Rapid adaptation of endocytosis, exocytosis and eisosomes after an acute increase in membrane tension in yeast cells

  1. Joël Lemière
  2. Yuan Ren
  3. Julien Berro  Is a corresponding author
  1. Yale University, United States

Abstract

During clathrin-mediated endocytosis in eukaryotes, actin assembly is required to overcome large membrane tension and turgor pressure. However, the molecular mechanisms by which the actin machinery adapts to varying membrane tension remain unknown. In addition, how cells reduce their membrane tension when they are challenged by hypotonic shocks remains unclear. We used quantitative microscopy to demonstrate that cells rapidly reduce their membrane tension using three parallel mechanisms. In addition to using their cell wall for mechanical protection, yeast cells disassemble eisosomes to buffer moderate changes in membrane tension on a minute time scale. Meanwhile, a temporary reduction of the rate of endocytosis for 2 to 6 minutes, and an increase in the rate of exocytosis for at least 5 minutes allow cells to add large pools of membrane to the plasma membrane. We built on these results to submit the cells to abrupt increases in membrane tension and determine that the endocytic actin machinery of fission yeast cells rapidly adapts to perform clathrin-mediated endocytosis. Our study sheds light on the tight connection between membrane tension regulation, endocytosis and exocytosis.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Joël Lemière

    Department of Molecular Biophysics and Biochemistry, Department of Cell Biology, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Yuan Ren

    Department of Molecular Biophysics and Biochemistry, Department of Cell Biology, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Julien Berro

    Department of Molecular Biophysics and Biochemistry, Department of Cell Biology, Yale University, New Haven, United States
    For correspondence
    julien.berro@yale.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9560-8646

Funding

National Institute of General Medical Sciences (R01GM115636)

  • Julien Berro

American Cancer Society (IRG 58-012-58)

  • Julien Berro

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

Reviewing Editor

  1. Christophe Lamaze, Institut Curie

Version history

  1. Received: August 13, 2020
  2. Accepted: May 12, 2021
  3. Accepted Manuscript published: May 13, 2021 (version 1)
  4. Version of Record published: April 27, 2022 (version 2)

Copyright

© 2021, Lemière 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. Joël Lemière
  2. Yuan Ren
  3. Julien Berro
(2021)
Rapid adaptation of endocytosis, exocytosis and eisosomes after an acute increase in membrane tension in yeast cells
eLife 10:e62084.
https://doi.org/10.7554/eLife.62084

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