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Methylation of ESCRT-III components regulates the timing of cytokinetic abscission

Author

Listed:
  • Aurélie Richard

    (UMR7126 Epigenetics and Cell Fate)

  • Jérémy Berthelet

    (UMR7126 Epigenetics and Cell Fate)

  • Delphine Judith

    (Institut Cochin)

  • Tamara Advedissian

    (Institut Pasteur, Université Paris Cité, CNRS UMR3691, Membrane Traffic and Cell Division Unit)

  • Javier Espadas

    (University of Geneva)

  • Guillaume Jannot

    (UMR7126 Epigenetics and Cell Fate)

  • Angélique Amo

    (UMR7126 Epigenetics and Cell Fate)

  • Damarys Loew

    (PSL Research University, Centre de Recherche, CurieCoreTech Mass Spectrometry Proteomics)

  • Berangere Lombard

    (PSL Research University, Centre de Recherche, CurieCoreTech Mass Spectrometry Proteomics)

  • Alexandre G. Casanova

    (Institute for Advanced Biosciences)

  • Nicolas Reynoird

    (Institute for Advanced Biosciences)

  • Aurélien Roux

    (University of Geneva)

  • Clarisse Berlioz-Torrent

    (Institut Cochin)

  • Arnaud Echard

    (Institut Pasteur, Université Paris Cité, CNRS UMR3691, Membrane Traffic and Cell Division Unit)

  • Jonathan B. Weitzman

    (UMR7126 Epigenetics and Cell Fate)

  • Souhila Medjkane

    (UMR7126 Epigenetics and Cell Fate)

Abstract

Abscission is the final stage of cytokinesis, which cleaves the intercellular bridge (ICB) connecting two daughter cells. Abscission requires tight control of the recruitment and polymerization of the Endosomal Protein Complex Required for Transport-III (ESCRT-III) components. We explore the role of post-translational modifications in regulating ESCRT dynamics. We discover that SMYD2 methylates the lysine 6 residue of human CHMP2B, a key ESCRT-III component, at the ICB, impacting the dynamic relocation of CHMP2B to sites of abscission. SMYD2 loss-of-function (genetically or pharmacologically) causes CHMP2B hypomethylation, delayed CHMP2B polymerization and delayed abscission. This is phenocopied by CHMP2B lysine 6 mutants that cannot be methylated. Conversely, SMYD2 gain-of-function causes CHMP2B hypermethylation and accelerated abscission, specifically in cells undergoing cytokinetic challenges, thereby bypassing the abscission checkpoint. Additional experiments highlight the importance of CHMP2B methylation beyond cytokinesis, namely during ESCRT-III-mediated HIV-1 budding. We propose that lysine methylation signaling fine-tunes the ESCRT-III machinery to regulate the timing of cytokinetic abscission and other ESCRT-III dependent functions.

Suggested Citation

  • Aurélie Richard & Jérémy Berthelet & Delphine Judith & Tamara Advedissian & Javier Espadas & Guillaume Jannot & Angélique Amo & Damarys Loew & Berangere Lombard & Alexandre G. Casanova & Nicolas Reyno, 2024. "Methylation of ESCRT-III components regulates the timing of cytokinetic abscission," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47717-3
    DOI: 10.1038/s41467-024-47717-3
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    References listed on IDEAS

    as
    1. Aurélie Bertin & Nicola Franceschi & Eugenio Mora & Sourav Maity & Maryam Alqabandi & Nolwen Miguet & Aurélie Cicco & Wouter H. Roos & Stéphanie Mangenot & Winfried Weissenhorn & Patricia Bassereau, 2020. "Human ESCRT-III polymers assemble on positively curved membranes and induce helical membrane tube formation," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    2. Cyril Addi & Adrien Presle & Stéphane Frémont & Frédérique Cuvelier & Murielle Rocancourt & Florine Milin & Sandrine Schmutz & Julia Chamot-Rooke & Thibaut Douché & Magalie Duchateau & Quentin Giai Gi, 2020. "The Flemmingsome reveals an ESCRT-to-membrane coupling via ALIX/syntenin/syndecan-4 required for completion of cytokinesis," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
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