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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...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2021
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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. |
format | Online Article Text |
id | pubmed-8253823 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
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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