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Stem cell-specific ecdysone signaling regulates the development and function of a Drosophila sleep homeostat

Complex behaviors arise from neural circuits that are assembled from diverse cell types. Sleep is a conserved and essential behavior, yet little is known regarding how the nervous system generates neuron types of the sleep-wake circuit. Here, we focus on the specification of Drosophila sleep-promoti...

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Autores principales: Wani, Adil R, Chowdhury, Budhaditya, Luong, Jenny, Chaya, Gonzalo Morales, Patel, Krishna, Isaacman-Beck, Jesse, Shafer, Orie, Kayser, Matthew S., Syed, Mubarak Hussain
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10592846/
https://www.ncbi.nlm.nih.gov/pubmed/37873323
http://dx.doi.org/10.1101/2023.09.29.560022
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author Wani, Adil R
Chowdhury, Budhaditya
Luong, Jenny
Chaya, Gonzalo Morales
Patel, Krishna
Isaacman-Beck, Jesse
Shafer, Orie
Kayser, Matthew S.
Syed, Mubarak Hussain
author_facet Wani, Adil R
Chowdhury, Budhaditya
Luong, Jenny
Chaya, Gonzalo Morales
Patel, Krishna
Isaacman-Beck, Jesse
Shafer, Orie
Kayser, Matthew S.
Syed, Mubarak Hussain
author_sort Wani, Adil R
collection PubMed
description Complex behaviors arise from neural circuits that are assembled from diverse cell types. Sleep is a conserved and essential behavior, yet little is known regarding how the nervous system generates neuron types of the sleep-wake circuit. Here, we focus on the specification of Drosophila sleep-promoting neurons—long-field tangential input neurons that project to the dorsal layers of the fan-shaped body neuropil in the central complex (CX). We use lineage analysis and genetic birth dating to identify two bilateral Type II neural stem cells that generate these dorsal fan-shaped body (dFB) neurons. We show that adult dFB neurons express Ecdysone-induced protein E93, and loss of Ecdysone signaling or E93 in Type II NSCs results in the misspecification of the adult dFB neurons. Finally, we show that E93 knockdown in Type II NSCs affects adult sleep behavior. Our results provide insight into how extrinsic hormonal signaling acts on NSCs to generate neuronal diversity required for adult sleep behavior. These findings suggest that some adult sleep disorders might derive from defects in stem cell-specific temporal neurodevelopmental programs.
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spelling pubmed-105928462023-10-24 Stem cell-specific ecdysone signaling regulates the development and function of a Drosophila sleep homeostat Wani, Adil R Chowdhury, Budhaditya Luong, Jenny Chaya, Gonzalo Morales Patel, Krishna Isaacman-Beck, Jesse Shafer, Orie Kayser, Matthew S. Syed, Mubarak Hussain bioRxiv Article Complex behaviors arise from neural circuits that are assembled from diverse cell types. Sleep is a conserved and essential behavior, yet little is known regarding how the nervous system generates neuron types of the sleep-wake circuit. Here, we focus on the specification of Drosophila sleep-promoting neurons—long-field tangential input neurons that project to the dorsal layers of the fan-shaped body neuropil in the central complex (CX). We use lineage analysis and genetic birth dating to identify two bilateral Type II neural stem cells that generate these dorsal fan-shaped body (dFB) neurons. We show that adult dFB neurons express Ecdysone-induced protein E93, and loss of Ecdysone signaling or E93 in Type II NSCs results in the misspecification of the adult dFB neurons. Finally, we show that E93 knockdown in Type II NSCs affects adult sleep behavior. Our results provide insight into how extrinsic hormonal signaling acts on NSCs to generate neuronal diversity required for adult sleep behavior. These findings suggest that some adult sleep disorders might derive from defects in stem cell-specific temporal neurodevelopmental programs. Cold Spring Harbor Laboratory 2023-10-02 /pmc/articles/PMC10592846/ /pubmed/37873323 http://dx.doi.org/10.1101/2023.09.29.560022 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Wani, Adil R
Chowdhury, Budhaditya
Luong, Jenny
Chaya, Gonzalo Morales
Patel, Krishna
Isaacman-Beck, Jesse
Shafer, Orie
Kayser, Matthew S.
Syed, Mubarak Hussain
Stem cell-specific ecdysone signaling regulates the development and function of a Drosophila sleep homeostat
title Stem cell-specific ecdysone signaling regulates the development and function of a Drosophila sleep homeostat
title_full Stem cell-specific ecdysone signaling regulates the development and function of a Drosophila sleep homeostat
title_fullStr Stem cell-specific ecdysone signaling regulates the development and function of a Drosophila sleep homeostat
title_full_unstemmed Stem cell-specific ecdysone signaling regulates the development and function of a Drosophila sleep homeostat
title_short Stem cell-specific ecdysone signaling regulates the development and function of a Drosophila sleep homeostat
title_sort stem cell-specific ecdysone signaling regulates the development and function of a drosophila sleep homeostat
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10592846/
https://www.ncbi.nlm.nih.gov/pubmed/37873323
http://dx.doi.org/10.1101/2023.09.29.560022
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