Ketotifen is a microglial stabilizer by inhibiting secretory vesicle acidification

Aims: Microglia survey the brain environment by sensing alarm signals to provide the first line of defense against injury or infection after which they acquire an activated phenotype, but they also respond to chemical signals sent from brain mast cells, sentinels of the immune system, when these are...

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Autores: Ramírez-Ponce, M. Pilar, Flores Cordero, Juan Antonio, Barrella, Lorenzo, Alés González de la Higuera, Eva María
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Institución:Universidad de Sevilla (US)
Repositorio:idUS. Depósito de Investigación de la Universidad de Sevilla
OAI Identifier:oai:idus.us.es:11441/149455
Acceso en línea:https://hdl.handle.net/11441/149455
https://doi.org/10.1016/j.lfs.2023.121537
Access Level:acceso abierto
Palabra clave:Microglia
Acidification
Calcium signaling
Exocytosis
Ketotifen
Secretory vesicles
Neuroinflammation
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spelling Ketotifen is a microglial stabilizer by inhibiting secretory vesicle acidificationRamírez-Ponce, M. PilarFlores Cordero, Juan AntonioBarrella, LorenzoAlés González de la Higuera, Eva MaríaMicrogliaAcidificationCalcium signalingExocytosisKetotifenSecretory vesiclesNeuroinflammationAims: Microglia survey the brain environment by sensing alarm signals to provide the first line of defense against injury or infection after which they acquire an activated phenotype, but they also respond to chemical signals sent from brain mast cells, sentinels of the immune system, when these are degranulated in response to noxious agents. Nevertheless, excessive microglia activation damages the surrounding healthy neural tissue causing progressive loss of neurons and inducing chronic inflammation. Thus, it would be of intense interest the development and application of agents which prevent mast cell mediator release and inhibit the actions of such mediators once released on microglia. Main methods: Fluorescence measurements of fura-2 and quinacrine were used to measure intracellular Ca2+ signaling and exocytotic vesicle fusion in resting and activated microglia. Key findings: We show that treatment of microglia with a cocktail of mast cell mediators induces microglia activation, phagocytosis, and exocytosis, and reveal by the first-time microglia undergo a phase of vesicular acidification just before the exocytotic fusion occurs. This acidification is an important process for vesicular maturation and contributes with ~25 % to the content that the vesicle can store and later release by exocytosis. Pre-incubation with ketotifen, a mast cell stabilizer and H1R antagonist completely abolished histaminemediated calcium signaling and acidification of microglial organelles, and concomitantly reduced the discharge of vesicle contents. Significance: These results highlight a key role for vesicle acidification in microglial physiology and provide a potential therapeutic target for diseases related to mast cell and microglia-mediated neuroinflammation.ElsevierFisiología Médica y BiofísicaBioquímica Médica y Biología Molecular e InmunologíaJunta de Andalucía2023info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttps://hdl.handle.net/11441/149455https://doi.org/10.1016/j.lfs.2023.121537reponame:idUS. Depósito de Investigación de la Universidad de Sevillainstname:Universidad de Sevilla (US)InglésLIFE SCIENCES, 319.BIO-236https://www.sciencedirect.com/science/article/pii/S0024320523001716?via%3Dihubinfo:eu-repo/semantics/openAccessoai:idus.us.es:11441/1494552026-06-17T12:51:07Z
dc.title.none.fl_str_mv Ketotifen is a microglial stabilizer by inhibiting secretory vesicle acidification
title Ketotifen is a microglial stabilizer by inhibiting secretory vesicle acidification
spellingShingle Ketotifen is a microglial stabilizer by inhibiting secretory vesicle acidification
Ramírez-Ponce, M. Pilar
Microglia
Acidification
Calcium signaling
Exocytosis
Ketotifen
Secretory vesicles
Neuroinflammation
title_short Ketotifen is a microglial stabilizer by inhibiting secretory vesicle acidification
title_full Ketotifen is a microglial stabilizer by inhibiting secretory vesicle acidification
title_fullStr Ketotifen is a microglial stabilizer by inhibiting secretory vesicle acidification
title_full_unstemmed Ketotifen is a microglial stabilizer by inhibiting secretory vesicle acidification
title_sort Ketotifen is a microglial stabilizer by inhibiting secretory vesicle acidification
dc.creator.none.fl_str_mv Ramírez-Ponce, M. Pilar
Flores Cordero, Juan Antonio
Barrella, Lorenzo
Alés González de la Higuera, Eva María
author Ramírez-Ponce, M. Pilar
author_facet Ramírez-Ponce, M. Pilar
Flores Cordero, Juan Antonio
Barrella, Lorenzo
Alés González de la Higuera, Eva María
author_role author
author2 Flores Cordero, Juan Antonio
Barrella, Lorenzo
Alés González de la Higuera, Eva María
author2_role author
author
author
dc.contributor.none.fl_str_mv Fisiología Médica y Biofísica
Bioquímica Médica y Biología Molecular e Inmunología
Junta de Andalucía
dc.subject.none.fl_str_mv Microglia
Acidification
Calcium signaling
Exocytosis
Ketotifen
Secretory vesicles
Neuroinflammation
topic Microglia
Acidification
Calcium signaling
Exocytosis
Ketotifen
Secretory vesicles
Neuroinflammation
description Aims: Microglia survey the brain environment by sensing alarm signals to provide the first line of defense against injury or infection after which they acquire an activated phenotype, but they also respond to chemical signals sent from brain mast cells, sentinels of the immune system, when these are degranulated in response to noxious agents. Nevertheless, excessive microglia activation damages the surrounding healthy neural tissue causing progressive loss of neurons and inducing chronic inflammation. Thus, it would be of intense interest the development and application of agents which prevent mast cell mediator release and inhibit the actions of such mediators once released on microglia. Main methods: Fluorescence measurements of fura-2 and quinacrine were used to measure intracellular Ca2+ signaling and exocytotic vesicle fusion in resting and activated microglia. Key findings: We show that treatment of microglia with a cocktail of mast cell mediators induces microglia activation, phagocytosis, and exocytosis, and reveal by the first-time microglia undergo a phase of vesicular acidification just before the exocytotic fusion occurs. This acidification is an important process for vesicular maturation and contributes with ~25 % to the content that the vesicle can store and later release by exocytosis. Pre-incubation with ketotifen, a mast cell stabilizer and H1R antagonist completely abolished histaminemediated calcium signaling and acidification of microglial organelles, and concomitantly reduced the discharge of vesicle contents. Significance: These results highlight a key role for vesicle acidification in microglial physiology and provide a potential therapeutic target for diseases related to mast cell and microglia-mediated neuroinflammation.
publishDate 2023
dc.date.none.fl_str_mv 2023
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://hdl.handle.net/11441/149455
https://doi.org/10.1016/j.lfs.2023.121537
url https://hdl.handle.net/11441/149455
https://doi.org/10.1016/j.lfs.2023.121537
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv LIFE SCIENCES, 319.
BIO-236
https://www.sciencedirect.com/science/article/pii/S0024320523001716?via%3Dihub
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:idUS. Depósito de Investigación de la Universidad de Sevilla
instname:Universidad de Sevilla (US)
instname_str Universidad de Sevilla (US)
reponame_str idUS. Depósito de Investigación de la Universidad de Sevilla
collection idUS. Depósito de Investigación de la Universidad de Sevilla
repository.name.fl_str_mv
repository.mail.fl_str_mv
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