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A neural progenitor mitotic wave is required for asynchronous axon outgrowth and morphology

Spatiotemporal mechanisms generating neural diversity are fundamental for understanding neural processes. Here, we investigated how neural diversity arises from neurons coming from identical progenitors. In the dorsal thorax of Drosophila, rows of mechanosensory organs originate from the division of...

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Autores principales: Lacoste, Jérôme, Soula, Hédi, Burg, Angélique, Audibert, Agnès, Darnat, Pénélope, Gho, Michel, Louvet-Vallée, Sophie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8933001/
https://www.ncbi.nlm.nih.gov/pubmed/35254258
http://dx.doi.org/10.7554/eLife.75746
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author Lacoste, Jérôme
Soula, Hédi
Burg, Angélique
Audibert, Agnès
Darnat, Pénélope
Gho, Michel
Louvet-Vallée, Sophie
author_facet Lacoste, Jérôme
Soula, Hédi
Burg, Angélique
Audibert, Agnès
Darnat, Pénélope
Gho, Michel
Louvet-Vallée, Sophie
author_sort Lacoste, Jérôme
collection PubMed
description Spatiotemporal mechanisms generating neural diversity are fundamental for understanding neural processes. Here, we investigated how neural diversity arises from neurons coming from identical progenitors. In the dorsal thorax of Drosophila, rows of mechanosensory organs originate from the division of sensory organ progenitor (SOPs). We show that in each row of the notum, an anteromedial located central SOP divides first, then neighbouring SOPs divide, and so on. This centrifugal wave of mitoses depends on cell-cell inhibitory interactions mediated by SOP cytoplasmic protrusions and Scabrous, a secreted protein interacting with the Delta/Notch complex. Furthermore, when this mitotic wave was reduced, axonal growth was more synchronous, axonal terminals had a complex branching pattern and fly behaviour was impaired. We show that the temporal order of progenitor divisions influences the birth order of sensory neurons, axon branching and impact on grooming behaviour. These data support the idea that developmental timing controls axon wiring neural diversity.
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spelling pubmed-89330012022-03-19 A neural progenitor mitotic wave is required for asynchronous axon outgrowth and morphology Lacoste, Jérôme Soula, Hédi Burg, Angélique Audibert, Agnès Darnat, Pénélope Gho, Michel Louvet-Vallée, Sophie eLife Cell Biology Spatiotemporal mechanisms generating neural diversity are fundamental for understanding neural processes. Here, we investigated how neural diversity arises from neurons coming from identical progenitors. In the dorsal thorax of Drosophila, rows of mechanosensory organs originate from the division of sensory organ progenitor (SOPs). We show that in each row of the notum, an anteromedial located central SOP divides first, then neighbouring SOPs divide, and so on. This centrifugal wave of mitoses depends on cell-cell inhibitory interactions mediated by SOP cytoplasmic protrusions and Scabrous, a secreted protein interacting with the Delta/Notch complex. Furthermore, when this mitotic wave was reduced, axonal growth was more synchronous, axonal terminals had a complex branching pattern and fly behaviour was impaired. We show that the temporal order of progenitor divisions influences the birth order of sensory neurons, axon branching and impact on grooming behaviour. These data support the idea that developmental timing controls axon wiring neural diversity. eLife Sciences Publications, Ltd 2022-03-07 /pmc/articles/PMC8933001/ /pubmed/35254258 http://dx.doi.org/10.7554/eLife.75746 Text en © 2022, Lacoste et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Lacoste, Jérôme
Soula, Hédi
Burg, Angélique
Audibert, Agnès
Darnat, Pénélope
Gho, Michel
Louvet-Vallée, Sophie
A neural progenitor mitotic wave is required for asynchronous axon outgrowth and morphology
title A neural progenitor mitotic wave is required for asynchronous axon outgrowth and morphology
title_full A neural progenitor mitotic wave is required for asynchronous axon outgrowth and morphology
title_fullStr A neural progenitor mitotic wave is required for asynchronous axon outgrowth and morphology
title_full_unstemmed A neural progenitor mitotic wave is required for asynchronous axon outgrowth and morphology
title_short A neural progenitor mitotic wave is required for asynchronous axon outgrowth and morphology
title_sort neural progenitor mitotic wave is required for asynchronous axon outgrowth and morphology
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8933001/
https://www.ncbi.nlm.nih.gov/pubmed/35254258
http://dx.doi.org/10.7554/eLife.75746
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