Total levels, localization patterns, and proportions of sperm exhibiting phospholipase C zeta are significantly correlated with fertilization rates after intracytoplasmic sperm injection

Fertility and Sterility

Volumn 104, Issue 3, 2015, Pages 561-568.e4

  Yelumalai, Suseela ^a   Yeste, Marc ^a   Jones, Celine ^a   Amdani, Siti N ^a   Kashir, Junaid ^a   Mounce, Ginny ^a   Da Silva, Sarah J Martins ^b,c   Barratt, Christopher L ^b,c   McVeigh, Enda ^a   Coward, Kevin ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c NINEWELLS HOSPITAL   (United Kingdom)

Author keywords

In vitro fertilization; intracytoplasmic sperm injection; oocyte activation; phospholipase C zeta; total fertilization failure

Indexed keywords

PHOSPHOLIPASE C; PHOSPHOLIPASE C ZETA; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE PHOSPHODIESTERASE; PLCZ1 PROTEIN, HUMAN;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME LOCALIZATION; FEMALE; FERTILIZATION; FERTILIZATION IN VITRO; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; INFERTILITY; INTRACYTOPLASMIC SPERM INJECTION; MALE; PRIORITY JOURNAL; SEMEN ANALYSIS; SPERM; SPERMATOZOON COUNT; SPERMATOZOON DENSITY; SPERMATOZOON HEAD; SPERMATOZOON MOTILITY; CASE CONTROL STUDY; CLINICAL TRIAL; ENZYMOLOGY; FERTILITY; GREAT BRITAIN; IMMUNOHISTOCHEMISTRY; MIDDLE AGED; MULTICENTER STUDY; PATHOPHYSIOLOGY; SPERMATOZOON; TREATMENT OUTCOME; YOUNG ADULT;

ADULT; BIOMARKERS; CASE-CONTROL STUDIES; FEMALE; FERTILITY; FERTILIZATION IN VITRO; GREAT BRITAIN; HUMANS; IMMUNOHISTOCHEMISTRY; INFERTILITY; MALE; MIDDLE AGED; PHOSPHOINOSITIDE PHOSPHOLIPASE C; SPERM COUNT; SPERM INJECTIONS, INTRACYTOPLASMIC; SPERM MOTILITY; SPERM-OVUM INTERACTIONS; SPERMATOZOA; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84940718062     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2015.05.018     Document Type: Article

References (56)

1. M.N. Mascarenhas, S.R. Flaxman, T. Boerma, S. Vanderpoel, and G.A. Stevens National, regional, and global trends in infertility prevalence since 1990: a systematic analysis of 277 health surveys PLoS Med 9 2012 e1001356
2. Human Fertilisation and Embryology Authority: Fertility treatment in 2012: trends and figures. Available at: http://www.hfea.gov.uk/docs/FertilityTreatment2012TrendsFigures.PDF. Accessed October 11, 2014.
3. S. Bhattacharya, A. Maheshwari, and J. Mollison Factors associated with failed treatment: an analysis of 121,744 women embarking on their first IVF cycles PLoS One 8 2013 e82249
4. G. Palermo, H. Joris, P. Devroey, and A.C. Van Steirteghem Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte Lancet 340 1992 17 18
5. F. Vanden Meerschaut, L. Leybaert, D. Nikiforaki, C. Qian, B. Heindryckx, and P. De Sutter Diagnostic and prognostic value of calcium oscillatory pattern analysis for patients with ICSI fertilization failure Hum Reprod 28 2013 87 98
6. F. Vanden Meerschaut, D. Nikiforaki, B. Heindryckx, and P. De Sutter Assisted oocyte activation following ICSI fertilization failure Reprod Biomed Online 28 2014 560 571
7. M.S. Kupka, A.P. Ferraretti, J. de Mouzon, K. Erb, T. D'Hooghe, J.A. Castilla, and et al. Assisted reproductive technology in Europe, 2010: results generated from European registers by ESHRE Hum Reprod 29 2014 2099 2113
8. K. Yanagida, Y. Fujikura, and H. Katayose The present status of artificial oocyte activation in assisted reproductive technology Reprod Med Biol 7 2008 133 142
9. A.H. Dam, I. Feenstra, J.R. Westphal, L. Ramos, R.J. van Golde, and J.A. Kremer Globozoospermia revisited Hum Reprod Update 13 2007 63 75
10. J.E. Swain, and T.B. Pool ART failure: oocyte contributions to unsuccessful fertilization Hum Reprod Update 14 2008 431 446
11. S.P. Flaherty, D. Payne, and C.D. Matthews Fertilization failures and abnormal fertilization after intracytoplasmic sperm injection Hum Reprod 13 Suppl 1 1998 155 164
12. V.Y. Rawe, S.B. Olmedo, F.N. Nodar, G.D. Doncel, A.A. Acosta, and A.D. Vitullo Cytoskeletal organization defects and abortive activation in human oocytes after IVF and ICSI failure Mol Hum Reprod 6 2000 510 516
13. J. Kashir, B. Heindryckx, C. Jones, P. De Sutter, J. Parrington, and K. Coward Oocyte activation, phospholipase C zeta and human infertility Hum Reprod Update 16 2010 690 703
14. K.T. Jones, J. Carroll, J.A. Merriman, D.G. Whittingham, and T. Kono Repetitive sperm-induced Ca2+ transients in mouse oocytes are cell cycle dependent Development 121 1995 3259 3266
15. V.L. Horner, and M.F. Wolfner Transitioning from egg to embryo: triggers and mechanisms of egg activation Dev Dyn 237 2008 527 544
16. J. Kashir, R. Deguchi, C. Jones, K. Coward, and S.A. Stricker Comparative biology of sperm factors and fertilization-induced calcium signals across the animal kingdom Mol Reprod Dev 80 2013 787 815
17. K. Swann, C.M. Saunders, N.T. Rogers, and F.A. Lai PLCzeta(zeta): a sperm protein that triggers Ca2+ oscillations and egg activation in mammals Semin Cell Dev Biol 17 2006 264 273
18. S.N. Amdani, C. Jones, and K. Coward Phospholipase C zeta (PLCζ): oocyte activation and clinical links to male factor infertility Adv Biol Regul 53 2013 292 308
19. L. Cox, M.G. Larman, C.M. Saunders, K. Hashimoto, K. Swann, and F.A. Lai Sperm phospholipase Czeta from humans and cynomolgus monkeys triggers Ca2+ oscillations, activation and development of mouse oocytes Reproduction 124 2002 611 623
20. C.M. Saunders, M.G. Larman, J. Parrington, L.J. Cox, J. Royse, L.M. Blayney, and et al. PLCζ: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development Development 129 2002 3533 3544
21. S.Y. Yoon, J.H. Eum, J.E. Lee, H.C. Lee, Y.S. Kim, J.E. Han, and et al. Recombinant human phospholipase C zeta 1 induces intracellular calcium oscillations and oocyte activation in mouse and human oocytes Hum Reprod 27 2012 1768 1780
22. M. Nomikos, Y. Yu, K. Elgmati, M. Theodoridou, K. Campbell, V. Vassilakopoulou, and et al. Phospholipase Cζ rescues failed oocyte activation in a prototype of male factor infertility Fertil Steril 99 2013 76 85
23. S.Y. Yoon, T. Jellerette, A.M. Salicioni, H.C. Lee, M.S. Yoo, K. Coward, and 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 118 2008 3671 3681
24. E. Heytens, J. Parrington, K. Coward, C. Young, S. Lambrecht, S.Y. Yoon, and et al. Reduced amounts and abnormal forms of phospholipase C zeta (PLCζ) in spermatozoa from infertile men Hum Reprod 24 2009 2417 2428
25. J. Kashir, C. Jones, G. Mounce, W.M. Ramadan, B. Lemmon, B. Heindryckx, and 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 99 2013 107 117
26. H.C. Lee, M. Arny, D. Grow, D. Dumesic, R.A. Fissore, and T. Jellerette-Nolan Protein phospholipase C Zeta1 expression in patients with failed ICSI but with normal sperm parameters J Assist Reprod Genet 31 2014 749 756
27. J. Kashir, M. Nomikos, F.A. Lai, and K. Swann Sperm-induced Ca2+ release during egg activation in mammals Biochem Biophys Res Commun 450 2014 1204 1211
28. M. Nomikos, J.R. Sanders, M. Theodoridou, J. Kashir, E. Matthews, G. Nounesis, and et al. Sperm-specific post-acrosomal WW-domain binding protein (PAWP) does not cause Ca2+ release in mouse oocytes Mol Hum Reprod 20 2014 938 947
29. P. Grasa, K. Coward, C. Young, and J. Parrington The pattern of localization of the putative oocyte activation factor, phospholipase Czeta, in uncapacitated, capacitated, and ionophore-treated human spermatozoa Hum Reprod 23 2008 2513 2522
30. J. Kashir, A. Heynen, C. Jones, C. Durrans, J. Craig, J. Gadea, and et al. Effects of cryopreservation and density-gradient washing on phospholipase C zeta concentrations in human spermatozoa Reprod Biomed Online 23 2011 263 267
31. J. Escoffier, S. Yassine, H.C. Lee, G. Martinez, J. Delaroche, C. Coutton, and 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 21 2015 157 168
32. World Health Organization (WHO) World Health Organization Laboratory Manual for the Examination and Processing of Human Semen 2010 WHO Geneva
33. J. Kashir, N. Sermondade, C. Sifer, S.L. Oo, C. Jones, G. Mounce, and 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 27 2012 3150 3160
34. G.D. Palermo, Q.V. Neri, T. Takeuchi, and Z. Rosenwaks ICSI: where we have been and where we are going Semin Reprod Med 27 2009 191 201
35. Q.V. Neri, B. Lee, Z. Rosenwaks, K. Machaca, and G.D. Palermo Understanding fertilization through intracytoplasmic sperm injection (ICSI) Cell Calcium 55 2014 24 37
36. D.S. Guzick, J.W. Overstreet, P. Factor-Litvak, C.K. Brazil, S.T. Nakajima, C. Coutifaris, and et al. Sperm morphology, motility, and concentration in fertile and infertile men N Engl J Med 345 2001 1388 1393
37. B.A. Keel Within- and between-subject variation in semen parameters in infertile men and normal semen donors Fertil Steril 85 2006 128 134
38. M.K. Samplaski, A. Agarwal, R. Sharma, and E. Sabanegh New generation of diagnostic tests for infertility: review of specialized semen tests Int J Urol 17 2010 839 847
39. C.L. Barratt, S. Mansell, C. Beaton, S. Tardif, and S.K. Oxenham Diagnostic tools in male infertility-the question of sperm dysfunction Asian J Androl 13 2011 53 58
40. J. Kashir, M. Konstantinidis, C. Jones, B. Heindryckx, P. De Sutter, J. Parrington, and 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 98 2012 423 431
41. J. Kashir, M. Konstantinidis, C. Jones, B. Lemmon, H.C. Lee, R. Hamer, and et al. A maternally inherited autosomal point mutation in human phospholipase C zeta (PLCζ) leads to male infertility Hum Reprod 27 2012 222 231
42. K. Coward, C.P. Ponting, H.-Y. Chang, O. Hibbitt, P. Savolainen, K.T. Jones, and et al. Phospholipase Cζ, the trigger of egg activation in mammals, is present in a non-mammalian species Reproduction 130 2005 157 163
43. K. Coward, C.P. Ponting, N. Zhang, C. Young, C.J. Huang, C.M. Chou, and et al. Identification and functional analysis of an ovarian form of the egg activation factor phospholipase C zeta (PLCζ) in pufferfish Mol Reprod Dev 78 2011 48 56
44. M. Ito, T. Shikano, S. Oda, T. Horiguchi, S. Tanimoto, T. Awaji, and 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 78 2008 1081 1090
45. S. Mizushima, S. Takagi, T. Ono, Y. Atsumi, A. Tsukada, N. Saito, and et al. Phospholipase Czeta mRNA expression and its potency during spermatogenesis for activation of quail oocyte as a sperm factor Mol Reprod Dev 76 2009 1200 1207
46. A.T. Wu, P. Sutovsky, G. Manandhar, W. Xu, M. Katayama, B.N. Day, and et al. PAWP, a sperm-specific WW domain-binding protein, promotes meiotic resumption and pronuclear development during fertilization J Biol Chem 282 2007 12164 12175
47. M. Aarabi, H. Balakier, S. Bashar, S.I. Moskovtsev, P. Sutovsky, C.L. Librach, and et al. Sperm-derived WW domain-binding protein, PAWP, elicits calcium oscillations and oocyte activation in humans and mice FASEB J 28 2014 4434 4440
48. M. Aarabi, Z. Qin, W. Xu, J. Mewburn, and R. Oko Sperm-borne protein, PAWP, initiates zygotic development in Xenopus laevis by eliciting intracellular calcium release Mol Reprod Dev 77 2010 249 256
49. M. Aarabi, H. Balakier, S. Bashar, S.I. Moskovtsev, P. Sutovsky, C.L. Librach, and et al. Sperm content of postacrosomal WW binding protein is related to fertilization outcomes in patients undergoing assisted reproductive technology Fertil Steril 102 2014 440 447
50. M. Aarabi, P. Sutovsky, and R. Oko Re: Is PAWP the 'real' sperm factor? Asian J Androl 17 2015 446 449
51. M. Nomikos, K. Swann, and F.A. Lai Is PAWP the "real" sperm factor? Asian J Androl 17 2015 444 446
52. M.L. Vadnais, and L.G. Gerton From PAWP to "Pop": opening up new pathways to fatherhood Asian J Androl 17 2015 443 444
53. R. Beck-Fruchter, M. Lavee, A. Weiss, Y. Geslevich, and E. Shalev Rescue intracytoplasmic sperm injection: a systematic review Fertil Steril 101 2014 690 698
54. N.G. Mahutte, and A. Arici Failed fertilization: Is it predictable? Curr Opin Obstet Gynecol 15 2003 211 218
55. W.M. Ramadan, J. Kashir, C. Jones, and K. Coward Oocyte activation and phospholipase C zeta (PLCζ): diagnostic and therapeutic implications for assisted reproductive technology Cell Commun Signal 10 2012 12
56. M. Nomikos, K. Swann, and F.A. Lai Starting a new life: sperm PLC-zeta mobilizes the Ca2+ signal that induces egg activation and embryo development: an essential phospholipase C with implications for male infertility Bioessays 34 2012 126 134