Human NMDAR autoantibodies disrupt excitatory-inhibitory balance, leading to hippocampal network hypersynchrony.

CP: Neuroscience NMDA receptor NMDA receptor encephalitis autoantibodies excitatory-inhibitory imbalance microglia network oscillation neural network modeling θ-γ coupling

Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
31 10 2023
Historique:
received: 31 05 2022
revised: 30 06 2023
accepted: 07 09 2023
medline: 6 11 2023
pubmed: 28 9 2023
entrez: 28 9 2023
Statut: ppublish

Résumé

Anti-NMDA receptor autoantibodies (NMDAR-Abs) in patients with NMDAR encephalitis cause severe disease symptoms resembling psychosis and cause cognitive dysfunction. After passive transfer of patients' cerebrospinal fluid or human monoclonal anti-GluN1-autoantibodies in mice, we find a disrupted excitatory-inhibitory balance resulting from CA1 neuronal hypoexcitability, reduced AMPA receptor (AMPAR) signaling, and faster synaptic inhibition in acute hippocampal slices. Functional alterations are also reflected in widespread remodeling of the hippocampal proteome, including changes in glutamatergic and GABAergic neurotransmission. NMDAR-Abs amplify network γ oscillations and disrupt θ-γ coupling. A data-informed network model reveals that lower AMPAR strength and faster GABA

Identifiants

pubmed: 37768823
pii: S2211-1247(23)01178-6
doi: 10.1016/j.celrep.2023.113166
pii:
doi:

Substances chimiques

Receptors, N-Methyl-D-Aspartate 0
Autoantibodies 0
Receptors, AMPA 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

113166

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests J.D. receives royalties from Euroimmun for the use of the NMDA receptor as an antibody test.

Auteurs

Mihai Ceanga (M)

Section of Translational Neuroimmunology, Department of Neurology, Jena University Hospital, 07747 Jena, Germany.

Vahid Rahmati (V)

Section of Translational Neuroimmunology, Department of Neurology, Jena University Hospital, 07747 Jena, Germany.

Holger Haselmann (H)

Section of Translational Neuroimmunology, Department of Neurology, Jena University Hospital, 07747 Jena, Germany.

Lars Schmidl (L)

Section of Translational Neuroimmunology, Department of Neurology, Jena University Hospital, 07747 Jena, Germany.

Daniel Hunter (D)

Université de Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, UMR 5297, 33000 Bordeaux, France.

Anna-Katherina Brauer (AK)

Institute of Clinical Neuroimmunology, Klinikum der Universität München, Ludwig Maximilians University Munich, Martinsried, Germany; Biomedical Center, Ludwig Maximilians University Munich, Martinsried, Germany.

Sabine Liebscher (S)

Institute of Clinical Neuroimmunology, Klinikum der Universität München, Ludwig Maximilians University Munich, Martinsried, Germany; Biomedical Center, Ludwig Maximilians University Munich, Martinsried, Germany; Munich Cluster for Systems Neurology (SyNergy), Munich, Germany.

Jakob Kreye (J)

Department of Neurology and Experimental Neurology, Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, 10117 Berlin, Germany; German Center for Neurodegenerative Diseases (DZNE) Berlin, Berlin, Germany; Department of Pediatric Neurology, Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, 10117 Berlin, Germany.

Harald Prüss (H)

Department of Neurology and Experimental Neurology, Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, 10117 Berlin, Germany; German Center for Neurodegenerative Diseases (DZNE) Berlin, Berlin, Germany.

Laurent Groc (L)

Université de Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, UMR 5297, 33000 Bordeaux, France.

Stefan Hallermann (S)

Carl Ludwig Institute for Physiology, Faculty of Medicine, Leipzig University, 04103 Leipzig, Germany.

Josep Dalmau (J)

Catalan Institution for Research and Advanced Studies (ICREA) and IDIBAPS-Hospital Clinic, University of Barcelona, 08036 Barcelona, Spain.

Alessandro Ori (A)

Leibniz Institute on Aging - Fritz Lipmann Institute (FLI), 07745 Jena, Germany.

Manfred Heckmann (M)

Department of Neurophysiology, Institute of Physiology, University of Würzburg, 97070 Würzburg, Germany.

Christian Geis (C)

Section of Translational Neuroimmunology, Department of Neurology, Jena University Hospital, 07747 Jena, Germany. Electronic address: christian.geis@med.uni-jena.de.

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Classifications MeSH