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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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Published in: | PloS one 2023-09, Vol.18 (9), p.e0291409-e0291409 |
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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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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.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0291409</identifier><language>eng</language><publisher>San Francisco: Public Library of Science</publisher><subject>Actin ; Biology and Life Sciences ; Bristles ; Cells ; Epithelial cells ; Epithelium ; Filopodia ; Fruit flies ; Genotype & phenotype ; Insects ; Ligands ; Medicine and Health Sciences ; Nervous system ; Notch protein ; Pattern formation ; Patterning ; Peripheral nervous system ; Proteins ; Research and Analysis Methods ; Sensory bristles ; Social Sciences ; Stains & staining ; Thorax ; Tissues</subject><ispartof>PloS one, 2023-09, Vol.18 (9), p.e0291409-e0291409</ispartof><rights>2023 Presser et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2023 Presser et al 2023 Presser et al</rights><rights>2023 Presser et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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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.</description><subject>Actin</subject><subject>Biology and Life Sciences</subject><subject>Bristles</subject><subject>Cells</subject><subject>Epithelial cells</subject><subject>Epithelium</subject><subject>Filopodia</subject><subject>Fruit flies</subject><subject>Genotype & phenotype</subject><subject>Insects</subject><subject>Ligands</subject><subject>Medicine and Health Sciences</subject><subject>Nervous system</subject><subject>Notch protein</subject><subject>Pattern formation</subject><subject>Patterning</subject><subject>Peripheral nervous system</subject><subject>Proteins</subject><subject>Research and Analysis Methods</subject><subject>Sensory bristles</subject><subject>Social Sciences</subject><subject>Stains & 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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. 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subjects | Actin Biology and Life Sciences Bristles Cells Epithelial cells Epithelium Filopodia Fruit flies Genotype & phenotype Insects Ligands Medicine and Health Sciences Nervous system Notch protein Pattern formation Patterning Peripheral nervous system Proteins Research and Analysis Methods Sensory bristles Social Sciences Stains & staining Thorax Tissues |
title | Scabrous is distributed via signaling filopodia to modulate Notch response during bristle patterning in Drosophila |
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