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Tubular endocytosis drives remodelling of the apical surface during epithelial morphogenesis in Drosophila

During morphogenesis, remodelling of cell shape requires the expansion or contraction of plasma membrane domains. Here we identify a mechanism underlying the restructuring of the apical surface during epithelial morphogenesis in Drosophila. We show that the retraction of villous protrusions and subs...

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Autores principales: Fabrowski, Piotr, Necakov, Aleksandar S., Mumbauer, Simone, Loeser, Eva, Reversi, Alessandra, Streichan, Sebastian, Briggs, John A. G., De Renzis, Stefano
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Pub. Group 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3753550/
https://www.ncbi.nlm.nih.gov/pubmed/23921440
http://dx.doi.org/10.1038/ncomms3244
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author Fabrowski, Piotr
Necakov, Aleksandar S.
Mumbauer, Simone
Loeser, Eva
Reversi, Alessandra
Streichan, Sebastian
Briggs, John A. G.
De Renzis, Stefano
author_facet Fabrowski, Piotr
Necakov, Aleksandar S.
Mumbauer, Simone
Loeser, Eva
Reversi, Alessandra
Streichan, Sebastian
Briggs, John A. G.
De Renzis, Stefano
author_sort Fabrowski, Piotr
collection PubMed
description During morphogenesis, remodelling of cell shape requires the expansion or contraction of plasma membrane domains. Here we identify a mechanism underlying the restructuring of the apical surface during epithelial morphogenesis in Drosophila. We show that the retraction of villous protrusions and subsequent apical plasma membrane flattening is an endocytosis-driven morphogenetic process. Quantitation of endogenously tagged GFP::Rab5 dynamics reveals a massive increase in apical endocytosis that correlates with changes in apical morphology. This increase is accompanied by the formation of tubular plasma membrane invaginations that serve as platforms for the de novo generation of Rab5-positive endosomes. We identify the Rab5-effector Rabankyrin-5 as a regulator of this pathway and demonstrate that blocking dynamin activity results in the complete inhibition of tubular endocytosis, in the disappearance of Rab5 endosomes, and in the inhibition of surface flattening. These data collectively demonstrate a requirement for endocytosis in morphogenetic remodelling during epithelial development.
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spelling pubmed-37535502013-08-27 Tubular endocytosis drives remodelling of the apical surface during epithelial morphogenesis in Drosophila Fabrowski, Piotr Necakov, Aleksandar S. Mumbauer, Simone Loeser, Eva Reversi, Alessandra Streichan, Sebastian Briggs, John A. G. De Renzis, Stefano Nat Commun Article During morphogenesis, remodelling of cell shape requires the expansion or contraction of plasma membrane domains. Here we identify a mechanism underlying the restructuring of the apical surface during epithelial morphogenesis in Drosophila. We show that the retraction of villous protrusions and subsequent apical plasma membrane flattening is an endocytosis-driven morphogenetic process. Quantitation of endogenously tagged GFP::Rab5 dynamics reveals a massive increase in apical endocytosis that correlates with changes in apical morphology. This increase is accompanied by the formation of tubular plasma membrane invaginations that serve as platforms for the de novo generation of Rab5-positive endosomes. We identify the Rab5-effector Rabankyrin-5 as a regulator of this pathway and demonstrate that blocking dynamin activity results in the complete inhibition of tubular endocytosis, in the disappearance of Rab5 endosomes, and in the inhibition of surface flattening. These data collectively demonstrate a requirement for endocytosis in morphogenetic remodelling during epithelial development. Nature Pub. Group 2013-08-07 /pmc/articles/PMC3753550/ /pubmed/23921440 http://dx.doi.org/10.1038/ncomms3244 Text en Copyright © 2013, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved. http://creativecommons.org/licenses/by/3.0/ This article is licensed under a Creative Commons Attribution 3.0 Unported Licence. To view a copy of this licence visit http://creativecommons.org/licenses/by/3.0/.
spellingShingle Article
Fabrowski, Piotr
Necakov, Aleksandar S.
Mumbauer, Simone
Loeser, Eva
Reversi, Alessandra
Streichan, Sebastian
Briggs, John A. G.
De Renzis, Stefano
Tubular endocytosis drives remodelling of the apical surface during epithelial morphogenesis in Drosophila
title Tubular endocytosis drives remodelling of the apical surface during epithelial morphogenesis in Drosophila
title_full Tubular endocytosis drives remodelling of the apical surface during epithelial morphogenesis in Drosophila
title_fullStr Tubular endocytosis drives remodelling of the apical surface during epithelial morphogenesis in Drosophila
title_full_unstemmed Tubular endocytosis drives remodelling of the apical surface during epithelial morphogenesis in Drosophila
title_short Tubular endocytosis drives remodelling of the apical surface during epithelial morphogenesis in Drosophila
title_sort tubular endocytosis drives remodelling of the apical surface during epithelial morphogenesis in drosophila
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3753550/
https://www.ncbi.nlm.nih.gov/pubmed/23921440
http://dx.doi.org/10.1038/ncomms3244
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