The translation regulator Zar1l controls timing of meiosis in <i>Xenopus</i> oocytes

Heim, Andreas; Niedermeier, Marie L.; Stengel, Florian; Mayer, Thomas

doi:10.1242/dev.200900

Cited by 9 publications

(6 citation statements)

References 74 publications

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“…Additionally, one of the nonsynonymous mutations appears to be a de novo mutation in the New Mexico population that has risen to high frequency. The gene, ZAR1l, is important for coordination of mRNA translation during early embryonic development and is conserved across vertebrate lineages (Heim et al., 2022; Sangiorgio et al., 2008). Some of these outliers, particularly those that appear to have arisen de novo in specific populations, have reached high frequency, and were not segregating in the eastern sampling locations, may be the result of selection as painted turtles spread to inhabit the diverse environmental conditions of the western United States.…”

Section: Discussionmentioning

confidence: 99%

Demographic history and genomic signatures of selection in a widespread vertebrate ectotherm

Judson,

Hoekstra,

Janzen

2024

Molecular Ecology

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Environmental conditions vary greatly across large geographic ranges, and yet certain species inhabit entire continents. In such species, genomic sequencing can inform our understanding of colonization history and the impact of selection on the genome as populations experience diverse local environments. As ectothermic vertebrates are among the most vulnerable to environmental change, it is critical to understand the contributions of local adaptation to population survival. Widespread ectotherms offer an opportunity to explore how species can successfully inhabit such differing environments and how future climatic shifts will impact species' survival. In this study, we investigated the widespread painted turtle (Chrysemys picta) to assess population genomic structure, demographic history, and genomic signatures of selection in the western extent of the range. We found support for a substantial role of serial founder effects in shaping population genomic structure: demographic analysis and runs of homozygosity were consistent with bottlenecks of increasing severity from eastern to western populations during and following the Last Glacial Maximum, and edge populations were more strongly diverged and had less genetic diversity than those from the centre of the range. We also detected outlier loci, but allelic patterns in many loci could be explained by either genetic surfing or selection. While range expansion complicates the identification of loci under selection, we provide candidates for future study of local adaptation in a long‐lived, widespread ectotherm that faces an uncertain future as the global climate continues to rapidly change.

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Section: Discussionmentioning

confidence: 99%

Demographic history and genomic signatures of selection in a widespread vertebrate ectotherm

Judson,

Hoekstra,

Janzen

2024

Molecular Ecology

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“…However, this mouse regulatory region has a consensus site for ZAR1 binding (TSC element) (Charlesworth et al, 2012). It remains to be determined whether a Zar1 interaction contributes to the temporal pattern of translation observed, as proposed in Xenopus oocytes (Heim et al, 2022). In addition to a distinct initial timing of activation, translation between MI and MII follows a different pattern for the two mRNAs, with ribosome loading and the rate of translation of Mos reaching a plateau around 5-6 h or MI, whereas ribosome loading and translation of the CcnB1 mRNA continues to increase between MI and MII.…”

Section: Discussionmentioning

confidence: 99%

Multiple intersecting pathways are involved in the phosphorylation of CPEB1 to activate translation during mouse oocyte meiosis

Kunitomi,

Romero,

Daldello

et al. 2024

Preprint

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The RNA-binding protein cytoplasmic polyadenylation element binding 1 (CPEB1) plays a fundamental role in the regulation of mRNA translation in oocytes. However, the nature of protein kinase cascades modulating the activity of CPEB1 is still a matter of controversy. Using genetic and pharmacological tools and detailed time courses, here we have reevaluated the relationship between CPEB1 phosphorylation and the activation of translation during mouse oocyte maturation. We show that both the CDK1/MAPK and AURKA/PLK1 pathways converge on the phosphorylation of CPEB1 during prometaphase. Only inactivation of the CDK1/MAPK pathway disrupts translation, while inactivation of either pathway leads to CPEB1 stabilization. However, stabilization of CPEB1 induced by inactivation of the AURKA/PLK1 does not affect translation, indicating that destabilization/degradation can be dissociated from translational activation. The accumulation of the endogenous CCNB1 protein closely recapitulates the translation data. These findings support the overarching hypothesis that the activation of translation in prometaphase in mouse oocytes relies on a CDK1-dependent CPEB1 phosphorylation, and this translational activation precedes CPEB1 destabilization.

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“…9), additional “early events” may exist. Recently, a partial degradation of the RNA-Binding protein, Zar1L, was observed within 2 hrs after progesterone exposure and was proposed to regulate Mos translation [52]. Zar1L degradation is a potential “early event” that could be tested using our Cip1-based experimental approach and could provide a molecular link to the early translation of Mos.…”

Section: Discussionmentioning

confidence: 99%

Regulation of Oocyte Meiotic Maturation: Unraveling the Interplay between PKA Inhibition and Cdk1 Activation

Santoni,

Sekhsoukh,

Castella

et al. 2023

Preprint

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Oocyte meiosis is arrested at the first prophase stage, until hormonal stimulation triggers progression into the meiotic divisions. This process, called meiotic maturation, depends on extensive post-transcriptional events. In all vertebrates, two bottleneck events orchestrate meiosis resumption: first, the inhibition of PKA and, second, the activation of Cdk1, the master regulator of eukaryotic cell division. However, the molecular events occurring between these two steps are almost unknown. To address this issue, we took advantage of a Cdk1 inhibitor to identify the early events that depend on PKA downregulation and occur independently of Cdk1 activity. Unexpectedly, we show that accumulation of Cyclin B1 and Mos, the kinase responsible for MAPK activation in oocytes, are regulated in an opposing manner by a two-step mechanism. PKA downregulation induces first the accumulation of Cyclin B1 without any increase of its translation, independently of Cdk1 activation. Subsequently, the rate of Cyclin B1 translation increases in response to Cdk1 activation. In contrast, Mos translation begins downstream PKA inhibition, but the protein does not accumulate until Cdk1 is activated. These intertwined regulations create the positive feedback loops required for the full activation of Cdk1. Additionally, we show that two consecutive waves of translation occur during the G2-M transition, the first induced by PKA inhibition and the second by Cdk1 activation. Finally, we demonstrate that Arpp19, the only known early substrate of PKA inXenopusoocytes, is not involved in the control of these early events. This study reveals that PKA downregulation promotes multiple molecular pathways that converge on the activation of Cdk1 to induce the G2/M transition in vertebrate oocytes.

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The translation regulator Zar1l controls timing of meiosis in Xenopus oocytes

Cited by 9 publications

References 74 publications

Demographic history and genomic signatures of selection in a widespread vertebrate ectotherm

Demographic history and genomic signatures of selection in a widespread vertebrate ectotherm

Multiple intersecting pathways are involved in the phosphorylation of CPEB1 to activate translation during mouse oocyte meiosis

Regulation of Oocyte Meiotic Maturation: Unraveling the Interplay between PKA Inhibition and Cdk1 Activation

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