Myeloid C/EBPβ deficiency reshapes microglial gene expression and is protective in experimental autoimmune encephalomyelitis

Background CCAAT/enhancer binding protein β (C/EBPβ) is a transcription factor that regulates the expression of important pro-inflammatory genes in microglia. Mice deficient for C/EBPβ show protection against excitotoxic and ischemic CNS damage, but the involvement in this neuroprotective effect of...

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Autores: Pulido Salgado, Marta, Vidal Taboada, José Manuel, García-Díaz Barriga, Gerardo, Serratosa i Serdà, Joan, Valente, Tony, Castillo, Paola, Matalonga, Jonathan, Straccia, Marco, Canals i Coll, Josep M., Valledor Fernández, Annabel, Solà i Subirana, Carme, Saura Martí, Josep
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2017
País:España
Institución:Universidad de Barcelona
Repositorio:Dipòsit Digital de la UB
OAI Identifier:oai:diposit.ub.edu:2445/108976
Acceso en línea:https://hdl.handle.net/2445/108976
Access Level:acceso abierto
Palabra clave:Malalties neurodegeneratives
Encefalomielitis
Genètica mèdica
Inflamació
RNA
Neurodegenerative Diseases
Encephalomyelitis
Medical genetics
Inflammation
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spelling Myeloid C/EBPβ deficiency reshapes microglial gene expression and is protective in experimental autoimmune encephalomyelitisPulido Salgado, MartaVidal Taboada, José ManuelGarcía-Díaz Barriga, GerardoSerratosa i Serdà, JoanValente, TonyCastillo, PaolaMatalonga, JonathanStraccia, MarcoCanals i Coll, Josep M.Valledor Fernández, AnnabelSolà i Subirana, CarmeSaura Martí, JosepMalalties neurodegenerativesEncefalomielitisGenètica mèdicaInflamacióRNANeurodegenerative DiseasesEncephalomyelitisMedical geneticsInflammationRNABackground CCAAT/enhancer binding protein β (C/EBPβ) is a transcription factor that regulates the expression of important pro-inflammatory genes in microglia. Mice deficient for C/EBPβ show protection against excitotoxic and ischemic CNS damage, but the involvement in this neuroprotective effect of the various C/EBPβ-expressing cell types is not solved. Since C/EBPβ-deficient microglia show attenuated neurotoxicity in culture, we hypothesized that specific C/EBPβ deficiency in microglia could be neuroprotective in vivo. In this study, we have tested this hypothesis by generating mice with myeloid C/EBPβ deficiency. Methods Mice with myeloid C/EBPβ deficiency were generated by crossing LysMCre and C/EBPβfl/fl mice. Primary microglial cultures from C/EBPβfl/fl and LysMCre-C/EBPβfl/fl mice were treated with lipopolysaccharide ± interferon γ (IFNγ) for 6 h, and gene expression was analyzed by RNA sequencing. Gene expression and C/EBPβ deletion were analyzed in vivo in microglia isolated from the brains of C/EBPβfl/fl and LysMCre-C/EBPβfl/fl mice treated systemically with lipolysaccharide or vehicle. Mice of LysMCre-C/EBPβfl/fl or control genotypes were subjected to experimental autoimmune encephalitis and analyzed for clinical signs for 52 days. One- or two-way ANOVA or Kruskal-Wallis with their appropriate post hoc tests were used. Results LysMCre-C/EBPβfl/fl mice showed an efficiency of C/EBPβ deletion in microglia of 100 and 90% in vitro and in vivo, respectively. These mice were devoid of female infertility, perinatal mortality and reduced lifespan that are associated to full C/EBPβ deficiency. Transcriptomic analysis of C/EBPβ-deficient primary microglia revealed C/EBPβ-dependent expression of 1068 genes, significantly enriched in inflammatory and innate immune responses GO terms. In vivo, microglial expression of the pro-inflammatory genes Cybb, Ptges, Il23a, Tnf and Csf3 induced by systemic lipopolysaccharide injection was also blunted by C/EBPβ deletion. CNS expression of C/EBPβ was upregulated in experimental autoimmune encephalitis and in multiple sclerosis samples. Finally, LysMCre-C/EBPβfl/fl mice showed robust attenuation of clinical signs in experimental autoimmune encephalitis. Conclusion This study provides new data that support a central role for C/EBPβ in the biology of activated microglia, and it offers proof of concept for the therapeutic potential of microglial C/EBPβ inhibition in multiple sclerosis.BioMed Central2017info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfhttps://hdl.handle.net/2445/108976Articles publicats en revistes (Biomedicina)reponame:Dipòsit Digital de la UBinstname:Universidad de BarcelonaInglésReproducció del document publicat a: https://doi.org/10.1186/s12974-017-0834-5Journal of Neuroinflammation, 2017, vol. 14, num. 54https://doi.org/10.1186/s12974-017-0834-5cc-by (c) Pulido Salgado et al., 2017http://creativecommons.org/licenses/by/3.0/esinfo:eu-repo/semantics/openAccessoai:diposit.ub.edu:2445/1089762026-05-27T06:46:51Z
dc.title.none.fl_str_mv Myeloid C/EBPβ deficiency reshapes microglial gene expression and is protective in experimental autoimmune encephalomyelitis
title Myeloid C/EBPβ deficiency reshapes microglial gene expression and is protective in experimental autoimmune encephalomyelitis
spellingShingle Myeloid C/EBPβ deficiency reshapes microglial gene expression and is protective in experimental autoimmune encephalomyelitis
Pulido Salgado, Marta
Malalties neurodegeneratives
Encefalomielitis
Genètica mèdica
Inflamació
RNA
Neurodegenerative Diseases
Encephalomyelitis
Medical genetics
Inflammation
RNA
title_short Myeloid C/EBPβ deficiency reshapes microglial gene expression and is protective in experimental autoimmune encephalomyelitis
title_full Myeloid C/EBPβ deficiency reshapes microglial gene expression and is protective in experimental autoimmune encephalomyelitis
title_fullStr Myeloid C/EBPβ deficiency reshapes microglial gene expression and is protective in experimental autoimmune encephalomyelitis
title_full_unstemmed Myeloid C/EBPβ deficiency reshapes microglial gene expression and is protective in experimental autoimmune encephalomyelitis
title_sort Myeloid C/EBPβ deficiency reshapes microglial gene expression and is protective in experimental autoimmune encephalomyelitis
dc.creator.none.fl_str_mv Pulido Salgado, Marta
Vidal Taboada, José Manuel
García-Díaz Barriga, Gerardo
Serratosa i Serdà, Joan
Valente, Tony
Castillo, Paola
Matalonga, Jonathan
Straccia, Marco
Canals i Coll, Josep M.
Valledor Fernández, Annabel
Solà i Subirana, Carme
Saura Martí, Josep
author Pulido Salgado, Marta
author_facet Pulido Salgado, Marta
Vidal Taboada, José Manuel
García-Díaz Barriga, Gerardo
Serratosa i Serdà, Joan
Valente, Tony
Castillo, Paola
Matalonga, Jonathan
Straccia, Marco
Canals i Coll, Josep M.
Valledor Fernández, Annabel
Solà i Subirana, Carme
Saura Martí, Josep
author_role author
author2 Vidal Taboada, José Manuel
García-Díaz Barriga, Gerardo
Serratosa i Serdà, Joan
Valente, Tony
Castillo, Paola
Matalonga, Jonathan
Straccia, Marco
Canals i Coll, Josep M.
Valledor Fernández, Annabel
Solà i Subirana, Carme
Saura Martí, Josep
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Malalties neurodegeneratives
Encefalomielitis
Genètica mèdica
Inflamació
RNA
Neurodegenerative Diseases
Encephalomyelitis
Medical genetics
Inflammation
RNA
topic Malalties neurodegeneratives
Encefalomielitis
Genètica mèdica
Inflamació
RNA
Neurodegenerative Diseases
Encephalomyelitis
Medical genetics
Inflammation
RNA
description Background CCAAT/enhancer binding protein β (C/EBPβ) is a transcription factor that regulates the expression of important pro-inflammatory genes in microglia. Mice deficient for C/EBPβ show protection against excitotoxic and ischemic CNS damage, but the involvement in this neuroprotective effect of the various C/EBPβ-expressing cell types is not solved. Since C/EBPβ-deficient microglia show attenuated neurotoxicity in culture, we hypothesized that specific C/EBPβ deficiency in microglia could be neuroprotective in vivo. In this study, we have tested this hypothesis by generating mice with myeloid C/EBPβ deficiency. Methods Mice with myeloid C/EBPβ deficiency were generated by crossing LysMCre and C/EBPβfl/fl mice. Primary microglial cultures from C/EBPβfl/fl and LysMCre-C/EBPβfl/fl mice were treated with lipopolysaccharide ± interferon γ (IFNγ) for 6 h, and gene expression was analyzed by RNA sequencing. Gene expression and C/EBPβ deletion were analyzed in vivo in microglia isolated from the brains of C/EBPβfl/fl and LysMCre-C/EBPβfl/fl mice treated systemically with lipolysaccharide or vehicle. Mice of LysMCre-C/EBPβfl/fl or control genotypes were subjected to experimental autoimmune encephalitis and analyzed for clinical signs for 52 days. One- or two-way ANOVA or Kruskal-Wallis with their appropriate post hoc tests were used. Results LysMCre-C/EBPβfl/fl mice showed an efficiency of C/EBPβ deletion in microglia of 100 and 90% in vitro and in vivo, respectively. These mice were devoid of female infertility, perinatal mortality and reduced lifespan that are associated to full C/EBPβ deficiency. Transcriptomic analysis of C/EBPβ-deficient primary microglia revealed C/EBPβ-dependent expression of 1068 genes, significantly enriched in inflammatory and innate immune responses GO terms. In vivo, microglial expression of the pro-inflammatory genes Cybb, Ptges, Il23a, Tnf and Csf3 induced by systemic lipopolysaccharide injection was also blunted by C/EBPβ deletion. CNS expression of C/EBPβ was upregulated in experimental autoimmune encephalitis and in multiple sclerosis samples. Finally, LysMCre-C/EBPβfl/fl mice showed robust attenuation of clinical signs in experimental autoimmune encephalitis. Conclusion This study provides new data that support a central role for C/EBPβ in the biology of activated microglia, and it offers proof of concept for the therapeutic potential of microglial C/EBPβ inhibition in multiple sclerosis.
publishDate 2017
dc.date.none.fl_str_mv 2017
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/2445/108976
url https://hdl.handle.net/2445/108976
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Reproducció del document publicat a: https://doi.org/10.1186/s12974-017-0834-5
Journal of Neuroinflammation, 2017, vol. 14, num. 54
https://doi.org/10.1186/s12974-017-0834-5
dc.rights.none.fl_str_mv cc-by (c) Pulido Salgado et al., 2017
http://creativecommons.org/licenses/by/3.0/es
info:eu-repo/semantics/openAccess
rights_invalid_str_mv cc-by (c) Pulido Salgado et al., 2017
http://creativecommons.org/licenses/by/3.0/es
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv BioMed Central
publisher.none.fl_str_mv BioMed Central
dc.source.none.fl_str_mv Articles publicats en revistes (Biomedicina)
reponame:Dipòsit Digital de la UB
instname:Universidad de Barcelona
instname_str Universidad de Barcelona
reponame_str Dipòsit Digital de la UB
collection Dipòsit Digital de la UB
repository.name.fl_str_mv
repository.mail.fl_str_mv
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