A transient blood IL-17 increase triggers neuroinflammation in cerebellum and motor incoordination in hyperammonemic rats

Abstract Patients with liver cirrhosis may show minimal hepatic encephalopathy (MHE) with motor incoordination which is reproduced in hyperammonemic rats. Hyperammonemia induces peripheral inflammation which triggers neuroinflammation and enhanced GABAergic neurotransmission in cerebellum and motor...

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Main Authors: Yaiza M. Arenas, Carmina Montoliu, Marta Llansola, Vicente Felipo
Format: Article
Language:English
Published: BMC 2024-11-01
Series:Journal of Neuroinflammation
Subjects:
Online Access:https://doi.org/10.1186/s12974-024-03310-5
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author Yaiza M. Arenas
Carmina Montoliu
Marta Llansola
Vicente Felipo
author_facet Yaiza M. Arenas
Carmina Montoliu
Marta Llansola
Vicente Felipo
author_sort Yaiza M. Arenas
collection DOAJ
description Abstract Patients with liver cirrhosis may show minimal hepatic encephalopathy (MHE) with motor incoordination which is reproduced in hyperammonemic rats. Hyperammonemia induces peripheral inflammation which triggers neuroinflammation and enhanced GABAergic neurotransmission in cerebellum and motor incoordination. The mechanisms involved remain unknown. The aims were to assess if the early increase of peripheral IL-17 triggers motor incoordination in hyperammonemic rats and to identify some underlying mechanisms. We assessed if blocking peripheral IL-17 with anti-IL-17 at 2–4 days of hyperammonemia prevents motor incoordination and analyzed underlying mechanisms. Hyperammonemia induces a transient blood IL-17 increase at days 3–4. This is associated with increased IL-17 receptor membrane expression and activation in cerebellum, leading to NADPH oxidase activation, increased superoxide production and MLCK that induce blood–brain barrier (BBB) permeabilization by reducing occludin and ZO-1. BBB permeabilization facilitates the entry of IL-17, which increases in cerebellum and activates microglia. This increases TNFα and the TNFR1-S1PR2-CCL2-BDNF-TrkB pathway. This enhances GABAergic neurotransmission which impairs motor coordination. Blocking peripheral IL-17 with anti-IL-17 prevents all the above process and prevents motor incoordination. Early treatment to reduce blood IL-17 may be a useful treatment to reverse motor incoordination in patients with MHE. Graphical abstract
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spelling doaj-art-96f9965d64294101823129b211b43f412025-08-20T02:38:33ZengBMCJournal of Neuroinflammation1742-20942024-11-0121112210.1186/s12974-024-03310-5A transient blood IL-17 increase triggers neuroinflammation in cerebellum and motor incoordination in hyperammonemic ratsYaiza M. Arenas0Carmina Montoliu1Marta Llansola2Vicente Felipo3Laboratory of Neurobiology, Centro de Investigación Príncipe FelipeDepartamento de Patología, Facultad de Medicina, Universidad ValenciaLaboratory of Neurobiology, Centro de Investigación Príncipe FelipeLaboratory of Neurobiology, Centro de Investigación Príncipe FelipeAbstract Patients with liver cirrhosis may show minimal hepatic encephalopathy (MHE) with motor incoordination which is reproduced in hyperammonemic rats. Hyperammonemia induces peripheral inflammation which triggers neuroinflammation and enhanced GABAergic neurotransmission in cerebellum and motor incoordination. The mechanisms involved remain unknown. The aims were to assess if the early increase of peripheral IL-17 triggers motor incoordination in hyperammonemic rats and to identify some underlying mechanisms. We assessed if blocking peripheral IL-17 with anti-IL-17 at 2–4 days of hyperammonemia prevents motor incoordination and analyzed underlying mechanisms. Hyperammonemia induces a transient blood IL-17 increase at days 3–4. This is associated with increased IL-17 receptor membrane expression and activation in cerebellum, leading to NADPH oxidase activation, increased superoxide production and MLCK that induce blood–brain barrier (BBB) permeabilization by reducing occludin and ZO-1. BBB permeabilization facilitates the entry of IL-17, which increases in cerebellum and activates microglia. This increases TNFα and the TNFR1-S1PR2-CCL2-BDNF-TrkB pathway. This enhances GABAergic neurotransmission which impairs motor coordination. Blocking peripheral IL-17 with anti-IL-17 prevents all the above process and prevents motor incoordination. Early treatment to reduce blood IL-17 may be a useful treatment to reverse motor incoordination in patients with MHE. Graphical abstracthttps://doi.org/10.1186/s12974-024-03310-5HyperammonemiaHepatic encephalopathyMotor incoordinationIL-17Blood–brain barrierNeuroinflammation
spellingShingle Yaiza M. Arenas
Carmina Montoliu
Marta Llansola
Vicente Felipo
A transient blood IL-17 increase triggers neuroinflammation in cerebellum and motor incoordination in hyperammonemic rats
Journal of Neuroinflammation
Hyperammonemia
Hepatic encephalopathy
Motor incoordination
IL-17
Blood–brain barrier
Neuroinflammation
title A transient blood IL-17 increase triggers neuroinflammation in cerebellum and motor incoordination in hyperammonemic rats
title_full A transient blood IL-17 increase triggers neuroinflammation in cerebellum and motor incoordination in hyperammonemic rats
title_fullStr A transient blood IL-17 increase triggers neuroinflammation in cerebellum and motor incoordination in hyperammonemic rats
title_full_unstemmed A transient blood IL-17 increase triggers neuroinflammation in cerebellum and motor incoordination in hyperammonemic rats
title_short A transient blood IL-17 increase triggers neuroinflammation in cerebellum and motor incoordination in hyperammonemic rats
title_sort transient blood il 17 increase triggers neuroinflammation in cerebellum and motor incoordination in hyperammonemic rats
topic Hyperammonemia
Hepatic encephalopathy
Motor incoordination
IL-17
Blood–brain barrier
Neuroinflammation
url https://doi.org/10.1186/s12974-024-03310-5
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