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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| Format: | Article |
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eLife Sciences Publications Ltd
2020-01-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/49774 |
| _version_ | 1811180739500179456 |
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| author | Natalia Wesolowska Ivan Avilov Pedro Machado Celina Geiss Hiroshi Kondo Masashi Mori Peter Lenart |
| author_facet | Natalia Wesolowska Ivan Avilov Pedro Machado Celina Geiss Hiroshi Kondo Masashi Mori Peter Lenart |
| author_sort | Natalia Wesolowska |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-11T09:07:14Z |
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| id | doaj.art-74385f3219b441b8b152dd61277bf0f5 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:07:14Z |
| publishDate | 2020-01-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-74385f3219b441b8b152dd61277bf0f52022-12-22T04:32:35ZengeLife Sciences Publications LtdeLife2050-084X2020-01-01910.7554/eLife.49774Actin assembly ruptures the nuclear envelope by prying the lamina away from nuclear pores and nuclear membranes in starfish oocytesNatalia Wesolowska0Ivan Avilov1Pedro Machado2Celina Geiss3Hiroshi Kondo4Masashi Mori5Peter Lenart6https://orcid.org/0000-0002-3927-248XCell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL), Heidelberg, GermanyMax Planck Institute for Biophysical Chemistry, Göttingen, GermanyElectron Microscopy Core Facility, European Molecular Biology Laboratory (EMBL), Heidelberg, GermanyCell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL), Heidelberg, GermanyCell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL), Heidelberg, GermanyCell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL), Heidelberg, GermanyCell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany; Max Planck Institute for Biophysical Chemistry, Göttingen, GermanyThe 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.https://elifesciences.org/articles/49774oocyte meiosisnuclear envelopestarfish oocyteselectron microscopysuperresolution |
| spellingShingle | Natalia Wesolowska Ivan Avilov Pedro Machado Celina Geiss Hiroshi Kondo Masashi Mori Peter Lenart Actin assembly ruptures the nuclear envelope by prying the lamina away from nuclear pores and nuclear membranes in starfish oocytes eLife oocyte meiosis nuclear envelope starfish oocytes electron microscopy superresolution |
| 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 | oocyte meiosis nuclear envelope starfish oocytes electron microscopy superresolution |
| url | https://elifesciences.org/articles/49774 |
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