Circadian regulation of endoplasmic reticulum calcium response in cultured mouse astrocytes

The circadian clock, an internal time-keeping system orchestrates 24 hr rhythms in physiology and behavior by regulating rhythmic transcription in cells. Astrocytes, the most abundant glial cells, play crucial roles in CNS functions, but the impact of the circadian clock on astrocyte functions remai...

Full description

Saved in:
Bibliographic Details
Main Authors: Ji Eun Ryu, Kyu-Won Shim, Hyun Woong Roh, Minsung Park, Jae-Hyung Lee, Eun Young Kim
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2024-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/96357
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1846141177357664256
author Ji Eun Ryu
Kyu-Won Shim
Hyun Woong Roh
Minsung Park
Jae-Hyung Lee
Eun Young Kim
author_facet Ji Eun Ryu
Kyu-Won Shim
Hyun Woong Roh
Minsung Park
Jae-Hyung Lee
Eun Young Kim
author_sort Ji Eun Ryu
collection DOAJ
description The circadian clock, an internal time-keeping system orchestrates 24 hr rhythms in physiology and behavior by regulating rhythmic transcription in cells. Astrocytes, the most abundant glial cells, play crucial roles in CNS functions, but the impact of the circadian clock on astrocyte functions remains largely unexplored. In this study, we identified 412 circadian rhythmic transcripts in cultured mouse cortical astrocytes through RNA sequencing. Gene Ontology analysis indicated that genes involved in Ca2+ homeostasis are under circadian control. Notably, Herpud1 (Herp) exhibited robust circadian rhythmicity at both mRNA and protein levels, a rhythm disrupted in astrocytes lacking the circadian transcription factor, BMAL1. HERP regulated endoplasmic reticulum (ER) Ca2+ release by modulating the degradation of inositol 1,4,5-trisphosphate receptors (ITPRs). ATP-stimulated ER Ca2+ release varied with the circadian phase, being more pronounced at subjective night phase, likely due to the rhythmic expression of ITPR2. Correspondingly, ATP-stimulated cytosolic Ca2+ increases were heightened at the subjective night phase. This rhythmic ER Ca2+ response led to circadian phase-dependent variations in the phosphorylation of Connexin 43 (Ser368) and gap junctional communication. Given the role of gap junction channel (GJC) in propagating Ca2+ signals, we suggest that this circadian regulation of ER Ca2+ responses could affect astrocytic modulation of synaptic activity according to the time of day. Overall, our study enhances the understanding of how the circadian clock influences astrocyte function in the CNS, shedding light on their potential role in daily variations of brain activity and health.
format Article
id doaj-art-2f587f1ff5344b11b6a0058a0f81bb3f
institution Kabale University
issn 2050-084X
language English
publishDate 2024-11-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj-art-2f587f1ff5344b11b6a0058a0f81bb3f2024-12-04T15:34:16ZengeLife Sciences Publications LtdeLife2050-084X2024-11-011310.7554/eLife.96357Circadian regulation of endoplasmic reticulum calcium response in cultured mouse astrocytesJi Eun Ryu0https://orcid.org/0009-0000-1438-5018Kyu-Won Shim1Hyun Woong Roh2Minsung Park3Jae-Hyung Lee4https://orcid.org/0000-0002-5085-6988Eun Young Kim5https://orcid.org/0000-0001-6466-8622Neuroscience Graduate Program, Department of Biomedical Sciences, Ajou University Graduate School of Medicine, Suwon, Republic of Korea; Department of Brain Science, Ajou University School of Medicine, Suwon, Republic of KoreaInterdisciplinary Program in Bioinformatics, Seoul National University, Seoul, Republic of KoreaNeuroscience Graduate Program, Department of Biomedical Sciences, Ajou University Graduate School of Medicine, Suwon, Republic of Korea; Department of Psychiatry, Ajou University School of Medicine, Suwon, Republic of KoreaNeuroscience Graduate Program, Department of Biomedical Sciences, Ajou University Graduate School of Medicine, Suwon, Republic of Korea; Department of Brain Science, Ajou University School of Medicine, Suwon, Republic of KoreaDepartment of Oral Microbiology, College of Dentistry, Kyung Hee University, Seoul, Republic of KoreaNeuroscience Graduate Program, Department of Biomedical Sciences, Ajou University Graduate School of Medicine, Suwon, Republic of Korea; Department of Brain Science, Ajou University School of Medicine, Suwon, Republic of KoreaThe circadian clock, an internal time-keeping system orchestrates 24 hr rhythms in physiology and behavior by regulating rhythmic transcription in cells. Astrocytes, the most abundant glial cells, play crucial roles in CNS functions, but the impact of the circadian clock on astrocyte functions remains largely unexplored. In this study, we identified 412 circadian rhythmic transcripts in cultured mouse cortical astrocytes through RNA sequencing. Gene Ontology analysis indicated that genes involved in Ca2+ homeostasis are under circadian control. Notably, Herpud1 (Herp) exhibited robust circadian rhythmicity at both mRNA and protein levels, a rhythm disrupted in astrocytes lacking the circadian transcription factor, BMAL1. HERP regulated endoplasmic reticulum (ER) Ca2+ release by modulating the degradation of inositol 1,4,5-trisphosphate receptors (ITPRs). ATP-stimulated ER Ca2+ release varied with the circadian phase, being more pronounced at subjective night phase, likely due to the rhythmic expression of ITPR2. Correspondingly, ATP-stimulated cytosolic Ca2+ increases were heightened at the subjective night phase. This rhythmic ER Ca2+ response led to circadian phase-dependent variations in the phosphorylation of Connexin 43 (Ser368) and gap junctional communication. Given the role of gap junction channel (GJC) in propagating Ca2+ signals, we suggest that this circadian regulation of ER Ca2+ responses could affect astrocytic modulation of synaptic activity according to the time of day. Overall, our study enhances the understanding of how the circadian clock influences astrocyte function in the CNS, shedding light on their potential role in daily variations of brain activity and health.https://elifesciences.org/articles/96357astrocytescircadiangap junctionsCa2+Herpud1endoplasmic reticulum
spellingShingle Ji Eun Ryu
Kyu-Won Shim
Hyun Woong Roh
Minsung Park
Jae-Hyung Lee
Eun Young Kim
Circadian regulation of endoplasmic reticulum calcium response in cultured mouse astrocytes
eLife
astrocytes
circadian
gap junctions
Ca2+
Herpud1
endoplasmic reticulum
title Circadian regulation of endoplasmic reticulum calcium response in cultured mouse astrocytes
title_full Circadian regulation of endoplasmic reticulum calcium response in cultured mouse astrocytes
title_fullStr Circadian regulation of endoplasmic reticulum calcium response in cultured mouse astrocytes
title_full_unstemmed Circadian regulation of endoplasmic reticulum calcium response in cultured mouse astrocytes
title_short Circadian regulation of endoplasmic reticulum calcium response in cultured mouse astrocytes
title_sort circadian regulation of endoplasmic reticulum calcium response in cultured mouse astrocytes
topic astrocytes
circadian
gap junctions
Ca2+
Herpud1
endoplasmic reticulum
url https://elifesciences.org/articles/96357
work_keys_str_mv AT jieunryu circadianregulationofendoplasmicreticulumcalciumresponseinculturedmouseastrocytes
AT kyuwonshim circadianregulationofendoplasmicreticulumcalciumresponseinculturedmouseastrocytes
AT hyunwoongroh circadianregulationofendoplasmicreticulumcalciumresponseinculturedmouseastrocytes
AT minsungpark circadianregulationofendoplasmicreticulumcalciumresponseinculturedmouseastrocytes
AT jaehyunglee circadianregulationofendoplasmicreticulumcalciumresponseinculturedmouseastrocytes
AT eunyoungkim circadianregulationofendoplasmicreticulumcalciumresponseinculturedmouseastrocytes