Gut microbiota modulates expression of genes involved in the astrocyte-neuron lactate shuttle in the hippocampus

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dc.contributor.authorMargineanu, Michael B.
dc.contributor.authorSherwin, Eoin
dc.contributor.authorGolubeva, Anna V.
dc.contributor.authorPeterson, Veronica L.
dc.contributor.authorHoban, Alan E.
dc.contributor.authorFiumelli, Hubert
dc.contributor.authorRea, Kieran
dc.contributor.authorCryan, John F.
dc.contributor.authorMagistretti, Pierre J.
dc.contributor.funderKing Abdullah University of Science and Technologyen
dc.contributor.funderScience Foundation Irelanden
dc.date.accessioned2022-03-31T15:42:48Z
dc.date.available2022-03-31T15:42:48Z
dc.date.issued2020-12
dc.date.updated2022-03-31T15:20:26Z
dc.description.abstractThe gut microbiota modulates brain physiology, development, and behavior and has been implicated as a key regulator in several central nervous system disorders. Its effect on the metabolic coupling between neurons and astrocytes has not been studied to date, even though this is an important component of brain energy metabolism and physiology and it is perturbed in neurodegenerative and cognitive disorders. In this study, we have investigated the mRNA expression of 6 genes encoding proteins implicated in the astrocyte-neuron lactate shuttle (Atp1a2, Ldha, Ldhb, Mct1, Gys1, Pfkfb3), in relation to different gut microbiota manipulations, in the mouse brain hippocampus, a region with critical functions in cognition and behavior. We have discovered that Atp1a2 and Pfkfb3, encoding the ATPase, Na+/K+ transporting, alpha 2 subunit, respectively and 6-phosphofructo-2-kinase/fructose-2,6-biphosphatase 3, two genes predominantly expressed in astrocytes, were upregulated in the hippocampus after microbial colonization of germ-free mice for 24 h, compared with conventionally raised mice. Pfkfb3 was also upregulated in germ-free mice compared with conventionally raised mice, while an increase in Atp1a2 expression in germ-free mice was confirmed only at the protein level by Western blot. In a separate cohort of mice, Atp1a2 and Pfkfb3 mRNA expression was upregulated in the hippocampus following 6-week dietary supplementation with prebiotics (fructoand galactooligosaccharides) in an animal model of chronic psychosocial stress. To our knowledge, these findings are the first to report an influence of the gut microbiota and prebiotics on mRNA expression of genes implicated in the metabolic coupling between neurons and astrocytes. (c) 2020 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)en
dc.description.statusPeer revieweden
dc.description.versionPublished Versionen
dc.format.mimetypeapplication/pdfen
dc.identifier.citationMargineanu, M. B., Sherwin, E., Golubeva, A. V., Peterson, V. L., Hoban, A. E., Fiumelli, H., Rea, K., Cryan, J. F. and Magistretti, P. J. (2020) 'Gut microbiota modulates expression of genes involved in the astrocyte-neuron lactate shuttle in the hippocampus', European Neuropsychopharmacology, 41, pp. 152-159. doi: 10.1016/j.euroneuro.2020.11.006en
dc.identifier.doi10.1016/j.euroneuro.2020.11.006en
dc.identifier.endpage159en
dc.identifier.issn0924-977X
dc.identifier.journaltitleEuropean Neuropsychopharmacologyen
dc.identifier.startpage152en
dc.identifier.urihttps://hdl.handle.net/10468/13024
dc.identifier.volume41en
dc.language.isoenen
dc.publisherElsevier B.V.en
dc.relation.projectinfo:eu-repo/grantAgreement/SFI/SFI Research Centres/12/RC/2273/IE/Alimentary Pharmabiotic Centre (APC) - Interfacing Food & Medicine/en
dc.rights© 2020 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)en
dc.rights.urihttps://creativecommons.org/licenses/by-nc-nd/4.0/en
dc.subjectAerobic glycolysisen
dc.subjectBrainen
dc.subjectMetabolismen
dc.subjectAbsenceen
dc.subjectGut microbiotaen
dc.subjectBrain energy metabolismen
dc.subjectHippocampusen
dc.subjectAstrocyte-neuron lactate shuttleen
dc.titleGut microbiota modulates expression of genes involved in the astrocyte-neuron lactate shuttle in the hippocampusen
dc.typeArticle (peer-reviewed)en
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