Advertisement

Fertilization in Starfish and Sea Urchin: Roles of Actin

  • Jong Tai Chun
  • Filip Vasilev
  • Nunzia Limatola
  • Luigia Santella
Chapter
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 65)

Abstract

Marine animals relying on “external fertilization” provide advantageous opportunities to study the mechanisms of gamete activation and fusion, as well as the subsequent embryonic development. Owing to the large number of eggs that are easily available and handled, starfish and sea urchins have been chosen as favorable animal models in this line of research for over 150 years. Indeed, much of our knowledge on fertilization came from studies in the echinoderms. Fertilization involves mutual stimulation between eggs and sperm, which leads to morphological, biochemical, and physiological changes on both sides to ensure successful gamete fusion. In this chapter, we review the roles of actin in the fertilization of starfish and sea urchin eggs. As fertilization is essentially an event that takes place on the egg surface, it has been predicted that suboolemmal actin filaments would make significant contributions to sperm entry. A growing body of evidence from starfish and sea urchin eggs suggests that the prompt reorganization of the actin pools around the time of fertilization plays crucial regulatory roles not only in guiding sperm entry but also in modulating intracellular Ca2+ signaling and egg activation.

Notes

Acknowledgment

The authors are grateful to D. Caramiello for maintenance of A. aranciacus and P. lividus and to R. Graziano, F. Iamunno, and G. Lanzotti at the AMOBIO Unit of the Stazione Zoologica Anton Dohrn who prepared samples for scanning electron microscopy. We also acknowledge G. Gragnaniello for the preparation of the figures and C. Caccavale for her graphic design of Fig 3.1.

References

  1. Allbritton NL, Meyer T, Stryer L (1992) Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science 258:1812–1815CrossRefPubMedGoogle Scholar
  2. Behnke O, Forer A, Emmersen J (1971) Actin in sperm tails and meiotic spindles. Nature 234:408–410CrossRefPubMedGoogle Scholar
  3. Bose DD, Thomas DW (2009) The actin cytoskeleton differentially regulates NG115-401L cell ryanodine receptor and inositol 1,4,5-trisphosphate receptor induced calcium signaling pathways. Biochem Biophys Res Commun 379:594–599CrossRefPubMedPubMedCentralGoogle Scholar
  4. Carlier M-F, Pantaloni D, Korn ED (1986) The exchangeability of actin-bound calcium with various divalent cations to high-affinity and low-affinity binding sites on ATP-G-actin. J Biol Chem 261:10778–10784PubMedGoogle Scholar
  5. Carron CP, Longo FJ (1982) Relation of cytoplasmic alkalinization to microvillar elongation and microfilament formation in the sea urchin egg. Dev Biol 89:128–137CrossRefPubMedGoogle Scholar
  6. Chiba K, Kado RT, Jaffe LA (1990) Development of calcium release mechanisms during starfish oocyte maturation. Dev Biol 140:300–306CrossRefPubMedGoogle Scholar
  7. Chiba K, Kontani K, Tadenuma H, Katada T, Hoshi M (1993) Induction of starfish oocyte maturation by the ßɣ subunit of starfish G protein and possible existence of the subsequent effector in cytoplasm. Mol Biol Cell 4:1027–1034CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chun JT, Santella L (2009a) The actin cytoskeleton in meiotic maturation and fertilization of starfish eggs. Biochem Biophys Res Commun 384:141–143CrossRefPubMedGoogle Scholar
  9. Chun JT, Santella L (2009b) Roles of the actin-binding proteins in intracellular Ca2+ signalling. Acta Physiol (Oxf) 195:61–70CrossRefGoogle Scholar
  10. Chun JT, Puppo A, Vasilev F, Gragnaniello G, Garante E, Santella L (2010) The biphasic increase of PIP2 in the fertilized eggs of starfish: new roles in actin polymerization and Ca2+ signaling. PLoS One 5:e14100CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chun JT, Vasilev F, Santella L (2013) Antibody against the actin-binding protein depactin attenuates Ca2+ signaling in starfish eggs. Biochem Biophys Res Commun 441:301–307CrossRefPubMedGoogle Scholar
  12. Chun JT, Limatola N, Vasilev F, Santella L (2014) Early events of fertilization in sea urchin eggs are sensitive to actin-binding organic molecules. Biochem Biophys Res Commun 450:1166–1174CrossRefPubMedGoogle Scholar
  13. Cohen G, Rubinstein S, Gur Y, Breitbart H (2004) Crosstalk between protein kinase A and C regulates phospholipase D and F-actin formation during sperm capacitation. Dev Biol 267:230–241CrossRefPubMedGoogle Scholar
  14. Correa LM, Thomas A, Meyers SA (2007) The macaque sperm actin cytoskeleton reorganizes in response to osmotic stress and contributes to morphological defects and decreased motility. Biol Reprod 77:942–953CrossRefPubMedGoogle Scholar
  15. Dale B, De Santis A (1981) The effect of cytochalasin B and D on the fertilization of sea urchins. Dev Biol 83:232–237CrossRefPubMedGoogle Scholar
  16. Dale B, de Santis A, Hoshi M (1979) Membrane response to 1-methyladenine requires the presence of the nucleus. Nature 282:89–90CrossRefPubMedGoogle Scholar
  17. Dan J (1952) Studies on the acrosome. I. Reaction to egg-water and other stimuli. Biol Bull 103:54–66CrossRefGoogle Scholar
  18. Dan JC, Kitahara A, Kohri T (1954) Studies on the acrosome. II. Acrosome reaction in starfish spermatozoa. Biol Bull 107:203–218CrossRefGoogle Scholar
  19. Dorée M, Kishimoto T (1981) Calcium-mediated transduction of the honnonal message in 1-methyladenine-induced meiosis reinitiation of starfish cocytes. In: Goem J, Peaud-Lendel C (eds) Metabolism and molecular activities of cytokinins. Springer, Berlin, pp 338–348CrossRefGoogle Scholar
  20. Dorée M, Kishimoto T, Le Peuch CJ, Demaille JG, Kanatani H (1981) Calcium-mediated transduction of the hormonal message in meiosis reinitiation of starfish oocytes: modulation following injection of cholera toxin and cAMP-dependent protein kinase. Exp Cell Res 135:237–249CrossRefPubMedGoogle Scholar
  21. Dufossé A (1847) Observations sur le developpement des oursins (Echinus esculentus). Comptes Rendus Hebdomadaires des Seances del Academie des Sciences 24:15–18Google Scholar
  22. Dvoráková K, Moore HD, Sebková N, Palecek J (2005) Cytoskeleton localization in the sperm head prior to fertilization. Reproduction 130:61–69CrossRefPubMedGoogle Scholar
  23. Fol H (1879) Recherches sur la fécondation et le commencement de l’hénogénie chez divers animaux. Mem Soc Phys Hist Nat Genève 26:392–397Google Scholar
  24. Footer MJ, Kerssemakers JW, Theriot JA, Dogterom M (2007) Direct measurement of force generation by actin filament polymerization using an optical trap. Proc Natl Acad Sci U S A 104:2181–2186CrossRefPubMedPubMedCentralGoogle Scholar
  25. Fujimoto T, Miyawaki A, Mikoshiba K (1995) Inositol 1,4,5-trisphosphate receptor-like protein in plasmalemmal caveolae is linked to actin filaments. J Cell Sci 108:7–15PubMedGoogle Scholar
  26. Fukatsu K, Bannai H, Zhang S, Nakamura H, Inoue T, Mikoshiba K (2004) Lateral diffusion of inositol 1,4,5-trisphosphate receptor type 1 is regulated by actin filaments and 4.1N in neuronal dendrites. J Biol Chem 279:48976–48982CrossRefPubMedGoogle Scholar
  27. Gershman LC, Selden LA, Estes JE (1986) High affinity binding of divalent cations to actin monomers is much stronger than previously reported. Biochem Biophys Res Commun 135:607–614CrossRefPubMedGoogle Scholar
  28. Gordon NK, Gordon R (2016) Embryogenesis explained. World Scientific Press, Singapore, p 657CrossRefGoogle Scholar
  29. Hertwig O (1876) Beiträge zur Kenntniss der Bildung, Befruchtung und Theilung des thierischen Eies. Morphol Jahr 1:347–452Google Scholar
  30. Hirai S, Kubota J, Kanatani H (1971) Induction of cytoplasmic maturation by 1-methyladenine in starfish oocytes after removal of the germinal vesicle. Exp Cell Res 68:137–143CrossRefPubMedGoogle Scholar
  31. Hirohashi N, Kamei N, Kubo H, Sawada H, Matsumoto M, Hoshi M (2008) Egg and sperm recognition systems during fertilization. Develop Growth Differ 50(Suppl 1):S221–S238CrossRefGoogle Scholar
  32. Holy J, Schatten G (1991) Spindle pole centrosomes of sea urchin embryos are partially composed of material recruited from maternal stores. Dev Biol 147:343–353CrossRefPubMedGoogle Scholar
  33. Jaffe LF (1993) Classes and mechanisms of calcium waves. Cell Calcium 14:736–745CrossRefPubMedGoogle Scholar
  34. Jaffe LA, Gallo CJ, Lee RH, Ho YK, Jones TL (1993) Oocyte maturation in starfish is mediated by the beta gamma-subunit complex of a G-protein. J Cell Biol 121:775–783CrossRefPubMedGoogle Scholar
  35. Just EE (1939) The biology of the cell surface. P. Blakiston’s Son, Philadelphia, pp 75–103Google Scholar
  36. Kamei N, Glabe CG (2003) The species-specific egg receptor for sea urchin sperm adhesion is EBR1, a novel ADAMTS protein. Genes Dev 17:2502–2507CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kanatani H, Hiramoto Y (1970) Site of action of 1-methyladenine in inducing oocyte maturation in starfish. Exp Cell Res 61:280–284CrossRefPubMedGoogle Scholar
  38. Kanatani H, Shirai H, Nakanishi K, Kurokawa T (1969) Isolation and identification on meiosis inducing substance in starfish Asterias amurensis. Nature 221:273–274CrossRefPubMedGoogle Scholar
  39. Kyozuka K, Chun JT, Puppo A, Gragnaniello G, Garante E, Santella L (2008) Actin cytoskeleton modulates calcium signaling during maturation of starfish oocytes. Dev Biol 320:426–435CrossRefPubMedGoogle Scholar
  40. Kyozuka K, Chun JT, Puppo A, Gragnaniello G, Garante E, Santella L (2009) Guanine nucleotides in the meiotic maturation of starfish oocytes: regulation of the actin cytoskeleton and of Ca2+ signaling. PLoS One 4:e6296CrossRefPubMedPubMedCentralGoogle Scholar
  41. Lange K (1999) Microvillar Ca++ signaling: a new view of an old problem. J Cell Physiol 180:19–34CrossRefPubMedGoogle Scholar
  42. Lénárt P, Bacher CP, Daigle N, Hand AR, Eils R, Terasaki M, Ellenberg J (2005) A contractile nuclear actin network drives chromosome congression in oocytes. Nature 436:812–818CrossRefPubMedGoogle Scholar
  43. Lim D, Kyozuka K, Gragnaniello G, Carafoli E, Santella L (2001) NAADP+ initiates the Ca2+ response during fertilization of starfish oocytes. FASEB J 15:2257–2267CrossRefPubMedGoogle Scholar
  44. Lim D, Lange K, Santella L (2002) Activation of oocytes by latrunculin A. FASEB J 16:1050–1056CrossRefPubMedGoogle Scholar
  45. Lim D, Ercolano E, Kyozuka K, Nusco GA, Moccia F, Lange K, Santella L (2003) The M-phase-promoting factor modulates the sensitivity of the Ca2+ stores to inositol 1,4,5-trisphosphate via the actin cytoskeleton. J Biol Chem 278:42505–42514CrossRefPubMedGoogle Scholar
  46. Limatola N, Chun JT, Kyozuka K, Santella L (2015) Novel Ca2+ increases in the maturing oocytes of starfish during the germinal vesicle breakdown. Cell Calcium 58:500–510CrossRefPubMedGoogle Scholar
  47. Luo L (2002) Actin cytoskeleton regulation in neuronal morphogenesis and structural plasticity. Annu Rev Cell Dev Biol 18:601–635CrossRefPubMedGoogle Scholar
  48. Mah SA, Swanson WJ, Vacquier VD (2005) Positive selection in the carbohydrate recognition domains of sea urchin sperm receptor for egg jelly (suREJ) proteins. Mol Biol Evol 22:533–541CrossRefPubMedGoogle Scholar
  49. Majstoravich S, Zhang J, Nicholson-Dykstra S, Linder S, Friedrich W, Siminovitch KA, Higgs HN (2004) Lymphocyte microvilli are dynamic, actin-dependent structures that do not require Wiskott-Aldrich syndrome protein (WASp) for their morphology. Blood 104:1396–1403CrossRefPubMedGoogle Scholar
  50. Matsumoto M, Kawase O, Islam MS, Naruse M, Watanabe SN, Ishikawa R, Hoshi M (2008) Regulation of the starfish sperm acrosome reaction by cGMP, pH, cAMP and Ca2+. Int J Dev Biol 52:523–526CrossRefPubMedGoogle Scholar
  51. Meijer L, Guerrier P (1984) Maturation and fertilization in starfish oocytes. Int Rev Cytol 86:129–196CrossRefPubMedGoogle Scholar
  52. Miyazaki S (2006) Thirty years of calcium signals at fertilization. Semin Cell Dev Biol 17:233–243CrossRefPubMedGoogle Scholar
  53. Miyazaki SI, Ohmori H, Sasaki S (1975) Action potential and non-linear current-voltage relation in starfish oocytes. J Physiol 246:37–54CrossRefPubMedPubMedCentralGoogle Scholar
  54. Moccia F (2007) Latrunculin A depolarizes starfish oocytes. Comp Biochem Physiol A Mol Integr Physiol 148:845–852CrossRefPubMedGoogle Scholar
  55. Moody WJ, Bosma MM (1985) Hormone-induced loss of surface membrane during maturation of starfish oocytes: differential effects on potassium and calcium channels. Dev Biol 112:396–404CrossRefPubMedGoogle Scholar
  56. Moreau M, Guerrier P, Doree M, Ashley CC (1978) Hormone-induced release of intracellular Ca2+ triggers meiosis in starfish oocytes. Nature 272:251–253CrossRefPubMedGoogle Scholar
  57. Moy GW, Mendoza LM, Schulz JR, Swanson WJ, Glabe CG, Vacquier VD (1996) The sea urchin sperm receptor for egg jelly is a modular protein with extensive homology to the human polycystic kidney disease protein, PKD1. J Cell Biol 133:809–817CrossRefPubMedGoogle Scholar
  58. Nusco GA, Lim D, Sabala P, Santella L (2002) Ca2+ response to cADPr during maturation and fertilization of starfish oocytes. Biochem Biophys Res Commun 290:1015–1021CrossRefPubMedGoogle Scholar
  59. Nusco GA, Chun JT, Ercolano E, Lim D, Gragnaniello G, Kyozuka K, Santella L (2006) Modulation of calcium signalling by the actin-binding protein cofilin. Biochem Biophys Res Commun 348:109–114CrossRefPubMedGoogle Scholar
  60. Ohlendieck K, Lennarz WJ (1996) Molecular mechanisms of gamete recognition in sea urchin fertilization. Curr Top Dev Biol 32:39–58CrossRefPubMedGoogle Scholar
  61. Ohlendieck K, Partin JS, Stears RL, Lennarz WJ (1994) Developmental expression of the sea urchin egg receptor for sperm. Dev Biol 165:53–62CrossRefPubMedGoogle Scholar
  62. Parrington J, Davis LC, Galione A, Wessel G (2007) Flipping the switch: how a sperm activates the egg at fertilization. Dev Dyn 236:2027–2038CrossRefPubMedGoogle Scholar
  63. Pitnick S, Hosken DJ, Birkhead TR (2009) Sperm morphological diversity. In: Birkhead TR et al (eds) Sperm biology: an evolutionary perspective. Academic, London, pp 69–149CrossRefGoogle Scholar
  64. Puppo A, Chun JT, Gragnaniello G, Garante E, Santella L (2008) Alteration of the cortical actin cytoskeleton deregulates Ca2+ signaling, monospermic fertilization, and sperm entry. PLoS One 3:e3588CrossRefPubMedPubMedCentralGoogle Scholar
  65. Ridgway EB, Gilkey JC, Jaffe LF (1977) Free calcium increases explosively in activating medaka eggs. Proc Natl Acad Sci U S A 74:623–627CrossRefPubMedPubMedCentralGoogle Scholar
  66. Santella L, Chun JT (2011) Actin, more than just a housekeeping protein at the scene of fertilization. Sci China Life Sci 54:733–743CrossRefPubMedGoogle Scholar
  67. Santella L, Kyozuka K (1994) Reinitiation of meiosis in starfish oocytes requires an increase in nuclear Ca2+. Biochem Biophys Res Commun 203:674–680CrossRefPubMedGoogle Scholar
  68. Santella L, De Riso L, Gragnaniello G, Kyozuka K (1999) Cortical granule translocation during maturation of starfish oocytes requires cytoskeletal rearrangement triggered by InsP3-mediated Ca2+ release. Exp Cell Res 248:567–574CrossRefPubMedGoogle Scholar
  69. Santella L, Lim D, Moccia F (2004) Calcium and fertilization: the beginning of life. Trends Biochem Sci 29:400–408CrossRefPubMedGoogle Scholar
  70. Santella L, Puppo A, Chun JT (2008) The role of the actin cytoskeleton in calcium signaling in starfish oocytes. Int J Dev Biol 52:571–584CrossRefPubMedGoogle Scholar
  71. Santella L, Vasilev F, Chun JT (2012) Fertilization in echinoderms. Biochem Biophys Res Commun 425:588–594CrossRefPubMedGoogle Scholar
  72. Santella L, Limatola N, Chun JT (2015) Calcium and actin in the saga of awakening oocytes. Biochem Biophys Res Commun 460:104–113CrossRefPubMedGoogle Scholar
  73. Santella L, Limatola N, Chun JT (2016) The fertilization process: a new way to look at an old phenomenon. Atlas of Science another view on science. https://atlasofscience.org/the-fertilization-process-a-new-way-to-look-at-an-old-phenomenon/
  74. Schatten H, Walter M, Biessmann H, Schatten G (1988) Microtubules are required for centrosome expansion and positioning while microfilaments are required for centrosome separation in sea urchin eggs during fertilization and mitosis. Cell Motil Cytoskeleton 11:248–259CrossRefPubMedGoogle Scholar
  75. Schroeder TE, Stricker SA (1983) Morphological changes during maturation of starfish oocytes: surface ultrastructure and cortical actin. Dev Biol 98:373–384CrossRefPubMedGoogle Scholar
  76. Steinhardt R, Zucker R, Schatten G (1977) Intracellular calcium release at fertilization in the sea urchin egg. Dev Biol 58:185–196CrossRefPubMedPubMedCentralGoogle Scholar
  77. Stricker SA (1999) Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev Biol 211:157–176CrossRefPubMedGoogle Scholar
  78. Stricker SA, Schatten G (1991) The cytoskeleton and nuclear disassembly during germinal vesicle breakdown in starfish oocytes. Develop Growth Differ 33:163–171CrossRefGoogle Scholar
  79. Svitkina T (2018) The actin cytoskeleton and actin-based motility. doi:  https://doi.org/10.1101/cshperspect.a018267.
  80. Terasaki M (1994) Redistribution of cytoplasmic components during germinal vesicle breakdown in starfish oocytes. J Cell Sci 107:1797–1805PubMedGoogle Scholar
  81. Terasaki M (1996) Actin filament translocations in sea urchin eggs. Cell Motil Cytoskeleton 34:48–56CrossRefPubMedGoogle Scholar
  82. Tilney LG, Inoué S (1982) Acrosomal reaction of Thyone sperm. II. The kinetics and possible mechanism of acrosomal process elongation. J Cell Biol 93:820–827CrossRefPubMedGoogle Scholar
  83. Tilney LG, Jaffe LA (1980) Actin, microvilli, and the fertilization cone of sea urchin eggs. J Cell Biol 87:771–782CrossRefPubMedGoogle Scholar
  84. Tilney LG, Hatano S, Ishikawa H, Mooseker MS (1973) The polymerization of actin: its role in the generation of the acrosomal process of certain echinoderm sperm. J Cell Biol 59:109–126CrossRefPubMedPubMedCentralGoogle Scholar
  85. Trimmer JS, Vacquier VD (1986) Activation of sea urchin gametes. Annu Rev Cell Biol 2:1–26CrossRefPubMedGoogle Scholar
  86. Vacquier VD (2012) The quest for the sea urchin egg receptor for sperm. Biochem Biophys Res Commun 425:583–587CrossRefPubMedGoogle Scholar
  87. Vacquier VD, Moy GW (1977) Isolation of bindin: the protein responsible for adhesion of sperm to sea urchin eggs. Proc Natl Acad Sci U S A 74:2456–2460CrossRefPubMedPubMedCentralGoogle Scholar
  88. Vasilev F, Chun JT, Gragnaniello G, Garante E, Santella L (2012) Effects of ionomycin on egg activation and early development in starfish. PLoS One 7:e39231CrossRefPubMedPubMedCentralGoogle Scholar
  89. Vasilev F, Limatola N, Park DR, Kim UH, Santella L, Chun JT (2018) Disassembly of subplasmalemmal actin filaments induces cytosolic Ca2+ increases in Astropecten aranciacus eggs. Cell Physiol Biochem (under review)Google Scholar
  90. Wang Y, Mattson MP, Furukawa K (2002) Endoplasmic reticulum calcium release is modulated by actin polymerization. J Neurochem 82:945–952CrossRefPubMedGoogle Scholar
  91. Welch MD, Mallavarapu A, Rosenblatt J, Mitchison TJ (1997) Actin dynamics in vivo. Curr Opin Cell Biol 9:54–61CrossRefPubMedGoogle Scholar
  92. Wessel GM, Conner SD, Berg L (2002) Cortical granule translocation is microfilament mediated and linked to meiotic maturation in the sea urchin oocyte. Development 129:4315–4325PubMedGoogle Scholar
  93. Whitaker M (1994) Exocytosis in sea urchin eggs. Ann N Y Acad Sci 710:248–253CrossRefPubMedGoogle Scholar
  94. Whitaker M (2006) Calcium at fertilization and in early development. Physiol Rev 86:25–88CrossRefPubMedPubMedCentralGoogle Scholar
  95. Whitaker MJ, Baker PF (1983) Calcium-dependent exocytosis in an in vitro secretory granule plasma membrane preparation from sea urchin eggs and the effects of some inhibitors of cytoskeletal function. Proc R Soc Lond B Biol Sci 218:397–413CrossRefPubMedGoogle Scholar
  96. Wilson NF, Snell WJ (1998) Microvilli and cell-cell fusion during fertilization. Trends Cell Biol 8:93–96CrossRefPubMedGoogle Scholar
  97. Ziomek CA, Epel D (1975) Polyspermy block of Spisula eggs is prevented by cytochalasin B. Science 189:139–141CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biology and Evolution of Marine OrganismsStazione Zoologica Anton DohrnNapoliItaly

Personalised recommendations