ESCRT-III-dependent adhesive and mechanical changes are triggered by a mechanism detecting alteration of Septate Junction integrity in Drosophila epithelial cells
- École Polytechnique Fédérale de Lausanne, Switzerland
- Jagiellonian University, Poland
- 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.
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ESCRT-III-dependent adhesive and mechanical changes are triggered by a mechanism detecting alteration of Septate Junction integrity in Drosophila epithelial cellsGOOGLEDryad Digital Repository, doi:10.5061/dryad.dbrv15f7h.
Article and author information
Author details
Thomas Esmangart de Bournonville
Funding
Fondation pour la Recherche Médicale (FDT202001010770)
- Mariusz K Jaglarz
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
- Utpal Banerjee, University of California, Los Angeles, United States
Version history
- Preprint posted: May 24, 2023 (view preprint)
- Received: July 25, 2023
- Accepted: February 1, 2024
- Accepted Manuscript published: February 2, 2024 (version 1)
- Accepted Manuscript updated: February 5, 2024 (version 2)
- Version of Record published: March 22, 2024 (version 3)
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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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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