A new vision of the origin and the oocyte development in the Ostariophysi applied to Gymnotus sylvius (Teleostei: Gymnotiformes)

Based on new knowledge coming from marine perciform species, the origin of oocytes and their development in the Ostariophysi, Gymnotus sylvius is described. In both Gymnotus sylvius and marine perciform fish, oogonia are found in the germinal epithelium that forms the surface of the ovarian lamellae. At the commencement of folliculogenesis, proliferation of oogonia and their entrance into meiosis gives rise to germ cell nests that extend into the stroma from the germinal epithelium. Both cell nests and the germinal epithelium are supported by the same basement membrane that separates them from the stroma. At the time of meiotic arrest, oocytes in a cell nest become separated one from the other as processes of prefollicle cells, these being derived from epithelial cells in the germinal epithelium, gradually encompass and individualize them while also synthesizing a basement membrane around themselves during folliculogenesis. The oocyte enters primary growth while still within the cell nest. At the completion of folliculogenesis, the oocyte and follicle cells, composing the follicle, are encompassed by a basement membrane. The follicle remains connected to the germinal epithelium as the both share a portion of common basement membrane. Cells originating from the stroma encompass the ovarian follicle, except where there is a shared basement membrane, to form the theca. The follicle, basement membrane and theca form the follicular complex. Oocyte development occurs inside the follicular complex. Development is divided into the stages primary and secondary growth, oocyte maturation and ovulation. Cortical alveoli appear in the ooplasm just prior to the beginning of secondary growth, the vitellogenic stage that begins with yolk deposition and proceeds until the oocyte is full-grown and the ooplasm is filled with yolk globules. Maturation is characterized by the germinal vesicle or nuclear migration, germinal vesicle breakdown or nuclear envelop fragmentation and the resumption of meiosis. At the ovulation the egg is released from the follicular complex into the ovarian lumen. When compared to marine Perciformes that lay pelagic eggs, oocyte development in Gymnotus sylvius has fewer steps within the stages of development, the two most remarkable being the absence of oil droplet formation during primary and secondary growth, (and the consequent absence of the oil droplets fusion during maturation), and the hydrolysis of yolf preceding ovulation.

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Characterization of inhibin α subunit (inha) in the zebrafish: evidence for a potential feedback loop between the pituitary and ovary

Reproduction ◽

10.1530/rep-09-0198 ◽

2009 ◽

Vol 138 (4) ◽

pp. 709-719 ◽

Cited By ~ 28

Author(s):

Shui-Kei Poon ◽

Wai-Kin So ◽

Xiaobin Yu ◽

Lin Liu ◽

Wei Ge

Keyword(s):

Feedback Loop ◽

Transforming Growth Factor ◽

Germinal Vesicle ◽

Transforming Growth Factor Β ◽

Inhibitory Effect ◽

Follicle Cells ◽

Germinal Vesicle Breakdown ◽

Α Subunit ◽

Vitellogenic Stage

Inhibin and activin are closely related disulphide-linked dimers that belong to the transforming growth factor β superfamily. Although inhibin has been extensively studied in mammals, the information about its existence and function in lower vertebrates is very scarce. Using zebrafish as a model, the present study demonstrated that the inhibin-specific α subunit (inha) was predominantly expressed in the gonads and no transcript could be detected in other tissues including the pituitary and brain. In the ovary, the expression ofinhawas restricted to the somatic follicle cells surrounding the oocyte, together with the β subunits (inhbaaandinhbb). This was further supported by the absence of its expression in the ovulated unfertilized eggs. During folliculogenesis,inhaexpression in the follicles slightly but steadily increased from primary growth to the mid-vitellogenic stage; however, its expression surged dramatically at the full-grown stage. Interestingly, the expression level ofinhadecreased significantly in the follicles whose oocytes were undergoing spontaneous maturation or germinal vesicle breakdown. When tested on cultured ovarian fragments, both goldfish pituitary extract and forskolin significantly stimulatedinhaexpression. Further experiments showed that recombinant zebrafish FSH but not LH significantly increasedinhaexpression in the same assay system. When testedin vitro, human inhibin A exhibited a slight but significant inhibitory effect on 17α, 20β-dihydroxyprogesterone-induced oocyte maturation after 4 h incubation. The stimulation ofinhaexpression by FSH and the potential inhibition of FSH by inhibin suggest a possible existence of a negative feedback loop between the pituitary and ovary in the zebrafish.

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Involvement of catecholamines in the regulation of oocyte maturation in frogs

Zygote ◽

10.1017/s0967199402002356 ◽

2002 ◽

Vol 10 (3) ◽

pp. 271-281 ◽

Cited By ~ 8

Author(s):

Inés Ramos ◽

Susana Cisint ◽

Claudia A. Crespo ◽

Marcela F. Medina ◽

Silvia N. Fernández

Keyword(s):

Oocyte Maturation ◽

Germinal Vesicle ◽

Significant Inhibition ◽

Follicle Cells ◽

Germinal Vesicle Breakdown ◽

Nuclear Maturation ◽

Dose Dependent ◽

Metabolic Behaviour

The present study investigates the role of catecholamines in the regulation of Bufo arenarum oocyte maturation. The metabolic changes in the oxidation of carbohydrates and the meiotic resumption evinced by the germinal vesicle breakdown were used as indicators of cytoplasmic and nuclear maturation, respectively. The results obtained suggest that noradrenaline (norepinephrine) could be one of the factors responsible for the metabolic behaviour that characterises cytoplasmically immature oocytes. The use of adrenaline (epinephrine), on the other hand, induced a metabolic change which made oocytes cytoplasmically mature. The effect of both catecholamines, which was dose-dependent, was observed in ovarian oocytes (surrounded by follicle cells) as well as in coelomic oocytes (free from follicle cells), suggesting the presence of adrenergic receptors in the gamete. The results obtained using adrenergic agonists and antagonists suggest that the effect of adrenaline would be due to an interaction with β2-receptors. Although catecholamines have an influence on the determination of the stage of cytoplasmic maturation of the oocytes, they do not affect nuclear maturation by themselves. Nevertheless, pretreatment of follicles with adrenaline caused a significant inhibition in progesterone-induced nuclear maturation even though this effect was markedly weaker when using noradrenaline.

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1-Methyladenine: a starfish oocyte maturation-inducing substance

Zygote ◽

10.1017/s0967199400130047 ◽

1999 ◽

Vol 8 (S1) ◽

pp. S9-S11 ◽

Cited By ~ 4

Author(s):

Masatoshi Mita

Keyword(s):

Oocyte Maturation ◽

Hormone Receptor ◽

Ovarian Follicle ◽

Germinal Vesicle ◽

Follicle Cells ◽

Glycoprotein Hormone ◽

Late Prophase ◽

Immature Oocytes ◽

Extracellular Region ◽

Glycoprotein Hormone Receptor

1-Methyladenine (1-MeAde) in starfish was the first compound to be identified as an oocyte maturation-inducing substance (MIS) among invertebrates in 1969 by Kanatani and co-workers. In starfish, the ripe ovary contains a huge number of fully grown oocytes of almost equal size. Each oocyte possesses a large nucleus (germinal vesicle, GV), which is arrested in late prophase of the first maturation division. The oocyte is surrounded by a single follicle layer. Such immature oocytes are not fertilisable. Resumption of meiosis in immature oocytes can be induced by 1-MeAde, and the mature oocytes thus become fertilisable (Kanatani et al., 1969; Kanatani, 1985). 1-MeAde is produced by ovarian follicle cells upon stimulation with a gonad-stimulating substance (GSS) released from the radial nerves (Fig. 1).It has been demonstrated that GSS is a peptide hormone (Kanatani et al., 1971). The action of GSS on 1-MeAde production in follicle cells appears to be mediated by its receptor, G-proteins and adenylyl cyclase (Mita & Nagahama, 1991). These findings suggest that a G-protein coupled (seven transmembrane type) receptor is involved in GSS signal transduction, similarly to the pituitary-gonadal axis in vertebrates.Thus, using degenerate probes derived from consensus sequences of the mammalian glycoprotein hormone (GTH and TSH) receptors, cDNA was cloned from mRNA of ovaries of Asterina pectinifera. The cDNA showed striking structural homology with members of the glycoprotein hormone receptor family in the transmembrane region, and contained a very large extracellular region. Expression was observed in isolated ovarian follicle cells. Thus, it seems likely that the glycoprotein hormone receptor (GTHR) family gene is related to GSS receptor in ovarian follicle cells. The phylogenic relatedness of the starfish GTHR was also assessed in relation to other vertebrate GTHRs. The analysis showed that the starfish gene diverged before differentiation of the gonadotropin (LH and FSH) and TSH receptors in vertebrates.

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Optimization of Novel Follicle Culture System to Generate Developmentally Competent Oocytes

Indian Journal of Animal Research ◽

10.18805/ijar.b-1141 ◽

2020 ◽

Author(s):

Jongwon Kim ◽

Jung Kyu Choi

Keyword(s):

Culture System ◽

Ovarian Follicle ◽

Formation Rate ◽

Germinal Vesicle ◽

Ovarian Follicles ◽

Germinal Vesicle Breakdown ◽

Follicle Culture ◽

Nuclear Maturation ◽

Follicle Diameter

This study aimed to develop a novel culture system for porcine ovarian follicles that yields developmentally competent oocytes. We mechanically isolated ovarian follicles of various sizes 325–500 mm and treated them with ovine follicle stimulating hormone OFSH at different concentrations 0–400 mIU. Follicle diameter, antrum formation and cumulus oocyte complex COC recovery rate were significantly higher p andlt; 0.05 under the 0 and 50 mIU OFSH treatments compared with the remaining concentrations 100, 200 and 400 mIU. Additionally, follicles cultured for 3 and 4 d differed significantly p andlt; 0.05 in follicle diameter, antrum formation rate and COC recovery from those cultured for 5 and 6 d. Follicle characteristics did not differ across diameter: those at 250–300, 301–400 and 401–500 mm in vitro had antrum formation rates of 90%, 92% and 90%, along with COC recovery of 78%, 82% and 85%, respectively. Furthermore, nuclear maturation percentages for oocytes that experienced germinal vesicle breakdown (GVBD) were 10%, 13% and 14%, depending on the size of the originating follicle (250–300, 301–400 and 401–500 mm). Nuclear maturation for metaphase II (MII) oocytes derived from follicles of those three sizes were 1%, 2% and 1%, respectively. After 3 d of culture, the 250–300 mm group differed significantly from other size groups in follicle diameter and COC recovery. This study provides insight into establishing effective protocols of ovarian follicle culture, thus improving efforts to preserve large-mammal fertility.

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In Vitro Reconstruction of Xenopus Oocyte Ovulation

International Journal of Molecular Sciences ◽

10.3390/ijms20194766 ◽

2019 ◽

Vol 20 (19) ◽

pp. 4766 ◽

Cited By ~ 2

Author(s):

Alexander A. Tokmakov ◽

Yuta Matsumoto ◽

Takumi Isobe ◽

Ken-Ichi Sato

Keyword(s):

Mapk Pathway ◽

Germinal Vesicle ◽

Ovarian Follicles ◽

Follicle Cells ◽

Germinal Vesicle Breakdown ◽

Follicle Rupture ◽

Ovulation Inhibition ◽

The Matrix ◽

Clawed Frog

Progesterone is widely used to induce maturation of isolated fully grown oocytes of the African clawed frog, Xenopus laevis. However, the hormone fails to release oocytes from the layer of surrounding follicle cells. Here, we report that maturation and follicle rupture can be recapitulated in vitro by treating isolated follicular oocytes with progesterone and low doses of the matrix metalloproteinase (MMP), collagenase, which are ineffective in the absence of the steroid. Using this in vitro ovulation model, we demonstrate that germinal vesicle breakdown (GVBD) and oocyte liberation from ovarian follicles occur synchronously during ovulation. Inhibition of the MAPK pathway in these experimental settings suppresses both GVBD and follicular rupture, whereas inhibition of MMP activity delays follicular rupture without affecting GVBD. These results highlight importance of MAPK and MMP activities in the ovulation process and provide the first evidence for their involvement in the release of oocytes from ovarian follicles in frogs. The in vitro ovulation model developed in our study can be employed for further dissection of ovulation.

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Role of follicle wall in meiosis reinitiation induced by insulin in Rana pipiens oocytes

AJP Endocrinology and Metabolism ◽

10.1152/ajpendo.1981.241.1.e51 ◽

1981 ◽

Vol 241 (1) ◽

pp. E51-E56 ◽

Cited By ~ 4

Author(s):

C. A. Lessman ◽

A. W. Schuetz

Keyword(s):

Oocyte Maturation ◽

Rana Pipiens ◽

Ovarian Follicle ◽

Insulin Dose ◽

Germinal Vesicle ◽

Complete Removal ◽

Germinal Vesicle Breakdown ◽

Maturation In Vitro

The involvement of the ovarian follicle wall in insulin induction of Rana pipiens oocyte maturation in vitro was examined. Complete removal of the follicle wall significantly decreased, but did not obliterate, oocyte maturation (i.e., germinal vesicle breakdown, GVBD) induced by insulin. Dose-response studies of GVBD induction revealed that oocytes within intact follicles were at least 100 times more sensitive to insulin than denuded oocytes. Addition of cyanoketone, a steroid biosynthesis inhibitor, to intact follicles also suppressed insulin-induced GVBD. Inhibitory effects of either follicle wall removal or cyanoketone were not observed when denuded oocytes were treated with progesterone. Addition of either progesterone or pregnenolone to insulin-treated denuded oocytes augmented the oocyte GVBD response compared to either steroid alone and essentially replaced the effect of the follicle wall. In summary, steroidogenesis in the follicle wall appears to be a major factor contributing to the ability of insulin to induce GVBD. However, whether insulin stimulates follicle wall steroidogenesis or simply augments the biological activity of endogenous basal steroid levels is unresolved. The in vitro results show that oocyte maturation can be modulated by the combined actions of several hormones. Such steroid-insulin interactions may also be relevant to understanding the control of oocyte maturation in amphibians and other vertebrates, including mammals, under physiological conditions in vivo.

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Effect of insulin on spontaneous and progesterone-induced GVBD on Bufo arenarum denuded oocytes

Zygote ◽

10.1017/s0967199404002709 ◽

2004 ◽

Vol 12 (3) ◽

pp. 185-195 ◽

Cited By ~ 5

Author(s):

G. Sánchez Toranzo ◽

F. Bonilla ◽

L. Zelarayán ◽

J. Oterino ◽

M. I. Bühler

Keyword(s):

Germinal Vesicle ◽

Peptide Hormone ◽

Inhibitory Effect ◽

Reproductive Period ◽

Follicle Cells ◽

Germinal Vesicle Breakdown ◽

Bufo Arenarum ◽

Hormonal Stimulus ◽

Different Response ◽

Maturation Promoting Factor

Progesterone is considered as the physiological steroid hormone that triggers meiosis reinitiation in amphibian oocytes. Nevertheless, isolated oocytes can be induced to undergo germinal vesicle breakdown (GVBD) in a saline medium by means of treatment with various hormones or inducing agents such as other steroid hormones, insulin or an insulin-like growth factor. It has been demonstrated that Bufo arenarum oocytes obtained during the reproductive period (spring–summer) resume meiosis with no need of an exogenous hormonal stimulus if deprived of their enveloping follicle cells, a phenomenon called spontaneous maturation. This study was undertaken to evaluate the participation of the purine and phosphoinositide pathway in the insulin-induced maturation of oocytes competent and incompetent to mature spontaneously, as well as to determine whether the activation of the maturation promoting factor (MPF) involved the activation of cdc25 phosphatase in Bufo arenarum denuded oocytes. Our results indicate that insulin was able to induce GBVD in oocytes incompetent to mature spontaneously and to enhance spontaneous and progesterone-induced maturation. In addition, high intracellular levels of purines such as cAMP or guanosine can reversibly inhibit the progesterone and insulin-induced maturation process in Bufo arenarum as well as spontaneous maturation. Assays of the inhibition of phosphatidylinositol-4,5-bisphosphate (PIP2) hydrolysis and its turnover by neomycin and lithium chloride respectively exhibited a different response in insulin- or progesterone-treated oocytes, suggesting that phosphoinositide turnover or hydrolysis of PIP2 is involved in progesterone- but not in insulin-induced maturation. In addition, the inhibitory effect of vanadate suggests that an inactive pre-maturation promoting factor (pre-MPF), activated by dephosphorylation of Thr-14 and Tyr-15 on p34cdc2, is present in Bufo arenarum full-grown oocytes; this step would be common to both spontaneous and hormone-induced maturation. The data presented here strongly suggest that insulin initiates at the cell surface a chain of events leading to GVBD. However, our studies point to the existence of certain differences between the steroid and the peptide hormone pathways, although both involve the decrease in intracellular levels of cAMP, the activation of phosphodiesterase (PDE) and the activation of pre-MPF.

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Involvement of G protein and purines in Rhinella arenarum oocyte maturation

Zygote ◽

10.1017/s0967199411000657 ◽

2012 ◽

Vol 21 (3) ◽

pp. 221-230 ◽

Cited By ~ 2

Author(s):

L.I. Zelarayán ◽

M.T. Ajmat ◽

F. Bonilla ◽

M.I. Bühler

Keyword(s):

Germinal Vesicle ◽

Reproductive Period ◽

Follicle Cells ◽

Intracellular Camp ◽

Dependent Manner ◽

Germinal Vesicle Breakdown ◽

Membrane Effects ◽

Rhinella Arenarum ◽

Hormonal Stimulus ◽

Dose Dependent

SummaryWe investigated the participation of Gαi protein and of intracellular cAMP levels on spontaneous and progesterone-mediated maturation in Rhinella arenarum fully grown follicles and denuded oocytes.Although progesterone is the established maturation inducer in amphibians, Rhinella arenarum oocytes obtained during the reproductive period (competent oocytes) resume meiosis with no need for an exogenous hormonal stimulus if deprived of their enveloping follicular cells, a phenomenon called spontaneous maturation. In amphibian oocytes, numerous signalling mechanisms have been involved in the rapid, non-genomic, membrane effects of progesterone, but most of these are not fully understood.The data presented here demonstrate that activation of the Gαi protein by Mas-7 induced maturation in non-competent oocytes and also an increase in GVBD (germinal vesicle breakdown) in competent oocytes. Similar results were obtained with intact follicles independent of the season. The activation of adenylyl cyclase (AC) by forskolin seems to inhibit both spontaneous and progesterone-induced GVBD. In addition, the high intracellular levels of cAMP caused by activation of AC by forskolin treatment or addition of db-cAMP inhibited maturation that had been induced by Mas-7 and in a dose-dependent manner. Treatment with H-89, a protein kinase A (PKA) inhibitor, was able to trigger GVBD in a dose-dependent manner in non-competent oocytes and increased the percentages of GVBD in oocytes competent to mature spontaneously. The results obtained with whole follicles and denuded oocytes were similar, which suggested that effects on AC and PKA were not mediated by follicle cells. The fact that Mas-7 was able to induce maturation in non-competent oocytes in a similar manner to progesterone and to increase spontaneous maturation suggests that Gαi activation could be an important step in meiosis resumption. Thus, the decrease in cAMP as a result of the regulation of the G proteins on AC and the inactivation of PKA by H-89 could contribute to the activation of MPF (maturation promoting factor) and induce maturation of the oocytes of Rhinella arenarum.

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Oogenesis in Laetacara araguaiae (Ottoni and Costa, 2009) (Labriformes: Cichlidae)

Zygote ◽

10.1017/s0967199415000465 ◽

2015 ◽

Vol 24 (4) ◽

pp. 502-510 ◽

Cited By ~ 1

Author(s):

Amanda Pereira dos Santos-Silva ◽

Diógenes Henrique de Siqueira-Silva ◽

Alexandre Ninhaus-Silveira ◽

Rosicleire Veríssimo-Silveira

Keyword(s):

Ovarian Follicle ◽

Secondary Growth ◽

Cichlid Fish ◽

Germinal Vesicle ◽

Ornamental Fish ◽

Maturation Stage ◽

Adult Females ◽

Transmission Electron ◽

Cortical Alveolus ◽

Initial Deposition

SummaryWe aimed to analyze the oogenesis of adult females of the cichlid fish Laetacara araguaiae. The specimens’ gonads were removed and processed for light and transmission electron microscopy. Oogenesis in L. araguaiae showed the following characteristics: a germinal epithelium with three types of oogonia (A-undifferentiated, A-differentiated and B-oogonia), oocytes at meiotic prophase stage and ovarian follicle formation. Oocytes showing primary growth with pre-vitellogenic and cortical alveolus were observed. Similar to data for other cichlids, oocytes in secondary growth or vitellogenesis were characterized by the initial deposition of yolk microgranules. The event that characterizes the maturation stage is nucleolus migration, also called the germinal vesicle, to the oocyte periphery in the direction of the micropyle. The follicular complex undergoes several changes throughout the oocyte stages. To the best of our knowledge this study is the first to describe L. araguaiae oogenesis. Moreover, this study is the first step to better understand the reproductive biology of this species, which shows great potential for use as an ornamental fish.

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Activation of maturation promoting factor in Bufo arenarum oocytes: injection of mature cytoplasm and germinal vesicle contents

Zygote ◽

10.1017/s0967199406003820 ◽

2006 ◽

Vol 14 (4) ◽

pp. 305-316 ◽

Cited By ~ 5

Author(s):

G. Sánchez Toranzo ◽

F. Bonilla ◽

L. Zelarayán ◽

J. Oterino ◽

M.I. Bühler

Keyword(s):

Protein Synthesis ◽

Germinal Vesicle ◽

Reproductive Period ◽

Cyclin B ◽

Follicle Cells ◽

Cdc25 Phosphatase ◽

Germinal Vesicle Breakdown ◽

Bufo Arenarum ◽

Hormonal Stimulus ◽

Maturation Promoting Factor

SummaryAlthough progesterone is the established maturation inducer in amphibians, Bufo arenarum oocytes obtained during the reproductive period (spring–summer) resume meiosis with no need of an exogenous hormonal stimulus if deprived of their enveloping follicle cells, a phenomenon called spontaneous maturation. In this species it is possible to obtain oocytes competent and incompetent to undergo spontaneous maturation according to the seasonal period in which animals are captured. Reinitiation of meiosis is regulated by maturation promoting factor (MPF), a complex of the cyclin-dependent kinase p34cdc2 and cyclin B. Although the function and molecule of MPF are common among species, the formation and activation mechanisms of MPF differ according to species. This study was undertaken to evaluate the presence of pre-MPF in Bufo arenarum oocytes incompetent to mature spontaneously and the effect of the injection of mature cytoplasm or germinal vesicle contents on the resumption of meiosis. The results of our treatment of Bufo arenarum immature oocytes incompetent to mature spontaneously with sodium metavanadate (NaVO3) and dexamethasone (DEX) indicates that these oocytes have a pre-MPF, which activates and induces germinal vesicle breakdown (GVBD) by dephosphorylation on Thr-14/Tyr-15 by cdc25 phosphatase and without cyclin B synthesis. The injection of cytoplasm containing active MPF is sufficient to activate an amplification loop that requires the activation of cdc25 and protein kinase C, the decrease in cAMP levels, and is independent of protein synthesis. However, the injection of germinal vesicle content also induces GVBD in the immature receptor oocyte, a process dependent on protein synthesis but not on cdc25 phosphatase or PKC activity.

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