Purpose: The aim of this study was to evaluate expression of Post-Acrosomal WW Binding Protein (PAWP) in infertile men with low and high fertilization post ICSI and also globozoospermic men.
Materials and Methods: Semen samples were collected from 18 infertile men with previously failed or low fertilization (< 25%) post ICSI, 10 men with high fertilization (>50%) post ICSI, 15 globozoospermic men, and 21 fertile individuals. Then, expression of PAWP was assessed at RNA with quantitative Real Time PCR.
Results: Relative expression of PAWP in sperm was significantly (P < .05) lower in infertile men with globozoospermia (41.5 ± 5.7) or low fertilization rate (43.3±10.4) compared to fertile (138.8 ± 17.3)or men with high fertilization (211.6 ± 75.6). In addition, a significant positive correlation (r = 0.628; P = .001) was observed between percentage of fertilization with the relative expression of PAWP.
Conclusion: Considering solid recent evidences regarding PLC? as the main sperm factor involved in oocyte activation, therefore co-localization of PLC? with PAWP in perinuclear theca may account for the above observation and it is likely that PAWP may have other functions and/or it may assist PLC?.
Bonduelle M, Camus M, De Vos A, Staessen C, Tournaye H, Van Assche E, Verheyen G, Devroey P, Liebaers I, Van Steirteghem A. Seven years of intracytoplasmic sperm injection and follow-up of 1987 subsequent children. Hum Reprod. 1999; 1: 243-264.
Nudell D M, Lipshultz L I. Is intracytoplasmic sperm injection safe? Current status and future concerns. Curr Urol Rep. 2001; 2: 423-431.
Flaherty S P, Payne D, Matthews C D. Fertilization failures and abnormal fertilization after intracytoplasmic sperm injection. Hum Reprod.1998; 1:155-164.
Sousa M, Tesarik J Ultrastructural analysis of fertilization failure after intracytoplasmic sperm injection. Hum Reprod. 1994;9: 2374-2380.
Emery B R, Wilcox A L, Aoki V W, Peterson C M, Carrell D T. In vitro oocyte maturation and subsequent delayed fertilization is associated with increased embryo aneuploidy. Fertil Steril. 2005; 84: 027–1029.
Van Blerkom J Sperm centrosome dysfunction: a possible new class of male factor infertility in the human. Mol Hum Reprod.1996; 2: 349–354.
Nasr-Esfahani MH, Razavi S, Tavalaee M. Failed fertilization after ICSI and spermiogenic defects. Fertil Steril. 2008; 89: 892-8.
Tavalaee M, Razavi S, Nasr-Esfahani MH. Influence of sperm chromatin anomalies on assisted reproductive technology outcome. Fertil Steril. 2009; 91:1119-26.
Swain J E, Pool T B. ART failure: oocyte contributions to unsuccessful fertilization. Hum Reprod. 2008;14: 431–446.
Dozortsev D, Qian C, Ermilov A, Rybouchkin A, De Sutter P, Dhont M. Sperm-associated oocyte-activating factor is released from the spermatozoon within 30 minutes after injection as a result of the sperm-oocyte interaction. Hum Reprod. 1997;12: 2792-2796.
Muciaccia B, Sette C, Paronetto M P, Barchi M, Pensini S, D'Agostino A, Gandini L, Geremia R, Stefanini M, Rossi P. Expression of a truncated form of KIT tyrosine kinase in human spermatozoa correlates with sperm DNA integrity. Hum Reprod. 2010; 25: 2188-2202.
Oko R, Sutovsky P. Biogenesis of sperm perinuclear theca and its role in sperm functional competence and fertilization. J Reprod Immunol. 2009; 83:2–7.
Machaca K. Ca2+ signaling differentiation during oocyte maturation. J Cell Physiol. 2007; 213: 331–340.
Balakier H, Dziak E, Sojecki A, Librach C, Michalak M, Opas M. Calcium-binding proteins and calcium-release channels in human maturing oocytes, pronuclear zygotes and early preimplantation embryos. Hum Reprod. 2002;17: 2938-47.
Aarabi M, Yu Y, Xu W, Tse MY, Pang SC, Yi YJ, Sutovsky P, Oko R. 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.
Fujimoto S, Yoshida N, FukuiT, Amanai M, Isobe T, Itagaki C, Izumi T, Perry A C. Mammalian phospholipase Czeta induces oocyte activation from the sperm perinuclear matrix. Dev Biol. 2004; 274: 370-383
Saunders C M, Larman M G, Parrington J, Cox L J, Royse J, Blayney L M, Swann K, Lai F A. PLC zeta: a sperm-specific trigger of Ca (2+) oscillations in eggs and embryo development. Development. 2002;129: 3533-3544.
Wu, AT, Sutovsky P, Manandhar G, Xu W, Katayama M, Day B N, Park K W, Yi Y J, Xi Y W, Prather R S, Oko R, PAWP, a sperm-specific WW domain-binding protein, promotes meiotic resumption and pronuclear development during fertilization. J. Biol. Chem. 2007; 282: 12164-12175.
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.
Muciaccia B, Sette C, Paronetto MP, Barchi M, Pensini S, D'Agostino A, Gandini L, Geremia R, Stefanini M, Rossi P. Expression of a truncated form of KIT tyrosine kinase in human spermatozoa correlates withsperm DNA integrity. Hum Reprod. 2010; 25:2188-202.
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: 797-808.
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: 2513–2522.
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: 2417-2428.
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. 2011; 26: 3372-87.
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. 2012; 27: 222-31.
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: 3671-81.
Kashir J, Jones C, Mounce G, Ramadan WM, Lemmon B, Heindryckx B et al. Variance in total levels of phospholipase C zeta (PLC-ζ) 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.
Wu, A. T., Sutovsky, P., Xu, W., van der Spoel, A. C., Platt, F. M., Oko, R. The postacrosomal assembly of sperm head protein, PAWP, is independent of acrosome formation and dependent on microtubular manchette transport. Dev. Biol. 2007; 312: 471–483.
Aarabi M, Balakier H, Bashar S, Moskovtsev SI, Sutovsky P, Librach CL, Oko R. Sperm content of postacrosomal WW binding protein is related to fertilization outcomes in patients undergoing assisted reproductive technology. Fertil Steril. 2014; 102: 440-7.
Nomikos M, Sanders JR, Theodoridou M, Kashir J, Matthews E, Nounesis G, Lai FA, Swann K. Sperm-specific post-acrosomal WW-domain binding protein (PAWP) does not cause Ca2+ release in mouse oocytes. Mol Hum Reprod. 2014; 20:938-47.
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; 36:348-355.
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: 588-596.
Aghajanpour S, Ghaedi K, Salamian A, Deemeh MR, Tavalaee M, Moshtaghian J, Parrington J, Nasr-Esfahani MH. Quantitative expression of phospholipase C zeta, as an index to assess fertilization potential of a semen sample. Hum Reprod. 2011; 26: 2950-6.
World Health Organization. WHO Laboratory Manual for the Examination and Processing of Human Semen 5th edn. Cambridge, UK: Cambridge University Press. 2010.
Nasr-Esfahani M H, Tavalaee M, Deemeh M R, Arbabian M, Parrington J. Can Assessment of Total Acrosin Activity Help Predict Failed or Low Fertilization Rate ICSI for Implementation of Artificial Oocyte Activation? Open Androl J. 2010; 2:19–26.
Vaerman J L, Saussoy P, Ingargiola I. Evaluation of real-time PCR data. J. Biol. Regul Homeost. Agents. 2004 ;18: 212–214.
Berridge M J. Inositol trisphosphate and calcium signalling mechanisms. Biochim. Biophys Acta. 2009;1793: 933-940.
Swann K, Larman M G, Saunders C M, Lai F A. The cytosolic sperm factor that triggers Ca2+ oscillations and egg activation in mammals is a novel phospholipase C: PLCzeta. Reproduction. 2004; 127: 431-439.
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.
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.
Bechoua S, Chiron A, Delcleve-Paulhac S, Sagot P, Jimenez C. Fertilisation and pregnancy outcome after ICSI in globozoospermic patients without assisted oocyte activation. Andrologia. 2009 ;41: 55-58.
Elinati E, Kuentz P, Redin C, Jaber S, Vanden Meerschaut F, Makarian J, Koscinski I, Nasr-Esfahani M H, Demirol A, Gurgan T, Louanjli N, Iqbal N, Bisharah M, Pigeon F C, Gourabi H, De Briel D, Brugnon F, Gitlin S A, Grillo J M, Ghaedi K, Deemeh M R, Tanhaei S, Modarres P, Heindryckx B, Benkhalifa M, Nikiforaki D, Oehninger S C, De Sutter P, Muller J, Viville S. Globozoospermia is mainly due to DPY19L2 deletion via non-allelic homologous recombination involving two recombination hotspots. Hum Mol Genet. 2012; 21: 3695-3702.
Stone S, O'Mahony F, Khalaf Y, Taylor A, Braude P. A normal livebirth after intracytoplasmic sperm injection for globozoospermia without assisted oocyte activation: case report. Hum Reprod. 2000;15:139-141.
Kuentz P, Vanden Meerschaut F, Elinati E, Nasr-Esfahani M H, Gurgan T, Iqbal N, Carré-Pigeon F, Brugnon F, Gitlin S A, Velez de la Calle J, Kilani Z, De Sutter P, Viville S. Assisted oocyte activation overcomes fertilization failure in globozoospermic patients regardless of the DPY19L2 status. Hum Reprod. 2013; 28: 1054-1061.
Hecht N, Cavalcanti M C, Nayudu P, Behr R, Reichenbach M, Weidner W, Steger K. Protamine-1 represents a sperm specific gene transcript: a study in Callithrix jacchus and Bos taurus. Andrologia. 2011;43: 167-173.
Azad N, Nazarian H, Nazari L, Ghaffari Novin M, Piryaei A, Heidari MH, Masteri Farahani R, Sadjadpour SS. Evaluation of PAWP and PLC? Expression in Infertile Men with Previous ICSI Fertilization Failure. Urol J. 2018; 4.
Satouh Y, Nozawa K, Ikawa M. Sperm postacrosomal WW domain-binding protein is not required for mouse egg activation. Biol Reprod. 2015; 93: 94.
Freour T, Barragan M, Ferrer-Vaquer A, Rodríguez A, Vassena R. WBP2NL/PAWP mRNA and protein expression in sperm cells are not related to semen parameters, fertilization rate, or reproductive outcome. J Assist Reprod Genet. 2017;34: 803-810.