Rupture of nuclear envelope in starfish oocytes proceeds by F-actin-driven segregation of pore-dense and pore-free membranes

The nucleus of oocytes, traditionally referred to as the germinal vesicle, is unusually large and its nuclear envelope (NE) is densely packed with nuclear pore complexes (NPCs) stockpiled for embryonic development. We have shown that breakdown of this specialized NE during meiosis of starfish oocyte...

Full description

Saved in:
Bibliographic Details
Published inbioRxiv
Main Authors Wesolowska, Natalia, Machado, Pedro, Avilov, Ivan, Geiss, Celina, Kondo, Hiroshi, Mori, Masashi, Schwab, Yannick, Lenart, Peter
Format Paper
LanguageEnglish
Published Cold Spring Harbor Cold Spring Harbor Laboratory Press 28.06.2019
Subjects
Actin
Cytoskeleton
Electron microscopy
Filaments
Filopodia
Meiosis
Membrane vesicles
Membranes
Microscopy
Microtubules
Nuclear membranes
Oocytes
Rupture
Somatic cells
Tubules
Online AccessGet full text

Cover

More Information
Summary:The nucleus of oocytes, traditionally referred to as the germinal vesicle, is unusually large and its nuclear envelope (NE) is densely packed with nuclear pore complexes (NPCs) stockpiled for embryonic development. We have shown that breakdown of this specialized NE during meiosis of starfish oocytes is mediated by an Arp2/3-nucleated F-actin shell, in contrast to microtubule-driven tearing in somatic cells. The detailed mechanism of how the cytoskeletal forces disrupt the NE remains poorly understood in any system. Here, we address the mechanism of F-actin-driven NE rupture by using live-cell and correlated super-resolution light and electron microscopy. We show that actin is nucleated within the lamina and sprouts filopodia-like spikes towards the nuclear membranes forcing lamina and nuclear membranes apart. These F-actin spikes protrude pore-free nuclear membranes, whereas the adjoining membrane stretches accumulate packed NPCs associated with the still-intact lamin network. NPC conglomerates sort into a distinct tubular-vesicular membrane network, while breaks appear in pore-free, ER-like regions. Together, our work reveals a novel function for Arp2/3-mediated membrane shaping in NE rupture that is likely to have broad relevance in regulating NE dynamics in diverse other contexts such as nuclear rupture frequently observed in cancer cells. Footnotes * This is a revised version of the manuscript including additional high resolution light microscopy data. While the main findings remain the same, these new data significantly strengthened our conclusions and our proposed model for actin-driven nuclear envelope rupture.
DOI:10.1101/480434