Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Deshpande, Ojas, de-Carvalho, Jorge, Vieira, Diana V., Telley, Ivo A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2021
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
_version_ 1784600023979261952
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
work_keys_str_mv AT deshpandeojas astralmicrotubulecrosslinkingsafeguardsuniformnucleardistributioninthedrosophilasyncytium
AT decarvalhojorge astralmicrotubulecrosslinkingsafeguardsuniformnucleardistributioninthedrosophilasyncytium
AT vieiradianav astralmicrotubulecrosslinkingsafeguardsuniformnucleardistributioninthedrosophilasyncytium
AT telleyivoa astralmicrotubulecrosslinkingsafeguardsuniformnucleardistributioninthedrosophilasyncytium