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Actin assembly ruptures the nuclear envelope by prying the lamina away from nuclear pores and nuclear membranes in starfish oocytes

The nucleus of oocytes (germinal vesicle) is unusually large and its nuclear envelope (NE) is densely packed with nuclear pore complexes (NPCs) that are stockpiled for embryonic development. We showed that breakdown of this specialized NE is mediated by an Arp2/3-nucleated F-actin ‘shell’ in starfis...

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Autores principales: Wesolowska, Natalia, Avilov, Ivan, Machado, Pedro, Geiss, Celina, Kondo, Hiroshi, Mori, Masashi, Lenart, Peter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7028370/
https://www.ncbi.nlm.nih.gov/pubmed/31989921
http://dx.doi.org/10.7554/eLife.49774
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author Wesolowska, Natalia
Avilov, Ivan
Machado, Pedro
Geiss, Celina
Kondo, Hiroshi
Mori, Masashi
Lenart, Peter
author_facet Wesolowska, Natalia
Avilov, Ivan
Machado, Pedro
Geiss, Celina
Kondo, Hiroshi
Mori, Masashi
Lenart, Peter
author_sort Wesolowska, Natalia
collection PubMed
description The nucleus of oocytes (germinal vesicle) is unusually large and its nuclear envelope (NE) is densely packed with nuclear pore complexes (NPCs) that are stockpiled for embryonic development. We showed that breakdown of this specialized NE is mediated by an Arp2/3-nucleated F-actin ‘shell’ in starfish oocytes, in contrast to microtubule-driven tearing in mammalian fibroblasts. Here, we address the mechanism of F-actin-driven NE rupture by correlated live-cell, super-resolution and electron microscopy. We show that actin is nucleated within the lamina, sprouting filopodia-like spikes towards the nuclear membranes. These F-actin spikes protrude pore-free nuclear membranes, whereas the adjoining stretches of membrane accumulate NPCs that are associated with the still-intact lamina. Packed NPCs sort into a distinct membrane network, while breaks appear in ER-like, pore-free regions. We reveal a new function for actin-mediated membrane shaping in nuclear rupture that is likely to have implications in other contexts, such as nuclear rupture observed in cancer cells.
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spelling pubmed-70283702020-02-20 Actin assembly ruptures the nuclear envelope by prying the lamina away from nuclear pores and nuclear membranes in starfish oocytes Wesolowska, Natalia Avilov, Ivan Machado, Pedro Geiss, Celina Kondo, Hiroshi Mori, Masashi Lenart, Peter eLife Cell Biology The nucleus of oocytes (germinal vesicle) is unusually large and its nuclear envelope (NE) is densely packed with nuclear pore complexes (NPCs) that are stockpiled for embryonic development. We showed that breakdown of this specialized NE is mediated by an Arp2/3-nucleated F-actin ‘shell’ in starfish oocytes, in contrast to microtubule-driven tearing in mammalian fibroblasts. Here, we address the mechanism of F-actin-driven NE rupture by correlated live-cell, super-resolution and electron microscopy. We show that actin is nucleated within the lamina, sprouting filopodia-like spikes towards the nuclear membranes. These F-actin spikes protrude pore-free nuclear membranes, whereas the adjoining stretches of membrane accumulate NPCs that are associated with the still-intact lamina. Packed NPCs sort into a distinct membrane network, while breaks appear in ER-like, pore-free regions. We reveal a new function for actin-mediated membrane shaping in nuclear rupture that is likely to have implications in other contexts, such as nuclear rupture observed in cancer cells. eLife Sciences Publications, Ltd 2020-01-28 /pmc/articles/PMC7028370/ /pubmed/31989921 http://dx.doi.org/10.7554/eLife.49774 Text en © 2020, Wesolowska et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Wesolowska, Natalia
Avilov, Ivan
Machado, Pedro
Geiss, Celina
Kondo, Hiroshi
Mori, Masashi
Lenart, Peter
Actin assembly ruptures the nuclear envelope by prying the lamina away from nuclear pores and nuclear membranes in starfish oocytes
title Actin assembly ruptures the nuclear envelope by prying the lamina away from nuclear pores and nuclear membranes in starfish oocytes
title_full Actin assembly ruptures the nuclear envelope by prying the lamina away from nuclear pores and nuclear membranes in starfish oocytes
title_fullStr Actin assembly ruptures the nuclear envelope by prying the lamina away from nuclear pores and nuclear membranes in starfish oocytes
title_full_unstemmed Actin assembly ruptures the nuclear envelope by prying the lamina away from nuclear pores and nuclear membranes in starfish oocytes
title_short Actin assembly ruptures the nuclear envelope by prying the lamina away from nuclear pores and nuclear membranes in starfish oocytes
title_sort actin assembly ruptures the nuclear envelope by prying the lamina away from nuclear pores and nuclear membranes in starfish oocytes
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7028370/
https://www.ncbi.nlm.nih.gov/pubmed/31989921
http://dx.doi.org/10.7554/eLife.49774
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