity and Ca2+ oscillatory behavior in mouse eggs. Dev Biol. 2003;254:163–71.PubMed
52.
Malcuit C, Kurokawa M, Fissore RA. Calcium oscillations and mammalian egg activation. J Cell Physiol. 2006;206:565–73.PubMed
53.
Stitzel ML, Seydoux G. Regulation of the oocyte-to-zygote transition. Science. 2007;316:407–8.PubMed
54.
Ducibella T, Fissore R. The roles of Ca2+, downstream protein kinases, and oscillatory signaling in regulating fertilization and the activation of development. Dev Biol. 2008;315:257–79.PubMedPubMedCentral
55.
Wong CC, Loewke KE, Bossert NL, Behr B, De Jonge CJ, Baer TM, et al. Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nat Biotechnol. 2010;28:1115–21.
56.
Yu Y, Saunders CM, Lai FA, Swann K. Preimplantation development of mouse oocytes activated by different levels of human phospholipase C zeta. Hum Reprod. 2008;23:365–73.PubMed
57.
Swann K. A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs. Development. 1990;110:1295–302.PubMed
58.
Kyozuka K, Deguchi R, Mohri T, Miyazaki S. Injection of sperm extract mimics spatiotemporal dynamics of Ca2+ responses and progression of meiosis at fertilization of ascidian oocytes. Development. 1998;125:4099–105.PubMed
59.
Stricker SA. Intracellular injections of a soluble sperm factor trigger calcium oscillations and meiotic maturation in unfertilized oocytes of a marine worm. Dev Biol. 1997;186:185–201.PubMed
60.
Dong JB, Tang TS, Sun FZ. Xenopus and chicken sperm contain a cytosolic soluble protein factor which can trigger calcium oscillations in mouse eggs. Biochem Biophys Res Commun. 2000;268:947–51.PubMed
61.
Coward K, Campos-Mendoza A, Larman M, Hibbitt O, McAndrew B, Bromage N, et al. Teleost fish spermatozoa contain a cytosolic protein factor that induces calcium release in sea urchin egg homogenates and triggers calcium oscillations when injected into mouse oocytes. Biochem Biophys Res Commun. 2003;305:299–304.
62.
Coward K, Ponting CP, Chang HY, Hibbitt O, Savolainen P, Jones KT, et al. Phospholipase Czeta, the trigger of egg activation in mammals, is present in a non-mammalian species. Reproduction. 2005;130:157–63.
63.
Nakano Y, Shirakawa H, Mitsuhashi N, Kuwabara Y, Miyazaki S. Spatiotemporal dynamics of intracellular calcium in the mouse egg injected with a spermatozoon. Mol Hum Reprod. 1997;3:1087–93.PubMed
64.
Parrington J, Swann K, Shevchenko VI, Sesay AK, Lai FA. Calcium oscillations in mammalian eggs triggered by a soluble sperm protein. Nature. 1996;25:364–8.
65.
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;124:2267–74.PubMed
66.
Sette C, Bevilacqua A, Geremia R, Rossi P. Involvement of phospholipase Cgamma1 in mouse egg activation induced by a truncated form of the C-kit tyrosine kinase present in spermatozoa. J Cell Biol. 1998;142:1063–74.PubMedPubMedCentral
67.
Sette C, Paronetto MP, Barchi M, Bevilacqua A, Geremia R, Rossi P. Tr-kit-induced resumption of the cell cycle in mouse eggs requires activation of a Src-like kinase. EMBO J. 2002;21:5386–95.PubMedPubMedCentral
68.
Wu AT, Sutovsky P, Manandhar G, Xu W, Katayama M, Day BN, et al. PAWP, a sperm-specific WW domain-binding protein, promotes meiotic resumption and pronuclear development during fertilization. J Biol Chem. 2007;282:12164–75.
69.
Aarabi M, Qin Z, Xu W, Mewburn J, Oko R. Sperm-borne protein, PAWP, initiates zygotic development in Xenopus laevis by eliciting intracellular calcium release. Mol Reprod Dev. 2010;77:249–56.PubMed
70.
Swann K. Different triggers for calcium oscillations in mouse eggs involve a ryanodine-sensitive calcium store. Biochem J. 1992;287(Pt 1):79–84.PubMedPubMedCentral
71.
Jones KT, Carroll J, Whittingham DG. Ionomycin, thapsigargin, ryanodine, and sperm induced Ca2+ release increase during meiotic maturation of mouse oocytes. J Biol Chem. 1994;270:6671–7.
72.
Kline JT, Kline D. Regulation of intracellular calcium in the mouse egg: evidence for inositol trisphosphate-induced calcium release, but not calcium induced calcium release. Biol Reprod. 1994;50:193–203.PubMed
73.
Nader N, Kulkarni RP, Dib M, Machaca K. How to make a good egg! The need for remodeling of Ca2+ signaling to mediate the egg-to-embryo transition. Cell Calcium. 2013;53:41–54.PubMed
74.
Wolosker H, Kline D, Bian Y, Blackshaw S, Cameron AM, Fralich TJ, et al. Molecularly cloned mammalian glucosamine-6-phosphate deaminase localizes to transporting epithelium and lacks oscillin activity. FASEB J. 1998;12:91–9.
75.
Parrington J, Jones KT, Lai FA, Swann K. The soluble sperm factor that causes Ca2+ release from sea urchin egg homogenates also triggers Ca2+ oscillations after injection into mouse eggs. Biochem J. 1999;341:1–4.PubMedPubMedCentral
76.
Swann K, Larman MG, Saunders CM, Lai FA. The cytosolic sperm factor that triggers Ca2+ oscillations and egg activation in mammals is a novel phospholipase C: PLCzeta. Reproduction. 2004;127(4):431–9.PubMed
77.
Kashir J, Nomikos M, Swann K, Lai FA. PLCζ or PAWP: revisiting the putative mammalian sperm factor that triggers egg activation and embryogenesis. Mol Hum Reprod. 2015;21(5):383–8.PubMed
78.
Jones KT, Soeller C, Cannell MB. The passage of Ca2+ and fluorescent markers between the sperm and egg after fusion in the mouse. Development. 1998;125:4627–35.PubMed
79.
Jones KT, Matsuda M, Parrington J, Katan M, Swann K. Different Ca2+-releasing abilities of sperm extracts compared with tissue extracts and phospholipase C isoforms in sea urchin egg homogenate and mouse eggs. Biochem J. 2000;346(pt 3):743–9.PubMedPubMedCentral
80.
Runft LL, Carroll DJ, Gillett J, Giusti AF, O’Neill FJ, Foltz KR. Identification of a starfish egg PLC-gamma that regulates Ca2+ release at fertilization. Dev Biol. 2004;269:220–36.PubMed
81.
Coward K, Owen H, Tunwell R, Swann K, Parrington J. Phospholipid binding properties and functional characterization of a sea urchin phospholipase Cdelta in urchin and mouse eggs. Biochem Biophys Res Commun. 2007;357:964–70.PubMed
82.
Igarashi H, Knott JG, Schultz RM, Williams CJ. Alterations of PLCbeta1 in mouse eggs change calcium oscillatory behavior following fertilization. Dev Biol. 2007;312:321–30.PubMedPubMedCentral
83.
Yin X, Eckberg WR. Characterization of phospholipases C beta and gamma and their possible roles in Chaetopterus egg activation. Mol Reprod Dev. 2009;76:460–70.PubMed
84.
Aarabi M, Balakier H, Bashar S, Moskovtsev SI, Sutovsky P, Librach CL, et al. Sperm-derived WW domain-binding protein, PAWP, elicits calcium oscillations and oocyte activation in humans and mice. FASEB J. 2014;28:4434–40.
85.
Nomikos M, Sanders JR, Parthimos D, Buntwal L, Calver BL, Stamatiadis P, et al. Essential role of the EF-hand domain in targeting sperm phospholipase Czeta to membrane phosphatidylinositol 4,5-bisphosphate (PIP2). J Biol Chem. 2015;290:29519–30.
86.
Nomikos M, Sanders JR, Theodoridou M, Kashir J, Matthews E, Nounesis G, et al. Sperm-specific postacrosomal WW-domain binding protein (PAWP) does not cause Ca2+ release in mouse oocytes. Mol Hum Reprod. 2014;20:938–47.PubMedPubMedCentral
87.
Nomikos M, Sanders JR, Kashir J, Sanusi R, Buntwal L, Love D, et al. Functional disparity between human PAWP and PLCζ in the generation of Ca2+ oscillations for oocyte activation. Mol Hum Reprod. 2015b;21:702–10.PubMed
88.
Satouh Y, Nozawa K, Ikawa M. Sperm postacrosomal WW domain-binding protein is not required for mouse egg activation. Biol Reprod. 2015;93.
89.
Saunders CM, Larman MG, Parrington J, Cox LJ, Royse J, Blayney LM, et al. PLC zeta: a sperm-specific trigger of Ca(2+) oscillations in eggs and embryo development. Development. 2002;129:3533–44.
90.
Cox LJ, Larman MG, Saunders CM, Hashimoto K, Swann K, Lai FA. Sperm phospholipase C zeta from humans and cynomolgus monkeys triggers Ca2+ oscillations, activation and development of mouse oocytes. Reproduction. 2002;124:611–23.PubMed
91.
Yoneda A, Kashima M, Yoshida S, Terada K, Nakagawa S, Sakamoto A, et al. Molecular cloning, testicular postnatal expression, and oocyte-activating potential of porcine phospholipase C zeta. Reproduction. 2006;132:393–401.
92.
Yoon SY, Jellerette T, Salicioni AM, Lee HC, Yoo MS, Coward K, et al. Human sperm devoid of PLC, zeta 1 fail to induce Ca2+ release and are unable to initiate the first step of embryo development. J Clin Invest. 2008;118:3671–81.
93.
Young C, Grasa P, Coward K, Davis LC, Parrington J. Phospholipase C zeta undergoes dynamic changes in its pattern of localization in sperm during capacitation and the acrosome reaction. Fertil Steril. 2009;91:2230–42.PubMed
94.
Bedford-Guaus SJ, McPartlin LA, Xie J, Westmiller SL, Buffone MG, Roberson MS. Molecular cloning and characterization of phospholipase C zeta in equine sperm and testis reveals species-specific differences in expression of catalytically active protein. Biol Reprod. 2011;85:78–88.PubMed
95.
Suh PG, Park JI, Manzoli L, Cocco L, Peak JC, Katan M, et al. Multiple roles of phosphoinositide-specific phospholipase C isozymes. BMB Rep. 2008;41:415–34.
96.
Lee B, Yoon SY, Malcuit C, Parys JB, Fissore RA. Inositol 1 4,5-trisphosphate receptor 1 degradation in mouse eggs and impact on [Ca2+]i oscillations. J Cell Physiol. 2010;222:238–47.PubMedPubMedCentral
97.
Kouchi Z, Fukami K, Shikano T, Oda S, Nakamura Y, Takenawa T, et al. Recombinant phospholipase Czeta has high Ca2+ sensitivity and induces Ca2+ oscillations in mouse eggs. J Biol Chem. 2004;279:10408–12.
98.
Nomikos M, Blayney LM, Larman MG, Campbell K, Rossbach A, Saunders CM, et al. Role of phospholipase C-zeta domains in Ca2+-dependent phosphatidylinositol 4,5-bisphosphate hydrolysis and cytoplasmic Ca2+ oscillations. J Biol Chem. 2005;280:31011–8.
99.
Kouchi Z, Shikano T, Nakamura Y, Shirakawa H, Fukami K, Miyazaki S. The role of EF-hand domains and C2 domain in regulation of enzymatic activity of phospholipase Czeta. J Biol Chem. 2005;280(22):21015–21.PubMed
100.
Nomikos M, Kashir J, Swann K, Lai FA. Sperm PLCζ: from structure to Ca2+ oscillations, egg activation and therapeutic potential. FEBS Lett. 2013;587:3609–16.PubMed
101.
Nomikos M, Mulgrew-Nesbitt A, Pallavi P, Mihalyne G, Zaitseva I, Swann K, et al. Binding of phosphoinositide-specific phospholipase C-zeta (PLC-zeta) to phospholipid membranes: potential role of an unstructured cluster of basic residues. J Biol Chem. 2007;282:16644–53.
102.
Nomikos M, Elgmati K, Theodoridou M, Calver BL, Nounesis G, Swann K, et al. Phospholipase Czeta binding to PtdIns(4,5)P2 requires the XY-linker region. J Cell Sci. 2011;124:2582–259.
103.
Nomikos M, Elgmati K, Theodoridou M, Georgilis A, Gonzalez-Garcia JR, Nounesis G, et al. Novel regulation of PLCzeta activity via its XY-linker. Biochem J. 2011;438:427–32.
104.
Larman MG, Saunders CM, Carroll J, Lai FA, Swann K. Cell cycle-dependent Ca2+ oscillations in mouse embryos are regulated by nuclear targeting of PLCzeta. J Cell Sci. 2004;117:2513–21.PubMed
105.
Ito M, Shikano T, Oda S, Horiguchi T, Tanimoto S, Awaji T, et al. Difference in Ca2+ oscillation-inducing activity and nuclear translocation ability of PLCZ1, an egg-activating sperm factor candidate, between mouse, rat, human, and medaka fish. Biol Reprod. 2008;78:1081–90.
106.
Swann K, Lai FA. Egg activation at fertilization by a soluble sperm protein. ​Physiol Rev. 2016;96(1):127–49.
107.
Fujimoto S, Yoshida N, Fukui T, Amanai M, Isobe T, Itagaki C, et al. Mammalian phospholipase Czeta induces oocyte activation from the sperm perinuclear matrix. Dev Biol. 2004;274:370–83.
108.
Kurokawa M, Sato K, Wu H, He C, Malcuit C, Black SJ, et al. Functional, biochemical, and chromatographic characterization of the complete [Ca2+]i oscillation-inducing activity of porcine sperm. Dev Biol. 2005;285:376–92.
109.
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;72:992–6.PubMed
110.
Bedford-Guaus SJ, Yoon SY, Fissore RA, Choi YH, Hinrichs K. Microinjection of mouse phospholipase C zeta complementary RNA into mare oocytes induces long-lasting intracellular calcium oscillations and embryonic development. Reprod Fertil Dev. 2008;20:875–83.PubMed
111.
Coward K, Ponting CP, Zhang N, Young C, Huang CJ, Chou CM, et al. Identification and functional analysis of an ovarian form of the egg activation factor phospholipase C zeta (PLCζ) in pufferfish. Mol Reprod Dev. 2011;78:48–56.
112.
Hachem A, Godwin J, Ruas M, Lee HC, Ferrer Buitrago M, Ardestani G, et al. PLCζ is the physiological trigger of the Ca2+ oscillations that induce embryogenesis in mammals but conception can occur in its absence. Development. 2017;14:2914–24.
113.
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.PubMedPubMedCentral
114.
Satouh Y, Ikawa M. New insights into the molecular events of mammalian fertilization. Trends Biochem Sci. 2018;43(10):818–28.PubMedPubMedCentral
115.
Jones KT. Mammalian sperm contain two factors for calcium release and egg activation: phospholipase C zeta and a cryptic activating factor. Mol Hum Reprod. 2018;24(10):465–8.PubMed
116.
Harada Y, Matsumoto T, Hirahara S, Nakashima A, Ueno S, Oda S, et al. Characterization of a sperm factor for egg activation at fertilization of the newt Cynops pyrrhogaster. Dev Biol. 2007;306(2):797–808.
117.
Miyara F, Aubriot FX, Glissant A, Nathan C, Douard S, Stanovici A, et al. Multiparameter analysis of human oocytes at metaphase II stage after IVF failure in non-male infertility. Hum Reprod. 2003;18:1494–503.
118.
Kilani S, Chapman MG. Meiotic spindle normality predicts live birth in patients with recurrent in vitro fertilization failure. Fertil Steril. 2014;101:403–6.PubMed
119.
Gasca S, Reyftmann L, Pellestor F, Re’me T, Assou S, Anahory T, et al. Total fertilization failure and molecular abnormalities in metaphase II oocytes. Reprod BioMed Online. 2008;17:772–81.
120.
Grøndahl ML, Borup R, Vikesa J, Ernst E, Andersen CY, Lykke-Hartmann K. The dormant and the fully competent oocyte: comparing the transcriptome of human oocytes from primordial follicles and in metaphase II. Mol Hum Reprod. 2013;19:600–17.PubMed
121.
Li Y, Li RQ, Ou SB, Zhang NF, Ren L, Wei LN, et al. Increased GDF9 and BMP15 mRNA levels in cumulus granulosa cells correlate with oocyte maturation, fertilization, and embryo quality in humans. Reprod Biol Endocrinol. 2014;12:81.
122.
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
123.
Yeste M, Jones C, Amdani SN, Coward K. Oocyte activation and fertilisation: crucial contributors from the sperm and oocyte. Results Probl Cell Differ. 2017;59:213–39.PubMed
124.
Levasseur M, Carroll M, Jones KT, McDougall A. A novel mechanism controls the Ca2+ oscillations triggered by activation of ascidian eggs and has an absolute requirement for Cdk1 activity. J Cell Sci. 2007;120:1763–71.
125.
Cheng Y, Zhong Z, Latham KE. Strain-specific spontaneous activation during mouse oocyte maturation. Fertil Steril. 2012;98(1):200–6.PubMedPubMedCentral
126.
Puppo A, Chun JT, Gragnaniello G, Garante E, Santella L. Alteration of the cortical actin cytoskeleton deregulates Ca2+ signaling, monospermic fertilization, and sperm entry. PLoS One. 2008;3(10).
127.
Santella L, Limatola N, Chun JT. Calcium and actin in the saga of awakening oocytes. Biochem Biophys Res Commun. 2015;460(1):104–13.PubMed
128.
Limatola N, Vasilev F, Chun JT, Santella L. Altered actin cytoskeleton in ageing eggs of starfish affects fertilization process. Exp Cell Res. 2019a;381(2):179–90.PubMed
129.
Limatola N, Vasilev F, Chun JT, Santella L. Sodium-mediated fast electrical depolarization does not prevent polyspermic fertilization in Paracentrotus lividus eggs. Zygote. 2019b;27(4):241–9.PubMed
130.
Saleh A, Kashir J, Thanassoulas A, Safieh-Garabedian B, Lai FA, Nomikos M. Essential role of sperm-specific PLC-zeta in egg activation and male factor infertility: an update. Front Cell Dev Biol. 2020;8:28.PubMedPubMedCentral
131.
Halet G, Tunwell R, Balla T, Swann K, Carroll J. The dynamics of plasma membrane PtdIns(4,5)P2 at fertilization of mouse eggs. J Cell Sci. 2002;115:2139–49.PubMed
132.
Yu Y, Nomikos M, Theodoridou M, Nounesis G, Lai FA, Swann K. PLCζ causes Ca2+ oscillations in mouse eggs by targeting intracellular and not plasma membrane PI(45)P(2). Mol Biol Cell. 2012;23:371–80.PubMedPubMedCentral
133.
Swann K, Lai FA. PLCζ and the initiation of Ca(2+) oscillations in fertilizing mammalian eggs. Cell Calcium. 2013;53:55–62.PubMed
134.
Yoda A, Oda S, Shikano T, Kouchi Z, Awaji T, Shirakawa H, et al. Ca2+ oscillation-inducing phospholipase C zeta expressed in mouse eggs is accumulated to the pronucleus during egg activation. Dev Biol. 2004;268:245–57.
135.
Perry ACF, Wakayama T, Yanagimachi R. A novel transcomplementation assay suggests full mammalian oocyte activation is coordinately initiated by multiple, submembrane sperm compartments. Biol Reprod. 1999;60:747–55.PubMed
136.
Manandhar G, Toshimori K. Fate of postacrosomal perinuclear theca recognized by monoclonal antibody MN13 after sperm head microinjection and its role in oocyte activation in mice. Biol Reprod. 2003;68:655–63.PubMed
137.
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;61:362–78.PubMed
138.
Nakai M, Ito J, Sato K, Noguchi J, Kaneko H, Kashiwazaki N, et al. Pre-treatment of sperm reduces success of ICSI in the pig. Reproduction. 2011;142:285–93.
139.
Kaewmala K, Uddin MJ, Cinar MU, Große-Brinkhaus C, Jonas E, Tesfaye D, et al. Investigation into association and expression of PLCz and COX-2 as candidate genes for boar sperm quality and fertility. Reprod Domest Anim. 2012;47:213–23.
140.
Grasa P, Coward K, Young C, Parrington J. The pattern of localization of the putative oocyte activation factor, phospholipase Czeta, in uncapacitated, capacitated, and ionophore-treated human spermatozoa. Hum Reprod. 2008;23:2513–22.PubMed
141.
Heytens E, Parrington J, Coward K, Young C, Lambrecht S, Yoon SY, et al. Reduced amounts and abnormal forms of phospholipase C zeta (PLCzeta) in spermatozoa from infertile men. Hum Reprod. 2009;24:2417–28.
142.
Kashir J, Jones C, Lee HC, Rietdorf K, Nikiforaki D, Durrans C, et al. Loss of activity mutations in phospholipase C zeta (PLCζ) abolishes calcium oscillatory ability of human recombinant protein in mouse oocytes. Hum Reprod. 2011a;26:3372–87.
143.
Kashir J, Heynen A, Jones C, Durrans C, Craig J, Gadea J, et al. Effects of cryopreservation and density-gradient washing on phospholipase C zeta concentrations in human spermatozoa. Reprod BioMed Online. 2011b;23:263–7.
144.
Kashir J, Jones C, Mounce G, Ramadan WM, Lemmon B, Heindryckx B, et al. Variance in total levels of phospholipase C zeta (PLC-zeta) in human sperm may limit the applicability of quantitative immunofluorescent analysis as a diagnostic indicator of oocyte activation capability. Fertil Steril. 2013;99:107–17.
145.
Ramalho-Santos J. A sperm's tail: the importance of getting it right. Hum Reprod. 2011;26(9):2590–1.PubMed
146.
Bi Y, Xu WM, Wong HY, Zhu H, Zhou ZM, Chan HC, et al. NYD-SP27, a novel intrinsic decapacitation factor in sperm. Asian J Androl. 2009;11(2):229–39.
147.
Mejía-Flores I, Chiquete-Félix N, Palma-Lara I, Uribe-Carvajal S, de Lourdes Juárez-Mosqueda M. During capacitation in bull spermatozoa, actin and PLC-ζ undergo dynamic interactions. Zygote. 2017;25(5):558–66.PubMed
148.
Escoffier J, Yassine S, Lee HC, Martinez G, Delaroche J, Coutton C, et al. Subcellular localization of phospholipase Cζ in human sperm and its absence in DPY19L2-deficient sperm are consistent with its role in oocyte activation. Mol Hum Reprod. 2015;21:157–68.
149.
Mizushima S, Takagi S, Ono T, Atsumi Y, Tsukada A, Saito N, et al. Phospholipase Cζ mRNA expression and its potency during spermatogenesis for activation of quail oocyte as a sperm factor. Mol Reprod Dev. 2009;76:1200–7.
150.
Aarabi M, Yu Y, Xu W, Tse MY, Pang SC, Yi YJ, et al. The testicular and epididymal expression profile of PLCζ in mouse and human does not support its role as a sperm-borne oocyte activating factor. PLoS One. 2012;7:e33496.
151.
Kashir J, Konstantinidis M, Jones C, Lemmon B, Lee HC, Hamer R, et al. A maternally inherited autosomal point mutation in human phospholipase C zeta (PLCζ) leads to male infertility. Hum Reprod. 2012a;27:222–31.
152.
Kashir J, Konstantinidis M, Jones C, Heindryckx B, De Sutter P, Parrington J, et al. 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. 2012b;98:423–31.
153.
Ferrer-Vaquer A, Barragan M, Freour T, Vernaeve V, Vassena R. PLCζ sequence, protein levels, and distribution in human sperm do not correlate with semen characteristics and fertilization rates after ICSI. J Assist Reprod Genet. 2016;33(6):747–56.PubMedPubMedCentral
154.
Escoffier J, Lee HC, Yassine S, Zouari R, Martinez G, Karaouzène T, et al. 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. 2016;25:878–91.
155.
Javadian-Elyaderani S, Ghaedi K, Tavalaee M, Rabiee F, Deemeh MR, Nasr-Esfahani MH. Diagnosis of genetic defects through parallel assessment of PLCζ and CAPZA3 in infertile men with history of failed oocyte activation. Iran J Basic Med Sci. 2016;19:281–9.PubMedPubMedCentral
156.
Nomikos M, Stamatiadis P, Sanders JR, Beck K, Calver BL, Buntwal L, et al. Male infertility-linked point mutation reveals a vital binding role for the C2 domain of sperm PLCzeta. Biochem J. 2017;474:1003–16.
157.
Dai J, Dai C, Guo J, Zheng W, Zhang T, Li Y, et al. Novel homozygous variations in PLCZ1 lead to poor or failed fertilization characterized by abnormal localization patterns of PLCζ in sperm. Clin Genet. 2019. https://​doi.​org/​10.​1111/​cge.​13636.
158.
Torra-Massana M, Cornet-Bartolomé D, Barragán M, Durban M, Ferrer-Vaquer A, Zambelli F, et al. Novel phospholipase C zeta 1 mutations associated with fertilization failures after ICSI. Hum Reprod. 2019;34(8):1494–504.
159.
Janghorban-Laricheh E, Ghazavi-Khorasgani N, Tavalaee M, Zohrabi D, Abbasi H, Nasr-Esfahani MH. An association between sperm PLCζ levels and varicocele? J Assist Reprod Genet. 2016;33:1649–55.PubMedPubMedCentral
160.
Mu J, Zhang Z, Wu L, Fu J, Chen B, Yan Z, et al. The identification of novel mutations in PLCZ1 responsible for human fertilization failure and a therapeutic intervention by artificial oocyte activation. Mol Hum Reprod. 2020. https://​doi.​org/​10.​1093/​molehr/​gaaa003.
161.
162.
Azad N, Nazarian H, Ghaffari Novin M, Masteri Farahani R, Piryaei A, Heidari MH. Phospholipase C zeta parameters in sperm from polymorphic teratozoospermic men. Ann Anat. 2018a;215:63–70.PubMed
163.
Azad N, Nazarian H, Ghaffari Novin M, Masteri Farahani R, Piryaei A, Heidari MH, et al. Oligoasthenoteratozoospermic (OAT) men display altered phospholipase C ζ (PLCζ) localization and a lower percentage of sperm cells expressing PLCζ and post-acrosomal sheath WW domain-binding protein (PAWP). Bosn J Basic Med Sci. 2018b;18:178–84.
164.
Tavalaee M, Nomikos M, Lai FA, Nasr-Esfahani MH. Expression of sperm PLCζ and clinical outcomes of ICSI-AOA in men affected by globozoospermia due to DPY19L2 deletion. Reprod BioMed Online. 2018;36:348–55.PubMed
165.
Park JH, Kim SK, Kim J, Kim JH, Chang JH, Jee BC, et al. Relationship between phospholipase C zeta immunoreactivity and DNA fragmentation and oxidation in human sperm. Obstet Gynecol Sci. 2015;58:232–8.
166.
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. 2017a;18:588–96.PubMed
167.
Tavalaee M, Kiani-Esfahani A, Nasr-Esfahani MH. Relationship between phospholipase C-zeta, semen parameters, and chromatin status. Syst Biol Reprod Med. 2017b;63:259–68.PubMed
168.
169.
Nikiforaki D, Vanden Meerschaut F, De Gheselle S, Qian C, Van den Abbeel E, De Vos WH, et al. Sperm involved in recurrent partial hydatidiform moles cannot induce the normal pattern of calcium oscillations. Fertil Steril. 2014;102(2):581–588.e1.
170.
Nickkho-Amiry M, Horne G, Akhtar M, Mathur R, Brison DR. Hydatidiform molar pregnancy following assisted reproduction. J Assist Reprod Genet. 2019;36(4):667–71.PubMedPubMedCentral
171.
Barratt CL, Aitken RJ, Björndahl L, Carrell DT, de Boer P, Kvist U, et al. Sperm DNA: organization, protection and vulnerability: from basic science to clinical applications--a position report. Hum Reprod. 2010;25:824–38.
172.
Nicopoullos J, Vicens-Morton A, Lewis SEM, Lee K, Larsen P, Ramsay J, et al. Novel use of COMET parameters of sperm DNA damage may increase its utility to diagnose male infertility and predict live births following both IVF and ICSI. Hum Reprod. 2019;34(10):1915–23.
173.
Virro MR, Larson-Cook KL, Evenson DP. Sperm chromatin structure assay (SCSA) parameters are related to fertilization, blastocyst development, and ongoing pregnancy in in vitro fertilization and intracytoplasmic sperm injection cycles. Fertil Steril. 2004;81:1289–95.PubMed
174.
Robinson L, Gallos ID, Conner SJ, Rajkhowa M, Miller D, Lewis S, et al. The effect of sperm DNA fragmentation on miscarriage rates: a systematic review and meta-analysis. Hum Reprod. 2012;27:2908–17.PubMed
175.
Osman A, Alsomait H, Seshadri S, El-Toukhy T, Khalaf Y. The effect of sperm DNA fragmentation on live birth rate after IVF or ICSI: a systematic review and meta-analysis. Reprod BioMed Online. 2015;30:120–7.PubMed
176.
Rahimizadeh P, Topraggaleh TR, Nasr-Esfahani MH, Ziarati N, Mirshahvaladi S, Esmaeili V, et al. The alteration of PLCζ protein expression in unexplained infertile and asthenoteratozoospermic patients: a potential effect on sperm fertilization ability. Mol Reprod Dev. 2019. https://​doi.​org/​10.​1002/​mrd.​23293.
177.
178.
Verza S Jr, Esteves SC. Sperm defect severity rather than sperm source is associated with lower fertilization rates after intracytoplasmic sperm injection. Int Braz J Urol. 2008;34:49–56.PubMed
179.
Nordhoff V, Fricke RK, Schüring AN, Zitzmann M, Kliesch S. Treatment strategies for severe oligoasthenoteratozoospermia (OAT) (<0.1 million/mL) patients. Andrology. 2015;3(5):856–63.PubMed
180.
De Vos A, Van De Velde H, Joris H, Verheyen G, Devroey P, Van Steirteghem A. Influence of individual sperm morphology on fertilization, embryo morphology, and pregnancy outcome of intracytoplasmic sperm injection. Fertil Steril. 2003;79:42–8.PubMed
181.
Coban O, Serdarogullari M, Onar Sekerci Z, Bilgin EM, Serakinci N. Evaluation of the impact of sperm morphology on embryo aneuploidy rates in a donor oocyte program. Syst Biol Reprod Med. 2018;64(3):169–73.PubMed
182.
Dam AH, Feenstra I, Westphal JR, Ramos L, van Golde RJ, Kremer JA. Globozoospermia revisited. Hum Reprod Update. 2007;13(1):63–75.PubMed
183.
Taylor SL, Yoon SY, Morshedi MS, Lacey DR, Jellerette T, Fissore RA, et al. Complete globozoospermia associated with PLCζ deficiency treated with calcium ionophore and ICSI results in pregnancy. Reprod BioMed Online. 2010;20:559–64.
184.
Tejara A, Mollá M, Muriel L, Remohi J, Pellicer A, De Pablo JL. Successful pregnancy and childbirth after intracytoplasmic sperm injection with calcium ionophore oocyte activation in a globozoospermic patient. Fertil Steril. 2008;90:1202.e1–5.
185.
Aghajanpour S, Ghaedi K, Salamian A, Deemeh MR, Tavalaee M, Moshtaghian J, et al. Quantitative expression of phospholipase C zeta, as an index to assess fertilization potential of a semen sample. Hum Reprod. 2011;26:2950–6.
186.
Kashir J, Sermondade N, Sifer C, Oo SL, Jones C, Mounce G, et al. Motile sperm organelle morphology evaluation-selected globozoospermic human sperm with an acrosomal bud exhibits novel patterns and higher levels of phospholipase C zeta. Hum Reprod. 2012;27:3150–60.
187.
Kamali-Dolat Abadi M, Tavalaee M, Shahverdi A, Nasr-Esfahani MH. Evaluation of PLCζ and PAWP expression in globozoospermic individuals. Cell J. 2016;18:438–45.PubMedPubMedCentral
188.
Sermondade N, Hafhouf E, Dupont C, Bechoua S, Palacios C, Eustache F, et al. Successful childbirth after intracytoplasmic morphologically selected sperm injection without assisted oocyte activation in a patient with globozoospermia. Hum Reprod. 2011;26(11):2944–9.
189.
Esteves SC. Clinical management of infertile men with nonobstructive azoospermia. Asian J Androl. 2015;17(3):459–70.PubMedPubMedCentral
190.
Tanaka A, Nagayoshi M, Takemoto Y, Tanaka I, Kusunoki H, Watanabe S, et al. Fourteen babies born after round spermatid injection into human oocytes. Proc Natl Acad Sci U S A. 2015;112(47):14629–34.
191.
Ogura A, Matsuda J, Yanagimachi R. Birth of normal young after electrofusion of mouse oocytes with round spermatids. Proc Natl Acad Sci U S A. 1994;91(16):7460–2.PubMedPubMedCentral
192.
Kimura Y, Yanagimachi R. Mouse oocytes injected with testicular spermatozoa or round spermatids can develop into normal offspring. Development. 1995;121(8):2397–405.PubMed
193.
Yanagimachi R, Wakayama T, Kishikawa H, Fimia GM, Monaco L, Sassone-Corsi P. Production of fertile offspring from genetically infertile male mice. Proc Natl Acad Sci U S A. 2004;101(6):1691–5.PubMedPubMedCentral
194.
Tesarik J, Mendoza C. Spermatid injection into human oocytes. I. Laboratory techniques and special features of zygote development. Hum Reprod. 1996;11(4):772–9.PubMed
195.
Tesarik J, Rolet F, Brami C, Sedbon E, Thorel J, Tibi C, et al. Spermatid injection into human oocytes. II. Clinical application in the treatment of infertility due to non-obstructive azoospermia. Hum Reprod. 1996;11(4):780–3.
196.
Vanderzwalmen P, Zech H, Birkenfeld A, Yemini M, Bertin G, Lejeune B, et al. Intracytoplasmic injection of spermatids retrieved from testicular tissue: influence of testicular pathology, type of selected spermatids and oocyte activation. Hum Reprod. 1997;12(6):1203–13.
197.
Barak Y, Kogosowski A, Goldman S, Soffer Y, Gonen Y, Tesarik J. Pregnancy and birth after transfer of embryos that developed from single-nucleated zygotes obtained by injection of round spermatids into oocytes. Fertil Steril. 1998;70(1):67–70.PubMed
198.
Gianaroli L, Selman HA, Magli MC, Colpi G, Fortini D, Ferraretti AP. Birth of a healthy infant after conception with round spermatids isolated from cryopreserved testicular tissue. Fertil Steril. 1999;72(3):539–41.PubMed
199.
Van den Veyver IB, Al-Hussaini TK. Biparental hydatidiform moles: a maternal effect mutation affecting imprinting in the offspring. Hum Reprod Update. 2006;12:233–42 3.PubMed
200.
Silber SJ, Johnson L. Are spermatid injections of any clinical value? ROSNI and ROSI revisited. Round spermatid nucleus injection and round spermatid injection. Hum Reprod. 1998;13(3):509–15.PubMed
201.
Silber SJ, Johnson L, Verheyen G, Van Steirteghem A. Round spermatid injection. Fertil Steril. 2000;73(5):897–900.PubMed
202.
Tanaka A, Suzuki K, Nagayoshi M, Tanaka A, Takemoto Y, Watanabe S, et al. Ninety babies born after round spermatid injection into oocytes: survey of their development from fertilization to 2 years of age. Fertil Steril. 2018;110(3):443–51.
203.
Yazawa H, Yanagida K, Sato A. Human round spermatids from azoospermic men exhibit oocyte-activation and Ca2+ oscillation-inducing activities. Zygote. 2007;15(4):337–46.PubMed
204.
Ogonuki N, Inoue K, Ogura A. Birth of normal mice following round spermatid injection without artificial oocyte activation. J Reprod Dev. 2011;57(4):534–8.PubMed
205.
Yazawa H, Yanagida K, Sato A. Oocyte activation and Ca(2+) oscillation-inducing abilities of mouse round/elongated spermatids and the developmental capacities of embryos from spermatid injection. Hum Reprod. 2001;16(6):1221–8.PubMed
206.
Loren J, Lacham-Kaplan O. The employment of strontium to activate mouse oocytes: effects on spermatid-injection outcome. Reproduction. 2006;131(2):259–67.PubMed
207.
Hirabayashi M, Kato M, Hochi S. Factors affecting full-term development of rat oocytes microinjected with fresh or cryopreserved round spermatids. Exp Anim. 2008;57(4):401–5.PubMed
208.
Hirabayashi M, Kato M, Kitada K, Ohnami N, Hirao M, Hochi S. Activation regimens for full-term development of rabbit oocytes injected with round spermatids. Mol Reprod Dev. 2009;76(6):573–9.PubMed
209.
Yazawa H, Yanagida K, Katayose H, Hayashi S, Sato A. Comparison of oocyte activation and Ca2+ oscillation-inducing abilities of round/elongated spermatids of mouse, hamster, rat, rabbit and human assessed by mouse oocyte activation assay. Hum Reprod. 2000;15(12):2582–90.PubMed
210.
Yelumalai S, Yeste M, Jones C, Amdani SN, Kashir J, Mounce G, et al. Total levels, localization patterns, and proportions of sperm exhibiting phospholipase C zeta are significantly correlated with fertilization rates after intracytoplasmic sperm injection. Fertil Steril. 2015;104:561–8.e4.
211.
Ozil JP, Banrezes B, Tóth S, Pan H, Schultz RM. Ca2+ oscillatory pattern in fertilized mouse eggs affects gene expression and development to term. Dev Biol. 2006;300(2):534–44.PubMed
212.
Whitaker M. Calcium signalling in early embryos. Philos Trans R Soc Lond Ser B Biol Sci. 2008;363(1495):1401–18.
213.
Hudmon A, Schulman H. Structure-function of the multifunctional Ca2+/calmodulin-dependent protein kinase II. Biochem J. 2002;364(Pt 3):593–611.PubMedPubMedCentral
214.
Bos-Mikich A, Whittingham DG, Jones KT. Meiotic and mitotic Ca2+ oscillations affect cell composition in resulting blastocysts. Dev Biol. 1997;182(1):172–9.PubMed
215.
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;128:697–702.PubMed
216.
Rogers NT, Halet G, Piao Y, Carroll J, Ko MS, Swann K. The absence of a Ca(2+) signal during mouse egg activation can affect parthenogenetic preimplantation development, gene expression patterns, and blastocyst quality. Reproduction. 2006;132(1):45–57.PubMed
217.
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
218.
Yeste M, Jones C, Amdani SN, Yelumalai S, Mounce G, da Silva SJ, et al. Does advancing male age influence the expression levels and localisation patterns of phospholipase C zeta (PLCζ) in human sperm? Sci Rep. 2016;6:27543.
219.
Kashir J, Buntwal L, Nomikos M, Calver BL, Stamatiadis P, Ashley P, et al. Antigen unmasking enhances visualization efficacy of the oocyte activation factor, phospholipase C zeta, in mammalian sperm. Mol Hum Reprod. 2017;23:54–67.
220.
Ebner T, Montag M, Oocyte Activation Study Group, Montag M, Van der Ven K, Van der Ven H, et al. Live birth after artificial oocyte activation using a ready-to-use ionophore: a prospective multicentre study. Reprod BioMed Online. 2015 Apr;30(4):359–65.
221.
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;17:662–8.PubMed
222.
Ma SF, Liu XY, Miao DQ, Han ZB, Zhang X, Miao YL, et al. Parthenogenetic activation of mouse oocytes by strontium chloride: a search for the best conditions. Theriogenology. 2005;64:1142–57.
223.
Neri QV, Lee B, Rosenwaks Z, Machaca K, Palermo GD. Understanding fertilization through intracytoplasmic sperm injection (ICSI). Cell Calcium. 2014;55:24–37.PubMed
224.
Sanusi R, Yu Y, Nomikos M, Lai FA, Swann K. Rescue of failed oocyte activation after ICSI in a mouse model of male factor infertility by recombinant phospholipase Cζ. Mol Hum Reprod. 2015;21:783–91.PubMedPubMedCentral
225.
Yoon SY, Eum JH, Lee JE, Lee HC, Kim YS, Han JE, et al. Recombinant human phospholipase C zeta 1 induces intracellular calcium oscillations and oocyte activation in mouse and human oocytes. Hum Reprod. 2012;27(6):1768–80.
226.
Nomikos M, Yu Y, Elgmati K, Theodoridou M, Campbell K, Vassilakopoulou V, et al. Phospholipase Cζ rescues failed oocyte activation in a prototype of male factor infertility. Fertil Steril. 2013b;99:76–85.
227.
Miao YL, Stein P, Jefferson WN, Padilla-Banks E, Williams CJ. Calcium influx-mediated signaling is required for complete mouse egg activation. Proc Natl Acad Sci U S A. 2012;109(11):4169–74.PubMedPubMedCentral
228.
Bernhardt ML, Stein P, Carvacho I, Krapp C, Ardestani G, Mehregan A, et al. TRPM7 and CaV3.2 channels mediate Ca2+ influx required for egg activation at fertilization. Proc Natl Acad Sci U S A. 2018;115(44):E10370–8.
229.
Ozil JP, Sainte-Beuve T, Banrezes B. [Mg2+]o/[Ca2+]o determines Ca2+ response at fertilization: tuning of adult phenotype? Reproduction. 2017;154(5):675–93.PubMed
230.
Herrick JR, Strauss KJ, Schneiderman A, Rawlins M, Stevens J, Schoolcraft WB, et al. The beneficial effects of reduced magnesium during the oocyte-to-embryo transition are conserved in mice, domestic cats and humans. Reprod Fertil Dev. 2015;27(2):323–31.
Metadaten
Titel
Increasing associations between defects in phospholipase C zeta and conditions of male infertility: not just ICSI failure?
verfasst von
Junaid Kashir
Publikationsdatum
14.04.2020
Verlag
Springer US
Erschienen in
Journal of Assisted Reproduction and Genetics / Ausgabe 6/2020
Print ISSN: 1058-0468
Elektronische ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-020-01748-z

Weitere Artikel der Ausgabe 6/2020

Journal of Assisted Reproduction and Genetics 6/2020 Zur Ausgabe

Letter to Editor

In response to the article titled Thoughts on the Ethics of Gestational Surrogacy: Perspectives from Religions, Western Liberalism, and Comparisons with Adoption Issue Date: January 2020

Assisted Reproduction Technologies

Blastocyst mitochondrial DNA (mtDNA) is not affected by oocyte vitrification: a sibling oocyte study

Commentary

Ovarian tissue cryopreservation as standard of care: what does this mean for pediatric populations?

Reproductive Physiology and Disease

Delta-9 THC can be detected and quantified in the semen of men who are chronic users of inhaled cannabis

Assisted Reproduction Technologies

Infertility influencers: an analysis of information and influence in the fertility webspace

Reproductive physiology and disease

Role of the superior ovarian nerve in the regulation of follicular development and steroidogenesis in the morning of diestrus 1

Neu im Fachgebiet Gynäkologie und Geburtshilfe

23.04.2024 | Medikamente in Schwangerschaft und Stillzeit | Nachrichten

ICI-Therapie in der Schwangerschaft wird gut toleriert

23.04.2024 | Depression antepartal oder postpartal | Nachrichten

Weniger postpartale Depressionen nach Esketamin-Einmalgabe

22.04.2024 | DGIM 2024 | Kongressbericht | Nachrichten

Bei RSV-Impfung vor 60. Lebensjahr über Off-Label-Gebrauch aufklären!

20.04.2024 | EAU 2024 | Kongressbericht | Nachrichten

Harnwegsinfektprophylaxe: Es geht auch ohne Antibiotika
weitere anzeigen

Update Gynäkologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert – ganz bequem per eMail.

Newsletter bestellen