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A release-and-capture mechanism generates an essential non-centrosomal microtubule array during tube budding

Non-centrosomal microtubule arrays serve crucial functions in cells, yet the mechanisms of their generation are poorly understood. During budding of the epithelial tubes of the salivary glands in the Drosophila embryo, we previously demonstrated that the activity of pulsatile apical-medial actomyosi...

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Autores principales: Gillard, Ghislain, Girdler, Gemma, Röper, Katja
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8253823/
https://www.ncbi.nlm.nih.gov/pubmed/34215746
http://dx.doi.org/10.1038/s41467-021-24332-0
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author Gillard, Ghislain
Girdler, Gemma
Röper, Katja
author_facet Gillard, Ghislain
Girdler, Gemma
Röper, Katja
author_sort Gillard, Ghislain
collection PubMed
description Non-centrosomal microtubule arrays serve crucial functions in cells, yet the mechanisms of their generation are poorly understood. During budding of the epithelial tubes of the salivary glands in the Drosophila embryo, we previously demonstrated that the activity of pulsatile apical-medial actomyosin depends on a longitudinal non-centrosomal microtubule array. Here we uncover that the exit from the last embryonic division cycle of the epidermal cells of the salivary gland placode leads to one centrosome in the cells losing all microtubule-nucleation capacity. This restriction of nucleation activity to the second, Centrobin-enriched, centrosome is key for proper morphogenesis. Furthermore, the microtubule-severing protein Katanin and the minus-end-binding protein Patronin accumulate in an apical-medial position only in placodal cells. Loss of either in the placode prevents formation of the longitudinal microtubule array and leads to loss of apical-medial actomyosin and impaired apical constriction. We thus propose a mechanism whereby Katanin-severing at the single active centrosome releases microtubule minus-ends that are then anchored by apical-medial Patronin to promote formation of the longitudinal microtubule array crucial for apical constriction and tube formation.
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spelling pubmed-82538232021-07-20 A release-and-capture mechanism generates an essential non-centrosomal microtubule array during tube budding Gillard, Ghislain Girdler, Gemma Röper, Katja Nat Commun Article Non-centrosomal microtubule arrays serve crucial functions in cells, yet the mechanisms of their generation are poorly understood. During budding of the epithelial tubes of the salivary glands in the Drosophila embryo, we previously demonstrated that the activity of pulsatile apical-medial actomyosin depends on a longitudinal non-centrosomal microtubule array. Here we uncover that the exit from the last embryonic division cycle of the epidermal cells of the salivary gland placode leads to one centrosome in the cells losing all microtubule-nucleation capacity. This restriction of nucleation activity to the second, Centrobin-enriched, centrosome is key for proper morphogenesis. Furthermore, the microtubule-severing protein Katanin and the minus-end-binding protein Patronin accumulate in an apical-medial position only in placodal cells. Loss of either in the placode prevents formation of the longitudinal microtubule array and leads to loss of apical-medial actomyosin and impaired apical constriction. We thus propose a mechanism whereby Katanin-severing at the single active centrosome releases microtubule minus-ends that are then anchored by apical-medial Patronin to promote formation of the longitudinal microtubule array crucial for apical constriction and tube formation. Nature Publishing Group UK 2021-07-02 /pmc/articles/PMC8253823/ /pubmed/34215746 http://dx.doi.org/10.1038/s41467-021-24332-0 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Gillard, Ghislain
Girdler, Gemma
Röper, Katja
A release-and-capture mechanism generates an essential non-centrosomal microtubule array during tube budding
title A release-and-capture mechanism generates an essential non-centrosomal microtubule array during tube budding
title_full A release-and-capture mechanism generates an essential non-centrosomal microtubule array during tube budding
title_fullStr A release-and-capture mechanism generates an essential non-centrosomal microtubule array during tube budding
title_full_unstemmed A release-and-capture mechanism generates an essential non-centrosomal microtubule array during tube budding
title_short A release-and-capture mechanism generates an essential non-centrosomal microtubule array during tube budding
title_sort release-and-capture mechanism generates an essential non-centrosomal microtubule array during tube budding
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8253823/
https://www.ncbi.nlm.nih.gov/pubmed/34215746
http://dx.doi.org/10.1038/s41467-021-24332-0
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