1. Physics of Living Systems

Ezrin enrichment on curved membranes requires a specific conformation or interaction with a curvature-sensitive partner

  1. Feng-Ching Tsai  Is a corresponding author
  2. Aurelie Bertin
  3. Hugo Bousquet
  4. John Manzi
  5. Yosuke Senju
  6. Meng-Chen Tsai
  7. Laura Picas
  8. Stephanie Miserey-Lenkei
  9. Pekka Lappalainen
  10. Emmanuel Lemichez
  11. Evelyne Coudrier  Is a corresponding author
  12. Patricia Bassereau  Is a corresponding author
  1. Institut Curie, France
  2. University of Helsinki, Finland
  3. Université Côte d'Azur, France
  4. Institut de Recherche en Infectiologie de Montpellier (IRIM), France
  5. Institut Pasteur, France
https://doi.org/10.7554/eLife.37262
Share this article
Cite this article
  1. Feng-Ching Tsai
  2. Aurelie Bertin
  3. Hugo Bousquet
  4. John Manzi
  5. Yosuke Senju
  6. Meng-Chen Tsai
  7. Laura Picas
  8. Stephanie Miserey-Lenkei
  9. Pekka Lappalainen
  10. Emmanuel Lemichez
  11. Evelyne Coudrier
  12. Patricia Bassereau
(2018)
Ezrin enrichment on curved membranes requires a specific conformation or interaction with a curvature-sensitive partner
eLife 7:e37262.
https://doi.org/10.7554/eLife.37262
  2. Download BibTeX
  3. Download .RIS

Abstract

One challenge in cell biology is to decipher the biophysical mechanisms governing protein enrichment on curved membranes and the resulting membrane deformation. The ERM protein ezrin is abundant and associated with cellular membranes that are flat, positively or negatively curved. Using in vitro and cell biology approaches, we assess mechanisms of ezrin's enrichment on curved membranes. We evidence that wild-type ezrin (ezrinWT) and its phosphomimetic mutant T567D (ezrinTD) do not deform membranes but self-assemble anti-parallelly, zipping adjacent membranes. EzrinTD's specific conformation reduces intermolecular interactions, allows binding to actin filaments, which reduces membrane tethering, and promotes ezrin binding to positively-curved membranes. While neither ezrinTD nor ezrinWT senses negative curvature alone, we demonstrate that interacting with curvature-sensing I-BAR-domain proteins facilitates ezrin enrichment in negatively-curved membrane protrusions. Overall, our work demonstrates that ezrin can tether membranes, or be targeted to curved membranes, depending on conformations and interactions with actin and curvature-sensing binding partners.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for the following figuresFigure 1 - figure supplement 1C, 1D, and 1GFigure 4 - figure supplement 1A and 1B.

Article and author information

Author details

  1. Feng-Ching Tsai

    Laboratoire Physico Chimie Curie, Institut Curie, Paris, France
    For correspondence
    feng-ching.tsai@curie.fr
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6869-5254

  2. Aurelie Bertin

    Laboratoire Physico Chimie Curie, Institut Curie, Paris, France
    Competing interests
    No competing interests declared.

  3. Hugo Bousquet

    UMR 144, Institut Curie, Paris, France
    Competing interests
    No competing interests declared.

  4. John Manzi

    Laboratoire Physico Chimie Curie, Institut Curie, Paris, France
    Competing interests
    No competing interests declared.

  5. Yosuke Senju

    Program in Cell and Molecular Biology, Institute of Biotechnology, University of Helsinki, Helsinki, Finland
    Competing interests
    No competing interests declared.

  6. Meng-Chen Tsai

    CNRS, Institut de Pharmacologie Moléculaire et Cellulaire, Université Côte d'Azur, Valbonne, France
    Competing interests
    No competing interests declared.

  7. Laura Picas

    CNRS UMR 9004, Institut de Recherche en Infectiologie de Montpellier (IRIM), Montpellier, France
    Competing interests
    No competing interests declared.

  8. Stephanie Miserey-Lenkei

    UMR 144, Institut Curie, Paris, France
    Competing interests
    No competing interests declared.

  9. Pekka Lappalainen

    Program in Cell and Molecular Biology, Institute of Biotechnology, University of Helsinki, Helsinki, Finland
    Competing interests
    Pekka Lappalainen, Reviewing editor, eLife.

  10. Emmanuel Lemichez

    Département de Microbiologie, Unité des Toxines Bactériennes, Institut Pasteur, Paris, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9080-7761

  11. Evelyne Coudrier

    UMR 144, Institut Curie, Paris, France
    For correspondence
    Evelyne.Coudrier@curie.fr
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6011-8922

  12. Patricia Bassereau

    Laboratoire Physico Chimie Curie, Institut Curie, Paris, France
    For correspondence
    patricia.bassereau@curie.fr
    Competing interests
    Patricia Bassereau, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8544-6778

Funding

Agence Nationale de la Recherche (ANR-15-CE18-0016-03)

  • Meng-Chen Tsai
  • Emmanuel Lemichez
  • Patricia Bassereau

H2020 European Research Council (339847)

  • Stephanie Miserey-Lenkei
  • Evelyne Coudrier
  • Patricia Bassereau

Human Frontier Science Program (RGP0005/2016)

  • Yosuke Senju
  • Pekka Lappalainen
  • Evelyne Coudrier
  • Patricia Bassereau

European Molecular Biology Organization (ALTF 1527-2014)

  • Feng-Ching Tsai

H2020 Marie Skłodowska-Curie Actions (H2020-MSCA-IF-2014)

  • Feng-Ching Tsai

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

Reviewing Editor

  1. Anna Akhmanova, Utrecht University, Netherlands

Version history

  1. Received: April 4, 2018
  2. Accepted: September 14, 2018
  3. Accepted Manuscript published: September 20, 2018 (version 1)
  4. Version of Record published: October 1, 2018 (version 2)

Copyright

© 2018, Tsai 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.

Metrics

  • 3,542
    views
  • 558
    downloads
  • 35
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Feng-Ching Tsai
  2. Aurelie Bertin
  3. Hugo Bousquet
  4. John Manzi
  5. Yosuke Senju
  6. Meng-Chen Tsai
  7. Laura Picas
  8. Stephanie Miserey-Lenkei
  9. Pekka Lappalainen
  10. Emmanuel Lemichez
  11. Evelyne Coudrier
  12. Patricia Bassereau
(2018)
Ezrin enrichment on curved membranes requires a specific conformation or interaction with a curvature-sensitive partner
eLife 7:e37262.
https://doi.org/10.7554/eLife.37262

Share this article

https://doi.org/10.7554/eLife.37262

Categories and tags

Further reading

    1. Physics of Living Systems

    Substrate evaporation drives collective construction in termites

    Giulio Facchini, Alann Rathery ... Andrea Perna
    Research Article

    Termites build complex nests which are an impressive example of self-organization. We know that the coordinated actions involved in the construction of these nests by multiple individuals are primarily mediated by signals and cues embedded in the structure of the nest itself. However, to date there is still no scientific consensus about the nature of the stimuli that guide termite construction, and how they are sensed by termites. In order to address these questions, we studied the early building behavior of Coptotermes gestroi termites in artificial arenas, decorated with topographic cues to stimulate construction. Pellet collections were evenly distributed across the experimental setup, compatible with a collection mechanism that is not affected by local topography, but only by the distribution of termite occupancy (termites pick pellets at the positions where they are). Conversely, pellet depositions were concentrated at locations of high surface curvature and at the boundaries between different types of substrate. The single feature shared by all pellet deposition regions was that they correspond to local maxima in the evaporation flux. We can show analytically and we confirm experimentally that evaporation flux is directly proportional to the local curvature of nest surfaces. Taken together, our results indicate that surface curvature is sufficient to organize termite building activity and that termites likely sense curvature indirectly through substrate evaporation. Our findings reconcile the apparently discordant results of previous studies.

    1. Microbiology and Infectious Disease
    2. Physics of Living Systems

    Yeast cell responses and survival during periodic osmotic stress are controlled by glucose availability

    Fabien Duveau, Céline Cordier ... Pascal Hersen
    Research Article

    Natural environments of living organisms are often dynamic and multifactorial, with multiple parameters fluctuating over time. To better understand how cells respond to dynamically interacting factors, we quantified the effects of dual fluctuations of osmotic stress and glucose deprivation on yeast cells using microfluidics and time-lapse microscopy. Strikingly, we observed that cell proliferation, survival, and signaling depend on the phasing of the two periodic stresses. Cells divided faster, survived longer, and showed decreased transcriptional response when fluctuations of hyperosmotic stress and glucose deprivation occurred in phase than when the two stresses occurred alternatively. Therefore, glucose availability regulates yeast responses to dynamic osmotic stress, showcasing the key role of metabolic fluctuations in cellular responses to dynamic stress. We also found that mutants with impaired osmotic stress response were better adapted to alternating stresses than wild-type cells, showing that genetic mechanisms of adaptation to a persistent stress factor can be detrimental under dynamically interacting conditions.

    1. Physics of Living Systems

    Hydrodynamics and multiscale order in confluent epithelia

    Josep-Maria Armengol-Collado, Livio Nicola Carenza, Luca Giomi
    Research Article Updated

    We formulate a hydrodynamic theory of confluent epithelia: i.e. monolayers of epithelial cells adhering to each other without gaps. Taking advantage of recent progresses toward establishing a general hydrodynamic theory of p-atic liquid crystals, we demonstrate that collectively migrating epithelia feature both nematic (i.e. p = 2) and hexatic (i.e. p = 6) orders, with the former being dominant at large and the latter at small length scales. Such a remarkable multiscale liquid crystal order leaves a distinct signature in the system’s structure factor, which exhibits two different power-law scaling regimes, reflecting both the hexagonal geometry of small cells clusters and the uniaxial structure of the global cellular flow. We support these analytical predictions with two different cell-resolved models of epithelia – i.e. the self-propelled Voronoi model and the multiphase field model – and highlight how momentum dissipation and noise influence the range of fluctuations at small length scales, thereby affecting the degree of cooperativity between cells. Our construction provides a theoretical framework to conceptualize the recent observation of multiscale order in layers of Madin–Darby canine kidney cells and pave the way for further theoretical developments.