1 Bio Mar Cell, Unité de Biologie du Développement UMR 7009
CNRS/Paris VI, Observatoire, Station Zoologique, Villefranche sur Mer, 06230
France
2 Department of Physiology, University College London, Gower Street, London,
WC1E 6BT, UK
3 Unité de Chronobiologie Théorique, Faculté des Sciences,
Université Libre de Bruxelles, Brussels, Belgium
* Author for correspondence (e-mail: r.dumollard{at}ucl.ac.uk)
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Summary |
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Key words: Fertilization, Egg, Calcium oscillations, Calcium wave pacemaker, Ins(1,4,5)P3, Endoplasmic reticulum, Cortex
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Introduction |
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In eggs, Ca2+ waves triggered by sperm entry result mainly from
the release of Ca2+ from intracellular stores by inositol 1,4,5
trisphosphate [Ins(1,4,5)P3]-induced Ca2+
release (IICR) (reviewed in Miyazaki et
al., 1993; Stricker,
1999
; McDougall et al.,
2000
). The mechanism underlying Ins(1,4,5)P3
production in eggs at the time of fertilization is still intensely debated.
Similarly, the nature of the sperm factor(s) inducing Ca2+ release
at fertilization remains elusive, although several competing groups agree that
it must be a protein, possibly a form of phospholipase C or an activator of it
(see Stricker, 1999
;
Swann and Parrington, 1999
;
Parrington et al., 2000
;
McDougall et al., 2000
;
Nixon et al., 2000
;
Runft and Jaffe, 2000
;
Mehlmann et al., 2001
;
Jaffe et al., 2001
;
Carroll, 2001
;
Runft et al., 2002
). Very
recently, a mammalian sperm factor was characterized and found to be a new
form of PLC [PLC
(Saunders et al.,
2002
)]. In most species, it seems reasonable to assume that the
entering sperm delivers a factor into the egg and that this factor generates
Ins(1,4,5)P3 either directly or indirectly.
The first wave, which we will refer to as the `fertilization
Ca2+ wave', is generally the largest and longest-lasting wave, and,
in some species, it is followed by repetitive Ca2+ waves of lower
amplitude and shorter duration. Ca2+ wave pacemakers elicit waves
for minutes (20-30 minutes in ascidians, 45-60 minutes in some molluscs, 90
minutes in nemerteans) or hours (4 hours in mammals), and they stop operating
at the end of the meiotic cell cycles (except in mammals, in which they stop
several hours after completion of meiosis, at the time of pronuclei
formation). The pacemaker site can be fixed in the cortex or undergo dramatic
movements as the cortex is reorganized in preparation for development
(Sardet et al., 2002).
Ca2+ wave pacemakers are either located in a region of enhanced
sensitivity to Ins(1,4,5)P3 or reside in the vicinity of a
local source of Ins(1,4,5)P3. Here, we briefly examine how
the subcellular organization of the Ca2+ release machinery may
create stable Ca2+ wave pacemakers in the egg. We also discuss how
spatially and temporally regulated production of
Ins(1,4,5)P3 can give rise to multiple calcium wave
pacemakers in a single egg cell.
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Different calcium wave pacemakers in different species |
---|
|
|
We do not completely understand why some eggs display repetitive
Ca2+ waves whereas others exhibit only a single wave. Recent work
on ascidian and mouse eggs reveals that arresting the egg in meiotic metaphase
is both sufficient and necessary to sustain sperm-triggered Ca2+
oscillations (for details, see Jones,
1998; Nixon et al.,
2000
; Carroll,
2001
). Meiotic `M-phase' thus favors repetitive Ca2+
waves (as in nemerteans, some molluscs, annelids, ascidians and mammals). By
contrast, only a single large fertilization Ca2+ wave is observed
when fertilization causes a rapid transition to an interphasic cytoplasm
(<20 minutes, as in fish or amphibians) and when fertilization takes place
during interphase (as in cnidarians or sea urchins). It remains to be seen
whether eggs of fish or amphibians can be made to undergo Ca2+
oscillations when blocked in meiotic M-phase after fertilization. The data
relating an M-phase stage of the cell cycle to the ability to generate
multiple Ca2+ transients is compelling in ascidian and mouse eggs
(reviewed in Nixon et al.,
2000
; Carroll,
2001
). In these eggs, regulation of the Ca2+ release
machinery by cell cycle factors probably participates in determining the
temporal pattern of the fertilization Ca2+ signals. However,
whether such regulation proves to be universal requires further research.
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The calcium signalling hardware in eggs |
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The egg cortex and cytoplasm are filled with an extensive and continuous ER
network (Speksnijder et al.,
1993; Jaffe and Terasaki,
1993
; Terasaki et al.,
1996
; Terasaki et al.,
2001
; Stricker et al.,
1998
; Kline et al.,
1999
). The ER network contains the intracellular Ca2+
channels the Ins(1,4,5)P3 receptors (IP3Rs) and
ryanodine receptors (RyRs) as well as the sarco-endoplasmic reticulum
Ca2+-ATPases (SERCAs) that pump calcium back into the ER.
Among the three known isoforms of IP3R found in somatic cells
(Taylor et al., 1999), IP3R1
is the most prevalent and functionally important isoform in the egg
[Xenopus (Runft et al.,
1999
; Brind et al.,
2000
); ascidian (Kyozuka et
al., 1998
)]. Low levels of IP3R2 and IP3R3 have been reported in
mouse eggs (Fissore et al.,
1999
), but their physiological roles remain unclear
(Brind et al., 2000
;
Jellerette et al., 2000
). The
other family of Ca2+ release channels (RyRs) is present on the
cortical ER of sea urchin eggs (McPherson
et al., 1992
) and in ascidian
(Albrieux et al., 2000
) and
mouse eggs (Ayabe et al.,
1995
). However, except for sea urchins, the involvement of RyRs in
the initiation and propagation of sperm-triggered calcium waves appears to be
minor, and their role remains unclear (reviewed in
McDougall et al., 2000
).
Eggs from all animal phyla seem principally to use Ca2+ release
from internal stores to generate single or repetitive Ca2+ waves at
fertilization. In some species, external Ca2+ is also used for the
fertilization wave [in molluscs (Deguchi
et al., 1996) (reviewed in
Sardet et al., 1998
)] or
contributes to the maintenance of the repetitive Ca2+ waves [in
mice (McGuiness et al., 1996) (reviewed in
Stricker, 1999
)]. In many
species, voltage-operated Ca2+ channels [VOCC
(Arnoult and Villaz, 1994
;
Leclerc et al., 2000
)] and
Ca2+-release-activated Ca2+ (CRAC) channels that mediate
so-called `capacitative Ca2+ entry'
(Arnoult et al., 1996
;
Jaconi et al., 1997
;
Csutora et al., 1999
; Machaca
et al., 2000; Putney et al.,
2001
) are also present, but their role at fertilization is still
ill defined.
In the mature mouse egg, the physiological Ca2+ load is
primarily cleared via SERCAs and plasma membrane Ca2+ ATPases
(PMCAs). A minor contribution may also be provided by the plasma membrane
Na+/Ca2+ exchanger
(Carroll, 2000). PMCAs are
probably responsible for Ca2+ efflux from ascidian eggs after each
Ca2+ wave (Kuthreiber et al.,
1993
) as well as for the loss of total Ca2+ content
after fertilization in sea urchin eggs
(Gillot et al., 1991
).
In the past few years, mitochondria have been shown to be major regulators
of Ca2+ signals (reviewed in
Rutter and Rizzuto, 2000;
Rizzuto et al., 2000
;
Duchen, 2000
). Sequestration
of Ca2+ by mitochondria has two regulatory effects on IICR,
suppressing positive and negative Ca2+ feedback on the opening of
the IP3R. In addition, ATP production by mitochondria might provide a further
means of modulating Ca2+ signals: ATP4- sensitizes the
IP3R (Mak et al., 1999
;
Mak et al., 2001
), whereas
Mg2+-complexed ATP is consumed to refill the ER Ca2+
stores. Mitochondria can thus provide negative or positive feedback on
Ins(1,4,5)P3-mediated Ca2+ signals. Such
negative feedback has been reported in a wide range of somatic cells. For
example, initiation of global Ca2+ waves in myocytes preferentially
occurs in mitochondrion-poor regions of the cell
(Boitier et al., 1999
). A
positive feedback effect of mitochondria on
Ins(1,4,5)P3-mediated signals has been reported only in
oligodendrocytes, in which Ca2+ wave initiation and amplification
sites are found in mitochondrion-rich regions of the cell
(Simpson et al., 1997
).
Except in sea urchins, in which mitochondria are a sink for cytosolic
Ca2+ (Eisen and Reynolds,
1985; Girard et al.,
1991
), the role mitochondria play in Ca2+ signalling in
eggs remains largely obscure. In mouse eggs, collapsing mitochondrial
potential impairs Ca2+ clearance from the cytosol
(Liu et al., 2001
), but no
picture of the regulation of Ca2+ oscillations by mitochondria can
be drawn from only this study. In ascidian eggs, mitochondria contribute to
the activity of the second Ca2+ wave pacemaker both by buffering
cytosolic Ca2+ and by locally providing ATP (R.D., unpublished).
Nevertheless, an understanding of the role of mitochondria in regulating
Ca2+ wave pacemakers will require measurement of the local
intracellular Ca2+ concentration and the local mitochondrial ATP
production in the vicinity of the IP3Rs. The recent development and
subcellular targeting of GFP-based Ca2+ and
Ins(1,4,5)P3 indicators as well as luciferase-based ATP
indicators should allow the direct measurement of mitochondrial
Ca2+ levels, intracellular ATP concentration and the
Ins(1,4,5)P3 concentration in the living zygote
(Hirose et al., 1999
;
Rutter and Rizzuto, 2000
).
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Ca2+ wave pacemakers in eggs reside in cortical ER-rich domains |
---|
In Xenopus and mouse eggs, at least, these ER-rich domains are
rich in IP3R1s (Terasaki et al.,
2001; Mehlmann et al.,
1996
; Fissore et al.,
1999
). The appearance of cortical ER-rich domains during
maturation correlates with an increase in sensitivity to
Ins(1,4,5)P3 and to sperm-induced Ca2+ release
(Chiba et al., 1990
;
Shiraishi et al., 1995
;
Mehlmann and Kline, 1994
;
Terasaki et al., 2001
)
(reviewed in Sardet et al.,
2002
). Local injections of Ins(1,4,5)P3 and
sperm extracts in mouse eggs have revealed that the egg cortex is a region of
higher sensitivity to Ins(1,4,5)P3 and to sperm extracts
(Oda et al., 1999
). Indeed,
although the abundance of ER in the egg cortex renders this region more
sensitive to Ins(1,4,5)P3, it is also exposed to the
highest concentrations of Ins(1,4,5)P3 as it is closest to
the source of PtdIns(4,5)P2 in the plasma membrane
(Halet et al., 2002
;
Sardet et al., 2002
).
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The organization of the ER network may regulate the Ca2+ wave pacemakers |
---|
The mouse MII pacemaker appears to be an example of this type of pacemaker.
In the mature mouse egg, ER-rich domains are larger in the vegetal cortex
(Kline et al., 1999), whereas
mitochondria are more abundant in the animal hemisphere
(Calarco, 1995
;
Van Blerkom et al., 2002
). The
MII pacemaker of the mouse egg resides in the ER-enriched vegetal cortex,
which is probably a site of enhanced sensitivity to
Ins(1,4,5)P3. Therefore, similarly to the somatic cell
Ca2+ wave pacemakers, the mouse MII pacemaker site appears to be
determined by the organization of the Ca2+ stores of the egg, with
Ins(1,4,5)P3 acting as global messenger
(Fig. 1, Fig. 2A).
Interestingly, an artificial pacemaker can be induced in the ascidian egg
by global uncaging of caged Ins(1,4,5)P3
(cIns(1,4,5)P3) or its poorly metabolised analogue
cgPtdIns(4,5)P2 [caged
1-(a-Glycerophosphoryl)-D-myo-inositol 4,5-bisphosphate, P4(5)]. This
artificial pacemaker, localized in the animal pole of the ascidian egg,
functions under globally elevated Ins(1,4,5)P3 levels and
thus resides in the region of highest sensitivity to
Ins(1,4,5)P3
(Dumollard and Sardet, 2001)
(Figs 1 and
2). In common with the mouse
MII pacemaker, the location of this artificial pacemaker can be explained by
asymmetries in the distribution of the ER along the animal-vegetal axis of the
ascidian egg. In these eggs, the ER-rich domains invade the whole egg except
for the vegetal subcortex, where most mitochondria accumulate
(Fig. 2)
(Dumollard and Sardet, 2001
).
The corollary of this is that the sperm-triggered MII pacemaker in the
ascidian egg, located in the vegetal pole (the site opposite the artificial
pacemaker), is not at a site of enhanced Ins(1,4,5)P3
sensitivity. This indicates that the general organization of the ER stores in
these eggs is not sufficient to determine the pacemaker site. The pacemakers
in the ascidian egg may then rely on mechanisms other than a global increase
in Ins(1,4,5)P3 levels.
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Local and dynamic production of Ins(1,4,5)P3 defines the Ca2+ wave pacemaker site |
---|
Hypothesizing local production of Ins(1,4,5)P3 even in
the large egg cell raises the question of how such a gradient is maintained.
Indeed, as Ins(1,4,5)P3 diffuses rapidly through the
cytosol, locally produced Ins(1,4,5)P3 would quickly
invade the whole cell, making Ins(1,4,5)P3 gradients
energy consuming to maintain without dynamic Ins(1,4,5)P3
production. Theoretically, repetitive Ca2+ waves can result from
either a sustained increase in Ins(1,4,5)P3 levels or an
oscillating production of Ins(1,4,5)P3
(Jacob, 1990). In ascidians, a
single, large and sustained Ins(1,4,5)P3 increase
(achieved by uncaging cgPtdIns(4,5)P2 in the whole egg,
Fig. 1) mimics the first series
of Ca2+ oscillations, indicating that the ascidian MI pacemaker is
driven by a continuous moving source of Ins(1,4,5)P3
induced by sperm entry (Dumollard and
Sardet, 2001
). Similarly in mouse eggs, a slow and continuous
uncaging of cIns(1,4,5)P3 can reproduce the
sperm-triggered Ca2+ oscillations
(Jones and Nixon, 2000
).
Therefore, the mouse MII Ca2+ wave pacemaker can also be regulated
by a single and sustained increase in Ins(1,4,5)P3 levels
(Fig. 1). Furthermore, the
Ca2+ transients triggered by the ascidian MI and artificial
pacemakers, as well as those triggered by the mouse MII pacemaker, are all
preceded by a characteristic slow rise in Ca2+ levels called a
`pacemaker Ca2+ rise' (Fig.
1) (Jones and Nixon,
2000
; Dumollard and Sardet,
2001
). This `pacemaker Ca2+ rise' is a hallmark of
low-frequency (period >20 seconds) Ca2+ oscillations generated
under constantly elevated Ins(1,4,5)P3 levels
(Jacob, 1990
;
Marchant and Parker, 2001
),
which further suggests that a single and sustained
Ins(1,4,5)P3 increase regulates the ascidian MI pacemaker
and the mouse MII pacemaker.
By contrast, the ascidian MII pacemaker cannot be reproduced by a
long-lasting increase in Ins(1,4,5)P3 levels in the egg,
and no `pacemaker Ca2+ rise' precedes these Ca2+
transients (Fig. 1) (Dumollard and Sardet, 2001).
An oscillating production of Ins(1,4,5)P3 from the
contraction pole might underlie the activity of the ascidian Ca2+
wave MII pacemaker (Fig. 1).
The recent finding that the mammalian sperm factor is possibly a
Ca2+-activated phospholipase C (PLC)
(Rice et al., 2000
;
Saunders et al., 2002
) argues
in favor of Ins(1,4,5)P3 oscillations driving
sperm-triggered Ca2+ oscillations in eggs. Indeed, the prolonged
stimulation of a Ca2+-activated PLC can result in Ca2+
oscillations regulated by an oscillating production of
Ins(1,4,5)P3 (for details, see
Meyer and Stryer, 1988
). In
addition, Ins(1,4,5)P3 oscillations regulating repetitive
Ca2+ waves during prolonged exposure to agonists have now been
observed in several types of somatic cells
(Hirose et al., 1999
;
Nash et al., 2001
). The issue
of Ins(1,4,5)P3 oscillations is an intensively debated
topic in cell physiology, and the Ca2+ wave pacemakers in eggs
could provide an invaluable experimental system to resolve such questions in
the future.
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A role for vegetal Ca2+ wave pacemakers in development |
---|
The polarized nature of the calcium signals may in itself influence
embryonic patterning by regulating early embryonic cleavages. In ascidians,
nemerteans and mouse, the egg cortex is polarized along the animal-vegetal
axis and, in ascidians, this polarity amplifies after fertilization through
actomyosin-driven cortical contractions
(Sardet et al., 2002). Is the
generation of repetitive Ca2+ waves from the vegetal cortical
pacemaker a mechanism used to prime the vegetal pole region for later
developmental events such as cleavage or gastrulation, which, in nemerteans
and ascidians, takes place in the vegetal/dorsal pole of the embryo? Mouse
embryos were long thought to have no significant polarity until the late
cleavage stage, but recent marking experiments show that in fact, as in
ascidians and nemerteans, although regulation can override this polarity,
there is a relationship between the animal-vegetal axis, the sperm entry point
and the developmental axes of pre- and post-implantation embryos (reviewed in
Lu et al., 2001
).
Finding out whether Ca2+ wave patterns play a role in later
development will require studies that interfere with the normal
spatio-temporal pattern of Ca2+ waves without perturbing mitosis
and cleavage. The rather simple ascidian embryo, which displays two different
meiotic Ca2+ wave pacemakers and develops into a swimming tadpole
within a day, is particularly suited to studies of the relationship between
meiotic Ca2+ waves and development
(Fig. 2)
(Dumollard and Sardet, 2001).
It should be possible in the future to relate patterns of Ca2+
waves and phenotypic differences in embryos.
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Acknowledgments |
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