Hammond Memorial Lecture. Are follicular maturation and oocyte maturation independent processes?
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[Induction of oocyte maturation at stages of incomplete vitellogenesis in toads and the starred sturgeon].
The intracellular injection of cytoplasm from the maturing oocytes of X. laevis and A. stellatus in oocytes of the same species which did not complete the vitellogenesis and are not able to mature under the effect of progesterone resulted in the disintegration of the germinal vesicle membrane in the oocytes of all sizes under study. In X. laevis the ability to mature under the effect of progesterone appears in the oocytes with the diameter over 1.1 mm. Cycloheximide inhibits the germinal vesicle membrane disintegration in the X. laevis oocytes, but not in those of A. stellatus. Cycloheximide inhibits the pseudogastrulation which was observed in the X. laevis oocytes with the diameter from 0.8 to 1.4 mm.
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RNAseq analysis of oocyte maturation from the germinal vesicle stage to metaphase II in pig and human.
During maturation oocytes at the germinal vesicle (GV) stage progress to metaphase II (MII). However, during in vitro maturation a proportion often fail to progress. To understand these processes, we employed RNA sequencing to examine the transcriptome profile of these three groups of oocytes from the pig. We compared our findings with similar public oocyte data from humans. The transcriptomes in oocytes that failed to progress was similar to those that did. We found in both species, the most upregulated genes in MII oocytes were associated with chromosome segregation and cell cycle processes, while the most down regulated genes were relevant to ribosomal and mitochondrial pathways. Moreover, those genes involved in chromosome segregation during GV to MII transition were conserved in pig and human. We also compared MII and GV oocyte transcriptomes at the isoform transcript level in both species. Several thousands of genes (including DTNBP1, MAPK1, RAB35, GOLGA7, ATP1A1 and ATP2B1) identified as not different in expression at a gene transcript level were found to have differences in isoform transcript levels. Many of these genes were involved in ATPase-dependent or GTPase-dependent intracellular transport in pig and human, respectively. In conclusion, our study suggests the failure to progress to MII in vitro may not be regulated at the level of the genome and that many genes are differentially regulated at the isoform level, particular those involved ATPase- or GTPase-dependent intracellular transport.
Humans↗
Mammalian oocyte maturation: model systems and their physiological relevance.
Maturation of mammalian oocytes is studied mainly in two dissimilar in vitro models: isolated oocytes maturing spontaneously in culture, and hormone-induced maturation of follicle-enclosed oocytes. In this discussion the following aspects of maturation in vitro in the two aforementioned models were compared: timing of germinal vesicle breakdown (GVB), involvement of cyclic nucleotides, protein synthesis and divalent cations. A third approach to the study of oocyte maturation in vitro, namely oocyte co-culture with follicular constituents was adopted in order to test the role of follicular components in the control of the resumption of meiosis. Such studies demonstrated an inhibitory action of granulosa cells, granulosa cell-conditioned medium and of follicular fluid upon the spontaneous maturation of the co-cultured oocytes. Furthermore, addition of LH to co-cultures of oocytes and granulosa cells induced resumption of meiosis. Although oocytes obtained by spontaneous or by hormone-induced maturation cannot be distinguished morphologically, the developmental potential of oocytes matured spontaneously has been questioned, at least in some species. Furthermore, analysis of the kinetics of spontaneous maturation suggests that oocytes dislodged from their follicles escape physiologic mechanisms ensuring meiotic arrest and skip some of the regulatory steps involved in the normal hormonal triggering of maturation. Oocyte co-culture with granulosa cells offers a close approximation to physiological conditions in that meiotic maturation depends on hormonal stimulation, while the system permits the application of separate treatments to the oocyte-cumulus complex and granulosa cells. As in any in vitro system, critical evaluation is required to discriminate between artifacts inherent in the model and physiological processes.
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Effect of hypophysectomy on mouse oocyte maturation in vitro.
There was no difference in frequency of maturation of oocytes obtained from mice hypophysectomized for 2 weeks compared to those from sham-operated or untreated (control) animals of the same age. By 7 weeks, and also at 12 and 17 weeks, the incidence of polar body formation in vitro was significantly reduced. The number of oocytes which remained meiotically inactive in culture was increased at 7, 12 and 17 weeks after hypophysectomy. This decrease in spontaneous oocyte maturation in vitro could be partly overcome by administering exogenous PMSG, oestradiol-17beta or PMSG + oestradiol-17beta, but not progesteron or hCG, to hypophysectomized mice.
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Rat oocyte maturation in vitro: relief of cyclic AMP inhibition by gonadotropins.
The hormone-independent, spontaneous maturation that rat oocytes undergo in vitro can be inhibited by derivatives of cyclic AMP and inhibitors of cyclic nucleotide phosphodiesterase. In this study, we have shown that this inhibition of maturation can be partially relieved by preparations of ovine and rat luteinizing hormone or follicle-stimulating hormone. The ability of gonadotropins to foster the resumption of maturation in cultures of cyclic AMP-inhibited oocytes suggests that this system is suitable for studies of the hormonal control of oocyte development. The dose and time dependency of the response to gonadotropins has been examined in order to study the role of these hormones in oocyte maturation and to compare this effect to other known responses of the cumulus-oocyte complex. These studies show that highly purified preparations of rat gonadotropins are less effective inducers of maturation than the more commonly used, but considerably less purified, preparations of ovine gonadotropins. Almost complete relief of inhibition is observed, however, when the oocytes are exposed to a combination of rat luteinizing hormone and follicle-stimulating hormone. Oocyte maturation was not influenced by the sex steroids progesterone or 17beta-estradiol. Our results suggest that: (i) cyclic AMP is involved in the intrafollicular inhibition of oocyte maturation; (ii) both gonadotropins are required for maximal stimulation of the resumption of oocyte meiosis; and (iii) steroids are not involved in this response to gonadotropins.
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IVM rescue: Effect of growth hormone supplementation combined to autologous cumulus co-culture on GV oocyte maturation and competency.
OBJECTIVE: IVM rescue is based on the in vitro maturation of mainly Germinal Vesicle (GV) oocytes collected from stimulated cycles. The objective was to investigate the effects of growth hormone (GH) and autologous cumulus cells co culture (CC) on oocyte meiosis resumption and maturation after 32 h post cumulus denudation, in order to obtain additional embryos for the couple as a rescue system to increase the changes of cumulative pregnancy. MATERIAL AND METHODS: Our study concerned 300 patients who underwent ICSI cycles, during which a total of 1940 cumulus-complex-oocytes were retrieved, giving 1260 metaphase II stage (MII), 200 at the metaphase I stage, and 480 at the Germinal Vesicle (GV) stage. Mature oocytes were microinjected on the same day of retrieval. Immature GV oocytes were divided into four groups, with the first undergoing in vitro maturation (IVM) without cumulus cells (group 1) and the second undergoing IVM with CC (group 2), the third undergoing IVM without CC and with GH (group 3), the fourth undergoing IVM with CC and with GH (group 4). After 32 h of IVM, the matured oocytes, underwent microinjection, followed by embryonic development monitoring. RESULTS: When comparing the IVM outcomes, we observed a significant increase in oocyte maturation, fertilization rates and the percentage of 8-cell embryos on day 3 across the different study groups (p < 0.001) (Figs. 2-5). Furthermore, all study groups (1-4) exhibited notably blastulation rates, with group 3 demonstrating the most promising clinical outcomes. A preliminary pregnancy rate of approximately 20% was recorded in group 3, suggesting a potential improvement in the developmental competence of oocytes matured under specific conditions. CONCLUSION: The IVM rescue of germinal vesicle oocyte could serve as an additional strategy to increase the chance getting extra embryos to patients. Autologous cumulus cells co-culture combined to GH supplementation to IVM media, appear to play a crucial role to enhance successful meiosis resumption, oocyte maturation and competency to support embryos development when the injected spermatozoa is not carrier of severe genome and epigenomic decays.
Humans↗
Action of porcine follicular fluid oocyte maturation inhibitor in vitro: possible role of the cumulus cells.
To study the mode of action of porcine follicular fluid oocyte maturation inhibitor isolated cumulus-enclosed or mechanically denuded pig oocytes were used. Two types of culture media were employed, a complex containing 15% pig serum (TC199A) and a defined, minimal medium (BMOC). The maturation of cumulus-enclosed oocytes was comparable in the two types of culture media, but only in the complex medium did the cumulus cells remain functional in terms of morphology and progesterone secretion. The low molecular weight portion of follicular fluid partially inhibited oocyte meiosis and cumulus progesterone secretion in 199A. No inhibition of oocyte maturation was seen when follicular fluid was added to BMOC. Since denuded oocytes did not respond to follicular fluid in either culture medium, it is suggested that the cumulus cells may mediate the action of the follicular fluid oocyte maturation inhibitor.
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Specificity of inhibition by steroids of porcine oocyte maturation in vitro.
In order to examine the influence of several steroids on the process of oocyte maturation, denuded (adherent cumulus granulosa cells mechanically removed) and intact (cumulus granulosa cells left attached) porcine oocytes were cultured in the presence or absence of estradiol-17 beta, estradiol-17 alpha, testosterone, cortisol, progesterone, or the nonsteroidal estrogen diethyl stilbestrol (all at 10 microgram/ml) in defined medium that contained either BSA or dextran. Estradiol-17 beta was the only steroid to exert a significant inhibitory effect on the maturation of denuded oocytes, and did so only in BSA supplemented medium. The inhibition was reversible in that oocytes, cultured in steroid-free medium after initial culture in estradiol-17 beta medium, resumed meiotic maturation. Oocytes took up 3H-estradiol-17 beta in both media, although less radiolabel entered oocytes in BSA supplemented medium. The majority of label in the oocytes, when cultured with either medium, was not displaced by excess radioinert estradiol-17 beta or progesterone, nor were the oocytes saturated even when cultured in 10(-6) M estradiol-17 beta. Autoradiography of sectioned oocytes after culture in 3H-estradiol-17 beta has shown that there was no selective accumulation of silver grains over the germinal vesicle as was the case with granulosa cell nuclei. This observation suggests that estradiol-17 beta may not act at the level of the oocyte nucleus.
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The effect of LH on the fertilizability and developmental capacity of rat oocytes matured in vitro.
The effect of adding LH (10 microgram NIH-LH-B8/ml) to the medium in which oocytes were undergoing maturation in vitro was studied. The fertilizability of the oocytes was evaluated in the sterile oviduct of a unilaterally ovariectomized, mated recipient. Freshly ovulated oocytes, used as a control of the method, were fertilized at a rate of 72%. Only 14% of oocytes matured in culture (without LH) were penetrated by spermatozoa, and 11% were fertilized normally. Addition of LH to the medium increased these proportions to 43 and 33% respectively. Oocytes matured in the presence of LH were able to develop into apparently normal rats. It is concluded that, although oocytes can mature in vitro spontaneously, and that these matured oocytes can be fertilized, addition of LH increases the numbers 3-fold. LH therefore has a direct maturation-promoting action on the rat oocyte-cumulus complex in vitro.
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Method for the preparation of active maturation promoting factor (MPF) from in vitro matured oocytes of Xenopus laevis.
A method for the large scale extraction of Maturation Promoting Factor (MPF) from in vitro matured oocytes of Xenopus laevis is described. MPF has been previously described only as a component(s) of hormone-matured cytoplasm within amphibian oocytes (or eggs) which is able to induce the reinitiation of the meiotic process from late diplotene stage until second metaphase arrest, when microinjected into diplotene arrested (fully grown) recipient oocytes. Standard biochemical methods for the extraction and purification of this factor(s) haven been unsuccessful due to its extreme instability and sensitivity to dilution. The procedure is dependent upon the inclusion of sodium fluoride (NaF) in the extraction medium with its effect presumably due to its ability to inhibit phosphorprotein phosphatases. The successful preservation of MPF activity described in this report permits further attempts to be made to isolate and characterize this, to date, elusive cytoplasmic factor, which plays a key role in the complex cellular processes involved in the hormone-dependent differentiation of an oocyte into an egg.
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Lactate concentrations in pre-ovulatory follicles of pro-oestrous rats before and after onset of oocyte maturation.
Lactate concentrations were determined in pre-ovulatory follicles of rats at pro-oestrus before and after onset of oocyte maturation. It appeared that high concentrations prevail before and after the time of the expected LH surge (27 mM). The level in serum was about 5 mM. Explanted oocytes obtained from pre-puberal rats and surrounded by cumulus cells, matured in the presence of 20 mM lactate as sole exogenous energy source. It is argued that oxygen may be the limiting factor suppressing oocyte maturation in vivo.
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Luteinizing hormone-accelerated redistribution of lysosome-like organelles preceding dissolution of the nuclear envelope in rat oocytes maturing in vitro.
Maturation of the mammalian oocyte is characterized in part by dissolution of the nuclear envelope, or germinal vesicle breakdown (GVB). By fluorescence microscopy after vital uptake of acridine orange (AO), redistribution and perinuclear accumulation of organelles corresponding to lysosomes occur before GVB in rat oocytes undergoing meiotic maturation in vitro. In follicle-enclosed oocytes explanted during the preovulatory gonadotropin surge (GS) and individually cultured as such in chemically defined medium at approximately 22 degrees C, lysosomes aggregated into disperse clusters after 30 min; by 60 min, perinuclear concentration of lysosomes and their essential disappearance from the cortical ooplasm were observed. GVB occurred within 120 min. In contrast, follicle-enclosed oocytes explanted before the GS displayed a generally homogeneous distribution of lysosomes and intact GV for up to 5 h in culture. In oocytes aspirated from follicles before the GS, partially denuded of granulosa cells, and cultivated without added hormone, most lysosomes concentrated around the GV within 60 min, with GVB occurring generally by 120 min. Luteinizing hormone (LH) added in vitro to the isolated preparation at 3 or 30 x 10(-8) M sharply accelerated these events. The effects of LH, not seen with 1.5 x 10(-8) M hormone, were blocked by anti-LH IgG. Up to 60 x 10(-8) M follicle-stimulating hormone or 80 x 10(-8) M prolactin were ineffective in accelerating lysosome redistribution or GVB. After GVB, lysosomes became once again uniformly dispersed and unresponsive, even to 60 x 10(-8) M added LH, a finding consistent with tachyphylaxis of target cells by independent criteria. The present data, all statistically significant at P less than 0.05, demonstrate that mobilization of lysosomes before GVB is a specific response to factors that promote resumption of meiotic maturation of rat oocytes.
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[Formation of the cortical reaction in the process of oocyte maturation in the starred sturgeon].
The chronology of maturation process and cortical reaction development was studied in the Volga sevryuga oocytes. The germinal vesicle breakdown was first noted at 14 tau 0 following the injection of hypophysial suspension to the female and observed in the vast majority of oocytes at 17 tau 0; different phases of the I maturation division were found at 21 to 25 tau 0 and metaphase II at 33 tau 0. The ability to respond by cortical reaction to the activating stimulus (glass needle pricking) was first observed at 17 tau 0, i.e. soon after the germinal vesicle breakdown, but the appearance of the ability for cortical reaction was not connected causatively with the latter process. The cortical reaction in the maturing oocytes (17 to 25 tau 0) is characterized by the following features: in some oocytes the rate of the wave of granule breakdown is much lower than in the mature eggs; in ca. 80% of oocytes with the normal rate of cortical reaction the process of release of the contents of cortical granules in inhibited in the animal pole region and accordingly the contact of cytoplasm with the membranes is preserved in this region for a long time.
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Relationship between steroidogenesis and oocyte maturation in rat graafian follicles cultured in vitro.
Rat Graafian follicles were dissected from ovaries during the morning of proestrus and incubated in various media. After an 8 h incubation period, ovarian follicles were collected and analyzed, by radioimmunoassay, for progesterone, 17 alpha-hydroxyprogesterone, androstenedione, estradiol-17 beta, and dihydrotestosterone. Following incubation in proestrus (a.m.) serum, preovulatory follicles secreted all these steroids and the output of progesterone, 17 alpha-hydroxyprogesterone and androstenedione was markedly stimulated following the addition of LH to the media. Follicle-enclosed oocytes resumed meiosis when incubated in proestrus serum without added LH. However, germinal vesicle break-down (GVBD) under these conditions was considerably slower than that observed following addition of LH to the medium. "Spontaneous" maturation of oocytes in proestrus serum was associated with increased production of steroids. Oocyte maturation and steroidogenesis both occurred following incubation of ovarian follicles in serum obtained from hypophysectomized rats. Addition of LH to the media markedly accelerated these responses. These results suggest that oocyte maturation and steroidogenesis also occur in cultured ovarian follicles in the absence of gonadotrophic hormones. The relationship between steroidogenesis and/or spontaneous oocyte maturation are discussed.
Androstenedione↗
A reversible, hydrogen ion blockade of spontaneous oocyte maturation in the starfish: locus of action.
Starfish (Asterias forbesi) oocytes encased within their follicle cells mature spontaneously during a portion of the normal reproductive period when released from the ovary into seawater. A previous report has shown that oocytes isolated in acidic seawater do not mature spontaneously but retain the capacity to do so when returned to normal seawater. The object of this study was to determine the mechanism by which acidic pH reversibly blocks spontaneous oocyte maturation in isolated follicles. Incidence of spontaneous oocyte maturation in follicles isolated in acidic seawater decreased as pH decreased from 7 to 4. Oocytes in which spontaneous maturation was inhibited (ASW at pH 4.7 TO 5.4) underwent germinal vesicle breakdown with the addition of 1-methyladenine. Oocytes isolated in acidic seawater (pH 4 or 5) with intact follicle cells matured spontaneously when transferred immediately to normal seawater pH 8); after four hours, 60-65% of the follicles incubated in seawater at pH 5 matured spontaneously when returned to normal seawater as compared to less than 10% of the follicles maintained at pH 4. Inhibition of spontaneous maturation was not reversible in the absence of the follicle cells. Oocytes isolated in acidic seawater with their follicle cells did not spontaneously mature when transferred to calcium-free seawater at pH 8. The results obtained support the hypothesis that acidic seawater reversibly inhibits spontaneous oocyte maturation by interfering with the release of meiosis-inducing substance from the follicle cells.
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Amphibian oocyte maturation and protein synthesis: related inhibition by cyclic AMP, theophylline, and papaverine.
Two inhibitors of cyclic AMP phosphodiesterase (3':5'-cyclic-AMP 5'-nucleotidohydrolase, EC 3.1.4.17), theophylline and papaverine, inhibit the maturation of Xenopus laevis oocytes induced by four different stimuli: human chorionic gonadotropin, progesterone, testosterone, and lanthanum ions. Addition of 1 mM cyclic AMP to the medium delays maturation by approximately 2 hr. Papaverine, theophylline, and cyclic AMP inhibit amino acid incorporation into oocyte proteins by 50% or more but do not inhibit amino acid uptake. The capacity of theophylline to block maturation and protein synthesis is reversed in a parallel fashion by addition of 1-5 mM calcium ion to the medium. Addition of papaverine, theophylline, and cycloheximide to oocytes at different times after hormonal treatment shows that the step sensitive to blockage by the three drugs is coincident and precedes germinal vesicle breakdown by about 1.5 hr. Theophylline and papaverine do not increase endogenous cyclic AMP levels in oocytes but do block the decrease of cyclic AMP levels observed 3 hr after progesterone treatment. Both drugs inhibit oocyte cyclic AMP phosphodiesterase measured in vivo and severely inhibit the stimulus of calcium uptake caused by progesterone and human chorionic gonadotropin. These results suggest that cyclic AMP, theophylline, and papaverine may block oocyte maturation by inhibiting protein synthesis, possibly via a cyclic AMP-dependent protein kinase as shown in reticulocytes [Datta, A., De Haro, C., Sierra, J. & Ochoa, S. (1977) Proc. Natl. Acad. Sci., USA 74, 1463-1467].
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Inhibition of (3H)vitellogenin uptake by isolated amphibian oocytes injected with cytoplasm from progesterone-treated mature oocytes.
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Animals↗