Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-23T23:26:54.879Z Has data issue: false hasContentIssue false
  • English
  • Français

Sodium-mediated fast electrical depolarization does not prevent polyspermic fertilization in Paracentrotus lividus eggs

Published online by Cambridge University Press:  09 August 2019

Nunzia Limatola ,
Filip Vasilev ,
Jong Tai Chun  and
Luigia Santella Open the ORCID record for Luigia Santella [Opens in a new window]
Nunzia Limatola
Affiliation:
Department of Biology and Evolution of Marine Organisms
Filip Vasilev
Affiliation:
Department of Biology and Evolution of Marine Organisms
Jong Tai Chun
Affiliation:
Department of Biology and Evolution of Marine Organisms
Luigia Santella*
Affiliation:
Department of Research Infrastructures for Marine Biological Resources, Stazione Zoologica Anton Dohrn, Napoli, Italy
*
Address for correspondence: Luigia Santella. Stazione Zoologica Anton Dohrn, Villa Comunale 80121, Napoli, Italy. Tel: +39 0815833289. Fax: +39 0817641355. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

During sea urchins fertilization, the activating spermatozoon triggers a series of physiological changes that transforms the quiescent egg into a dynamic zygote. It has been suggested that several of these egg activation events, e.g. sperm-induced plasma membrane depolarization and the Ca2+-linked cortical reaction, play additional roles to prevent the entry of supernumerary spermatozoa. In particular, the abrupt shift in egg membrane potential at fertilization, which is sustained by a Na+ influx, has been considered as a fast mechanism to block polyspermy. To test the relevance of the Na+-mediated fast electrical block to polyspermy, we fertilized sea urchin eggs in artificial seawater with a low concentration of Na+; nearly all the eggs were still monospermic, as judged by the number of Hoechst 33422-stained sperm. When fertilized in normal seawater, eggs that were pre-incubated in the low Na+ medium exhibited impaired elevation of the fertilization envelope. Nevertheless, these eggs manifested entry of a single spermatozoon, suggesting that the fertilization envelope was not the primary determinant of the block to polyspermy. Furthermore, we showed that the abnormal cleavage patterns displayed by eggs pre-incubated in low Na+, which were often considered a hallmark of polyspermy, were due to the alterations in the cortical actin filaments dynamics following fertilization, and not to the formation of multipolar spindles associated with supernumerary sperm centrosomes. Hence, our results suggested that Paracentrotus lividus eggs do not utilize Na+ to rapidly prevent additional spermatozoa from entering the egg, at variance with the hypothesis of an electrical fast block to polyspermy.

Keywords

ActinCortical reactionFast blockPolyspermySea urchinSodium depletion
Type
Research Article
Information
Zygote , Volume 27 , Issue 4 , August 2019 , pp. 241 - 249
Copyright
© Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Present address: Centre de Recherche du Centre Hospitalier de l’Université de Montréal, (CRCHUM) Montréal, Canada.

References

Burgess, DR and Schroeder, TE (1977) Polarized bundles of actin filaments within microvilli of fertilized sea urchin eggs. J Cell Biol 74, 1032–7.CrossRefGoogle ScholarPubMed
Byrnes, WM and Newman, SA (2014) Ernest Everett Just: egg and embryo as excitable systems. J Exp Zool B Mol Dev Evol 322, 191–201.CrossRefGoogle ScholarPubMed
Chambers, EL and De Armendi, J (1979) Membrane potential, action potential and activation potential of eggs of the sea urchin Lytechinus variegatus . Exp Cell Res 122, 203–18.CrossRefGoogle ScholarPubMed
Chun, JT, Puppo, A, Vasilev, F, Gragnaniello, G, Garante, E and Santella, L (2010) The biphasic increase of PIP2 in the fertilized eggs of starfish: new roles in actin polymerization and Ca2+ signalling. PLoS One 5, e14100.CrossRefGoogle Scholar
Chun, JT, Vasilev, F and Santella, L (2013) Antibody against the actin-binding protein depactin attenuates Ca2+ signalling in starfish eggs. Biochem Biophys Res Commun 441, 301–7.CrossRefGoogle Scholar
Chun, JT, Limatola, N, Vasilev, F and Santella, L (2014) Early events of fertilization in sea urchin eggs are sensitive to actin-binding organic molecules. Biochem Biophys Res Commun 450, 1166–74.CrossRefGoogle ScholarPubMed
Chun, JT, Vasilev, F, Limatola, N and Santella, L (2018) Fertilization in starfish and sea urchin: roles of actin. In: Kloc, M and Kubiak, JZ (eds) Marine Organisms as Model Systems in Biology and Medicine, Series Title: Results and Problems in Cell Differentiation, Springer Nature, pp. 33–47.CrossRefGoogle Scholar
Clark, JM (1936) An experimental study of polyspermy. Biol Bull 70, 361–84.CrossRefGoogle Scholar
Dale, B (2014) Is the idea of a fast block to polyspermy based on artifact? Biochem Biophys Res Commun 450, 1159–65.CrossRefGoogle ScholarPubMed
Dale, B (2016) Achieving monospermy or preventing polyspermy. Res Rep Biol 7, 47–57.Google Scholar
Dale, B (2018) Polyspermy. In: Skinner, M (ed.) Encyclopedia of Reproduction, 2nd edition. Elsevier, USA.Google Scholar
Dale, B and De Felice, LJ (1984) Sperm activated channels in ascidian oocytes. Dev Biol 101, 235–9.CrossRefGoogle ScholarPubMed
Dale, B and De Santis, A (1981) Maturation and fertilization of the sea urchin oocyte: an electrophysiological study. Dev Biol 85, 474–84.CrossRefGoogle Scholar
Dale, B, De Felice, LJ and Taglietti, V (1978) Membrane noise and conductance increase during single spermatozoon–egg interactions. Nature 275, 217–9.CrossRefGoogle ScholarPubMed
Gilbert, SF (2014) The fast block to polyspermy. Developmental Biology, 10th edition. Sunderland (MA): Sinauer Associates. p. 129.Google Scholar
Gillot, I, Ciapa, B, Payan, P and Sardet, C (1991) The calcium content of cortical granules and the loss of calcium from sea urchin eggs at fertilization. Dev Biol 146, 396–405.CrossRefGoogle ScholarPubMed
Green, JD and Summers, RG (1980) Formation of the cortical concavity at fertilization in the sea urchin egg. Dev Growth Diff 22, 821–9.CrossRefGoogle Scholar
Hamaguchi, Y and Mabuchi, I (1986) Alpha-actinin accumulation in the cortex of echinoderm eggs during fertilization. Cell Motil Cytoskeleton 6, 549–59.CrossRefGoogle Scholar
Jaffe, LA (1976) Fast block to polyspermy in sea urchin eggs is electrically mediated. Nature 261, 68–71.CrossRefGoogle ScholarPubMed
Jaffe, LA (1980) Electrical polyspermy block in sea urchins: Nicotine and low sodium experiments. Dev Growth Diff 22, 503–7.CrossRefGoogle Scholar
Just, EE (1919) The fertilization-reaction in Echinarachnius parma. I. Cortical response of the egg to insemination. Biol Bull 36, 1–10.CrossRefGoogle Scholar
Just, EE (1929) The fertilization-reaction in eggs of Paracentrotus and Echinus . Biol Bull 57, 326–31.CrossRefGoogle Scholar
Just, EE (1939) The Biology of the Cell Surface. P. Blakiston’s Son and Co., Philadelphia, USA.Google Scholar
Kyozuka, K and Osanai, K (1988) Fertilization cone formation in starfish oocytes: The role of the egg cortex actin microfilaments in sperm incorporation. Gamete Res 20, 275–85.CrossRefGoogle ScholarPubMed
Kyozuka, K, Chun, JT, Puppo, A, Gragnaniello, G, Garante, E and Santella, L (2009) Guanine nucleotides in the meiotic maturation of starfish oocytes: regulation of the actin cytoskeleton and of Ca2+ signalling. PLoS One 4, e6296.CrossRefGoogle Scholar
Limatola, N, Chun, JT, Kyozuka, K and Santella, L (2015) Novel Ca2+ increases in the maturing oocytes of starfish during the germinal vesicle breakdown. Cell Calcium 58, 500–10.CrossRefGoogle ScholarPubMed
Limatola, N, Vasilev, F, Chun, JT and Santella, L (2019) Altered actin cytoskeleton in ageing eggs of starfish affects fertilization process. Exp Cell Res 381, 179–90.CrossRefGoogle ScholarPubMed
Miyazaki, SI, Ohmori, H and Sasaki, S (1975) Potassium rectifications of the starfish oocyte membrane and their changes during oocyte maturation. J Physiol 246, 55–78.CrossRefGoogle ScholarPubMed
Moody, WJ and Lansman, JB (1983) Developmental regulation of Ca2+ and K+ currents during hormone-induced maturation of starfish oocytes. Proc Natl Acad Sci USA 80, 3096–100.CrossRefGoogle Scholar
Nusco, GA, Chun, JT, Ercolano, E, Lim, D, Gragnaniello, G, Kyozuka, K and Santella, L (2006) Modulation of calcium signalling by the actin-binding protein cofilin. Biochem Biophys Res Commun 348, 109–14.CrossRefGoogle ScholarPubMed
Puppo, A, Chun, JT, Gragnaniello, G, Garante, E and Santella, L (2008) Alteration of the cortical actin cytoskeleton deregulates Ca2+ signalling, monospermic fertilization, and sperm entry. PLoS One 3, e3588.CrossRefGoogle Scholar
Ramos, I and Wessel, GM (2013) Calcium pathway machinery at fertilization in echinoderms. Cell Calcium 53, 16–23.CrossRefGoogle ScholarPubMed
Rothschild, L (1954) Polyspermy. Q Rev Biol 29, 332–42.CrossRefGoogle ScholarPubMed
Runft, LL, Jaffe, LA and Mehlmann, LM (2002) Egg activation at fertilization: where it all begins. Dev Biol 245, 237–54.CrossRefGoogle ScholarPubMed
Santella, L, Lim, D and Moccia, F (2004) Calcium and fertilization: the beginning of life. Trends Biochem Sci 29, 400–8.CrossRefGoogle ScholarPubMed
Santella, L, Vasilev, F and Chun, JT (2012) Fertilization in echinoderms. Biochem Biophys Res Commun 425, 588–94.CrossRefGoogle ScholarPubMed
Santella, L, Limatola, N and Chun, JT (2014) Actin cytoskeleton and fertilization in starfish eggs . In: Sawada, H, Inoue, N and Iwano, M (eds) Sexual Reproduction in Animals and Plants. Springer Verlag, pp. 141–55.CrossRefGoogle Scholar
Santella, L, Limatola, N and Chun, JT (2015) Calcium and actin in the saga of awakening oocytes. Biochem Biophys Res Commun 460, 104–13.CrossRefGoogle ScholarPubMed
Santella, L, Limatola, N and Chun, JT (2016) The fertilization process: a new way to look at an old phenomenon. Atlas of Science: Another View on Science http://atlasofscience.org pp. 1–3.Google Scholar
Santella, L, Limatola, N, Vasilev, F and Chun, JT (2018) Maturation and fertilization of echinoderm eggs: role of actin cytoskeleton dynamics. Biochem Biophys Res Commun 506, 361–71.CrossRefGoogle ScholarPubMed
Schatten, G and Mazia, D (1976) The penetration of the spermatozoon through the sea urchin egg at fertilization. Exp Cell Res 98, 325–37.CrossRefGoogle ScholarPubMed
Schatten, H, Schatten, G, Mazia, D, Balczon, R and Simerly, C (1986) Behavior of centrosomes during fertilization and cell division in mouse oocytes and in sea urchin eggs. Proc Natl Acad Sci USA 83, 105–9.CrossRefGoogle ScholarPubMed
Scheer, U (2014) Historical roots of centrosome research: discovery of Boveri’s microscope slides in Würzburg. Philos Trans R Soc Lond B Biol Sci 369, 20130469.CrossRefGoogle ScholarPubMed
Schuel, H and Schuel, R (1981) Rapid sodium-dependent block to polyspermy in sea urchin eggs. Dev Biol 87, 249–58.CrossRefGoogle ScholarPubMed
Schuel, H, Schuel, R, Dandekar, P, Boldt, J and Summers, RG (1982) Sodium requirements in hardening of the fertilization envelope and embryonic development in sea urchins. Biol Bull 162, 202–13.CrossRefGoogle Scholar
Stricker, SA (1999) Comparative biology of calcium signalling during fertilization and egg activation in animals. Dev Biol 211, 157–76.CrossRefGoogle ScholarPubMed
Terasaki, M (1996) Actin filament translocations in sea urchin eggs. Cell Motil Cytoskeleton 34, 48–56.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
Tilney, LG and Jaffe, LA (1980) Actin, microvilli, and the fertilization cone of sea urchin eggs. J Cell Biol 87, 771–82.CrossRefGoogle ScholarPubMed
Vacquier, VD (2012) The quest for the sea urchin egg receptor for sperm. Biochem Biophys Res Commun 425, 583–7.CrossRefGoogle ScholarPubMed
Vasilev, V, Chun, JT, Gragnaniello, G, Garante, E and Santella, L (2012) Effects of ionomycin on egg activation and early development in starfish. PLoS One 7, e39231.CrossRefGoogle ScholarPubMed
Vasilev, F, Limatola, N, Chun, JT and Santella, L (2019) Contributions of suboolemmal acidic vesicles and microvilli to the intracellular Ca2+ increase in the sea urchin eggs at fertilization. Int J Biol Sci 15, 757–75.CrossRefGoogle ScholarPubMed
Wessel, GM, Brooks, JM, Green, E, Haley, S, Voronina, E, Wong, J, Zaydfudim, V and Conner, S (2001) The biology of cortical granules. Int Rev Cytol 209, 117–206.CrossRefGoogle ScholarPubMed
Whitaker, M (2006) Calcium at fertilization and in early development. Physiol Rev 86, 25–88.CrossRefGoogle ScholarPubMed
Wong, JL and Wessel, GM (2006) Defending the zygote: search for the ancestral animal block to polyspermy. Curr Top Dev Biol 72, 1–151.Google ScholarPubMed
Yonemura, S and Mabuchi, I (1987) Wave of cortical actin polymerization in the sea urchin egg. Cell Motil Cytoskeleton 7, 46–53.CrossRefGoogle ScholarPubMed
Supplementary material: File

Limatola et al. supplementary material

Tables S1-S2

Download Limatola et al. supplementary material(File)
File 14.3 KB