Transient Opening of the Mitochondrial Permeability Transition Pore Induces Microdomain Calcium Transients in Astrocyte Processes

Agarwal, Amit; Wu, Pei-Hsun; Hughes, Ethan G.; Fukaya, Masahiro; Tischfield, Max A.; Langseth, Abraham J.; Wirtz, Denis; Bergles, Dwight E.

doi:10.1016/j.neuron.2016.12.034

Cited by 441Mitochondrial Function and PathologyNeuroscience and Neuropharmacology ResearchCalcium signaling and nucleotide metabolism

Transient Opening of the Mitochondrial Permeability Transition Pore Induces Microdomain Calcium Transients in Astrocyte Processes

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Agarwal, Amit, Wu, Pei-Hsun, Hughes, Ethan G., Fukaya, Masahiro, Tischfield, Max A., Langseth, Abraham J., Wirtz, Denis, Bergles, Dwight E.·2017·Neuron

DOI 10.1016/j.neuron.2016.12.034PMC PMC5308886

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Abstract

Astrocytes extend highly branched processes that form functionally isolated microdomains, facilitating local homeostasis by redistributing ions, removing neurotransmitters, and releasing factors to influence blood flow and neuronal activity. Microdomains exhibit spontaneous increases in calcium (Ca 2+), but the mechanisms and functional significance of this localized signaling are unknown. By developing conditional, membrane-anchored GCaMP3 mice, we found that microdomain activity that occurs in the absence of inositol triphosphate (IP3)-dependent release from endoplasmic reticulum arises through Ca 2+ efflux from mitochondria during brief openings of the mitochondrial permeability transition pore. These microdomain Ca 2+ transients were facilitated by the production of reactive oxygen species during oxidative phosphorylation and were enhanced by expression of a mutant form of superoxide dismutase 1 (SOD1 G93A) that causes astrocyte dysfunction and neurodegeneration in amyotrophic lateral sclerosis (ALS). By localizing mitochondria to microdomains, astrocytes ensure local metabolic support for energetically demanding processes and enable coupling between metabolic demand and Ca 2+ signaling events.

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Astrocyte Ca2+ dynamics and network responses become aberrant in mouse models of HD, AD, and ALS, possibly contributing to cognitive impairment and neuropathology.
“Astrocyte Ca2+ dynamics and network responses become aberrant in mouse models of HD53, AD54, and ALS55, possibly contributing to cognitive impairment and neuropathology43,53,56.”
From Reactive astrocyte nomenclature, definitions, and future directions (2021) · cites this paper as [55]
Optogenetics and DREADDs are potential tools to manipulate reactive astrocytes or to restore their aberrant Ca2+ signaling observed in mouse models of neurodegenerative diseases.
“Optogenetics25 and designer receptors exclusively activated by designer drugs (DREADDs)25 are potential tools to manipulate reactive astrocytes or to restore their aberrant Ca2+ signaling observed in mouse models of neurodegenerative diseases53–55.”
From Reactive astrocyte nomenclature, definitions, and future directions (2021) · cites this paper as [55]
Artificial intelligence can identify patterns of Ca2+ signaling in astrocytes.
“Artificial intelligence can identify patterns of Ca2+ signaling in astrocytes55,120.”
From Reactive astrocyte nomenclature, definitions, and future directions (2021) · cites this paper as [55]

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Authors: Agarwal, A., Wu, P.-H., Hughes, E. G., Fukaya, M., Tischfield, M. A., Langseth, A. J., Wirtz, D., & Bergles, D. E.
Affiliations: Johns Hopkins University (US)
Kitasato University (JP)
Corresponding author: Bergles, Dwight E.
ORCID: Agarwal, Amit
Wu, Pei-Hsun
Hughes, Ethan G.
Fukaya, Masahiro
Tischfield, Max A.
Langseth, Abraham J.
Wirtz, Denis
Bergles, Dwight E.
Venue: Neuron
Publisher: Elsevier BV
Published: 2017-02
Volume: 93
Issue: 3
Pages: 587-605.e7
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/j.neuron.2016.12.034
PMC: PMC5308886
OpenAlex: W2582695863
Cited by: 441
References: 54
Citations by year: 2026: 26 · 2025: 46 · 2024: 39 · 2023: 54 · 2022: 65 · 2021: 63 · 2020: 58 · 2019: 35 · 2018: 40 · 2017: 15
FWCI: 16.54
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 372 d)
Locations: Neuron (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Multiple Sclerosis Society
NARSAD Young Investigator Grant (#24161)
Brain & Behavior Research Foundation (MH084020)
Conte Center for Neuroscience (NS050274)
NIH
Brain Science Institute at Johns Hopkins
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
Keywords: mitochondrial permeability transition pore, astrocyte processes, calcium microdomains, mitochondrial calcium efflux, GCaMP3, reactive oxygen species, oxidative phosphorylation, superoxide dismutase 1, SOD1 G93A, amyotrophic lateral sclerosis, astrocyte dysfunction, mitochondrial localization, calcium signaling, energy metabolism
MeSH terms: Superoxide Dismutase-1, Mitochondrial Permeability Transition Pore, Amyotrophic Lateral Sclerosis, Animals, Astrocytes, Calcium, Endoplasmic Reticulum, Mitochondria, Oxidative Phosphorylation, Inositol 1,4,5-Trisphosphate, Reactive Oxygen Species, Mitochondrial Membrane Transport Proteins, Mice

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Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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Transient Opening of the Mitochondrial Permeability Transition Pore Induces Microdomain Calcium Transients in Astrocyte Processes

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