Astroglial Kir4.1 potassium channel deficit drives neuronal hyperexcitability and behavioral defects in Fragile X syndrome mouse model.

Animals Astrocytes / metabolism Fragile X Syndrome / metabolism Fragile X Mental Retardation Protein / metabolism Potassium Channels, Inwardly Rectifying / metabolism Mice, Knockout Disease Models, Animal Male Mice Neurons / metabolism Hippocampus / metabolism Behavior, Animal Potassium / metabolism Mice, Inbred C57BL RNA, Messenger / metabolism

Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
27 Apr 2024
Historique:
received: 27 07 2021
accepted: 03 04 2024
medline: 28 4 2024
pubmed: 28 4 2024
entrez: 27 4 2024
Statut: epublish

Résumé

Fragile X syndrome (FXS) is an inherited form of intellectual disability caused by the loss of the mRNA-binding fragile X mental retardation protein (FMRP). FXS is characterized by neuronal hyperexcitability and behavioral defects, however the mechanisms underlying these critical dysfunctions remain unclear. Here, using male Fmr1 knockout mouse model of FXS, we identify abnormal extracellular potassium homeostasis, along with impaired potassium channel Kir4.1 expression and function in astrocytes. Further, we reveal that Kir4.1 mRNA is a binding target of FMRP. Finally, we show that the deficit in astroglial Kir4.1 underlies neuronal hyperexcitability and several behavioral defects in Fmr1 knockout mice. Viral delivery of Kir4.1 channels specifically to hippocampal astrocytes from Fmr1 knockout mice indeed rescues normal astrocyte potassium uptake, neuronal excitability, and cognitive and social performance. Our findings uncover an important role for astrocyte dysfunction in the pathophysiology of FXS, and identify Kir4.1 channel as a potential therapeutic target for FXS.

Identifiants

DOI: 10.1038/s41467-024-47681-y PMID: 38678030
pubmed: 38678030
doi: 10.1038/s41467-024-47681-y
pii: 10.1038/s41467-024-47681-y
doi:

Substances chimiques

Fragile X Mental Retardation Protein 139135-51-6
Potassium Channels, Inwardly Rectifying 0
Kcnj10 (channel) 0
Fmr1 protein, mouse 0
Potassium RWP5GA015D
RNA, Messenger 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

3583

Subventions

Organisme : EC | EC Seventh Framework Programm | FP7 Ideas: European Research Council (FP7-IDEAS-ERC - Specific Programme: "Ideas" Implementing the Seventh Framework Programme of the European Community for Research, Technological Development and Demonstration Activities (2007 to 2013))
ID : 683154
Organisme : EC | Horizon 2020 Framework Programme (EU Framework Programme for Research and Innovation H2020)
ID : 722053
Organisme : Fondation Jérôme Lejeune (Jérôme Lejeune Foundation)
ID : 1535

Informations de copyright

© 2024. The Author(s).

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Auteurs

Danijela Bataveljic (D)

Neuroglial Interactions in Cerebral Physiology and Pathologies, Center for Interdisciplinary Research in Biology, Collège de France, CNRS, INSERM, Labex Memolife, Université PSL, Paris, France.
Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium.
ORCID: 0000-0002-9593-8231

Helena Pivonkova (H)

Neuroglial Interactions in Cerebral Physiology and Pathologies, Center for Interdisciplinary Research in Biology, Collège de France, CNRS, INSERM, Labex Memolife, Université PSL, Paris, France.
Department of Physiology, 2nd Faculty of Medicine, Charles University, Prague, Czech Republic.

Vidian de Concini (V)

Experimental and Molecular Immunology and Neurogenetics, CNRS UMR7355 and Orléans University, Orléans, France.

Betty Hébert (B)

Experimental and Molecular Immunology and Neurogenetics, CNRS UMR7355 and Orléans University, Orléans, France.

Pascal Ezan (P)

Neuroglial Interactions in Cerebral Physiology and Pathologies, Center for Interdisciplinary Research in Biology, Collège de France, CNRS, INSERM, Labex Memolife, Université PSL, Paris, France.

Sylvain Briault (S)

Experimental and Molecular Immunology and Neurogenetics, CNRS UMR7355 and Orléans University, Orléans, France.
Department of Genetics, Regional Hospital, Orléans, France.

Alexis-Pierre Bemelmans (AP)

Commissariat à l'Energie Atomique et aux Energies Alternatives (CEA), Département de la Recherche Fondamentale, Institut de biologie François Jacob, MIRCen, and CNRS UMR 9199, Université Paris-Sud, Neurodegenerative Diseases Laboratory, Fontenay-aux-Roses, 92260, France.
ORCID: 0000-0001-7605-5225

Jacques Pichon (J)

Experimental and Molecular Immunology and Neurogenetics, CNRS UMR7355 and Orléans University, Orléans, France.

Arnaud Menuet (A)

Experimental and Molecular Immunology and Neurogenetics, CNRS UMR7355 and Orléans University, Orléans, France.

Nathalie Rouach (N)

Neuroglial Interactions in Cerebral Physiology and Pathologies, Center for Interdisciplinary Research in Biology, Collège de France, CNRS, INSERM, Labex Memolife, Université PSL, Paris, France. nathalie.rouach@college-de-france.fr.
ORCID: 0000-0002-5574-888X

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Astroglial Kir4.1 potassium channel deficit...
questionsmedicales.fr › Cellules › Névroglie › Astrocytes › Astroglial Kir4.1 potassium channel deficit...
questionsmedicales.fr › Malformations et maladies congénitales, héréditaires et néonatales › Maladies génétiques congénitales › Maladies neurodégénératives héréditaires › Retard mental lié à l'X › Syndrome du chromosome X fragile › Astroglial Kir4.1 potassium channel deficit...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Nucléoprotéines › Protéines de liaison à l'ARN › Protéine du syndrome X fragile › Astroglial Kir4.1 potassium channel deficit...
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questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Astroglial Kir4.1 potassium channel deficit...
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