Sperm factors and oocyte activation: Current controversies and considerations

Biology of Reproduction

Volumn 93, Issue 2, 2015, Pages

  Amdani, Siti Nornadhirah ^a,b   Yeste, Marc ^a   Jones, Celine ^a   Coward, Kevin ^a  

^a JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^b UNIVERSITI BRUNEI DARUSSALAM   (Brunei Darussalam)

Author keywords

Intracellular calcium (Ca2+); Oocyte activation; PAWP; Perinuclear theca (PT); PLC ; Sperm oocyte activating factor (SOAF)

Indexed keywords

CALCIUM ION; CITRATE SYNTHASE; GLUTAMINE FRUCTOSE 6 PHOSPHATE AMINOTRANSFERASE; PHOSPHOLIPASE C; PHOSPHOLIPASE C ZETA 1; PROTEIN; SPERM OOCYTE ACTIVATING FACTOR; UNCLASSIFIED DRUG; WW DOMAIN BINDING PROTEIN 2;

CALCIUM CELL LEVEL; CALCIUM SIGNALING; EMBRYO DEVELOPMENT; FERTILIZATION; GAMETE; HUMAN; INTRACYTOPLASMIC SPERM INJECTION; MALE INFERTILITY; NONHUMAN; OOCYTE; PRIORITY JOURNAL; SHORT SURVEY; SPERM; SPERMATID; SPERMATOGENESIS; SPERMATOZOON HEAD; ANIMAL; FEMALE; FERTILITY; MALE; PHYSIOLOGY; PREGNANCY; SPERMATOZOON;

ANIMALS; CALCIUM SIGNALING; FEMALE; FERTILIZATION; HUMANS; MALE; OOCYTES; PREGNANCY; SPERM-OVUM INTERACTIONS; SPERMATOZOA;

EID: 84941559686     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.115.130609     Document Type: Short Survey

References (80)

1. Kline D, Kline JT. Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg. Dev Biol 1992; 149: 80-99.
2. Stricker SA. Comparative biology of calcium signalling during fertilization and egg activation in mammals. Dev Biol 1999; 211:157-176.
3. Ducibella T, Fissore R. The roles of Ca2+, downstream protein kinases, and oscillatory signalling in regulating fertilization and the activation of development. Dev Biol 2007; 315:257-279.
4. Kashir J, Deguchi R, Jones C, Coward K, Stricker S. Comparative biology of sperm factors and fertilization-induced calcium signals across the animal kingdom. Mol Reprod Dev 2013; 80:787-815.
5. Swann K, Yu Y. The dynamics of calcium oscillations that activate mammalian eggs. Int J Dev Biol 2008; 52:585-594.
6. Carroll J. The initiation and regulation of Ca2+ signalling at fertilization in mammals. Semin Cell Dev Biol 2001; 12:37-43.
7. Saunders CM, Larman MG, Parrington J, Cox LJ, Royse J, Blayney LM, Swann K, Lai FA. PLC Zeta: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development. Development 2002; 129:3533-3544.
8. Saunders CM, Swann K, Lai FA. PLCζ, a sperm-specific PLC and its potential role in fertilization. Biochem Soc Symp 2007; 74:23-36.
9. Wu AT, Sutovsky P, Manandhar G, Xu W, Katayama M, Day BN, Park KW, Yi YJ, Xi YW, Prather RS, 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.
10. Dale B, Wilding M, Coppola G, Tosti E. How do spermatozoa activate oocytes? Reprod Biomed Online 2010; 21:1-3.
11. 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.
12. Nomikos M, Yu Y, Elgmati K, Theodoridou M, Campbell K, Vassilakopoulou V, Zikos C, Livaniou E, Amso N, Nounesis G, Swann K, Lai FA. Phospholipase Cζ rescues failed oocyte activation in a prototype of male factor infertility. Fertil Steril 2013; 99:76-85.
13. Nomikos M, Swann K, Lai FA. Is PAWP the ''real'' sperm factor? Asian J Androl 2015; 17:444-446.
14. Aarabi M, Balakier H, Bashar S, Moskovtsev SI, Sutovsky P, Librach CL, Oko R. Sperm-derived WW domain-binding protein, PAWP, elicits calcium oscillations and oocyte activation in humans and mice. FASEB 2014; 28:4434-4440.
15. Aarabi M, Sutovsky P, Oko R. Re: Is PAWP the ''real'' sperm factor? Asian J Androl 2015; 17:446-449.
16. Swann K. A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs. Development 1990; 110: 1295-1302.
17. Miyazaki S, Shirakawa H, Nakada K, Honda Y. Essential role of the inositol 1,4,5-triphosphate receptor/Ca2+ release channel in Ca2+ waves and Ca2+ oscillations at fertilization in mammalian eggs. Dev Biol 1993; 158:62-78.
18. Ducibella T, Huneau D, Angelichio E, Xu Z, Schultz RM, Kopf GS, Fissore R, Madoux S, Ozil JP. Egg-to-embryo transition is driven by differential responses to Ca2+ oscillation number. Dev Biol 2002; 250: 280-291.
19. Miyazaki S, Ito M. Calcium signals for egg activation in mammals. J Pharmacol Sci 2006; 100:545-552.
20. Whitaker M. Calcium at fertilization and in early development. Physiol Rev 2006; 86:25-88.
21. Von Stetina JR, Orr-Weaver TL. Developmental control of oocyte maturation and egg activation in metazoan models. Cold Spring Harb Perspect Biol 2011; 3:a005553.
22. Amdani SN, Jones C, Coward K. Phospholipase C zeta (PLCζ): oocyte activation and clinical links to male factor infertility. Adv Biol Regul 2013; 53:292-308.
23. Wakai T, Zhang N, Vangheluwe P, Fissore RA. Regulation of endoplasmic reticulum Ca(2+) oscillations in mammalian eggs. J Cell Sci 2013; 126:5714-5724.
24. Lee S, Yoon Y, Fissore RA. Regulation of fertilization-initiated [Ca2+]i oscillations in mammalian eggs; a multi-prolonged approach. Semin Cell Dev Biol 2006; 17:274-284.
25. Nomikos M, Swann K, Lai FA. Starting a new life: sperm PLC-zeta mobilizes the Ca2+ signal that induces egg activation and embryo development. Bioessays 2011; 34:126-134.
26. Ramadan WM, Kashir J, Jones C, Coward K. Phospholipase C zeta and its potential role in infertility treatment. Cell Commun Signal 2012; 10:12.
27. Gresset A, Sondek J, Harden TK. The phospholipase C isozymes and their regulation. Subcell Biochem 2012; 58:61-94.
28. Coward K, Ponting CP, Zhang N, Young C, Huang CJ, Chou CM, Kashir J, Fissore RA, Parrington J. 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.
29. 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; 61:362-378.
30. Aul RB, Oko RJ. The major subacrosomal occupant of bull spermatozoa is a novel histone H2B variant associated with the forming acrosome during spermiogenesis. Dev Biol 2002; 242:376-387.
31. Kimura Y, Yanagimachi R, Kuretake S, Bortkiewicz H, Perry AC, Yanagimachi H. Analysis of mouse oocyte activation suggests the involvement of sperm perinuclear material. Biol Reprod 1998; 58: 1407-1415.
32. Perry AC, Wakayama T, Yanagimachi R. A novel trans-complementation assay suggests full mammalian oocyte activation is coordinately initiated by multiple, submembrane sperm components. Biol Reprod 1999; 60: 747-755.
33. Perry AC, Wakayama T, Cooke IM, Yanagimachi R. Mammalian oocyte activation by the synergistic action of discrete sperm head components: induction of calcium transients and involvement of proteolysis. Dev Biol 2000; 217:386-393.
34. Swann K, Igusa Y, Miyazaki S. Evidence of an inhibitory effect of protein kinase C on G-protein-mediated repetitive calcium transients in hamster eggs. EMBO J 1989; 8:3711-3718.
35. Parrington J, Swann K, Schevchenko VI, Sesay AK, Lai FA. Calcium oscillations in mammalian eggs triggered by a soluble sperm factor. Nature 1996; 379:364-368.
36. Parrington J. Does a soluble sperm factor trigger calcium release in the egg at fertilization? J Androl 2001; 22:1-11.
37. Parrington J, Davis LC, Galione A, Wessel G. Flipping the switch: how a sperm activated the egg at fertilization. Dev Dyn 2007; 236:2027-2038.
38. Rybouchkin AV, Van der Straeten F, Quatacker J, De Sutter P, Dhont M. Fertilization and pregnancy after assisted oocyte activation and intracytoplasmic sperm injection in a case of round-headed sperm associated with deficient oocyte activation capacity. Fertil Steril 1997; 68:1144-1147.
39. 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; 17:662-668.
40. Vanden Meerschaut F, Leybaert L, Nikiforaki D, Qian C, Heindryckx B, De Sutter P. Diagnostic and prognostic value of calcium oscillatory pattern analysis for patients with ICSI fertilization failure. Hum Reprod 2012; 28: 87-98.
41. 2+ signaling at fertilization. Curr Top Dev Biol 1998; 39:215-243.
42. Montag M, Parrington J, Swann K, Lai FA, van der Ven H. Presence and localization of oscillin in human spermatozoa in relation to the integrity of the sperm membrane. FEBS Lett 1998; 423:357-361.
43. Wolosker H, Kline D, Bian Y, Blackshaw S, Cameron AM, Fralich TJ, Schnaar RL, Snyder SH. Molecularly cloned mammalian glucosamine-6-phosphate deaminase localizes to transporting epithelium and lacks oscillin activity. FASEB J 1998; 12:91-99.
44. 2+ release in mammalian oocytes. Mol Reprod Dev 1999; 52:277-287.
45. Fissore RA, Reis MM, Palermo GD. Isolation of the Ca2+ releasing component(s) of mammalian sperm extracts: the search continues. Mol Hum Reprod 1999; 5:189-192.
46. 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.
47. Yoneda A, Kashima M, Yoshida S, Terada K, Nakagawa S, Sakamoto A, Hayakawa K, Suzuki K, Ueda J, Watanabe T. Molecular cloning, testicular postnatal expression, and oocyte-activating potential of porcine phospholipase Czeta. Reproduction 2006; 132:393-401.
48. 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: 2230-2242.
49. Wu AT, Sutovsky P, Xu W, van der Spoel AC, Platt FM, 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.
50. Ito C, Yamatoya K, Yoshida K, Kyono K, Yao R, Noda T, Toshimori K. Appearance of an oocyte activation-related substance during spermatogenesis in mice and humans. Hum Reprod 2010; 25:2734-2744.
51. 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; 102:440-447.
52. Fujimoto S, Yoshida N, Fukui T, Amanai M, Isobe T, Itagaki C, Izumi T, Perry AC. Mammalian phospholipase Czeta induces oocyte activation from the sperm perinuclear matrix. Dev Biol 2004; 274:370-383.
53. Swann K, Saunders CM, Rogers NT, Lai FA. PLC Zeta (zeta): a sperm protein that triggers Ca2+ oscillations and egg activation in mammals. Semin Cell Dev Biol 2006; 17:264-273.
54. Yoon SY, Fissore RA. Release of phospholipase C zeta and [Ca2+]I oscillation-inducing activity during mammalian fertilization. Reproduction 2007; 134:695-704.
55. Grasa P, Coward K, Young C, Parrington J. The pattern of localization of the putative oocyte activation factor, phospholipase C zeta, in uncapacitated, capacitated, and ionophore-treated human spermatozoa. Hum Reprod 2008; 23:2513-2522.
56. Escoffier J, Yassine S, Lee HC, Martinez G, Delaroch J, Coutton C, Karaouzene T, Zouari R, Metzler-Guillemain C, Pernet-Gallay K, Hennebicq S, Ray PF, 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: 157-168.
57. Nomikos M, Elgmati K, Theodoridou M, Georgilis A, Gonzalez-Garcia JR, Nounesis G, Swann K, Lai FA. Novel regulation of PLCζ activity via its XY-linker. Biochem J 2011; 438:427-432.
58. 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; 77:249-256.
59. Swann K, Lai FA. PLCζ and the initiation of Ca2+ oscillations in fertilizing mammalian eggs. Cell Calcium 2013; 53:55-62.
60. Kashir J, Jones C, Lee HC, Rietdorf K, Nikiforaki D, Durrans C, Ruas M, Tee ST, Heindryckx B, Galione A, De Sutter P, Fissore RA, et al. Loss of activity mutation in phospholipase C zeta (PLCζ) abolishes calcium oscillatory ability of human recombinant protein in mouse oocytes. Hum Reprod 2011; 26:3372-3387.
61. 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 Ca2+ release and are unable to initiate the first step of embryo development. J Clin Invest 2008; 118:3671-3681.
62. Heytens E, Parrington J, Coward K, Young C, Lambrecht S, Yoon SY, Fissore RA, Hamer R, Deane CM, Ruas M, Grasa P, Soleimani R, et al. Reduced amounts and abnormal forms of phospholipase C zeta (PLCzeta) in spermatozoa from infertile men. Hum Reprod 2009; 24:2417-2428.
63. Kashir J, Konstantinidis M, Jones C, Lemmon B, Lee HC, Hamer R, Heindryckx B, Deane CM, De Sutter P, Fissore RA, Parrington J, Wells D, et al. A maternally inherited autosomal point mutation in human phospholipase C zeta (PLCζ) leads to male infertility. Hum Reprod 2012; 27:222-231.
64. Pan Q, Ju Z, Huang J, Zhang Y, Qi C, Gao Q, Zhou L, Li Q, Wang L, Zhong J, Liu M, Wang C. PLCz functional haplotypes modulating promoter transcriptional activity are associated with semen quality traits in Chinese Holstein bulls. PLoS One 2013; 8:e58795.
65. Kennedy CE, Krieger KB, Sutovsky M, Xu W, Vargovic P, Didion BA, Ellersieck MR, Hennessy ME, Verstegen J, Oko, R, Sutovsky P. Protein expression pattern of PAWP in bull spermatozoa is associated with sperm quality and fertility following artificial insemination. Mol Reprod Dev 2014; 81:436-449.
66. Knott JG, Kurokawa M, Fissore RA, Schultz RM, Williams CJ. Transgenic RNA interference reveals role for mouse sperm phospholipase C zeta triggering Ca2+ oscillation during fertilization. Biol Reprod 2005; 72:992-996.
67. Kouchi Z, Fukami K, Shikano T, Oda S, Nakamura Y, Takenawa T, Miyazaki S. Recombinant phospholipase Czeta has high Ca2+ sensitivity and induces Ca2+ oscillations in mouse eggs. J Biol Chem 2004; 279: 10408-10412.
68. Nomikos M, Blayney LM, Larman MG, Campbell K, Rossbach A, Saunders CM, Swann K, Lai FA. Role of phospholipase C-zeta domains in Ca2+-dependent phosphatidylinositiol 4,5-biphosphate hydrolysis and cytoplasmic Ca2+ oscillations. J Biol Chem 2005; 280:31011-31018.
69. Aarabi M, Yu Y, Xu W, Tse MY, Pang SC, Yi YJ. 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.
70. Yelumalai S, Yeste M, Jones C, Amdani SN, Kashir J, Mounce G, Da Silva SM, Barratt CL, McVeigh E, Coward K. Total levels, localization patterns and proportions of sperm exhibiting phospholipase C zeta (PLCζ) are significantly correlated with fertilization rates following intracytoplasmic sperm injection. Fertil Steril (in press). Published online ahead of print 12 June 2015; DOI 10.1016/j.fertnstert.2015.05.018.
71. Nasr-Esfahani MH, Deemeh MR, Tavalaee M. Artificial oocyte activation intracytoplasmic sperm injection. Fertil Steril 2010; 94:520-526.
72. Yoon SY, Eum JH, Lee JE, Lee HC, Kim YS, Han JE, Won HJ, Park SH, Shim SH, Lee WS, Fissore RA, Lee DR, et al. Recombinant human phospholipase C zeta 1 induces intracellular calcium oscillations and oocyte activation in mouse and human oocytes. Hum Reprod 2012; 27: 1768-1780.
73. Cooney MA, Malcuit C, Cheon B, Holland MK, Fissore RA, D'Cruz NT. Species-specific differences in the activity and nuclear localization of murine and bovine phospholipase C zeta 1. Biol Reprod 2010; 83:92-101.
74. Kashir J, Sermondade N, Sifer C, Oo SL, Jones C, Mounce G, Turner K, Child T, McVeigh E, Coward K. 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; 27:3150-3160.
75. Kashir J, Jones C, Mounce G, Ramadan WM, Lemmon B, Heindryckx B, De Sutter P, Parrington J, Turner K, Child T, McVeigh E, Coward K. Variance in total levels of phospholipase C zeta (PLC-f) in human sperm may limit the applicability of quantitative immunofluorescent analysis as a diagnostic indicator of oocyte activation capability. Fertil Steril 2013; 99: 107-117.
76. Zanetti N, Mayorga LS. Acrosomal swelling and membrane docking are required for hybrid vesicle formation during the human sperm acrosome reaction. Biol Reprod 2009; 81:396-405.
77. 2+ release in mouse oocytes. Mol Hum Reprod 2014; 20:938-947.
78. Vadnais ML, Gerton GL. From PAWP to ''Pop'': opening up new pathways to fatherhood. Asian J Androl 2015; (in press). Published online ahead of print 23 January 2015; DOI:10.4103/1008-682X.142140.
79. Ito M, Nagaoka K, Kuroda K, Kawano N, Yoshida K, Harada Y, Shikano T, Miyado M, Oda S, Toshimori K, Mizukami Y, Murata T, et al. Arrest of spermatogenesis at round spermatids in PLCz1 deficient mice. In: Abstracts of the 11th International Symposium on Spermatology; June 26-June 29, 2010; Okinawa, Japan.
80. Universal Protein Resource [Internet]. http://www.uniprot.org/. Accessed 18 March 2015.