At the end of cell division, the nuclear envelope reassembles around the decondensing chromosomes. Female meiosis culminates in two consecutive cell divisions of the oocyte, meiosis I and II, which are separated by a brief transition phase known as interkinesis. Due to the absence of chromosome decondensation and the suppression of genome replication during interkinesis, it has been widely assumed that the nuclear envelope does not reassemble between meiosis I and II. By analyzing interkinesis in C. elegans oocytes, we instead show that an atypical structure made of two lipid bilayers, which we termed the interkinetic envelope, surrounds the surface of the segregating chromosomes. The interkinetic envelope shares common features with the nuclear envelope but also exhibits specific characteristics that distinguish it, including its lack of continuity with the endoplasmic reticulum, unique protein composition, assembly mechanism, and function in chromosome segregation. These distinct attributes collectively define the interkinetic envelope as a unique and specialized structure that has been previously overlooked.
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December 26 2024
An interkinetic envelope surrounds chromosomes between meiosis I and II in C. elegans oocytes
Layla El Mossadeq
,
Layla El Mossadeq
(Conceptualization, Investigation, Methodology, Visualization, Writing - original draft, Writing - review & editing)
1
Université Paris Cité, CNRS, Institut Jacques Monod
, Paris, France
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Laura Bellutti
,
Laura Bellutti
(Investigation, Methodology)
1
Université Paris Cité, CNRS, Institut Jacques Monod
, Paris, France
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Rémi Le Borgne
,
Rémi Le Borgne
(Methodology, Visualization)
1
Université Paris Cité, CNRS, Institut Jacques Monod
, Paris, France
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Julie C. Canman
,
Julie C. Canman
(Methodology, Writing - review & editing)
2Department of Pathology and Cell Biology,
Columbia University
, New York, NY, USA
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Lionel Pintard
,
Lionel Pintard
(Methodology)
1
Université Paris Cité, CNRS, Institut Jacques Monod
, Paris, France
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Jean-Marc Verbavatz
,
Jean-Marc Verbavatz
(Methodology, Supervision)
1
Université Paris Cité, CNRS, Institut Jacques Monod
, Paris, France
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Peter Askjaer
,
Peter Askjaer
(Methodology, Resources)
3
Andalusian Center for Developmental Biology, CSIC/JA/Universidad Pablo de Olavide
, Seville, Spain
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Julien Dumont
(Conceptualization, Funding acquisition, Investigation, Methodology, Project administration, Supervision, Visualization, Writing - original draft, Writing - review & editing)
1
Université Paris Cité, CNRS, Institut Jacques Monod
, Paris, France
Correspondence to Julien Dumont: [email protected]
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Layla El Mossadeq
Conceptualization, Investigation, Methodology, Visualization, Writing - original draft, Writing - review & editing
1
Université Paris Cité, CNRS, Institut Jacques Monod
, Paris, France
Laura Bellutti
Investigation, Methodology
1
Université Paris Cité, CNRS, Institut Jacques Monod
, Paris, France
Rémi Le Borgne
Methodology, Visualization
1
Université Paris Cité, CNRS, Institut Jacques Monod
, Paris, France
Julie C. Canman
Methodology, Writing - review & editing
2Department of Pathology and Cell Biology,
Columbia University
, New York, NY, USA
Lionel Pintard
Methodology
1
Université Paris Cité, CNRS, Institut Jacques Monod
, Paris, France
Jean-Marc Verbavatz
Methodology, Supervision
1
Université Paris Cité, CNRS, Institut Jacques Monod
, Paris, France
Peter Askjaer
Methodology, Resources
3
Andalusian Center for Developmental Biology, CSIC/JA/Universidad Pablo de Olavide
, Seville, Spain
Correspondence to Julien Dumont: [email protected]
Disclosures: The authors declare no competing interests exist.
Received:
March 20 2024
Revision Received:
September 24 2024
Accepted:
November 18 2024
Online ISSN: 1540-8140
Print ISSN: 0021-9525
Funder(s):
Centre National de la Recherche Scientifique
Funder(s):
University Paris Cité
Funder(s):
National Institutes of Health
- Award Id(s): R01GM117407,R01GM130764
Funder(s):
Spanish Agencia Estatal de Investigación
Funder(s):
European Regional Development Fund
- Award Id(s): PID2019-105069GB-I00
Funder(s):
Ligue Nationale Contre le Cancer
- Award Id(s): RS30J21DOC17_ELMOSSADEQ
Funder(s):
European Research Council
- Award Id(s): ERC-CoG ChromoSOMe 819179
© 2024 El Mossadeq et al.
2024
El Mossadeq et al.
This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
This work is licensed under a
Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License
.
J Cell Biol (2025) 224 (3): e202403125.
Article history
Received:
March 20 2024
Revision Received:
September 24 2024
Accepted:
November 18 2024
Citation
Layla El Mossadeq, Laura Bellutti, Rémi Le Borgne, Julie C. Canman, Lionel Pintard, Jean-Marc Verbavatz, Peter Askjaer, Julien Dumont; An interkinetic envelope surrounds chromosomes between meiosis I and II in C. elegans oocytes. J Cell Biol 3 March 2025; 224 (3): e202403125. doi: https://doi.org/10.1083/jcb.202403125
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