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Microvilli-derived Extracellular Vesicles Govern Morphogenesis in Drosophila wing epithelium

View ORCID ProfileIlse Hurbain, Anne-Sophie Macé, Maryse Romao, Lucie Sengmanivong, Laurent Ruel, View ORCID ProfileRenata Basto, View ORCID ProfilePascal P. Thérond, View ORCID ProfileGraça Raposo, View ORCID ProfileGisela D’Angelo
doi: https://doi.org/10.1101/2020.11.01.363697
Ilse Hurbain
1Institut Curie, PSL Research University, CNRS, UMR144, 26 rue d’Ulm, 75248 Paris Cedex 05, France
2Institut Curie, PSL Research University, CNRS, UMR144, Cell and Tissue Imaging Facility (PICT-IBiSA), 26, rue d’Ulm, 75248 Paris Cedex 05, France
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Anne-Sophie Macé
1Institut Curie, PSL Research University, CNRS, UMR144, 26 rue d’Ulm, 75248 Paris Cedex 05, France
2Institut Curie, PSL Research University, CNRS, UMR144, Cell and Tissue Imaging Facility (PICT-IBiSA), 26, rue d’Ulm, 75248 Paris Cedex 05, France
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Maryse Romao
1Institut Curie, PSL Research University, CNRS, UMR144, 26 rue d’Ulm, 75248 Paris Cedex 05, France
2Institut Curie, PSL Research University, CNRS, UMR144, Cell and Tissue Imaging Facility (PICT-IBiSA), 26, rue d’Ulm, 75248 Paris Cedex 05, France
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Lucie Sengmanivong
1Institut Curie, PSL Research University, CNRS, UMR144, 26 rue d’Ulm, 75248 Paris Cedex 05, France
2Institut Curie, PSL Research University, CNRS, UMR144, Cell and Tissue Imaging Facility (PICT-IBiSA), 26, rue d’Ulm, 75248 Paris Cedex 05, France
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Laurent Ruel
3Université Côte d’Azur; UMR7277 CNRS; Inserm U1091; Institute of Biology Valrose (iBV); Parc Valrose; 06108 Nice cedex2, France
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Renata Basto
1Institut Curie, PSL Research University, CNRS, UMR144, 26 rue d’Ulm, 75248 Paris Cedex 05, France
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Pascal P. Thérond
3Université Côte d’Azur; UMR7277 CNRS; Inserm U1091; Institute of Biology Valrose (iBV); Parc Valrose; 06108 Nice cedex2, France
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Graça Raposo
1Institut Curie, PSL Research University, CNRS, UMR144, 26 rue d’Ulm, 75248 Paris Cedex 05, France
2Institut Curie, PSL Research University, CNRS, UMR144, Cell and Tissue Imaging Facility (PICT-IBiSA), 26, rue d’Ulm, 75248 Paris Cedex 05, France
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Gisela D’Angelo
1Institut Curie, PSL Research University, CNRS, UMR144, 26 rue d’Ulm, 75248 Paris Cedex 05, France
2Institut Curie, PSL Research University, CNRS, UMR144, Cell and Tissue Imaging Facility (PICT-IBiSA), 26, rue d’Ulm, 75248 Paris Cedex 05, France
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  • For correspondence: gisela.dangelo@curie.fr
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ABSTRACT

The regulation and coordination of developmental processes involves the secretion of morphogens and membrane carriers, including extracellular vesicles, which facilitate their transport over long distance. The long-range activity of the Hedgehog morphogen is conveyed by extracellular vesicles. However, the site and the molecular basis of their biogenesis remains unknown. By combining fluorescence and electron microscopy combined with genetics and cell biology approaches, we investigated the origin and the cellular mechanisms underlying extracellular vesicle biogenesis, and their contribution to Drosophila wing disc development, exploiting Hedgehog as a long-range morphogen. We show that microvilli of Drosophila wing disc epithelium are the site of generation of small extracellular vesicles that transport Hedgehog across the tissue. This process requires the Prominin-like protein, whose activity, together with interacting cytoskeleton components and lipids, is critical for maintaining microvilli integrity and function in secretion. Our results provide the first evidence that microvilli-derived extracellular vesicles contribute to Hedgehog long-range signaling activity highlighting their physiological significance in tissue development in vivo.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵* gisela.dangelo{at}curie.fr

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted November 02, 2020.
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Microvilli-derived Extracellular Vesicles Govern Morphogenesis in Drosophila wing epithelium
Ilse Hurbain, Anne-Sophie Macé, Maryse Romao, Lucie Sengmanivong, Laurent Ruel, Renata Basto, Pascal P. Thérond, Graça Raposo, Gisela D’Angelo
bioRxiv 2020.11.01.363697; doi: https://doi.org/10.1101/2020.11.01.363697
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Microvilli-derived Extracellular Vesicles Govern Morphogenesis in Drosophila wing epithelium
Ilse Hurbain, Anne-Sophie Macé, Maryse Romao, Lucie Sengmanivong, Laurent Ruel, Renata Basto, Pascal P. Thérond, Graça Raposo, Gisela D’Angelo
bioRxiv 2020.11.01.363697; doi: https://doi.org/10.1101/2020.11.01.363697

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