Amyloid-β-induced alteration of fast and localized calcium elevations in cultured astrocytes

Abstract Alzheimer’s disease (AD) is a progressive neurodegenerative disorder that causes cognitive decline. Uncovering the mechanisms of neurodegeneration in the early stages is essential to establish a treatment for AD. Recent research has proposed the hypothesis that amyloid-β (Aβ) oligomers elic...

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Main Authors: Kaito Nakata, Joe Sakamoto, Kohei Otomo, Masanao Sato, Hirokazu Ishii, Motosuke Tsutsumi, Ryosuke Enoki, Tomomi Nemoto
Format: Article
Language:English
Published: Nature Portfolio 2025-05-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-025-03931-7
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author Kaito Nakata
Joe Sakamoto
Kohei Otomo
Masanao Sato
Hirokazu Ishii
Motosuke Tsutsumi
Ryosuke Enoki
Tomomi Nemoto
author_facet Kaito Nakata
Joe Sakamoto
Kohei Otomo
Masanao Sato
Hirokazu Ishii
Motosuke Tsutsumi
Ryosuke Enoki
Tomomi Nemoto
author_sort Kaito Nakata
collection DOAJ
description Abstract Alzheimer’s disease (AD) is a progressive neurodegenerative disorder that causes cognitive decline. Uncovering the mechanisms of neurodegeneration in the early stages is essential to establish a treatment for AD. Recent research has proposed the hypothesis that amyloid-β (Aβ) oligomers elicit an excessive glutamate release from astrocytes toward synapses through intracellular free Ca2+ ([Ca2+] i ) elevations in astrocytes, finally resulting in neuronal dendritic spine loss. Under physiological conditions, astrocytic [Ca2+] i elevations range spatially from microdomains to network-wide propagation and temporally from milliseconds to tens of seconds. Astrocytic localized and fast [Ca2+] i elevations might correlate with glutamate release; however, the Aβ-induced alteration of localized, fast astrocytic [Ca2+] i elevations remains unexplored. In this study, we quantitatively investigated the Aβ dimers-induced changes in the spatial and temporal patterns of [Ca2+] i in a primary culture of astrocytes by two-photon excitation spinning-disk confocal microscopy. The frequency of fast [Ca2+] i elevations occurring locally in astrocytes (≤ 0.5 s, ≤ 35 µm2) and [Ca2+] i event occupancy relative to cell area significantly increased after exposure to Aβ dimers. The effect of Aβ dimers appeared above 500 nM, and these Aβ dimers-induced [Ca2+] i elevations were primarily mediated by a metabotropic purinergic receptor (P2Y1 receptor) and Ca2+ release from the endoplasmic reticulum. Our findings suggest that the Aβ dimers-induced alterations and hyperactivation of astrocytic [Ca2+] i is a candidate cellular mechanism in the early stages of AD.
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spelling doaj-art-609e5d09a7d54b848f45e3e5d6a7d6352025-08-20T03:22:07ZengNature PortfolioScientific Reports2045-23222025-05-0115111010.1038/s41598-025-03931-7Amyloid-β-induced alteration of fast and localized calcium elevations in cultured astrocytesKaito Nakata0Joe Sakamoto1Kohei Otomo2Masanao Sato3Hirokazu Ishii4Motosuke Tsutsumi5Ryosuke Enoki6Tomomi Nemoto7School of Life Science, The Graduate University for Advanced Studies, SOKENDAIDivision of Biophotonics, National Institute for Physiological Sciences (NIPS), National Institutes of Natural Sciences (NINS)Division of Biophotonics, National Institute for Physiological Sciences (NIPS), National Institutes of Natural Sciences (NINS)Laboratory of Applied Molecular Entomology, Division of Applied Bioscience, Research Faculty of Agriculture, Hokkaido UniversitySchool of Life Science, The Graduate University for Advanced Studies, SOKENDAIDivision of Biophotonics, National Institute for Physiological Sciences (NIPS), National Institutes of Natural Sciences (NINS)School of Life Science, The Graduate University for Advanced Studies, SOKENDAISchool of Life Science, The Graduate University for Advanced Studies, SOKENDAIAbstract Alzheimer’s disease (AD) is a progressive neurodegenerative disorder that causes cognitive decline. Uncovering the mechanisms of neurodegeneration in the early stages is essential to establish a treatment for AD. Recent research has proposed the hypothesis that amyloid-β (Aβ) oligomers elicit an excessive glutamate release from astrocytes toward synapses through intracellular free Ca2+ ([Ca2+] i ) elevations in astrocytes, finally resulting in neuronal dendritic spine loss. Under physiological conditions, astrocytic [Ca2+] i elevations range spatially from microdomains to network-wide propagation and temporally from milliseconds to tens of seconds. Astrocytic localized and fast [Ca2+] i elevations might correlate with glutamate release; however, the Aβ-induced alteration of localized, fast astrocytic [Ca2+] i elevations remains unexplored. In this study, we quantitatively investigated the Aβ dimers-induced changes in the spatial and temporal patterns of [Ca2+] i in a primary culture of astrocytes by two-photon excitation spinning-disk confocal microscopy. The frequency of fast [Ca2+] i elevations occurring locally in astrocytes (≤ 0.5 s, ≤ 35 µm2) and [Ca2+] i event occupancy relative to cell area significantly increased after exposure to Aβ dimers. The effect of Aβ dimers appeared above 500 nM, and these Aβ dimers-induced [Ca2+] i elevations were primarily mediated by a metabotropic purinergic receptor (P2Y1 receptor) and Ca2+ release from the endoplasmic reticulum. Our findings suggest that the Aβ dimers-induced alterations and hyperactivation of astrocytic [Ca2+] i is a candidate cellular mechanism in the early stages of AD.https://doi.org/10.1038/s41598-025-03931-7Amyloid-βAlzheimer’s diseaseAstrocyteCa2+Two-photon microscopy
spellingShingle Kaito Nakata
Joe Sakamoto
Kohei Otomo
Masanao Sato
Hirokazu Ishii
Motosuke Tsutsumi
Ryosuke Enoki
Tomomi Nemoto
Amyloid-β-induced alteration of fast and localized calcium elevations in cultured astrocytes
Scientific Reports
Amyloid-β
Alzheimer’s disease
Astrocyte
Ca2+
Two-photon microscopy
title Amyloid-β-induced alteration of fast and localized calcium elevations in cultured astrocytes
title_full Amyloid-β-induced alteration of fast and localized calcium elevations in cultured astrocytes
title_fullStr Amyloid-β-induced alteration of fast and localized calcium elevations in cultured astrocytes
title_full_unstemmed Amyloid-β-induced alteration of fast and localized calcium elevations in cultured astrocytes
title_short Amyloid-β-induced alteration of fast and localized calcium elevations in cultured astrocytes
title_sort amyloid β induced alteration of fast and localized calcium elevations in cultured astrocytes
topic Amyloid-β
Alzheimer’s disease
Astrocyte
Ca2+
Two-photon microscopy
url https://doi.org/10.1038/s41598-025-03931-7
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AT masanaosato amyloidbinducedalterationoffastandlocalizedcalciumelevationsinculturedastrocytes
AT hirokazuishii amyloidbinducedalterationoffastandlocalizedcalciumelevationsinculturedastrocytes
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