Phospholipase Cζ (PLCζ) versus postacrosomal sheath WW domain-binding protein (PAWP): Which molecule will survive as a sperm factor?
calcium
fertilization
oocyte
phospholipase C
sperm
Journal
Animal science journal = Nihon chikusan Gakkaiho
ISSN: 1740-0929
Titre abrégé: Anim Sci J
Pays: Australia
ID NLM: 100956805
Informations de publication
Date de publication:
Historique:
received:
03
11
2019
revised:
26
12
2019
accepted:
27
12
2019
entrez:
29
3
2020
pubmed:
29
3
2020
medline:
29
8
2020
Statut:
ppublish
Résumé
During mammalian fertilization, sperm is fused with the oocyte's membrane, triggering the resumption of meiosis from the metaphase II arrest, the extrusion of the second polar body, and the exocytosis of cortical granules; these events are collectively called 'oocyte activation.' In all species studied to date, the transient rise in the cytosolic level of calcium (in particular, the repeated calcium increases called 'calcium oscillations' in mammals) is required for these events. Researchers have focused on identifying the factor(s) that can induce calcium oscillations during fertilization. Sperm-specific phospholipase C, i.e., PLC zeta (PLCζ), is a strong candidate of the factor(s), and several research groups using different species obtained evidence that PLCζ is a sperm factor that can induce calcium oscillations during fertilization. However, postacrosomal sheath Tryptophan-Tryptophan (WW)-domain-binding protein (PAWP) was recently shown to have a pivotal role in inducing calcium oscillations in some species. In this review, we focus on PLCζ and PAWP as sperm factors, and we discuss this controversy: Which of these two molecules survives as a sperm factor?
Identifiants
pubmed: 32219949
doi: 10.1111/asj.13345
pmc: PMC7140179
doi:
Substances chimiques
Carrier Proteins
0
Seminal Plasma Proteins
0
WBP2NL protein, human
0
Phospholipases
EC 3.1.-
Calcium
SY7Q814VUP
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13345Subventions
Organisme : Japan Society for the Promotion of Science
ID : 15H04584
Pays : International
Organisme : Japan Society for the Promotion of Science
ID : 17K08054
Pays : International
Organisme : Ministry of Education, Culture, Sports, Science and Technology
Pays : International
Informations de copyright
© 2020 The Authors. Animal Science Journal published by John Wiley & Sons Australia, Ltd on behalf of Japanese Society of Animal Science.
Références
Aarabi, M., Balakier, H., Bashar, S., Moskovtsev, S. I., Sutovsky, P., Librach, C. L., & Oko, R. (2014a). Sperm content of postacrosomal WW binding protein is related to fertilization outcomes in patients undergoing assisted reproductive technology. Fertility and Sterility, 102(2), 440-447. https://doi.org/10.1016/j.fertnstert.2014.05.003
Aarabi, M., Balakier, H., Bashar, S., Moskovtsev, S. I., Sutovsky, P., Librach, C. L., & Oko, R. (2014b). Sperm-derived WW domain-binding protein, PAWP, elicits calcium oscillations and oocyte activation in humans and mice. FASEB Journal, 28(10), 4434-4440. https://doi.org/10.1096/fj.14-256495
Aarabi, M., Qin, Z., Xu, W., Mewburn, J., & Oko, R. (2010). Sperm-borne protein, PAWP, initiates zygotic development in xenopus laevis by eliciting intracellular calcium release. Molecular Reproduction and Development, 77(3), 249-256. https://doi.org/10.1002/mrd.21140
Bedford-Guaus, S. J., McPartlin, L. A., Xie, J., Westmiller, S. L., Buffone, M. G., & Roberson, M. S. (2011). Molecular cloning and characterization of phospholipase C ζ in equine sperm and testis reveals species-specific differences in expression of catalytically active protein. Biology of Reproduction, 85(1), 78-88. https://doi.org/10.1095/biolreprod.110.089466
Bedford-Guaus, S. J., Yoon, S. J., Fissore, R. A., Choi, Y. H., & Hinrichs, K. (2008). Microinjection of mouse phospholipase C zeta complementary RNA into mare oocytes induces long-lasting intracellular calcium oscillations and embryonic development. Reproduction, Fertility and Development, 20(8), 875-883. https://doi.org/10.1071/RD08115
Bernhardt, M. L., Kong, B. Y., Kim, A. M., O'Halloran, T. V., & Woodruff, T. K. (2012). A zinc-dependent mechanism regulates meiotic progression in mammalian oocytes. Biology of Reproduction, 86(4), 114. https://doi.org/10.1095/biolreprod.111.097253
Bittova, L., Sumandea, M., & Cho, W. (1999). A structure-function study of the C2 domain of cytosolic phospholipase A2. Identification of essential calcium ligands and hydrophobic membrane binding residues. Journal of Biological Chemistry, 274(14), 9665-9672. https://doi.org/10.1074/jbc.274.14.9665
Carroll, D. J., Ramarao, C. S., Mehlmann, L. M., Roche, S., Terasaki, M., & Jaffe, L. A. (1997). Calcium release at fertilization in starfish oocytes is mediated by phospholipase cgamma. Journal of Cell Biology, 138(6), 1303-1311. https://doi.org/10.1083/jcb.138.6.1303
Chen, H. I., & Sudol, M. (1995). The WW domain of yes-associated protein binds a proline-rich ligand that differs from the consensus established for src homology 3-binding modules. Proceedings of the National Academy of Sciences of the United States of America, 92(17), 7819-7823. https://doi.org/10.1073/pnas.92.17.7819
Cooney, M. A., Malcuit, C., Cheon, B., Holland, M. K., Fissore, R. A., & D'Cruz, N. T. (2010). Species-specific differences in the activity and nuclear localization of murine and bovine phospholipase C ζ 1. Biology of Reproduction, 83(1), 92-101. https://doi.org/10.1095/biolreprod.109.079814
Coward, K., Kubota, H., Hibbitt, O., McIlhinney, J., Kohri, K., & Parrington, J. (2006). Expression of a fluorescent recombinant form of sperm protein phospholipase C zeta in mouse epididymal sperm by in vivo gene transfer into the testis. Fertility and Sterility, 85(Suppl 1), 1281-1289. https://doi.org/10.1016/j.fertnstert.2005.12.012
Coward, K., Ponting, C. P., Zhang, N., Young, C., Huang, C. J., Chou, C. M., … Parrington, J. (2011). Identification and functional analysis of an ovarian form of the oocyte activation factor phospholipase C ζ (PLCζ) in pufferfish. Molecular Reproduction and Development, 78(1), 48-56. https://doi.org/10.1002/mrd.21262
Cox, L. J., Larman, M. G., Saunders, C. M., Hashimoto, K., Swann, K., & Lai, F. A. (2002). Sperm phospholipase C ζ from humans and cynomolgus monkeys triggers Ca2+ oscillations, activation and development of mouse oocytes. Reproduction, 124(5), 611-623.
Dale, B., & Santella, L. (1985). Sperm-oocyte interaction in the sea-urchin. Journal of Cell Science, 74, 153-167.
Deguchi, R., Shirakawa, H., Oda, S., Mohri, T., & Miyazaki, S. (2000). Spatiotemporal analysis of Ca(2+) waves in relation to the sperm entry site and animal-vegetal axis during Ca(2+) oscillations in fertilized mouse oocytes. Developmental Biology, 218(2), 299-313. https://doi.org/10.1006/dbio.1999.9573
Ducibella, T., Schultz, R. M., & Ozil, J. P. (2006). Role of calcium signals in early development. Seminars in Cell and Developmental Biology, 17(2), 324-332. https://doi.org/10.1016/j.semcdb.2006.02.010
Duncan, F. E., Que, E. L., Zhang, N., Feinberg, E. C., O'Halloran, T. V., & Woodruff, T. K. (2016). The zinc spark is an inorganic signature of human oocyte activation. Scientific Reports, 26(6), 24737. https://doi.org/10.1038/srep24737
Essen, L. O., Perisic, O., Cheung, R., Katan, M., & Williams, R. L. (1996). Crystal structure of a mammalian phosphoinositide-specific phospholipase C delta. Nature, 380(6575), 595-602. https://doi.org/10.1038/380595a0
Fujimoto, S., Yoshida, N., Fukui, T., Amanai, M., Isobe, T., Itagaki, C., … Perry, A. C. (2004). Mammalian phospholipase czeta induces oocyte activation from the sperm perinuclear matrix. Developmental Biology, 274(2), 370-383. https://doi.org/10.1016/j.ydbio.2004.07.025
Fukami, K., Inanobe, S., Kanemaru, K., & Nakamura, Y. (2010). Phospholipase C is a key enzyme regulating intracellular calcium and modulating the phosphoinositide balance. Progress in Lipid Research, 49(4), 429-437. https://doi.org/10.1016/j.plipres.2010.06.001
Grasa, P., Coward, K., Young, C., & Parrington, J. (2008). The pattern of localization of the putative oocyte activation factor, phospholipase C ζ, in uncapacitated, capacitated, and ionophore-treated human spermatozoa. Human Reproduction, 23(11), 2513-2522. https://doi.org/10.1093/humrep/den280
Grobler, J. A., & Hurley, J. H. (1996). Expression, characterization, and crystallization of the catalytic core of rat phosphatidylinositide-specific phospholipase C delta 1. Protein Science, 5(4), 680-686. https://doi.org/10.1002/pro.5560050412
Hachem, A., Godwin, J., Ruas, M., Lee, H. C., Ferrer Buitrago, M., Ardestani, G., … Parrington, J. (2017). PLCζ is the physiological trigger of the Ca (2+) oscillations that induce embryogenesis in mammals but conception can occur in its absence. Development, 144(16), 2914-2924. https://doi.org/10.1242/dev.150227
Hamilton, L. E., Suzuki, J., Acteau, G., Shi, M., Xu, W., Meinsohn, M. C., … Oko, R. (2018). WBP2 shares a common location in mouse spermatozoa with WBP2NL/PAWP and like its descendent is a candidate mouse oocyte-activating factor. Biology of Reproduction, 99(6), 1171-1183. https://doi.org/10.1093/biolre/ioy156
Harada, Y., Matsumoto, T., Hirahara, S., Nakashima, A., Ueno, S., Oda, S., … Iwao, Y. (2007). Characterization of a sperm factor for oocyte activation at fertilization of the newt Cynops pyrrhogaster. Developmental Biology, 306(2), 797-808. https://doi.org/10.1016/j.ydbio.2007.04.019
Heytens, E., Parrington, J., Coward, K., Young, C., Lambrecht, S., Yoon, S. Y., … De Sutter, P. (2009). Reduced amounts and abnormal forms of phospholipase C ζ (PLCζ) in spermatozoa from infertile men. Human Reproduction, 24(10), 2417-2428. https://doi.org/10.1093/humrep/dep207
Hinrichs, K., Choi, Y. H., Love, C. C., Chung, Y. G., & Varner, D. D. (2006). Production of horse foals via direct injection of roscovitine-treated donor cells and activation by injection of sperm extract. Reproduction, 131(6), 1063-1072. https://doi.org/10.1530/rep.1.01095
Ito, J., Parrington, J., & Fissore, R. A. (2011). PLCζ and its role as a trigger of development in vertebrates. Molecular Reproduction and Development, 78(10-11), 846-853. https://doi.org/10.1002/mrd.21359
Ito, M., Shikano, T., Kuroda, K., & Miyazaki, S. (2008). Relationship between nuclear sequestration of PLCζ and termination of PLCζ-induced Ca2+ oscillations in mouse oocytes. Cell Calcium, 44(4), 400-410. https://doi.org/10.1016/j.ceca.2008.02.003
Ito, M., Shikano, T., Oda, S., Horiguchi, T., Tanimoto, S., Awaji, T., … Miyazaki, S. (2008). Difference in Ca2+ oscillation-inducing activity and nuclear translocation ability of PLCZ1, an oocyte-activating sperm factor candidate, between mouse, rat, human, and medaka fish. Biology of Reproduction, 78(6), 1081-1090. https://doi.org/10.1095/biolreprod.108.067801
Jones, K. T. (2005). Mammalian oocyte activation: From Ca2+ spiking to cell cycle progression. Reproduction, 130(6), 813-823.
Jones, K. T., Carroll, J., Merriman, J. A., Whittingham, D. G., & Kono, T. (1995). Repetitive sperm-induced Ca2+ transients in mouse oocytes are cell cycle dependent. Development, 121(10), 3259-3266.
Kadamur, G., & Ross, E. M. (2013). Mammalian phospholipase C. Annual Review of Physiology, 75, 127-154. https://doi.org/10.1146/annurev-physiol-030212-183750
Katan, M. (1998). Families of phosphoinositide-specific phospholipase C: Structure and function. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, 1436(1-2), 5-17. https://doi.org/10.1016/S0005-2760(98)00125-8
Kennedy, C. E., Krieger, K. B., Sutovsky, M., Xu, W., Vargovic, P., Didion, B. A., … Sutovsky, P. (2014). Protein expression pattern of PAWP in bull spermatozoa is associated with sperm quality and fertility following artificial insemination. Molecular Reproduction and Development, 81(5), 436-449. https://doi.org/10.1002/mrd.22309
Kim, A. M., Vogt, S., O'Halloran, T. V., & Woodruff, T. K. (2010). Zinc availability regulates exit from meiosis in maturing mammalian oocytes. Nature Chemical Biology, 6(9), 674-681. https://doi.org/10.1038/nchembio.419
Kim, S. T., & Gye, M. C. (2003). Activation of mouse oocytes following intracytoplasmic injection of chicken sperm extract. Reproduction in Domestic Animals, 38(5), 401-404. https://doi.org/10.1046/j.1439-0531.2003.00455.x
Kline, D., & Kline, J. T. (1992). Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse oocyte. Developmental Biology, 149(1), 80-89. https://doi.org/10.1016/0012-1606(92)90265-I
Knott, J. G., Kurokawa, M., Fissore, R. A., Schultz, R. M., & Williams, C. J. (2005). Transgenic RNA interference reveals role for mouse sperm phospholipase cζ in triggering Ca2+ oscillations during fertilization. Biology of Reproduction, 72(4), 992-996. https://doi.org/10.1095/biolreprod.104.036244
Kono, T., Carroll, J., Swann, K., & Whittingham, D. G. (1995). Nuclei from fertilized mouse embryos have calcium-releasing activity. Development, 121(4), 1123-1128.
Kouchi, Z., Fukami, K., Shikano, T., Oda, S., Nakamura, Y., Takenawa, T., & Miyazaki, S. (2004). Recombinant phospholipase cζ has high Ca2+ sensitivity and induces Ca2+ oscillations in mouse oocytes. Journal of Biological Chemistry, 279(11), 10408-10412. https://doi.org/10.1074/jbc.M313801200
Kouchi, Z., Shikano, T., Nakamura, Y., Shirakawa, H., Fukami, K., & Miyazaki, S. (2005). The role of EF-hand domains and C2 domain in regulation of enzymatic activity of phospholipase cζ. The Journal of Biological Chemistry, 280(22), 21015-21021. https://doi.org/10.1074/jbc.M412123200
Kuroda, K., Ito, M., Shikano, T., Awaji, T., Yoda, A., Takeuchi, H., … Miyazaki, S. (2006). The role of X/Y linker region and N-terminal EF-hand domain in nuclear translocation and Ca2+ oscillation-inducing activities of phospholipase cζ, a mammalian oocyte-activating factor. The Journal of Biological Chemistry, 281(38), 27794-27805. https://doi.org/10.1074/jbc.m603473200
Kurokawa, M., Sato, K., & Fissore, R. A. (2004). Mammalian fertilization: From sperm factor to phospholipase cζ. Biology of the Cell, 96(1), 37-45. https://doi.org/10.1016/j.biolcel.2003.11.003
Kurokawa, M., Sato, K., Wu, H., He, C., Malcuit, C., Black, S. J., … Fissore, R. A. (2005). Functional, biochemical, and chromatographic characterization of the complete [Ca2+]i oscillation-inducing activity of porcine sperm. Developmental Biology, 285(2), 376-392. https://doi.org/10.1016/j.ydbio.2005.06.029
Kurokawa, M., Yoon, S. Y., Alfandari, D., Fukami, K., Sato, K., & Fissore, R. A. (2007). Proteolytic processing of phospholipase czeta and [Ca2+]i oscillations during mammalian fertilization. Developmental Biology, 312(1), 407-418. https://doi.org/10.1016/j.ydbio.2007.09.040
Larman, M. G., Saunders, C. M., Carroll, J., Lai, F. A., & Swann, K. (2004). Cell cycle-dependent Ca2+ oscillations in mouse embryos are regulated by nuclear targeting of PLCζ. Journal of Cell Science, 117(Pt 12), 2513-2521. https://doi.org/10.1242/jcs.01109
Lomasney, J. W., Cheng, H. F., Roffler, S. R., & King, K. (1999). Activation of phospholipase C delta 1 through C2 domain by a Ca(2+)-enzyme-phosphatidylserine ternary complex. The Journal of Biological Chemistry, 274(31), 21995-22001. https://doi.org/10.1074/jbc.274.31.21995
Machaty, Z., Bonk, A. J., Kuhholzer, B., & Prather, R. S. (2000). Porcine oocyte activation induced by a cytosolic sperm factor. Molecular Reproduction and Development, 57(3), 290-295. https://doi.org/10.1002/1098-2795(200011)57:3<290::aid-mrd11>3.0.co;2-#
Malcuit, C., Knott, J. G., He, C., Wainwright, T., Parys, J. B., Robl, J. M., & Fissore, R. A. (2005). Fertilization and inositol 1,4,5-trisphosphate (IP3)-induced calcium release in type-1 inositol 1,4,5-trisphosphate receptor down-regulated bovine oocytes. Biology of Reproduction, 73(1), 2-13. https://doi.org/10.1095/biolreprod.104.037333
Marangos, P., FitzHarris, G., & Carroll, J. (2003). Ca2+ oscillations at fertilization in mammals are regulated by the formation of pronuclei. Development, 130(7), 1461-1472. https://doi.org/10.1242/dev.00340
McDougall, A., Levasseur, M., O'Sullivan, A. J., & Jones, K. T. (2000). Cell cycle-dependent repetitive Ca (2+) waves induced by a cytosolic sperm extract in mature ascidian oocytes mimic those observed at fertilization. Journal of Cell Science, 113(Pt 19), 3453-3462.
Medkova, M., & Cho, W. (1999). Interplay of C1 and C2 domains of protein kinase C-alpha in its membrane binding and activation. The Journal of Biological Chemistry, 274(28), 19852-19861. https://doi.org/10.1074/jbc.274.28.19852
Miyazaki, S., Shirakawa, H., Nakada, K., & Honda, Y. (1993). Essential role of the inositol 1,4,5-trisphosphate receptor/Ca2+ release channel in Ca2+ waves and Ca2+ oscillations at fertilization of mammalian oocytes. Developmental Biology, 158(1), 62-78. https://doi.org/10.1006/dbio.1993.1168
Miyazaki, S., Shirakawa, H., Nakada, K., Honda, Y., Yuzaki, M., Nakade, S., & Mikoshiba, K. (1992). Antibody to the inositol trisphosphate receptor blocks thimerosal-enhanced Ca (2+)-induced Ca2+ release and Ca2+ oscillations in hamster oocytes. FEBS Letters, 309(2), 180-184. https://doi.org/10.1016/0014-5793(92)81090-9
Miyazaki, S., Yuzaki, M., Nakada, K., Shirakawa, H., Nakanishi, S., Nakade, S., & Mikoshiba, K. (1992). Block of Ca2+ wave and Ca2+ oscillation by antibody to the inositol 1,4,5-trisphosphate receptor in fertilized hamster oocytes. Science, 257(5067), 251-255. https://doi.org/10.1126/science.1321497
Mizushima, S., Hiyama, G., Shiba, K., Inaba, K., Dohra, H., Ono, T., … Sasanami, T. (2014). The birth of quail chicks after intracytoplasmic sperm injection. Development, 141(19), 3799-3806. https://doi.org/10.1242/dev.111765
Mizushima, S., Takagi, S., Ono, T., Atsumi, Y., Tsukada, A., Saito, N., & Shimada, K. (2009). Phospholipase cζ mRNA expression and its potency during spermatogenesis for activation of quail oocyte as a sperm factor. Molecular Reproduction and Development, 76(12), 1200-1207. https://doi.org/10.1002/mrd.21097
Nakai, M., Ito, J., Sato, K., Noguchi, J., Kaneko, H., Kashiwazaki, N., & Kikuchi, K. (2011). Pre-treatment of sperm reduces success of ICSI in the pig. Reproduction, 142(2), 285-293. https://doi.org/10.1530/REP-11-0073
Nakanishi, T., Ishibashi, N., Kubota, H., Inoue, K., Ogonuki, N., Ogura, A., … Baba, T. (2008). Birth of normal offspring from mouse oocytes activated by a phospholipase cζ protein lacking three EF-hand domains. Journal of Reproduction and Development, 54(4), 244-249. https://doi.org/10.1262/jrd.19168
Nomikos, M., Blayney, L. M., Larman, M. G., Campbell, K., Rossbach, A., Saunders, C. M., … Lai, F. A. (2005). Role of phospholipase C-ζ domains in Ca2+-dependent phosphatidylinositol 4,5-bisphosphate hydrolysis and cytoplasmic Ca2+ oscillations. The Journal of Biological Chemistry, 280(35), 31011-31018. https://doi.org/10.1074/jbc.m500629200
Nomikos, M., Elgmati, K., Theodoridou, M., Georgilis, A., Gonzalez-Garcia, J. R., Nounesis, G., … Lai, F. A. (2011). Novel regulation of PLCζ activity via its XY-linker. Biochemical Journal, 438(3), 427-432. https://doi.org/10.1042/BJ20110953
Nomikos, M., Sanders, J. R., Kashir, J., Sanusi, R., Buntwal, L., Love, D., … Lai, F. A. (2015). Functional disparity between human PAWP and PLCζ in the generation of Ca2+ oscillations for oocyte activation. Molecular Human Reproduction, 21(9), 702-710. https://doi.org/10.1093/molehr/gav034
Nomikos, M., Sanders, J. R., Theodoridou, M., Kashir, J., Matthews, E., Nounesis, G., … Swann, K. (2014). Sperm-specific post-acrosomal WW-domain binding protein (PAWP) does not cause Ca2+ release in mouse oocytes. Molecular Human Reproduction, 20(10), 938-947. https://doi.org/10.1093/molehr/gau056
Nomikos, M., Theodoridou, M., Elgmati, K., Parthimos, D., Calver, B. L., Buntwal, L., … Lai, F. A. (2014). Human PLCζ exhibits superior fertilization potency over mouse PLCζ in triggering the Ca(2+) oscillations required for mammalian oocyte activation. Molecular Human Reproduction, 20(6), 489-498. https://doi.org/10.1093/molehr/gau011
Nozawa, K., Satouh, Y., Fujimoto, T., Oji, A., & Ikawa, M. (2018). Sperm-borne phospholipase C ζ-1 ensures monospermic fertilization in mice. Scientific Reports, 8(1), 1-10. https://doi.org/10.1038/s41598-018-19497-6
Nuccitelli, R., Yim, D. L., & Smart, T. (1993). The sperm-induced Ca2+ wave following fertilization of the xenopus oocyte requires the production of ins(1, 4, 5)P3. Developmental Biology, 158(1), 200-212. https://doi.org/10.1006/dbio.1993.1179
Ogonuki, N., Sankai, T., Yagami, K., Shikano, T., Oda, S., Miyazaki, S., & Ogura, A. (2001). Activity of a sperm-borne oocyte-activating factor in spermatozoa and spermatogenic cells from cynomolgus monkeys and its localization after oocyte activation. Biology of Reproduction, 65(2), 351-357. https://doi.org/10.1095/biolreprod65.2.351
Ozil, J. P., Banrezes, B., Toth, S., Pan, H., & Schultz, R. M. (2006). Ca2+ oscillatory pattern in fertilized mouse oocytes affects gene expression and development to term. Developmental Biology, 300(2), 534-544. https://doi.org/10.1016/j.ydbio.2006.08.041
Parrington, J., Swann, K., Shevchenko, V. I., Sesay, A. K., & Lai, F. A. (1996). Calcium oscillations in mammalian oocytes triggered by a soluble sperm protein. Nature, 379(6563), 364-368. https://doi.org/10.1038/379364a0
Que, E. L., Bleher, R., Duncan, F. E., Kong, B. Y., Gleber, S. C., Vogt, S., … O'Halloran, T. V. (2015). Quantitative mapping of zinc fluxes in the mammalian oocyte reveals the origin of fertilization-induced zinc sparks. Nature Chemistry, 7(2), 130-139. https://doi.org/10.1038/nchem.2133
Que, E. L., Duncan, F. E., Lee, H. C., Hornick, J. E., Vogt, S., Fissore, R. A., … Woodruff, T. K. (2019). Bovine oocytes release zinc in response to parthenogenetic and sperm-induced oocyte activation. Theriogenology, 127, 41-48. https://doi.org/10.1016/j.theriogenology.2018.12.031
Rebecchi, M. J., & Pentyala, S. N. (2000). Structure, function, and control of phosphoinositide-specific phospholipase C. Physiological Reviews, 80(4), 1291-1335. https://doi.org/10.1152/physrev.2000.80.4.1291
Ross, P. J., Beyhan, Z., Iager, A. E., Yoon, S. Y., Malcuit, C., Schellander, K., … Cibelli, J. B. (2008). Parthenogenetic activation of bovine oocytes using bovine and murine phospholipase C zeta. BMC Developmental Biology, 8, 8-16. https://doi.org/10.1186/1471-213X-8-16
Runft, L. L., Jaffe, L. A., & Mehlmann, L. M. (2002). Oocyte activation at fertilization: Where it all begins. Developmental Biology, 245(2), 237-254. https://doi.org/10.1006/dbio.2002.0600
Sato, K., Wakai, T., Seita, Y., Takizawa, A., Fissore, R. A., Ito, J., & Kashiwazaki, N. (2013). Molecular characteristics of horse phospholipase C ζ (PLCζ). Animal Science Journal, 84(4), 359-368. https://doi.org/10.1111/asj.12044
Satouh, Y., Nozawa, K., & Ikawa, M. (2015). Sperm postacrosomal WW domain-binding protein is not required for mouse oocyte activation. Biology of Reproduction, 93(4), 94. https://doi.org/10.1095/biolreprod.115.131441
Saunders, C. M., Larman, M. G., Parrington, J., Cox, L. J., Royse, J., Blayney, L. M., … Lai, F. A. (2002). PLC ζ: A sperm-specific trigger of ca(2+) oscillations in oocytes and embryo development. Development, 129(15), 3533-3544.
Seita, Y., Ito, J., & Kashiwazaki, N. (2009). Removal of acrosomal membrane from sperm head improves development of rat zygotes derived from intracytoplasmic sperm injection. Journal of Reproduction and Development, 55(5), 475-479. https://doi.org/10.1262/jrd.20216
Sette, C., Bevilacqua, A., Bianchini, A., Mangia, F., Geremia, R., & Rossi, P. (1997). Parthenogenetic activation of mouse oocytes by microinjection of a truncated c-kit tyrosine kinase present in spermatozoa. Development, 124(11), 2267-2274.
Sone, Y., Ito, M., Shirakawa, H., Shikano, T., Takeuchi, H., Kinoshita, K., & Miyazaki, S. (2005). Nuclear translocation of phospholipase C-ζ, an oocyte-activating factor, during early embryonic development. Biochemical and Biophysical Research Communications, 330(3), 690-694. https://doi.org/10.1016/j.bbrc.2005.03.032
Stice, S. L., & Robl, J. M. (1990). Activation of mammalian oocytes by a factor obtained from rabbit sperm. Molecular Reproduction and Development, 25(3), 272-280. https://doi.org/10.1002/mrd.1080250309
Stricker, S. A. (1999). Comparative biology of calcium signaling during fertilization and oocyte activation in animals. Developmental Biology, 211(2), 157-176. https://doi.org/10.1006/dbio.1999.9340
Suh, P. G., Park, J. I., Manzoli, L., Cocco, L., Peak, J. C., Katan, M., … Ryu, S. H. (2008). Multiple roles of phosphoinositide-specific phospholipase C isozymes. BMB Reports, 41(6), 415-434. https://doi.org/10.5483/bmbrep.2008.41.6.415
Sutovsky, P. (2015). New approaches to boar semen evaluation, processing and improvement. Reproduction in Domestic Animals, 50(Suppl 2), 11-19. https://doi.org/10.1111/rda.12554
Sutovsky, P., Aarabi, M., Miranda-Vizuete, A., & Oko, R. (2015). Negative biomarker based male fertility evaluation: Sperm phenotypes associated with molecular-level anomalies. Asian Journal of Andrology, 17(4), 554-560. https://doi.org/10.4103/1008-682X.153847
Suzuki, T., Yoshida, N., Suzuki, E., Okuda, E., & Perry, A. C. (2010). Full-term mouse development by abolishing Zn2+-dependent metaphase II arrest without Ca2+ release. Development, 137(16), 2659-2669. https://doi.org/10.1242/dev.049791
Swann, K. (1990). A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster oocytes. Development, 110(4), 1295-1302.
Swann, K. (1996). Soluble sperm factors and Ca2+ release in oocytes at fertilization. Reviews of Reproduction, 1(1), 33-39.
Swann, K., & Parrington, J. (1999). Mechanism of Ca2+ release at fertilization in mammals. Journal of Experimental Zoology, 285(3), 267-275. https://doi.org/10.1002/(SICI)1097-010X(19991015)285:3<267:AID-JEZ10>3.0.CO;2-P
Swann, K., Saunders, C. M., Rogers, N. T., & Lai, F. A. (2006). PLCζ(ζ): A sperm protein that triggers Ca2+ oscillations and oocyte activation in mammals. Seminars in Cell and Developmental Biology, 17(2), 264-273. https://doi.org/10.1016/j.semcdb.2006.03.009
Whitaker, M. (2006). Calcium at fertilization and in early development. Physiological Reviews, 86(1), 25-88. https://doi.org/10.1152/physrev.00023.2005
Wilding, M., Kyozuka, K., Russo, G. L., Tosti, E., & Dale, B. (1997). A soluble extract from human spermatozoa activates ascidian oocytes. Development, Growth & Differentiation, 39(3), 329-336. https://doi.org/10.1046/j.1440-169x.1997.t01-2-00008.x
Wolosker, H., Kline, D., Bian, Y., Blackshaw, S., Cameron, A. M., Fralich, T. J., … Snyder, S. H. (1998). Molecularly cloned mammalian glucosamine-6-phosphate deaminase localizes to transporting epithelium and lacks oscillin activity. FASEB Journal, 12(1), 91-99. https://doi.org/10.1096/fasebj.12.1.91
Wu, A. T., Sutovsky, P., Manandhar, G., Xu, W., Katayama, M., Day, B. N., … Oko, R. (2007). PAWP, a sperm-specific WW domain-binding protein, promotes meiotic resumption and pronuclear development during fertilization. The Journal of Biological Chemistry, 282(16), 12164-12175. https://doi.org/10.1074/jbc.M609132200
Wu, H., He, C. L., & Fissore, R. A. (1997). Injection of a porcine sperm factor triggers calcium oscillations in mouse oocytes and bovine oocytes. Molecular Reproduction and Development, 46(2), 176-189. https://doi.org/10.1002/(sici)1098-2795(199702)46:2<176::aid-mrd8>3.0.co;2-n
Xu, Z., Kopf, G. S., & Schultz, R. M. (1994). Involvement of inositol 1,4,5-trisphosphate-mediated Ca2+ release in early and late events of mouse oocyte activation. Development, 120(7), 1851-1859.
Yanagimachi, R. (1994). Mammalian fertilization. In E. Knobil, & J. D. Neill (Eds.), The physiology of reproduction (2nd ed., pp. 189-317). New York, NY: Raven.
Yazawa, H., Yanagida, K., Katayose, H., Hayashi, S., & Sato, A. (2000). 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. Human Reproduction, 15(12), 2582-2590. https://doi.org/10.1093/humrep/15.12.2582
Yoda, A., Oda, S., Shikano, T., Kouchi, Z., Awaji, T., Shirakawa, H., … Miyazaki, S. (2004). Ca2+ oscillation-inducing phospholipase C ζ expressed in mouse oocytes is accumulated to the pronucleus during oocyte activation. Developmental Biology, 268(2), 245-257. https://doi.org/10.1016/j.ydbio.2003.12.028
Yoneda, A., Kashima, M., Yoshida, S., Terada, K., Nakagawa, S., Sakamoto, A., … Watanabe, T. (2006). Molecular cloning, testicular postnatal expression, and oocyte-activating potential of porcine phospholipase cζ. Reproduction, 132(3), 393-401. https://doi.org/10.1530/rep.1.01018
Yoneda, A., & Watanabe, T. (2015). Involvement of mouse and porcine PLCζ-induced calcium oscillations in preimplantation development of mouse embryos. Biochemical and Biophysical Research Communications, 460(2), 476-481. https://doi.org/10.1016/j.bbrc.2015.03.058
Yoon, S. Y., Eum, J. H., Lee, J. E., Lee, H. C., Kim, Y. S., Han, J. E., … Yoon, T. K. (2012). Recombinant human phospholipase C zeta 1 induces intracellular calcium oscillations and oocyte activation in mouse and human oocytes. Human Reproduction, 27(6), 1768-1780. https://doi.org/10.1093/humrep/des092
Yoon, S. Y., & Fissore, R. A. (2007). Release of phospholipase C ζand [Ca2+]i oscillation-inducing activity during mammalian fertilization. Reproduction, 134(5), 695-704. https://doi.org/10.1530/REP-07-0259
Yoon, S. Y., Jellerette, T., Salicioni, A. M., Lee, H. C., Yoo, M. S., Coward, K., … Fissore, R. A. (2008). Human sperm devoid of PLC, ζ 1 fail to induce Ca (2+) release and are unable to initiate the first step of embryo development. Journal of Clinical Investigation, 118(11), 3671-3681. https://doi.org/10.1172/JCI36942
Young, C., Grasa, P., Coward, K., Davis, L. C., & Parrington, J. (2009). Phospholipase C ζ undergoes dynamic changes in its pattern of localization in sperm during capacitation and the acrosome reaction. Fertility and Sterility, 91(5 Suppl), 2230-2242. https://doi.org/10.1016/j.fertnstert.2008.05.021
Yu, Y., Saunders, C. M., Lai, F. A., & Swann, K. (2008). Preimplantation development of mouse oocytes activated by different levels of human phospholipase C zeta. Human Reproduction, 23(2), 365-373. https://doi.org/10.1093/humrep/dem350
Zhang, N., Duncan, F. E., Que, E. L., O'Halloran, T. V., & Woodruff, T. K. (2016). The fertilization-induced zinc spark is a novel biomarker of mouse embryo quality and early development. Scientific Reports, 6, 22772. https://doi.org/10.1038/srep22772
Zheng, L., Krishnamoorthi, R., Zolkiewski, M., & Wang, X. (2000). Distinct Ca2+ binding properties of novel C2 domains of plant phospholipase dalpha and beta. The Journal of Biological Chemistry, 275(26), 19700-19706. https://doi.org/10.1074/jbc.M001945200