Scavenger receptor endocytosis controls apical membrane morphogenesis in the Drosophila airways
Abstract
The acquisition of distinct branch sizes and shapes is a central aspect in tubular organ morphogenesis and function. In the Drosophila airway tree, the interplay of apical ECM components with the underlying membrane and cytoskeleton controls tube elongation, but the link between ECM composition with apical membrane morphogenesis and tube size regulation is elusive. Here, we characterized Emp (epithelial membrane protein), a Drosophila CD36-homologue belonging to the scavenger receptor class B protein-family. emp mutant embryos fail to internalize the luminal chitin deacetylases Serp and Verm at the final stages of airway maturation and die at hatching with liquid filled airways. Emp localizes in apical epithelial membranes and shows cargo selectivity for LDLr-domain containing proteins. emp mutants also display over elongated tracheal tubes with increased levels of the apical proteins Crb, DE-cad and phosphorylated Src (p-Src). We show that Emp associates with and organizes the βH-Spectrin cytoskeleton and is itself confined by apical F-actin bundles. Overexpression or loss of its cargo protein Serp lead to abnormal apical accumulations of Emp and perturbations in p-Src levels. We propose that during morphogenesis, Emp senses and responds to luminal cargo levels by initiating apical membrane endocytosis along the longitudinal tube axis and thereby restricts airway elongation.
Data availability
All data generated or analyzed during this study are included in the manuscript and supporting files. Unprocessed Western blots are provided as source data files in zip format.
Article and author information
Author details
Funding
Vetenskapsrådet
- Christos Samakovlis
Cancerfonden
- Christos Samakovlis
O. E. och Edla Johanssons Vetenskapliga Stiftelse
- Vasilios Tsarouhas
Magnus Bergvalls Stiftelse (2021-04453)
- Vasilios Tsarouhas
Deutsche Forschungsgemeinschaft (KFO309)
- Christos Samakovlis
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Elisabeth Knust, Max-Planck Institute of Molecular Cell Biology and Genetics, Germany
Version history
- Received: November 17, 2022
- Accepted: September 13, 2023
- Accepted Manuscript published: September 14, 2023 (version 1)
Copyright
© 2023, Pinheiro 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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