Adenosine-independent regulation of the sleep–wake cycle by astrocyte activity
Abstract Astrocytes play a crucial role in regulating sleep–wake behavior, and adenosine signaling is generally thought to be involved. Here we show multiple lines of evidence supporting that modulation of the sleep–wake behavior by astrocyte Ca2+ activity could occur without adenosine signaling. In...
Main Authors: | , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Nature Publishing Group
2023-02-01
|
Series: | Cell Discovery |
Online Access: | https://doi.org/10.1038/s41421-022-00498-9 |
_version_ | 1811166074072203264 |
---|---|
author | Wanling Peng Xiaotong Liu Guofen Ma Zhaofa Wu Ziyue Wang Xiang Fei Meiling Qin Lizhao Wang Yulong Li Siyu Zhang Min Xu |
author_facet | Wanling Peng Xiaotong Liu Guofen Ma Zhaofa Wu Ziyue Wang Xiang Fei Meiling Qin Lizhao Wang Yulong Li Siyu Zhang Min Xu |
author_sort | Wanling Peng |
collection | DOAJ |
description | Abstract Astrocytes play a crucial role in regulating sleep–wake behavior, and adenosine signaling is generally thought to be involved. Here we show multiple lines of evidence supporting that modulation of the sleep–wake behavior by astrocyte Ca2+ activity could occur without adenosine signaling. In the basal forebrain and the brainstem, two brain regions that are known to be essential for sleep–wake regulation, chemogenetically-induced astrocyte Ca2+ elevation significantly modulated the sleep–wake cycle. Although astrocyte Ca2+ level positively correlated with the amount of extracellular adenosine, as revealed by a genetically encoded adenosine sensor, we found no detectable change in adenosine level after suppressing astrocyte Ca2+ elevation, and transgenic mice lacking one of the major extracellular ATP-adenosine conversion enzymes showed similar extracellular adenosine level and astrocyte Ca2+-induced sleep modulation. Furthermore, astrocyte Ca2+ is dependent primarily on local neuronal activity, causing brain region-specific regulation of the sleep–wake cycle. Thus, neural activity-dependent astrocyte activity could regulate the sleep–wake behavior independent of adenosine signaling. |
first_indexed | 2024-04-10T15:46:36Z |
format | Article |
id | doaj.art-9c675df3ac1a4b12b29bd9596c539343 |
institution | Directory Open Access Journal |
issn | 2056-5968 |
language | English |
last_indexed | 2024-04-10T15:46:36Z |
publishDate | 2023-02-01 |
publisher | Nature Publishing Group |
record_format | Article |
series | Cell Discovery |
spelling | doaj.art-9c675df3ac1a4b12b29bd9596c5393432023-02-12T12:04:24ZengNature Publishing GroupCell Discovery2056-59682023-02-019112510.1038/s41421-022-00498-9Adenosine-independent regulation of the sleep–wake cycle by astrocyte activityWanling Peng0Xiaotong Liu1Guofen Ma2Zhaofa Wu3Ziyue Wang4Xiang Fei5Meiling Qin6Lizhao Wang7Yulong Li8Siyu Zhang9Min Xu10Institute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of SciencesInstitute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of SciencesCenter for Brain Science of Shanghai Children’s Medical Center, Department of Anatomy and Physiology, Shanghai Jiao Tong University School of MedicineState Key Laboratory of Membrane Biology, Peking University School of Life SciencesCenter for Brain Science of Shanghai Children’s Medical Center, Department of Anatomy and Physiology, Shanghai Jiao Tong University School of MedicineInstitute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of SciencesInstitute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of SciencesCenter for Brain Science of Shanghai Children’s Medical Center, Department of Anatomy and Physiology, Shanghai Jiao Tong University School of MedicineState Key Laboratory of Membrane Biology, Peking University School of Life SciencesCenter for Brain Science of Shanghai Children’s Medical Center, Department of Anatomy and Physiology, Shanghai Jiao Tong University School of MedicineInstitute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of SciencesAbstract Astrocytes play a crucial role in regulating sleep–wake behavior, and adenosine signaling is generally thought to be involved. Here we show multiple lines of evidence supporting that modulation of the sleep–wake behavior by astrocyte Ca2+ activity could occur without adenosine signaling. In the basal forebrain and the brainstem, two brain regions that are known to be essential for sleep–wake regulation, chemogenetically-induced astrocyte Ca2+ elevation significantly modulated the sleep–wake cycle. Although astrocyte Ca2+ level positively correlated with the amount of extracellular adenosine, as revealed by a genetically encoded adenosine sensor, we found no detectable change in adenosine level after suppressing astrocyte Ca2+ elevation, and transgenic mice lacking one of the major extracellular ATP-adenosine conversion enzymes showed similar extracellular adenosine level and astrocyte Ca2+-induced sleep modulation. Furthermore, astrocyte Ca2+ is dependent primarily on local neuronal activity, causing brain region-specific regulation of the sleep–wake cycle. Thus, neural activity-dependent astrocyte activity could regulate the sleep–wake behavior independent of adenosine signaling.https://doi.org/10.1038/s41421-022-00498-9 |
spellingShingle | Wanling Peng Xiaotong Liu Guofen Ma Zhaofa Wu Ziyue Wang Xiang Fei Meiling Qin Lizhao Wang Yulong Li Siyu Zhang Min Xu Adenosine-independent regulation of the sleep–wake cycle by astrocyte activity Cell Discovery |
title | Adenosine-independent regulation of the sleep–wake cycle by astrocyte activity |
title_full | Adenosine-independent regulation of the sleep–wake cycle by astrocyte activity |
title_fullStr | Adenosine-independent regulation of the sleep–wake cycle by astrocyte activity |
title_full_unstemmed | Adenosine-independent regulation of the sleep–wake cycle by astrocyte activity |
title_short | Adenosine-independent regulation of the sleep–wake cycle by astrocyte activity |
title_sort | adenosine independent regulation of the sleep wake cycle by astrocyte activity |
url | https://doi.org/10.1038/s41421-022-00498-9 |
work_keys_str_mv | AT wanlingpeng adenosineindependentregulationofthesleepwakecyclebyastrocyteactivity AT xiaotongliu adenosineindependentregulationofthesleepwakecyclebyastrocyteactivity AT guofenma adenosineindependentregulationofthesleepwakecyclebyastrocyteactivity AT zhaofawu adenosineindependentregulationofthesleepwakecyclebyastrocyteactivity AT ziyuewang adenosineindependentregulationofthesleepwakecyclebyastrocyteactivity AT xiangfei adenosineindependentregulationofthesleepwakecyclebyastrocyteactivity AT meilingqin adenosineindependentregulationofthesleepwakecyclebyastrocyteactivity AT lizhaowang adenosineindependentregulationofthesleepwakecyclebyastrocyteactivity AT yulongli adenosineindependentregulationofthesleepwakecyclebyastrocyteactivity AT siyuzhang adenosineindependentregulationofthesleepwakecyclebyastrocyteactivity AT minxu adenosineindependentregulationofthesleepwakecyclebyastrocyteactivity |