Abstract
Starfish oocytes provide optimal opportunities to study meiotic progression and fertilization in vitro. A large and synchronized population of oocytes in the gonad can be induced to undergo maturation by addition of the hormone 1-methyladenine (1-MA). Successful monospermic fertilization is normally achieved when the eggs are in the interval between breakdown of the large nucleus (germinal vesicle) and extrusion of the first polar body. Insemination outside this temporal window frame gives rise to polyspermy. Although immature oocytes may become polyspermic because they are unable to form the fertilization envelope, which has been intuitively believed to serve as a mechanical block to polyspermy, overly mature eggs usually incorporate supernumerary sperm despite full elevation of the fertilization envelope. During the course of meiotic progression of the oocytes and of egg activation at fertilization, the cortical actin cytoskeleton undergoes dynamic changes. In this review, we discuss the role of the actin cytoskeleton during the meiotic maturation and at fertilization, focusing on its modulatory effects on intracellular Ca2+ signaling, cortical granule exocytosis, and sperm incorporation.
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1 Introduction
Oocytes of marine animals are an exceptional model system for the study of fertilization and embryonic development. Although ovulation in mammals only releases a few oocytes, starfish and sea urchin provide many eggs that are highly accessible. Fertilization and subsequent development of echinoderms can be easily observed with minimal experimental requirement, as they reproduce by “external fertilization” in seawater. At the peak of the breeding season, sea urchin ovaries are filled with eggs that have completed meiosis and contain haploid DNA (Vacquier 2011). Thus, a substantial population (<20 %) of the oocytes at the GV (germinal vesicle; i.e., the nucleus) stage can be obtained only before the peak of breeding season. At variance with the sea urchin, starfish oocytes in the female gonad at the peak of the breeding season are fully grown, yet they are arrested at prophase I of meiosis. Only upon hormonal stimulation (methyladenine, 1-MA) from the adhering follicle cells, the oocytes re-enter the meiotic cycle and are spawned into seawater (Kanatani 1973; Meijer and Guerrier 1984). Thus, even if belonging to the same phylum, sea urchin and starfish display a fundamental difference in the way in which their eggs are fertilized. Sea urchin eggs are fertilized after the completion of meiosis (haploid stage, n), but starfish eggs are normally fertilized before the completion of the first meiotic division (Fig. 13.1A). In starfish, the period between germinal vesicle breakdown (GVBD) and the extrusion of the first polar body (2n) represents the optimal period for successful fertilization. Indeed, insemination of the starfish oocytes before or after this period results in a high rate of polyspermic fertilization. As an experimental model, starfish provides some advantages over sea urchin eggs in that (a) meiotic maturation can be induced in vitro, and (b) the large cell dimensions (Fig. 13.1B) facilitate microinjection and fluorescence imaging (Santella et al. 2008, 2012; Santella and Chun 2011). Starfish oocytes thus provide an optimal opportunity to examine the cytoplasmic changes that occur during meiotic maturation and fertilization.
2 Cytoplasmic Changes During Meiotic Maturation of Oocytes
2.1 Morphological Transition
During meiotic maturation, oocytes display changes in the nucleus, where chromosome reshuffling and dissolution of the nuclear membranes take place, but also morphological alteration of their surface. Before and after the maturation process, a striking structural reorganization of the cortex occurs in sea urchin eggs (Runnström 1963; Franklin 1963; Lönning 1967; Longo 1978). Transmission electron microscopy (TEM) has revealed that numerous long microvilli that are present on the surface of immature oocytes nearly disappear in mature eggs (Dale and Santella 1985). These microvilli are filled with actin filaments (Tilney and Jaffe 1980). The cortex of starfish oocytes also undergoes mechanical and morphological changes during meiotic maturation. The microvilli become shorter, and the cortical granules are translocated and positioned perpendicularly to the plasma membrane (Hirai and Shida 1979; Longo et al. 1995; Santella et al. 1999). Change of the actin cytoskeleton is often shown by the transient formation of a F-actin spike a few minutes after 1-MA addition (Schroeder 1981; Schroeder and Stricker 1983), whereas the rigidity of the cell and its F-actin content decrease at the time of GVDB (Shôji et al. 1978; Heil-Chapdelaine and Otto 1996). Thus, it appears that the actin cytoskeleton is regulated differently, presumably playing different roles, in different subcellular domains. Because the cell nucleus is enriched with actin molecules that normally do not form filaments (Clark and Merriam 1977), the role of the “spilling” actin at the time of GVDB, when the nucleoplasm inevitably intermixes with cytoplasm, is of obvious interest.
2.2 Signaling Pathways to Meiotic Maturation
The starfish oocyte maturation hormone (1-MA) operates through a receptor on the plasma membrane because microinjected 1-MA does not induce oocyte maturation (Kanatani and Hiramoto 1970; Shida and Hirai 1978). The identity of this receptor has not been determined as yet, but it is known that its activation leads to the release of Gβγ proteins (Jaffe et al. 1993; Chiba et al. 1995), which in turn activate a phosphatidylinositol-3-kinase (PI3K)-producing phosphatidylinositol-3,4,5-trisphosphate (PIP3) from phosphatidylinositol-4,5-bisphoshate (PIP2). An important target of the PI3K signaling pathway is the Akt/PKB kinase, which directly downregulates Myt1 and upregulates Cdc25, leading to the activation of the universal cell-cycle regulator, the cyclin B-Cdc2 complex (Masui 2001; Prigent and Hunt 2004; Kishimoto 2011).
2.3 Intracellular Ca2+ Increase During Meiotic Maturation
Artificial elevation of intracellular Ca2+ level can induce nuclear maturation of starfish oocytes, suggesting that Ca2+ is the functional downstream effector of 1-MA (Moreau et al. 1978). Nonetheless, the maturation of starfish oocytes can proceed without detectable Ca2+ transients or in the presence of Ca2+ chelators (Witchel and Steinhardt 1990), suggesting that the breakdown of the nuclear envelope and meiotic resumption may not be under the control of Ca2+. However, direct microinjection of the Ca2+ chelator BAPTA into the GV blocked the disassembly of the nuclear envelope (Santella and Kyozuka 1994; Santella et al. 1998), suggesting that Ca2+ signal in the GV subcellular domain may be important. A more recent investigation has shown that the 1-MA-triggered Ca2+ wave always initiates in the vegetal hemisphere of the starfish oocyte and propagates to the animal pole through the superficial domains of the cortex, raising the question of the involvement of the Ca2+-releasing pathway linked to the 1,4,5-inositol trisphosphate (InsP3) receptors, as the latter are known to be more sensitive in the animal pole of the egg (Lim et al. 2003; Kyozuka et al. 2008). Because 1-MA can induce the Ca2+ response in the absence of external Ca2+, the involvement of nicotinic acid adenine dinucleotide phosphate (NAADP) in the process also becomes questionable, as NAADP is known to act mainly by inducing Ca2+ influx in starfish oocytes.
2.4 Sensitization of the Ca2+-Releasing Mechanisms
Starfish oocytes undergoing meiotic maturation become progressively more sensitive to InsP3. Thus, mature eggs respond to the same dose of InsP3 with a much higher level of Ca2+ release (Chiba et al. 1990; Lim et al. 2003). This response might be partly explained by the observation that the endoplasmic reticulum (ER), which constitutes the major intracellular Ca2+ store of the oocyte, undergoes extensive restructuring during meiotic maturation (Stricker 2006). The morphological changes of the ER parallel the alteration of the actin cytoskeleton, which readily responds to 1-MA and forms thick bundles that align perpendicularly to the egg surface 50 min after the addition of the activating hormone (Santella et al. 2008; Santella and Chun 2011). Because the sensitization of the InsP3-dependent Ca2+-releasing mechanism induced by 1-MA is blocked by agents promoting actin depolymerization, that is, latrunculin-A (LAT-A), it appears that changes of the actin cytoskeleton have a role in optimizing the Ca2+-releasing mechanism in maturing oocytes (Lim et al. 2002). The actin cytoskeleton may contribute to the process, either by assisting the mobilization of Ca2+ from the ER or by changing the microdomain environment of the ion channels. We have provided support for this idea by demonstrating that the magnitude, kinetics, or onset of Ca2+ signaling in response to the fertilizing sperm, or to Ca2+-linked second messengers such as InsP3 and cyclic ADP ribose (cADPr), are significantly modified by interfering with the dynamic changes of the actin cytoskeleton: that is, with the actin-binding protein cofilin (Nusco et al. 2006), LAT-A, with Jasplakinolide, heparin (Puppo et al. 2008), or the PIP2-sequestering domain of PLC-δ1 (Chun et al. 2010). Interestingly, the exposure of the mature eggs of some starfish species, such as Astropecten aranciacus, to these treatments triggers an auto-catalyzing Ca2+ wave in the absence of fertilizing sperms or of Ca2+-mobilizing second messengers. The Ca2+ wave induced by LAT-A originates largely from the intracellular stores, and its spatiotemporal pattern in Ca2+-free seawater is highly reminiscent of the fertilization Ca2+ wave induced by sperm, although it requires a latent period of 6–10 min (Lim et al. 2002). This effect was not observed in the GV-stage oocytes, suggesting that the threshold for the triggering of the spontaneous Ca2+ release is much lower in mature eggs, and that the trigger itself is dependent on the actin cytoskeleton. Alternatively, Ca2+ may be released during the process of actin treadmilling (Lange and Gartzke 2006), and it may simply reflect a slower turnover rate of the actin filaments in immature oocytes. In other words, F-actin may contribute to intracellular Ca2+ homeostasis and ion flux either by modulating the ion channel activities, or by a more direct mechanism in which the polymerization and depolymerization cycle of actin filaments in the local environment may sequester and release cytosolic Ca2+ (Lange and Gartzke 2006; Chun and Santella 2009).
2.5 Changes of the Electrical Property of the Plasma Membrane During Meiotic Maturation
The aforementioned changes of cytoplasm are accompanied by decrease of oocyte stiffness within 7–8 min after 1-MA addition and by the decrease in K+ conductance that leads to depolarization of the membrane potential (Miyazaki et al. 1975; Miyazaki and Hirai 1979). An abrupt switching of the membrane potential from the initial level of −70 to −90 mV to a new stable state of −10 to −20 mV takes place concurrently with, or shortly before, GVBD in the maturing oocytes of A. aranciacus (Dale et al. 1979). Thus, the resting potential of mature eggs is far less negative than that of the immature oocytes. However, the membrane potential can be restored to the original level of the GV-stage oocytes as the eggs become overripe in seawater (Miyazaki et al. 1975; Miyazaki and Hirai 1979).
3 Signals of Fertilization and Egg Activation
3.1 Generation and Propagation of the Intracellular Ca2+ Wave
Mature eggs are metabolically repressed, but interaction with the fertilizing sperm triggers a series of events that are collectively termed “egg activation.” The two earliest detectable changes at fertilization are rapid depolarization of the egg plasma membrane and Ca2+ influx, which are followed by the intracellular Ca2+ wave propagating from the site of successful sperm–egg interaction (Steinhardt et al. 1971; Shen and Buck 1993). It has been shown that intracellular Ca2+ increase at fertilization can be recapitulated by the combined effect of Ca2+-mobilizing second messengers, namely, InsP3, NAADP, and cADPr. InsP3 is generated by the hydrolysis of phosphatidylinositol-4,5-bisphosphate (PIP2) in the plasma membrane by phospholipase C. Several isozymes that catalyze this process have been identified, and fertilization is thought to activate at least one of them. In analogy to the InsP3 receptor (Streb et al. 1983; Furuichi et al. 1989), cADPr may bind to the cADPr-sensitive ryanodine receptor complex and release Ca2+ from the internal stores (Carafoli et al. 2001; Lee 2002; Santella and Chun 2013). The Ca2+-releasing activities of both InsP3 and ryanodine receptors are facilitated by Ca2+ itself through a “Ca2+-induced Ca2+ release” (CICR) mechanism, whereas the activity of the channels responding to NAADP does not display direct CICR properties and may involve a distinct intracellular (or extracellular) Ca2+ store (Santella et al. 2000; Moccia et al. 2003; Galione and Churchill 2002). At variance with the findings in the sea urchin eggs where NAADP releases Ca2+ from lysosome-like acidic stores (Churchill et al. 2002), the Ca2+ increase induced by microinjected NAADP in starfish eggs appear to require external Ca2+ and is mediated by the activation of ion channels on the plasma membrane (Runft et al. 2002; Santella et al. 2004). Thus, these three second messengers may contribute to distinct aspects of Ca2+ signaling in fertilized eggs of starfish. NAADP may trigger an initial Ca2+ increase in the egg cortex whereas InsP3 contributes to egg-wide propagation of the Ca2+ waves (Lim et al. 2001; Santella et al. 2004; Santella and Chun 2013).
3.2 Morphological Changes of the Egg Cortex During Fertilization
Within a few minutes after fertilization, the actin bundles in the subplasmalemmal zones begin to be translocated centripetally in concert with the internalization of the sperm (Terasaki 1996; Puppo et al. 2008; Vasilev et al. 2012). In addition, the sperm that makes the initial contact with the egg induces the formation of the fertilization cone which is filled with actin filaments (Tilney and Jaffe 1980). Microinjection of starfish eggs with heparin not only inhibits Ca2+ signaling but also induces hyperpolymerization of subplasmalemmal actin (Puppo et al. 2008). These eggs with perturbed actin cytoskeleton exhibit multiple fertilization cones but fail to form the functional tethering that leads to sperm incorporation. Similarly, eggs whose actin meshwork at the plasma membrane is perturbed by ionomycin fail to display the centripetal movement of the F-actin fibers at fertilization and often fail to incorporate sperm (Vasilev et al. 2012).
3.3 Changes of the Electrical Property of the Plasma Membrane at Fertilization during Meiotic Maturation
Fertilization also induces rapid changes of the membrane potentials in eggs. After successful binding of sperm, sea urchin eggs either fire a rapid action potential to a positive value of about +20 mV or display a step depolarization (DeFelice and Dale 1979); this is followed by a slower depolarization that initiates simultaneously with the cortical granule exocytosis and elevation of the fertilization envelope. The membrane potential of the fertilized sea urchin eggs remains at positive values for a few minutes but gradually returns to the negative value.
4 Block to Polyspermy
Although attracting multiple sperm, the eggs normally incorporate a single sperm in vitro. The elevation of the thick fertilization envelope in fertilized eggs of echinoderm led to the idea that such a structure may serve as a mechanical block to polyspermy. However, this process is rather slow; thus, the block to polyspermy may require an additional faster mechanism. A very rapid event that occurs before elevation of the vitelline envelope in fertilized eggs is of special interest. Just (1939) was among the first to describe the possibility of the fast block to polyspermy. He stated, “one can follow the wave in the ectoplasm which begins at the point of sperm-entry and sweeps over the egg,” and emphasized that “with membrane-separation, the eggs undergo some change; and it is this change—not its result, membrane separation—which constitutes the block to the entrance of additional spermatozoa.” He then added that “this block, which is more subtle than the mechanical obstacle interposed by the presence of a separated membrane, is established before membrane-separation occurs.” Indeed, in one of the first experiments to study the nature of the block to polyspermy, Rothschild and Swann (1951, 1952) demonstrated that sea urchin eggs establish monospermic fertilization as early as 2 s after insemination, suggesting that a fast mechanism must be established on the egg surface to reduce the probability of successful refertilization.
As to the physicochemical event underlying the fast block to polyspermy, several hypotheses have been set forth, including those based on the early increase of hydrogen peroxide and protease that would inhibit the binding of supernumerary sperm (Vacquier et al. 1972). A hypothesis that drew special attention proposed that the fast partial block to polyspermy is electrically mediated by the rapidly changing membrane potential of the egg at fertilization, which renders the egg unreceptive to supernumerary sperm (Jaffe 1976). In support of the view that the establishment of monospermy is linked to the amplitude of the membrane depolarization at fertilization, sea urchin eggs artificially arrested at positive potentials were shown to be prevented from being fertilized by sperm. The “electrical block” hypothesis has been somewhat controversial (Dale and Monroy 1981; Dale and DeFelice 2010). Its main shortcoming, admitted also by its supporters, is that the electrical block is not absolute and can be overridden by high concentration of sperm. Thus, it has been generally agreed that insemination with excess sperm causes polyspermic fertilization in the eggs of many marine animals. However, Just (1939) had already contradicted this idea by showing that eggs of Arbacia were never polyspermic even “if a thick sperm-suspension be added to the eggs as early as one second after the first insemination.” He added, “I have also made the initial insemination with the heaviest sperm-concentration procurable, i.e., ‘dry’ sperm as it exudes from the male, and have obtained only mono-spermic fertilization.” He showed that polyspermy in Arbacia may occur when the ectoplasm of the fertilizable eggs was injured and thus slowed in reacting to the stimulus of the first sperm. Such injury was very apparent in the eggs with extremely heavy insemination. This observation and the failure of positively held membrane potentials to preclude fertilization of the eggs by excess sperm (Jaffe 1976) imply that an additional factor besides membrane potential may ensure the integrity of eggs and thus guide monospermy. Dale (1985) reported that the sperm receptivity of sea urchin oocytes and eggs was independent of their resting potentials when their jelly layers were kept intact, suggesting that the properties of the egg surface may confer fine regulation of monospermic fertilization.
5 Meiotic Stages of Oocytes and Polyspermy
The idea that polyspermy is linked to the regional anatomy of egg surface and cortex can be examined in starfish oocytes at different meiotic maturation stages. As mentioned, the morphology of the starfish oocyte changes with meiotic progression, as judged by the structure of microvilli and cortical actin cytoskeleton. Meiotically immature oocytes are prone to polyspermy upon insemination and fail to elevate the fertilization envelope (Fig. 13.2). They lack an effective fast or slow block to polyspermy (Santella et al. 2012). The progress of cytoplasmic maturation in sea urchin oocytes is also accompanied by structural modifications of the surface layer in a direction that favors monospermic fertilization (Runnström and Monné 1945; Runnström 1963). However, most starfish eggs overmatured beyond the extrusion of second polar bodies display polyspermy at fertilization despite their ability to elevate a normal fertilization envelope (Fujimori and Hirai 1979). The explanation for the polyspermy of these overmature eggs might be twofold. Firstly, the tendency to produce polyspermy may be linked to the electrical properties of the plasma membrane. For instance, the resting potential of the mature eggs of A. pectinifera at the optimum period is much less negative (−30 mV) than those of immature (−70 mV) and overmature eggs (−55 mV) because the membrane permeability to K+ decreases during GVBD but is restored during overmaturation (Miyazaki et al. 1975). The peak of the activation potential in the overmature eggs at fertilization (−4 mV) is also not as high as in the mature eggs at the optimum period (+12 mV), rendering them less effective in preventing the entry of supernumerary sperm in the light of the “electrical block” hypothesis (Miyazaki and Hirai 1979; Dale et al. 1979; Moody and Bosma 1985). Second, the increased tendency to polyspermy outside the aforementioned “optimum period” might be caused by the lack of the natural physiological propensity of the egg cytoplasm. Classical studies had indicated that the dispersal of nuclear contents into the cytoplasm and cortex is a prerequisite for cytoplasmic maturation (Delage 1901; Chambers 1921). After the GVDB, a signal or a diffusible substance from the GV may interact with the egg cortex to induce the structural modifications that are essential for egg activation and monospermic sperm incorporation. Indeed, at variance with previous findings (Hirai et al. 1971), the InsP3-dependent Ca2+ response was much slower, with no cortical granules exocytosis in the mature eggs of A. pectinifera whose GV had been removed before the addition of 1-MA, whereas Ca2+ signaling and elevation of the vitelline layer in response to NAADP and fertilizing sperm were not much affected by enucleation (Lim et al. 2001). On the other hand, eggs matured cortically with low doses of 1-MA displayed an increased rate of polyspermy (Hirohashi et al. 2008). These eggs underwent no GVDB but displayed full elevation of the fertilization envelope. Thus, it is conceivable that either underexposure or overexposure to the nucleus-borne signals during maturation and overmaturation leads to subtle differences in the structure and function of the egg ectoplasm, which may disarray the eggs toward polyspermy.
The translocation of the cortical granules and vesicles that takes place during the meiotic maturation of oocytes may contribute to shielding the eggs from the attack of supernumerary sperm (Longo et al. 1995). At fertilization, these granules and vesicles undergo exocytosis and their extrusion gives rise to full elevation of fertilization envelope (Fig. 13.3). However, the finding that polyspermy can take place even with full elevation of the fertilization envelope in overmature eggs (Fig. 13.4) indicates that the mechanical block by the fertilization envelope is no guarantee for monospermic fertilization. The fast mechanism preventing the entry of supernumerary sperm may have become disrupted in these eggs. As mentioned, this could be caused by the altered electrical property of the plasma membrane, or may be attributed to the overall failure of the cytoplasmic mechanism in the egg surface that controls sperm interaction and incorporation.
6 Role of the Actin Cytoskeleton
One of the most evident morphological consequences of meiotic maturation and overmaturation in starfish eggs is the change of the actin cytoskeleton. Although the signaling pathways leading to it are beyond the scope of this review, the relevance of the actin cytoskeleton to the control of sperm interaction and incorporation may be worth mentioning. Egg microvilli may be involved in deciding sperm receptivity, and their number on the surface of aged mammalian oocytes is severely reduced (Santella et al. 1985). In starfish, a decline in the proper functional interactions between sperm and aged eggs has been suggested (Chambers 1921; Just 1939). Our recent studies on starfish eggs have indicated that the alteration of the structural organization in subplasmalemmal actin filaments renders the egg surface less reactive to the first sperm and more receptive to supernumerary sperm (Puppo et al. 2008; Chun et al. 2010; Vasilev et al. 2012). Eggs with hyperpolymerization of the subplasmalemmal actin displayed the formation of numerous irregularly shaped fertilization cones (thus, polyspermic), yet also displayed unfunctional tethering of the sperm, suggesting a more direct role of actin in sperm interaction and incorporation (Puppo et al. 2008). As mentioned, actin has a modulatory role on the intracellular Ca2+ release and influx (Lim et al. 2002; Nusco et al. 2006; Kyozuka et al. 2008; Chun et al. 2010), but it must be emphasized that actin also is a critical factor in controlling exocytosis of the cortical granules. Despite the early claim that intracellular Ca2+ elevation is solely important for exocytosis (Steinhardt and Epel 1974; Vacquier 1975; Whitaker and Baker 1983), we have shown that, when the actin cytoskeleton in the cortex is perturbed, intracellular Ca2+ increase does not induce discharge of the cortical granules (Kyozuka et al. 2008; Puppo et al. 2008; Chun et al. 2010).
7 Concluding Remarks
Although belonging to the same phylum, sea urchin and starfish have evolved to use a fundamentally different temporal scheme at fertilization. Although fertilization of sea urchin awaits the completion of the egg meiosis, natural fertilization of starfish anticipates the meiotic program. To ensure monospermy, the starfish eggs must be fertilized when they are at the incomplete stage of meiosis; that is, during the interval between the GVDB and the extrusion of the first polar body. The reason why starfish evolved to adopt this seemingly premature fertilization scheme has not been clarified, but it may have been inevitable because the same hormone 1-MA not only stimulates oocyte maturation but also promotes spawning of mature gametes (Meijer and Guerrier 1984). Anyhow, the capability of controlling meiotic maturation with 1-MA in vitro makes starfish an excellent model system in the study of the relationship among the cellular events that take place during meiotic maturation, fertilization, and egg activation: that is, intracellular Ca2+ signaling, dynamic changes of the actin cytoskeleton, and the modulation of ion channel activities. The rapid rearrangement of the actin cytoskeleton during meiotic maturation and fertilization may be a well-calculated reconfiguration of the cell structure that is linked to the fine regulation of Ca2+ signaling, vesicle exocytosis, and sperm incorporation. On the other hand, although the fertilization envelope of the echinoderm egg may provide mechanical protection of the early embryo, the other functions that have been proposed may require careful examination in future studies. The fully elevated fertilization membrane was not sufficient to ensure monospermic fertilization (Fig. 13.4) nor was it a chemical barrier to protect the zygote or early embryo (Vasilev et al. 2012). In view of the relative ease of applying imaging and electrophysiological methods following microinjection, starfish oocytes may provide opportunities to study the reciprocal regulation of cytoskeletal changes and ion channel activities.
References
Carafoli E, Santella L, Branca D, Brini M (2001) Generation, control, and processing of cellular calcium signals. Crit Rev Biochem Mol Biol 36(2):107–260
Chambers R (1921) Microdissection studies. III. Some problems in the maturation and fertilization of the echinoderm egg. Biol Bull 41(6):318–350
Chiba K, Kado RT, Jaffe LA (1990) Development of calcium release mechanisms during starfish oocyte maturation. Dev Biol 140(2):300–306
Chiba K, Longo FJ, Kontani K, Katada T, Hoshi M (1995) A periodic network of G protein beta gamma subunit coexisting with cytokeratin filament in starfish oocytes. Dev Biol 169(2): 415–420
Chun JT, Santella L (2009) Roles of the actin-binding proteins in intracellular Ca2+ signalling. Acta Physiol (Oxf) 195(1):61–70
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(11):e14100
Churchill GC, Okada Y, Thomas JM, Genazzani AA, Patel S, Galione A (2002) NAADP mobilizes Ca2+ from reserve granules, lysosome-related organelles, in sea urchin eggs. Cell 111(5):703–708
Clark TG, Merriam RW (1977) Diffusible and bound actin nuclei of Xenopus laevis oocytes. Cell 12(4):883–891
Dale B (1985) Sperm receptivity in sea urchin oocytes and eggs. J Exp Biol 118:85–97
Dale B, DeFelice L (2010) Polyspermy prevention: facts and artifacts? J Assist Reprod Genet 28(3):199–207
Dale B, Monroy A (1981) How is polyspermy prevented? Gamete Res 4:151–169
Dale B, Santella L (1985) Sperm–oocyte interaction in the sea-urchin. J Cell Sci 74:153–167
Dale B, de Santis A, Hoshi M (1979) Membrane response to 1-methyladenine requires the presence of the nucleus. Nature (Lond) 282(5734):89–90
DeFelice LJ, Dale B (1979) Voltage response to fertilization and polyspermy in sea urchin eggs and oocytes. Dev Biol 72(2):327–341
Delage Y (1901) Etudes experimentales sur la maturation cytoplasmique et sur la parthenogenese artificielle chez les echinodermes. Arch Zool Exp Gen 9(3):284–336
Franklin L (1963) Morphology of gamete membrane fusion and of sperm entry into oocytes of the sea urchin. J Cell Biol 25(2):81–100
Fujimori T, Hirai S (1979) Differences in starfish oocyte susceptibility to polyspermy during the course of maturation. Biol Bull 157(2):249–257
Furuichi T, Yoshikawa S, Miyawaki A, Wada K, Maeda N, Mikoshiba K (1989) Primary structure and functional expression of the inositol 1,4,5-trisphosphate-binding protein P400. Nature (Lond) 342(6245):32–38
Galione A, Churchill GC (2002) Interactions between calcium release pathways: multiple messengers and multiple stores. Cell Calcium 32(5–6):343–354
Heil-Chapdelaine RA, Otto JJ (1996) Characterization of changes in F-actin during maturation of starfish oocytes. Dev Biol 177(1):204–216
Hirai S, Shida H (1979) Shortening of microvilli during the maturation of starfish oocyte from which vitelline coat was removed. Bull Mar Biol St Asamushi Tohoku Univ 16:161–167
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(1):137–143
Hirohashi N, Harada K, Chiba K (2008) Hormone-induced cortical maturation ensures the slow block to polyspermy and does not couple with meiotic maturation in starfish. Dev Biol 318(1): 194–202
Jaffe LA (1976) Fast block to polyspermy in sea urchin eggs is electrically mediated. Nature (Lond) 261(5555):68–71
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(4):775–783
Just EE (1939) The biology of the cell surface. P. Blakiston’s son & Co., Inc. Philadelphia, USA
Kanatani H (1973) Maturation-inducing substance in starfishes. Int Rev Cytol 35(1):253–298
Kanatani H, Hiramoto Y (1970) Site of action of 1-methyladenine in inducing oocyte maturation in starfish. Exp Cell Res 61(2):280–284
Kishimoto T (2011) A primer on meiotic resumption in starfish oocytes: the proposed signaling pathway triggered by maturation-inducing hormone. Mol Reprod Dev 78(10–11):704–707
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(2):426–435
Lange K, Gartzke J (2006) F-actin-based Ca signaling-a critical comparison with the current concept of Ca signaling. J Cell Physiol 209(2):270–287
Lee HC (ed) (2002) Cyclic ADP-ribose and NAADP. Structures, metabolism and functions. Kluwer Academic, Dordrecht
Lim D, Kyozuka K, Gragnaniello G, Carafoli E, Santella L (2001) NAADP+ initiates the Ca2+ response during fertilization of starfish oocytes. FASEB J 15(12):2257–2267
Lim D, Lange K, Santella L (2002) Activation of oocytes by latrunculin A. FASEB J 16(9): 1050–1056
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(43):42505–42514
Longo FJ (1978) Insemination of immature sea urchin (Arbacia punctulata) eggs. Dev Biol 62(2):271–291
Longo FJ, Woerner M, Chiba K, Hoshi M (1995) Cortical changes in starfish (Asterina pectinifera) oocytes during 1-methyladenine-induced maturation and fertilisation/activation. Zygote 3(3): 225–239
Lönning S (1967) Studies of the ultrastructure of sea urchin eggs and the changes induced at insemination. Sarsia 30(1):31–48
Masui Y (2001) From oocyte maturation to the in vitro cell cycle: the history of discoveries of maturation-promoting factor (MPF) and cytostatic factor (CSF). Differentiation 69(1):1–17
Meijer L, Guerrier P (1984) Maturation and fertilization in starfish oocytes. Int Rev Cytol 86(1): 129–196
Miyazaki S, Hirai S (1979) Fast polyspermy block and activation potential. Correlated changes during oocyte maturation of a starfish. Dev Biol 70(2):327–340
Miyazaki SI, Ohmori H, Sasaki S (1975) Potassium rectifications of the starfish oocyte membrane and their changes during oocyte maturation. J Physiol (Lond) 246(1):55–78
Moccia F, Lim D, Nusco GA, Ercolano E, Santella L (2003) NAADP activates a Ca2+ current that is dependent on F-actin cytoskeleton. FASEB J 17(13):1907–1909
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(2): 396–404
Moreau M, Guerrier P, Doree M, Ashley CC (1978) Hormone-induced release of intracellular Ca2+ triggers meiosis in starfish oocytes. Nature (Lond) 272(5650):251–253
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(1):109–114
Prigent C, Hunt T (2004) Oocyte maturation and cell cycle control: a farewell symposium for Pr. Marcel Dorée. Biol Cell 96(3):181–185
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(10):e3588
Rothschild L, Swann MM (1951) The fertilization reaction in the sea urchin. The probability of a successful sperm–egg collision. J Exp Biol 28(3):403–416
Rothschild L, Swann MM (1952) The fertilization reaction in the sea urchin. The block to polyspermy. J Exp Biol 29(3):469–483
Runft LL, Jaffe LA, Mehlmann LM (2002) Egg activation at fertilization: where it all begins. Dev Biol 245(2):237–254
Runnström J (1963) Sperm-induced protrusions in sea urchin oocytes: a study of phase separation and mixing in living cytoplasm. Dev Biol 7(1):38–50
Runnström J, Monné L (1945) On some properties of the surface layers of immature and mature sea urchin eggs, especially the changes accompanying nuclear and cytoplasmic maturation. Arkiv für Zoologie 36A(18):1–26
Santella L, Chun JT (2011) Actin, more than just a housekeeping protein at the scene of fertilization. Sci China Life Sci 54(8):733–743
Santella L, Chun JT (2013) Calcium signaling by cyclic ADP-ribose and NAADP. In: Lennarz WJ Lane MD (eds.) The Encyclopedia of Biological Chemistry 3:331–336. Academic Press, Waltham, MA, USA
Santella L, Kyozuka K (1994) Reinitiation of meiosis in starfish oocytes requires an increase in nuclear Ca2+. Biochem Biophys Res Commun 203(1):674–680
Santella L, Alikani M, Talansky BE, Cohen J, Dale B (1985) Is the human oocyte plasma membrane polarized? Hum Reprod 7(7):999–1003
Santella L, De Riso L, Gragnaniello G, Kyozuka K (1998) Separate activation of the cytoplasmic and nuclear calcium pools in maturing starfish oocytes. Biochem Biophys Res Commun 252(1):1–4
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(2):567–574
Santella L, Kyozuka K, Genazzani AA, De Riso L, Carafoli E (2000) Nicotinic acid adenine dinucleotide phosphate-induced Ca2+ release. Interactions among distinct Ca2+ mobilizing mechanisms in starfish oocytes. J Biol Chem 275(12):8301–8306
Santella L, Lim D, Moccia F (2004) Calcium and fertilization: the beginning of life. Trends Biochem Sci 29(8):400–408
Santella L, Puppo A, Chun JT (2008) The role of the actin cytoskeleton in calcium signaling in starfish oocytes. Int J Dev Biol 52(5–6):571–584
Santella L, Vasilev F, Chun JT (2012) Fertilization in echinoderms. Biochem Biophys Res Commun 425(3):588–594
Schroeder TE (1981) Microfilament-mediated surface change in starfish oocytes in response to 1-methyladenine: implications for identifying the pathway and receptor sites for maturation-inducing hormones. J Cell Biol 90(2):362–371
Schroeder TE, Stricker SA (1983) Morphological changes during maturation of starfish oocytes: surface ultrastructure and cortical actin. Dev Biol 98(2):373–384
Shen SS, Buck WR (1993) Sources of calcium in sea urchin eggs during the fertilization response. Dev Biol 157(1):157–169
Shida H, Hirai S (1978) Site of 1-methyladenine receptors in the maturation of starfish oocytes. Dev Growth Differ 20:205–211
Shôji Y, Hamaguchi MS, Hiramoto Y (1978) Mechanical properties of the endoplasm in starfish oocytes. Exp Cell Res 117(1):79–87
Steinhardt RA, Epel D (1974) Activation of sea-urchin eggs by a calcium ionophore. Proc Natl Acad Sci USA 71(5):1915–1919
Steinhardt RA, Lundin L, Mazia D (1971) Bioelectric responses of the echinoderm egg to fertilization. Proc Natl Acad Sci USA 68(10):2426–2430
Streb H, Irvine RF, Berridge MJ, Schulz I (1983) Release of Ca2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-trisphosphate. Nature (Lond) 306(5938):67–69
Stricker SA (2006) Structural reorganizations of the endoplasmic reticulum during egg maturation and fertilization. Semin Cell Dev Biol 17(2):303–313
Terasaki M (1996) Actin filament translocations in sea urchin eggs. Cell Motil Cytoskeleton 34(1): 48–56
Tilney LG, Jaffe LA (1980) Actin, microvilli, and the fertilization cone of sea urchin eggs. J Cell Biol 87(3):771–782
Vacquier VD (1975) The isolation of intact cortical granules from sea urchin eggs: calcium ions trigger granule discharge. Dev Biol 43(1):62–74
Vacquier VD (2011) Laboratory on sea urchin fertilization. Mol Reprod Dev 78(8):553–564
Vacquier VD, Epel D, Douglas LA (1972) Sea urchin eggs release protease activity at fertilization. Nature (Lond) 237(5349):34–36
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(6):e39231
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(1213):397–413
Witchel HJ, Steinhardt RA (1990) 1-Methyladenine can consistently induce a fura-detectable transient calcium increase which is neither necessary nor sufficient for maturation in oocytes of the starfish Asterina miniata. Dev Biol 141(2):393–398
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Santella, L., Limatola, N., Chun, J.T. (2014). Actin Cytoskeleton and Fertilization in Starfish Eggs. In: Sawada, H., Inoue, N., Iwano, M. (eds) Sexual Reproduction in Animals and Plants. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54589-7_13
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