Stem cell-specific ecdysone signaling regulates the development of dorsal fan-shaped body neurons and sleep homeostasis.

IF 8.1 1区 生物学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY
Current Biology Pub Date : 2024-11-04 Epub Date: 2024-10-08 DOI:10.1016/j.cub.2024.09.020
Adil R Wani, Budhaditya Chowdhury, Jenny Luong, Gonzalo Morales Chaya, Krishna Patel, Jesse Isaacman-Beck, Matthew S Kayser, Mubarak Hussain Syed
{"title":"Stem cell-specific ecdysone signaling regulates the development of dorsal fan-shaped body neurons and sleep homeostasis.","authors":"Adil R Wani, Budhaditya Chowdhury, Jenny Luong, Gonzalo Morales Chaya, Krishna Patel, Jesse Isaacman-Beck, Matthew S Kayser, Mubarak Hussain Syed","doi":"10.1016/j.cub.2024.09.020","DOIUrl":null,"url":null,"abstract":"<p><p>Complex behaviors arise from neural circuits that assemble from diverse cell types. Sleep is a conserved behavior essential for survival, yet little is known about how the nervous system generates neuron types of a sleep-wake circuit. Here, we focus on the specification of Drosophila 23E10-labeled dorsal fan-shaped body (dFB) long-field tangential input neurons that project to the dorsal layers of the fan-shaped body neuropil in the central complex. We use lineage analysis and genetic birth dating to identify two bilateral type II neural stem cells (NSCs) that generate 23E10 dFB neurons. We show that adult 23E10 dFB neurons express ecdysone-induced protein 93 (E93) and that loss of ecdysone signaling or E93 in type II NSCs results in their misspecification. Finally, we show that E93 knockdown in type II NSCs impairs adult sleep behavior. Our results provide insight into how extrinsic hormonal signaling acts on NSCs to generate the 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.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":" ","pages":"4951-4967.e5"},"PeriodicalIF":8.1000,"publicationDate":"2024-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11537841/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Current Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1016/j.cub.2024.09.020","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/10/8 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Complex behaviors arise from neural circuits that assemble from diverse cell types. Sleep is a conserved behavior essential for survival, yet little is known about how the nervous system generates neuron types of a sleep-wake circuit. Here, we focus on the specification of Drosophila 23E10-labeled dorsal fan-shaped body (dFB) long-field tangential input neurons that project to the dorsal layers of the fan-shaped body neuropil in the central complex. We use lineage analysis and genetic birth dating to identify two bilateral type II neural stem cells (NSCs) that generate 23E10 dFB neurons. We show that adult 23E10 dFB neurons express ecdysone-induced protein 93 (E93) and that loss of ecdysone signaling or E93 in type II NSCs results in their misspecification. Finally, we show that E93 knockdown in type II NSCs impairs adult sleep behavior. Our results provide insight into how extrinsic hormonal signaling acts on NSCs to generate the 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.

干细胞特异性蜕皮激素信号调节背扇形体神经元的发育和睡眠稳态。
复杂的行为产生于由不同类型细胞组成的神经回路。睡眠是一种对生存至关重要的保守行为,但人们对神经系统如何产生睡眠-觉醒回路的神经元类型知之甚少。在这里,我们重点研究了果蝇23E10标记的背侧扇形体(dFB)长场切向输入神经元的规格,这些神经元投射到中央复合体中扇形体神经鞘的背层。我们利用品系分析和遗传测年法鉴定了两种生成 23E10 dFB 神经元的双侧 II 型神经干细胞(NSCs)。我们发现,成年 23E10 dFB 神经元表达蜕皮激素诱导蛋白 93(E93),而 II 型神经干细胞中蜕皮激素信号或 E93 的缺失会导致它们的规格错误。最后,我们发现在 II 型 NSCs 中敲除 E93 会损害成人的睡眠行为。我们的研究结果让我们深入了解了外在激素信号如何作用于 NSCs,从而产生成人睡眠行为所需的神经元多样性。这些发现表明,一些成人睡眠障碍可能源于干细胞特异性时间神经发育程序的缺陷。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Current Biology
Current Biology 生物-生化与分子生物学
CiteScore
11.80
自引率
2.20%
发文量
869
审稿时长
46 days
期刊介绍: Current Biology is a comprehensive journal that showcases original research in various disciplines of biology. It provides a platform for scientists to disseminate their groundbreaking findings and promotes interdisciplinary communication. The journal publishes articles of general interest, encompassing diverse fields of biology. Moreover, it offers accessible editorial pieces that are specifically designed to enlighten non-specialist readers.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信