Letter | Published:

Splicing of oskar RNA in the nucleus is coupled to its cytoplasmic localization

Abstract

oskar messenger RNA localization at the posterior pole of the Drosophila oocyte is essential for germline and abdomen formation in the future embryo1,2. The nuclear shuttling proteins Y14/Tsunagi and Mago nashi are required for oskar mRNA localization, and they co-localize with oskar mRNA at the posterior pole of the oocyte3,4,5. Their human homologues, Y14/RBM8 and Magoh, are core components of the exon–exon junction complex (EJC)6,7,8,9. The EJC is deposited on mRNAs in a splicing-dependent manner, 20–24 nucleotides upstream of exon–exon junctions, independently of the RNA sequence6,7,8. This indicates a possible role of splicing in oskar mRNA localization, challenging the established notion that the oskar 3′ untranslated region (3′UTR) is sufficient for this process. Here we show that splicing at the first exon–exon junction of oskar RNA is essential for oskar mRNA localization at the posterior pole. We revisit the issue of sufficiency of the oskar 3′UTR for posterior localization and show that the localization of unrelated transcripts bearing the oskar 3′UTR is mediated by endogenous oskar mRNA. Our results reveal an important new function for splicing: regulation of messenger ribonucleoprotein complex assembly and organization for mRNA cytoplasmic localization.

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Acknowledgements

We thank A.-M. Voie for embryo injections for transgenesis, S. Curado for the oskA87, Nanos-Gal4:VP16 recombinant stock, A. Cyrklaff for the oskar in situ probe, P. Rørth for the pCog-Gal4:VP16 driver, D. St Johnston for anti-Staufen antibody, and members of the Ephrussi laboratory, V. Hachet and E. Izaurralde for advice and comments on the manuscript. O.H. was supported in part by a predoctoral ‘allocation de recherche’ from the French government.

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Correspondence to Anne Ephrussi.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Figure 1

oskΔi1 mRNA introns 2 and 3 are correctly spliced. (PDF 78 kb)

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Further reading

Figure 1: oskar mRNA produced from an intronless oskar gene fails to localize at the posterior of the oocyte.
Figure 2: The first intron of oskar is required for oskar mRNA localization.
Figure 3: Splicing at the first exon–exon junction of oskar mRNA is essential for its localization at the posterior pole of the oocyte.
Figure 4: lacZosk3′UTR mRNA localization at the posterior of the oocyte depends on endogenous oskar mRNA.

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