Electrostatic lateral interactions drive ESCRT-III heteropolymer assembly

  1. Sudeep Banjade
  2. Shaogeng Tang
  3. Yousuf H Shah
  4. Scott D Emr  Is a corresponding author
  1. Cornell University, United States

Abstract

Self-assembly of ESCRT-III complex is a critical step in all ESCRT-dependent events. ESCRT-III hetero-polymers adopt variable architectures, but the mechanisms of inter-subunit recognition in these hetero-polymers to create flexible architectures remain unclear. We demonstrate in vivo and in vitro that the Saccharomyces cerevisiae ESCRT-III subunit Snf7 uses a conserved acidic helix to recruit its partner Vps24. Charge-inversion mutations in this helix inhibit Snf7-Vps24 lateral interactions in the polymer, while rebalancing the charges rescues the functional defects. These data suggest that Snf7-Vps24 assembly occurs through electrostatic interactions on one surface, rather than through residue-to-residue specificity. We propose a model in which these cooperative electrostatic interactions in the polymer propagate to allow for specific inter-subunit recognition, while sliding of laterally interacting polymers enable changes in architecture at distinct stages of vesicle biogenesis. Our data suggest a mechanism by which interaction specificity and polymer flexibility can be coupled in membrane-remodeling heteropolymeric assemblies.

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All data generated are included in the manuscript and supporting files.

Article and author information

Author details

  1. Sudeep Banjade

    Weill Institute for Cell and Molecular Biology, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Shaogeng Tang

    Weill Institute of Cell and Molecular Biology, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3904-492X
  3. Yousuf H Shah

    Weill Institute of Cell and Molecular Biology, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Scott D Emr

    Weill Institute of Cell and Molecular Biology, Cornell University, Ithaca, United States
    For correspondence
    sde26@cornell.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5408-6781

Funding

Cornell University (CU3704)

  • Scott D Emr

Damon Runyon Cancer Research Foundation (DRG-2273-16)

  • Sudeep Banjade

National Institute of General Medical Sciences (T32GM007273)

  • Shaogeng Tang

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

Reviewing Editor

  1. William I Weis, Stanford University School of Medicine, United States

Version history

  1. Received: February 18, 2019
  2. Accepted: June 25, 2019
  3. Accepted Manuscript published: June 27, 2019 (version 1)
  4. Version of Record published: July 29, 2019 (version 2)

Copyright

© 2019, Banjade 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. Sudeep Banjade
  2. Shaogeng Tang
  3. Yousuf H Shah
  4. Scott D Emr
(2019)
Electrostatic lateral interactions drive ESCRT-III heteropolymer assembly
eLife 8:e46207.
https://doi.org/10.7554/eLife.46207

Share this article

https://doi.org/10.7554/eLife.46207

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