Cortical granule exocytosis is triggered by different thresholds of calcium during fertilisation in sea urchin eggs

Matese, John C.; McClay, David R.

doi:10.1017/s0967199400005086

Cited by 12 publications

(7 citation statements)

References 57 publications

(108 reference statements)

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“…6A). These data complement the assays of CGE by FE formation and support the hypothesis of differential sensitivity of cortical granule subpopulations to available free Ca 2+ (Blank et al, 1998;Matese and McClay, 1998;Terasaki, 1995). Variability in the threshold Ca 2+ concentration that activates the fusion machinery of cortical granules is one possible explanation for the observed phenomenon.…”

Section: Gβγ Signaling Is Upstream Of Ca 2+ Releasesupporting

confidence: 80%

βγ subunits of heterotrimeric G-proteins contribute to Ca2+ release at fertilization in the sea urchin

Voronina

Wessel

2004

Journal of Cell Science

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A cytoplasmic Ca2+ transient is required for egg activation at fertilization in all animals. The pathway leading to release of Ca2+ from the endoplasmic reticulum in echinoderms includes activation of a SRC homolog, followed by phospholipase Cγ activation, and formation of inositol trisphosphate. However, the upstream activators or modulators of this signaling pathway are not known. We recently identified four Gα subunits of heterotrimeric G-proteins present in the sea urchin egg, and here we find that activation of G-proteins of the Gαs and Gαq type, but not Gαi or Gα12 type, is required for normal Ca2+ dynamics at fertilization. The effects of these G-proteins are mediated by the Gβγ subunits, occur upstream of the cytoplasmic Ca2+ release, and influence both the amplitude of Ca2+ release and the duration of the lag phase. We propose integration of the G-protein input into the framework of signaling at sea urchin fertilization.

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Section: Gβγ Signaling Is Upstream Of Ca 2+ Releasesupporting

confidence: 80%

βγ subunits of heterotrimeric G-proteins contribute to Ca2+ release at fertilization in the sea urchin

Voronina

Wessel

2004

Journal of Cell Science

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“…We were concerned that the pH L ASH may be related to Ca 2ϩ -stimulated exocytosis, which occurs 6 -8 s after the main [Ca 2ϩ ] i rise in urchin eggs (13,33) and which alkalinizes cortical granules upon plasmalemmal fusion (12,14). Our conclusion is that the pH L ASH is not due to exocytosis based on the following evidence: (a) Deeper pH L events are too remote to be due to fusion with the plasma membrane, although it might be argued that these deeper pH L ARES artifactually represents the "tail" of exocytotic events emanating from out of the plane of focus, recording from thin optical slices (2-3% of the egg diameter) at the egg equator means that the curvature of the plasma membrane is minimal, and out-of-focus cortical granules will not overlap this in-focus region.…”

Section: Discussionmentioning

confidence: 99%

Fertilization and Nicotinic Acid Adenine Dinucleotide Phosphate Induce pH Changes in Acidic Ca2+ Stores in Sea Urchin Eggs

Morgan

Galione

2007

Journal of Biological Chemistry

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The second messenger nicotinic acid adenine dinucleotide phosphate (NAADP) releases Ca 2؉ from the acidic Ca 2؉ stores of many organisms, including those of the sea urchin egg. We investigated whether the pH within the lumen of these acidic organelles changes in response to stimuli. Fertilization activates the egg by Ca 2؉ release dependent upon NAADP, and accordingly, we report that fertilization also alters organellar pH in a spatio-temporally complex manner. Upon sperm fusion, vesicles deep in the egg center slowly acidify, whereas cortical vesicles undergo a rapid alkalinization. The cortical vesicle alkalinization is independent of exocytosis and cytosolic pH but coincides with the NAADP-dependent fertilization Ca 2؉ wave. Microinjection of NAADP mimicked the fertilization cortical response, suggesting that it occurred within NAADP-sensitive acidic Ca 2؉ stores. Our data show that NAADP and physiological stimuli alter the pH within intracellular organelles and suggest that NAADP signals through pH as well as Ca 2؉ .The sea urchin egg is an invaluable cell model for studying Ca 2ϩ signaling since the discovery of new second messengers and new Ca 2ϩ stores in this system has subsequently proven to have a major impact on mammalian biology (1). The mechanism of activation of the egg upon fertilization encompasses the rapid increases in the cytosolic pH and intracellular Ca 2ϩ concentration ([Ca 2ϩ ] i ) important for fertilization envelope formation, DNA and protein synthesis, and embryological development (2). The pattern of [Ca 2ϩ ] i changes within the egg are highly organized spatio-temporally and reflect the precisely timed and placed recruitment of different families of Ca 2ϩ channels resident upon either the plasma membrane or intracellular organelles (2, 3). After the initial transient "cortical flash" caused by Ca 2ϩ influx across the plasma membrane (2-5), Ca 2ϩ release from intracellular stores is manifest as a Ca 2ϩ wave that propagates across the entire egg initiating from the point of sperm entry (2). These phasic elevations in [Ca 2ϩ ] i are driven by a complex interplay between the second messengers inositol 1,4,5-trisphosphate, cyclic adenosine diphosphoribose, and nicotinic acid adenine dinucleotide phosphate (NAADP) 2 (1). Importantly, the relative contribution of each messenger to each phase of the Ca 2ϩ signal is different, e.g. NAADP is the only messenger implicated in the cortical flash (4, 5), whereas cyclic adenosine diphosphoribose probably plays a later role in prolonging the main Ca 2ϩ spike (6).NAADP not only evokes a cortical flash but, as first revealed in sea urchin egg, also releases Ca 2ϩ from acidic Ca 2ϩ stores that are lysosome-like organelles (possibly yolk platelets in eggs), whereas inositol 1,4,5-trisphosphate and cyclic adenosine diphosphoribose release Ca 2ϩ from the neutral endoplasmic reticulum (1, 7). Recently in sea urchin egg homogenate, we revealed that the luminal pH (pH L ) of these acidic stores is dynamic and increases upon NAADP-induced Ca 2ϩ release, whic...

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“…In sea urchins, fertilization results in a single wave of [Ca 2+ ] i elevation which spreads across the egg from the point of sperm fusion and, after a lag time following the [Ca 2+ ] i wave of approximately 8-10 seconds (37), CGs undergo exocytosis within seconds (145). This rapid secretion of CGs has been demonstrated by membrane capacitance changes (146) as well as live cell imaging with fluorescent lipophilic probes (37) and differential interference contrast microscopy (37,(147)(148)(149). Interestingly, CG exocytosis does not occur in a synchronous wave corresponding directly to the [Ca 2+ ] i wave, but rather occurs in a stochastic manner with subpopulations of CGs undergoing exocytosis at distinct times following [Ca 2+ ] i elevation (37,147,148).…”

Section: Kinetics Of Cg Exocytosis In Sea Urchin Eggsmentioning

confidence: 99%

Calcium and The Control of Mammalian Cortical Granule Exocytosis

Allison¹

2001

Front Biosci

103

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At fertilization, the release of intracellular calcium is necessary and sufficient for most, if not virtually all, of the major events of egg activation that are responsible for the onset of embryonic development. In mammalian eggs, repetitive calcium oscillations stimulate egg activation events through calcium-dependent effectors, such as calmodulin, protein kinases, and specific proteins involved in exocytosis. One of the earliest calcium-dependent events is the exocytosis of cortical granules (CGs), a secretory event resulting in the block to polyspermy and the prevention of triploidy. Emerging studies suggest that CG release in mature eggs is dependent upon calcium-dependent proteins similar to those in somatic cells employed to undergo calcium-regulated exocytosis. In contrast, pre-ovulatory oocytes are incompetent to undergo CG exocytosis due to deficiencies in the ability to release and respond to increases in intracellular calcium. The development of competence to release and respond to calcium is relevant to both animal and human in vitro fertilization programs that largely utilize ovarian oocytes not all of which are fully activation competent.

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Cortical granule exocytosis is triggered by different thresholds of calcium during fertilisation in sea urchin eggs

Cited by 12 publications

References 57 publications

βγ subunits of heterotrimeric G-proteins contribute to Ca2+ release at fertilization in the sea urchin

βγ subunits of heterotrimeric G-proteins contribute to Ca2+ release at fertilization in the sea urchin

Fertilization and Nicotinic Acid Adenine Dinucleotide Phosphate Induce pH Changes in Acidic Ca2+ Stores in Sea Urchin Eggs

Calcium and The Control of Mammalian Cortical Granule Exocytosis

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