Managing the Oocyte Meiotic Arrest—Lessons from Frogs and Jellyfish

Jessus, Catherine; Munro, Catriona; Houliston, Evelyn

doi:10.3390/cells9051150

Cited by 25 publications

(33 citation statements)

References 239 publications

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“…Furthermore, the proposed model focuses on the early steps downstream of mPR and does not encompass the complexity of the multiple signaling pathways that have been implicated in the release of Xenopus oocyte meiotic arrest in addition to mPR signaling, including G-protein coupled receptors, cAMP-PKA, and RNA polyadenylation to regulate translation to name a few (reviewed in [ 15 , 62 , 63 ]). In addition, to significant crosstalk between the different signaling cascades, including the Mos-MAPK and Plk1 kinase cascades [ 64 ].…”

Section: Discussionmentioning

confidence: 99%

Membrane progesterone receptor induces meiosis in Xenopus oocytes through endocytosis into signaling endosomes and interaction with APPL1 and Akt2

et al. 2020

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The steroid hormone progesterone (P4) mediates many physiological processes through either nuclear receptors that modulate gene expression or membrane P4 receptors (mPRs) that mediate nongenomic signaling. mPR signaling remains poorly understood. Here we show that the topology of mPRβ is similar to adiponectin receptors and opposite to that of G-protein-coupled receptors (GPCRs). Using Xenopus oocyte meiosis as a well-established physiological readout of nongenomic P4 signaling, we demonstrate that mPRβ signaling requires the adaptor protein APPL1 and the kinase Akt2. We further show that P4 induces clathrin-dependent endocytosis of mPRβ into signaling endosome, where mPR interacts transiently with APPL1 and Akt2 to induce meiosis. Our findings outline the early steps involved in mPR signaling and expand the spectrum of mPR signaling through the multitude of pathways involving APPL1.

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Section: Discussionmentioning

confidence: 99%

Membrane progesterone receptor induces meiosis in Xenopus oocytes through endocytosis into signaling endosomes and interaction with APPL1 and Akt2

et al. 2020

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“…However, the role of BiD in influencing cytoskeletal dynamics is not well understood, and this effect of cytaster induction has not been reported before. Interestingly, RSK is a component of the MAPK pathway, which is responsible for the suppression of cell cycle progression and MT growth, in eggs of many species (Jessus et al, 2020;McDougall et al, 2012;Stephano and Gould, 2000). Additionally, depletion of RSK in human cells has been seen to result in a loss of MT nucleation and polymerization (Park et al, 2016).…”

Section: Bi-d1870-induced Cytasters In Phallusia Oocytes Form a Hexagonal Latticementioning

confidence: 99%

Self-organized optimal packing of kinesin-5-driven microtubule asters scales with cell size

Khetan

Prulière

Hebras

et al. 2021

Journal of Cell Science

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Radial microtubule (MT) arrays or asters determine cell geometry in animal cells. Multiple asters interacting with motors such as in syncytia form intracellular patterns, but the mechanical principles are not clear. Here, we report oocytes of the marine ascidian Phallusia mammillata treated with a drug BI-D1870 spontaneously form cytoplasmic MT asters, or cytasters. These asters form steady state segregation patterns in a shell just under the membrane. Cytaster centers tessellate the oocyte cytoplasm, i.e. divide it into polygonal structures, dominated by hexagons in a kinesin-5 dependent manner, while inter-aster MTs form ‘mini-spindles’. A computational model of multiple asters interacting with kinesin-5 can reproduce both tessellation patterns and mini-spindles in a manner specific to MTs per aster, MT lengths and kinesin-5 density. Simulations predict the hexagonal tessellation patterns scale with increasing cell size, when the packing fraction of asters in cells∼1.6. This self-organized in vivo tessellation by cytasters is comparable to the ‘circle packing problem’, suggesting an intrinsic mechanical pattern forming module potentially relevant to understand the role of collective mechanics of cytoskeletal elements in embryogenesis.

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“…It is well established that the prophase arrest of fully-grown vertebrate oocytes is maintained by high levels of cAMP and activity of the cAMP-dependent kinase (PKA) [41][42][43]. In Xenopus oocytes, the constitutively active Gαs-protein coupled receptor 185 (GPR185) results in high adenylate cyclase activity that maintains the high levels of cAMP [44].…”

Section: The Interplay Between Pka and Protein Synthesismentioning

confidence: 99%

Translational Control of Xenopus Oocyte Meiosis: Toward the Genomic Era

Meneau

Dupré

Jessus

et al. 2020

Cells

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The study of oocytes has made enormous contributions to the understanding of the G2/M transition. The complementarity of investigations carried out on various model organisms has led to the identification of the M-phase promoting factor (MPF) and to unravel the basis of cell cycle regulation. Thanks to the power of biochemical approaches offered by frog oocytes, this model has allowed to identify the core signaling components involved in the regulation of M-phase. A central emerging layer of regulation of cell division regards protein translation. Oocytes are a unique model to tackle this question as they accumulate large quantities of dormant mRNAs to be used during meiosis resumption and progression, as well as the cell divisions during early embryogenesis. Since these events occur in the absence of transcription, they require cascades of successive unmasking, translation, and discarding of these mRNAs, implying a fine regulation of the timing of specific translation. In the last years, the Xenopus genome has been sequenced and annotated, enabling the development of omics techniques in this model and starting its transition into the genomic era. This review has critically described how the different phases of meiosis are orchestrated by changes in gene expression. The physiological states of the oocyte have been described together with the molecular mechanisms that control the critical transitions during meiosis progression, highlighting the connection between translation control and meiosis dynamics.

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Managing the Oocyte Meiotic Arrest—Lessons from Frogs and Jellyfish

Cited by 25 publications

References 239 publications

Membrane progesterone receptor induces meiosis in Xenopus oocytes through endocytosis into signaling endosomes and interaction with APPL1 and Akt2

Membrane progesterone receptor induces meiosis in Xenopus oocytes through endocytosis into signaling endosomes and interaction with APPL1 and Akt2

Self-organized optimal packing of kinesin-5-driven microtubule asters scales with cell size

Translational Control of Xenopus Oocyte Meiosis: Toward the Genomic Era

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