Scavenger receptor endocytosis controls apical membrane morphogenesis in the Drosophila airways

  1. Ana Sofia Pinheiro
  2. Vasilios Tsarouhas  Is a corresponding author
  3. Kirsten André Senti
  4. Badrul Arefin
  5. Christos Samakovlis  Is a corresponding author
  1. Stockholm University, Sweden
  2. Institute of Molecular Biotechnology, Austria
  3. University of Gothenburg, Sweden

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

  1. Ana Sofia Pinheiro

    Department of Molecular Biosciences, Stockholm University, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  2. Vasilios Tsarouhas

    Department of Molecular Biosciences, Stockholm University, Stockholm, Sweden
    For correspondence
    Vasilios.Tsarouhas@su.se
    Competing interests
    The authors declare that no competing interests exist.
  3. Kirsten André Senti

    Institute of Molecular Biotechnology, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  4. Badrul Arefin

    Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1117-9125
  5. Christos Samakovlis

    Department of Molecular Biosciences, Stockholm University, Stockholm, Sweden
    For correspondence
    christos.samakovlis@scilifelab.se
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9153-6040

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

  1. Elisabeth Knust, Max-Planck Institute of Molecular Cell Biology and Genetics, Germany

Version history

  1. Received: November 17, 2022
  2. Accepted: September 13, 2023
  3. 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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  1. Ana Sofia Pinheiro
  2. Vasilios Tsarouhas
  3. Kirsten André Senti
  4. Badrul Arefin
  5. Christos Samakovlis
(2023)
Scavenger receptor endocytosis controls apical membrane morphogenesis in the Drosophila airways
eLife 12:e84974.
https://doi.org/10.7554/eLife.84974

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