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The golgin Lava lamp mediates dynein-based Golgi movements during Drosophila cellularization

Abstract

Drosophila melanogaster cellularization is a dramatic form of cytokinesis in which a membrane furrow simultaneously encapsulates thousands of cortical nuclei of the syncytial embryo to generate a polarized cell layer. Formation of this cleavage furrow depends on Golgi-based secretion and microtubules1,2,3. During cellularization, specific Golgi move along microtubules, first to sites of furrow formation and later to accumulate within the apical cytoplasm of the newly forming cells3. Here we show that Golgi movements and furrow formation depend on cytoplasmic dynein. Furthermore, we demonstrate that Lava lamp (Lva), a golgin protein that is required for cellularization, specifically associates with dynein, dynactin, cytoplasmic linker protein-190 (CLIP-190) and Golgi spectrin, and is required for the dynein-dependent targeting of the secretory machinery. The Lva domains that bind these microtubule-dependent motility factors inhibit Golgi movement and cellularization in a live embryo injection assay. Our results provide new evidence that golgins promote dynein-based motility of Golgi membranes.

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Figure 1: Golgi body movements are microtubule- and dynein-dependent.
Figure 2: Golgi-localized cytoplasmic dynein, Lva and spectrin associate in cellularizing embryos.
Figure 3: Lva binds microtubule motility factors through central and C-terminal domains, and Golgi membrane through N-terminal domains.
Figure 4: The microtubule motility-factor-binding domains of Lva disrupt Golgi movement and furrowing in live embryos, consistent with an adaptor model for Lva function.

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Acknowledgements

The authors thank B. Sullivan for his valued contributions during the early phase of this study, D. Branton, K. Miller, J. Scholey, C. Field, D. Ready, C. Field and B. Suter for their generous antibody gifts, A. Royou and R. Karess for the MyoII–GFP stock, A. De Lozanne, J. Fischer and W. Sullivan for their comments on the manuscript, S. Paige and L. Zhou for technical assistance, and the entire Sisson laboratory for contributions, both big and small. We sincerely apologize to those whose outstanding work was not cited due to referencing constraints. This study was supported by the National Institutes of Health grants GM067013 (J.C.S.) and GM053695 (T.S.H.), and The March of Dimes Basil O'Connor Award (J.C.S.).

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Correspondence to John C. Sisson.

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Papoulas, O., Hays, T. & Sisson, J. The golgin Lava lamp mediates dynein-based Golgi movements during Drosophila cellularization. Nat Cell Biol 7, 612–618 (2005). https://doi.org/10.1038/ncb1264

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