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Developmental pruning of sensory neurites by mechanical tearing in Drosophila

Mechanical forces actively shape cells during development, but little is known about their roles during neuronal morphogenesis. Developmental neurite pruning, a critical circuit specification mechanism, often involves neurite abscission at predetermined sites by unknown mechanisms. Pruning of Drosop...

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Autores principales: Krämer, Rafael, Wolterhoff, Neele, Galic, Milos, Rumpf, Sebastian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9856751/
https://www.ncbi.nlm.nih.gov/pubmed/36648440
http://dx.doi.org/10.1083/jcb.202205004
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author Krämer, Rafael
Wolterhoff, Neele
Galic, Milos
Rumpf, Sebastian
author_facet Krämer, Rafael
Wolterhoff, Neele
Galic, Milos
Rumpf, Sebastian
author_sort Krämer, Rafael
collection PubMed
description Mechanical forces actively shape cells during development, but little is known about their roles during neuronal morphogenesis. Developmental neurite pruning, a critical circuit specification mechanism, often involves neurite abscission at predetermined sites by unknown mechanisms. Pruning of Drosophila sensory neuron dendrites during metamorphosis is triggered by the hormone ecdysone, which induces local disassembly of the dendritic cytoskeleton. Subsequently, dendrites are severed at positions close to the soma by an unknown mechanism. We found that ecdysone signaling causes the dendrites to become mechanically fragile. Severing occurs during periods of increased pupal morphogenetic tissue movements, which exert mechanical forces on the destabilized dendrites. Tissue movements and dendrite severing peak during pupal ecdysis, a period of strong abdominal contractions, and abolishing ecdysis causes non-cell autonomous dendrite pruning defects. Thus, our data establish mechanical tearing as a novel mechanism during neurite pruning.
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spelling pubmed-98567512023-01-21 Developmental pruning of sensory neurites by mechanical tearing in Drosophila Krämer, Rafael Wolterhoff, Neele Galic, Milos Rumpf, Sebastian J Cell Biol Article Mechanical forces actively shape cells during development, but little is known about their roles during neuronal morphogenesis. Developmental neurite pruning, a critical circuit specification mechanism, often involves neurite abscission at predetermined sites by unknown mechanisms. Pruning of Drosophila sensory neuron dendrites during metamorphosis is triggered by the hormone ecdysone, which induces local disassembly of the dendritic cytoskeleton. Subsequently, dendrites are severed at positions close to the soma by an unknown mechanism. We found that ecdysone signaling causes the dendrites to become mechanically fragile. Severing occurs during periods of increased pupal morphogenetic tissue movements, which exert mechanical forces on the destabilized dendrites. Tissue movements and dendrite severing peak during pupal ecdysis, a period of strong abdominal contractions, and abolishing ecdysis causes non-cell autonomous dendrite pruning defects. Thus, our data establish mechanical tearing as a novel mechanism during neurite pruning. Rockefeller University Press 2023-01-17 /pmc/articles/PMC9856751/ /pubmed/36648440 http://dx.doi.org/10.1083/jcb.202205004 Text en © 2023 Krämer et al. https://creativecommons.org/licenses/by/4.0/This article is available under a Creative Commons License (Attribution 4.0 International, as described at https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Krämer, Rafael
Wolterhoff, Neele
Galic, Milos
Rumpf, Sebastian
Developmental pruning of sensory neurites by mechanical tearing in Drosophila
title Developmental pruning of sensory neurites by mechanical tearing in Drosophila
title_full Developmental pruning of sensory neurites by mechanical tearing in Drosophila
title_fullStr Developmental pruning of sensory neurites by mechanical tearing in Drosophila
title_full_unstemmed Developmental pruning of sensory neurites by mechanical tearing in Drosophila
title_short Developmental pruning of sensory neurites by mechanical tearing in Drosophila
title_sort developmental pruning of sensory neurites by mechanical tearing in drosophila
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9856751/
https://www.ncbi.nlm.nih.gov/pubmed/36648440
http://dx.doi.org/10.1083/jcb.202205004
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