Hypoxia compromises the mitochondrial metabolism of Alzheimer’s disease microglia via HIF1

Genetic Alzheimer’s disease (AD) risk factors associate with reduced defensive amyloid β plaque-associated microglia (AβAM), but the contribution of modifiable AD risk factors to microglial dysfunction is unknown. In AD mouse models, we observe concomitant activation of the hypoxia-inducible factor...

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Autores: March Díaz, Rosana, Lara-Ureña, Nieves, Romero-Molina, Carmen, Heras-Garvin, Antonio, Ortega de San Luis, Clara, Álvarez-Vergara, María I., Sánchez García, Manuel A., Sánchez-Mejias, Elisabeth, Dávila, José C., Rosales-Nieves, Alicia E., Forja, Cristina, Navarro-Garrido, Victoria, Gómez-Arboledas, Ángela, Sánchez-Mico, María V., Viehweger, Adrian, Gerpe, Almudena, Hodson, Emma J., Vizuete, Marisa, Bishop, Tammie, Serrano-Pozo, Alberto, López-Barneo, José, Berra, Edurne, Vitorica, Javier, Pascual Bravo, Alberto
Formato: artículo
Estado:Versión aceptada para publicación
Fecha de publicación:2021
País:España
Recursos:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/260192
Acesso em linha:http://hdl.handle.net/10261/260192
Access Level:acceso abierto
Palavra-chave:Hypoxia
Alzheimer’s disease
Microglia
HIF1
Aerobic respiration
Anaerobic glycolysis
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network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv Hypoxia compromises the mitochondrial metabolism of Alzheimer’s disease microglia via HIF1
title Hypoxia compromises the mitochondrial metabolism of Alzheimer’s disease microglia via HIF1
spellingShingle Hypoxia compromises the mitochondrial metabolism of Alzheimer’s disease microglia via HIF1
March Díaz, Rosana
Hypoxia
Alzheimer’s disease
Microglia
HIF1
Aerobic respiration
Anaerobic glycolysis
title_short Hypoxia compromises the mitochondrial metabolism of Alzheimer’s disease microglia via HIF1
title_full Hypoxia compromises the mitochondrial metabolism of Alzheimer’s disease microglia via HIF1
title_fullStr Hypoxia compromises the mitochondrial metabolism of Alzheimer’s disease microglia via HIF1
title_full_unstemmed Hypoxia compromises the mitochondrial metabolism of Alzheimer’s disease microglia via HIF1
title_sort Hypoxia compromises the mitochondrial metabolism of Alzheimer’s disease microglia via HIF1
dc.creator.none.fl_str_mv March Díaz, Rosana
Lara-Ureña, Nieves
Romero-Molina, Carmen
Heras-Garvin, Antonio
Ortega de San Luis, Clara
Álvarez-Vergara, María I.
Sánchez García, Manuel A.
Sánchez-Mejias, Elisabeth
Dávila, José C.
Rosales-Nieves, Alicia E.
Forja, Cristina
Navarro-Garrido, Victoria
Gómez-Arboledas, Ángela
Sánchez-Mico, María V.
Viehweger, Adrian
Gerpe, Almudena
Hodson, Emma J.
Vizuete, Marisa
Bishop, Tammie
Serrano-Pozo, Alberto
López-Barneo, José
Berra, Edurne
Vitorica, Javier
Pascual Bravo, Alberto
author March Díaz, Rosana
author_facet March Díaz, Rosana
Lara-Ureña, Nieves
Romero-Molina, Carmen
Heras-Garvin, Antonio
Ortega de San Luis, Clara
Álvarez-Vergara, María I.
Sánchez García, Manuel A.
Sánchez-Mejias, Elisabeth
Dávila, José C.
Rosales-Nieves, Alicia E.
Forja, Cristina
Navarro-Garrido, Victoria
Gómez-Arboledas, Ángela
Sánchez-Mico, María V.
Viehweger, Adrian
Gerpe, Almudena
Hodson, Emma J.
Vizuete, Marisa
Bishop, Tammie
Serrano-Pozo, Alberto
López-Barneo, José
Berra, Edurne
Vitorica, Javier
Pascual Bravo, Alberto
author_role author
author2 Lara-Ureña, Nieves
Romero-Molina, Carmen
Heras-Garvin, Antonio
Ortega de San Luis, Clara
Álvarez-Vergara, María I.
Sánchez García, Manuel A.
Sánchez-Mejias, Elisabeth
Dávila, José C.
Rosales-Nieves, Alicia E.
Forja, Cristina
Navarro-Garrido, Victoria
Gómez-Arboledas, Ángela
Sánchez-Mico, María V.
Viehweger, Adrian
Gerpe, Almudena
Hodson, Emma J.
Vizuete, Marisa
Bishop, Tammie
Serrano-Pozo, Alberto
López-Barneo, José
Berra, Edurne
Vitorica, Javier
Pascual Bravo, Alberto
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Instituto de Salud Carlos III
Ministerio de Educación, Cultura y Deporte (España)
Ministerio de Economía, Industria y Competitividad (España)
European Commission
Junta de Andalucía
Fundación Domingo Martínez
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Hypoxia
Alzheimer’s disease
Microglia
HIF1
Aerobic respiration
Anaerobic glycolysis
topic Hypoxia
Alzheimer’s disease
Microglia
HIF1
Aerobic respiration
Anaerobic glycolysis
description Genetic Alzheimer’s disease (AD) risk factors associate with reduced defensive amyloid β plaque-associated microglia (AβAM), but the contribution of modifiable AD risk factors to microglial dysfunction is unknown. In AD mouse models, we observe concomitant activation of the hypoxia-inducible factor 1 (HIF1) pathway and transcription of mitochondrial-related genes in AβAM, and elongation of mitochondria, a cellular response to maintain aerobic respiration under low nutrient and oxygen conditions. Overactivation of HIF1 induces microglial quiescence in cellulo, with lower mitochondrial respiration and proliferation. In vivo, overstabilization of HIF1, either genetically or by exposure to systemic hypoxia, reduces AβAM clustering and proliferation and increases Aβ neuropathology. In the human AD hippocampus, upregulation of HIF1α and HIF1 target genes correlates with reduced Aβ plaque microglial coverage and an increase of Aβ plaque-associated neuropathology. Thus, hypoxia (a modifiable AD risk factor) hijacks microglial mitochondrial metabolism and converges with genetic susceptibility to cause AD microglial dysfunction.
publishDate 2021
dc.date.none.fl_str_mv 2021
2022
2022
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_816b
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dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/260192
url http://hdl.handle.net/10261/260192
dc.language.none.fl_str_mv Inglés
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https://doi.org/10.1038/s43587-021-00054-2

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spelling Hypoxia compromises the mitochondrial metabolism of Alzheimer’s disease microglia via HIF1March Díaz, RosanaLara-Ureña, NievesRomero-Molina, CarmenHeras-Garvin, AntonioOrtega de San Luis, ClaraÁlvarez-Vergara, María I.Sánchez García, Manuel A.Sánchez-Mejias, ElisabethDávila, José C.Rosales-Nieves, Alicia E.Forja, CristinaNavarro-Garrido, VictoriaGómez-Arboledas, ÁngelaSánchez-Mico, María V.Viehweger, AdrianGerpe, AlmudenaHodson, Emma J.Vizuete, MarisaBishop, TammieSerrano-Pozo, AlbertoLópez-Barneo, JoséBerra, EdurneVitorica, JavierPascual Bravo, AlbertoHypoxiaAlzheimer’s diseaseMicrogliaHIF1Aerobic respirationAnaerobic glycolysisGenetic Alzheimer’s disease (AD) risk factors associate with reduced defensive amyloid β plaque-associated microglia (AβAM), but the contribution of modifiable AD risk factors to microglial dysfunction is unknown. In AD mouse models, we observe concomitant activation of the hypoxia-inducible factor 1 (HIF1) pathway and transcription of mitochondrial-related genes in AβAM, and elongation of mitochondria, a cellular response to maintain aerobic respiration under low nutrient and oxygen conditions. Overactivation of HIF1 induces microglial quiescence in cellulo, with lower mitochondrial respiration and proliferation. In vivo, overstabilization of HIF1, either genetically or by exposure to systemic hypoxia, reduces AβAM clustering and proliferation and increases Aβ neuropathology. In the human AD hippocampus, upregulation of HIF1α and HIF1 target genes correlates with reduced Aβ plaque microglial coverage and an increase of Aβ plaque-associated neuropathology. Thus, hypoxia (a modifiable AD risk factor) hijacks microglial mitochondrial metabolism and converges with genetic susceptibility to cause AD microglial dysfunction.R.M.-D. was the recipient of a Sara Borrell fellowship from Instituto de Salud Carlos III (ISCIII) (CD09/0007). N.L.-U., C.O.-d.S.L., C.R.-M. and M.I.A.-V. were the recipients of FPU fellowships from Spanish Ministry of Education, Culture and Sport (FPU14/02115, AP2010‐1598, FPU16/02050 and FPU15/02898, respectively). A.H.-G. was the recipient of an FPI fellowship from the Spanish Ministry of Education, Culture and Sport (BES-2010-033886). This work was supported by grants from the Spanish MINEICO, ISCIII and FEDER (European Union) (SAF2012‐33816, SAF2015‐64111‐R, SAF2017-90794-REDT and PIE13/0004 to A.P.); by the Regional Government of Andalusia co-funded by CEC and FEDER funds (European Union) (‘Proyectos de Excelencia’; P12‐CTS‐2138 and P12‐CTS‐2232 to A.P.); by the ‘Ayuda de Biomedicina 2018’, Fundación Domingo Martínez (to A.P.) ; by the ISCIII of Spain, co-financed by FEDER funds (European Union) through grants PI18/01556 (to J.V.) and PI18/01557 (to A. Gutierrez); by Junta de Andalucía, co-financed by FEDER funds (grants UMA18-FEDERJA-211 (to A. Gutierrez) and US‐1262734 (to J.V.)); and by Spanish MINEICO (BFU2016-76872-R and BES-2011-047721 to E.B.).Peer reviewedSpringer NatureInstituto de Salud Carlos IIIMinisterio de Educación, Cultura y Deporte (España)Ministerio de Economía, Industria y Competitividad (España)European CommissionJunta de AndalucíaFundación Domingo MartínezConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202220222021info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_816bPostprintinfo:eu-repo/semantics/acceptedVersioninfo:eu-repo/semantics/preprintapplication/pdfhttp://hdl.handle.net/10261/260192reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/MECD//FPU14%2F02115info:eu-repo/grantAgreement/MECD//AP2010‐1598info:eu-repo/grantAgreement/MECD//FPU16%2F02050info:eu-repo/grantAgreement/MECD//FPU15%2F02898info:eu-repo/grantAgreement/MINECO//SAF2012‐33816info:eu-repo/grantAgreement/MINECO//SAF2015‐64111‐Rinfo:eu-repo/grantAgreement/MINECO//SAF2017-90794-REDTinfo:eu-repo/grantAgreement/MINECO//BFU2016-76872-Rinfo:eu-repo/grantAgreement/MICINN//BES-2011-047721info:eu-repo/grantAgreement/MICINN//BES-2010-033886https://doi.org/10.1038/s43587-021-00054-2Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2601922026-05-22T06:33:51Z
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