Actin cytoskeleton modulates calcium signaling during maturation of starfish oocytes

Kyozuka, Keiichiro; Chun, Jong Tai; Puppo, Agostina; Gragnaniello, Gianni; Garante, Ezio; Santella, Luigia

doi:10.1016/j.ydbio.2008.05.549

Cited by 48 publications

(95 citation statements)

References 75 publications

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“…In line with this finding, all the tested agents that promote assembly or disassembly of the actin cytoskeleton e.g. latrunculin-A (LAT-A), heparin, G-proteins inhibitors, and jasplakinolide ( Figure 2) significantly affected the spatiotemporal pattern of the 1-MA-induced Ca 2+ release [86,87]. Furthermore, the 1-MA-induced cortical Ca 2+ release was also potentiated by the actin binding protein cofilin that reorganizes the actin cytoskeleton, as its preinjection into the starfish oocytes enhanced the Ca 2+ liberation nearly by two-fold [88].…”

Section: Calcium Signaling During Maturation and Fertilization Of Stasupporting

confidence: 69%

“…Since fertilization cone is filled with actin filaments that are continuous to the subjacent regions, the failed block to polyspermy and the aborted sperm entry in these eggs might be attributed to the severely altered actin networks at the subplasmalemmal region and inside the fertilization cones. These results, at variance with previous suggestions [107], add more weight to the idea that a proper structural organization and control of the actin cytoskeleton in the cortex is required for the initiation of the Ca 2+ signal and for the cortical granules exocytosis [86,105].…”

Section: Calcium and Actin At Fertilizationcontrasting

confidence: 53%

“…More recently, it was demonstrated that the 1-MA-mediated Ca 2+ increase always initiates at the vegetal hemisphere of the oocytes and that the sites of Ca 2+ release are largely restricted to the subplasmalemmal regions. The Ca 2+ wave arrives at the opposite side of the oocytes in about 20 seconds [86]. Apparently, the Ca 2+ liberation by 1-MA was not linked to the second messengers, namely InsP 3 , cADPr or NAADP, but was inhibited by the structural alteration of the cortical actin cytoskeleton.…”

Section: Calcium Signaling During Maturation and Fertilization Of Stamentioning

confidence: 91%

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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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Section: Calcium Signaling During Maturation and Fertilization Of Stasupporting

confidence: 69%

Section: Calcium and Actin At Fertilizationcontrasting

confidence: 53%

Section: Calcium Signaling During Maturation and Fertilization Of Stamentioning

confidence: 91%

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

Santella

Chun

2011

Sci. China Life Sci.

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“…In terms of upstream processes that might regulate such Ca 2+ signals in starfish oocytes, reorganizations of the cortical actin network may play a key role, based on: i) the rapid restructuring of actin filaments that routinely occurs before GVBD in 1-MA-treated controls; ii) the fact that the 1-MA-induced calcium wave propagates exclusively in the cortical region where actin filaments are concentrated, and iii) the findings that experimental manipulations to hypo-or hyperpolymerize cortical actin serve to disrupt normal Ca 2+ dynamics and maturation (Kyozuka et al, 2008;Chun and Santella, 2009;Chun et al, 2013). The precise mechanisms by which a remodeling of the actin network might affect Ca 2+ release capabilities in starfish oocytes are not known.…”

Section: Echinodermata (Starfish Sea Urchins)mentioning

confidence: 99%

Calcium signals and oocyte maturation in marine invertebrates

Deguchi¹,

Takeda²,

Stricker³

2015

Int. J. Dev. Biol.

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In various oocytes and eggs of animals, transient elevations in cytoplasmic calcium ion concentrations are known to regulate key processes during fertilization and the completion of meiosis. However, whether or not calcium transients also help to reinitiate meiotic progression at the onset of oocyte maturation remains controversial. This article summarizes reports of calcium signals playing essential roles during maturation onset (=germinal vesicle breakdown, GVBD) in several kinds of marine invertebrate oocytes. Conversely, other data from the literature, as well as previously unpublished findings for jellyfish oocytes, fail to support the view that calcium signals are required for GVBD. In addition to assessing the effects of calcium transients on GVBD in marine invertebrate oocytes, the ability of maturing oocytes to enhance their calcium-releasing capabilities after GVBD is also reviewed. Furthermore, possible explanations are proposed for the contradictory results that have been obtained regarding calcium signals during oocyte maturation in marine invertebrates.

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“…During the ''slow'' block the extracellular ''vitelline'' layer surrounding the oocyte is lifted and converted into a fertilization envelope. In starfish (echinoderm), lifting of the VL has been shown to depend on actin remodeling beginning at the site of sperm entry (Chun and Santella, 2009;Chun et al, 2010;Kyozuka et al, 2008;Puppo et al, 2008).…”

Section: Polyspermy Barriermentioning

confidence: 99%

The eggshell in the C. elegans oocyte‐to‐embryo transition

Johnston

Dennis

2011

Genesis

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Summary: In egg-laying animals, embryonic development takes place within the highly specialized environment provided by the eggshell and its underlying extracellular matrix. Far from being simply a passive physical support, the eggshell is a key player in many early developmental events. Herein, we review current understanding of eggshell structure, biosynthesis, and function in zygotic development of the nematode, C. elegans. Beginning at sperm contact or entry, eggshell layers are produced sequentially. The earlier outer layers are required for secretion or organization of inner layers, and layers differ in composition and function. Developmental events that depend on the eggshell include polyspermy barrier generation, high fidelity meiotic chromosome segregation, osmotic barrier synthesis, polar body extrusion, anterior-posterior polarization, and organization of membrane and cortical proteins. The C. elegans eggshell is proving to be an excellent, tractable system to study the molecular cues of the extracellular matrix that instruct cell polarity and early development. genesis 50:333-349, 2012. V V C 2011 Wiley Periodicals, Inc.

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Actin cytoskeleton modulates calcium signaling during maturation of starfish oocytes

Cited by 48 publications

References 75 publications

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

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

Calcium signals and oocyte maturation in marine invertebrates

The eggshell in the C. elegans oocyte‐to‐embryo transition

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