A surfactant lipid layer of endosomal membranes facilitates airway gas filling in Drosophila.

Drosophila Rabs Rop/Munc18 SNARE acid sphingomyelinase air-liquid interface airways exosome secretion lysosome secretion surfactant film

Journal

Current biology : CB
ISSN: 1879-0445
Titre abrégé: Curr Biol
Pays: England
ID NLM: 9107782

Informations de publication

Date de publication:
04 Dec 2023
Historique:
received: 03 01 2022
revised: 14 09 2023
accepted: 26 10 2023
medline: 7 12 2023
pubmed: 23 11 2023
entrez: 22 11 2023
Statut: ppublish

Résumé

The mechanisms underlying the construction of an air-liquid interface in respiratory organs remain elusive. Here, we use live imaging and genetic analysis to describe the morphogenetic events generating an extracellular lipid lining of the Drosophila airways required for their gas filing and animal survival. We show that sequential Rab39/Syx1A/Syt1-mediated secretion of lysosomal acid sphingomyelinase (Drosophila ASM [dASM]) and Rab11/35/Syx1A/Rop-dependent exosomal secretion provides distinct components for lipid film assembly. Tracheal inactivation of Rab11 or Rab35 or loss of Rop results in intracellular accumulation of exosomal, multi-vesicular body (MVB)-derived vesicles. On the other hand, loss of dASM or Rab39 causes luminal bubble-like accumulations of exosomal membranes and liquid retention in the airways. Inactivation of the exosomal secretion in dASM mutants counteracts this phenotype, arguing that the exosomal secretion provides the lipid vesicles and that secreted lysosomal dASM organizes them into a continuous film. Our results reveal the coordinated functions of extracellular vesicle and lysosomal secretions in generating a lipid layer crucial for airway gas filling and survival.

Identifiants

pubmed: 37992718
pii: S0960-9822(23)01459-8
doi: 10.1016/j.cub.2023.10.058
pii:
doi:

Substances chimiques

Surface-Active Agents 0
Lipids 0
Rop protein, Drosophila 0
Nerve Tissue Proteins 0
Drosophila Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

5132-5146.e5

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Auteurs

Vasilios Tsarouhas (V)

Stockholm University, Department of Molecular Biosciences, The Wenner-Gren Institute, 10691 Stockholm, Sweden; Science for Life Laboratory, SciLifeLab, 171 65 Stockholm, Sweden. Electronic address: vasilios.tsarouhas@su.se.

Dan Liu (D)

Stockholm University, Department of Molecular Biosciences, The Wenner-Gren Institute, 10691 Stockholm, Sweden.

Georgia Tsikala (G)

Stockholm University, Department of Molecular Biosciences, The Wenner-Gren Institute, 10691 Stockholm, Sweden; IMBB, 70013 Heraklion, Crete, Greece.

Ylva Engström (Y)

Stockholm University, Department of Molecular Biosciences, The Wenner-Gren Institute, 10691 Stockholm, Sweden.

Maura Strigini (M)

IMBB, 70013 Heraklion, Crete, Greece.

Christos Samakovlis (C)

Stockholm University, Department of Molecular Biosciences, The Wenner-Gren Institute, 10691 Stockholm, Sweden; Science for Life Laboratory, SciLifeLab, 171 65 Stockholm, Sweden; ECCPS, Justus Liebig University of Giessen, 35390 Giessen, Germany. Electronic address: christos.samakovlis@scilifelab.se.

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Classifications MeSH