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Astral microtubule cross-linking safeguards uniform nuclear distribution in the Drosophila syncytium
The early insect embryo develops as a multinucleated cell distributing the genome uniformly to the cell cortex. Mechanistic insight for nuclear positioning beyond cytoskeletal requirements is missing. Contemporary hypotheses propose actomyosin-driven cytoplasmic movement transporting nuclei or repul...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Rockefeller University Press
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8594625/ https://www.ncbi.nlm.nih.gov/pubmed/34766978 http://dx.doi.org/10.1083/jcb.202007209 |
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author | Deshpande, Ojas de-Carvalho, Jorge Vieira, Diana V. Telley, Ivo A. |
author_facet | Deshpande, Ojas de-Carvalho, Jorge Vieira, Diana V. Telley, Ivo A. |
author_sort | Deshpande, Ojas |
collection | PubMed |
description | The early insect embryo develops as a multinucleated cell distributing the genome uniformly to the cell cortex. Mechanistic insight for nuclear positioning beyond cytoskeletal requirements is missing. Contemporary hypotheses propose actomyosin-driven cytoplasmic movement transporting nuclei or repulsion of neighbor nuclei driven by microtubule motors. Here, we show that microtubule cross-linking by Feo and Klp3A is essential for nuclear distribution and internuclear distance maintenance in Drosophila. Germline knockdown causes irregular, less-dense nuclear delivery to the cell cortex and smaller distribution in ex vivo embryo explants. A minimal internuclear distance is maintained in explants from control embryos but not from Feo-inhibited embryos, following micromanipulation-assisted repositioning. A dimerization-deficient Feo abolishes nuclear separation in embryo explants, while the full-length protein rescues the genetic knockdown. We conclude that Feo and Klp3A cross-linking of antiparallel microtubule overlap generates a length-regulated mechanical link between neighboring microtubule asters. Enabled by a novel experimental approach, our study illuminates an essential process of embryonic multicellularity. |
format | Online Article Text |
id | pubmed-8594625 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Rockefeller University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-85946252022-07-03 Astral microtubule cross-linking safeguards uniform nuclear distribution in the Drosophila syncytium Deshpande, Ojas de-Carvalho, Jorge Vieira, Diana V. Telley, Ivo A. J Cell Biol Article The early insect embryo develops as a multinucleated cell distributing the genome uniformly to the cell cortex. Mechanistic insight for nuclear positioning beyond cytoskeletal requirements is missing. Contemporary hypotheses propose actomyosin-driven cytoplasmic movement transporting nuclei or repulsion of neighbor nuclei driven by microtubule motors. Here, we show that microtubule cross-linking by Feo and Klp3A is essential for nuclear distribution and internuclear distance maintenance in Drosophila. Germline knockdown causes irregular, less-dense nuclear delivery to the cell cortex and smaller distribution in ex vivo embryo explants. A minimal internuclear distance is maintained in explants from control embryos but not from Feo-inhibited embryos, following micromanipulation-assisted repositioning. A dimerization-deficient Feo abolishes nuclear separation in embryo explants, while the full-length protein rescues the genetic knockdown. We conclude that Feo and Klp3A cross-linking of antiparallel microtubule overlap generates a length-regulated mechanical link between neighboring microtubule asters. Enabled by a novel experimental approach, our study illuminates an essential process of embryonic multicellularity. Rockefeller University Press 2021-11-12 /pmc/articles/PMC8594625/ /pubmed/34766978 http://dx.doi.org/10.1083/jcb.202007209 Text en © 2021 Deshpande et al. https://creativecommons.org/licenses/by-nc-sa/4.0/http://www.rupress.org/terms/This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/). |
spellingShingle | Article Deshpande, Ojas de-Carvalho, Jorge Vieira, Diana V. Telley, Ivo A. Astral microtubule cross-linking safeguards uniform nuclear distribution in the Drosophila syncytium |
title | Astral microtubule cross-linking safeguards uniform nuclear distribution in the Drosophila syncytium |
title_full | Astral microtubule cross-linking safeguards uniform nuclear distribution in the Drosophila syncytium |
title_fullStr | Astral microtubule cross-linking safeguards uniform nuclear distribution in the Drosophila syncytium |
title_full_unstemmed | Astral microtubule cross-linking safeguards uniform nuclear distribution in the Drosophila syncytium |
title_short | Astral microtubule cross-linking safeguards uniform nuclear distribution in the Drosophila syncytium |
title_sort | astral microtubule cross-linking safeguards uniform nuclear distribution in the drosophila syncytium |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8594625/ https://www.ncbi.nlm.nih.gov/pubmed/34766978 http://dx.doi.org/10.1083/jcb.202007209 |
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