1 Département dObstétrique-Gynécologie, Université de Montréal, Centre de Recherche du CHUM, Hôpital Saint-Luc, 264 René-Lévesque Est, Montréal, Québec, Canada H2X 1P1
2 Département des Sciences Biologiques, Université de Montréal, C.P. 6128, Succ. Centre-Ville, Montréal, Québec, Canada H3C 3J7
3 Urology Research Laboratory, Royal Victoria Hospital, McGill University, 687, Pine Avenue W., Montréal, Québec, Canada H3A 1A1
*Author for correspondence (e-mail: dubefran{at}medclin.umontreal.ca)
Accepted October 5, 2001
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SUMMARY |
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Key words: cAMP, Meiotic maturation, Surf clam, Fertilization, Prophase arrest
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Introduction |
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The current view is that cAMP-dependent phosphorylation by protein kinase A (PKA) regulates the activity of one or more proteins, which are still to be identified, one of which may be MPF (Meijer and Arion, 1991; Rime et al., 1992
; Matten et al., 1994
), that would maintain prophase I arrest as long as they are in their phosphorylated form. A decrease in cAMP levels would result in their dephosphorylation, and hence, in the release from prophase I block. This view is supported by the observations that injecting prophase I oocytes with the catalytic subunit of protein kinase A prevents or retards GVBD, whereas injecting the regulatory subunit, on the contrary, is sufficient to trigger GVBD and further meiotic maturation [(Maller and Krebs, 1977
; Huchon et al., 1981
) for Xenopus laevis] [(Bornslaeger et al., 1986
) for mouse]. Moreover, maintaining high oocyte cAMP levels by incubation in the presence of either forskolin (6 ß-[ß'-(piperidino)propionyl]-, hydrochloride), an adenylyl cyclase activator, or IBMX (3-isobutyl-1-methylxanthine), a phosphodiesterase inhibitor, prevents spontaneous or progesterone-induced meiotic maturation in mammalian and amphibian oocytes, respectively [(Schultz et al., 1983
; Urner et al., 1983
; Sato and Koide, 1984
) for mouse] [(Schorderet-Slatkine and Baulieu, 1982
) for Xenopus laevis].
One notable exception to this general rule is the invertebrate ophiuroid echinoderm, Amphipholis kochii, in which the isolated prophase I oocytes may be stimulated to undergo meiosis reinitiation upon the addition of forskolin (Yamashita, 1988). The interpretation of this unusual observation is, however, limited as the natural, presumably hormonal, trigger for meiosis reinitiation in this species is not known. In addition, whether or not the forskolin treatment mimicks the normal physiological process remains to be established. Interestingly, it has recently been shown, in two species of nemertean worms, that their oocytes could be induced to undergo meiotic maturation from prophase I with various agents raising their intracellular cAMP (Stricker and Smythe, 2001
). Also, serotonin-stimulated meiosis reinitiation could be triggered in the absence of external Ca2+ (and in the absence of MAP kinase activation) and was accompanied by a required increase of cAMP (Stricker and Smythe, 2001
). This serotonin-stimulated meiotic reinitiation, however, uses a signalling pathway that differs from the physiological process (i.e. spontaneous maturation upon release in Ca2+-containing seawater) which requires Ca2+ fluxes and MAP kinase activation (Stricker and Smythe, 2001
). Nevertheless, these observations highlight the fact that increased cAMP may stimulate, rather than inhibit, meiotic maturation, at least in some species, whether or not this is the normal physiological process.
However, in another echinoderm (starfish), it has been shown that 1-methyl-adenine-induced meiotic maturation of oocytes is accompanied by a decrease in cAMP which, if altered, does not prevent but at least retards meiotic progression (Mazzei et al., 1981; Meijer and Zarutskie, 1987
). Thus, there appears to be an almost universal decrease in oocyte cAMP, which is sufficient to trigger the release of oocytes from prophase I arrest or at least positively affects it. However, echinoderms and vertebrates belong to deuterostome animals and, as such, have a quite different developmental regulation than the more primitive protostome animals such as annelids and molluscs. For example, oocytes from deuterostome animals rely on intracellular Ca2+ stores for their initial activation, whereas oocytes from protostome animals require external sources of Ca2+ for their activation (Jaffe, 1983
; Colas and Dubé, 1998
). Little is known, however, about the possible involvement of cAMP in the regulation of meiotic maturation, especially in those protostome species that are normally fertilized at the prophase I stage.
The arrested oocytes of surf clam, a bivalve mollusc, are released at the prophase I stage, and fertilization normally reinitiates the full meiotic maturation process, up to formation of pronuclei without a secondary arrest in metaphase I. Artificial activation may be induced through the use of compounds, such as ionophore or high K+ seawater (Allen, 1953; Schuetz, 1975
), and by the neurohormone serotonin (Hirai et al., 1988
), which raises intracellular Ca2+ concentration, presumably through binding to endogenous specific receptors. It has been briefly mentioned, without providing detailed experimental results, that cAMP-raising treatments, such as incubating oocytes in the presence of forskolin or IBMX, prevent induction of GVBD by sperm or 5-HT (serotonin, 5-hydroxytryptamine), but not by KCl (Sato et al., 1985
). However, previous attempts to actually measure cAMP levels during the course of meiotic maturation in surf clam oocytes were inconclusive (Adeyemo et al., 1987
). These observations nevertheless led to the suggestion that oocytes from protostome animals were also relying on decreased intracellular cAMP to achieve meiotic maturation.
The aim of the present work was to re-examine the involvement of cAMP in triggering meiotic maturation in surf clam oocytes. It also aimed at better characterizing the signaling pathway utilized by putative serotonin receptors that radioligand-binding studies had characterized as pharmacologically atypical and different from all known mammalian serotonin receptors (Krantic et al., 1993). We report that, contrary to previous reports, treatments of oocytes with forskolin, IBMX, or both, have no inhibitory effect on meiotic maturation induced by high K+ or serotonin. We further show that, contrary to expectations, intracellular cAMP indeed increases upon triggering activation and that altering this increase slows down the meiotic maturation process. Our work establishes that release from prophase I arrest in oocytes is not universally dependent on, or accompanied by, decreased cAMP and that alternative pathways exist, with protostome animals providing this new original model. The implications of these findings for a better general understanding of the regulation of meiotic maturation and MPF activation are discussed.
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Materials and Methods |
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Artificial sea water (ASW) and calcium-free sea water (CaFSW) were prepared according to the Marine Biological Laboratory (MBL) formulae (Cavanaugh, 1975) with the addition of 2 mM HEPES (N-2-hydroxyethylpiperazine-N''-2-ethane sulfonic acid), pH 8.0, and 2mM ethylene glycol bis (ß-aminoethyl ether) N,N'-tetraacetic acid (EGTA) for the CaFSW. GA (glucamine acetate) buffer was prepared with 250 mM N-methyl glucamine, 250 mM potassium gluconate, 50 mM HEPES and 10 mM EGTA, and adjusted to pH 7.4 with glacial acetic acid. GA-formol solution was prepared by mixing formaldehyde (37% v/v) with GA buffer at approximately 10% v/v in solution and was mixed 1:1 with the oocytes to be fixed.
Fertilization or artificial activation of oocytes
Oocytes were washed several times by sedimentation and resuspended in ASW as a 1% (v/v) suspension. K+ activation was performed by adding known amounts of isotonic KCl (0.52 M) to obtain the final desired concentrations (1-52 mM). Serotonin was prepared as a 1 mM stock solution in ASW and used at a final concentration of 5 µM. Ammonium chloride (NH4Cl) was used at a final concentration of 10 mM by adding 1 M stock solution in ASW, adjusted to pH 8.0 just prior to use, to oocyte suspensions. Fertilization was achieved by adding a 10,000- or 50,000-fold dilution of dry sperm maintained at 4°C until use. Lower concentrations of oocytes (0.2%) were used for fertilization experiments. The percentage of GVBD was determined under the light microscope by randomly counting 100-200 fixed oocytes per sample. In some experiments, the oocyte DNA was stained with the fluorescent dye Hoechst 33258 and observed under the Leitz Diaplan fluorescence microscope for the cytological observations.
Measurement of cAMP by RIA
Conditions for the preparation of oocytes are described in the legends of each figure. Briefly, tubes containing oocytes were rapidly centrifuged to pellet oocytes and discard ASW. These tubes were rapidly transferred to a container filled with liquid nitrogen. The tubes collected in this fashion were then stored at 80°C if the extraction of cAMP were not to be performed immediately. For homogenization and extraction of cAMP, frozen samples were left for incubation at 20 °C for 30 minutes in the presence of 0.5 ml 90% ethanol. Near the end of 30 minutes, oocytes suspended in ethanol were transferred to a Kimble and Kontes tissue homogenizer on ice and were homogenized for one to two minutes. A volume equivalent to 1/200 of the whole homogenate was taken out to evaluate the extent of homogenization under light microscopy. After transferring the homogenate to an Eppendorf tube, the homogenization tube was washed using 0.5 ml 90% EtOH and added to the Eppendorf tube. After an additional 30 minutes at 20°C, tubes were centrifuged (12,000 g) for 15 minutes at 4°C. The supernatant was separated from the pellet and either immediately evaporated in a SpeedVac concentrator or kept at 80°C for later use. The pellets of centrifuged homogenates were either solubilized in 0.5 NaOH or kept at 4°C for later determinations of protein content by Detergent-Compatible (DC) protein assay (BIO-RAD).
Intracellular cAMP levels were measured by radioimmunoassay (Brooker et al., 1979). Samples and standards were incubated with the anti-cAMP antibody and [125I]-TME-ScAMP (25 000 cpm/100 µl) in phosphate-buffered saline (PBS: 0.14 M NaCl, 0.01 M sodium phosphate, pH 7.5) at 4°C for 20 hours. A pre-precipitated second antibody preparation containing 1% normal rabbit serum and 2% goat anti-rabbit antibody in PBS was then added, and samples were centrifuged (750 g) after six hours at 4°C. Radioactivity in the pellets was measured in a Gamma counter. Results are reported as picomoles cAMP per mg protein. The sensitivity of the assay was 5 pmoles per tube. Inter- and intra-assay coefficients of variation were less than 10%.
Statistical analysis
All the cAMP measurements that required statistical analysis were compared with the cAMP measurements of control groups at corresponding times by ANOVA (analysis of variance, P<0.05). Multiple comparisons were performed using either the Dunnets method (comparisons of each treatment versus control) or the Student-Newman-Keuls method (comparisons of each treament at indicated times with each other) as indicated. Significantly different measurements are depicted by asterisks (*).
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Results |
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Cyclic AMP increases upon fertilization
Even though excess K+- or 5-HT-induced oocyte activation mimick sperm-induced activation almost perfectly, we wanted to verify whether a normal fertilization would also result in increased oocyte cAMP, despite a previous report stating that no detectable changes occurred under this condition (Adeyemo et al., 1987). On the contrary, Figure 6 shows that fertilization indeed results in an early and steady increase of cAMP before GVBD. Despite the slower kinetics of GVBD, owing to imperfect synchrony of oocytes upon fertilization (20±11 at 20 minutes, 86.5±3.5 at 30 minutes, %GVBD±s.e.m.; Fig. 6), this rise in cAMP surpasses that seen after the addition of 5-HT (Fig. 5). This is related to the absence of a detectable secondary decrease over the monitored period, which may be due to this poorer synchrony of activation of fertilized oocytes (Fig. 6). Therefore, under this condition, the exact kinetics of the rise in oocyte cAMP cannot be perfectly assessed. The measured cAMP cannot originate from spermatozoa as most of them were washed out prior to oocyte sampling, and the remaining ones accounted for very few cells. Moreover, in some experiments in which insemination did not result in a successful fertilization, as evidenced by GVBD, no change in cAMP could be detected (not shown). This confirms that the rise in oocyte cAMP does not only occur during artificial activation but also during the normal process of fertilization in Spisula oocytes.
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Discussion |
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In this report, we show that cAMP-raising treatments do not inhibit 5-HT- or KCl-induced GVBD in Spisula oocytes, even when using the same compounds at concentrations ten times higher than those previously reported inhibitory (Sato et al., 1985). Other cAMP analogs tested, dbcAMP, 8-bromo-cAMP and Sp-cAMPs, were similarly inefficient in inhibiting GVBD, including dbcAMP, even at concentrations ten times higher than those reported to be inhibitory (Sato et al., 1985
). The reason for the discrepancy between our results and the previous ones is unclear. Sperm-induced GVBD is blocked in the presence of IBMX and forskolin, but we have shown that this inhibition is at the level of sperm-oocyte fusion/incorporation. We thus interpret this inhibition as an effect on the sperm itself, which becomes unable to fertilize the oocyte when raising its cAMP content. One likely possibility is that the acrosome reaction is somewhat affected by this treatment, perhaps prematurely triggered, as this process is generally associated with increased cAMP levels (Breitbart and Spungin, 1997
). However, further investigations would be required to confirm this hypothesis.
Surprisingly, in addition, direct measurements of oocyte cAMP showed that it increases by 20% to 40% very soon after triggering meiosis reinitiation in Spisula oocytes by 5-HT, KCl or sperm, in strong contrast with all other animal species so far studied. Our results contradict previous attempts that failed to detect any significant changes in oocyte cAMP levels after fertilization (Adeyemo et al., 1987). This could be due to the experimenters use of a less sensitive technique to measure cAMP. However, under the conditions they used (oocyte concentrations of 10% v/v), poor fertilizations and/or synchrony might have resulted, as it has been established that fertilization rates decrease dramatically above oocyte concentrations of 0.5%, in this species (Clotteau and Dubé, 1993
). It should be noted that the observed rise in cAMP after addition of 5-HT cannot be taken as indicative that the putative 5-HT receptor present on oocytes (Krantic et al., 1991
; Krantic et al., 1993
) is of a Gs-protein-coupled type as a similar rise of cAMP is seen in KCl-activated oocytes, which proceed through GVBD not by a receptor-mediated process but presumably because of the opening of voltage-gated Ca2+ channels (Colas and Dubé, 1998
). Taken altogether, these results reveal an unsuspected rise of oocyte cAMP at the onset of release from prophase I arrest, which is in contrast with what occurs in all other animal species so far studied.
Is the rise in oocyte cAMP required for GVBD?
As mentioned above, the presence of forskolin and IBMX are not inhibitory but, instead, they stimulate the normal rise in cAMP seen after activation by KCl or serotonin. However, even prolonged incubations in the presence of these chemicals (>three hours) did not result in GVBD unless another activating agent was subsequently added to the oocytes. This indicates that the rise of cAMP is not sufficient to trigger GVBD.
To test whether the rise of cAMP was required for GVBD, oocytes were incubated with an adenylyl cyclase inhibitor, SQ 22,536. Whereas the basal level of cAMP in resting oocytes was not significantly altered by this inhibitor, it considerably reduced the rise of cAMP normally seen after the addition of 5-HT (Fig. 7B). This treatment did not prevent GVBD induced by either KCl or 5-HT but significantly retarded it in both cases. We conclude that the rise in cAMP, if not absolutely required for GVBD, at least facilitates it and contributes to the normal kinetics of meiotic maturation. Since the inhibitor did not compeletely abolish the cAMP rise, we cannot rule out the possibility that in the complete absence of any increased cAMP, GVBD might have been completely prevented. Notwithstanding this limitation, the rise in cAMP reported here is positively correlated to the onset of GVBD, which is unique, to our knowledge, in the animal kingdom, with the exception of brittle star oocytes in which forskolin triggers GVBD (Yamashita, 1988). In the latter species, however, the physiological trigger for the release from prophase I arrest is not known, and it is uncertain to what extent the activation by forskolin mimicks the normal process.
The rise in cAMP is neither Ca2+ nor pH sensitive but tightly coupled to activation
Two well known ionic changes accompany Spisula oocyte activation, namely, an increased Ca2+ influx raising the internal Ca2+ concentration, which is absolutely required for GVBD to occur (Dubé, 1988; Colas and Dubé, 1998
), and a 0.4 U increase of pHi, driven by an Na+/H+ exchanger, which is dispensable for GVBD (Dubé and Eckberg, 1997
). In order to test whether either of these two ionic processes could be causally related to the rise of cAMP, we performed several experimental manipulations known to alter Ca2+ or pHi and verified their effects on cAMP levels.
Adding 5 to 52 mM K+ to oocyte suspensions promotes Ca2+ influxes to increasing amplitudes beyond and above a threshold level that results in GVBD (Dubé, 1988). We did not observe any changes in cAMP levels in oocytes that did not reach the threshold for GVBD, indicating that the rise in cAMP is not especially sensitive to moderate Ca2+ rises. Similarly, artificially increasing the pHi with NH4Cl, at or above the level reached by activated oocytes, but without inducing GVBD (Dubé and Eckberg, 1997
), did not affect the level of oocyte cAMP (Fig. 7A), suggesting that the normal rise in pHi is unlikely to be causally related to the observed rise of cAMP. Interestingly, the inverse might be possible; for example, the increase in pHi might be caused by increased cAMP if the Spisula oocyte Na+/H+ exchanger were, for example, of the beta type which is activated by cAMP (Malapert et al., 1997
). Moreover, when the rise of cAMP is partly inhibited by SQ 22,536, the observed retardation in GVBD is reminiscent of that observed when the pHi rise is directly prevented either by amiloride derivatives or Na+-free seawater (Dubé and Eckberg, 1997
). Thus, the rise in cAMP does not seem specifically Ca2+- nor pHi-sensitive but rather appears as an all-or-none process tightly coupled to the activated state of oocytes committed to undergo GVBD. Interestingly, this is similar to the all-or-none overall increase in protein phosphorylation observed under identical experimental conditions (Dubé et al., 1991
), a process that may be itself, at least partly, related to increased cAMP and enhanced activity of PKA.
How can a rise in cAMP be involved in the steps leading to MPF activation and GVBD?
The key biochemical process for achieving GVBD is the activation of MPF, a cdc2-cyclin complex that must undergo tyrosine dephosphorylation of cdc2 by the phosphatase cdc25 to be active. Although this process is most probably a universal convergent point in the release from prophase arrest, there appears to be considerable variation in the upstream events leading to active MPF from one species to another.
A drop in oocyte cAMP is associated with release from prophase arrest by reducing PKA activity which, in turn, is thought to maintain the arrest by phosphorylation of a regulatory susbtrate, which remains to be identified. In starfish oocyte maturation, cAMP seems to negatively affect the activation of MPF through mik1, wee1 and cdc25 (Meijer and Arion, 1991), although a decrease in cAMP alone is insufficient to trigger oocyte activation (Meijer et al., 1989
). In Xenopus oocytes, the cascade leading to MPF activation is thought to involve an early phosphorylation of a cytoplasmic polyadenylation element binding factor (CPEB), which in turn induces c-mos synthesis and accumulation (Mendez et al., 2000
) followed by the activation of MAP-kinase and MPF (Nebreda et al., 1993
; Posada et al., 1993
; Shibuya and Ruderman, 1993
). However, along this sequence of events, there are positive feedback loops (Matten et al., 1996
), which make the identification of causal effects difficult. The nature of the early link between PKA and c-mos translation is not known, but there appears to be no effect of PKA on c-mos accumulation once MAP kinase is activated (Faure et al., 1998
). On the other hand, the accumulation of cyclin B1 is more dependent upon reduced PKA activity (Frank-Vaillant et al., 1999
).
However, in Spisula oocytes as opposed to Xenopus oocytes, there is no need for new protein synthesis for completion of meiosis I (Hunt et al., 1992), and thus no accumulation of c-mos appears to be involved. In more closely related nemertean oocytes, meiosis reinitiation (from prophase I to metaphase I) can be induced by serotonin through an increase in cAMP, and without any Ca2+ fluxes or MAP kinase activation as occur during the physiological process of spontaneous maturation upon release of oocytes in Ca2+-containing seawater (Stricker and Smythe, 2001
). In contrast, in Spisula oocytes, release from prophase arrest (up to full meiotic maturation) absolutely requires external Ca2+, whether KCl, serotonin or a normal fertilization (Colas and Dubé, 1998
) triggers it. Indeed, in Spisula oocytes, activation by serotonin seems to perfectly mimic fertilization, and no differences in signalling pathways used by these two modes of activation have been detected so far. The discrepancy between nemertean and Spisula oocytes might be related to the fact that the former secondarily arrests at metaphase I, whereas the latter do not. In light of current knowledge, it is thus difficult to speculate about which process could be positively affected by increased cAMP and enhanced PKA activity to promote cell cycle re-entry in Spisula oocytes. The temporal sequence of events seems to involve an early Ca2+ rise (Dubé, 1988
) and an increase in cAMP (this work), a slightly later activation of MAP kinase followed by MPF activation (Shibuya et al., 1992
; Walker et al., 1999
). Further investigations will be required to establish the causal relationships between these various events and to identify any specific substrate phosphorylated by PKA that may contribute to oocyte activation.
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ACKNOWLEDGMENTS |
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REFERENCES |
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Abergdam, E., Hanski, E. and Dekel, N. (1987). Maintenance of meiotic arrest in isolated rat oocytes by the invasive adenylate cyclase of Bordetella pertussis. Biol. Reprod. 36, 530-535.[Abstract]
Adeyemo, O., Shirai, H. and Koide, S. S. (1987). Cyclic nucleotide content and protein phosphorylation during maturation of Spisula oocytes. Gamete Res. 16, 251-258.[Medline]
Allen, R. D. (1953). Fertilization and artificial activation in the egg of the surf clam Spisula solidissima. Biol. Bull. 105, 213-239.
Bornslaeger, E. A., Mattei, P. M. and Schultz, R. M. (1986). Involvement of cAMP-dependent protein kinase and protein phosphorylation in the regulation of mouse oocyte maturation. Dev. Biol. 114, 453-462.[Medline]
Breitbart, H. and Spungin, B. (1997). The biochemistry of the acrosome reaction. Mol. Hum. Reprod. 3, 195-202.[Abstract]
Brooker, G., Jeffrey, F. H., Wesley, L. T. and Robert, D. M. (1979). Radioimmunoassay of cyclic AMP and cyclic GMP. Adv. Cyc. Nucl. Res. 10, 1-33.
Cavanaugh, G. M. (1975). Formulas and methods VI of the Marine Biological Laboratory. Woods Hole, MA.
Cicirelli, M. F. and Smith, L. D. (1985). Cyclic AMP levels during the maturation of Xenopus oocytes. Dev. Biol. 108, 254-258.[Medline]
Clotteau, G. and Dubé, F. (1993). Optimization of fertilization parameters for rearing surf clams. Aquaculture 114, 339-353.
Colas, P. and Dubé, F. (1998). Meiotic maturation in mollusc oocytes. Semin. Cell Develop. Biol. 9, 539-548.[Medline]
Dekel, N. (1996). Protein phosphorylation/dephosphorylation in the meiotic cell cycle of mammalian oocytes. J. Reprod. Fertil. 1, 82-88.
Dubé, F. and Eckberg, W. R. (1997). Intracellular pH increase driven by an Na+/H+ exchanger upon activation of surf clam oocytes. Dev. Biol. 190, 41-45.[Medline]
Dubé, F. (1988). The relationships between early ionic events, the pattern of protein synthesis, and oocyte activation in the surf clam, Spisula solidissima. Dev. Biol. 126, 233-241.[Medline]
Dubé, F., Dufresne, L., Coutu, L. and Clotteau, G. (1991). Protein phosphorylation during activation of surf clam oocytes. Dev. Biol. 146, 473-482.[Medline]
Faure, S., Morin, N. and Dorée, M. (1998). Inactivation of protein kinase A is not required for c-mos translation during meiotic maturation of Xenopus oocytes. Oncogene 17, 1215-1221.[Medline]
Ferrell, J. E. Jr. (1999). Xenopus oocyte maturation: new lessons from a good egg. Bioessays 21, 833-842.[Medline]
Frank-Vaillant, M., Jessus, C., Ozon, R., Maller, J. L. and Haccard, O. (1999). Two distinct mechanisms control the accumulation of cyclin B1 and mos in Xenopus oocytes in response to progesterone. Mol. Biol. Cell. 10, 3279-3288.
Heikinheimo, O. and Gibbons, W. E. (1998). The molecular mechanisms of oocyte maturation and early embryonic development are unveiling new insights into reproductive medicine. Mol. Hum. Reprod. 4, 745-756.[Abstract]
Hirai, S., Kishimoto, T., Kadam, A. L., Kanatani, H. and Koide, S. S. (1988). Induction of spawning and oocyte maturation by 5-hydroxytryptamine in the surf clam. J. Exp. Zool. 245, 318-321.
Huchon, D., Ozon, R., Fischer, E. H. and Demaille, J. G. (1981). The pure inhibitor of cAMP-dependent protein kinase initiates Xenopus laevis meiotic maturation. Mol. Cell. Endocrinol. 22, 211-222.[Medline]
Hunt, T., Luca, F. C. and Ruderman, J. V. (1992). The requirements for protein synthesis and degradation, and the control of destruction of cyclins A and B in the meiotic and mitotic cell cycles of the clam embryo. J. Cell. Biol. 116, 707-724.[Abstract]
Jaffe, L. F. (1983). Source of calcium in egg activation: a review and hypothesis. Dev. Biol. 99, 265-276.[Medline]
Krantic, S., Dubé, F., Quirion, R. and Guerrier, P. (1991). Pharmacology of the serotonin-induced meiosis reinitiation in Spisula solidissima oocytes. Dev. Biol. 146, 491-498.[Medline]
Krantic, S., Guerrier, P. and Dubé, F. (1993). Meiosis reinitiation in surf clam oocytes is mediated via a 5-hydorxytryptamine5 serotonin membrane receptor and a vitelline enenveloppessociated high affinity binding site. J. Biol. Chem. 268, 7983-7989.
Malapert, M., Guizouara, H., Fievet, B., Jahns, R., Garcia-Romeu, F., Motais, R. and Borgese, F. (1997). Regulation of Na+/H+ antiporter in trout red blood cells. J. Exp. Biol. 200, 353-360.
Maller, J. L. (1985). Regulation of amphibian oocyte maturation. Cell Differ. 16, 211-221.[Medline]
Maller, J. L. and Krebs, E. G. (1977). Progesterone-stimulated meiotic cell division in Xenopus oocytes. Induction by regulatory subunit and inhibition by catalytic cubunit of adenosine 3':5'-monophosphate-dependent protein kinase. J. Biol. Chem. 252, 1712-1718.[Abstract]
Matten, W., Daar, I. and Vande Woude, G. F. (1994). Protein kinase A acts at multiple points to inhibit Xenopus oocyte maturation. Mol. Cell. Biol. 14, 4419-4426.[Abstract]
Matten, W., Copeland, T. D., Ahn, N. G. and Vande Woude, G. F. (1996). Positive feedback between MAP kinase and Mos during Xenopus oocyte maturation. Dev. Biol. 179, 485-482.[Medline]
Mazzei, G., Meijer, L., Moreau, M. and Guerrier, P. (1981). Rôle of calcium and cyclic nucleotides during meiosis reinitiation in starfish oocytes. Cell Differ. 10, 139-145.
Meijer, L. and Zarutskie, P. (1987). Starfish oocyte maturation: 1-methyladenine triggers a drop of cAMP concentration related to the hormone-dependent period. Dev. Biol. 121, 306-315.[Medline]
Meijer, L. and Arion, D. (1991). Negative control of cdc2 kinase activation by cAMP in starfish oocytes. Cold Spring Harbor Symp. Quant. Biol. 56, 591-598.[Medline]
Meijer, L., Dostmann, W., Geneiser, M. G., Butt, E. and Jastorff, B. (1989) Starfish oocyte maturation: Evidence for a cyclic AMP-dependent inhibitory pathway. Dev. Biol. 133, 58-66.[Medline]
Mendez, R., Hake, L. E., Andresson, T., Littlepage, L. E., Ruderman, J. V. and Richter, J. D. (2000). Phosphorylation of CPE binding factor by Eg2 regulates translation of c-mos mRNA. Nature 404, 302-307.[Medline]
Nebreda, A. R., Hill, C., Gomez, N., Cohen, P. and Hunt, T. (1993). The protein kinase mos activates MAP kinase kinase in vitro and stimulates the MAP kinase pathway in mammalian somatic cells in vivo. FEBS Lett. 333, 183-187.[Medline]
Posada, J., Yew, N., Ahn, N. G., Vande Woude, G. F. and Cooper, J. A. (1993). Mos stimulates MAP kinase in Xenopus oocytes and activates a MAP kinase kinase in vitro. Mol. Cell. Biol. 13, 2546-2553.[Abstract]
Rime, H., Haccard, O. and Ozon, R. (1992). Activation of p34cdc2 kinase by cyclin is negatively regulated by cyclic AMP-dependent protein kinase in Xenopus oocytes. Dev. Biol. 151, 105-110.[Medline]
Sato, E. and Koide, S. S. (1984). Forskolin and mouse oocyte maturation in vitro. J. Exp. Zool. 230, 125-129.[Medline]
Sato, E., Wood, H. N., Lynn, D. G., Sahni, M. K. and Koide, S. S. (1985). Meiotic arrest in oocytes regulated by a Spisula factor. Biol. Bull. 169, 334-341.
Schorderet-Slatkine, S. and Baulieu, E. E. (1982). Forskolin increases cAMP and inhibits progesterone induced meiosis reinitiation in Xenopus laevis oocytes. Endocrinol. 111, 1385-1387.[Abstract]
Schuetz, A. W. (1975). Induction of nuclear breakdown and meiosis in Spisula solidissima oocytes by calcium ionophore. J. Exp. Zool. 191, 433-440.[Medline]
Schultz, R. M., Montgomery, R. R. and Belanoff, J. R. (1983). Regulation of mouse oocyte meiotic maturation: implication of a decrease in oocyte cAMP and protein dephosphorylation in commitment to resume meiosis. Dev. Biol. 97, 264-273.[Medline]
Shibuya, E. K., Boulton, T. G., Cobb, M. H. and Ruderman, J. V. (1992). Activation of p42 MAP kinase and the release of oocytes from cell cycle arrest. EMBO J. 11, 3963-3975.[Abstract]
Shibuya, E. K. and Ruderman, J. V. (1993). Mos induces the in vitro activation of mitogen-activated protein kinases in lysates of frog oocytes and mammalian somatic cells. Mol. Biol. Cell 4, 781-790.[Abstract]
Stricker, S. A. and Smythe, T. L. (2001). 5-HT causes an increase in cAMP that stimulates, rather than inhibits, oocyte maturation in marine nemertean worms. Development 128, 1415-1427.
Urner, F., Herrmann, W. L., Baulieu, E. E. and Schorderet-Slatkine, S. (1983). Inhibition of denuded mouse oocyte meiotic maturation by forskolin, an activator of adenylate cyclase. Endocrinol. 113, 1170-1172.[Abstract]
Vivarelli, E., Conti, M., De Felici, M. and Siracusa, G. (1983). Meiotic resumption and intracellular cAMP levels in mouse oocytes treated with compounds which act on cAMP metabolism. Cell. Differ. 12, 271-276.[Medline]
Walker, J., Minshall, N., Hake, L., Richter, J. and Standart, N. (1999). The clam 3'UTR masking element-binding protein p82 is a member of the CPEB family. RNA 5, 14-26.
Yamashita, M. (1988). Involvement of cAMP in initiating maturation of the brittle-star Amphipholis kochii oocytes: induction of oocyte maturation by inhibitors of cyclic nucleotide phosphodiesterase and activators of adenylate cyclase. Dev. Biol. 114, 453-462.