Abstract
A complex program of translational repression, mRNA localization, and translational activation ensures that Oskar (Osk) protein accumulates only at the posterior pole of the Drosophila oocyte. Inappropriate expression of Osk disrupts embryonic axial patterning, and is lethal. A key factor in translational repression is Bruno (Bru), which binds to regulatory elements in the osk mRNA 3′ UTR. After posterior localization of osk mRNA, repression by Bru must be alleviated. Here we describe an in vivo assay system to monitor the spatial pattern of Bru-dependent repression, separate from the full complexity of osk regulation. This assay reveals a form of translational activation—region-specific activation—which acts regionally in the oocyte, is not mechanistically coupled to mRNA localization, and functions by inhibiting repression by Bru. We also show that Bru dimerizes and identify mutations that disrupt this interaction to test its role in vivo. Loss of dimerization does not disrupt repression, as might have been expected from an existing model for the mechanism of repression. However, loss of dimerization does impair regional activation of translation, suggesting that dimerization may constrain, not promote, repression. Our work provides new insight into the question of how localized mRNAs become translationally active, showing that repression of osk mRNA is locally inactivated by a mechanism acting independent of mRNA localization.
Highlights
Localized mRNAs function in many biological settings to facilitate region-specific protein synthesis [1,2,3]
Proteins are often enriched to specific regions within cells via localization of mRNAs
Translational repression could be a prerequisite for mRNA localization, if the act of translation interferes with that process
Summary
Localized mRNAs function in many biological settings to facilitate region-specific protein synthesis [1,2,3]. Translational repression of these mRNAs helps restrict distribution of the encoded proteins, an essential property if the protein has adverse effects at inappropriate locations. The Osk protein, whose distribution during oogenesis is restricted to the extreme posterior region of later stage oocytes, acts as a posterior determinant responsible for posterior patterning of the embryos and formation of the embryonic germline (reviewed in [5]). Mis- or overexpression of Osk, such that the protein is not tightly restricted to the posterior of the oocyte, leads to a reorganization of the embryonic body plan and ectopic formation of germ cells [7,8].
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