Cited by 159Gut microbiota and healthTryptophan and brain disordersMemory and Neural Mechanisms

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Obesity Impairs Short-Term and Working Memory through Gut Microbial Metabolism of Aromatic Amino Acids

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Arnoriaga-Rodríguez, María, Mayneris-Perxachs, Jordi, Burokas, Aurelijus, Contreras-Rodríguez, Oren, Blasco, Gerard, Coll, Clàudia, Biarnés, Carles, Miranda-Olivos, Romina, Latorre, Jèssica, Moreno-Navarrete, José-Maria, Castells-Nobau, Anna, Sabater, Mònica, Palomo-Buitrago, María Encarnación, Puig, Josep, Pedraza, Salvador, Gich, Jordi, Pérez-Brocal, Vicente, Ricart, Wifredo, Moya, Andrés, Fernández-Real, Xavier, Ramió-Torrentà, Lluís, Pamplona, Reinald, Sol, Joaquim, Jové, Mariona, Portero-Otin, Manuel, Maldonado, Rafael, Fernández-Real, José Manuel·2020·Cell Metabolism

DOI 10.1016/j.cmet.2020.09.002

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Abstract

The gut microbiome has been linked to fear extinction learning in animal models. Here, we aimed to explore the gut microbiome and memory domains according to obesity status. A specific microbiome profile associated with short-term memory, working memory, and the volume of the hippocampus and frontal regions of the brain differentially in human subjects with and without obesity. Plasma and fecal levels of aromatic amino acids, their catabolites, and vegetable-derived compounds were longitudinally associated with short-term and working memory. Functionally, microbiota transplantation from human subjects with obesity led to decreased memory scores in mice, aligning this trait from humans with that of recipient mice. RNA sequencing of the medial prefrontal cortex of mice revealed that short-term memory associated with aromatic amino acid pathways, inflammatory genes, and clusters of bacterial species. These results highlight the potential therapeutic value of targeting the gut microbiota for memory impairment, specifically in subjects with obesity.

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Authors: Arnoriaga-Rodríguez, M., Mayneris-Perxachs, J., Burokas, A., Contreras-Rodríguez, O., Blasco, G., Coll, C., Biarnés, C., Miranda-Olivos, R., Latorre, J., Moreno-Navarrete, J.-M., Castells-Nobau, A., Sabater, M., Palomo-Buitrago, M. E., Puig, J., Pedraza, S., Gich, J., Pérez-Brocal, V., Ricart, W., Moya, A., Fernández-Real, X., Ramió-Torrentà, L., Pamplona, R., Sol, J., Jové, M., Portero-Otin, M., Maldonado, R., & Fernández-Real, J. M.
Affiliations: Universitat Pompeu Fabra (ES)
Institut d'Investigació Biomèdica de Girona (ES)
Hospital Universitari de Girona Doctor Josep Trueta (ES)
Parque Sanitario Pere Virgili (ES)
Spanish Biomedical Research Centre in Physiopathology of Obesity and Nutrition (ES)
Universitat de Girona (ES)
École Polytechnique Fédérale de Lausanne (CH)
Universitat de Lleida (ES)
Corresponding author: Maldonado, Rafael
ORCID: Burokas, Aurelijus
Blasco, Gerard
Coll, Clàudia
Biarnés, Carles
Latorre, Jèssica
Sabater, Mònica
Palomo-Buitrago, María Encarnación
Puig, Josep
Pedraza, Salvador
Ricart, Wifredo
Pamplona, Reinald
Jové, Mariona
Maldonado, Rafael
Venue: Cell Metabolism
Publisher: Elsevier BV
Published: 2020-10
Volume: 32
Issue: 4
Pages: 548-560.e7
ISSN: 1550-4131 (ISSN-L)
DOI: 10.1016/j.cmet.2020.09.002
OpenAlex: W3091836995
Cited by: 157
References: 106
Citations by year: 2026: 15 · 2025: 26 · 2024: 26 · 2023: 37 · 2022: 28 · 2021: 22 · 2020: 3
FWCI: 7.30
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 370 d)
Locations: Cell Metabolism (publishedVersion)
PubMed (publishedVersion)
DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
Funders: Department of Health and Social Care (SLT002/16/00250)
European Regional Development Fund (1.2.2-LMT-K-718-02-0014)
Seventh Framework Programme (2013-602891)
Instituto de Salud Carlos III (PI18/01022, PI15/01934, SAF2017-84060-R, SAF2015-65878-R)
Centro de Investigación Biomédica en Red-Fisiopatología de la Obesidad y Nutrición
Institució Catalana de Recerca i Estudis Avançats (RD16/0017/0020, 16/0017/0020)
European Commission
Ministerio de Ciencia, Innovación y Universidades (RTI2018-099200-B-I00)
Lietuvos Mokslo Taryba
Generalitat de Catalunya
Ministerio de Economía y Competitividad (Prometeo/2018/A/133)
European Social Fund (CP18/00009, SLT006/17/00236)
Agència de Gestió d'Ajuts Universitaris i de Recerca (2017-669, SGR2017-669)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords: obesity, gut microbiota, short-term memory, working memory, aromatic amino acids, gut microbiota metabolism, microbiota transplantation, hippocampus, frontal cortex, memory impairment, inflammatory genes, fear extinction learning
MeSH terms: Gastrointestinal Microbiome, Adult, Aged, Animals, Cross-Sectional Studies, Female, Humans, Magnetic Resonance Imaging, Male, Memory, Short-Term, Mice, Inbred C57BL, Middle Aged, Obesity, Case-Control Studies, Amino Acids, Aromatic, Mice, Metabolomics

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Obesity Impairs Short-Term and Working Memory through Gut Microbial Metabolism of Aromatic Amino Acids

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