NAADP and InsP3 play distinct roles at fertilization in starfish oocytes

Moccia, Francesco; Nusco, Gilda A.; Lim, Dmitry; Kyozuka, Keiichiro; Santella, Luigia

doi:10.1016/j.ydbio.2006.02.011

Cited by 44 publications

(39 citation statements)

References 56 publications

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“…On the other hand, it is conceivable that the initial rise of the Ca 2+ wave might have elicited cortical flash in a similar way whereby a Ca 2+ wave driven by ionomycin or uncaged second messengers (e.g. InsP 3 , cADPr, and NAADP) gives rise to ion influx and cortical flash in starfish eggs [16,24,51,132]. Whereas the cADPrelicited ion current in starfish oocytes was mainly through Na + channels, the train of action potentials that coincide with the cortical flash following LAT-A treatment required both Na + and Ca 2+ in the extracellular space [71].…”

Section: Discussionmentioning

confidence: 99%

Disassembly of Subplasmalemmal Actin Filaments Induces Cytosolic Ca2+ Increases in Astropecten aranciacus Eggs

Vasilev

Limatola

Park

et al. 2018

Cell Physiol Biochem

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Background/Aims: Eggs of all animal species display intense cytoplasmic Ca²⁺ increases at fertilization. Previously, we reported that unfertilized eggs of Astropecten aranciacus exposed to an actin drug latrunculin A (LAT-A) exhibit similar Ca²⁺ waves and cortical flashes after 5-10 min time lag. Here, we have explored the molecular mechanisms underlying this unique phenomenon. Methods: Starfish eggs were pretreated with various agents such as other actin drugs or inhibitors of phospholipase C (PLC), and the changes of the intracellular Ca²⁺ levels were monitored by use of Calcium Green in the presence or absence of LAT-A. The concomitant changes of the actin cytoskeleton were visualized with fluorescent F-actin probes in confocal microscopy. Results: We have shown that the LAT-A-induced Ca²⁺ increases are related to the disassembly of actin flaments: i) not only LAT-A but also other agents depolymerizing F-actin (i.e. cytochalasin B and mycalolide B) induced similar Ca²⁺ increases, albeit with slightly lower efficiency; ii) drugs stabilizing F-actin (i.e. phalloidin and jasplakinolide) either blocked or significantly delayed the LAT-A-induced Ca²⁺ increases. Further studies utilizing pharmacological inhibitors of PLC (U-73122 and neomycin), dominant negative mutant of PLC-ɣ, specific sequestration of PIP2 (RFP-PH), InsP₃ uncaging, and quantitation of endogenous InsP₃ all indicated that LAT-A induces Ca²⁺ increases by stimulating PLC rather than sensitizing InsP₃ receptors. In support of the idea, it bears emphasis that LAT-A timely increased intracellular contents of InsP₃ with concomitant decrease of PIP2 levels in the plasma membrane. Conclusion: Taken together, our results suggest that suboolemmal actin filaments may serve as a scaffold for cell signaling and modulate the activity of the key enzyme involved in intracellular Ca²⁺ signaling.

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Section: Discussionmentioning

confidence: 99%

Disassembly of Subplasmalemmal Actin Filaments Induces Cytosolic Ca2+ Increases in Astropecten aranciacus Eggs

Vasilev

Limatola

Park

et al. 2018

Cell Physiol Biochem

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“…For example, in starfish, desensitization of NAADP receptors can prevent or disrupt the IP 3 -mediated Ca 2ϩ wave. The IP 3 wave, in turn, can contribute to NAADP-induced membrane depolarization by activating Ca 2ϩ -dependent Na ϩ channels (Moccia et al, 2006). This finding suggests that there is cooperation between external and internal Ca 2ϩ signals to induce or enhance various activation events.…”

Section: Triggers Of Egg Activation Spermmentioning

confidence: 95%

Transitioning from egg to embryo: Triggers and mechanisms of egg activation

Horner

Wolfner

2008

Developmental Dynamics

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177

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The transition from mature oocyte to developing embryo requires a coordinated series of events, collectively known as egg activation. Egg activation includes changes to egg coverings to prevent polyspermy, release of oocyte meiotic arrest, generation of haploid female and male pronuclei, changes in maternal mRNAs and protein populations, and cytoskeletal rearrangements. In many animals, egg activation is triggered by fertilization, which increases intracellular calcium within the oocyte and thereby regulates molecular events of egg activation. In other animals, fertilization-independent external signals, including mechanical stimulation of eggs and/or changes in ionic milieu, trigger activation. Recent studies have clarified the upstream portion of pathways leading to eggshell changes and cell cycle resumption and have identified activation-induced changes in maternal mRNA and protein profiles that can identify molecular players in the downstream events of egg activation. We review signals that trigger activation and how they link to subsequent molecular events of egg activation. Developmental Dynamics 237:527-544, 2008.

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“…The tentative conclusion is that the NAADP-dependent Ca 2+ entry may contribute to the stimulation of InsP 3 -producing PLCγ in starfish oocytes (Runft et al, 2004), which requires micromolar concentration of priming Ca 2+ (Rhee, 2001). Alternatively, the NAADP-induced Ca 2+ may help sensitize the InsP 3 Rs through a process of CICR (Moccia et al, 2006). At any rate, these results suggest that Ca 2+ signaling during starfish fertilization is initiated by NAADP, although it has been assumed to be exclusively under the control of the InsP 3 .…”

Section: Ca 2+ -Linked Second Messengers Other Than Insp 3 May Play Amentioning

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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NAADP and InsP3 play distinct roles at fertilization in starfish oocytes

Cited by 44 publications

References 56 publications

Disassembly of Subplasmalemmal Actin Filaments Induces Cytosolic Ca2+ Increases in Astropecten aranciacus Eggs

Disassembly of Subplasmalemmal Actin Filaments Induces Cytosolic Ca2+ Increases in Astropecten aranciacus Eggs

Transitioning from egg to embryo: Triggers and mechanisms of egg activation

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

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