1 Cell Biology Unit, Stazione Zoologica Anton Dohrn, 80121 Napoli; and 2 Department of Animal Science, University of Basilicata, 85100 Potenza, Italy
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ABSTRACT |
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By using the whole cell voltage-clamp
technique, we studied changes in plasma membrane permeability at
different meiotic stages of bovine oocytes. Follicular oocytes were
matured in vitro and activated by Ca2+ ionophore. Oocytes
at germinal vesicle (GV), germinal vesicle breakdown (GVBD), metaphase
I (MI), metaphase II (MII), and meiosis exit were used for
electrophysiological recording. By clamping the oocytes at 30 mV, we
found that the L-type voltage-dependent Ca2+ channels were
active at the GV stage and that their activity decreased after the GVBD
stage. Furthermore, the resting potential decreased from the GV to the
MI stage and increased again at MII. A significant decrease of the
steady-state conductance occurred from the GV to the MI stage, followed
by a sharp increase at the MII stage. With the addition of organic
L-type Ca2+ channel blockers (nifedipine and verapamil), we
inhibited the Ca2+ currents. However, only in the case of
verapamil was there a decrease of in vitro maturation efficiency. Our
results suggest that, in addition to the cumulus-oocyte junctions, the
plasma membrane channels provide another mode of Ca2+ entry
into bovine oocytes during meiosis.
oocyte maturation; L-type calcium channels; meiosis
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INTRODUCTION |
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IN MAMMALS, FOLLICULAR OOCYTES are arrested in the diplotene stage of the first meiotic prophase [germinal vesicle (GV) stage] until the start of follicle maturation release from the follicle environment (16). cAMP is suspected to maintain the meiotic arrest when transmitted from cumulus cells to the oocyte through gap junctions (1, 6, 15, 21). In response to the luteinizing hormone (LH) surge, cumulus cells transmit a Ca2+ signal to the oocyte (17), leading to gap junction regression (50). Simultaneously, cAMP levels decrease, which in turn releases the oocyte from meiotic arrest (46). These consecutive events are preceded by a relatively long lag phase lasting from the GV stage to germinal vesicle breakdown (GVBD), which is characterized by high protein synthesis and transcriptional activity (26). During this lag phase, cumulus-oocyte communication is open and the intracytoplasmatic cAMP levels are high (11). The oocyte then completes meiosis I by extruding the first polar body and begins the second meiotic division. This is characterized by a cell cycle block at metaphase II (MII) that lasts until fertilization. Sperm-oocyte interaction, as well as pharmacological substances, e.g., Ca2+ ionophore or ethanol, may induce meiosis completion and trigger early embryo development (8, 49, 57).
Meiosis and mitosis are regulated by two enzymes, histone 1 (H1) and mitogen-activated protein (MAP) kinase. H1, or maturation-promoting factor (MPF), is composed of cylin B and p34cdc2 subunits, which display a cyclical activity peaking at the metaphase stage (18, 56). MAP kinase is part of a kinase cascade that is likely initiated by c-mos (45). This pathway seems to be apparently involved in meiotic spindle organization, extrusion of the first polar body, and meiotic arrest at the MII stage (7).
It is well known that Ca2+ is involved in oocyte maturation (Ref. 25 for review). In the hamster (19) and mouse (5), a series of spontaneous Ca2+ oscillations occur in the oocyte after isolation from the follicle up to the GVBD stage. After these oscillations have subsided, Ca2+ does not affect further meiotic progression. In bovine and pig, no Ca2+ oscillations occur during meiosis progression; however, Ca2+ is necessary for meiotic progression since 1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid (BAPTA), a Ca2+ chelator, causes a delay or block of meiosis (22). At fertilization, a new series of oscillations related to meiotic completion occurs (36). The Ca2+ ionophore, A-23187, induces meiosis resumption in oocytes blocked either at the GV stage (55) or MII (30, 48, 53) stage. Because extracellular Ca2+ is required for in vitro GVBD (14) and for first meiotic division (41), it appears that Ca2+ ion transport throughout the plasma membrane plays a functional role in maturation.
L-type Ca2+ channels are involved in numerous physiological processes (2, 24). These voltage-gated channels have been found in oocytes of the marine invertebrates (tunicates) (10) as well as in mammalian oocytes (39). In the mouse, Murnane and De Felice (38) showed a selective increase of these channels on the oocyte plasma membrane after puberty, corresponding to meiotic competence occurrence.
In this study, we have analyzed the electrical properties of the plasma membrane in bovine oocytes at different meiotic stages, focusing primarily on the activity of L-type voltage-dependent Ca2+ channels.
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MATERIALS AND METHODS |
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Materials. If not otherwise stated, all chemicals were purchased from Sigma Chemical (St. Louis, MO).
Oocyte source.
Ovaries from slaughtered cows were collected from the abattoir and
transported in a thermal bag at 30-35°C to the laboratory within
3-4 h of collection. The laboratory temperature was 30°C. Immature oocytes were collected from 2- to 8-mm follicles by an 18-gauge needle under controlled pressure (50-70 mmHg).
Cumulus-oocyte complexes (COC) were isolated from the follicular fluid
and washed three times with TCM199 supplemented with 5% FCS and 10 mM
HEPES. The COC were then transferred into maturation medium (TCM199
supplemented with 10% FCS, 10 IU/ml LH, 0.1 IU/ml follicle-stimulating
hormone, and 1 µg/ml 17-estradiol) (40 µl/COC) and left in an
incubator at 39°C in 5% CO2 humidified air. Twenty-four
hours later, the COC were freed from the cumulus cells by vortexing for
3 min and were parthenogenetically activated by 5-min exposure to 5 µM Ca2+ ionophore, A-23187, in Fert-TALP medium
(42) as described by Liu et al. (30). The
oocytes were then transferred in Fert-TALP medium and kept in the
incubator until the electrical recording, scheduled 15-16 h after
the ionophore treatment. At the time of the electrophysiological
studies, batches of oocytes (control groups) were submitted to the same
A-23187 treatment, followed by 3.5 h of incubation in culture
dishes (Nunclon, Nunc, Denmark) that contained Fert-TALP supplemented
with 2.5 mM 6-dimethylaminopurine. Finally, the oocytes were
transferred in Fert-TALP medium covered with embryo-tested oil
(Medicult, Denmark) and cultured in a gas mixture of 5%
CO2, 7% O2, and 88% N2 for 1 day.
Zygotes and embryos were cultured in SOF medium containing
amino acids and BSA (51) in the previous gas mixture for 8 days postactivation for blastocyst development.
Electrophysiology. Electrical recording was performed at 37°C on oocytes at the following stages: GV, promptly isolated from follicles; GVBD, after 8 h of maturation; metaphase I (MI), after 12 h of maturation; and MII, after 24 h of maturation (47). Meiosis exit occurred 15-16 h after Ca2+ ionophore treatment, corresponding to the time span related to the decrease of MPF and MAP kinases (29) and the extrusion of the second polar body. Before micromanipulation, the oocytes at all stages were freed from the cumulus as described above, and the zona pellucida was removed by incubating the oocytes in 0.5% pronase for 1.5-2 min at 37°C.
The zona-free oocytes were subsequently placed in a recording chamber that contained 2 ml of Ham's F-10 (Mascia Brunelli, Italy). Oocytes were voltage clamped by standard techniques (4). Patch pipettes of 10-MMeiosis progression assessment.
Just before the experiment, samples from each stage were fixed with
acetic-ethanol (1:3) and stained with acetic-lacmoid (Aldrich) for
assessing meiotic progression. Confocal analysis was also performed on
batches of oocytes to obtain additional information on the examined
meiotic stages. The oocytes were fixed for 1 h in 2% formaldehyde
in PBS, transferred in 0.01% Triton X-100 in PBS supplemented with
0.01% sodium azide, and kept at 4°C for 48 h. After being
washed three times with PBS, the oocytes were stained to identify DNA
with 0.01% propidium iodide supplemented with 0.01% Triton X-100 and
0.1 mM EDTA. After being washed three times in PBS, the oocytes were
double stained after a 20-min incubation with either FITC-conjugated
wheat germ lectin at the GV and GVBD stages to visualize the nuclear
membrane or with FITC-conjugated anti--tubulin at the MI and MII
stages to visualize the meiotic spindle. Finally, after being washed
twice with PBS, the oocytes were scanned with an Olympus Fluoview
confocal microscope.
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RESULTS |
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A total of 335 oocytes (14 replications) were parthenogenetically activated and produced a cleavage rate of 81.5 ± 6.2% and an expanded blastocyst production of 22.7 ± 4.7%. Examination of the fixed oocytes showed that the majority reached the stages studied, i.e., GV, 92.6% (25/27); GVBD, 85.7% (30/35); MI, 71.4% (20/28); MII, 84.2% (32/38); and meiosis exit, 73.3% (22/30).
The resting potentials of the oocytes at particular meiotic
stages are shown in Fig. 1A.
These potentials did not differ from the GV stage to the GVBD stage,
decreased significantly (P < 0.05) at the MI stage,
increased (P < 0.05) again at the MII stage and, finally, decreased at the meiosis exit stage. By clamping the cells at
30 mV and applying ramps of 10-mV depolarizing and hyperpolarizing steps, a series of whole cell currents were generated. The outward currents suggested a rectifier K+ channel similar to that
described in the human oocyte by De Felice et al. (13). To
obtain steady-state conductance, we plotted the peak current amplitude
against the tip potential. This resulted in a linear relationship (Fig.
1B). The steady-state conductance current-voltage
(I-V) significantly decreased (P < 0.01) from the GV to the GVBD and MI stages; it increased
(P < 0.01) at MII and, finally, decreased again at the
meiosis exit stage (Fig. 1C).
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From the voltage clamp of 30 mV to test potentials, we observed an
inward component of current activating in 30 ms and slowly inactivating
in 250 ms, reaching a plateau in 500 ms. Typical leak-subtracted
currents from
30 mV and I-V curves for the leak-subtracted currents at
30-mV voltage clamp are shown in Fig.
2 for each stage. Their amplitude,
calculated as the difference between the peak and the steady state,
significantly (P < 0.01) decreased from GVBD to the
subsequent stages.
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At 30-mV voltage clamp, the addition of 10 mM external
Ca2+ to the bath increased the inward component at all
stages. The I-V relationship of the peak amplitude at high
Ca2+ concentration is shown in Fig. 2. The inward component
increased at all the examined stages, with a maximum difference at the
GV stage. Moreover, the pattern in the high Ca2+ regime was
shifted toward more positive voltage values (Fig. 2). High
Ca2+ also caused a transient hyperpolarization of the
plasma membrane at both the GV and MII stages. Ca2+
currents were completely inhibited in the GV and GVBD stages by adding
to the bath either nifedipine or verapamil at concentrations >5 µM.
Moreover, maturing GV oocytes in the presence of either 100 µM
verapamil or 100 µM nifedipine caused decreased (P < 0.01) cleavage efficiency (45 or 62% vs. 89%) and blastocyst
development (10 or 31% vs. 32%) in the case of verapamil.
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DISCUSSION |
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In this study, we have shown that the plasma membrane of bovine oocytes undergoes profound electrical modification throughout meiosis. In particular, differences among meiotic stages were found in the resting potential as well as in steady-state conductance and voltage-gated Ca2+ channel activity. Little is known about the relationship between the resting potential of plasma membrane and the cell cycle. A change in plasma membrane polarization and ion permeability has already been described during maturation in invertebrate (37), amphibian (54), and mammalian (38, 43, 44) oocytes. We measured a stable negative resting potential and changes related to oocyte activation (12). It is likely that in the bovine oocyte, a low resting potential in both the GV and MII stages is associated with a "standby" status. In the case of GV, we suggest that the plasma membrane waits for a signal to resume meiosis, in which there is a large exchange of Ca2+ ions. As soon as cell cycle progression is resumed, the plasma membrane depolarizes. In such a case, however, it is difficult to explain the resting potential of GVBD, which represents the first stage of meiosis resumption. This may reflect meiosis vs. mitosis, bearing in mind that GV to GVBD is a period in which the metabolic oocyte activity is high (20, 26), cumulus-oocyte communication is intact (50), and cytoplasmic cAMP is elevated (11, 58).
The plasma membrane permeability, measured as steady-state conductance, is high at the GV stage and decreases during meiosis with little restoration at the MII stage. A similarity between these values at the GV and MII stages was reported in the mouse (38). Hence, the highest permeability corresponds to the two meiotic arrest phases. It is feasible that the high-ion exchange is related to the large metabolic activity of the GV stage or to the preparation of the plasma membrane for fertilization at the MII stage.
The I-V relationship of the leak-subtracted peak currents at different holding voltages, as well as the results obtained at high Ca2+ regime and the sensitivity at pharmacological agents, strongly suggest that these currents represent L-type Ca2+ channels. This is in agreement with previous findings in mouse (38) and invertebrate (10) oocytes. L-type Ca2+ channels have been demonstrated to underlay meiosis resumption in mussel (52), Pleurodeles (40), and in mammalian (39) oocytes. In bovine oocytes, the predominance of these channels at the GV and GVBD stages suggests a role for Ca2+ during the first meiotic resumption. Indeed, during maturation, the activity of plasma membrane Ca2+ channels decreases. This pattern may support the cytosolic Ca2+ rise at GV in addition to the LH and/or the growth factor-mediated Ca2+ surge via cumulus-oocyte communication (23, 31). In contrast, the low plasma membrane Ca2+ channel activity at the MII stage argues for a minor role of external Ca2+, whereas intracellular Ca2+ mobilization mechanisms appear to be more important for oocyte activation and fertilization.
The mechanism of how Ca2+ affects meiosis progression is unclear. However, we know that 1) BAPTA delays kinase activity and inhibits maturation (22); 2) Ca2+ may influence protein synthesis that is essential in maturational processes (28); and 3) Ca2+ modulates gap junction functionality, allowing cumulus-mediated intracytoplasmatic cAMP levels (58). In bovine oocytes, it has been shown that Ca2+ participates in the progression of meiosis, although spontaneous Ca2+ oscillations do not occur as in hamster and mouse oocytes (19, 22). D-Myo-inositol 1,4,5-trisphosphate (IP3)-induced Ca2+ release has been suggested as a primary mechanism for maturation of bovine oocytes because the cytoplasmic IP3 receptors increase in number during the meiotic progression (22). A minor role has been attributed to Ca2+ release through ryanodine receptors, which are poorly expressed in bovine oocytes (22).
Differential mechanisms of Ca2+ release in bovine oocytes could explain the effect of Ca2+ channel inhibitors during in vitro maturation. Since verapamil inhibits L-type Ca2+ channels, whereas nifedipine inhibits only the dihydropyridine (DHP)-sensitive L-type Ca2+ channels (33), we suppose that either 1) non-DHP-sensitive L-type Ca2+ channels play a role in maturation or 2) lower inward flux of Ca2+ caused by verapamil negatively affects maturation. On the basis of these findings, it seems likely that cumulus cells mediate intracytoplasmatic Ca2+ influx and, notwithstanding Ca2+ channel block, support the outcome of maturation in at least some oocytes.
In summary, these results suggest that in bovine oocytes, at the start of meiosis, in addition to the LH-mediated Ca2+ surge, Ca2+ entry arises through Ca2+ channels on the oocyte plasma membrane other than via gap junction cumulus-oocyte communication. Because the oocyte plasma membrane does not contain LH receptors, the initial Ca2+ influx comes from cumulus cells. This may cause a change in membrane potential and gating of voltage-dependent Ca2+ channels. The intracytoplasmatic Ca2+ rise may undergo a self-amplifying mechanism (Ca2+-induced Ca2+ release, IP3-induced Ca2+ release, or Ca2+-induced IP3 release) (3). If such a mechanism exists, it could potentiate the cumulus-oocyte communication necessary for metabolic exchange and the high cAMP levels during early maturation. High Ca2+ would then close the gap junctions (27), causing a drop in cAMP.
We have also shown that the MII stage is characterized by an increase of steady-state conductance due to K+ channels that is not accompanied by Ca2+ channel activity. In mammals, sperm-mediated oocyte activation is accompanied by a hyperpolarization of the plasma membrane due to Ca2+-activated K+ channels (9, 34, 35). Because we parthenogenetically activate oocytes by using Ca2+ ionophore, thus simulating the sperm-mediated Ca2+ surge, our data support the idea that in bovine oocytes external Ca2+ is not involved in meiosis exit. Indeed, the intracytoplasmatic Ca2+ surge may activate K+ channels. The decrease of Ca2+ channels during maturation may be correlated with the maturation of Ca2+ release mechanisms occurring at MII (32). These findings suggest that whereas external Ca2+ influences sperm-mediated Ca2+ elevation at fertilization, it mainly depends on intracellular Ca2+ stores.
In conclusion, during meiosis the plasma membrane of bovine oocytes undergoes a progressive depolarization and Ca2+ channel depletion. These findings provide new information and insight into the mechanisms and dynamics of meiosis.
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ACKNOWLEDGEMENTS |
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We thank Prof. L. J. De Felice and Dr. E. Brown for helpful comments and critical revision of the manuscript. We also thank G. Gargiulo for computer acquisition and photography.
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FOOTNOTES |
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Address for reprint requests and other correspondence: E. Tosti, Stazione Zoologica, Villa Comunale, 80121 Napoli, Italy (E-mail tosti{at}alpha.szn.it).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 26 May 2000; accepted in final form 18 July 2000.
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