Scavenger receptor endocytosis controls apical membrane morphogenesis in the Drosophila airways
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 extracellular matrix (ECM) components with the underlying membrane and cytoskeleton controls tube elongation, but the link betwe...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2023-09-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/84974 |
| _version_ | 1797662299012464640 |
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| author | Ana Sofia Pinheiro Vasilios Tsarouhas Kirsten André Senti Badrul Arefin Christos Samakovlis |
| author_facet | Ana Sofia Pinheiro Vasilios Tsarouhas Kirsten André Senti Badrul Arefin Christos Samakovlis |
| author_sort | Ana Sofia Pinheiro |
| collection | DOAJ |
| description | 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 extracellular matrix (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 homolog 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. |
| first_indexed | 2024-03-11T18:58:08Z |
| format | Article |
| id | doaj.art-0e020977133d4f73a81d7dde7a8c5e7f |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-03-11T18:58:08Z |
| publishDate | 2023-09-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-0e020977133d4f73a81d7dde7a8c5e7f2023-10-10T14:02:35ZengeLife Sciences Publications LtdeLife2050-084X2023-09-011210.7554/eLife.84974Scavenger receptor endocytosis controls apical membrane morphogenesis in the Drosophila airwaysAna Sofia Pinheiro0Vasilios Tsarouhas1https://orcid.org/0000-0002-2933-1351Kirsten André Senti2Badrul Arefin3https://orcid.org/0000-0003-1117-9125Christos Samakovlis4https://orcid.org/0000-0002-9153-6040Science for Life Laboratory, Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Stockholm, SwedenScience for Life Laboratory, Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Stockholm, SwedenScience for Life Laboratory, Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Stockholm, Sweden; IMBA – Institute of Molecular Biotechnology, Austrian Academy of Sciences, Vienna, AustriaScience for Life Laboratory, Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Stockholm, Sweden; Sahlgrenska Academy, Gothenburg University, Gothenburg, SwedenScience for Life Laboratory, Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Stockholm, Sweden; Cardiopulmonary Institute, Justus Liebig University of Giessen, Giessen, GermanyThe 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 extracellular matrix (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 homolog 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.https://elifesciences.org/articles/84974endocytosis-recyclingairwaysscavenger receptorsrc kinaseCD36cytoskeleton |
| spellingShingle | Ana Sofia Pinheiro Vasilios Tsarouhas Kirsten André Senti Badrul Arefin Christos Samakovlis Scavenger receptor endocytosis controls apical membrane morphogenesis in the Drosophila airways eLife endocytosis-recycling airways scavenger receptor src kinase CD36 cytoskeleton |
| title | Scavenger receptor endocytosis controls apical membrane morphogenesis in the Drosophila airways |
| title_full | Scavenger receptor endocytosis controls apical membrane morphogenesis in the Drosophila airways |
| title_fullStr | Scavenger receptor endocytosis controls apical membrane morphogenesis in the Drosophila airways |
| title_full_unstemmed | Scavenger receptor endocytosis controls apical membrane morphogenesis in the Drosophila airways |
| title_short | Scavenger receptor endocytosis controls apical membrane morphogenesis in the Drosophila airways |
| title_sort | scavenger receptor endocytosis controls apical membrane morphogenesis in the drosophila airways |
| topic | endocytosis-recycling airways scavenger receptor src kinase CD36 cytoskeleton |
| url | https://elifesciences.org/articles/84974 |
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