piRNAs and Aubergine cooperate with Wispy poly(A) polymerase to stabilize mRNAs in the germ plasm

Dufourt, Jérémy; Bontonou, Gwénaëlle; Chartier, Aymeric; Jahan, Camille; Meunier, Anne Cécile; Pierson, Stéphanie; Harrison, Paul F.; Papin, Catherine; Beilharz, Traude H.; Simonelig, Martine

doi:10.1038/s41467-017-01431-5

Cited by 63 publications

(60 citation statements)

References 55 publications

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“…While intriguing, other studies have suggested that Aubergine may bind directly and preferentially to germ plasm‐enriched mRNAs to stabilize them. In contrast, in the soma Aubergine/mRNA interactions lead to mRNA degradation …”

Section: Ontogeny and Organization Of Germplasmmentioning

confidence: 99%

Germ granules in Drosophila

Trcek

Lehmann

2019

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Germ granules are hallmarks of all germ cells. Early ultrastructural studies in Drosophila first described these membraneless granules in the oocyte and early embryo as filled with amorphous to fibrillar material mixed with RNA. Genetic studies identified key protein components and specific mRNAs that regulate germ cell‐specific functions. More recently these ultrastructural studies have been complemented by biophysical analysis describing germ granules as phase‐transitioned condensates. In this review, we provide an overview that connects the composition of germ granules with their function in controlling germ cell specification, formation and migration, and illuminate these mysterious condensates as the gatekeepers of the next generation.

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Section: Ontogeny and Organization Of Germplasmmentioning

confidence: 99%

Germ granules in Drosophila

Trcek

Lehmann

2019

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124

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“…However, more subtle changes to adenylation-state can also be determined by such visualizations. For example, in a previous analysis in the fly embryo, as little as ~5% of a transcript population could be identified as differential between samples (27). We therefore propose that the experimental analysis tools are now in place to systematically mine RNAdriven cellular asymmetries in developmental and disease biology.…”

Section: Discussionmentioning

confidence: 97%

“…The steady-state transcriptome represents adenylated mRNA reflective of a spectrum of metabolic states that include newly-transcribed (long-tails), silenced (short-tails), reactivated (long-tails), actively-translated (mid-range-tail) and ageing transcripts (shortening-tails). Because the steadystate length represents a sum of these activities, we reasoned that visualization of the lengthdistribution might be more informative than a simple numerical descriptor such as the mean or median sequenced length, which may hide complex distribution patterns (Fig 2b; (27). We therefore generated an interactive visualization tool to analyze the cumulative distribution of poly(A)-lengths for any gene of interest.…”

Section: Gld-2 Broadly Regulates the Oogenic Transcriptomementioning

confidence: 99%

Widespread cytoplasmic polyadenylation programs asymmetry in the germline and early embryo

Boag

Harrison

Barugahare

et al. 2018

Preprint

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BACKGROUND:The program of embryonic development is launched by selective activation of a silent maternal transcriptome. In Caenorhabditis elegans, nuclei of the adult germline are responsible for the synthesis of at least two distinct mRNA populations; those required for housekeeping functions, and those that program the oocyte-to-embryo transition. We mapped this separation by changes to the length-distribution of poly(A)-tails that depend on GLD-2 mediated cytoplasmic polyadenylation and its regulators genome-wide. RESULTS:More than 1000 targets of cytoplasmic polyadenylation were identified by differential polyadenylation. Amongst mRNA with the greatest dependence on GLD-2 were those encoding RNA binding proteins with known roles in spatiotemporal patterning such as mex-5 and pos-1. In General, the 3' UTR of GLD-2 targets were longer, contained cytosine-patches, and were enriched for non-standard polyadenylation-motifs. To identify the deadenylase that initiated transcript silencing, we depleted the known deadenylases in the gld-2(0) mutant background. Only the loss of CCF-1 suppressed the short-tailed phenotype of GLD-2 targets suggesting that in addition to its general role in RNA turnover, this is the major deadenylase for regulatory silencing of maternal mRNA. Analysis of poly(A)-tail length-change in the embryo lacking specific RNA-binding proteins revealed new candidates for asymmetric expression in the first embryonic divisions. CONCLUSION:The concerted action of RNA binding proteins exquisitely regulates GLD-2 activity in space and time. We present our data as interactive web resources for a model where GLD-2 mediated cytoplasmic polyadenylation regulates target mRNA at each stage of worm germline and early embryonic development.

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“…More recently, we have demonstrated the role of Aubergine (Aub) in the localization of germ cell mRNAs to the germ plasm. 12,13 Aub is one of the three PIWI proteins in Drosophila. PIWI proteins belong to a specific clade of Argonaute proteins that bind 23-30 nucleotides (nt)-long small RNAs referred to as Piwiinteracting RNAs (piRNAs).…”

Section: Introductionmentioning

confidence: 99%

“…12,18 In contrast, in the germ plasm Aub recruits Wispy, the germline-specific cytoplasmic poly(A) polymerase, leading to poly(A) tail elongation and stabilization of Aub-bound mRNAs. 13 Thus, Aub and piRNAs play a central role in the localization of germ cell mRNAs through two opposite functions in mRNA stability: mRNA destabilization in the bulk of the embryo and stabilization in the germ plasm. The role of piRNAs and PIWI proteins in cellular mRNA regulation in other contexts, including mouse spermiogenesis and sex determination in Bombyx, also depends on their function in the regulation of mRNA stability.…”

Section: Introductionmentioning

confidence: 99%

The PIWI protein Aubergine recruits eIF3 to activate translation in the germ plasm

et al. 2020

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Piwi-interacting RNAs (piRNAs) and PIWI proteins are essential in germ cells to repress transposons and regulate mRNAs. In Drosophila, piRNAs bound to the PIWI protein Aubergine (Aub) are transferred maternally to the embryo and regulate maternal mRNA stability through two opposite roles. They target mRNAs by incomplete base pairing, leading to their destabilization in the soma and stabilization in the germ plasm. Here, we report a function of Aub in translation. Aub is required for translational activation of nanos mRNA, a key determinant of the germ plasm. Aub physically interacts with the poly(A)-binding protein (PABP) and the translation initiation factor eIF3. Polysome gradient profiling reveals the role of Aub at the initiation step of translation. In the germ plasm, PABP and eIF3d assemble in foci that surround Aub-containing germ granules, and Aub acts with eIF3d to promote nanos translation. These results identify translational activation as a new mode of mRNA regulation by Aub, highlighting the versatility of PIWI proteins in mRNA regulation.

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piRNAs and Aubergine cooperate with Wispy poly(A) polymerase to stabilize mRNAs in the germ plasm

Cited by 63 publications

References 55 publications

Germ granules in Drosophila

Germ granules in Drosophila

Widespread cytoplasmic polyadenylation programs asymmetry in the germline and early embryo

The PIWI protein Aubergine recruits eIF3 to activate translation in the germ plasm

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