2. Academic Validation
  3. A surfactant lipid layer of endosomal membranes facilitates airway gas filling in Drosophila

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

  • Curr Biol. 2023 Nov 20:S0960-9822(23)01459-8. doi: 10.1016/j.cub.2023.10.058.
Vasilios Tsarouhas 1,  Dan Liu 2,  Georgia Tsikala 3,  Ylva Engström 2,  Maura Strigini 4,  Christos Samakovlis 5
Affiliations

Affiliations

  • 1 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.
  • 2 Stockholm University, Department of Molecular Biosciences, The Wenner-Gren Institute, 10691 Stockholm, Sweden.
  • 3 Stockholm University, Department of Molecular Biosciences, The Wenner-Gren Institute, 10691 Stockholm, Sweden; IMBB, 70013 Heraklion, Crete, Greece.
  • 4 IMBB, 70013 Heraklion, Crete, Greece.
  • 5 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.
PMID: 37992718 DOI: 10.1016/j.cub.2023.10.058
Abstract

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.

Keywords

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

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