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Human ESCRT-III polymers assemble on positively curved membranes and induce helical membrane tube formation

Author

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  • Aurélie Bertin

    (Laboratoire Physico Chimie Curie, Institut Curie, PSL Research University, CNRS UMR168
    Sorbonne Université)

  • Nicola Franceschi

    (Laboratoire Physico Chimie Curie, Institut Curie, PSL Research University, CNRS UMR168
    Sorbonne Université
    Univ. Grenoble Alpes, CEA, CNRS, Institut de Biologie Structurale (IBS), 71, avenue des Martyrs)

  • Eugenio Mora

    (Laboratoire Physico Chimie Curie, Institut Curie, PSL Research University, CNRS UMR168
    Sorbonne Université)

  • Sourav Maity

    (Moleculaire Biofysica, Zernike Instituut, Rijksuniversiteit Groningen, Nijenborgh 4)

  • Maryam Alqabandi

    (Laboratoire Physico Chimie Curie, Institut Curie, PSL Research University, CNRS UMR168
    Sorbonne Université)

  • Nolwen Miguet

    (Univ. Grenoble Alpes, CEA, CNRS, Institut de Biologie Structurale (IBS), 71, avenue des Martyrs)

  • Aurélie Cicco

    (Laboratoire Physico Chimie Curie, Institut Curie, PSL Research University, CNRS UMR168
    Sorbonne Université)

  • Wouter H. Roos

    (Moleculaire Biofysica, Zernike Instituut, Rijksuniversiteit Groningen, Nijenborgh 4)

  • Stéphanie Mangenot

    (Laboratoire Physico Chimie Curie, Institut Curie, PSL Research University, CNRS UMR168
    Sorbonne Université)

  • Winfried Weissenhorn

    (Univ. Grenoble Alpes, CEA, CNRS, Institut de Biologie Structurale (IBS), 71, avenue des Martyrs)

  • Patricia Bassereau

    (Laboratoire Physico Chimie Curie, Institut Curie, PSL Research University, CNRS UMR168
    Sorbonne Université)

Abstract

Endosomal sorting complexes for transport-III (ESCRT-III) assemble in vivo onto membranes with negative Gaussian curvature. How membrane shape influences ESCRT-III polymerization and how ESCRT-III shapes membranes is yet unclear. Human core ESCRT-III proteins, CHMP4B, CHMP2A, CHMP2B and CHMP3 are used to address this issue in vitro by combining membrane nanotube pulling experiments, cryo-electron tomography and AFM. We show that CHMP4B filaments preferentially bind to flat membranes or to tubes with positive mean curvature. Both CHMP2B and CHMP2A/CHMP3 assemble on positively curved membrane tubes. Combinations of CHMP4B/CHMP2B and CHMP4B/CHMP2A/CHMP3 are recruited to the neck of pulled membrane tubes and reshape vesicles into helical “corkscrew-like” membrane tubes. Sub-tomogram averaging reveals that the ESCRT-III filaments assemble parallel and locally perpendicular to the tube axis, highlighting the mechanical stresses imposed by ESCRT-III. Our results underline the versatile membrane remodeling activity of ESCRT-III that may be a general feature required for cellular membrane remodeling processes.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-16368-5
    DOI: 10.1038/s41467-020-16368-5
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    Cited by:

    1. Nebojsa Jukic & Alma P. Perrino & Frédéric Humbert & Aurélien Roux & Simon Scheuring, 2022. "Snf7 spirals sense and alter membrane curvature," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. 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.
    3. B. Vijayalakshmi Ayyar & Khalil Ettayebi & Wilhelm Salmen & Umesh C. Karandikar & Frederick H. Neill & Victoria R. Tenge & Sue E. Crawford & Erhard Bieberich & B. V. Venkataram Prasad & Robert L. Atma, 2023. "CLIC and membrane wound repair pathways enable pandemic norovirus entry and infection," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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