Fertilization of the starfish Astropecten aurantiacus

Dale, Brian; Dan-Sohkawa, Marina; Santis, A. De; Hoshi, Motonori

doi:10.1016/0014-4827(81)90132-4

Cited by 35 publications

(19 citation statements)

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“…The first detectable electrical change of the egg plasma membrane is the fertilization potential, whose rise is slower than that of the sea urchin egg. The cortical reaction initiates simultaneously with the fertilization potential before the spermatozoon is completely inside the oocyte (Dale et al, 1981). It has been a matter of continued debate in the past whether the activation of the egg requires sperm attachment or penetration into the egg (Shapiro and Eddy, 1980).…”

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confidence: 99%

The role of the actin cytoskeleton in calcium signaling in starfish oocytes

Santella

Puppo²,

Chun³

2008

Int. J. Dev. Biol.

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Ca 2+ is the most universal second messenger in cells from the very first moment of fertilization. In all animal species, fertilized eggs exhibit massive mobilization of intracellular Ca 2+ to orchestrate the initial events of development. Echinoderm eggs have been an excellent model system for studying fertilization and the cell cycle due to their large size and abundance. In preparation for fertilization, the cell cycle-arrested oocytes must undergo meiotic maturation. Studies of starfish oocytes have shown that Ca 2+ signaling is intimately involved in this process. Our knowledge of the molecular mechanism of meiotic maturation and fertilization has expanded greatly in the past two decades due to the discovery of cell cycle-related kinases and Ca 2+ -mobilizing second messengers. However, the molecular details of their actions await elucidation of other cellular elements that assist in the creation and transduction of Ca 2+ signals. In this regard, the actin cytoskeleton, the receptors for second messengers and the Ca 2+ -binding proteins also require more attention. This article reviews the physiological significance and the mechanism of intracellular Ca 2+ mobilization in starfish oocytes during maturation and fertilization. KEY WORDS: cell activation, sperm-egg interaction, meiosis, germinal vesicle, cyclic ADP ribose, NAADP Starfish oocytes and maturation-promoting factorStarfish oocytes have contributed greatly to our understanding of the molecular mechanisms controlling the cell cycle (maturation) and fertilization. During oogenesis, the oocytes undergo cell growth and differentiation bringing them to the end of the first prophase of meiosis where they remain synchronously arrested until spawning (Fig. 1). At this stage of maturation, the oocytes are characterized by a very large nucleus (approximately 60 µm in diameter) termed the germinal vesicle (GV) (Fig. 2). The starfish oocyte has several advantages as an experimental model system. First, the cell is large and nearly transparent, making it suitable for imaging experiments after microinjection of fluorescent markers. Second, maturation (or meiosis re-initiation) can be induced in vivo and in vitro by the hormone 1-methyladenine (1-MA), rendering the oocytes successfully fertilizable (Kanatani et al., 1969;Meijer and Guerrier, 1984). The first visible sign of oocyte maturation is the germinal vesicle breakdown (GVBD) in which the large nucleus breaks down to release its nucleoplasm into the cytoplasm 20-30 minutes after the application of the hormone. This is how the starfish oocyte is conspicuously different from sea urchin eggs, which are already mature at the time of spawning. In sea urchins, the haploid egg pronucleus has a Int. J. Dev. Biol. 52: 571-584 (2008) doi: 10.1387/ijdb.072560ls Abbreviations used in this paper: cADPr, cyclic-ADPribose; CaMKII, calmodulin dependent kinase II; CICR, calcium induced calcium release; GV, germinal vesicle; GVBD, germinal vesicle breakdown; InsP3, inositol 1,4,5-trisphosphate; LAT-A, latrunculin-...

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confidence: 99%

The role of the actin cytoskeleton in calcium signaling in starfish oocytes

Santella

Puppo²,

Chun³

2008

Int. J. Dev. Biol.

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“…This first phase seems to correspond to a step depolarization triggered by sperm-egg collision (spermgated channel) because no such step depolarization is observed in the parthenogenetic activation of eggs. Such a depolarization specific to spermegg collision has been reported earlier in sea urchin (6,27), tunicate (7) and amphibia (21,33) eggs, though not in starfish oocytes (5). This type of sperm-gated depolarization in various species of echinoderm eggs triggers a regenerative action potential associated with transient levels of intracellular calcium (1 2, 27 and 34).…”

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confidence: 54%

Fertilization Potential of the Medaka Egg

Itô¹,

Shimamoto²

1989

Dev Growth Differ

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Fertilization of the medaka egg in 10% Ringer's solution generates a depolarization of 4 mV just before the appearance of a characteristically longer hyperpolarization (25). The depolarization appears to be the result of a nonspecific leak triggered by sperm stimulation and the amplitude of the depolarization is thought to be independent of [Ca2+l0 (25). We have investigated the ionic dependence of this depolarization. An initial small depolarization (3-4 mV; duration, 5-8 sec) is followed by a rising phase of a spike-like depolarization in the range of 10-60 mV. The amplitude of this spike-like depolarization is propodional to log [Ca2+], ranging from 0.33-18 mM. Calcium antagonists, e.g. 10 mM cobalt or 10 pg/ml verapamil in 10% Ringer do not block the depolarization in the presence of 1.1 mM CaCI2.

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“…However, fertilization of starfish A. aranciacus does not involve this primary electrical event and the membrane depolarization leads directly to the fertilization potential. The lack of the primary event during the activation of starfish eggs was attributed to the acrosome reaction that takes place remotely at the outer surface of the jelly coat [96]. Hence, the morphological events at fertilization are closely linked to the physiological responses such as Ca 2+ signaling and the electrical changes.…”

Section: Ca 2+ Signaling During Egg Fertilizationmentioning

confidence: 99%

Actin, more than just a housekeeping protein at the scene of fertilization

Santella

Chun

2011

Sci. China Life Sci.

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Since the first demonstration of sperm entry into the fertilized eggs of Mediterranean sea urchin Paracentrotus lividus by Hertwig (1876), enormous progress and insights have been made on this topic. However, the precise molecular mechanisms underlying fertilization are largely unknown. The two most dramatic changes taking place in the zygote immediately after fertilization are: (i) a sharp increase of intracellular Ca 2+ that initiates at the sperm interaction site and traverses the egg cytoplasm as a wave, and (ii) the concomitant dynamic rearrangement of the actin cytoskeleton. Traditionally, this has been studied most extensively in the sea urchin eggs, but another echinoderm, starfish, whose eggs are much bigger and transparent, has facilitated experimental approaches using microinjection and fluorescent imaging methodologies. Thus in starfish, it has been shown that the sperm-induced Ca 2+ increase in the fertilized egg can be recapitulated by several Ca 2+ -evoking second messengers, namely inositol 1,4,5-trisphosphate (InsP 3 ), cyclic ADP-ribose (cADPr) and nicotinic acid adenine dinucleotide phosphate (NAADP), which may play distinct roles in the generation and propagation of the Ca 2+ waves. Interestingly, it has also been found that the dynamic rearrangement of the actin cytoskeleton in the fertilized eggs plays pivotal roles in guiding monospermic sperm entry and in the fine modulation of the intracellular Ca 2+ signaling. As it is well known that Ca 2+ regulates the structure of the actin cytoskeleton, our finding that Ca 2+ signaling can be reciprocally affected by the state of the actin cytoskeleton raises an intriguing possibility that actin and Ca 2+ signaling may form a 'positive feedback loop' that accelerates the downstream events of fertilization. Perturbation of the cortical actin networks also inhibits cortical granules exocytosis. Polymerizing actin bundles also compose the 'acrosome process,' a tubular structure protruding from the head of fertilizing sperm. Hence, actin, which is one of the most strictly conserved proteins in eukaryotes, modulates almost all major aspects of fertilization. starfish, calcium, egg maturation, fertilization, PIP2, actin cytoskeleton, cofilin Citation:Santella L, Chun J T. Actin, more than just a housekeeping protein at the scene of fertilization.

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Fertilization of the starfish Astropecten aurantiacus

Cited by 35 publications

References 15 publications

The role of the actin cytoskeleton in calcium signaling in starfish oocytes

The role of the actin cytoskeleton in calcium signaling in starfish oocytes

Fertilization Potential of the Medaka Egg

Actin, more than just a housekeeping protein at the scene of fertilization

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