Somatic cells regulate maternal mRNA translation and developmental competence of mouse oocytes

Chen, Jing; Torcia, Simona; Xie, Fang; Lin, Chih-Jen; Çakmak, Hakan; Franciosi, Federica; Horner, Kathleen; Onodera, Courtney; Song, Jun S.; Cedars, Marcelle I.; Ramalho-Santos, Miguel; Conti, Marco

doi:10.1038/ncb2873

Cited by 140 publications

(122 citation statements)

References 48 publications

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“…Upon meiotic maturation, oocytes undergo two consecutive M phases and arrest again at metaphase of meiosis II (MII). Many maternal mRNAs are translationally activated during this process (Chen et al, 2013;Piccioni et al, 2005). These temporally translated proteins play key roles in meiotic spindle assembly, MII arrest maintenance and mRNA clearance during maternalzygotic transition (MZT).…”

Section: Introductionmentioning

confidence: 99%

A MAPK cascade couples maternal mRNA translation and degradation to meiotic cell cycle progression in mouse oocytes

et al. 2017

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Mammalian oocyte maturation depends on the translational activation of stored maternal mRNAs upon meiotic resumption. Cytoplasmic polyadenylation element binding protein 1 (CPEB1) is a key oocyte factor that regulates maternal mRNA translation. However, the signal that triggers CPEB1 activation at the onset of mammalian oocyte maturation is not known. We provide evidence that a mitogen-activated protein kinase (MAPK) cascade couples maternal mRNA translation to meiotic cell cycle progression in mouse oocytes by triggering CPEB1 phosphorylation and degradation. Mutations of the phosphorylation sites or ubiquitin E3 ligase binding sites in CPEB1 have a dominant-negative effect in oocytes, and mimic the phenotype of ERK1/2 knockout, by impairing spindle assembly and mRNA translation. Overexpression of the CPEB1 downstream translation activator DAZL in ERK1/2-deficient oocytes partially rescued the meiotic defects, indicating that ERK1/2 is essential for spindle assembly, metaphase II arrest and maternal-zygotic transition (MZT) primarily by triggering the translation of key maternal mRNAs. Taken together, ERK1/2-mediated CPEB1 phosphorylation/degradation is a major mechanism of maternal mRNA translational activation, and is crucial for mouse oocyte maturation and MZT.

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Section: Introductionmentioning

confidence: 99%

A MAPK cascade couples maternal mRNA translation and degradation to meiotic cell cycle progression in mouse oocytes

et al. 2017

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“…In general, this is achieved by modulating mRNA polyadenylation where translation is suppressed by poly-adenylation and activated by deadenylation to induce development and meiosis (11)(12)(13). Recent data have shown that translation of a subset of oocyte mRNAs that are critical for early embryo development are also under the control of surrounding follicular (granulosa) cell inputs (14), but the signals are still poorly understood.…”

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confidence: 99%

Identification of Maturation-Specific Proteins by Single-Cell Proteomics of Human Oocytes

Virant‐Klun

Leicht

Hughes

et al. 2016

Molecular & Cellular Proteomics

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Oocytes undergo a range of complex processes via oogenesis, maturation, fertilization, and early embryonic development, eventually giving rise to a fully functioning organism. To understand proteome composition and diversity during maturation of human oocytes, here we have addressed crucial aspects of oocyte collection and proteome analysis, resulting in the first proteome and secretome maps of human oocytes. Starting from 100 oocytes collected via a novel serum-free hanging drop culture system, we identified 2,154 proteins, whose function indicate that oocytes are largely resting cells with a proteome that is tailored for homeostasis, cellular attachment, and interaction with its environment via secretory factors.

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“…In follicle, activation of ERK1/2 is central for induction of oocyte maturation by the EGF pathway since inhibition of the EGF receptor abrogates cumulus expansion, oocyte maturation, and ovulation (46,47). Recently, it has been shown that cumulus cell derived EGF-like peptide (AREG) regulates translation of a subset of transcripts within the mouse oocyte during maturation, and perturbation of this factor affects oocyte quality (10). These reports indicate an important role of cAMP in oocyte maturation and acquisition of developmental competence through the EGF pathway.…”

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confidence: 99%

Transcriptomic analysis of cyclic AMP response in bovine cumulus cells

Khan

Guillemette

Sirard

et al. 2015

Physiological Genomics

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Khan DR, Guillemette C, Sirard MA, Richard FJ. Transcriptomic analysis of cyclic AMP response in bovine cumulus cells. Physiol Genomics 47: 432-442, 2015. First published June 16, 2015 doi:10.1152/physiolgenomics.00043.2015.-Acquisition of oocyte developmental competence needs to be understood to improve clinical outcomes of assisted reproduction. The stimulation of cumulus cell concentration of cyclic adenosine 3=5=-monophosphate (cAMP) by pharmacological agents during in vitro maturation (IVM) participates in improvement of oocyte quality. However, precise coordination and downstream targets of cAMP signaling in cumulus cells are largely unknown. We have previously demonstrated better embryo development after cAMP stimulation for first 6 h during IVM. Using this model, we investigated cAMP signaling in cumulus cells through in vitro culture of cumulus-oocyte complexes (COCs) in the presence of cAMP raising agents: forskolin, IBMX, and dipyridamole (here called FID treatment). Transcriptomic analysis of cumulus cells indicated that FID-induced differentially expressed transcripts were implicated in cumulus expansion, steroidogenesis, cell metabolism, and oocyte competence. Functional genomic analysis revealed that protein kinase-A (PKA), extracellular signal regulated kinases (ERK1/2), and calcium (Ca 2ϩ ) pathways as key regulators of FID signaling. Inhibition of PKA (H89) in FID-supplemented COCs or substitution of FID with calcium ionophore (A23187) demonstrated that FID activated primarily the PKA pathway which inhibited ERK1/2 phosphorylation and was upstream of calcium signaling. Furthermore, inhibition of ERK1/2 phosphorylation by FID supported a regulation by dual specific phosphatase (DUSP1) via PKA. Our findings imply that cAMP (FID) regulates cell metabolism, steroidogenesis, intracellular signaling and cumulus expansion through PKA which modulates these functions through optimization of ERK1/2 phosphorylation and coordination of calcium signaling. These findings have implications for development of new strategies for improving oocyte in vitro maturation leading to better developmental competence. cumulus cells; cyclic AMP; cell signaling; oocyte maturation; transcriptomics; PKA; ERK1/2 FOLLICULOGENESIS IS CHARACTERIZED by cumulus-oocyte communication, which heralds better oocyte competence. This communication is mediated by gap junctions and affects accumulation of maternal factors within the oocyte that are essential to support early embryonic development (49). Also, through gap junctions, cumulus cells transfer cyclic adenosine 3=5=-monophosphate (cAMP) to the oocyte where one role of cAMP is to maintain arrest at meiotic prophase-I (12, 50). Oocyte resumes meiotic division (oocyte maturation) either in response to preovulatory luteinizing hormone (LH) surge or on its removal from its follicular environment (13,18). Additionally, a decline in intracellular cAMP can induce oocyte meiotic resumption, which presages a progressive closure of cumulusoocyte cross talk and transfer of maternal factors t...

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Somatic cells regulate maternal mRNA translation and developmental competence of mouse oocytes

Cited by 140 publications

References 48 publications

A MAPK cascade couples maternal mRNA translation and degradation to meiotic cell cycle progression in mouse oocytes

A MAPK cascade couples maternal mRNA translation and degradation to meiotic cell cycle progression in mouse oocytes

Identification of Maturation-Specific Proteins by Single-Cell Proteomics of Human Oocytes

Transcriptomic analysis of cyclic AMP response in bovine cumulus cells

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