Cortical microtubule pulling forces contribute to the union of the parental genomes in the C. elegans zygote

Abstract

Previously, we reported that the Polo-like kinase PLK-1 phosphorylates the single C. elegans lamin (LMN-1) to trigger lamina depolymerization during mitosis. We showed that this event is required to form a pronuclear envelopes scission event that removes membranes on the juxtaposed oocyte and sperm pronuclear envelopes in the zygote, allowing the parental chromosomes to merge in a single nucleus after segregation (Velez-Aguilera et al., 2020). Here we show that cortical microtubule pulling forces contribute to pronuclear envelopes scission by promoting mitotic spindle elongation, and conversely, nuclear envelope remodeling facilitates spindle elongation. We also demonstrate that weakening the pronuclear envelopes via PLK-1-mediated lamina depolymerization, is a prerequisite for the astral microtubule pulling forces to trigger pronuclear membranes scission. Finally, we provide evidence that PLK-1 mainly acts via lamina depolymerization in this process. These observations thus indicate that temporal coordination between lamina depolymerization and mitotic spindle elongation facilitates pronuclear envelopes scission and parental genomes unification.

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All the raw data are provided in the manuscript

Article and author information

Author details

  1. Griselda Velez-Aguilera

    Cell Cycle and Development, Institut Jacques Monod, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9662-8833
  2. Batool Ossareh-Nazari

    Cell Cycle and Development, Institut Jacques Monod, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Lucie Van Hove

    Cell Cycle and Development, Institut Jacques Monod, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Nicolas Joly

    Cell Cycle and Development, Institut Jacques Monod, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Lionel Pintard

    Cell Cycle and Development, Institut Jacques Monod, Paris, France
    For correspondence
    Lionel.PINTARD@ijm.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0286-4630

Funding

Agence Nationale de la Recherche (ANR-17-CE13-0011)

  • Lionel Pintard

Consejo Nacional de Ciencia y Tecnología (CVU 364106)

  • Griselda Velez-Aguilera

Agence Nationale de la Recherche (ANR-18-IDEX-0001)

  • Nicolas Joly

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

Reviewing Editor

  1. Jon Pines, Institute of Cancer Research Research, United Kingdom

Publication history

  1. Preprint posted: November 19, 2021 (view preprint)
  2. Received: November 19, 2021
  3. Accepted: March 4, 2022
  4. Accepted Manuscript published: March 8, 2022 (version 1)
  5. Version of Record published: March 25, 2022 (version 2)

Copyright

© 2022, Velez-Aguilera 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. Griselda Velez-Aguilera
  2. Batool Ossareh-Nazari
  3. Lucie Van Hove
  4. Nicolas Joly
  5. Lionel Pintard
(2022)
Cortical microtubule pulling forces contribute to the union of the parental genomes in the C. elegans zygote
eLife 11:e75382.
https://doi.org/10.7554/eLife.75382
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