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Astrocyte uncoupling as a cause of human temporal lobe epilepsy

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Bedner, Peter, Dupper, Alexander, Hüttmann, Kerstin, Müller, Julia, Herde, Michel K., Dublin, Pavel, Deshpande, Tushar, Schramm, Johannes +5 more·2015·Brain
DOI 10.1093/brain/awv067PMC PMC5963418
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Abstract

Glial cells are now recognized as active communication partners in the central nervous system, and this new perspective has rekindled the question of their role in pathology. In the present study we analysed functional properties of astrocytes in hippocampal specimens from patients with mesial temporal lobe epilepsy without (n = 44) and with sclerosis (n = 75) combining patch clamp recording, K(+) concentration analysis, electroencephalography/video-monitoring, and fate mapping analysis. We found that the hippocampus of patients with mesial temporal lobe epilepsy with sclerosis is completely devoid of bona fide astrocytes and gap junction coupling, whereas coupled astrocytes were abundantly present in non-sclerotic specimens. To decide whether these glial changes represent cause or effect of mesial temporal lobe epilepsy with sclerosis, we developed a mouse model that reproduced key features of human mesial temporal lobe epilepsy with sclerosis. In this model, uncoupling impaired K(+) buffering and temporally preceded apoptotic neuronal death and the generation of spontaneous seizures. Uncoupling was induced through intraperitoneal injection of lipopolysaccharide, prevented in Toll-like receptor4 knockout mice and reproduced in situ through acute cytokine or lipopolysaccharide incubation. Fate mapping confirmed that in the course of mesial temporal lobe epilepsy with sclerosis, astrocytes acquire an atypical functional phenotype and lose coupling. These data suggest that astrocyte dysfunction might be a prime cause of mesial temporal lobe epilepsy with sclerosis and identify novel targets for anti-epileptogenic therapeutic intervention.

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  • Functions lost or altered in reactive astrocytes include neurotransmitter and ion buffering in mouse HD models, communication via gap junctions in the sclerotic hippocampus of patients with epilepsy, phagocytic clearance of dystrophic neurites, and metabolic coupling by glycolysis-derived d-serine and lactate in mouse AD models.

    “Functions lost or altered in reactive astrocytes include neurotransmitter and ion buffering in mouse HD models58, communication via gap junctions in the sclerotic hippocampus of patients with epilepsy59, phagocytic clearance of dystrophic neurites60, and metabolic coupling by glycolysis-derived d-serine61 and lactate62 in mouse AD models.”

    From Reactive astrocyte nomenclature, definitions, and future directions (2021) · cites this paper as [59]

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Authors
Bedner, P., Dupper, A., Hüttmann, K., Müller, J., Herde, M. K., Dublin, P., Deshpande, T., Schramm, J., Häussler, U., Haas, C. A., Henneberger, C., Theis, M., & Steinhäuser, C.
Affiliations
  • University of Bonn (DE)
  • University Medical Center Freiburg (DE)
ORCID
Venue
Brain
Publisher
Oxford University Press (OUP)
Published
2015-03-12
Volume
138
Issue
5
Pages
1208-1222
ISSN
  • 0006-8950 (ISSN-L)
  • 1460-2156
DOI
10.1093/brain/awv067
PMC
PMC5963418
OpenAlex
W2147191089
Cited by
328
References
2
Citations by year
2026: 18 · 2025: 29 · 2024: 26 · 2023: 31 · 2022: 32 · 2021: 42 · 2020: 31 · 2019: 27 · 2018: 23 · 2017: 24 · 2016: 30 · 2015: 12 · 2014: 1
FWCI
24.10
Type
journal article
Language
en
Open access
Locations
  • Brain (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • UCL Discovery (University College London) (submittedVersion)
  • FreiDok plus (Universitätsbibliothek Freiburg) (submittedVersion)
Topics
  • Health Sciences › Medicine › Psychiatry and Mental health › Epilepsy research and treatment
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Connexins and lens biology
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
mesial temporal lobe epilepsy, hippocampal sclerosis, electrical coupling, potassium buffering, lipopolysaccharide, TLR4, neuronal apoptosis, spontaneous seizures, glial dysfunction
MeSH terms
Animals, Astrocytes, Electroencephalography, Epilepsy, Temporal Lobe, Hippocampus, Humans, Male, Sclerosis, Seizures, Gap Junctions, Mice

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