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An RNA-based Feed-forward Mechanism Ensures Motor Switching in Oskar MRNA Transport

Overview
Journal J Cell Biol
Specialty Cell Biology
Date 2023 May 22
PMID 37213090
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Abstract

Regulated recruitment and activity of motor proteins is essential for intracellular transport of cargoes, including messenger ribonucleoprotein complexes (RNPs). Here, we show that orchestration of oskar RNP transport in the Drosophila germline relies on interplay between two double-stranded RNA-binding proteins, Staufen and the dynein adaptor Egalitarian (Egl). We find that Staufen antagonizes Egl-mediated transport of oskar mRNA by dynein both in vitro and in vivo. Following delivery of nurse cell-synthesized oskar mRNA into the oocyte by dynein, recruitment of Staufen to the RNPs results in dissociation of Egl and a switch to kinesin-1-mediated translocation of the mRNA to its final destination at the posterior pole of the oocyte. We additionally show that Egl associates with staufen (stau) mRNA in the nurse cells, mediating its enrichment and translation in the ooplasm. Our observations identify a novel feed-forward mechanism, whereby dynein-dependent accumulation of stau mRNA, and thus protein, in the oocyte enables motor switching on oskar RNPs by downregulating dynein activity.

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References
1.
St Johnston D, Brown N, Gall J, JANTSCH M . A conserved double-stranded RNA-binding domain. Proc Natl Acad Sci U S A. 1992; 89(22):10979-83. PMC: 50466. DOI: 10.1073/pnas.89.22.10979. View

2.
Laver J, Li X, Ancevicius K, Westwood J, Smibert C, Morris Q . Genome-wide analysis of Staufen-associated mRNAs identifies secondary structures that confer target specificity. Nucleic Acids Res. 2013; 41(20):9438-60. PMC: 3814352. DOI: 10.1093/nar/gkt702. View

3.
Jambor H, Mueller S, Bullock S, Ephrussi A . A stem-loop structure directs oskar mRNA to microtubule minus ends. RNA. 2014; 20(4):429-39. PMC: 3964905. DOI: 10.1261/rna.041566.113. View

4.
Little S, Sinsimer K, Lee J, Wieschaus E, Gavis E . Independent and coordinate trafficking of single Drosophila germ plasm mRNAs. Nat Cell Biol. 2015; 17(5):558-68. PMC: 4417036. DOI: 10.1038/ncb3143. View

5.
Newmark P, BOSWELL R . The mago nashi locus encodes an essential product required for germ plasm assembly in Drosophila. Development. 1994; 120(5):1303-13. DOI: 10.1242/dev.120.5.1303. View