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

  1. Natalia Wesolowska
  2. Ivan Avilov
  3. Pedro Machado
  4. Celina Geiss
  5. Hiroshi Kondo
  6. Masashi Mori
  7. Peter Lenart  Is a corresponding author
  1. European Molecular Biology Laboratory (EMBL), Germany
  2. Max Planck Institute for Biophysical Chemistry, Germany

Abstract

The nucleus of oocytes (germinal vesicle) is unusually large and its nuclear envelope (NE) is densely packed with nuclear pore complexes (NPCs) 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 membrane stretches accumulate NPCs associated with the still-intact lamina. Packed NPCs sort into a distinct membrane network, while breaks appear in ER-like, pore-free regions. Thereby, 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.

Data availability

Full resolution EM montages are provided as supplemental files.

Article and author information

Author details

  1. Natalia Wesolowska

    Cell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Ivan Avilov

    Max Planck Institute for Biophysical Chemistry, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Pedro Machado

    Electron Microscopy Core Facility, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Celina Geiss

    Cell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Hiroshi Kondo

    Cell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Masashi Mori

    Cell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Peter Lenart

    Cell Biology and Biophysics Unit, Max Planck Institute for Biophysical Chemistry, Heidelberg, Germany
    For correspondence
    plenart@mpibpc.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3927-248X

Funding

Deutsche Forschungsgemeinschaft (SPP 1464)

  • Natalia Wesolowska

European Molecular Biology Laboratory

  • Natalia Wesolowska
  • Pedro Machado
  • Celina Geiss
  • Hiroshi Kondo
  • Masashi Mori
  • Peter Lenart

Max Planck Society

  • Ivan Avilov
  • Peter Lenart

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. R Dyche Mullins, University of California, San Francisco, United States

Version history

  1. Received: June 28, 2019
  2. Accepted: January 24, 2020
  3. Accepted Manuscript published: January 28, 2020 (version 1)
  4. Version of Record published: February 18, 2020 (version 2)

Copyright

© 2020, Wesolowska et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Natalia Wesolowska
  2. Ivan Avilov
  3. Pedro Machado
  4. Celina Geiss
  5. Hiroshi Kondo
  6. Masashi Mori
  7. Peter Lenart
(2020)
Actin assembly ruptures the nuclear envelope by prying the lamina away from nuclear pores and nuclear membranes in starfish oocytes
eLife 9:e49774.
https://doi.org/10.7554/eLife.49774

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https://doi.org/10.7554/eLife.49774

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