Reduced epilepsy development in synapsin 2 knockout mice with autistic behavior following early systemic treatment with interleukin-6 receptor antibody.


Journal

Epilepsy research
ISSN: 1872-6844
Titre abrégé: Epilepsy Res
Pays: Netherlands
ID NLM: 8703089

Informations de publication

Date de publication:
03 2023
Historique:
received: 15 12 2022
revised: 09 02 2023
accepted: 23 02 2023
pubmed: 5 3 2023
medline: 15 3 2023
entrez: 4 3 2023
Statut: ppublish

Résumé

Individuals with autism spectrum disorder (ASD) have an increased risk of developing epilepsy. Both ASD and epilepsy have been associated with increased levels of immune factors in the blood, including the proinflammatory cytokine interleukin 6 (IL-6). Mice lacking the synapsin 2 gene (Syn2 KO) exhibit ASD-like behavior and develop epileptic seizures. Their brains display neuroinflammatory changes including elevated IL-6 levels. We aimed to investigate the effect of systemic IL-6 receptor antibody (IL-6R ab) treatment on seizure development and frequency in Syn2 KO mice. Weekly systemic (i.p.) injections of IL-6R ab or saline were given to Syn2 KO mice starting either early in life at 1 month of age, before seizure debut or at 3 months of age, directly after seizure debut and continued for 4 or 2 months, respectively. Seizures were provoked by handling the mice three times per week. The neuroinflammatory response and synaptic protein levels in the brain were determined by ELISA, immunohistochemistry and western blots. In an additional group of Syn2 KO mice, with IL-6R ab treatment early in life, ASD-related behavioral tests including social interaction and repetitive self-grooming, as well as cognitive memory and depressive-/anxiety-like tests, and actigraphy measurements of circadian sleep-awake rhythm were analyzed. The IL-6R ab treatment reduced seizure development and frequency in Syn2 KO mice when initiated before, but not after, seizure debut. However, early treatment did not reverse the neuroinflammatory response or the imbalance in synaptic protein levels in the brain previously reported in Syn2 KO mice. The treatment did not affect social interaction, performance in memory, depressive-/anxiety-like tests or the sleep-awake rhythm of Syn2 KO mice. These findings suggest the involvement of IL-6 receptor signaling during epilepsy development in Syn2 KO mice, without significant alterations of the immune reaction in the brain, and independently of cognitive performance, mood and circadian sleep-awake rhythm.

Sections du résumé

BACKGROUND
Individuals with autism spectrum disorder (ASD) have an increased risk of developing epilepsy. Both ASD and epilepsy have been associated with increased levels of immune factors in the blood, including the proinflammatory cytokine interleukin 6 (IL-6). Mice lacking the synapsin 2 gene (Syn2 KO) exhibit ASD-like behavior and develop epileptic seizures. Their brains display neuroinflammatory changes including elevated IL-6 levels. We aimed to investigate the effect of systemic IL-6 receptor antibody (IL-6R ab) treatment on seizure development and frequency in Syn2 KO mice.
MATERIAL AND METHODS
Weekly systemic (i.p.) injections of IL-6R ab or saline were given to Syn2 KO mice starting either early in life at 1 month of age, before seizure debut or at 3 months of age, directly after seizure debut and continued for 4 or 2 months, respectively. Seizures were provoked by handling the mice three times per week. The neuroinflammatory response and synaptic protein levels in the brain were determined by ELISA, immunohistochemistry and western blots. In an additional group of Syn2 KO mice, with IL-6R ab treatment early in life, ASD-related behavioral tests including social interaction and repetitive self-grooming, as well as cognitive memory and depressive-/anxiety-like tests, and actigraphy measurements of circadian sleep-awake rhythm were analyzed.
RESULTS
The IL-6R ab treatment reduced seizure development and frequency in Syn2 KO mice when initiated before, but not after, seizure debut. However, early treatment did not reverse the neuroinflammatory response or the imbalance in synaptic protein levels in the brain previously reported in Syn2 KO mice. The treatment did not affect social interaction, performance in memory, depressive-/anxiety-like tests or the sleep-awake rhythm of Syn2 KO mice.
CONCLUSION
These findings suggest the involvement of IL-6 receptor signaling during epilepsy development in Syn2 KO mice, without significant alterations of the immune reaction in the brain, and independently of cognitive performance, mood and circadian sleep-awake rhythm.

Identifiants

pubmed: 36870094
pii: S0920-1211(23)00039-6
doi: 10.1016/j.eplepsyres.2023.107114
pii:
doi:

Substances chimiques

Synapsins 0
Interleukin-6 0
Immunoglobulins 0
Receptors, Interleukin-6 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

107114

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors have no competing interest to declare.

Auteurs

Filip Bäckström (F)

Inflammation and Stem Cell Therapy Group, Division of Clinical Neurophysiology, Department of Clinical Sciences, Lund University, Lund, Sweden; Lund Epilepsy Center, Department of Clinical Sciences, Lund University, Lund, Sweden; Translational Neurogenetics Unit, Department of Experimental Medical Science, Lund University, Lund, Sweden.

Matilda Ahl (M)

Inflammation and Stem Cell Therapy Group, Division of Clinical Neurophysiology, Department of Clinical Sciences, Lund University, Lund, Sweden; Lund Epilepsy Center, Department of Clinical Sciences, Lund University, Lund, Sweden.

Jenny Wickham (J)

Inflammation and Stem Cell Therapy Group, Division of Clinical Neurophysiology, Department of Clinical Sciences, Lund University, Lund, Sweden; Lund Epilepsy Center, Department of Clinical Sciences, Lund University, Lund, Sweden.

Christine T Ekdahl (CT)

Inflammation and Stem Cell Therapy Group, Division of Clinical Neurophysiology, Department of Clinical Sciences, Lund University, Lund, Sweden; Lund Epilepsy Center, Department of Clinical Sciences, Lund University, Lund, Sweden. Electronic address: christine.ekdahl_clementson@med.lu.se.

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Classifications MeSH