Advertisement

Universality and Diversity of a Fast, Electrical Block to Polyspermy During Fertilization in Animals

  • Yasuhiro Iwao
  • Kenta Izaki
Chapter
Part of the Diversity and Commonality in Animals book series (DCA)

Abstract

In the sexual reproduction of animals, fertilization is indispensable for the initiation of diploid embryonic development. Most animals exhibit monospermy, in which only one sperm enters an egg during normal fertilization. In monospermic species, a fast, electrical block on the egg membrane is one of the most important blocks to polyspermy. A fertilizing primary sperm usually causes a positive-going fertilization potential to prevent the subsequent entry of excess sperm. An increase in intracellular Ca2+ ([Ca2+]i) in the egg cytoplasm induced by the fertilizing sperm is necessary for egg activation and blocks polyspermy. The mechanism of voltage-dependent fertilization in monospermic amphibians is presented as a model system of vertebrate fertilization. The electrical polyspermy blocks in various animals are reviewed and their universality and diversity across the animal kingdom are discussed. Relationships between the fast, electrical block and [Ca2+]i increases in egg cytoplasm are discussed, as well as their changes throughout the course of animal evolution.

Keywords

Fertilization potential Fast polyspermy block [Ca2+]i increase Egg activation Sperm-egg fusion 

Notes

Acknowledgements

This work was supported by JSPS KAKENHI Grant Numbers, 22112518, 24112712, 26650083 to Y.I. and by The YU “Pump-Priming Program” for Fostering Research Activities.

References

  1. 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(10):4434–4440CrossRefPubMedGoogle Scholar
  2. Akiyama S, Iwao Y, Miura I (2011) Evidence for true fall-mating in Japanese newt Cynops pyrrhogaster. Zool Sci 28(10):758–763PubMedCrossRefGoogle Scholar
  3. al-Anzi B, Chandler DE (1998) A sperm chemoattractant is released from Xenopus egg jelly during spawning. Dev Biol 198(2):366–375PubMedCrossRefGoogle Scholar
  4. Arakawa M, Takeda N, Tachibana K, Deguchi R (2014) Polyspermy block in jellyfish eggs: collaborative controls by Ca(2+) and MAPK. Dev Biol 392(1):80–92PubMedCrossRefGoogle Scholar
  5. Bates RC, Fees CP, Holland WL, Winger CC, Batbayar K, Ancar R, Bergren T, Petcoff D, Stith BJ (2014) Activation of Src and release of intracellular calcium by phosphatidic acid during Xenopus laevis fertilization. Dev Biol 386(1):165–180CrossRefPubMedGoogle Scholar
  6. Berg C, Kirby C, Kline D, Jaffe LA (1986) Fertilization potential and polyspermy prevention in the egg of the hydrozoan Hydractinia echinata. Biol Bull (Woods Hole, Mass.) 171:485Google Scholar
  7. Bianchi E, Doe B, Goulding D, Wright GJ (2014) Juno is the egg Izumo receptor and is essential for mammalian fertilization. Nature 508(7497):483–487PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bothwell JH, Kisielewska J, Genner MJ, McAinsh MR, Brownlee C (2008) Ca2+ signals coordinate zygotic polarization and cell cycle progression in the brown alga Fucus serratus. Development 135(12):2173–2181PubMedCrossRefGoogle Scholar
  9. Boyle JA, Chen H, Bamburg JR (2001) Sperm incorporation in Xenopus laevis: characterisation of morphological events and the role of microfilaments. Zygote 9(2):167–181PubMedCrossRefGoogle Scholar
  10. Brawley SH (1987) A sodium-dependent, fast block to polyspermy occurs in eggs of fucoid algae. Dev Biol 124(2):390–397PubMedCrossRefGoogle Scholar
  11. Brawley SH (1991) The fast block against polyspermy in fucoid algae is an electrical block. Dev Biol 144(1):94–106PubMedCrossRefGoogle Scholar
  12. Brawley SH (1992) Fertilization in natural populations of the dioecious brown alga Fucus ceranoides and the importance of the polyspermy block. Mar Biol 113:145–157CrossRefGoogle Scholar
  13. 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(2):177–196PubMedCrossRefGoogle Scholar
  14. Brownlee C, Dale B (1990) Temporal and spatial correlation of fertilization current, calcium waves and cytoplasmic contraction in eggs of Ciona intestinalis. Proc R Soc Lond B Biol Sci 239(1296):321–328PubMedCrossRefGoogle Scholar
  15. Burnett LA, Sugiyama H, Bieber AL, Chandler DE (2011) Egg jelly proteins stimulate directed motility in Xenopus laevis sperm. Mol Reprod Dev 78(6):450–462PubMedCrossRefGoogle Scholar
  16. Busa WB, Nuccitelli R (1985) An elevated free cytosolic Ca2+ wave follows fertilization in eggs of the frog, Xenopus laevis. J Cell Biol 100(4):1325–1329PubMedCrossRefGoogle Scholar
  17. Campanella C, Caputo M, Vaccaro MC, De Marco N, Tretola L, Romano M, Prisco M, Camardella L, Flagiello A, Carotenuto R, Limatola E, Polzonetti-Magni A, Infante V (2011) Lipovitellin constitutes the protein backbone of glycoproteins involved in sperm-egg interaction in the amphibian Discoglossus pictus. Mol Reprod Dev 78(3):161–171PubMedCrossRefGoogle Scholar
  18. Carré D, Sardet C (1984) Fertilization and early development in Beroe ovata. Dev Biol 105(1):188–195PubMedCrossRefGoogle Scholar
  19. Carré D, Rouviere C, Sardet C (1991) In vitro fertilization in ctenophores: sperm entry, mitosis, and the establishment of bilateral symmetry in Beroe ovata. Dev Biol 147(2):381–391PubMedCrossRefGoogle Scholar
  20. Carroll DJ, Ramarao CS, Mehlmann LM, Roche S, Terasaki M, Jaffe LA (1997) Calcium release at fertilization in starfish eggs is mediated by phospholipase Cgamma. J Cell Biol 138(6):1303–1311PubMedPubMedCentralCrossRefGoogle Scholar
  21. Chambers EL, de Armendi J (1979) Membrane potential, action potential and activation potential of eggs of the sea urchin, Lytechinus variegatus. Exp Cell Res 122(1):203–218PubMedCrossRefGoogle Scholar
  22. 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(2):304–318PubMedCrossRefGoogle Scholar
  23. Correa LM, Cho C, Myles DG, Primakoff P (2000) A role for a TIMP-3-sensitive, Zn(2+)-dependent metalloprotease in mammalian gamete membrane fusion. Dev Biol 225(1):124–134PubMedCrossRefGoogle Scholar
  24. Coux G, Cabada MO (2006) Characterization of Bufo arenarum oocyte plasma membrane proteins that interact with sperm. Biochem Biophys Res Commun 343(1):326–333PubMedCrossRefGoogle Scholar
  25. 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 (PLCzeta) in pufferfish. Mol Reprod Dev 78(1):48–56PubMedCrossRefGoogle Scholar
  26. Cross NL, Elinson RP (1980) A fast block to polyspermy in frogs mediated by changes in the membrane potential. Dev Biol 75(1):187–198PubMedCrossRefGoogle Scholar
  27. Dale B (1988) Primary and secondary messengers in the activation of ascidian eggs. Exp Cell Res 177(1):205–211PubMedCrossRefGoogle Scholar
  28. Dale B, de Santis A, Ortolani G (1983) Electrical response to fertilization in ascidian oocytes. Dev Biol 99(1):188–193PubMedCrossRefGoogle Scholar
  29. David C, Halliwell J, Whitaker M (1988) Some properties of the membrane currents underlying the fertilization potential in sea urchin eggs. J Physiol 402:139–154PubMedPubMedCentralCrossRefGoogle Scholar
  30. Deguchi R (2007) Fertilization causes a single Ca2+ increase that fully depends on Ca2+ influx in oocytes of limpets (Phylum Mollusca, Class Gastropoda). Dev Biol 304(2):652–663PubMedCrossRefGoogle Scholar
  31. Deguchi R, Osanai K, Morisawa M (1996) Extracellular Ca2+ entry and Ca2+ release from inositol 1,4,5-trisphosphate-sensitive stores function at fertilization in oocytes of the marine bivalve Mytilus edulis. Development 122(11):3651–3660PubMedGoogle Scholar
  32. Deguchi R, Kondoh E, Itoh J (2005) Spatiotemporal characteristics and mechanisms of intracellular Ca(2+) increases at fertilization in eggs of jellyfish (Phylum Cnidaria, Class Hydrozoa). Dev Biol 279(2):291–307PubMedCrossRefGoogle Scholar
  33. Dufresne-Dube L, Dube F, Guerrier P, Couillard P (1983) Absence of a complete block to polyspermy after fertilization of Mytilus galloprovincialis (mollusca, pelecypoda) oocytes. Dev Biol 97(1):27–33PubMedCrossRefGoogle Scholar
  34. Dumollard R, Carroll J, Dupont G, Sardet C (2002) Calcium wave pacemakers in eggs. J Cell Sci 115(Pt 18):3557–3564PubMedCrossRefGoogle Scholar
  35. Dumollard R, Marangos P, Fitzharris G, Swann K, Duchen M, Carroll J (2004) Sperm-triggered [Ca2+] oscillations and Ca2+ homeostasis in the mouse egg have an absolute requirement for mitochondrial ATP production. Development 131(13):3057–3067PubMedCrossRefGoogle Scholar
  36. Ebchuqin E, Yokota N, Yamada L, Yasuoka Y, Akasaka M, Arakawa M, Deguchi R, Mori T, Sawada H (2014) Evidence for participation of GCS1 in fertilization of the starlet sea anemone Nematostella vectensis: implication of a common mechanism of sperm-egg fusion in plants and animals. Biochem Biophys Res Commun 451(4):522–528PubMedCrossRefGoogle Scholar
  37. Eckberg WR, Anderson WA (1985) Blocks to polyspermy in Chaetopterus. J Exp Zool 233(2):253–260PubMedCrossRefGoogle Scholar
  38. Eckberg WR, Miller AL (1995) Propagated and nonpropagated calcium transients during egg activation in the annelid, Chaetopterus. Dev Biol 172(2):654–664PubMedCrossRefGoogle Scholar
  39. Elinson RP (1973) Fertilization of frog body cavity eggs enhanced by treatments affecting the vitelline coat. J Exp Zool 183(3):291–301CrossRefGoogle Scholar
  40. Elinson RP (1986) Fertilization in amphibians: the ancestry of the block to polyspermy. Int Rev Cytol 101:59–100PubMedCrossRefGoogle Scholar
  41. Finkel T, Wolf DP (1980) Membrane potential, pH and the activation of surf clam oocytes. Gamete Res 3(3):299–304CrossRefGoogle Scholar
  42. Fontanilla RA, Nuccitelli R (1998) Characterization of the sperm-induced calcium wave in Xenopus eggs using confocal microscopy. Biophys J 75(4):2079–2087PubMedPubMedCentralCrossRefGoogle Scholar
  43. Gatenby JB, Hill JP (1924) On an ovum of Ornithorhynchus exhibiting polar bodies and polyspermy. J Cell Sci s2-68(270):229–238Google Scholar
  44. Gianaroli L, Tosti E, Magli C, Iaccarino M, Ferraretti AP, Dale B (1994) Fertilization current in the human oocyte. Mol Reprod Dev 38(2):209–214PubMedCrossRefGoogle Scholar
  45. Ginzburg AS (1972) Fertilization in fishes and the problem of polyspermy. Israel Program for Scientific Translations, Jerusalem (Translated from the Russian ed., 1968)Google Scholar
  46. Glahn D, Nuccitelli R (2003) Voltage-clamp study of the activation currents and fast block to polyspermy in the egg of Xenopus laevis. Develop Growth Differ 45(2):187–197CrossRefGoogle Scholar
  47. Goudeau H, Goudeau M (1989) A long-lasting electrically mediated block, due to the egg membrane hyperpolarization at fertilization, ensures physiological monospermy in eggs of the crab Maia squinado. Dev Biol 133(2):348–360PubMedCrossRefGoogle Scholar
  48. Goudeau M, Goudeau H (1993a) In the egg of the ascidian Phallusia mammillata, removal of external Ca2+ modifies the fertilization potential, induces polyspermy, and blocks the resumption of meiosis. Dev Biol 160(1):165–177PubMedCrossRefGoogle Scholar
  49. Goudeau M, Goudeau H (1993b) Successive electrical responses to insemination and concurrent sperm entries in the polyspermic egg of the ctenophore Beroe ovata. Dev Biol 156(2):537–551PubMedCrossRefGoogle Scholar
  50. Goudeau H, Goudeau M, Guibourt N (1992) The fertilization potential and associated membrane potential oscillations during the resumption of meiosis in the egg of the ascidian Phallusia mammillata. Dev Biol 153(2):227–241PubMedCrossRefGoogle Scholar
  51. Goudeau H, Depresle Y, Rosa A, Goudeau M (1994) Evidence by a voltage clamp study of an electrically mediated block to polyspermy in the egg of the ascidian Phallusia mammillata. Dev Biol 166(2):489–501PubMedCrossRefGoogle Scholar
  52. Gould M, Stephano JL (1987) Electrical responses of eggs to acrosomal protein similar to those induced by sperm. Science 235(4796):1654–1656PubMedCrossRefGoogle Scholar
  53. Gould MC, Stephano JL (2003) Polyspermy prevention in marine invertebrates. Microsc Res Tech 61(4):379–388PubMedCrossRefGoogle Scholar
  54. Gould-Somero M (1981) Localized gating of egg Na+ channels by sperm. Nature 291:254–256CrossRefGoogle Scholar
  55. Gould-Somero M, Jaffe LA, Holland LZ (1979) Electrically mediated fast polyspermy block in eggs of the marine worm, Urechis caupo. J Cell Biol 82(2):426–440PubMedCrossRefGoogle Scholar
  56. Grandin N, Charbonneau M (1991) Intracellular pH and intracellular free calcium responses to protein kinase C activators and inhibitors in Xenopus eggs. Development 112(2):461–470PubMedGoogle Scholar
  57. Grey RD, Bastiani MJ, Webb DJ, Schertel ER (1982) An electrical block is required to prevent polyspermy in eggs fertilized by natural mating of Xenopus laevis. Dev Biol 89(2):475–484PubMedCrossRefGoogle Scholar
  58. 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(2):797–808PubMedCrossRefGoogle Scholar
  59. 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(2):266–276PubMedCrossRefGoogle Scholar
  60. Hart NH (1990) Fertilization in teleost fishes: mechanisms of sperm-egg interactions. Int Rev Cytol 121:1–66PubMedCrossRefGoogle Scholar
  61. Hedrick JL (2008) Anuran and pig egg zona pellucida glycoproteins in fertilization and early development. Int J Dev Biol 52(5-6):683–701PubMedCrossRefGoogle Scholar
  62. Heifetz Y, Yu J, Wolfner MF (2001) Ovulation triggers activation of Drosophila oocytes. Dev Biol 234(2):416–424PubMedCrossRefGoogle Scholar
  63. Hughes RL, Hall LS (1998) Early development and embryology of the platypus. Philos Trans R Soc Lond Ser B Biol Sci 353(1372):1101–1114CrossRefGoogle Scholar
  64. Igusa Y, Miyazaki S (1986) Periodic increase of cytoplasmic free calcium in fertilized hamster eggs measured with calcium-sensitive electrodes. J Physiol 377:193–205PubMedPubMedCentralCrossRefGoogle Scholar
  65. Igusa Y, Miyazaki S, Yamashita N (1983) Periodic hyperpolarizing responses in hamster and mouse eggs fertilized with mouse sperm. J Physiol 340:633–647PubMedPubMedCentralCrossRefGoogle Scholar
  66. Iwamatsu T (2000) Fertilization in fishes. In: Tarín JJ, Cano A (eds) Fertilization in protozoa and metazoan animal. Springer, Berlin, pp 89–146CrossRefGoogle Scholar
  67. Iwamatsu T, Ohta I (1974) Cleavage initiating activities of sperm fractions injected into the egg of the medaka, Oryzias latipes. J Exp Zool 187(1):3–15PubMedCrossRefGoogle Scholar
  68. Iwao Y (1985) The membrane potential changes of amphibian eggs during species- and cross-fertilization. Dev Biol 111(1):26–34CrossRefGoogle Scholar
  69. Iwao Y (1987) The spike component of the fertilization potential in the toad, Bufo japonicus: changes during meiotic maturation and absence during cross-fertilization. Dev Biol 123(2):559–565PubMedCrossRefGoogle Scholar
  70. Iwao Y (1989) An electrically mediated block to polyspermy in the primitive urodele Hynobius nebulosus and phylogenetic comparison with other amphibians. Dev Biol 134(2):438–445PubMedCrossRefGoogle Scholar
  71. Iwao Y (2000a) Fertilization in amphibians. In: Tarín JJ, Cano A (eds) Fertilization in protozoa and metazoan animal. Springer, Berlin, pp 147–191CrossRefGoogle Scholar
  72. Iwao Y (2000b) Mechanisms of egg activation and polyspermy block in amphibians and comparative aspects with fertilization in other vertebrates. Zool Sci 17(6):699–709CrossRefGoogle Scholar
  73. Iwao Y (2012) Egg activation in physiological polyspermy. Reproduction 144(1):11–22PubMedCrossRefGoogle Scholar
  74. Iwao Y (2014) Chapter 15: Egg activation in polyspermy: its molecular mechanisms and evolution in vertebrates. In: Sawada H, Inoue N, Iwano M (eds) Sexual reproduction in animals and plants. Springer Open, pp 171–180CrossRefGoogle Scholar
  75. Iwao Y, Elinson RP (1990) Control of sperm nuclear behavior in physiologically polyspermic newt eggs: possible involvement of MPF. Dev Biol 142(2):301–312PubMedCrossRefGoogle Scholar
  76. Iwao Y, Fujimura T (1996) Activation of Xenopus eggs by RGD-containing peptides accompanied by intracellular Ca2+ release. Dev Biol 177(2):558–567CrossRefPubMedGoogle Scholar
  77. Iwao Y, Jaffe LA (1989) Evidence that the voltage-dependent component in the fertilization process is contributed by the sperm. Dev Biol 134(2):446–451CrossRefPubMedGoogle Scholar
  78. Iwao Y, Yamasaki H, Katagiri C (1985) Experiments pertaining to the suppression of accessory sperm in fertilized newt eggs. Develop Growth Differ 27(3):323–331CrossRefGoogle Scholar
  79. Iwao Y, Miki A, Kobayashi M, Onitake K (1994) Activation of Xenopus eggs by an extract of Cynops sperm. Develop Growth Differ 36(5):469–479CrossRefGoogle Scholar
  80. Iwao Y, Shiga K, Shiroshita A, Yoshikawa T, Sakiie M, Ueno T, Ueno S, Ijiri TW, Sato K (2014) The need of MMP-2 on the sperm surface for Xenopus fertilization: its role in a fast electrical block to polyspermy. Mech Dev 134:80–95CrossRefPubMedGoogle Scholar
  81. Jaffe LA (1976) Fast block to polyspermy in sea urchin eggs is electrically mediated. Nature 261(5555):68–71PubMedCrossRefGoogle Scholar
  82. Jaffe LA (1983a) Fertilization potential from eggs of the marine worms, Chaetopterus and Saccoglossus. In: Moody WJ, Grinnell AD (eds) The physiology of excitable cells. Alan R Liss, New York, pp 211–218Google Scholar
  83. Jaffe LF (1983b) Sources of calcium in egg activation: a review and hypothesis. Dev Biol 99(2):265–276PubMedCrossRefGoogle Scholar
  84. Jaffe LA, Gould M (1985) Polyspermy-preventing mechanisms. In: Metz CB, Monroy A (eds) Biology of fertilization, vol 3. Academic, New York, pp 223–250CrossRefGoogle Scholar
  85. Jaffe LA, Schlichter LC (1985) Fertilization-induced ionic conductances in eggs of the frog, Rana pipiens. J Physiol 358:299–319PubMedPubMedCentralCrossRefGoogle Scholar
  86. Jaffe LA, Gould-Somero M, Holland L (1979) Ionic mechanism of the fertilization potential of the marine worm, Urechis caupo (Echiura). J Gen Physiol 73(4):469–492PubMedCrossRefGoogle Scholar
  87. Jaffe LA, Gould-Somero M, Holland LZ (1982) Studies of the mechanism of the electrical polyspermy block using voltage clamp during cross-species fertilization. J Cell Biol 92(3):616–621PubMedCrossRefGoogle Scholar
  88. Jaffe LA, Cross NL, Picheral B (1983a) Studies of the voltage-dependent polyspermy block using cross-species fertilization of amphibians. Dev Biol 98(2):319–326PubMedCrossRefGoogle Scholar
  89. Jaffe LA, Sharp AP, Wolf DP (1983b) Absence of an electrical polyspermy block in the mouse. Dev Biol 96(2):317–323PubMedCrossRefGoogle Scholar
  90. Jaffe LA, Kado RT, Muncy L (1985) Propagating potassium and chloride conductances during activation and fertilization of the egg of the frog, Rana pipiens. J Physiol 368:227–242PubMedPubMedCentralCrossRefGoogle Scholar
  91. Jaffe LA, Giusti AF, Carroll DJ, Foltz KR (2001) Ca2+ signalling during fertilization of echinoderm eggs. Semin Cell Dev Biol 12(1):45–51PubMedCrossRefGoogle Scholar
  92. Kaneuchi T, Sartain CV, Takeo S, Horner VL, Buehner NA, Aigaki T, Wolfner MF (2014) Calcium waves occur as Drosophila oocytes activate. Proc Natl Acad Sci U S A 112(3):791–796CrossRefGoogle Scholar
  93. 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(10):787–815PubMedCrossRefGoogle Scholar
  94. Kashir J, Nomikos M, Lai FA, Swann K (2014) Sperm-induced Ca2+ release during egg activation in mammals. Biochem Biophys Res Commun 450(3):1204–1211PubMedCrossRefGoogle Scholar
  95. Katagiri C (1974) A high frequency of fertilization in premature and mature coelomic toad eggs after enzymic removal removal removal of vitelline membrane. J Embryol Exp Morphol 31(3):573–587PubMedGoogle Scholar
  96. Kato KH, Takemoto K, Kato E, Miyazaki K, Kobayashi H, Ikegami S (1998) Inhibition of sea urchin fertilization by jaspisin, a specific inhibitor of matrix metalloendoproteinase. Develop Growth Differ 40(2):221–230CrossRefGoogle Scholar
  97. Kline D (1988) Calcium-dependent events at fertilization of the frog egg: injection of a calcium buffer blocks ion channel opening, exocytosis, and formation of pronuclei. Dev Biol 126(2):346–361PubMedCrossRefGoogle Scholar
  98. 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(25):17624–17630PubMedGoogle Scholar
  99. Kline D, Nuccitelli R (1985) The wave of activation current in the Xenopus egg. Dev Biol 111(2):471–487PubMedCrossRefGoogle Scholar
  100. Kline D, Stewart-Savage J (1994) The timing of cortical granule fusion, content dispersal, and endocytosis during fertilization of the hamster egg: an electrophysiological and histochemical study. Dev Biol 162(1):277–287PubMedCrossRefGoogle Scholar
  101. Kline D, Jaffe LA, Tucker RP (1985) Fertilization potential and polyspermy prevention in the egg of the nemertean, Cerebratulus lacteus. J Exp Zool 236(1):45–52PubMedCrossRefGoogle Scholar
  102. Kline D, Jaffe LA, Kado RT (1986) A calcium-activated sodium conductance contributes to the fertilization potential in the egg of the nemertean worm Cerebratulus lacteus. Dev Biol 117(1):184–193PubMedCrossRefGoogle Scholar
  103. Kobayashi W, Baba Y, Shimozawa T, Yamamoto TS (1994) The fertilization potential provides a fast block to polyspermy in lamprey eggs. Dev Biol 161(2):552–562PubMedCrossRefGoogle Scholar
  104. Kondoh E, Tachibana K, Deguchi R (2006) Intracellular Ca2+ increase induces post-fertilization events via MAP kinase dephosphorylation in eggs of the hydrozoan jellyfish Cladonema pacificum. Dev Biol 293(1):228–241PubMedPubMedCentralCrossRefGoogle Scholar
  105. 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 Czeta. J Biol Chem 280(22):21015–21021PubMedCrossRefGoogle Scholar
  106. Kubo H (2005) Acquisition of fertilizability through oviduct-induced modification of envelope in Xenopus laevis egg. Trends Dev Biol 1:56–63Google Scholar
  107. Kubo H, Kotani M, Yamamoto Y, Hazato T (2008) Involvement of sperm proteases in the binding of sperm to the vitelline envelope in Xenopus laevis. Zool Sci 25(1):80–87PubMedCrossRefGoogle Scholar
  108. Kubo H, Shiga K, Harada Y, Iwao Y (2010) Analysis of a sperm surface molecule that binds to a vitelline envelope component of Xenopus laevis eggs. Mol Reprod Dev 77(8):728–735PubMedCrossRefGoogle Scholar
  109. Kyozuka K, Deguchi R, Mohri T, Miyazaki S (1998) Injection of sperm extract mimics spatiotemporal dynamics of Ca2+ responses and progression of meiosis at fertilization of ascidian oocytes. Development 125(20):4099–4105PubMedGoogle Scholar
  110. La Spina FA, Puga Molina LC, Romarowski A, Vitale AM, Falzone TL, Krapf D, Hirohashi N, Buffone MG (2016) Mouse sperm begin to undergo acrosomal exocytosis in the upper isthmus of the oviduct. Dev Biol 411(2):172–182PubMedPubMedCentralCrossRefGoogle Scholar
  111. Lambert C, Goudeau H, Franchet C, Lambert G, Goudeau M (1997) Ascidian eggs block polyspermy by two independent mechanisms: one at the egg plasma membrane, the other involving the follicle cells. Mol Reprod Dev 48(1):137–143PubMedCrossRefGoogle Scholar
  112. Lansman JB (1983) Voltage-clamp study of the conductance activated at fertilization in the starfish egg. J Physiol 345:353–372PubMedPubMedCentralCrossRefGoogle Scholar
  113. 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(1):233–241PubMedGoogle Scholar
  114. Leclerc C, Guerrier P, Moreau M (2000) Role of dihydropyridine-sensitive calcium channels in meiosis and fertilization in the bivalve molluscs Ruditapes philippinarum and Crassostrea gigas. Biol Cell 92(3-4):285–299PubMedCrossRefGoogle Scholar
  115. Lindsay L, Clark WH (1994) Signal transduction during shrimp oocyte activation by extracellular Mg2+: roles of inositol 1,4,5-trisphosphate, tyrosine kinases and G-proteins. Development 120:3463–3472Google Scholar
  116. Lindsay LL, Hertzler PL, Clark WH Jr (1992) Extracellular Mg2+ induces an intracellular Ca2+ wave during oocyte activation in the marine shrimp Sicyonia ingentis. Dev Biol 152(1):94–102PubMedCrossRefGoogle Scholar
  117. Longo FJ (1973) An ultrastructural analysis of polyspermy in the surf clam, Spisula solidissima. J Exp Zool 183(2):153–180PubMedCrossRefGoogle Scholar
  118. Lynn JW, Chambers EL (1984) Voltage clamp studies of fertilization in sea urchin eggs. I. Effect of clamped membrane potential on sperm entry, activation, and development. Dev Biol 102(1):98–109PubMedCrossRefGoogle Scholar
  119. Lynn JW, McCulloh DH, Chambers EL (1988) Voltage clamp studies of fertilization in sea urchin eggs. II. Current patterns in relation to sperm entry, nonentry, and activation. Dev Biol 128(2):305–323PubMedCrossRefGoogle Scholar
  120. Mahbub Hasan AK, Sato K, Sakakibara K, Ou Z, Iwasaki T, Ueda Y, Fukami Y (2005) Uroplakin III, a novel Src substrate in Xenopus egg rafts, is a target for sperm protease essential for fertilization. Dev Biol 286(2):483–492CrossRefPubMedGoogle Scholar
  121. Mahbub Hasan AK, Ou Z, Sakakibara K, Hirahara S, Iwasaki T, Sato K, Fukami Y (2007) Characterization of Xenopus egg membrane microdomains containing uroplakin Ib/III complex: roles of their molecular interactions for subcellular localization and signal transduction. Genes Cells 12(2):251–267CrossRefPubMedGoogle Scholar
  122. Mahbub Hasan AK, Hashimoto A, Maekawa Y, Matsumoto T, Kushima S, Ijiri TW, Fukami Y, Sato K (2014) The egg membrane microdomain-associated uroplakin III-Src system becomes functional during oocyte maturation and is required for bidirectional gamete signaling at fertilization in Xenopus laevis. Development 141(8):1705–1714CrossRefPubMedGoogle Scholar
  123. 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(2):137–175PubMedCrossRefGoogle Scholar
  124. McCulloh DH, Ivonnet PI, Landowne D, Chambers EL (2000) Calcium influx mediates the voltage-dependence of sperm entry into sea urchin eggs. Dev Biol 223(2):449–462PubMedCrossRefGoogle Scholar
  125. McDougall A, Levasseur M, O’Sullivan AJ, Jones KT (2000a) Cell cycle-dependent repetitive Ca(2+)waves induced by a cytosolic sperm extract in mature ascidian eggs mimic those observed at fertilization. J Cell Sci 113(Pt 19):3453–3462PubMedGoogle Scholar
  126. McDougall A, Shearer J, Whitaker M (2000b) The initiation and propagation of the fertilization wave in sea urchin eggs. Biol Cell 92(3-4):205–214PubMedCrossRefGoogle Scholar
  127. Miyazaki S (2006) Thirty years of calcium signals at fertilization. Semin Cell Dev Biol 17(2):233–243PubMedCrossRefGoogle Scholar
  128. Miyazaki S, Hirai S (1979) Fast polyspermy block and activation potential. Correlated changes during oocyte maturation of a starfish. Dev Biol 70(2):327–340PubMedCrossRefGoogle Scholar
  129. Miyazaki S, Igusa Y (1981) Fertilization potential in golden hamster eggs consists of recurring hyperpolarizations. Nature 290(5808):702–704PubMedCrossRefGoogle Scholar
  130. 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(3):931–935PubMedPubMedCentralCrossRefGoogle Scholar
  131. 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(5067):251–255PubMedCrossRefGoogle Scholar
  132. Mizote A, Okamoto S, Iwao Y (1999) Activation of Xenopus eggs by proteases: possible involvement of a sperm protease in fertilization. Dev Biol 208(1):79–92CrossRefPubMedGoogle Scholar
  133. 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. Mol Reprod Dev 76(12):1200–1207PubMedCrossRefGoogle Scholar
  134. Mizushima S, Hiyama G, Shiba K, Inaba K, Dohra H, Ono T, Shimada K, Sasanami T (2014) The birth of quail chicks after intracytoplasmic sperm injection. Development 141(19):3799–3806PubMedCrossRefGoogle Scholar
  135. Mohri T, Shirakawa H, Oda S, Sato MS, Mikoshiba K, Miyazaki S (2001) Analysis of Mn(2+)/Ca(2+) influx and release during Ca(2+) oscillations in mouse eggs injected with sperm extract. Cell Calcium 29(5):311–325PubMedCrossRefGoogle Scholar
  136. Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T (2006) GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization. Nat Cell Biol 8(1):64–71PubMedCrossRefGoogle Scholar
  137. Muro Y, Hasuwa H, Isotani A, Miyata H, Yamagata K, Ikawa M, Yanagimachi R, Okabe M (2016) Behavior of mouse spermatozoa in the female reproductive tract from soon after mating to the beginning of fertilization. Biol Reprod 94(4):80,1–80,7CrossRefGoogle Scholar
  138. Mutua J, Jinno Y, Sakata S, Okochi Y, Ueno S, Tsutsui H, Kawai T, Iwao Y, Okamura Y (2014) Functional diversity of voltage-sensing phosphatases in two urodele amphibians. Physiol Rep 2(7):1–13CrossRefGoogle Scholar
  139. Nagai K, Ishida T, Hashimoto T, Harada Y, Ueno S, Ueda Y, Kubo H, Iwao Y (2009) The sperm-surface glycoprotein, SGP, is necessary for fertilization in the frog, Xenopus laevis. Develop Growth Differ 51(5):499–510CrossRefGoogle Scholar
  140. Nakanishi A, Utsumi K, Iritani A (1990) Early nuclear events of in vitro fertilization in the domestic fowl (Gallus domesticus). Mol Reprod Dev 26(3):217–221PubMedCrossRefGoogle Scholar
  141. Nakano T, Kyozuka K (2014) Soluble sperm extract specifically recapitulates the initial phase of the Ca2+ response in the fertilized oocyte of P. occelata following a G-protein/PLCbeta signaling pathway. Zygote:1–15Google Scholar
  142. Nakano T, Kyozuka K, Deguchi R (2008) Novel two-step Ca2+ increase and its mechanisms and functions at fertilization in oocytes of the annelidan worm Pseudopotamilla occelata. Develop Growth Differ 50(5):365–379CrossRefGoogle Scholar
  143. Nixon VL, McDougall A, Jones KT (2000) Ca2+ oscillations and the cell cycle at fertilisation of mammalian and ascidian eggs. Biol Cell 92(3-4):187–196PubMedCrossRefGoogle Scholar
  144. Nuccitelli R (1980a) The electrical changes accompanying fertilization and cortical vesicle secretion in the medaka egg. Dev Biol 76(2):483–498PubMedCrossRefGoogle Scholar
  145. Nuccitelli R (1980b) The fertilization potential is not necessary for the block to polyspermy or the activation of development in the medaka egg. Dev Biol 76(2):499–504PubMedCrossRefGoogle Scholar
  146. Nuccitelli R (1987) The wave of activation current in the egg of the medaka fish. Dev Biol 122(2):522–534PubMedCrossRefGoogle Scholar
  147. Nuccitelli R, Kline D, Busa WB, Talevi R, Campanella C (1988) A highly localized activation current yet widespread intracellular calcium increase in the egg of the frog, Discoglossus pictus. Dev Biol 130(1):120–132PubMedCrossRefGoogle Scholar
  148. 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(1):200–212CrossRefPubMedGoogle Scholar
  149. Olson JH, Xiang X, Ziegert T, Kittelson A, Rawls A, Bieber AL, Chandler DE (2001) Allurin, a 21-kDa sperm chemoattractant from Xenopus egg jelly, is related to mammalian sperm-binding proteins. Proc Natl Acad Sci U S A 98(20):11205–11210PubMedPubMedCentralCrossRefGoogle Scholar
  150. Pearson GA, Brawley H (1996) Reproductive ecology of Fucus distichus (Phaeophyceae): an intertidal alga with successful external fertilization. Mar Ecol Progr Ser 143:211–223CrossRefGoogle Scholar
  151. Perry MM (1987) Nuclear events from fertilisation to the early cleavage stages in the domestic fowl (Gallus domesticus). J Anat 150:99–109PubMedPubMedCentralGoogle Scholar
  152. Ratzan WJ, Evsikov AV, Okamura Y, Jaffe LA (2011) Voltage sensitive phosphoinositide phosphatases of Xenopus: their tissue distribution and voltage dependence. J Cell Physiol 226(11):2740–2746PubMedPubMedCentralCrossRefGoogle Scholar
  153. Reinhart D, Ridgway J, Chandler DE (1998) Xenopus laevis fertilisation: analysis of sperm motility in egg jelly using video light microscopy. Zygote 6(2):173–182PubMedCrossRefGoogle Scholar
  154. Roberts S, Brownlee C (1995) Calcium influx, fertilisation potential and egg activation in Fucus serratus. Zygote 3(3):191–197PubMedCrossRefGoogle Scholar
  155. Rouvière C, Houliston E, Carré D, Chang P, Sardet C (1994) Characteristics of pronuclear migration in Beroe ovata. Cell Motil Cytoskeleton 29(4):301–311PubMedCrossRefGoogle Scholar
  156. Runft LL, Jaffe LA (2000) Sperm extract injection into ascidian eggs signals Ca(2+) release by the same pathway as fertilization. Development 127(15):3227–3236PubMedGoogle Scholar
  157. Runft LL, Jaffe LA, Mehlmann LM (2002) Egg activation at fertilization: where it all begins. Dev Biol 245(2):237–254CrossRefPubMedGoogle Scholar
  158. Sakakibara K, Sato K, Yoshino K, Oshiro N, Hirahara S, Mahbub Hasan AK, Iwasaki T, Ueda Y, Iwao Y, Yonezawa K, Fukami Y (2005) Molecular identification and characterization of Xenopus egg uroplakin III, an egg raft-associated transmembrane protein that is tyrosine-phosphorylated upon fertilization. J Biol Chem 280(15):15029–15037CrossRefPubMedGoogle Scholar
  159. Sato M, Tanaka-Sato H (2002) Fertilization, syngamy, and early embryonic development in the cricket Gryllus bimaculatus (De Geer). J Morphol 254(3):266–271PubMedCrossRefGoogle Scholar
  160. Sato K, Iwao Y, Fujimura T, Tamaki I, Ogawa K, Iwasaki T, Tokmakov AA, Hatano O, Fukami Y (1999) Evidence for the involvement of a Src-related tyrosine kinase in Xenopus egg activation. Dev Biol 209(2):308–320CrossRefPubMedGoogle Scholar
  161. Sato K, Tokmakov AA, He CL, Kurokawa M, Iwasaki T, Shirouzu M, Fissore RA, Yokoyama S, Fukami Y (2003) Reconstitution of Src-dependent phospholipase Cγ phosphorylation and transient calcium release by using membrane rafts and cell-free extracts from Xenopus eggs. J Biol Chem 278(40):38413–38420CrossRefPubMedGoogle Scholar
  162. Satouh Y, Nozawa K, Ikawa M (2015) Sperm postacrosomal WW domain-binding protein is not required for mouse egg activation. Biol Reprod 93(4):94, 1–7PubMedCrossRefGoogle Scholar
  163. 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(15):3533–3544PubMedPubMedCentralGoogle Scholar
  164. Schatten H, Chakrabarti A (2000) Fertilization in invertebrates. In: Tarín JJ, Cano A (eds) Fertilization in protozoa and metazoan animal. Springer, Berlin, pp 27–87CrossRefGoogle Scholar
  165. Schlichter LC, Elinson RP (1981) Electrical responses of immature and mature Rana pipiens oocytes to sperm and other activating stimuli. Dev Biol 83(1):33–41PubMedCrossRefGoogle Scholar
  166. Serrao EA, Brawley SH, Hedman J, Kautsky L, Samuelsson G (1999) Reproductive success of Fucus vesiculosus (Phaeophyceae) in the Baltic sea. J Phycol 35:254–269CrossRefGoogle Scholar
  167. Shilling FM, Kratzschmar 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(2):155–164CrossRefPubMedGoogle Scholar
  168. Shilling FM, Magie CR, Nuccitelli R (1998) Voltage-dependent activation of frog eggs by a sperm surface disintegrin peptide. Dev Biol 202(1):113–124CrossRefPubMedGoogle Scholar
  169. Snook RR, Hosken DJ, Karr TL (2011) The biology and evolution of polyspermy: insights from cellular and functional studies of sperm and centrosomal behavior in the fertilized egg. Reproduction 142(6):779–792PubMedCrossRefGoogle Scholar
  170. Speksnijder JE, Corson DW, Sardet C, Jaffe LF (1989) Free calcium pulses following fertilization in the ascidian egg. Dev Biol 135(1):182–190PubMedCrossRefGoogle Scholar
  171. Stephano JL, Gould MC (1997) The intracellular calcium increase at fertilization in Urechis caupo oocytes: activation without waves. Dev Biol 191(1):53–68PubMedCrossRefGoogle Scholar
  172. Stewart-Savage J, Grey RD (1984) Fertilization of investment-free Xenopus eggs. Exp Cell Res 154(2):639–642PubMedCrossRefGoogle Scholar
  173. Stewart-Savage J, Grey RD (1987) Loss of functional sperm entry into Xenopus eggs after activation correlates with a reduction in surface adhesivity. Dev Biol 120(2):434–446PubMedCrossRefGoogle Scholar
  174. Stith BJ (2015) Phospholipase C and D regulation of Src, calcium release and membrane fusion during Xenopus laevis development. Dev Biol 401(2):188–205PubMedPubMedCentralCrossRefGoogle Scholar
  175. Stricker SA (1995) Time-lapse confocal imaging of calcium dynamics in starfish embryos. Dev Biol 170(2):496–518PubMedCrossRefGoogle Scholar
  176. Stricker SA (1996) Repetitive calcium waves induced by fertilization in the nemertean worm Cerebratulus lacteus. Dev Biol 176(2):243–263PubMedCrossRefGoogle Scholar
  177. Stricker SA (1997) Intracellular injections of a soluble sperm factor trigger calcium oscillations and meiotic maturation in unfertilized oocytes of a marine worm. Dev Biol 186(2):185–201PubMedCrossRefGoogle Scholar
  178. Stricker SA (1999) Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev Biol 211(2):157–176PubMedCrossRefGoogle Scholar
  179. Stricker SA, Silva R, Smythe T (1998) Calcium and endoplasmic reticulum dynamics during oocyte maturation and fertilization in the marine worm Cerebratulus lacteus. Dev Biol 203(2):305–322PubMedCrossRefGoogle Scholar
  180. Stricker SA, Carroll DJ, Tsui WL (2010) Roles of Src family kinase signaling during fertilization and the first cell cycle in the marine protostome worm Cerebratulus. Int J Dev Biol 54(5):787–793CrossRefPubMedGoogle Scholar
  181. Swann K, Lai FA (2013) PLCzeta and the initiation of Ca(2+) oscillations in fertilizing mammalian eggs. Cell Calcium 53(1):55–62PubMedCrossRefGoogle Scholar
  182. Talevi R (1989) Polyspermic eggs in the anuran Discoglossus pictus develop normally. Development 105:343–349Google Scholar
  183. Talevi R, Campanella C (1988) Fertilization in Discoglossus pictus (Anura). I. Sperm-egg interactions in distinct regions of the dimple and occurrence of a late stage of sperm penetration. Dev Biol 130(2):524–535PubMedCrossRefGoogle Scholar
  184. Talevi R, Dale B, Campanella C (1985) Fertilization and activation potentials in Discoglossus pictus (Anura) eggs: a delayed response to activation by pricking. Dev Biol 111:316–323CrossRefGoogle Scholar
  185. Tatone C, Carbone MC (2006) Possible involvement of integrin-mediated signalling in oocyte activation: evidence that a cyclic RGD-containing peptide can stimulate protein kinase C and cortical granule exocytosis in mouse oocytes. Reprod Biol Endocrinol 4:48PubMedPubMedCentralCrossRefGoogle Scholar
  186. Togo T, Morisawa M (1997) Aminopeptidase-like protease released from oocytes affects oocyte surfaces and suppresses the acrosome reaction in establishment of polyspermy block in oocytes of the mussel Mytilus edulis. Dev Biol 182(2):219–227PubMedCrossRefGoogle Scholar
  187. Togo T, Osanai K, Morisawa M (1995) Existence of three mechanisms for blocking polyspermy in oocytes of the mussel Mytilus edulis. Biol Bull 189:330–339PubMedCrossRefGoogle Scholar
  188. Tosti E, Boni R, Cuomo A (2002) Fertilization and activation currents in bovine oocytes. Reproduction 124(6):835–846PubMedCrossRefGoogle Scholar
  189. Townley IK, Roux MM, Foltz KR (2006) Signal transduction at fertilization: the Ca2+ release pathway in echinoderms and other invertebrate deuterostomes. Semin Cell Dev Biol 17(2):293–302PubMedCrossRefGoogle Scholar
  190. Ueda Y, Yoshizaki N, Iwao Y (2002) Acrosome reaction in sperm of the frog, Xenopus laevis: its detection and induction by oviductal pars recta secretion. Dev Biol 243(1):55–64PubMedCrossRefGoogle Scholar
  191. Ueda Y, Kubo H, Iwao Y (2003) Characterization of the acrosome reaction-inducing substance in Xenopus (ARISX) secreted from the oviductal pars recta onto the vitelline envelope. Dev Biol 264(1):289–298PubMedCrossRefGoogle Scholar
  192. Ueno T, Ohgami T, Harada Y, Ueno S, Iwao Y (2014) Egg activation in physiologically polyspermic newt eggs: involvement of IP(3) receptor, PLCgamma, and microtubules in calcium wave induction. Int J Dev Biol 58(5):315–323PubMedCrossRefGoogle Scholar
  193. Vacquier VD (2012) The quest for the sea urchin egg receptor for sperm. Biochem Biophys Res Commun 425(3):583–587PubMedCrossRefGoogle Scholar
  194. Waddington D, Gribbin C, Sterling RJ, Sang HM, Perry MM (1998) Chronology of events in the first cell cycle of the polyspermic egg of the domestic fowl (Gallus domesticus). Int J Dev Biol 42(4):625–628PubMedGoogle Scholar
  195. Wakai T, Vanderheyden V, Yoon SY, Cheon B, Zhang N, Parys JB, Fissore RA (2012) Regulation of inositol 1,4,5-trisphosphate receptor function during mouse oocyte maturation. J Cell Physiol 227(2):705–717PubMedPubMedCentralCrossRefGoogle Scholar
  196. Webb SE, Miller AL (2014) Ca(2+) signaling during activation and fertilization in the eggs of teleost fish. Cell Calcium 53(1):24–31CrossRefGoogle Scholar
  197. Webb DJ, Nuccitelli R (1985) Fertilization potential and electrical properties of the Xenopus laevis egg. Dev Biol 107(2):395–406PubMedCrossRefGoogle Scholar
  198. Whitaker M (2006) Calcium at fertilization and in early development. Physiol Rev 86(1):25–88PubMedPubMedCentralCrossRefGoogle Scholar
  199. Whitaker M (2008) Calcium signalling in early embryos. Philos Trans R Soc Lond Ser B Biol Sci 363(1495):1401–1418CrossRefGoogle Scholar
  200. White KL, Passipieri M, Bunch TD, Campbell KD, Pate B (2007) Effects of arginine-glycine-aspartic acid (RGD) containing snake venom peptides on parthenogenetic development and in vitro fertilization of bovine oocytes. Mol Reprod Dev 74(1):88–96CrossRefPubMedGoogle Scholar
  201. Wong JL, Wessel GM (2006) Defending the zygote: search for the ancestral animal block to polyspermy. Curr Top Dev Biol 72:1–151PubMedGoogle Scholar
  202. 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(1):89–99PubMedCrossRefGoogle Scholar
  203. Yanagimachi R (1994) Mammalian fertilization. In: Knobil E, Neil JD (eds) The physiology of reproduction, 2nd edn. Raven Press, Ltd, New York, pp 189–317Google Scholar
  204. Yoshida M, Sensui N, Inoue T, Morisawa M, Mikoshiba K (1998) Role of two series of Ca2+ oscillations in activation of ascidian eggs. Dev Biol 203(1):122–113PubMedCrossRefGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratory of Reproductive Developmental Biology, Division of Earth Sciences, Biology, and ChemistryGraduate School of Sciences and Technology for Innovation, Yamaguchi UniversityYamaguchiJapan

Personalised recommendations