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Scabrous is distributed via signaling filopodia to modulate Notch response during bristle patterning in Drosophila

During development, cells in tissues must be patterned correctly in order to support tissue function and shape. The sensory bristles of the peripheral nervous system on the thorax of Drosophila melanogaster self-organizes from a unpatterned epithelial tissue to a regular spot pattern during pupal st...

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Autores principales: Presser, Adam, Freund, Olivia, Hassapelis, Theodora, Hunter, Ginger
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10511103/
https://www.ncbi.nlm.nih.gov/pubmed/37729137
http://dx.doi.org/10.1371/journal.pone.0291409
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author Presser, Adam
Freund, Olivia
Hassapelis, Theodora
Hunter, Ginger
author_facet Presser, Adam
Freund, Olivia
Hassapelis, Theodora
Hunter, Ginger
author_sort Presser, Adam
collection PubMed
description During development, cells in tissues must be patterned correctly in order to support tissue function and shape. The sensory bristles of the peripheral nervous system on the thorax of Drosophila melanogaster self-organizes from a unpatterned epithelial tissue to a regular spot pattern during pupal stages. Wild type patterning requires Notch-mediated lateral inhibition. Scabrous is a protein that can bind to and modify Notch receptor activity. Scabrous can be secreted, but it is also known to be localized to basal signaling filopodia, or cytonemes, that play a role in long-range Notch signaling. Here we show that Scabrous is primarily distributed basally, within the range of signaling filopodia extension. We show that filamentous actin dynamics are required for the distribution of Scabrous protein during sensory bristle patterning stages. We show that the Notch response of epithelial cells is sensitive to the level of Scabrous protein being expressed by the sensory bristle precursor cell. Our findings at the cell-level suggest a model for how epithelial cells engaged in lateral inhibition at a distance are sensitive local levels of Scabrous protein.
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spelling pubmed-105111032023-09-21 Scabrous is distributed via signaling filopodia to modulate Notch response during bristle patterning in Drosophila Presser, Adam Freund, Olivia Hassapelis, Theodora Hunter, Ginger PLoS One Research Article During development, cells in tissues must be patterned correctly in order to support tissue function and shape. The sensory bristles of the peripheral nervous system on the thorax of Drosophila melanogaster self-organizes from a unpatterned epithelial tissue to a regular spot pattern during pupal stages. Wild type patterning requires Notch-mediated lateral inhibition. Scabrous is a protein that can bind to and modify Notch receptor activity. Scabrous can be secreted, but it is also known to be localized to basal signaling filopodia, or cytonemes, that play a role in long-range Notch signaling. Here we show that Scabrous is primarily distributed basally, within the range of signaling filopodia extension. We show that filamentous actin dynamics are required for the distribution of Scabrous protein during sensory bristle patterning stages. We show that the Notch response of epithelial cells is sensitive to the level of Scabrous protein being expressed by the sensory bristle precursor cell. Our findings at the cell-level suggest a model for how epithelial cells engaged in lateral inhibition at a distance are sensitive local levels of Scabrous protein. Public Library of Science 2023-09-20 /pmc/articles/PMC10511103/ /pubmed/37729137 http://dx.doi.org/10.1371/journal.pone.0291409 Text en © 2023 Presser et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Presser, Adam
Freund, Olivia
Hassapelis, Theodora
Hunter, Ginger
Scabrous is distributed via signaling filopodia to modulate Notch response during bristle patterning in Drosophila
title Scabrous is distributed via signaling filopodia to modulate Notch response during bristle patterning in Drosophila
title_full Scabrous is distributed via signaling filopodia to modulate Notch response during bristle patterning in Drosophila
title_fullStr Scabrous is distributed via signaling filopodia to modulate Notch response during bristle patterning in Drosophila
title_full_unstemmed Scabrous is distributed via signaling filopodia to modulate Notch response during bristle patterning in Drosophila
title_short Scabrous is distributed via signaling filopodia to modulate Notch response during bristle patterning in Drosophila
title_sort scabrous is distributed via signaling filopodia to modulate notch response during bristle patterning in drosophila
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10511103/
https://www.ncbi.nlm.nih.gov/pubmed/37729137
http://dx.doi.org/10.1371/journal.pone.0291409
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