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γ-TuRCs and the augmin complex are required for the development of highly branched dendritic arbors in Drosophila

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Peer-reviewed

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Abstract

Microtubules are nucleated by γ-tubulin ring complexes (γ-TuRCs) and are essential for neuronal development. Nevertheless, γ-TuRC depletion has been reported to perturb only higher-order branching in elaborated Drosophila larval class IV dendritic arborization (da) neurons. This relatively mild phenotype has been attributed to defects in microtubule nucleation from Golgi outposts, yet most Golgi outposts lack associated γ-TuRCs. By analyzing dendritic arbor regrowth in pupae, we show that γ-TuRCs are also required for the growth and branching of primary and secondary dendrites, as well as for higher-order branching. Moreover, we identify the augmin complex (hereafter augmin), which recruits γ-TuRCs to the sides of pre-existing microtubules, as being required predominantly for higher-order branching. Augmin strongly promotes the anterograde growth of microtubules in terminal dendrites and thus terminal dendrite stability. Consistent with a specific role in higher-order branching, we find that augmin is expressed less strongly and is largely dispensable in larval class I da neurons, which exhibit few higher-order dendrites. Thus, γ-TuRCs are essential for various aspects of complex dendritic arbor development, and they appear to function in higher-order branching via the augmin pathway, which promotes the elaboration of dendritic arbors to help define neuronal morphology.

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Peer reviewed: True


Acknowledgements: We thank Melissa Rolls, Bing Ye and Yuh-Nung Jan for sharing fly lines. The work benefited from the Imaging Facility, Department of Zoology, University of Cambridge, supported by Matt Wayland and a Sir Isaac Newton Trust Research Grant (18.07ii(c)). We also acknowledge the ImagoSeine core facility of Institut Jacques Monod, member of France-BioImaging (ANR-10-INBS-04) and IBiSA, with the support of Labex “Who Am I”, Inserm Plan Cancer, Region Ile-de-France and Fondation Bettencourt Schueller.


Publication status: Published


Funder: Centre National de la Recherche Scientifique; Id: http://dx.do10.13039/10.13039/501100004794


Funder: Université Paris Cité; Id: http://dx.do10.13039/10.13039/501100009516


Funder: Royal Society; Id: http://dx.do10.13039/10.13039/501100000288


Funder: Isaac Newton Trust; Id: http://dx.do10.13039/10.13039/501100004815


Funder: University of Cambridge; Id: http://dx.do10.13039/10.13039/501100000735


Funder: Fondation Bettencourt Schueller; Id: http://dx.do10.13039/10.13039/501100007492

Journal Title

Journal of Cell Science

Conference Name

Journal ISSN

0021-9533
1477-9137

Volume Title

137

Publisher

The Company of Biologists Ltd

Rights and licensing

Except where otherwised noted, this item's license is described as http://creativecommons.org/licenses/by/4.0
Sponsorship
Wellcome Trust (105653/Z/14/Z)