Inhibitory Action of Cyclic Guanosine 5′-Phosphoric Acid (GMP) on Oocyte Maturation: Dependence on an Intact Cumulus

Hubbard, Christopher; Terranova, Paul F.

doi:10.1095/biolreprod26.4.628

Cited by 45 publications

(21 citation statements)

References 11 publications

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“…Recent observations have re-proposed a role for cGMP in the control of oocyte meiotic arrest and meiotic maturation [21], [22], [41], [42], [43]. LH causes a profound decrease in cGMP in the follicle and in the oocyte, which in turn should lead to activation of PDE3A.…”

Section: Discussionmentioning

confidence: 99%

Genetic Dissection of Epidermal Growth Factor Receptor Signaling during Luteinizing Hormone-Induced Oocyte Maturation

2011

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Recent evidence that luteinizing hormone (LH) stimulation of ovulatory follicles causes transactivation of the epidermal growth factor receptor (EGFR) has provided insights into the mechanisms of ovulation. However, the complete array of signals that promote oocyte reentry into the meiotic cell cycle in the follicle are still incompletely understood. To elucidate the signaling downstream of EGFR involved in oocyte maturation, we have investigated the LH responses in granulosa cells with targeted ablation of EGFR. Oocyte maturation and ovulation is disrupted when EGFR expression is progressively reduced. In granulosa cells from mice with either global or granulosa cell-specific disruption of EGFR signaling, LH-induced phosphorylation of MAPK3/1, p38MAPK, and connexin-43 is impaired. Although the LH-induced decrease in cGMP is EGFR-dependent in wild type follicles, LH still induces a decrease in cGMP in Egfrdelta/f Cyp19-Cre follicles. Thus compensatory mechanisms appear activated in the mutant. Spatial propagation of the LH signal in the follicle also is dependent on the EGF network, and likely is important for the control of signaling to the oocyte. Thus, multiple signals and redundant pathways contribute to regulating oocyte reentry into the cell cycle.

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Section: Discussionmentioning

confidence: 99%

Genetic Dissection of Epidermal Growth Factor Receptor Signaling during Luteinizing Hormone-Induced Oocyte Maturation

2011

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“…A functional role of cGMP in inhibition of spontaneous oocyte maturation has been postulated [34]. Subsequently, Tornell et al [35] demonstrated that ANP-stimulated accumulation of cGMP in isolated rat oocyte-cumulus cellular complexes led to inhibition of spontaneous oocyte maturation.…”

Section: Discussionmentioning

confidence: 99%

Hormonal Regulation of Natriuretic Peptide System during Induced Ovarian Follicular Development in the Rat1

Gutkowska

Jankowski

Sairam

et al. 1999

Biology of Reproduction

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All components of the natriuretic peptide (NP) system have been found in the ovary. The purpose of this study was to determine the hormonal regulation of the NP system during follicular growth and ovulation induced by gonadotropins eCG and hCG. Ovarian membrane binding, before and after treatment, revealed the presence of guanylyl cyclase-type receptors exclusively. Equine CG treatment increased Bmax from 225 +/- 50 fmol/mg protein in control animals to 354 +/- 51 fmol/mg protein, and additional hCG treatment increased it further to 492 +/- 130 fmol/mg protein (p < 0.05), without changing receptor affinity. The increased binding was consistent with increased ability of atrial natriuretic peptide (ANP) to activate guanylyl cyclase in the ovarian cells obtained from hormone-treated animals. In confirmation, autoradiography of 125I-tyroCNP and 125I-ANP binding to the rat ovary showed that both guanylyl cyclase GC-A and GC-B receptor subtypes are localized to the granulosa cells of antral follicles. Quantitative analysis of GC-A and GC-B receptors by reverse transcription-polymerase chain reaction showed that the expression level of both receptors started to increase at 2 h and reached maximal levels at 6 h following eCG treatment. Increased levels of GC-B mRNA were also observed 12 h after eCG injection. At 24 and 48 h the receptor levels were below basal. Stimulation of NP receptors by eCG was paralleled by activation of both ovarian ANP and C-type natriuretic peptide (CNP) gene expression. ANP mRNA increased as early as 1 h after eCG injection and remained elevated up to 6 h. CNP mRNA increased at 2 h after eCG injection, peaked (5-fold) at 6 h, and remained elevated 48 h later, a stage at which follicular maturation continues. Incubation of ovaries with ANP significantly decreased eCG-induced estradiol level, indicating the functionality of the ovarian NP system. These results implicate the NP system in the induction and maintenance of fluid balance in the rapidly developing ovarian follicle.

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“…Because cGMP can delay spontaneous maturation in rat oocytes [27] and the cAMP:cGMP ratio increases before oocyte maturation [28], we explored possible roles of cGMP by using dbcGMP and the fairly specific inhibitor of PDE5, zaprinast, which is a PDE5 antagonist in somatic cells [29]. When dbcGMP was added to HxϩFF-MAS-cultured oocytes, %GVBD was significantly lower than in the HxϩFF-MAS control group (21.9% Ϯ 8.0% vs. 82.4% Ϯ 5.1%) ( Table 1).…”

Section: Pharmacological Inhibitors On Ff-mas-induced and Spontaneousmentioning

confidence: 99%

Resumption of Meiosis Induced by Meiosis-Activating Sterol Has a Different Signal Transduction Pathway than Spontaneous Resumption of Meiosis in Denuded Mouse Oocytes Cultured In Vitro1

Faerge

Terry²,

Kalous

et al. 2001

Biology of Reproduction

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The sterol 4,4-dimethyl-5-cholesta-8,14,24-trien-3-ol (follicular fluid meiosis-activating sterol [FF-MAS]) isolated from human follicular fluid induces resumption of meiosis in mouse oocytes cultured in vitro. The purpose of this study was to examine the hypothesis that differential signal transduction mechanisms exist for FF-MAS-induced and spontaneous in vitro resumption of meiosis in mouse oocytes. Mouse oocytes were dissected from ovaries originating from mice primed with FSH 48 h before oocyte collection. Mechanically denuded germinal vesicle (GV) oocytes were in vitro matured in medium supplemented with hypoxanthine and FF-MAS or allowed to mature spontaneously; both groups were exposed to individual compounds known to inhibit specific targets in the cell. After 20-22 h of in vitro maturation, resumption of meiosis was assessed as the frequency of oocytes in GV breakdown (GVBD) stage. Pertussis toxin (2.5 microg/ml) did not influence resumption of meiosis in either group. Dibutyryl cyclic GMP (320 microM) inhibited FF-MAS-induced GVBD, but not spontaneous GVBD, whereas the subtype 5 phosphodiesterase-inhibitor zaprinast (50 microM) inhibited GVBD in both groups. Microinjection of the catalytic subunit of cAMP-dependent protein kinase into oocytes inhibited spontaneous GVBD, but not FF-MAS-induced GVBD. An inhibitor of cytoplasmic polyadenylation, cordycepin (80 microM), inhibited or retarded spontaneous GVBD to a further extent than it did FF-MAS-induced GVBD. Spontaneous GVBD was more sensitive to the histone H1 kinase-inhibitor olomoucine (250 microM) than was FF-MAS-induced GVBD. Addition of the mitogen-activated protein kinase (MAPK)-inhibitor PD 98059 (50 microM), phospholipase C-inhibitor U-73122 (10 microM), p21(ras)-inhibitor lovastatine (250 microM), and the src-like kinase inhibitor PP2 (20 microg/ml) inhibited FF-MAS-induced GVBD, but not spontaneous GVBD. Both MAPKs, extracellular regulated kinase (ERK) 1 and ERK2, were phosphorylated under FF-MAS-induced meiotic resumption, in contrast to spontaneous meiotic resumption, in which ERK1 and ERK2 phosphorylation occurred 2 h after GVBD. In the present study, we show that FF-MAS acts through an MAPK-dependent pathway, and we suggest that src-like kinase, p21(ras), and phosphoinositide signaling lie upstream of MAPK in the FF-MAS-activated signaling pathway. Clearly, striking pathway differences are present between spontaneous versus FF-MAS-induced meiotic resumption.

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Inhibitory Action of Cyclic Guanosine 5′-Phosphoric Acid (GMP) on Oocyte Maturation: Dependence on an Intact Cumulus

Cited by 45 publications

References 11 publications

Genetic Dissection of Epidermal Growth Factor Receptor Signaling during Luteinizing Hormone-Induced Oocyte Maturation

Genetic Dissection of Epidermal Growth Factor Receptor Signaling during Luteinizing Hormone-Induced Oocyte Maturation

Hormonal Regulation of Natriuretic Peptide System during Induced Ovarian Follicular Development in the Rat1

Resumption of Meiosis Induced by Meiosis-Activating Sterol Has a Different Signal Transduction Pathway than Spontaneous Resumption of Meiosis in Denuded Mouse Oocytes Cultured In Vitro1

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