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Posttranscriptional regulation in Drosophila oocytes and early embryos

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Abstract Molecular asymmetries underlying embryonic axis patterning and germ cell specification are established in Drosophila largely by position‐dependent translational regulation of maternally expressed messenger RNAs. Here, I review several mechanisms of posttranscriptional regulation in the Drosophila oocyte and syncytial embryo, and how they relate to embryonic patterning, with a strong emphasis on the most recent advances in the area. The review is not exhaustive, but focuses on examples that illustrate the interplay between specific regulatory events and the general metabolic machinery that governs translation and mRNA stability. Biophysical investigations into how the Bicoid gradient is formed are discussed, as are the elaborate mechanisms controlling how the Oskar and Nanos proteins become restricted to the posterior pole of the embryo. Work on Vasa, a translational activator of some germ line mRNAs and on 4EHP, a negative regulator that unproductively binds the 5′ cap structure of target mRNAs, is also briefly reviewed. Finally, the emerging understanding of the role of microRNAs in regulating translation of germ line mRNAs is also discussed. WIREs RNA 2011 2 408–416 DOI: 10.1002/wrna.70 This article is categorized under: Translation > Translation Regulation RNA Export and Localization > RNA Localization RNA in Disease and Development > RNA in Development

The anterior determinant Bcd is present in an anterior–posterior gradient in the early Drosophila embryo. bcd mRNA is deposited into the oocyte starting in mid‐oogenesis. It accumulates at the anterior pole but forms its own gradient. After egg activation and fertilization Bcd is synthesized from the spatially restricted mRNA.

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Proposed mechanism for Vas‐mediated translational activation of mei‐P26. Vas binds specifically to a U‐rich motif in the 3′ UTR of mei‐P26, and interacts directly with eIF5B. Thus, it could promote recruitment of the large ribosomal subunit (60S) to the small ribosomal subunit (40S) that is positioned at the translational start site (AUG), allowing elongation to proceed.

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Translational repression of cad at the anterior involves 4EHP, a cap‐binding protein that cannot bind eIF4G and thus cannot nucleate a translationally active cap‐binding complex. Note that this mechanism differs from that of Cup, which sequesters eIF4E. Here, competition is between 4EHP and eIF4E for binding to the cap.

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Translational repression of nos involves several mechanisms. A 90‐nucleotide region of the nos 3′ UTR termed the translational control element (TCE) contains binding sites for translational repressors. Glo binds to the stem of stem–loop III (SLIII) and represses nos translation during late oogenesis through an unknown mechanism. Smg binds to the loop of stem–loop II and can either recruit Cup, which sequesters eIF4E as for osk, or promote deadenylation of nos by recruiting the CCR4 deadenylase through a direct association with its POP2 subunit.

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Translational repression of unlocalized osk involves prevention of cap‐binding complex assembly. Bru binds to specific 3′ UTR elements (BRE, Bruno‐response elements) and recruits Cup, which in turn competes with eIF4G for binding to eIF4E. For simplicity only one BRE is shown, but three such elements are actually present in the osk 3′ UTR.

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mRNA localization and spatially restricted translational control restrict Osk and Nos to the posterior pole plasm of the oocyte. osk and nos mRNAs are deposited into the oocyte starting in mid‐oogenesis, and they preferentially accumulate at the posterior pole. However, these localization mechanisms are inefficient and a large proportion of these mRNAs remain outside this region. The unlocalized mRNAs are translationally repressed through several mechanisms, while these mRNAs are translationally active in the pole plasm. Less is known about the processes of derepression and activation of these mRNAs.

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Translation > Translation Regulation
RNA Export and Localization > RNA Localization
RNA in Disease and Development > RNA in Development

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