{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,3]],"date-time":"2026-04-03T00:19:15Z","timestamp":1775175555832,"version":"3.50.1"},"reference-count":104,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2022,4,29]],"date-time":"2022-04-29T00:00:00Z","timestamp":1651190400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Stazione Zoologica Anton Dohrn"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>In sea urchin, the immediate contact of the acrosome-reacted sperm with the egg surface triggers a series of structural and ionic changes in the egg cortex. Within one minute after sperm fuses with the egg plasma membrane, the cell membrane potential changes with the concurrent increases in intracellular Ca2+ levels. The consequent exocytosis of the cortical granules induces separation of the vitelline layer from the egg plasma membrane. While these cortical changes are presumed to prevent the fusion of additional sperm, the subsequent late phase (between 1 and 4 min after fertilization) is characterized by reorganization of the egg cortex and microvilli (elongation) and by the metabolic shift to activate de novo protein and DNA syntheses. The latter biosynthetic events are crucial for embryonic development. Previous studies suggested that the early phase of fertilization was not a prerequisite for these changes in the second phase since the increase in the intracellular pH induced by the exposure of unfertilized sea urchin eggs to ammonia seawater could start metabolic egg activation in the absence of the cortical granule exocytosis. In the present study, we have demonstrated that the incubation of unfertilized eggs in ammonia seawater induced considerable elongations of microvilli (containing actin filaments) as a consequence of the intracellular pH increase, which increased the egg\u2019s receptivity to sperm and made the eggs polyspermic at fertilization despite the elevation of the fertilization envelope (FE). These eggs also displayed compromised Ca2+ signals at fertilization, as the amplitude of the cortical flash was significantly reduced and the elevated intracellular Ca2+ level declined much faster. These results have also highlighted the importance of the increased internal pH in regulating Ca2+ signaling and the microvillar actin cytoskeleton during the late phase of the fertilization process.<\/jats:p>","DOI":"10.3390\/cells11091496","type":"journal-article","created":{"date-parts":[[2022,4,29]],"date-time":"2022-04-29T16:49:57Z","timestamp":1651250997000},"page":"1496","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["Regulation of the Actin Cytoskeleton-Linked Ca2+ Signaling by Intracellular pH in Fertilized Eggs of Sea Urchin"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5863-9999","authenticated-orcid":false,"given":"Nunzia","family":"Limatola","sequence":"first","affiliation":[{"name":"Department of Research Infrastructures for Marine Biological Resources, Stazione Zoologica Anton Dohrn, 80121 Napoli, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6070-4953","authenticated-orcid":false,"given":"Jong Tai","family":"Chun","sequence":"additional","affiliation":[{"name":"Department of Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn, 80121 Napoli, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7159-0499","authenticated-orcid":false,"given":"Luigia","family":"Santella","sequence":"additional","affiliation":[{"name":"Department of Research Infrastructures for Marine Biological Resources, Stazione Zoologica Anton Dohrn, 80121 Napoli, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,4,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0006-291X(02)02441-5","article-title":"Structural requirements for specie specific induction of the sperm acrosome reaction by sea urchin egg sulfated fucan","volume":"298","author":"Hirohashi","year":"2002","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"54","DOI":"10.2307\/1538405","article-title":"Studies on the acrosome. I reaction to egg-water and other stimuli","volume":"103","author":"Dan","year":"1952","journal-title":"Biol. Bull."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1016\/j.bbrc.2012.08.033","article-title":"Structure of acrosome reaction-inducing substance in the jelly coat of starfish eggs: A mini review","volume":"425","author":"Hoshi","year":"2012","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1016\/0014-4827(81)90132-4","article-title":"Fertilization of the starfish Astropecten aurantiacus","volume":"132","author":"Dale","year":"1981","journal-title":"Exp. Cell Res."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Puppo, A., Chun, J.T., Gragnaniello, G., Garante, E., and Santella, L. (2008). Alteration of the Cortical Actin Cytoskeleton Deregulates Ca2+ Signaling, Monospermic Fertilization, and Sperm Entry. PLoS ONE, 3.","DOI":"10.1371\/journal.pone.0003588"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1387\/ijdb.072560ls","article-title":"The role of the actin cytoskeleton in calcium signaling in starfish oocytes","volume":"52","author":"Santella","year":"2008","journal-title":"Int. J. Dev. Biol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1186\/s40851-020-00157-5","article-title":"Cellular and molecular aspects of oocyte maturation and fertilization: A perspective from the actin cytoskeleton","volume":"6","author":"Santella","year":"2020","journal-title":"Zool. Lett."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"2456","DOI":"10.1073\/pnas.74.6.2456","article-title":"Isolation of bindin: The protein responsible for adhesion of sperm to sea urchin eggs","volume":"74","author":"Vacquier","year":"1977","journal-title":"Proc. Natl. Acad. Sci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1016\/j.bbrc.2012.07.132","article-title":"The quest for the sea urchin egg receptor for sperm","volume":"425","author":"Vacquier","year":"2012","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2502","DOI":"10.1101\/gad.1133003","article-title":"The species-specific egg receptor for sea urchin sperm adhesion is EBR1, a novel ADAMTS protein","volume":"17","author":"Kamei","year":"2003","journal-title":"Genes Dev."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Wessel, G.M., Wada, Y., Yajima, M., and Kiyomoto, M. (2021). Bindin is essential for fertilization in the sea urchin. Proc. Natl. Acad. Sci. USA, 118.","DOI":"10.1073\/pnas.2109636118"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2426","DOI":"10.1073\/pnas.68.10.2426","article-title":"Bioelectric responses of the echinoderm egg to fertilization","volume":"68","author":"Steinhardt","year":"1971","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/0014-4827(79)90575-5","article-title":"Membrane potential, action potential and activation potential of eggs of the sea urchin, Lytechinus variegatus","volume":"122","author":"Chambers","year":"1979","journal-title":"Exp. Cell Res."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1","DOI":"10.2307\/1536454","article-title":"The fertilization reaction in Echinarachnius parma. I. Cortical response of the egg to insemination","volume":"36","author":"Just","year":"1919","journal-title":"Biol. Bull."},{"key":"ref_15","unstructured":"Just, E.E. (1939). The Biology of the Cell Surface, P. Blakiston\u2019s Son & Co., Inc."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1038\/261068a0","article-title":"Fast block to polyspermy in sea urchin eggs is electrically mediated","volume":"261","author":"Jaffe","year":"1976","journal-title":"Nature"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1017\/S0967199419000364","article-title":"Sodium-mediated fast electrical depolarization does not prevent polyspermic fertilization in Paracentrotus lividus eggs","volume":"27","author":"Limatola","year":"2019","journal-title":"Zygote"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1016\/j.bbrc.2015.03.028","article-title":"Calcium and actin in the saga of awakening oocytes","volume":"460","author":"Santella","year":"2015","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1038\/275217a0","article-title":"Membrane noise and conductance increase during single spermatozoon-egg interactions","volume":"275","author":"Dale","year":"1978","journal-title":"Nature"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1006\/dbio.1993.1120","article-title":"Sources of calcium in sea urchin eggs during the fertilization response","volume":"157","author":"Shen","year":"1993","journal-title":"Dev. Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1046\/j.1440-169X.1995.t01-5-00008.x","article-title":"Role of calcium influx during the latent period in sea urchin","volume":"37","author":"Jaffe","year":"1995","journal-title":"Develop. Growth Differ."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"757","DOI":"10.7150\/ijbs.28461","article-title":"Contributions of suboolemmal acidic vesicles and microvilli to the intracellular Ca2+ increase in the sea urchin eggs at fertilization","volume":"15","author":"Vasilev","year":"2019","journal-title":"Int. J. Biol. Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/0014-5793(91)81410-A","article-title":"A rapid change in phosphorylation on tyrosine accompanies fertilization of sea urchin eggs","volume":"295","author":"Ciapa","year":"1991","journal-title":"FEBS Lett."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1006\/dbio.2002.0600","article-title":"Egg Activation at Fertilization: Where It All Begins","volume":"245","author":"Runft","year":"2002","journal-title":"Dev. Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1152\/physrev.00023.2005","article-title":"Calcium at fertilization and in early development","volume":"86","author":"Whitaker","year":"2006","journal-title":"Physiol. Rev."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/0012-1606(83)90276-2","article-title":"Sources of calcium in egg activation: A review and hypothesis","volume":"99","author":"Jaffe","year":"1983","journal-title":"Dev. Biol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1068","DOI":"10.1007\/BF01952148","article-title":"Injection of a soluble sperm fraction into sea-urchin eggs triggers the cortical reaction","volume":"41","author":"Dale","year":"1985","journal-title":"Experientia"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"8301","DOI":"10.1074\/jbc.275.12.8301","article-title":"Nicotinic acid adenine dinucleotide phosphate-induced Ca2+ release: Interactions among distinct Ca2+ mobilizing mechanisms in starfish oocytes","volume":"275","author":"Santella","year":"2000","journal-title":"J. Biol. Chem."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2257","DOI":"10.1096\/fj.01-0157com","article-title":"NAADP+ initiates the Ca2+ response during fertilization of starfish oocytes","volume":"15","author":"Lim","year":"2001","journal-title":"FASEB J."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1016\/S0092-8674(02)01082-6","article-title":"NAADP mobilizes Ca(2+) from reserve granules, lysosome-related organelles, in sea urchin eggs","volume":"111","author":"Churchill","year":"2002","journal-title":"Cell"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1096\/fj.03-0178fje","article-title":"NAADP activates a Ca2+ current that is dependent on F-actin cytoskeleton","volume":"17","author":"Moccia","year":"2003","journal-title":"FASEB J."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1016\/j.tibs.2004.06.009","article-title":"Calcium and fertilization: The beginning of life","volume":"29","author":"Santella","year":"2004","journal-title":"Trends Biochem. Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/S0960-9822(03)00002-2","article-title":"Sperm deliver a new second messenger: NAADP","volume":"13","author":"Churchill","year":"2003","journal-title":"Curr. Biol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/0006-291X(64)90301-8","article-title":"A primary metabolic change of fertilization: Interconversion of pyridine nucleotides","volume":"17","author":"Epel","year":"1964","journal-title":"Biochim. Biophys. Res. Commun."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1259","DOI":"10.1073\/pnas.86.4.1259","article-title":"Respiratory burst oxidase of fertilization","volume":"86","author":"Heinecke","year":"1989","journal-title":"Proc. Nat. Acad. Sci. USA"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1007\/s11427-011-4202-x","article-title":"Actin, more than just a housekeeping protein at the scene of fertilization","volume":"54","author":"Santella","year":"2011","journal-title":"Sci. China Life Sci."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"588","DOI":"10.1016\/j.bbrc.2012.07.159","article-title":"Fertilization in echinoderms","volume":"425","author":"Santella","year":"2012","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1016\/j.bbrc.2018.09.084","article-title":"Maturation and fertilization of echinoderm eggs: Role of actin cytoskeleton dynamics","volume":"506","author":"Santella","year":"2018","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_39","first-page":"33","article-title":"Fertilization in Starfish and Sea Urchin: Roles of Actin","volume":"65","author":"Chun","year":"2018","journal-title":"Cell Differ."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1166","DOI":"10.1016\/j.bbrc.2014.06.057","article-title":"Early events of fertilization in sea urchin eggs are sensitive to actin-binding organic molecules","volume":"450","author":"Chun","year":"2014","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1086\/710126","article-title":"Effects of Salinity and pH of Seawater on the Reproduction of the Sea Urchin Paracentrotus lividus","volume":"239","author":"Limatola","year":"2020","journal-title":"Biol. Bull."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Limatola, N., Vasilev, F., Santella, L., and Chun, J.T. (2020). Nicotine Induces Polyspermy in Sea Urchin Eggs through a Non-Cholinergic Pathway Modulating Actin Dynamics. Cells, 9.","DOI":"10.3390\/cells9010063"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1083\/jcb.87.3.771","article-title":"Actin, microvilli, and the fertilization cone of sea urchin eggs","volume":"87","author":"Tilney","year":"1980","journal-title":"J. Cell Biol."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Chun, J.T., 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+ signaling. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0014100"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"2011","DOI":"10.1159\/000492523","article-title":"Disassembly of subplasmalemmal actin filaments induces cytosolic Ca2+ increases in Astropecten aranciacus eggs","volume":"48","author":"Vasilev","year":"2018","journal-title":"Cell Physiol. Biochem."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1038\/262661a0","article-title":"Intracellular pH and activation of sea urchin eggs after fertilisation","volume":"262","author":"Johnson","year":"1976","journal-title":"Nature"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1038\/272253a0","article-title":"Direct measurement of intracellular pH during metabolic derepression of the sea urchin egg","volume":"272","author":"Shen","year":"1978","journal-title":"Nature"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1038\/241400a0","article-title":"Development of K+-conductance and membrane potentials in unfertilized sea urchin eggs after exposure to NH4OH","volume":"241","author":"Steinhardt","year":"1973","journal-title":"Nature"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"899","DOI":"10.1073\/pnas.57.4.899","article-title":"Protein synthesis in sea urchin eggs: A \u201clate\u201d response to fertilization","volume":"57","author":"Epel","year":"1967","journal-title":"Proc. Nat. Acad. Sci USA."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"690","DOI":"10.1073\/pnas.71.3.690","article-title":"Chromosome cycles turned on in unfertilized sea urchin eggs exposed to NH40H","volume":"71","author":"Mazia","year":"1974","journal-title":"Proc. Nat. Acad. Sci. USA"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"422","DOI":"10.1016\/0012-1606(74)90158-4","article-title":"The stimulation of cytoplasmic polyadenylylation in sea urchin eggs by ammonia","volume":"37","author":"Wilt","year":"1974","journal-title":"Dev. Biol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1016\/0012-1606(75)90260-2","article-title":"DNA synthesis in unfertilized sea urchin eggs can be turned on and turned off by the addition and removal of procaine hydrochloride","volume":"47","author":"Vacquier","year":"1975","journal-title":"Dev. Biol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"536","DOI":"10.1038\/273536a0","article-title":"Mechanism of action of NH4Cl and other weak bases in the activation of sea urchin eggs","volume":"273","author":"Winkler","year":"1978","journal-title":"Nature"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1002\/jez.1401970115","article-title":"Fertilization acid of sea urchin eggs is not a consequence of cortical granule exocytosis","volume":"197","author":"Paul","year":"1976","journal-title":"J. Exp. Zool."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1083\/jcb.83.1.241","article-title":"pH regulates the polymerization of actin in the sea urchin egg cortex","volume":"83","author":"Begg","year":"1979","journal-title":"J. Cell Biol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"558","DOI":"10.1038\/287558a0","article-title":"Dual ionic controls for the activation of protein synthesis at fertilization","volume":"287","author":"Winkler","year":"1980","journal-title":"Nature"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1016\/S0014-4827(85)80050-1","article-title":"Microvillar elongation following parthenogenetic activation of sea urchin eggs","volume":"159","author":"Byrd","year":"1985","journal-title":"Exp. Cell Res."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"4469","DOI":"10.1073\/pnas.72.11.4469","article-title":"Turning on of activities in unfertilized sea urchin eggs: Correlation with changes of the surface","volume":"72","author":"Mazia","year":"1975","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1038\/scientificamerican1177-128","article-title":"The Program of Fertilization","volume":"237","author":"Epel","year":"1977","journal-title":"Sci. Am."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Limatola, N., Chun, J.T., Cherraben, S., Schmitt, J.L., Lehn, J.M., and Santella, L. (2021). Effects of Dithiothreitol on fertilization and early development in sea urchin. Cells., 10.","DOI":"10.3390\/cells10123573"},{"key":"ref_61","unstructured":"Sawada, H., Inuoe, N., and Iwano, M. (2014). Actin cytoskeleton and fertilization in starfish eggs. Sexual Reproduction in Animals and Plants\u2014Part II: Gametogenesis, Gamete Recognition, Activation, and Evolution, Springer Open."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1002\/(SICI)1097-0169(1996)34:1<48::AID-CM5>3.0.CO;2-E","article-title":"Actin filament translocations in sea urchin eggs","volume":"34","author":"Terasaki","year":"1996","journal-title":"Cell Motil. Cytoskelet."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1242\/jeb.26.2.164","article-title":"The fertilization reaction in the sea-urchin egg; a propagated response to sperm attachment","volume":"26","author":"Rothschild","year":"1949","journal-title":"J. Exp. Biol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1016\/0014-4827(71)90003-6","article-title":"Fertilization-associated light-scattering changes in eggs of the sea urchin Strongilocentrotus purpuratus","volume":"65","author":"Paul","year":"1971","journal-title":"Exp. Cell Res."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/0012-1606(75)90373-5","article-title":"Isolation and biological activity of the proteases released by sea urchin eggs following fertilization","volume":"44","author":"Carroll","year":"1975","journal-title":"Dev. Biol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1002\/mrd.1120010311","article-title":"Secretory functions of egg cortical granules in fertilization and development: Secretory functions of egg cortical granules in fertilization and development: A critical review","volume":"1","author":"Schuel","year":"1978","journal-title":"Gamete Res."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1016\/S0074-7696(01)09012-X","article-title":"The biology of cortical granules","volume":"209","author":"Wessel","year":"2001","journal-title":"Int. J. Cytol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/0014-4827(80)90188-3","article-title":"Intracellular pH controls the development of new potassium conductance after fertilization of the sea urchin egg","volume":"125","author":"Shen","year":"1980","journal-title":"Exp. Cell Res."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0922-3371(90)90019-S","article-title":"The initiation of development","volume":"29","author":"Epel","year":"1990","journal-title":"Cell Differ. Dev."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1002\/jcp.1030100304","article-title":"The release of calcium in Arbacia eggs on fertilization","volume":"10","author":"Mazia","year":"1937","journal-title":"J. Cell. Comp. Physiol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1915","DOI":"10.1073\/pnas.71.5.1915","article-title":"Activation of sea-urchin eggs by a calcium ionophore","volume":"71","author":"Steinhardt","year":"1974","journal-title":"Proc. Nat. Acad. Sci. USA"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1002\/cm.970070107","article-title":"Wave of cortical actin polymerization in the sea urchin egg","volume":"7","author":"Yonemura","year":"1987","journal-title":"Cell Motil. Cytoskelet."},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Collins, F., and Epel, D. (1977). The role of calcium ions in the acrosome reaction of sea urchin sperm: Regulation of exocytosis. Exp. Cell Res., 106.","DOI":"10.1016\/0014-4827(77)90258-0"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"338","DOI":"10.1016\/0012-1606(85)90093-4","article-title":"High pH-induced acrosome reaction and Ca2+ uptake in sea urchin sperm suspended in Na+-free seawater","volume":"110","author":"Darszon","year":"1985","journal-title":"Dev. Biol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"335","DOI":"10.2307\/1538583","article-title":"Studies on the Acrosome. III. Effect of Calcium Deficiency","volume":"107","author":"Dan","year":"1954","journal-title":"Biol. Bull."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"536","DOI":"10.1083\/jcb.77.2.536","article-title":"Polymerization of actin. IV. Role of Ca++ and H+ in the assembly of actin and in membrane fusion in the acrosomal reaction of echinoderm sperm","volume":"77","author":"Tilney","year":"1978","journal-title":"J. Cell Biol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1002\/(SICI)1097-4652(199907)180:1<19::AID-JCP3>3.0.CO;2-K","article-title":"Microvillar Ca++ signaling: A new view of an old problem","volume":"180","author":"Lange","year":"1999","journal-title":"J. Cell Physiol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1006\/jtbi.2000.2146","article-title":"Microvillar ion channels: Cytoskeletal modulation of ion fluxes","volume":"206","author":"Lange","year":"2000","journal-title":"J. Theor. Biol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1016\/j.ceca.2015.08.002","article-title":"Novel Ca2+ increases in the maturing oocytes of starfish during the germinal vesicle breakdown","volume":"58","author":"Limatola","year":"2015","journal-title":"Cell Calcium"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"396","DOI":"10.1016\/0012-1606(91)90241-T","article-title":"The calcium content of cortical granules and the loss of calcium from sea urchin eggs at fertilization","volume":"146","author":"Gillot","year":"1991","journal-title":"Dev. Biol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"1111","DOI":"10.1083\/jcb.116.5.1111","article-title":"Cortical localization of a calcium release channel in sea urchin eggs","volume":"116","author":"McPherson","year":"1992","journal-title":"J. Cell Biol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/j.ceca.2010.12.007","article-title":"Sea urchin eggs in the acid reign","volume":"50","author":"Morgan","year":"2011","journal-title":"Cell Calcium"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1111\/j.1469-7793.2001.0405k.x","article-title":"The effects of intracellular pH changes on resting cytosolic calcium in voltage-clamped snail neurons","volume":"530","author":"Willoughby","year":"2001","journal-title":"J. Physiol."},{"key":"ref_84","doi-asserted-by":"crossref","unstructured":"Li, S., Hao, B., Lu, Y., Yu, P., Lee, H.-C., and Yue, J. (2012). Intracellular alkalinization induces cytosolic Ca2+ increases by inhibiting sarco\/endoplasmic reticulum Ca2+-ATPase (SERCA). PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0031905"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/j.bbrc.2009.04.087","article-title":"The actin cytoskeleton in meiotic maturation and fertilization of starfish eggs","volume":"384","author":"Chun","year":"2009","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/0922-3371(89)90782-X","article-title":"Weak bases mimic the fertilization-associated chloride conductance increase and induce morphological changes in the cortex of Xenopus laevis eggs","volume":"26","author":"Charbonneau","year":"1989","journal-title":"Cell Differ. Dev."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1146\/annurev.ne.07.030184.001353","article-title":"Effects of intracellular H+ on the electrical properties of excitable cells","volume":"7","author":"Moody","year":"1984","journal-title":"Annu. Rev. Neurosci."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1002\/jez.b.22567","article-title":"Ernest Everett Just: Egg and embryo as excitable systems","volume":"322","author":"Byrnes","year":"2014","journal-title":"J. Exp. Zool. B Mol. Dev. Evol."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"361","DOI":"10.2307\/1537294","article-title":"An experimental study of polyspermy","volume":"70","author":"Clark","year":"1936","journal-title":"Biol. Bull."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"229","DOI":"10.2307\/1541052","article-title":"Polyspermy during the course of maturation","volume":"157","author":"Fujimori","year":"1979","journal-title":"Biol. Bull."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/j.yexcr.2019.05.007","article-title":"Altered actin cytoskeleton in ageing eggs of starfish affects fertilization process","volume":"381","author":"Limatola","year":"2019","journal-title":"Exp. Cell Res."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1017\/S0967199400002628","article-title":"Cortical changes in starfish (Asterina pectinifera) oocytes during 1-methyladenine-induced maturation and fertilisation\/activation","volume":"3","author":"Longo","year":"1995","journal-title":"Zygote"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1113\/jphysiol.1975.sp010880","article-title":"Potassium rectifications of the starfish oocyte membrane and their changes during oocyte maturation","volume":"246","author":"Miyazaki","year":"1975","journal-title":"J. Physiol."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1002\/mrd.23544","article-title":"Starfish oocytes of A. pectinifera reveal marked differences in sperm-induced electrical and intracellular calcium changes during oocyte maturation and at fertilization","volume":"89","author":"Mohri","year":"2022","journal-title":"Mol. Reprod. Dev."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"1050","DOI":"10.1096\/fj.02-0021com","article-title":"Activation of oocytes by latrunculin A","volume":"16","author":"Lim","year":"2002","journal-title":"FASEB J."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"845","DOI":"10.1016\/j.cbpa.2007.08.035","article-title":"Latrunculin A depolarizes starfish oocytes","volume":"148","author":"Moccia","year":"2007","journal-title":"Comp. Biochem. Physiol. A Mol. Integr. Physiol."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1002\/jez.1400130404","article-title":"The comparative efficiency of weak and strong bases in artificial parthenogenesis","volume":"13","author":"Loeb","year":"1912","journal-title":"J. Exp. Zool."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1038\/274190a0","article-title":"NH4Cl and other weak bases in the activation of sea urchin eggs","volume":"274","author":"Boron","year":"1978","journal-title":"Nature"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1042\/bj2500001","article-title":"Regulation of intracellular pH in eukaryotic cells","volume":"250","author":"Madshus","year":"1988","journal-title":"Biochem. J."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"516","DOI":"10.1152\/ajplegacy.1922.61.3.516","article-title":"The fertilization-reaction in Echinarachnius Parma. V. The existence in the inseminated egg of a period of special susceptibility to hypotonic seawater","volume":"61","author":"Just","year":"1922","journal-title":"Am. J. Physiol."},{"key":"ref_101","doi-asserted-by":"crossref","unstructured":"Limatola, N., Chun, J.T., and Santella, L. (2021). Fertilization and development of Arbacia lixula eggs are affected by osmolality conditions. BioSystems, 206.","DOI":"10.1016\/j.biosystems.2021.104448"},{"key":"ref_102","first-page":"409","article-title":"Metabolic regulation via intracellular pH","volume":"246","author":"Busa","year":"1984","journal-title":"Am. J. Physiol."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"1149","DOI":"10.1016\/j.bbrc.2014.05.100","article-title":"Intracellular pH in sperm physiology","volume":"450","author":"Nishigaki","year":"2014","journal-title":"Biochem Biophys. Res. Commun."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"895","DOI":"10.1042\/BCJ20200971","article-title":"Role of protons in calcium signaling","volume":"478","author":"Molinari","year":"2021","journal-title":"Biochem. J."}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/11\/9\/1496\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:04:28Z","timestamp":1760137468000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/11\/9\/1496"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,4,29]]},"references-count":104,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2022,5]]}},"alternative-id":["cells11091496"],"URL":"https:\/\/doi.org\/10.3390\/cells11091496","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,4,29]]}}}