Abstract
Fertilization is the union of gametes to initiate development of a new individual. The female gamete is formed during oogenesis. The process begins when, in the early embryo, primordial germ cells arise and subsequently colonize the genital ridges. They differentiate into oogonia, start meiosis, and become primary oocytes. The cell cycle of the primary oocytes then becomes arrested in mid-meiosis for an extended period of time. Prior to ovulation the oocytes undergo a growth phase and their sizes increase significantly. A hormonal cue then triggers oocyte maturation that involves the resumption of meiosis, the completion of the first meiotic division, and, as a result, the reduction in the diploid chromosome number. The cell cycle then stops again; in vertebrates this arrest occurs at the metaphase stage of the second meiotic division. Meiosis resumes at fertilization, when the sperm activates the egg, i.e., it causes a series of changes that are required for the initiation of embryo development. This is achieved by triggering an elevation in the egg’s intracellular free calcium concentration. In response, the fertilized egg completes meiosis and enters the first embryonic cell cycle.
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References
Aarabi M, Balakier H, Bashar S, Moskovtsev SI, Sutovsky P, Librach CL, Oko R (2014) Sperm-derived WW domain-binding protein, PAWP, elicits calcium oscillations and oocyte activation in humans and mice. FASEB J 28:4434–4440. doi: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. Mol Reprod Dev 77:249–256. doi:10.1002/mrd.21140
Adkins CE, Taylor CW (1999) Lateral inhibition of inositol 1,4,5-trisphosphate receptors by cytosolic Ca2+. Curr Biol 9:1115–1118. doi:10.1016/S0960-9822(99)80481-3
Allen RD, Griffin JL (1958) The time sequence of early events in the fertilization of sea urchin eggs: I. The latent period and the cortical reaction. Exp Cell Res 15:163–173. doi:10.1016/0014-4827(58)90072-7
Amiel A, Leclère L, Robert L, Chevalier S, Houliston E (2009) Conserved functions for Mos in eumetazoan oocyte maturation revealed by studies in a cnidarian. Curr Biol 19:305–311. doi:10.1016/j.cub.2008.12.054
Berridge MJ (2002) The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32:235–249. doi:10.1016/S0143416002001823
Berridge MJ, Galione A (1988) Cytosolic calcium oscillators. FASEB J 2:3074–3082
Bi M, Wassler MJ, Hardy DM (2002) Sperm adhesion to the extracellular matrix of the egg. In: Hardy DM (ed) Fertilization. Academic, San Diego
Bornslaeger EA, Mattei P, Schultz RM (1986) Involvement of cAMP-dependent protein kinase and protein phosphorylation in regulation of mouse oocyte maturation. Dev Biol 114:453–462. doi:10.1016/0012-1606(86)90209-5
Brawand D, Wahli W, Kaessmann H (2008) Loss of egg yolk genes in mammals and the origin of lactation and placentation. PLoS Biol 6:e63. doi:10.1371/journal.pbio.0060063
Breed WG, Leigh CM (1990) Morphological changes in the oocyte and its surrounding vestments during in vivo fertilization in the dasyurid marsupial sminthopsis crassicaudata. J Morphol 204:177–196. doi:10.1002/jmor.1052040207
Brind S, Swann K, Carroll J (2000) Inositol 1,4,5-trisphosphate receptors are downregulated in mouse oocytes in response to sperm or adenophostin A but not to increases in intracellular Ca2+ or egg activation. Dev Biol 223:251–265. doi:10.1006/dbio.2000.9728
Busa WB (1990) Involvement of calcium and inositol phosphates in amphibian egg activation. J Reprod Fertil Suppl 42:155–161
Busa WB, Nuccitelli R (1985) An elevated free cytosolic Ca2+ wave follows fertilization in eggs of the frog, Xenopus laevis. J Cell Biol 100:1325–1329. doi:10.1083/jcb.100.4.1325
Butterfield NJ (2000) Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26:386–404. doi:10.1666/0094-8373(2000)026<0386:BPNGNS>2.0.CO;2
Campbell KD, Reed WA, White KL (2000) Ability of integrins to mediate fertilization, intracellular calcium release, and parthenogenetic development in bovine oocytes. Biol Reprod 62:1702–1709. doi:10.1095/biolreprod62.6.1702
Carvacho I, Lee HC, Fissore RA, Clapham DE (2013) TRPV3 channels mediate strontium-induced mouse-egg activation. Cell Rep 5:1375–1386. doi:10.1016/j.celrep.2013.11.007
Castro A, Peter M, Magnaghi-Jaulin L, Vigneron S, Galas S, Lorca T, Labbé JC (2001) Cyclin B/cdc2 induces c-Mos stability by direct phosphorylation in Xenopus oocytes. Mol Biol Cell 12:2660–2671. doi:10.1091/mbc.12.9.2660
Charbonneau M, Moreau M, Picheral B, Vilain JP, Guerrier P (1983) Fertilization of amphibian eggs: a comparison of electrical responses between anurans and urodeles. Dev Biol 98:304–318. doi:10.1016/0012-1606(83)90361-5
Coggins L (1973) An ultrastructural and radioautographic study of early oogenesis in the toad Xenopus laevis. J Cell Sci 12:71–93
Colonna R, Tatone C, Malgaroli A, Eusebi F, Mangia F (1989) Effects of protein kinase C stimulation and free Ca2+ rise in mammalian egg activation. Gamete Res 24:171–183. doi:10.1002/mrd.1120240205
Conti M, Andersen CB, Richard FJ, Shitsukawa K, Tsafriri A (1998) Role of cyclic nucleotide phosphodiesterases in resumption of meiosis. Mol Cell Endocrinol 145:9–14. doi:10.1016/S0303-7207(98)00187-7
Coronado R, Morrissette J, Sukhareva M, Vaughan DM (1994) Structure and function of ryanodine receptors. Am J Physiol 266:1485–1504
Coward K, Campos-Mendoza A, Larman M, Hibbitt O, McAndrew B, Bromage N, Parrington J (2003) 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 305:299–304. doi:10.1016/S0006-291X(03)00753-8
Coward K, Ponting CP, Chang HY, Hibbitt O, Savolainen P, Jones KT, Parrington J (2005) Phospholipase Cζ, the trigger of egg activation in mammals, is present in a non-mammalian species. Reproduction 130:157–163. doi:10.1530/rep.1.00707
Coward K, Ponting CP, Zhang N, Young C, Huang CJ, Chou CM, Kashir J, Fissore RA, Parrington J (2011) Identification and functional analysis of an ovarian form of the egg activation factor phospholipase C zeta (PLCζ) in pufferfish. Mol Reprod Dev 78:48–56. doi:10.1002/mrd.21262
Cox LJ, Larman MG, Saunders CM, Hashimoto K, Swann K, Lai FA (2002) Sperm phospholipase Cζ from humans and cynomolgus monkeys triggers Ca2+ oscillations, activation and development of mouse oocytes. Reproduction 124:611–623. doi:10.1530/rep.0.1240611
Cuthbertson KR, Cobbold P (1985) Phorbol ester and sperm activate mouse oocytes by inducing sustained oscillations in cell Ca2+. Nature 316:541–542. doi:10.1038/316541a0
Daar I, Paules RS, Woude GV (1991) A characterization of cytostatic factor activity from Xenopus eggs and c-mos-transformed cells. J Cell Biol 114:329–335. doi:10.1083/jcb.114.2.329
Davail B, Pakdel F, Bujo H, Perazzolo LM, Waclawek M, Schneider WJ, Le Menn F (1998) Evolution of oogenesis: the receptor for vitellogenin from the rainbow trout. J Lipid Res 39:1929–1937
Day ML, McGuinness OM, Berridge MJ, Johnson MH (2000) Regulation of fertilization-induced Ca2+ spiking in the mouse zygote. Cell Calcium 28:47–54. doi:10.1054/ceca.2000.0128
Deguchi R, Shirakawa H, Oda S, Mohri T, Miyazaki S (2000) Spatiotemporal analysis of Ca2+ waves in relation to the sperm entry site and animal-vegetal axis during Ca2+ oscillations in fertilized mouse eggs. Dev Biol 218:299–313. doi:10.1006/dbio.1999.9573
De Young GW, Keizer J (1992) A single-pool inositol 1,4,5-trisphosphate-receptor-based model for agonist-stimulated oscillations in Ca2+ concentration. Proc Natl Acad Sci U S A 89:9895–9899. doi:10.1073/pnas.89.20.9895
Dong JB, Tang TS, Sun FZ (2000) Xenopus and chicken sperm contain a cytosolic soluble protein factor which can trigger calcium oscillations in mouse eggs. Biochem Biophys Res Commun 268:947–951. doi:10.1006/bbrc.2000.2218
Ducibella T, Duffy P, Kurasawa S, Kopf GS, Schultz RM (1991) The cortical reaction and modifications of the zona pellucida are stimulated by protein kinase C agonists in the mouse egg. J Cell Biol 115:461a. doi:10.1083/jcb.115.2.461
Dumont JN (1972) Oogenesis in Xenopus laevis (Daudin): I. Stages of oocyte development in laboratory maintained animals. J Morphol 136:153–179. doi:10.1002/jmor.1051360203
Dumont J, Umbhauer M, Rassinier P, Hanauer A, Verlhac MH (2005) p90Rsk is not involved in cytostatic factor arrest in mouse oocytes. J Cell Biol 169:227–231. doi:10.1083/jcb.200501027
Dupont G, Dumollard R (2004) Simulation of calcium waves in ascidian eggs: insights into the origin of the pacemaker sites and the possible nature of the sperm factor. J Cell Sci 117:4313–4323. doi:10.1242/jcs.01278
Dupont G, McGuinness OM, Johnson MH, Berridge MJ, Borgese F (1996) Phospholipase C in mouse oocytes: characterization of beta and gamma isoforms and their possible involvement in sperm-induced Ca2+ spiking. Biochem J 316:583–591
Dupré A, Haccard O, Jessus C (2011) Mos in the oocyte: how to use MAPK independently of growth factors and transcription to control meiotic divisions. J Signal Transduct 2011:350412. doi:10.1155/2011/350412
Elinson RP (1975) Site of sperm entry and a cortical contraction associated with egg activation in the frog Rana pipiens. Dev Biol 47:257–268. doi:10.1016/0012-1606(75)90281-X
Elinson R (1997) Amphibians. In: Gilbert SF, Raunio AM (eds) Embryology; constructing the organism. Sinauer Associates Inc. Publishers, Sunderland
Extavour CG, Akam M (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869–5884. doi:10.1242/dev.00804
Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel S-H, Tanasa B, Hogan PG, Lewis RS, Daly M, Rao A (2006) A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441:179–185. doi:10.1038/nature04702
Fisher DL, Brassac T, Galas S, Dorée M (1999) Dissociation of MAP kinase activation and MPF activation in hormone-stimulated maturation of Xenopus oocytes. Development 126:4537–4546
Fissore RA, Robl JM (1993) Sperm, inositol trisphosphate, and thimerosal-induced intracellular Ca2+ elevations in rabbit eggs. Dev Biol 159:122–130. doi:10.1006/dbio.1993.1226
Fissore RA, Robl JM (1994) Mechanism of calcium oscillations in fertilized rabbit eggs. Dev Biol 166:634–642. doi:10.1006/dbio.1994.1343
Fissore RA, Dobrinsky JR, Balise JJ, Duby RT, Robl JM (1992) Patterns of intracellular Ca2+ concentrations in fertilized bovine eggs. Biol Reprod 47:960–969. doi:10.1095/biolreprod47.6.960
Fissore RA, Pinto-Correia C, Robl JM (1995) Inositol trisphosphate-induced calcium release in the generation of calcium oscillations in bovine eggs. Biol Reprod 53:766–774. doi:10.1095/biolreprod53.4.766
Fluck R, Abraham V, Miller A, Galione A (1999) Microinjection of cyclic ADP-ribose triggers a regenerative wave of Ca2+ release and exocytosis of cortical alveoli in medaka eggs. Zygote 7:285–292
Foltz KR, Shilling FM (1993) Receptor-mediated signal transduction and egg activation. Zygote 1:276–279. doi:10.1017/S0967199400001593
Fontanilla RA, Nuccitelli R (1998) Characterization of the sperm-induced calcium wave in Xenopus eggs using confocal microscopy. Biophys J 75:2079–2087. doi:10.1017/S0967199400001593
Frank-Vaillant M, Jessus C, Ozon R, Maller JL, Haccard O (1999) Two distinct mechanisms control the accumulation of Cyclin B1 and Mos in Xenopus oocytes in response to progesterone. Mol Biol Cell 10:3279–3288. doi:10.1091/mbc.10.10.3279
Freeman RS, Meyer AN, Li J, Donoghue DJ (1992) Phosphorylation of conserved serine residues does not regulate the ability of mosxe protein kinase to induce oocyte maturation or function as cytostatic factor. J Cell Biol 116:725–735. doi:10.1083/jcb.116.3.725
Fukami K (2002) Structure, regulation, and function of phospholipase C isozymes. J Biochem 131:293–299
Furuno N, Nishizawa M, Okazaki K, Tanaka H, Iwashita J, Nakajo N, Ogawa Y, Sagata N (1994) Suppression of DNA replication via Mos function during meiotic divisions in Xenopus oocytes. EMBO J 13:2399–2410
Galione A, Swann K, Georgiou P, Whitaker M (1994) Regenerative and non-regenerative calcium transients in hamster eggs triggered by inositol 1,4,5-trisphosphate. J Physiol 480:465–474. doi:10.1113/jphysiol.1994.sp020375
Gatenby JB, Hill JP (1924) On an ovum of Ornithorhynchus exhibiting polar bodies and polyspermy. J Cell Sci s2-68:229–238
Gilkey JC (1983) Roles of calcium and pH in activation of eggs of the medaka fish, Oryzias latipes. J Cell Biol 97:669–678. doi:10.1083/jcb.97.3.669
Gilkey JC, Jaffe LF, Ridgway EB, Reynolds GT (1978) A free calcium wave traverses the activating egg of the medaka, Oryzias latipes. J Cell Biol 76:448–466. doi:10.1083/jcb.76.2.448
Goetz FW, Berndtson AK, Ranjan M (1991) Ovulation: mediators at the ovarian level. In: Pang PKT, Schreibman MP (eds) Vertebrate endocrinology: fundamentals and biomedical implications. Academic Press, Inc., San Diego
Gómez-Fernández C, López-Guerrero AM, Pozo-Guisado E, Álvarez IS, Martín-Romero FJ (2012) Calcium signaling in mouse oocyte maturation: the roles of STIM1, ORAI1 and SOCE. Mol Hum Reprod 18:194–203. doi:10.1093/molehr/gar071
Gómez-Fernández C, Pozo-Guisado E, Gañán-Parra M, Perianes MJ, Álvarez IS, Martín-Romero FJ (2009) Relocalization of STIM1 in mouse oocytes at fertilization: early involvement of store-operated calcium entry. Reproduction 138:211–221. doi:10.1530/rep-09-0126
Gondos B, Westergaard L, Byskov AG (1986) Initiation of oogenesis in the human fetal ovary: ultrastructural and squash preparation study. Am J Obstet Gynecol 155:189–195. doi:10.1016/0002-9378(86)90109-2
Grandin N, Charbonneau M (1992) Intracellular free Ca2+ changes during physiological polyspermy in amphibian eggs. Development 114:617–624
Hagiwara S, Jaffe LA (1979) Electrical properties of egg cell membranes. Annu Rev Biophys Bioeng 8:385–416. doi:10.1146/annurev.bb.08.060179.002125
Halet G, Tunwell R, Parkinson SJ, Carroll J (2004) Conventional PKCs regulate the temporal pattern of Ca2+ oscillations at fertilization in mouse eggs. J Cell Biol 164:1033–1044. doi:10.1083/jcb.200311023
Harada Y, Kawazoe M, Eto Y, Ueno S, Iwao Y (2011) The Ca2+ increase by the sperm factor in physiologically polyspermic newt fertilization: its signaling mechanism in egg cytoplasm and the species-specificity. Dev Biol 351:266–276. doi:10.1016/j.ydbio.2011.01.003
Harada Y, Matsumoto T, Hirahara S, Nakashima A, Ueno S, Oda S, Miyazaki S, Iwao Y (2007) Characterization of a sperm factor for egg activation at fertilization of the newt Cynops pyrrhogaster. Dev Biol 306:797–808. doi:10.1016/j.ydbio.2007.04.019
Hardy DM (2002) Fertilization. Academic, San Diego
Hardie RC (2007) TRP channels and lipids: from Drosophila to mammalian physiology. J Physiol 578:9–24. doi:10.1113/jphysiol.2006.118372
Hart NH (1990) Fertilization in teleost fishes: mechanisms of sperm-egg interactions. Int Rev Cytol 121:1–66. doi:10.1016/S0074-7696(08)60658-0
Hart NH, Donovan M (1983) Fine structure of the chorion and site of sperm entry in the egg of Brachydanio. J Exp Zool 227:277–296. doi:10.1002/jez.1402270212
Hashimoto N, Watanabe N, Furuta Y, Tamemoto H, Sagata N, Yokoyama M, Okazaki K, Nagayoshi M, Takeda N, Ikawa Y, Aizawai S (1994) Parthenogenetic activation of oocytes in c-mos-deficient mice. Nature 370:68–71. doi:10.1038/370068a0
Hashimoto Y, Maegawa S, Nagai T, Yamaha E, Suzuki H, Yasuda K, Inoue K (2004) Localized maternal factors are required for zebrafish germ cell formation. Dev Biol 268:152–161. doi:10.1016/j.ydbio.2003.12.013
Heytens E, Parrington J, Coward K, Young C, Lambrecht S, Yoon S-Y, Fissore RA, Hamer R, Deane CM, Ruas M, Grasa P, Soleimani R, Cuvelier CA, Gerris J, Dhont M, Deforce D, Leybaert L, De Sutter P (2009) Reduced amounts and abnormal forms of phospholipase C zeta (PLCζ) in spermatozoa from infertile men. Hum Reprod 24:2417–2428. doi:10.1093/humrep/dep207
Hilscher B, Hilscher W, Bulthoff-Ohnolz B, Kramer U, Birke A, Pelzer H, Gauss G (1974) Kinetics of gametogenesis. I. Comparative histological and autoradiographic studies of oocytes and transitional prospermatogonia during oogenesis and prespermatogenesis. Cell Tissue Res 154:443–470. doi:10.1007/BF00219667
Holt JE, Lane SI, Jones KT (2013) The control of meiotic maturation in mammalian oocytes. Curr Top Dev Biol 102:207–226. doi:10.1016/B978-0-12-416024-8.00007-6
Holt JE, Tran SM, Stewart JL, Minahan K, García-Higuera I, Moreno S, Jones KT (2011) The APC/C activator FZR1 coordinates the timing of meiotic resumption during prophase I arrest in mammalian oocytes. Development 138:905–913. doi:10.1242/dev.059022
Homa ST, Swann K (1994) Fertilization and early embryology: a cytosolic sperm factor triggers calcium oscillations and membrane hyperpolarizations in human oocytes. Hum Reprod 9:2356–2361
Houston DW, King ML (2000) A critical role for Xdazl, a germ plasm-localized RNA, in the differentiation of primordial germ cells in Xenopus. Development 127:447–456
Hughes RL, Hall LS (1998) Early development and embryology of the platypus. Philos Trans R Soc Lond B Biol Sci 353:1101–1114. doi:10.1098/rstb.1998.0269
Hyldig SM, Croxall N, Contreras DA, Thomsen PD, Alberio R (2011) Epigenetic reprogramming in the porcine germ line. BMC Dev Biol 11:11. doi:10.1186/1471-213X-11-11
Igusa Y, Miyazaki S (1983) Effects of altered extracellular and intracellular calcium concentration on hyperpolarizing responses of the hamster egg. J Physiol 340:611–632. doi:10.1113/jphysiol.1983.sp014783
Ikenishi K, Nieuwkoop PD (1978) Location and ultrastructure of primordial germ cells (PGCs) in Ambystoma mexicanum. Dev Growth Diff 20:1–9. doi:10.1111/j.1440-169X.1978.00001.x
Ito M, Nagaoka K, Kuroda K, Kawano N, Yoshida K, Harada Y, Shikano T, Miyado M, Oda S, Toshimori K, Mizukami Y, Murata T, Umezawa A, Miyazaki S, Miyado K (2010) Arrest of spermatogenesis at round spermatids in PLCZ1-deficient mice. In: Abstract at the 11th international symposium on spermatology, Okinawa
Ito M, Shikano T, Kuroda K, Miyazaki S (2008) Relationship between nuclear sequestration of PLCζ and termination of PLCζ-induced Ca2+ oscillations in mouse eggs. Cell Calcium 44:400–410. doi:10.1016/j.ceca.2008.02.003
Ito S (1972) Effects of media of different ionic composition on the activation potential of anuran egg cells. Dev Growth Differ 14:217–227. doi:10.1111/j.1440-169X.1972.00217.x
Iwamatsu T (1969) Changes of the chorion upon fertilization in the medaka, Oryzias latipes. Bull Aichi Univ Educ 18:43–56
Iwamatsu T (2000) Fertilization in fishes. In: Tarin JJ, Cano A (eds) Fertilization in protozoa and metazoan and animals. Springer, Berlin, Heidelberg
Iwamatsu T, Ota I (1974) Cleavage initiating activities of sperm fractions injected into the egg of the medaka, Oryzias latipes. J Exp Zool 187:3–15. doi:10.1002/jez.1401870103
Iwao Y (2000) Fertilization in amphibians. In: Tarin JJ, Cano A (eds) Fertilization in protozoa and metazoan animals. Springer, Berlin, Heidelberg
Iwao Y (2012) Egg activation in physiological polyspermy. Reproduction 144:11–22. doi:10.1530/rep-12-0104
Iwao Y, Fujimura T (1996) Activation of Xenopus eggs by RGD-containing peptides accompanied by intracellular Ca2+ release. Dev Biol 177:558–567. doi:10.1006/dbio.1996.0185
Iwao Y, Jaffe LA (1989) Evidence that the voltage-dependent component in the fertilization process is contributed by the sperm. Dev Biol 134:446–451. doi:10.1016/0012-1606(89)90117-6
Iwao Y, Miki A, Kobayashi M, Onitake K (1994) Activation of Xenopus eggs by an extract of Cynops sperm. Dev Growth Differ 36:469–479. doi:10.1111/j.1440-169X.1994.00469.x
Jaffe LF (1983) Sources of calcium in egg activation: a review and hypothesis. Dev Biol 99:265–276. doi:10.1016/0012-1606(83)90276-2
Jaffe LF (1991) The path of calcium in cytosolic calcium oscillations: a unifying hypothesis. Proc Natl Acad Sci U S A 88:9883–9887. doi:10.1073/pnas.88.21.9883
Jaffe LA, Cross NL (1986) Electrical regulation of sperm-egg fusion. Annu Rev Physiol 48:191–200. doi:10.1146/annurev.ph.48.030186.001203
Jaffe LA, Sharp AP, Wolf DP (1983) Absence of an electrical polyspermy block in the mouse. Dev Biol 96:317–323. doi:10.1016/0012-1606(83)90168-9
Jalabert B (2005) Particularities of reproduction and oogenesis in teleost fish compared to mammals. Reprod Nutr Dev 45:261–279
Jin F, Hamada M, Malureanu L, Jeganathan KB, Zhou W, Morbeck DE, van Deursen JM (2010) Cdc20 is critical for meiosis I and fertility of female mice. PLoS Genet 6:e1001147. doi:10.1371/journal.pgen.1001147
Johnson AD, Alberio R (2015) Primordial germ cells: the first cell lineage or the last cells standing? Development 142:2730–2739. doi:10.1242/dev.113993
Jones KT (1998) Ca2+ oscillations in the activation of the egg and development of the embryo in mammals. Int J Dev Biol 42:1–10
Jones KT (2007) Intracellular calcium in the fertilization and development of mammalian eggs. Clin Exp Pharmacol Physiol 34:1084–1089. doi:10.1111/j.1440-1681.2007.04726.x
Jones KT, Nixon VL (2000) Sperm-induced Ca2+ oscillations in mouse oocytes and eggs can be mimicked by photolysis of caged inositol 1,4,5-trisphosphate: evidence to support a continuous low level production of inositol 1,4,5-trisphosphate during mammalian fertilization. Dev Biol 225:1–12. doi:10.1006/dbio.2000.9826
Kanatsu-Shinohara M, Schultz RM, Kopf GS (2000) Acquisition of meiotic competence in mouse oocytes: absolute amounts of p34cdc2, cyclin B1, cdc25C, and wee1 in meiotically incompetent and competent oocytes. Biol Reprod 63:1610–1616. doi:10.1095/biolreprod63.6.1610
Kashir J, Deguchi R, Jones C, Coward K, Stricker SA (2013) Comparative biology of sperm factors and fertilization-induced calcium signals across the animal kingdom. Mol Reprod Dev 80:787–815. doi:10.1002/mrd.22222
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, Coward K (2012) A maternally inherited autosomal point mutation in human phospholipase C zeta (PLCζ) leads to male infertility. Hum Reprod 27:222–231. doi:10.1093/humrep/der384
Kinsey WH, Wu W, Macgregor E (2003) Activation of Src-family PTK activity at fertilization: role of the SH2 domain. Dev Biol 264:255–262. doi:10.1016/j.ydbio.2003.08.014
Kirschner LS, Yin Z, Jones GN, Mahoney E (2009) Mouse models of altered protein kinase A signaling. Endocr Relat Cancer 16:773–793. doi:10.1677/erc-09-0068
Kline D, Kline JT (1992) Thapsigargin activates a calcium influx pathway in the unfertilized mouse egg and suppresses repetitive calcium transients in the fertilized egg. J Biol Chem 267:17624–17630
Kline D, Nuccitelli R (1985) The wave of activation current in the Xenopus egg. Dev Biol 111:471–487. doi:10.1016/0012-1606(85)90499-3
Kline D, Simoncini L, Mandel G, Maue RA, Kado RT, Jaffe LA (1988) Fertilization events induced by neurotransmitters after injection of mRNA in Xenopus eggs. Science 241:464–467
Knott JG, Gardner AJ, Madgwick S, Jones KT, Williams CJ, Schultz RM (2006) Calmodulin-dependent protein kinase II triggers mouse egg activation and embryo development in the absence of Ca2+ oscillations. Dev Biol 296:388–395. doi:10.1016/j.ydbio.2006.06.004
Knott JG, Kurokawa M, Fissore RA, Schultz RM, Williams CJ (2005) Transgenic RNA interference reveals role for mouse sperm phospholipase Cζ in triggering Ca2+ oscillations during fertilization. Biol Reprod 72:992–996. doi:10.1095/biolreprod.104.036244
Kobayashi W, Yamamoto TS (1994) Fertilization of the lamprey (Lampetra japonica) eggs: implication of the presence of fast and permanent blocks against polyspermy. J Exp Zool 269:166–176. doi:10.1002/jez.1402690210
Koh S, Lee K, Wang C, Machaty Z (2007) Characterization of STIM1 gene expression in porcine oocytes. Biol Reprod 77(Suppl 1):139
Kono T, Jones KT, Bos-Mikich A, Whittingham DG, Carroll J (1996) A cell cycle-associated change in Ca2+ releasing activity leads to the generation of Ca2+ transients in mouse embryos during the first mitotic division. J Cell Biol 132:915–923. doi:10.1083/jcb.132.5.915
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 eggs. J Biol Chem 279:10408–10412. doi: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. J Biol Chem 280:21015–21021. doi:10.1074/jbc.M412123200
Kuo RC, Baxter GT, Thompson SH, Stricker SA, Patton C, Bonaventura J, Epel D (2000) NO is necessary and sufficient for egg activation at fertilization. Nature 406:633–636. doi:10.1038/35020577
Kuwana T, Maeda-Suga H, Fujimoto T (1986) Attraction of chick primordial germ cells by gonadal anlage in vitro. Anat Rec 215:403–406. doi:10.1002/ar.1092150411
Larabell CA, Rowning BA, Moon RT (2004) A PKC wave follows the calcium wave after activation of Xenopus eggs. Differentiation 72:41–47. doi:10.1111/j.1432-0436.2004.07201005.x
Lara-Gonzalez P, Westhorpe Frederick G, Taylor Stephen S (2012) The spindle assembly checkpoint. Curr Biol 22:R966–R980. doi:10.1016/j.cub.2012.10.006
Larman MG, Saunders CM, Carroll J, Lai FA, Swann K (2004) Cell cycle-dependent Ca2+ oscillations in mouse embryos are regulated by nuclear targeting of PLCζ. J Cell Sci 117:2513–2521. doi:10.1242/jcs.01109
Lawrence Y, Whitaker M, Swann K (1997) Sperm-egg fusion is the prelude to the initial Ca2+ increase at fertilization in the mouse. Development 124:233–241
Lee K, Wang C, Machaty Z (2012) STIM1 is required for Ca2+ signaling during mammalian fertilization. Dev Biol 367:154–162. doi:10.1016/j.ydbio.2012.04.028
Lee KW, Webb SE, Miller AL (1999) A wave of free cytosolic calcium traverses zebrafish eggs on activation. Dev Biol 214:168–180. doi:10.1006/dbio.1999.9396
Leikin YN, Zharova TV, Tjulina OV (1993) Novel oxaloacetate effect on mitochondrial Ca2+ movement. FEBS Lett 331:35–37. doi:10.1016/0014-5793(93)80292-3
Lemaître JM, Bocquet S, Méchali M (2002) Competence to replicate in the unfertilized egg is conferred by Cdc6 during meiotic maturation. Nature 419:718–722. doi:10.1038/nature01046
Lesch BJ, Page DC (2012) Genetics of germ cell development. Nat Rev Genet 13:781–794. doi:10.1038/nrg3294
Lim D, Kyozuka K, Gragnaniello G, Carafoli E, Santella L (2001) NAADP+ initiates the Ca2+ response during fertilization of starfish oocytes. FASEB J 15:2257–2267. doi:10.1096/fj.01-0157com
Liou J, Kim ML, Heo WD, Jones JT, Myers JW, Ferrell JE Jr, Meyer T (2005) STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr Biol 15:1235–1241. doi:10.1016/j.cub.2005.05.055
Liu J, Maller JL (2005) Xenopus Polo-like kinase Plx1: a multifunctional mitotic kinase. Oncogene 24:238–247. doi:10.1038/sj.onc.1208220
Lodé T (2012) Sex and the origin of genetic exchanges. Trends Evol Biol 4:e1. doi:10.4081/eb.2012.e1
Long JA, Mark-Kurik E, Johanson Z, Lee MS, Young GC, Min Z, Ahlberg PE, Newman M, Jones R, den Blaauwen J, Choo B, Trinajstic K (2015) Copulation in antiarch placoderms and the origin of gnathostome internal fertilization. Nature 517:196–199. doi:10.1038/nature13825
Lorca T, Cruzalegui FH, Fesquet D, Cavadore JC, Méry J, Means A, Dorée M (1993) Calmodulin-dependent protein kinase II mediates inactivation of MPF and CSF upon fertilization of Xenopus eggs. Nature 366:270–273. doi:10.1038/366270a0
Lorca T, Galas S, Fesquet D, Devault A, Cavadore JC, Dorée M (1991) Degradation of the proto-oncogene product p39mos is not necessary for cyclin proteolysis and exit from meiotic metaphase: requirement for a Ca2+-calmodulin dependent event. EMBO J 10:2087–2093
Machaca K (2004) Increased sensitivity and clustering of elementary Ca2+ release events during oocyte maturation. Dev Biol 275:170–182. doi:10.1016/j.ydbio.2004.08.004
Machaty Z, Bonk AJ, Kühholzer B, Prather RS (2000) Porcine oocyte activation induced by a cytosolic sperm factor. Mol Reprod Dev 57:290–295. doi:10.1002/1098-2795(200011)57:3<290::AID-MRD11>3.0.CO;2-#
Machaty Z, Mayes MA, Kovács LG, Balatti PA, Kim JH, Prather RS (1997) Activation of porcine oocytes via an exogenously introduced rat muscarinic M1 receptor. Biol Reprod 57:85–91. doi:10.1095/biolreprod57.1.85
Machaty Z, Ramsoondar JJ, Bonk AJ, Bondioli KR, Prather RS (2002) Capacitative calcium entry mechanism in porcine oocytes. Biol Reprod 66:667–674. doi:10.1095/biolreprod66.3.667
Madgwick S, Hansen DV, Levasseur M, Jackson PK, Jones KT (2006) Mouse Emi2 is required to enter meiosis II by reestablishing cyclin B1 during interkinesis. J Cell Biol 174:791–801. doi:10.1083/jcb.200604140
Maegawa S, Yasuda K, Inoue K (1999) Maternal mRNA localization of zebrafish DAZ-like gene. Mech Dev 81:223–226. doi:10.1016/S0925-4773(98)00242-1
Mammadova G, Iwasaki T, Tokmakov AA, Fukami Y, Sato K (2009) Evidence that phosphatidylinositol 3-kinase is involved in sperm-induced tyrosine kinase signaling in Xenopus egg fertilization. BMC Dev Biol 9:68. doi:10.1186/1471-213X-9-68
Mao L, Lou H, Lou Y, Wang N, Jin F (2014) Behaviour of cytoplasmic organelles and cytoskeleton during oocyte maturation. Reprod Biomed Online 28:284–299. doi:10.1016/j.rbmo.2013.10.016
Marangos P, Carroll J (2004) The dynamics of cyclin B1 distribution during meiosis I in mouse oocytes. Reproduction 128:153–162. doi:10.1530/rep.1.00192
Marangos P, FitzHarris G, Carroll J (2003) Ca2+ oscillations at fertilization in mammals are regulated by the formation of pronuclei. Development 130:1461–1472. doi:10.1242/dev.00340
Marangos P, Verschuren EW, Chen R, Jackson PK, Carroll J (2007) Prophase I arrest and progression to metaphase I in mouse oocytes are controlled by Emi1-dependent regulation of APCCdh1. J Cell Biol 176:65–75. doi:10.1083/jcb.200607070
Markoulaki S, Matson S, Ducibella T (2004) Fertilization stimulates long-lasting oscillations of CaMKII activity in mouse eggs. Dev Biol 272:15–25. doi:10.1016/j.ydbio.2004.04.008
Martín-Romero FJ, Ortíz-de-Galisteo JR, Lara-Laranjeira J, Domínguez-Arroyo JA, González-Carrera E, Álvarez IS (2008) Store-operated calcium entry in human oocytes and sensitivity to oxidative stress. Biol Reprod 78:307–315. doi:10.1095/biolreprod.107.064527
Masciarelli S, Horner K, Liu C, Park SH, Hinckley M, Hockman S, Nedachi T, Jin C, Conti M, Manganiello V (2004) Cyclic nucleotide phosphodiesterase 3A-deficient mice as a model of female infertility. J Clin Invest 114:196–205. doi:10.1172/JCI200421804
Masui Y, Markert CL (1971) Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J Exp Zool 177:129–145. doi:10.1002/jez.1401770202
Matsu-ura T, Michikawa T, Inoue T, Miyawaki A, Yoshida M, Mikoshiba K (2006) Cytosolic inositol 1,4,5-trisphosphate dynamics during intracellular calcium oscillations in living cells. J Cell Biol 173:755–765. doi:10.1083/jcb.200512141
Mattioli M, Galeati G, Bacci ML, Barboni B (1991) Changes in maturation-promoting activity in the cytoplasm of pig oocytes throughout maturation. Mol Reprod Dev 30:119–125. doi:10.1002/mrd.1080300208
McCulloh DH, Chambers EL (1992) Fusion of membranes during fertilization. Increases of the sea urchin egg’s membrane capacitance and membrane conductance at the site of contact with the sperm. J Gen Physiol 99:137–175. doi:10.1085/jgp.99.2.137
McCulloh DH, Rexroad CE Jr, Levitan H (1983) Insemination of rabbit eggs is associated with slow depolarization and repetitive diphasic membrane potentials. Dev Biol 95:372–377. doi:10.1016/0012-1606(83)90038-6
McGuinness OM, Moreton RB, Johnson MH, Berridge MJ (1996) A direct measurement of increased divalent cation influx in fertilised mouse oocytes. Development 122:2199–2206
Medina IR, Bregestovski PD (1988) Stretch-activated ion channels modulate the resting membrane potential during early embryogenesis. Proc R Soc Lond B Biol Sci 235:95–102. doi:10.1098/rspb.1988.0064
Mehlmann LM, Carpenter G, Rhee SG, Jaffe LA (1998) SH2 domain-mediated activation of phospholipase Cγ is not required to initiate Ca2+ release at fertilization of mouse eggs. Dev Biol 203:221–232. doi:10.1006/dbio.1998.9051
Mehlmann LM, Chattopadhyay A, Carpenter G, Jaffe LA (2001) Evidence that phospholipase C from the sperm is not responsible for initiating Ca2+ release at fertilization in mouse eggs. Dev Biol 236:492–501. doi:10.1006/dbio.2001.0329
Mei W, Lee KW, Marlow FL, Miller AL, Mullins MC (2009) hnRNP I is required to generate the Ca2+ signal that causes egg activation in zebrafish. Development 136:3007–3017. doi:10.1242/dev.037879
Messerschmidt DM, Knowles BB, Solter D (2014) DNA methylation dynamics during epigenetic reprogramming in the germline and preimplantation embryos. Genes Dev 28:812–828. doi:10.1101/gad.234294.113
Meyerhof PG, Masui Y (1977) Ca and Mg control of cytostatic factors from Rana pipiens oocytes which cause metaphase and cleavage arrest. Dev Biol 61:214–229. doi:10.1016/0012-1606(77)90293-7
Miao YL, Stein P, Jefferson WN, Padilla-Banks E, Williams CJ (2012) Calcium influx-mediated signaling is required for complete mouse egg activation. Proc Natl Acad Sci U S A 109:4169–4174. doi:10.1073/pnas.1112333109
Mikoshiba K (1993) Inositol 1,4,5-trisphosphate receptor. Trends Pharmacol Sci 14:86–89. doi:10.1016/0165-6147(93)90069-V
Missiaen L, Parys J, Smedt HD, Sienaert I, Sipma H, Vanlingen S, Maes K, Casteels R (1997) Effect of adenine nucleotides on myo-inositol-1,4,5-trisphosphate-induced calcium release. Biochem J 325:661–666
Miyazaki S (1988) Inositol 1,4,5-trisphosphate-induced calcium release and guanine nucleotide-binding protein-mediated periodic calcium rises in golden hamster eggs. J Cell Biol 106:345–353
Miyazaki S, Igusa Y (1981) Fertilization potential in golden hamster eggs consists of recurring hyperpolarizations. Nature 290:702–704. doi:10.1038/290702a0
Miyazaki S, Igusa Y (1982) Ca-mediated activation of a K current at fertilization of golden hamster eggs. Proc Natl Acad Sci U S A 79:931–935
Miyazaki S, Hashimoto N, Yoshimoto Y, Kishimoto T, Igusa Y, Hiramoto Y (1986) Temporal and spatial dynamics of the periodic increase in intracellular free calcium at fertilization of golden hamster eggs. Dev Biol 118:259–267. doi:10.1016/0012-1606(86)90093-X
Miyazaki S, Katayama Y, Swann K (1990) Synergistic activation by serotonin and GTP analogue and inhibition by phorbol ester of cyclic Ca2+ rises in hamster eggs. J Physiol 426:209–227. doi:10.1113/jphysiol.1990.sp018134
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 eggs. Dev Biol 158:62–78. doi:10.1006/dbio.1993.1168
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 eggs. Science 257:251–255. doi:10.1126/science.1321497
Mizushima S, Takagi S, Ono T, Atsumi Y, Tsukada A, Saito N, Shimada K (2008) Developmental enhancement of intracytoplasmic sperm injection (ICSI)-generated quail embryos by phospholipase Cζ cRNA. J Poult Sci 45:152–158. doi:10.2141/jpsa.45.152
Mohri T, Shirakawa H, Oda S, Sato MS, Mikoshiba K, Miyazaki S (2001) Analysis of Mn2+/Ca2+ influx and release during Ca2+ oscillations in mouse eggs injected with sperm extract. Cell Calcium 29:311–325. doi:10.1054/ceca.2000.0196
Morgan DO (1995) Principles of CDK regulation. Nature 374:131–134. doi:10.1038/374131a0
Nalefski EA, Falke JJ (1996) The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci 5:2375–2390. doi:10.1002/pro.5560051201
Nixon VL, Levasseur M, McDougall A, Jones KT (2002) Ca2+ oscillations promote APC/C-dependent Cyclin B1 degradation during metaphase arrest and completion of meiosis in fertilizing mouse eggs. Curr Biol 12:746–750. doi:10.1016/S0960-9822(02)00811-4
Nomikos M, Blayney LM, Larman MG, Campbell K, Rossbach A, Saunders CM, Swann K, Lai FA (2005) Role of phospholipase C-ζ domains in Ca2+-dependent phosphatidylinositol 4,5-bisphosphate hydrolysis and cytoplasmic Ca2+ oscillations. J Biol Chem 280:31011–31018. doi:10.1074/jbc.M500629200
Nomikos M, Elgmati K, Theodoridou M, Calver BL, Nounesis G, Swann K, Lai FA (2011a) Phospholipase Cζ binding to PtdIns(4,5)P requires the XY-linker region. J Cell Sci 124:2582–2590. doi:10.1242/jcs.083485
Nomikos M, Elgmati K, Theodoridou M, Georgilis A, Gonzalez-Garcia JR, Nounesis G, Swann K, Lai FA (2011b) Novel regulation of PLCζ activity via its XY-linker. Biochem J 438:427–432. doi:10.1042/BJ20110953
Nomikos M, Kashir J, Swann K, Lai FA (2013) Sperm PLCζ: from structure to Ca2+ oscillations, egg activation and therapeutic potential. FEBS Lett 587:3609–3616. doi:10.1016/j.febslet.2013.10.008
Nomikos M, Mulgrew-Nesbitt A, Pallavi P, Mihalyne G, Zaitseva I, Swann K, Lai FA, Murray D, McLaughlin S (2007) Binding of phosphoinositide-specific phospholipase C-ζ (PLC-ζ) to phospholipid membranes: potential role of an unstructured cluster of basic residues. J Biol Chem 282:16644–16653. doi:10.1074/jbc.M701072200
Nomikos M, Sanders JR, Theodoridou M, Kashir J, Matthews E, Nounesis G, Lai FA, Swann K (2014) Sperm-specific post-acrosomal WW-domain binding protein (PAWP) does not cause Ca2+ release in mouse oocytes. Mol Hum Reprod 20:938–947. doi:10.1093/molehr/gau056
Nomikos M, Swann K, Lai FA (2015) Is PAWP the "real" sperm factor? Asian J Androl 17:444–446. doi:10.4103/1008-682X.142145
Nuccitelli R (1980) The electrical changes accompanying fertilization and cortical vesicle secretion in the medaka egg. Dev Biol 76:483–498. doi:10.1016/0012-1606(80)90396-6
Nuccitelli R, Yim DL, Smart T (1993) The sperm-induced Ca2+ wave following fertilization of the Xenopus egg requires the production of Ins(1,4,5)P3. Dev Biol 158:200–212. doi:10.1006/dbio.1993.1179
Ohinata Y, Ohta H, Shigeta M, Yamanaka K, Wakayama T, Saitou M (2009) A signaling principle for the specification of the germ cell lineage in mice. Cell 137:571–584. doi:10.1016/j.cell.2009.03.014
Ohinata Y, Payer B, O'Carroll D, Ancelin K, Ono Y, Sano M, Barton SC, Obukhanych T, Nussenzweig M, Tarakhovsky A, Saitou M, Surani MA (2005) Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436:207–213. doi:10.1038/nature03813
Otani S, Iwai T, Nakahata S, Sakai C, Yamashita M (2009) Artificial fertilization by intracytoplasmic sperm injection in a teleost fish, the medaka (Oryzias latipes). Biol Reprod 80:175–183. doi:10.1095/biolreprod.108.069880
Ozil JP, Huneau D (2001) Activation of rabbit oocytes: the impact of the Ca2+ signal regime on development. Development 128:917–928
Ozil JP, Banrezes B, Tóth S, Pan H, Schultz RM (2006) Ca2+ oscillatory pattern in fertilized mouse eggs affects gene expression and development to term. Dev Biol 300:534–544. doi:10.1016/j.ydbio.2006.08.041
Ozil JP, Markoulaki S, Toth S, Matson S, Banrezes B, Knott JG, Schultz RM, Huneau D, Ducibella T (2005) Egg activation events are regulated by the duration of a sustained [Ca2+]cyt signal in the mouse. Dev Biol 282:39–54. doi:10.1016/j.ydbio.2005.02.035
Parrington J, Jones M, Tunwell R, Devader C, Katan M, Swann K (2002) Phospholipase C isoforms in mammalian spermatozoa: potential components of the sperm factor that causes Ca2+ release in eggs. Reproduction 123:31–39. doi:10.1530/rep.0.1230031
Parrington J, Swann K, Shevchenko VI, Sesay AK, Lai FA (1996) Calcium oscillations in mammalian eggs triggered by a soluble sperm protein. Nature 379:364–368. doi:10.1038/379364a0
Patiño R, Sullivan C (2002) Ovarian follicle growth, maturation, and ovulation in teleost fish. Fish Physiol Biochem 26:57–70. doi:10.1023/A:1023311613987
Pepling ME, Spradling AC (1998) Female mouse germ cells form synchronously dividing cysts. Development 125:3323–3328
Peres A (1986) Resting membrane potential and inward current properties of mouse ovarian oocytes and eggs. Pflugers Arch 407:534–540
Peters JM (2006) The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat Rev Mol Cell Biol 7:644–656. doi:10.1038/nrm1988
Petersen C, Berridge MJ, Borgese MF, Bennett DL (1995) Putative capacitative calcium entry channels: expression of Drosophila trp and evidence for the existence of vertebrate homologues. Biochem J 311:41–44
Polzonetti V, Cardinali M, Mosconi G, Natalini P, Meiri I, Carnevali O (2002) Cyclic ADPR and calcium signaling in sea bream (Sparus aurata) egg fertilization. Mol Reprod Dev 61:213–217. doi:10.1002/mrd.1150
Popp C, Dean W, Feng S, Cokus SJ, Andrews S, Pellegrini M, Jacobsen SE, Reik W (2010) Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463:1101–1105. doi:10.1038/nature08829
Prasad SV, Skinner SM, Carino C, Wang N, Cartwright J, Dunbar BS (2000) Structure and function of the proteins of the mammalian Zona pellucida. Cells Tissues Organs 166:148–164. doi:10.1159/000016730
Rice A, Parrington J, Jones KT, Swann K (2000) Mammalian sperm contain a Ca2+-sensitive phospholipase C activity that can generate InsP3 from PIP2 associated with intracellular organelles. Dev Biol 228:125–135. doi:10.1006/dbio.2000.9929
Ridgway EB, Gilkey JC, Jaffe LF (1977) Free calcium increases explosively in activating medaka eggs. Proc Natl Acad Sci U S A 74:623–627
Robinson R (2008) For Mammals, Loss of yolk and gain of milk went hand in hand. PLoS Biol 6:e77. doi:10.1371/journal.pbio.0060077
Rogers NT, Hobson E, Pickering S, Lai FA, Braude P, Swann K (2004) Phospholipase Cζ causes Ca2+ oscillations and parthenogenetic activation of human oocytes. Reproduction 128:697–702. doi:10.1530/rep.1.00484
Roos J, DiGregorio PJ, Yeromin AV, Ohlsen K, Lioudyno M, Zhang S, Safrina O, Kozak JA, Wagner SL, Cahalan MD (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol 169:435–445. doi:10.1083/jcb.200502019
Runft LL, Watras J, Jaffe LA (1999) Calcium release at fertilization of Xenopus eggs requires type I IP3 receptors, but not SH2 domain-mediated activation of PLCγ or Gq-mediated activation of PLC β. Dev Biol 214:399–411. doi:10.1006/dbio.1999.9415
Sagata N, Oskarsson M, Copeland T, Brumbaugh J, Vande Woude GF (1988) Function of c-mos proto-oncogene product in meiotic maturation in Xenopus oocytes. Nature 335:519–525. doi:10.1038/335519a0
Sakai N, Burgess S, Hopkins N (1997) Delayed in vitro fertilization of zebrafish eggs in Hank's saline containing bovine serum albumin. Mol Mar Biol Biotechnol 6:84–87
Sato K (2008) Signal transduction of fertilization in frog eggs and anti-apoptotic mechanism in human cancer cells: common and specific functions of membrane microdomains. Open Biochem J 2:49–59. doi:10.2174/1874091X00802010049
Satouh Y, Nozawa K, Ikawa M (2015) Sperm postacrosomal WW domain-binding protein is not required for mouse egg activation. Biol Reprod 93:94. doi:10.1095/biolreprod.115.131441
Saunders CM, Larman MG, Parrington J, Cox LJ, Royse J, Blayney LM, Swann K, Lai FA (2002) PLCζ: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development. Development 129:3533–3544
Saunders CM, Swann K, Lai FA (2007) PLCzeta, a sperm-specific PLC and its potential role in fertilization. Biochem Soc Symp 74:23–36. doi:10.1042/BSS0740023
Schatten G (1994) The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization. Dev Biol 165:299–335. doi:10.1006/dbio.1994.1256
Schatten G, Simerly C, Schatten H (1985) Microtubule configurations during fertilization, mitosis, and early development in the mouse and the requirement for egg microtubule-mediated motility during mammalian fertilization. Proc Natl Acad Sci U S A 82:4152–4156
Schatten H, Sun QY (2009) The role of centrosomes in mammalian fertilization and its significance for ICSI. Mol Hum Reprod 15:531–538. doi:10.1093/molehr/gap049
Schindler K, Schultz RM (2009) CDC14B acts through FZR1 (CDH1) to prevent meiotic maturation of mouse oocytes. Biol Reprod 80:795–803. doi:10.1095/biolreprod.108.074906
Schoenwolf GC (1997) Reptiles and embryos. In: Gilbert SF, Raunio AM (eds) Embryology. Constructing the organism. Sinauer Associates, Inc. Publishers, Sunderland
Selman K, Wallace RA, Sarka A, Qi X (1993) Stages of oocyte development in the zebrafish, Brachydanio rerio. J Morphol 218:203–224. doi:10.1002/jmor.1052180209
Sette C, Bevilacqua A, Bianchini A, Mangia F, Geremia R, Rossi P (1997) Parthenogenetic activation of mouse eggs by microinjection of a truncated c-kit tyrosine kinase present in spermatozoa. Development 124:2267–2274
Sette C, Paronetto MP, Barchi M, Bevilacqua A, Geremia R, Rossi P (2002) Tr-kit-induced resumption of the cell cycle in mouse eggs requires activation of a Src-like kinase. EMBO J 21:5386–5395. doi:10.1093/emboj/cdf553
Sever DM, Brizzi R (1998) Comparative biology of sperm storage in female salamanders. J Exp Zool 282:460–476. doi:10.1002/(SICI)1097-010X(199811/12)282:4/5<460::AID-JEZ5>3.0.CO;2-O
Sharma D, Kinsey WH (2008) Regionalized calcium signaling in zebrafish fertilization. Int J Dev Biol 52:561–570. doi:10.1387/ijdb.072523ds
Shen SS, Steinhardt RA (1984) Time and voltage windows for reversing the electrical block to fertilization. Proc Natl Acad Sci U S A 81:1436–1439
Shevchenko V, Hogben M, Ekong R, Parrington J, Lai FA (1998) The human glucosamine-6-phosphate deaminase gene: cDNA cloning and expression, genomic organization and chromosomal localization. Gene 216:31–38. doi:10.1016/S0378-1119(98)00335-7
Shiina Y, Kaneda M, Matsuyama K, Tanaka K, HiroiM DK (1993) Role of the extracellular Ca2+ on the intracellular Ca2+ changes in fertilized and activated mouse oocytes. J Reprod Fertil 97:143–150. doi:10.1530/jrf.0.0970143
Shilling FM, Krätzschmar J, Cai H, Weskamp G, Gayko U, Leibow J, Myles DG, Nuccitelli R, Blobel CP (1997) Identification of metalloprotease/disintegrins in Xenopus laevis testis with a potential role in fertilization. Dev Biol 186:155–164. doi:10.1006/dbio.1997.8586
Shilling FM, Magie CR, Nuccitelli R (1998) Voltage-dependent activation of frog eggs by a sperm surface disintegrin peptide. Dev Biol 202:113–124. doi:10.1006/dbio.1998.8982
Shirakawa H, Ito M, Sato M, Umezawa Y, Miyazaki S (2006) Measurement of intracellular IP during Ca2+ oscillations in mouse eggs with GFP-based FRET probe. Biochem Biophys Res Commun 345:781–788. doi:10.1016/j.bbrc.2006.04.133
Snow P, Yim DL, Leibow JD, Saini S, Nuccitelli R (1996) Fertilization stimulates an increase in inositol trisphosphate and inositol lipid levels in Xenopus eggs. Dev Biol 180:108–118. doi:10.1006/dbio.1996.0288
Specker JL, Sullivan CV (1994) Vitellogenesis in fishes: status and perspectives. In: Davey KG, Peter RE, Tobe SS (eds) Perspectives in comparative endocrinology. National Research Council, Ottawa
Speed RM (1982) Meiosis in the foetal mouse ovary: I. An analysis at the light microscope level using surface-spreading. Chromosoma 85:427–437
Stricker SA (1999) Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev Biol 211:157–176. doi:10.1006/dbio.1999.9340
Swann K (1990) A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs. Development 110:1295–1302
Swann K (1992) Different triggers for calcium oscillations in mouse eggs involve a ryanodine-sensitive calcium store. Biochem J 287:79–84
Swann K (1994) Ca2+ oscillations and sensitization of Ca2+ release in unfertilized mouse eggs injected with a sperm factor. Cell Calcium 15:331–339. doi:10.1016/0143-4160(94)90072-8
Swann K, Jones KT (2002) Membrane events of egg activation. In: Hardy DM (ed) Fertilization. Academic, San Diego
Swann K, Ozil JP (1994) Dynamics of the calcium signal that triggers mammalian egg activation. Int Rev Cytol 152:183–222. doi:10.1016/S0074-7696(08)62557-7
Swann K, Whitaker M (1986) The part played by inositol trisphosphate and calcium in the propagation of the fertilization wave in sea urchin eggs. J Cell Biol 103:2333–2342. doi:10.1083/jcb.103.6.2333
Swann K, Yu Y (2008) The dynamics of calcium oscillations that activate mammalian eggs. Int J Dev Biol 52:585–594. doi:10.1387/ijdb.072530ks
Swann K, Igusa Y, Miyazaki S (1989) Evidence for an inhibitory effect of protein kinase C on G-protein-mediated repetitive calcium transients in hamster eggs. EMBO J 8:3711–3718
Swann K, Parrington J, Jones KT (1998) On the search for the sperm oscillogen. Mol Hum Reprod 4:1010–1012
Swann K, Saunders CM, Rogers NT, Lai FA (2006) PLCζ(zeta): a sperm protein that triggers Ca2+ oscillations and egg activation in mammals. Semin Cell Dev Biol 17:264–273. doi:10.1016/j.semcdb.2006.03.009
Tachibana K, Tanaka D, Isobe T, Kishimoto T (2000) c-Mos forces the mitotic cell cycle to undergo meiosis II to produce haploid gametes. Proc Natl Acad Sci U S A 97:14301–14306. doi:10.1073/pnas.97.26.14301
Takahashi T, Kikuchi T, Kidokoro Y, Shirakawa H (2013) Ca2+ influx-dependent refilling of intracellular Ca2+ stores determines the frequency of Ca2+ oscillations in fertilized mouse eggs. Biochem Biophys Res Commun 430:60–65. doi:10.1016/j.bbrc.2012.11.024
Tan X, Chen DY, Yang Z, Wang YC, Li M, Schatten H, Sun QY (2001) Phosphorylation of p90rsk during meiotic maturation and parthenogenetic activation of rat oocytes: Correlation with MAP kinases. Zygote 9:269–276. doi:10.1017/S0967199401001290
Tarín JJ, Cano A (2000) Fertilization in protozoa and metazoan animals. Springer, Berlin, Heidelberg
Tatemoto H, Horiuchi T (1995) Requirement for protein synthesis during the onset of meiosis in bovine oocytes and its involvement in the autocatalytic amplification of maturation-promoting factor. Mol Reprod Dev 41:47–53. doi:10.1002/mrd.1080410108
Theusch EV, Brown KJ, Pelegri F (2006) Separate pathways of RNA recruitment lead to the compartmentalization of the zebrafish germ plasm. Dev Biol 292:129–141. doi:10.1016/j.ydbio.2005.12.045
Tokarz RR (1978) Oogonial proliferation, oogenesis, and folliculogenesis in nonmammalian vertebrates. In: Jones RE (ed) The vertebrate ovary. Plenum Press, New York
Tosti E, Palumbo A, Dale B (1993) Inositol tri-phosphate in human and ascidian spermatozoa. Mol Reprod Dev 35:52–56. doi:10.1002/mrd.1080350109
Tsunekawa N, Naito M, Sakai Y, Nishida T, Noce T (2000) Isolation of chicken vasa homolog gene and tracing the origin of primordial germ cells. Development 127:2741–2750
Tsuneyoshi N, Sumi T, Onda H, Nojima H, Nakatsuji N, Suemori H (2008) PRDM14 suppresses expression of differentiation marker genes in human embryonic stem cells. Biochem Biophys Res Commun 367:899–905. doi:10.1016/j.bbrc.2007.12.189
Turner PR, Jaffe LA, Fein A (1986) Regulation of cortical vesicle exocytosis in sea urchin eggs by inositol 1,4,5-trisphosphate and GTP-binding protein. J Cell Biol 102:70–76
Turner PR, Sheetz MP, Jaffe LA (1984) Fertilization increases the polyphosphoinositide content of sea urchin eggs. Nature 310:414–415. doi:10.1038/310414a0
Ukeshima A, Fujimoto T (1991) A fine morphological study of germ cells in asymmetrically developing right and left ovaries of the chick. Anat Rec 230:378–386. doi:10.1002/ar.1092300311
Verlhac MH, De Pennart H, Maro B, Cobb MH, Clarke HJ (1993) MAP kinase becomes stably activated at metaphase and is associated with microtubule-organizing centers during meiotic maturation of mouse oocytes. Dev Biol 158:330–340. doi:10.1006/dbio.1993.1192
Vig M, Peinelt C, Beck A, Koomoa DL, Rabah D, Koblan-Huberson M, Kraft S, Turner H, Fleig A, Penner R, Kinet JP (2006) CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 312:1220–1223. doi:10.1126/science.1127883
Wagner J, Fall CP, Hong F, Sims CE, Allbritton NL, Fontanilla RA, Moraru II, Loew LM, Nuccitelli R (2004) A wave of IP3 production accompanies the fertilization Ca2+ wave in the egg of the frog, Xenopus laevis: theoretical and experimental support. Cell Calcium 35:433–447. doi:10.1016/j.ceca.2003.10.009
Wallace RA, Selman K (1990) Ultrastructural aspects of oogenesis and oocyte growth in fish and amphibians. J Electron Microsc Tech 16:175–201. doi:10.1002/jemt.1060160302
Wang C, Lee K, Gajdócsi E, Papp ÁB, Machaty Z (2012) Orai1 mediates store-operated Ca2+ entry during fertilization in mammalian oocytes. Dev Biol 365:414–423. doi:10.1016/j.ydbio.2012.03.007
Wassarman PM, Jovine L, Qi H, Williams Z, Darie C, Litscher ES (2005) Recent aspects of mammalian fertilization research. Mol Cell Endocrinol 234:95–103. doi:10.1016/j.mce.2004.08.017
Weakley BS (1967) Light and electron microscopy of developing germ cells and follicle cells in the ovary of the golden hamster: twenty-four hours before birth to eight days post partum. J Anat 101:435–459
Webb SE, Miller AL (2013) Ca2+ signaling during activation and fertilization in the eggs of teleost fish. Cell Calcium 53:24–31. doi:10.1016/j.ceca.2012.11.002
Weber S, Eckert D, Nettersheim D, Gillis AJ, Schäfer S, Kuckenberg P, Ehlermann J, Werling U, Biermann K, Looijenga LH, Schorle H (2010) Critical function of AP-2 gamma/TCFAP2C in mouse embryonic germ cell maintenance. Biol Reprod 82:214–223. doi:10.1095/biolreprod.109.078717
Weissmann A (1885) The continuity of the germ-plasm as the foundation of a theory of heredity. In: Poulton EB, Schönland S, Shipley AE (eds) Essays upon heredity and kindred biological problems, 2nd edn. Clarendon, Oxford
Went DF, Krause G (1974) Egg activation in Pimpla turionellae (Hym.). Naturwissenschaften 61:407–408
Whitaker M (1996) Control of meiotic arrest. Rev Reprod 1:127–135
Whitaker M, Irvine RF (1984) Inositol 1,4,5-trisphosphate microinjection activates sea urchin eggs. Nature 312:636–639. doi:10.1038/312636a0
Whitaker MJ, Steinhardt RA (1982) Ionic regulation of egg activation. Q Rev Biophys 15:593–666. doi:10.1017/S0033583500003760
Whitaker M, Swann K (1993) Lighting the fuse at fertilization. Development 108:525–542
Whitington PM, Dixon KE (1975) Quantitative studies of germ plasm and germ cells during early embryogenesis of Xenopus laevis. J Embryol Exp Morphol 33:57–74
Whittingham DG (1980) Parthenogenesis in mammals. In: Oxford reviews of reproductive biology. Oxford University Press, New York
Williams CJ, Schultz RM, Kopf GS (1992) Role of G proteins in mouse egg activation: stimulatory effects of acetylcholine on the ZP2 to ZP2f conversion and pronuclear formation in eggs expressing a functional m1 muscarinic receptor. Dev Biol 151:288–296
Wishart GJ, Horrocks AJ (2000) Fertilization in birds. In: Tarin JJ, Cano A (eds) Fertilization in protozoa and metazoan animals. Springer, Berlin, Heidelberg
Wolosker H, Kline D, Bian Y, Blackshaw S, Cameron AM, Fralich TJ, Schnaar RL, Snyder SH (1998) Molecularly cloned mammalian glucosamine-6-phosphate deaminase localizes to transporting epithelium and lacks oscillin activity. FASEB J 12:91–99
Wu AT, Sutovsky P, Manandhar G, Xu W, Katayama M, Day BN, Park KW, Yi YJ, Xi YW, Prather RS, Oko R (2007) PAWP, a sperm-specific WW domain-binding protein, promotes meiotic resumption and pronuclear development during fertilization. J Biol Chem 282:12164–12175. doi:10.1074/jbc.M609132200
Wu H, He CL, Fissore RA (1997) Injection of a porcine sperm factor triggers calcium oscillations in mouse oocytes and bovine eggs. Mol Reprod Dev 46:176–189. doi:10.1002/(SICI)1098-2795(199702)46:2<176::AID-MRD8>3.0.CO;2-N
Wu H, Smyth J, Luzzi V, Fukami K, Takenawa T, Black SL, Allbritton NL, Fissore RA (2001) Sperm factor induces intracellular free calcium oscillations by stimulating the phosphoinositide pathway. Biol Reprod 64:1338–1349. doi:10.1095/biolreprod64.5.1338
Yamamoto S, Kubota HY, Yoshimoto Y, Iwao Y (2001) Injection of a sperm extract triggers egg activation in the newt Cynops pyrrhogaster. Dev Biol 230:89–99. doi:10.1006/dbio.2000.9949
Yang X, Sachs F (1989) Block of stretch-activated ion channels in Xenopus oocytes by gadolinium and calcium ions. Science 243:1068–1071. doi:10.1126/science.2466333
Yim DL, Opresko LK, Wiley HS, Nuccitelli R (1994) Highly polarized EGF receptor tyrosine kinase activity initiates egg activation in Xenopus. Dev Biol 162:41–55. doi:10.1006/dbio.1994.1065
Yoda A, Oda S, Shikano T, Kouchi Z, Awaji T, Shirakawa H, Kinoshita K, Miyazaki S (2004) Ca2+ oscillation-inducing phospholipase C zeta expressed in mouse eggs is accumulated to the pronucleus during egg activation. Dev Biol 268:245–257. doi:10.1016/j.ydbio.2003.12.028
Yoneda A, Kashima M, Yoshida S, Terada K, Nakagawa S, Sakamoto A, Hayakawa K, Suzuki K, Ueda J, Watanabe T (2006) Molecular cloning, testicular postnatal expression, and oocyte-activating potential of porcine phospholipase Cζ. Reproduction 132:393–401. doi:10.1530/rep.1.01018
Yoon SY, Fissore RA (2007) Release of phospholipase C ζ and [Ca2+]i oscillation-inducing activity during mammalian fertilization. Reproduction 134:695–704. doi:10.1530/rep-07-0259
Yoon C, Kawakami K, Hopkins N (1997) Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development 124:3157–3165
Yoon SY, Jellerette T, Salicioni AM, Lee HC, Yoo MS, Coward K, Parrington J, Grow D, Cibelli JB, Visconti PE, Mager J, Fissore RA (2008) 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 118:3671–3681. doi:10.1172/JCI36942
Young C, Grasa P, Coward K, Davis LC, Parrington J (2009) Phospholipase C zeta undergoes dynamic changes in its pattern of localization in sperm during capacitation and the acrosome reaction. Fertil Steril 91:2230–2242. doi:10.1016/j.fertnstert.2008.05.021
Yu F, Sun L, Machaca K (2009) Orai1 internalization and STIM1 clustering inhibition modulate SOCE inactivation during meiosis. Proc Natl Acad Sci U S A 106:17401–17406. doi:10.1073/pnas.0904651106
Yu Y, Nomikos M, Theodoridou M, Nounesis G, Lai FA, Swann K (2012) PLCζ causes Ca2+ oscillations in mouse eggs by targeting intracellular and not plasma membrane PI(4,5)P . Mol Biol Cell 23:371–380. doi:10.1091/mbc.E11-08-0687
Zhang SL, Yeromin AV, Zhang XH, Yu Y, Safrina O, Penna A, Roos J, Stauderman KA, Cahalan MD (2006) Genome-wide RNAi screen of Ca2+ influx identifies genes that regulate Ca2+ release-activated Ca2+ channel activity. Proc Natl Acad Sci U S A 103:9357–9362. doi:10.1073/pnas.0603161103
Zheng L, Krishnamoorthi R, Zolkiewski M, Wang X (2000) Distinct Ca2+ binding properties of novel C2 domains of plant phospholipase Dα and β. J Biol Chem 275:19700–19706. doi:10.1074/jbc.M001945200
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Machaty, Z., Miller, A.R., Zhang, L. (2017). Egg Activation at Fertilization. In: Pelegri, F., Danilchik, M., Sutherland, A. (eds) Vertebrate Development. Advances in Experimental Medicine and Biology, vol 953. Springer, Cham. https://doi.org/10.1007/978-3-319-46095-6_1
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