ESCRT-III-dependent adhesive and mechanical changes are triggered by a mechanism detecting alteration of Septate Junction integrity in Drosophila epithelial cells

  1. Thomas Esmangart de Bournonville
  2. Mariusz K Jaglarz
  3. Emeline Durel
  4. Roland Le Borgne  Is a corresponding author
  1. École Polytechnique Fédérale de Lausanne, Switzerland
  2. Jagiellonian University, Poland
  3. University of Rennes 1, CNRS, UMR 6290, France

Abstract

Barrier functions of proliferative epithelia are constantly challenged by mechanical and chemical constraints. How epithelia respond to and cope with disturbances of barrier functions to allow tissue integrity maintenance is poorly characterized. Cellular junctions play an important role in this process and intracellular traffic contribute to their homeostasis. Here, we reveal that, in Drosophila pupal notum, alteration of the bi- or tricellular septate junctions (SJs) triggers a mechanism with two prominent outcomes. On one hand, there is an increase in the levels of E-cadherin, F-Actin and non-muscle Myosin II in the plane of adherens junctions. On the other hand, β-integrin/Vinculin-positive cell contacts are reinforced along the lateral and basal membranes. We found that the weakening of SJ integrity, caused by the depletion of bi- or tricellular SJ components, alters ESCRT-III/Vps32/Shrub distribution, reduces degradation and instead favours recycling of SJ components, an effect that extends to other recycled transmembrane protein cargoes including Crumbs, its effector β-Heavy Spectrin Karst, and β-integrin. We propose a mechanism by which epithelial cells, upon sensing alterations of the septate junction, reroute the function of Shrub to adjust the balance of degradation/recycling of junctional cargoes and thereby compensate for barrier junction defects to maintain epithelial integrity.

Data availability

All data generated or analysed during this study are included in the manuscript and the supporting data files have been made available on Dryad and includes the data set DOI_10.5061_dryad.dbrv15f7h__v1. This dataset includes original stacks of confocal images from Fig. 1B-D and E-G, Fig. 2A,B,E and F, Fig. 3 A-D, Fig. 4 A-E, Fig. 5A,A',B,B',and D, Fig. 6 A-E' , Fig. 1S1 A-B and C,C', Fig. 2S1 A-B, D and E, Fig. 3S1 A,A' and C,C', , Fig. 5S1A-B', Fig. 5S2 A,B', and Fig.6S1 A-A' (including as well the confocal stacks used for quantification and statistical analyses); and detailed statistical analyses (Excel tables or Rtables) of Fig. 1 B'-D' and E'-G', Fig. 2 A',C,D and G, Fig. 5 C',D' and E, Fig. 6 F and G, Fig. 1S1 B',D and E, Fig 2S1 C,D' and E', Fig 3S1 B,D, Fig. 5S2 C and S6.

The following data sets were generated

Article and author information

Author details

  1. Thomas Esmangart de Bournonville

    Global Health Institute, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6012-1726
  2. Mariusz K Jaglarz

    Department of Developmental Biology and Invertebrate Morphology, Jagiellonian University, Krakow, Poland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1606-8339
  3. Emeline Durel

    Institut de Génétique et Développement de Rennes, University of Rennes 1, CNRS, UMR 6290, Rennes, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Roland Le Borgne

    Institut de Génétique et Développement de Rennes, University of Rennes 1, CNRS, UMR 6290, Rennes, France
    For correspondence
    roland.leborgne@univ-rennes1.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6892-278X

Funding

Fondation pour la Recherche Médicale (FDT202001010770)

  • Thomas Esmangart de Bournonville

Agence Nationale de la Recherche (ANR-20-CE13-0015)

  • Roland Le Borgne

Fondation ARC pour la Recherche sur le Cancer (PJA 20191209388)

  • Roland Le Borgne

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

Reviewing Editor

  1. Utpal Banerjee, University of California, Los Angeles, United States

Version history

  1. Received: July 25, 2023
  2. Accepted: February 1, 2024
  3. Accepted Manuscript published: February 2, 2024 (version 1)
  4. Accepted Manuscript updated: February 5, 2024 (version 2)

Copyright

© 2024, Esmangart de Bournonville 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. Thomas Esmangart de Bournonville
  2. Mariusz K Jaglarz
  3. Emeline Durel
  4. Roland Le Borgne
(2024)
ESCRT-III-dependent adhesive and mechanical changes are triggered by a mechanism detecting alteration of Septate Junction integrity in Drosophila epithelial cells
eLife 13:e91246.
https://doi.org/10.7554/eLife.91246

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https://doi.org/10.7554/eLife.91246

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