Interleukin-4 receptor signaling modulates neuronal network activity.


Journal

The Journal of experimental medicine
ISSN: 1540-9538
Titre abrégé: J Exp Med
Pays: United States
ID NLM: 2985109R

Informations de publication

Date de publication:
06 06 2022
Historique:
received: 06 09 2021
revised: 13 12 2021
accepted: 29 04 2022
entrez: 19 5 2022
pubmed: 20 5 2022
medline: 24 5 2022
Statut: ppublish

Résumé

Evidence is emerging that immune responses not only play a part in the central nervous system (CNS) in diseases but may also be relevant for healthy conditions. We discovered a major role for the interleukin-4 (IL-4)/IL-4 receptor alpha (IL-4Rα) signaling pathway in synaptic processes, as indicated by transcriptome analysis in IL-4Rα-deficient mice and human neurons with/without IL-4 treatment. Moreover, IL-4Rα is expressed presynaptically, and locally available IL-4 regulates synaptic transmission. We found reduced synaptic vesicle pools, altered postsynaptic currents, and a higher excitatory drive in cortical networks of IL-4Rα-deficient neurons. Acute effects of IL-4 treatment on postsynaptic currents in wild-type neurons were mediated via PKCγ signaling release and led to increased inhibitory activity supporting the findings in IL-4Rα-deficient neurons. In fact, the deficiency of IL-4Rα resulted in increased network activity in vivo, accompanied by altered exploration and anxiety-related learning behavior; general learning and memory was unchanged. In conclusion, neuronal IL-4Rα and its presynaptic prevalence appear relevant for maintaining homeostasis of CNS synaptic function.

Identifiants

pubmed: 35587822
pii: 213227
doi: 10.1084/jem.20211887
pmc: PMC9123307
pii:
doi:

Substances chimiques

Receptors, Interleukin-4 0
Interleukin-4 207137-56-2

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : German Research Foundation
ID : CRC 1080
Organisme : Germany Excellence Strategy
ID : EXC 2030-390661388
Organisme : Federal Ministry of Education and Research
ID : VIP + HaltMS-03VP07030
Organisme : Progressive MS Alliance
ID : PA-1604-08492

Informations de copyright

© 2022 Hanuscheck et al.

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Auteurs

Nicholas Hanuscheck (N)

Department of Neurology, Focus Program Translational Neuroscience and Immunotherapy, Rhine Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.

Carine Thalman (C)

Department of Neurology, Focus Program Translational Neuroscience and Immunotherapy, Rhine Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.

Micaela Domingues (M)

Department of Neurology, Focus Program Translational Neuroscience and Immunotherapy, Rhine Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.

Samantha Schmaul (S)

Department of Neurology, Focus Program Translational Neuroscience and Immunotherapy, Rhine Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.

Muthuraman Muthuraman (M)

Department of Neurology, Focus Program Translational Neuroscience and Immunotherapy, Rhine Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.

Florian Hetsch (F)

Institute for Pathophysiology, Focus Program Translational Neuroscience, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.

Manuela Ecker (M)

Department of Neurology, Focus Program Translational Neuroscience and Immunotherapy, Rhine Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.

Heiko Endle (H)

Department of Molecular and Translational Neuroscience, Cluster of Excellence-Cellular Stress Response in Aging-Associated Diseases and Center of Molecular Medicine Cologne, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Mohammadsaleh Oshaghi (M)

Department of Neurology, Focus Program Translational Neuroscience and Immunotherapy, Rhine Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.

Gianvito Martino (G)

Neuroimmunology Unit, Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute and Vita Salute San Raffaele University, Milan, Italy.

Tanja Kuhlmann (T)

Institute for Neuropathology, University Hospital Münster, Münster, Germany.

Katarzyna Bozek (K)

Center for Molecular Medicine, Faculty of Medicine and University Hospital Cologne; University of Cologne, Cologne, Germany.

Tim van Beers (T)

Molecular Cell Biology, Institute I of Anatomy, University of Cologne, Cologne, Germany.

Stefan Bittner (S)

Department of Neurology, Focus Program Translational Neuroscience and Immunotherapy, Rhine Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.

Jakob von Engelhardt (J)

Institute for Pathophysiology, Focus Program Translational Neuroscience, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.

Johannes Vogt (J)

Department of Neurology, Focus Program Translational Neuroscience and Immunotherapy, Rhine Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.
Department of Molecular and Translational Neuroscience, Cluster of Excellence-Cellular Stress Response in Aging-Associated Diseases and Center of Molecular Medicine Cologne, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Christina Francisca Vogelaar (CF)

Department of Neurology, Focus Program Translational Neuroscience and Immunotherapy, Rhine Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.

Frauke Zipp (F)

Department of Neurology, Focus Program Translational Neuroscience and Immunotherapy, Rhine Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.

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