Microbiota-derived metabolites as drivers of gut–brain communication

Ahmed, Hany; Leyrolle, Quentin; Koistinen, Ville; Kärkkäinen, Olli; Layé, Sophie; Delzenne, Nathalie; Hanhineva, Kati

doi:10.1080/19490976.2022.2102878

Cited by 462Gut microbiota and healthTryptophan and brain disordersGastrointestinal motility and disorders

Microbiota-derived metabolites as drivers of gut–brain communication

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Ahmed, Hany, Leyrolle, Quentin, Koistinen, Ville, Kärkkäinen, Olli, Layé, Sophie, Delzenne, Nathalie, Hanhineva, Kati·2022·Gut Microbes

DOI 10.1080/19490976.2022.2102878PMC PMC9341364

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Abstract

Alterations in the gut microbiota composition have been associated with a range of neurodevelopmental, neurodegenerative, and neuropsychiatric disorders. The gut microbes transform and metabolize dietary- and host-derived molecules generating a diverse group of metabolites with local and systemic effects. The bi-directional communication between brain and the microbes residing in the gut, the so-called gut–brain axis, consists of a network of immunological, neuronal, and endocrine signaling pathways. Although the full variety of mechanisms of the gut–brain crosstalk is yet to be established, the existing data demonstrates that a single metabolite or its derivatives are likely among the key inductors within the gut–brain axis communication. However, more research is needed to understand the molecular mechanisms underlying how gut microbiota associated metabolites alter brain functions, and to examine if different interventional approaches targeting the gut microbiota could be used in prevention and treatment of neurological disorders, as reviewed herein.Abbreviations:4-EPS 4-ethylphenylsulfate; 5-AVA(B) 5-aminovaleric acid (betaine); Aβ Amyloid beta protein; AhR Aryl hydrocarbon receptor; ASD Autism spectrum disorder; BBB Blood–brain barrier; BDNF Brain-derived neurotrophic factor; CNS Central nervous system; GABA ɣ-aminobutyric acid; GF Germ-free; MIA Maternal immune activation; SCFA Short-chain fatty acid; 3M-4-TMAB 3-methyl-4-(trimethylammonio)butanoate; 4-TMAP 4-(trimethylammonio)pentanoate; TMA(O) Trimethylamine(-N-oxide); TUDCA Tauroursodeoxycholic acid; ZO Zonula occludens proteins

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There is bidirectional communication between the gut microbiome and the central nervous system, referred to as the 'microbiota-gut-brain axis'.
“Evidence has unveiled the bidirectional communication between the gut microbiome and the central nervous system, referred to as the “microbiota–gut–brain axis”.”
From Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases (2024) · cites this paper as [30]

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The Meningeal Lymphatic System: A New Player in Neurophysiology
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Microbiota-derived acetate enables the metabolic fitness of the brain innate immune system during health and disease
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PYY modulation of cortical and hypothalamic brain areas predicts feeding behaviour in humans
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The gut microbiota-derived metabolite trimethylamine N-oxide is elevated in Alzheimer’s disease
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Microbiota modulate sympathetic neurons via a gut–brain circuit
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A reference map of potential determinants for the human serum metabolome
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In Vivo Evidence for Lactate as a Neuronal Energy Source
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Gut Microbiota-Produced Tryptamine Activates an Epithelial G-Protein-Coupled Receptor to Increase Colonic Secretion
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The microbiota regulate neuronal function and fear extinction learning
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Potent Neuroprotective Properties against the Alzheimer β-Amyloid by an Endogenous Melatonin-related Indole Structure, Indole-3-propionic Acid
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The impact of short-chain fatty acids on GLP-1 and PYY secretion from the isolated perfused rat colon
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Efficacy of omega-3 PUFAs in depression: A meta-analysis
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Gut microbial products regulate murine gastrointestinal motility via Toll-like receptor 4 signaling
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Differences in fecal microbial metabolites and microbiota of children with autism spectrum disorders
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Effects of the enteric bacterial metabolic product propionic acid on object-directed behavior, social behavior, cognition, and neuroinflammation in adolescent rats: Relevance to autism spectrum disorder
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Autism-related dietary preferences mediate autism-gut microbiome associations
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Maternal Fecal Microbiota Transplantation in Cesarean-Born Infants Rapidly Restores Normal Gut Microbial Development: A Proof-of-Concept Study
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Lactate Receptor Sites Link Neurotransmission, Neurovascular Coupling, and Brain Energy Metabolism
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Microbiota-derived short chain fatty acids modulate microglia and promote Aβ plaque deposition
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Colonic bacterial metabolites and human health
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Altered bile acid profile in mild cognitive impairment and Alzheimer's disease: Relationship to neuroimaging and CSF biomarkers
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Short-Chain Fatty Acids and Lipopolysaccharide as Mediators Between Gut Dysbiosis and Amyloid Pathology in Alzheimer’s Disease
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A Forward Chemical Genetic Screen Reveals Gut Microbiota Metabolites That Modulate Host Physiology
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Systematic assessment of secondary bile acid metabolism in gut microbes reveals distinct metabolic capabilities in inflammatory bowel disease
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Impact of intestinal microbiota on intestinal luminal metabolome
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Enteroendocrine cells sense bacterial tryptophan catabolites to activate enteric and vagal neuronal pathways
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Microbiota-driven transcriptional changes in prefrontal cortex override genetic differences in social behavior
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Ergothioneine – a diet‐derived antioxidant with therapeutic potential
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High-fiber diet mitigates maternal obesity-induced cognitive and social dysfunction in the offspring via gut-brain axis
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Short-chain fatty acids, prebiotics, synbiotics, and systemic inflammation: a systematic review and meta-analysis
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Bile acid signaling pathways from the enterohepatic circulation to the central nervous system
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Magnetic resonance spectroscopy reveals oral Lactobacillus promotion of increases in brain GABA, N-acetyl aspartate and glutamate
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Epigenetic modulation of inflammation and synaptic plasticity promotes resilience against stress in mice
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Background
Metabolic Signatures of Extreme Longevity in Northern Italian Centenarians Reveal a Complex Remodeling of Lipids, Amino Acids, and Gut Microbiota Metabolism
Collino, S., Montoliu, I., Martin, F.-P. J., Scherer, M., Mari, D., Salvioli, S., Bucci, L., Ostan, R., Monti, D., Biagi, E., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056564 · Cited by 270 · see citing works
Indole, a signaling molecule produced by the gut microbiota, negatively impacts emotional behaviors in rats
Jaglin, M., Rhimi, M., Philippe, C., Pons, N., Bruneau, A., Goustard, B., Daugé, V., Maguin, E., Naudon, L., & Rabot, S. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00216 · Cited by 269 · see citing works
Expression of the short chain fatty acid receptor GPR41/FFAR3 in autonomic and somatic sensory ganglia
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Bile acids permeabilize the blood brain barrier after bile duct ligation in rats via Rac1-dependent mechanisms
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The microbiota-gut-brain axis participates in chronic cerebral hypoperfusion by disrupting the metabolism of short-chain fatty acids
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Plasma and Fecal Metabolite Profiles in Autism Spectrum Disorder
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Gut microbiota drives age-related oxidative stress and mitochondrial damage in microglia via the metabolite N6-carboxymethyllysine
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Reduction of Endogenous Kynurenic Acid Formation Enhances Extracellular Glutamate, Hippocampal Plasticity, and Cognitive Behavior
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An integrated meta-analysis of peripheral blood metabolites and biological functions in major depressive disorder
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Role of intestinal microbiota in the generation of polyphenol‐derived phenolic acid mediated attenuation of Alzheimer's disease β‐amyloid oligomerization
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Cerebral low-molecular metabolites influenced by intestinal microbiota: a pilot study
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Butyrate enhances mitochondrial function during oxidative stress in cell lines from boys with autism
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Elevations of Endogenous Kynurenic Acid Produce Spatial Working Memory Deficits
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Regulation of blood–brain barrier integrity by microbiome-associated methylamines and cognition by trimethylamine N-oxide
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Intracerebroventricular injection of propionic acid, an enteric bacterial metabolic end-product, impairs social behavior in the rat: implications for an animal model of autism
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Tryptophan-metabolizing gut microbes regulate adult neurogenesis via the aryl hydrocarbon receptor
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Metabolic Network Analysis Reveals Altered Bile Acid Synthesis and Metabolism in Alzheimer’s Disease
Baloni, P., Funk, C. C., Yan, J., Yurkovich, J. T., Kueider-Paisley, A., Nho, K., Heinken, A., Jia, W., Mahmoudiandehkordi, S., Louie, G., et al. (2020) · Cell Reports Medicine · doi:10.1016/j.xcrm.2020.100138 · Cited by 211 · see citing works
Etiology of autistic features: the persisting neurotoxic effects of propionic acid
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The gut microbiota metabolite indole alleviates liver inflammation in mice
Beaumont, M., Neyrinck, A. M., Olivares, M., Rodriguez, J., Nédélec, A., Roumain, M., Bindels, L. B., Cani, P. D., Evenepoel, P., Muccioli, G. G., et al. (2018) · The FASEB Journal · doi:10.1096/fj.201800544 · Cited by 208 · see citing works
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Microbe-host interactions: influence of the gut microbiota on the enteric nervous system
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Lactobacillus plantarum DR7 alleviates stress and anxiety in adults: a randomised, double-blind, placebo-controlled study
Chong, H.-X., Yusoff, N., Hor, Y.-Y., Lew, L.-C., Jaafar, M. H., Choi, S. B., Yusoff, M. S. B., Wahid, N. A., Abdullah, M. F. I. L. B., Zakaria, N., et al. (2019) · Beneficial Microbes · doi:10.3920/bm2018.0135 · Cited by 207 · see citing works
The gut microbiome–derived metabolite trimethylamine N-oxide modulates neuroinflammation and cognitive function with aging
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TUDCA, a Bile Acid, Attenuates Amyloid Precursor Protein Processing and Amyloid-β Deposition in APP/PS1 Mice
Nunes, A. F., Amaral, J. D., Lo, A. C., Fonseca, M. B., Viana, R. J. S., Callaerts-Vegh, Z., D’Hooge, R., & Rodrigues, C. M. P. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8256-y · Cited by 192 · see citing works
Depression, Serotonin and Tryptophan
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Antiglycative and neuroprotective activity of colon‐derived polyphenol catabolites
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Ferulic Acid Is a Nutraceutical β-Secretase Modulator That Improves Behavioral Impairment and Alzheimer-like Pathology in Transgenic Mice
Mori, T., Koyama, N., Guillot‐Sestier, M., Tan, J., & Town, T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0055774 · Cited by 189 · see citing works
L-Carnitine intake and high trimethylamine N-oxide plasma levels correlate with low aortic lesions in ApoE−/− transgenic mice expressing CETP
Collins, H. L., Drazul-Schrader, D., Sulpizio, A. C., Koster, P. D., Williamson, Y., Adelman, S. J., Owen, K., Sanli, T., & Bellamine, A. (2016) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2015.10.108 · Cited by 189 · see citing works
Ferulic acid exerts neuroprotective effects against cerebral ischemia/reperfusion-induced injury via antioxidant and anti-apoptotic mechanisms in vitro and in vivo
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Phytochemicals and cognitive health: Are flavonoids doing the trick?
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“Among these interactions, the relationship between the gut and the brain is particularly prominent and is mediated through interconnected signaling pathways collectively known as the gut-brain axis (Ahmed et al., 2022).”

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Authors: Ahmed, H., Leyrolle, Q., Koistinen, V., Kärkkäinen, O., Layé, S., Delzenne, N., & Hanhineva, K.
Affiliations: University of Turku (FI)
UCLouvain (BE)
University of Eastern Finland (FI)
Université de Bordeaux (FR)
Corresponding author: Ahmed, Hany
ORCID: Ahmed, Hany
Leyrolle, Quentin
Koistinen, Ville
Kärkkäinen, Olli
Layé, Sophie
Delzenne, Nathalie
Hanhineva, Kati
Venue: Gut Microbes
Publisher: Informa UK Limited
Published: 2022-07-28
Volume: 14
Issue: 1
Pages: 2102878-2102878
ISSN: 1949-0976 (ISSN-L)
1949-0984
DOI: 10.1080/19490976.2022.2102878
PMC: PMC9341364
OpenAlex: W4288436705
Cited by: 462
References: 208
Citations by year: 2026: 135 · 2025: 161 · 2024: 110 · 2023: 48 · 2022: 7 · 2020: 1
FWCI: 26.69
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
doi.org/10.1080/policies-text-data-mining (tdm)
Locations: Gut Microbes (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Oskar-Bordeaux (Universite de Bordeaux) (submittedVersion, cc-by)
UTUPub (University of Turku) (submittedVersion)
HAL (submittedVersion, cc-by)
Digital Access to Libraries (Université catholique de Louvain (UCL), l'Université de Namur (UNamur) and the Université Saint-Louis (USL-B)) (submittedVersion, other-oa)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Chalmers Research (Chalmers University of Technology) (submittedVersion)
Funders: Academy of Finland ((Grant no 321716))
Marie Sklodowska-Curie ((Grant no 754412.)
Région Nouvelle Aquitaine ExoMarquAge ((135059720-13062120))
The Foundation for Medical Research
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Keywords: gut microbiota, gut microbiota metabolites, gut-brain axis, neurodevelopmental disorders, neurodegenerative diseases, neuropsychiatric disorders, short-chain fatty acids, trimethylamine N-oxide, bile acids, aryl hydrocarbon receptor, autism spectrum disorder, maternal immune activation, blood-brain barrier, brain-derived neurotrophic factor, germ-free mice
MeSH terms: Autism Spectrum Disorder, Gastrointestinal Microbiome, Brain, Fatty Acids, Volatile, Humans, Amyloid beta-Peptides

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Microbiota-derived metabolites as drivers of gut–brain communication

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