<i>Xenopus</i> oocyte prophase I meiotic arrest is released independently from a decrease in cAMP levels or PKA activity

Nader, Nader D.; Courjaret, Raphael Jean; Dib, Maya; Kulkarni, Rashmi; Machaca, Khaled

doi:10.1242/dev.136168

Cited by 19 publications

(22 citation statements)

References 84 publications

(105 reference statements)

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“…In fish and amphibians, follicle cells secrete steroid hormones that act on one or more types of oocyte membrane receptor. The extent and importance of the cAMP drop observed at maturation initiation vary in different systems studied, and other signaling pathways are likely to be important, at least in some species [39,40,43,44,45,46]. Upstream of the vertebrate follicle, LH production from the pituitary is under control of the master reproductive regulator GnRH receptor acting via Gα q and cytoplasmic Ca ++ release.…”

Section: Evolution Of Reproductive Regulationmentioning

confidence: 99%

“…In mouse oocytes, a cAMP decrease upon hormone stimulation triggers maturation; however, in fish and frog oocytes the degree and role of this decrease is debated. Several types of oocytes receptor (orange) may respond to steroid hormones (Pg) in different species of amphibians and fish, but the relative importance of multiple downstream signalling pathways remains to be clarified [1,43,44,45,46]. See text for discussion.…”

Section: Animalsmentioning

confidence: 99%

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A G protein–coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia

et al. 2020

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The reproductive hormones that trigger oocyte meiotic maturation and release from the ovary vary greatly between animal species. Identification of receptors for these maturation-inducing hormones (MIHs) and understanding how they initiate the largely conserved maturation process remain important challenges. In hydrozoan cnidarians including the jellyfish Clytia hemisphaerica, MIH comprises neuropeptides released from somatic cells of the gonad. We identified the receptor (MIHR) for these MIH neuropeptides in Clytia using cell culture-based "deorphanization" of candidate oocyte-expressed G protein-coupled receptors (GPCRs). MIHR mutant jellyfish generated using CRISPR-Cas9 editing had severe defects in gamete development or in spawning both in males and females. Female gonads, or oocytes isolated from MIHR mutants, failed to respond to synthetic MIH. Treatment with the cAMP analogue Br-cAMP to mimic cAMP rise at maturation onset rescued meiotic maturation and spawning. Injection of inhibitory antibodies to the alpha subunit of the G s heterodimeric protein (Gα S ) into wild-type oocytes phenocopied the MIHR mutants. These results provide the molecular links between MIH stimulation and meiotic maturation initiation in hydrozoan oocytes. Molecular phylogeny grouped Clytia MIHR with a subset of bilaterian neuropeptide receptors, including neuropeptide Y, gonadotropin inhibitory hormone (GnIH), pyroglutamylated RFamide, and luqin, all upstream regulators of sexual reproduction. This identification and functional characterization of a cnidarian peptide GPCR advances our understanding of oocyte maturation initiation and sheds light on the evolution of neuropeptide-hormone systems. OPEN ACCESSCitation: Quiroga Artigas G, Lapébie P, Leclère L, Bauknecht P, Uveira J, Chevalier S, et al. (2020) A G protein-coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia. PLoS Biol 18(3): e3000614. https:// ) to TM, as well as core funding kinase complex assures meiotic progression from prophase I arrest into M phase, while parallel Mos-MAP kinase activation steers polar body formation as well as cytostatic arrest once maturation is complete [2,3]. In contrast, the upstream physiological processes vary widely, as does the molecular nature of the maturation-inducing hormones (MIHs) that act on the oocyte to trigger maturation [1,4]. This reflects clade-specific acquisition of endocrine tissues such as ovarian follicles, the corpus cardiacum/corpus allatum in insects, or the pituitary in vertebrates [5,6]. These tissues act downstream of other neuroendocrine sites such as the vertebrate hypothalamus to integrate environmental, behavioral, and physiological information in order to achieve optimal conditions for gamete development and release [7]. The complex evolutionary history of hormonal reproductive regulation has made it challenging to unravel the crucial regulatory events operating within the oocyte at the onset of maturation.G protein-coupled receptors (GPCRs), the largest superfamily of integral ...

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Section: Evolution Of Reproductive Regulationmentioning

confidence: 99%

Section: Animalsmentioning

confidence: 99%

A G protein–coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia

et al. 2020

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“…Xenopus oocytes are arrested in the G2 stage of meiosis I 39 . The G2 arrest is maintained by AC-mediated production of cAMP which is believed to prevent oocyte maturation via PKA-mediated signalling events 39–41 . Hence, there is a constitutive production of cAMP in Xenopus oocytes.…”

Section: Discussionmentioning

confidence: 99%

Hydrogen sulfide stimulates CFTR in Xenopus oocytes by activation of the cAMP/PKA signalling axis

Perniss

Preiss

Nier

et al. 2017

Sci Rep

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Hydrogen sulfide (H2S) has been recognized as a signalling molecule which affects the activity of ion channels and transporters in epithelial cells. The cystic fibrosis transmembrane conductance regulator (CFTR) is an epithelial anion channel and a key regulator of electrolyte and fluid homeostasis. In this study, we investigated the regulation of CFTR by H2S. Human CFTR was heterologously expressed in Xenopus oocytes and its activity was electrophysiologically measured by microelectrode recordings. The H2S-forming sulphur salt Na2S as well as the slow-releasing H2S-liberating compound GYY4137 increased transmembrane currents of CFTR-expressing oocytes. Na2S had no effect on native, non-injected oocytes. The effect of Na2S was blocked by the CFTR inhibitor CFTR_inh172, the adenylyl cyclase inhibitor MDL 12330A, and the protein kinase A antagonist cAMPS-Rp. Na2S potentiated CFTR stimulation by forskolin, but not that by IBMX. Na2S enhanced CFTR stimulation by membrane-permeable 8Br-cAMP under inhibition of adenylyl cyclase-mediated cAMP production by MDL 12330A. These data indicate that H2S activates CFTR in Xenopus oocytes by inhibiting phosphodiesterase activity and subsequent stimulation of CFTR by cAMP-dependent protein kinase A. In epithelia, an increased CFTR activity may correspond to a pro-secretory response to H2S which may be endogenously produced by the epithelium or H2S-generating microflora.

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“…Constitutively active (CA) GPCRs in vertebrate oocytes maintain cytoplasmic cAMP levels high prior to maturation. Several types of oocytes receptor (orange) may respond to steroid hormones (Pg) in different species of amphibians and fish, but the relative importance of multiple downstream signalling pathways remains to be clarified [1,43,73,74]. See text for discussion.…”

Section: Figure 5 Mih-induced Oocyte Maturation Blocked By An Inhibimentioning

confidence: 99%

A G-protein-coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia

Artigas

Lapébie

Leclère

et al. 2019

Preprint

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The reproductive hormones that trigger oocyte meiotic maturation and release from the ovary vary greatly between animal species. Identification of receptors for these Maturation Inducing Hormones (MIHs), and understanding how they initiate the largely conserved maturation process, remain important challenges. In hydrozoan cnidarians including the jellyfish Clytia hemisphaerica, MIH comprises neuropeptides released from somatic cells of the gonad. We identified the receptor (MIHR) for these MIH neuropeptides in Clytia using cell culture-based "deorphanization" of candidate oocyte-expressed GPCRs. MIHR mutant jellyfish generated using CRISPR-Cas9 had severe defects in gamete development or in spawning both in males and females. Female gonads, or oocytes isolated from MIHR mutants, failed to respond to synthetic MIH. Treatment with the cAMP analogue 5'Br-cAMP to mimic cAMP rise at maturation onset rescued meiotic maturation and spawning. Injection of inhibitory antibodies to Gα S into wild type oocytes phenocopied the MIHR mutants. These results provide the molecular links between MIH stimulation and meiosis initiation in hydrozoan oocytes. Molecular phylogeny grouped Clytia MIHR with a subset of bilaterian neuropeptide receptors including Neuropeptide Y, Gonadotropin Inhibitory Hormone, pyroglutamylated RFamide and Luqin, all upstream regulators of sexual reproduction. This identification and functional characterisation of a cnidarian peptide GPCR advances our understanding of oocyte maturation initiation and sheds light on the evolution of neuropeptidehormone systems. Non-standard Abbreviations: MIH -Maturation Inducing Hormone; GVBD -Germinal VesicleBreakdown.

show abstract

Xenopus oocyte prophase I meiotic arrest is released independently from a decrease in cAMP levels or PKA activity

Cited by 19 publications

References 84 publications

A G protein–coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia

A G protein–coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia

Hydrogen sulfide stimulates CFTR in Xenopus oocytes by activation of the cAMP/PKA signalling axis

A G-protein-coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia

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