Multiple mechanisms collaborate to repress nanos translation in the Drosophila ovary and embryo

Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544, USA.
RNA (Impact Factor: 4.94). 04/2011; 17(5):967-77. DOI: 10.1261/rna.2478611
Source: PubMed


Translational control of gene expression is essential for development in organisms that rely on maternal mRNAs. In Drosophila, translation of maternal nanos (nos) mRNA must be restricted to the posterior of the early embryo for proper patterning of the anterior-posterior axis. Spatial control of nos translation is coordinated through the localization of a small subset of nos mRNA to the posterior pole late in oogenesis, activation of this localized mRNA, and repression of the remaining unlocalized nos mRNA throughout the bulk cytoplasm. Translational repression is mediated by the interaction of a cis-acting element in the nos 3' untranslated region with two proteins, Glorund (Glo) and Smaug (Smg), that function in the oocyte and embryo, respectively. The mechanism of Glo-dependent repression is unknown. Previous work suggests that Smg represses translation initiation but this model is not easily reconciled with evidence for polysome association of repressed nos mRNA. Using an in vitro translation system, we have decoupled translational repression of nos imposed during oogenesis from repression during embryogenesis. Our results suggest that both Glo and Smg regulate translation initiation, but by different mechanisms. Furthermore, we show that, during late oogenesis, nos translation is also repressed post-initiation and provide evidence that Glo mediates this event. This post-initiation block is maintained into embryogenesis during the transition to Smg-dependent regulation. We propose that the use of multiple modes of repression ensures inactivation of nos RNA that is translated at earlier stages of oogenesis and maintenance of this inactivate state throughout late oogenesis into embryogenesis.

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    • "RNAs rather than transcribe them de novo, consistent with the broad distribution of RNAs encoding Vasa and Seawi in early embryos that is later refined to the sMics during gastrulation (Juliano et al., 2006; Voronina et al., 2008). In other organisms such as Drosophila, mRNA localization is an important mechanism during early development (Becalska and Gavis, 2009) and localization of nanos RNA in the germ line depends on sites in its 3'-UTR (Andrews et al., 2011; Gavis et al., 1996). "
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    Molecular Reproduction and Development 07/2014; 81(8). DOI:10.1002/mrd.22223 · 2.53 Impact Factor
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    • "Alternatively, the dramatic increase in TTP levels that occurs during LPS stimulation could render the cellular levels of hnRNP F limiting for the interaction. The remodeling of mRNPs that takes place to allow mRNA degradation is generally associated with repression of translation initiation [46] and hnRNP F has previously been implicated in translational repression [33], [34], [47]; thus, an important question for future study is whether this activity of hnRNP F plays a role in TTP/BRF-mediated degradation of ARE-mRNAs. "
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    PLoS ONE 06/2014; 9(6):e100992. DOI:10.1371/journal.pone.0100992 · 3.23 Impact Factor
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    • "On the other hand, repression in late oocytes is poly(A) dependent, which may reflect an effect of Glorund on initiation as well. A comparison of the polysomal association of nos mRNA in total ovary extracts, which are enriched for early-stage oocytes, with that in late ovary and embryo extracts indicates a gradual shift to lighter fractions, consistent with the temporal acquisition of distinct mechanisms of translational repression (Andrews et al. 2011). "
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