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Egalitarian binds dynein light chain to establish oocyte polarity and maintain oocyte fate

Abstract

In many cell types polarized transport directs the movement of mRNAs and proteins from their site of synthesis to their site of action, thus conferring cell polarity1. The cytoplasmic dynein microtubule motor complex is involved in this process. In Drosophila melanogaster, the Egalitarian (Egl) and Bicaudal-D (BicD) proteins are also essential for the transport of macromolecules to the oocyte and to the apical surface of the blastoderm embryo2,3,4,5. Hence, Egl and BicD, which have been shown to associate4, may be part of a conserved core localization machinery in Drosophila, although a direct association between these molecules and the dynein motor complex has not been shown. Here we report that Egl interacts directly with Drosophila dynein light chain (Dlc), a microtubule motor component, through an Egl domain distinct from that which binds BicD4. We propose that the Egl–BicD complex is loaded through Dlc onto the dynein motor complex thereby facilitating transport of cargo. Consistent with this model, point mutations that specifically disrupt Egl–Dlc association also disrupt microtubule-dependant trafficking both to and within the oocyte, resulting in a loss of oocyte fate maintenance and polarity. Our data provide a direct link between a molecule necessary for oocyte specification and the microtubule motor complex, and supports the hypothesis that microtubule-mediated transport is important for preserving oocyte fate.

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Figure 1: Egl associates directly with Dlc.
Figure 2: Oocyte fate maintenance is impaired in egl3e mutant ovaries.
Figure 3: egldlc2pt mutant ovaries show a phenotype similar to egl3e mutant ovaries.
Figure 4: dlc mutant germ-line clones do not maintain oocyte fate.

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Acknowledgements

We wish to thank the members of the Lehmann Lab past and present for advice and reading of the manuscript. We thank K. Albrecht, J. Morris, L. Gilboa, V. Barbosa, D. Ish-Horowicz, S. Bullock and I. Davis for discussions. We thank F. Pelegri and A. Ephrussi for originally isolating the egl3e allele and C. Chang for technical assistance. We also thank M. Grunwald for making the Egl-Myc transgenic line. C.N. was partially supported by the Ann L. Siegel fellowship of the American Cancer Society and the Howard Hughes Medical Institute. H.P., J.A. and A.S. are supported in part by a National Health and Medical Research Council Program grant. R.L. is an investigator of the Howard Hughes Medical Institute.

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Correspondence to Ruth Lehmann.

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Navarro, C., Puthalakath, H., Adams, J. et al. Egalitarian binds dynein light chain to establish oocyte polarity and maintain oocyte fate. Nat Cell Biol 6, 427–435 (2004). https://doi.org/10.1038/ncb1122

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