Gut/brain axis and the microbiota

Mayer, Emeran A.; Tillisch, Kirsten; Gupta, Arpana

doi:10.1172/jci76304

Cited by 1,503Gut microbiota and healthGastrointestinal motility and disordersTryptophan and brain disorders

Gut/brain axis and the microbiota

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Mayer, Emeran A., Tillisch, Kirsten, Gupta, Arpana·2015·Journal of Clinical Investigation

DOI 10.1172/jci76304PMC PMC4362231

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Abstract

Tremendous progress has been made in characterizing the bidirectional interactions between the central nervous system, the enteric nervous system, and the gastrointestinal tract. A series of provocative preclinical studies have suggested a prominent role for the gut microbiota in these gut-brain interactions. Based on studies using rodents raised in a germ-free environment, the gut microbiota appears to influence the development of emotional behavior, stress- and pain-modulation systems, and brain neurotransmitter systems. Additionally, microbiota perturbations by probiotics and antibiotics exert modulatory effects on some of these measures in adult animals. Current evidence suggests that multiple mechanisms, including endocrine and neurocrine pathways, may be involved in gut microbiota-to-brain signaling and that the brain can in turn alter microbial composition and behavior via the autonomic nervous system. Limited information is available on how these findings may translate to healthy humans or to disease states involving the brain or the gut/brain axis. Future research needs to focus on confirming that the rodent findings are translatable to human physiology and to diseases such as irritable bowel syndrome, autism, anxiety, depression, and Parkinson's disease.

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The gut-brain axis is critical for several facets of CNS physiology, including microglial development and function.
“Sophisticated crosstalk between the CNS and the gut microbiome (known as the gut–brain axis) is critical for several facets of CNS physiology, including microglial development and function (Mayer et al., 2015; Fung et al., 2017).”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Mayer et al., 2015
Microglial activity is influenced by factors originating outside the CNS, including the gut.
“microglial activity is now known to be influenced by factors originating outside the CNS, including the gut.”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Mayer et al., 2015

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A role for the gut microbiota in IBS
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Influences of Dietary and Environmental Stress on Microbial Populations in the Murine Gastrointestinal Tract
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Colonic Motility Abnormality in Patients With Irritable Bowel Syndrome Exhibiting Abdominal Pain and Diarrhea
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Faecal microbiota composition and host–microbe cross-talk following gastroenteritis and in postinfectious irritable bowel syndrome
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Prenatal Stress Alters Bacterial Colonization of the Gut in Infant Monkeys
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Voices from within: gut microbes and the CNS
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Stressor Exposure Disrupts Commensal Microbial Populations in the Intestines and Leads to Increased Colonization by Citrobacter rodentium
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Mast Cell Tryptase Controls Paracellular Permeability of the Intestine
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Lactobacillus reuteri enhances excitability of colonic AH neurons by inhibiting calcium‐dependent potassium channel opening
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Evolving pathophysiologic models of functional gastrointestinal disorders
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Effects of intestinal microbiota on anxiety-like behavior
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Altered brain-gut axis in autism: comorbidity or causative mechanisms
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The microbiota–gut–brain axis in gastrointestinal disorders: stressed bugs, stressed brain or both?
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SCFAs Induce Mouse Neutrophil Chemotaxis through the GPR43 Receptor
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Altered colonic function and microbiota profile in a mouse model of chronic depression
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Transporters and receptors for short-chain fatty acids as the molecular link between colonic bacteria and the host
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Probiotics treatment improves diabetes-induced impairment of synaptic activity and cognitive function: behavioral and electrophysiological proofs for microbiome–gut–brain axis
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“22 and Figure 1), a range of effects of gut microbial modulation was reported on emotional behavior (38–43, 48, 68–70), learning and memory (42, 71, 72), social interactions (48, 58, 73), and ingestive behaviors (55).”
Commensal microbiota is fundamental for the development of inflammatory pain
Amaral, F. A., Sachs, D., Costa, V. V., Fagundes, C. T., Cisalpino, D., Cunha, T. M., Ferreira, S. H., Cunha, F. Q., Silva, T. A., Nicoli, J. R., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711891105 · Cited by 289 · see citing works
The intestinal barrier and its regulation by neuroimmune factors: Intestinal barrier and neuroimmune regulation
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Intestinal microbiota of infants with colic: development and specific signatures
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Disturbance of the gut microbiota in early-life selectively affects visceral pain in adulthood without impacting cognitive or anxiety-related behaviors in male rats
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Microbial endocrinology and infectious disease in the 21st century
Lyte, M. (2004) · Trends in Microbiology · doi:10.1016/j.tim.2003.11.004 · Cited by 268 · see citing works
Commensal microbiota modulate murine behaviors in a strictly contamination-free environment confirmed by culture-based methods
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Communication between gastrointestinal bacteria and the nervous system
Bravo, J. A., Julio-Pieper, M., Forsythe, P., Kunze, W., Dinan, T. G., Bienenstock, J., & Cryan, J. F. (2012) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2012.09.010 · Cited by 261 · see citing works
Neonatal maternal separation predisposes adult rats to colonic barrier dysfunction in response to mild stress
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Release of mast cell mediators into the jejunum by cold pain stress in humans
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Stress stimulates transepithelial macromolecular uptake in rat jejunum
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Evolution of cell–cell signaling in animals: did late horizontal gene transfer from bacteria have a role?
Iyer, L. M., Aravind, L., Coon, S. L., Klein, D. C., & Koonin, E. V. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.05.007 · Cited by 219 · see citing works
Review article: associations between immune activation, intestinal permeability and the irritable bowel syndrome
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Gut-Derived Sepsis Occurs When the Right Pathogen With the Right Virulence Genes Meets the Right Host: Evidence for In Vivo Virulence Expression in Pseudomonas aeruginosa
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The adoptive transfer of behavioral phenotype via the intestinal microbiota: experimental evidence and clinical implications
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Combination of Lactobacillus helveticus R0052 and Bifidobacterium longum R0175 reduces post-myocardial infarction depression symptoms and restores intestinal permeability in a rat model
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Norepinephrine increases the pathogenic potential of Campylobacter jejuni
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Lactobacillus farciminis treatment suppresses stress induced visceral hypersensitivity: a possible action through interaction with epithelial cell cytoskeleton contraction
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Increased oral detection, but decreased intestinal signaling for fats in mice lacking gut microbiota
Duca, F. A., Swartz, T. D., Sakar, Y., & Covasa, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039748 · Cited by 181 · see citing works
Priming for health: gut microbiota acquired in early life regulates physiology, brain and behaviour
Clarke, G., O'Mahony, S., Dinan, T., & Cryan, J. (2014) · Acta Paediatrica · doi:10.1111/apa.12674 · Cited by 179 · see citing works
Synergy between Lactobacillus paracasei and its bacterial products to counteract stress-induced gut permeability and sensitivity increase in rats
Eutamene, H., Lamine, F., Chabo, C., Theodorou, V., Rochat, F., Bergonzelli, G. E., Corthésy-Theulaz, I., Fioramonti, J., & Bueno, L. (2007) · The Journal of Nutrition · doi:10.1093/jn/137.8.1901 · Cited by 169 · see citing works
Human Metabolic Phenotypes Link Directly to Specific Dietary Preferences in Healthy Individuals
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Effects of intraduodenal injection of Lactobacillus johnsonii La1 on renal sympathetic nerve activity and blood pressure in urethane-anesthetized rats.
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Hughes, P. A., Zola, H., Penttila, I., Blackshaw, L. A., Andrews, J. M., & Krumbiegel, D. (2013) · The American Journal of Gastroenterology · doi:10.1038/ajg.2013.120 · Cited by 147 · see citing works
Up-regulation of intestinal type 1 taste receptor 3 and sodium glucose luminal transporter-1 expression and increased sucrose intake in mice lacking gut microbiota
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Friends with social benefits: host-microbe interactions as a driver of brain evolution and development?
Stilling, R. M., Bordenstein, S. R., Dinan, T. G., & Cryan, J. F. (2014) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2014.00147 · Cited by 135 · see citing works
Effects of probiotics and commensals on intestinal epithelial physiology: implications for nutrient handling
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Interdigestive small bowel motility and duodenal bacterial overgrowth in experimental acute pancreatitis
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Maladaptive Intestinal Epithelial Responses to Life Stress May Predispose Healthy Women to Gut Mucosal Inflammation
Alonso, C., Guilarte, M., Vicario, M., Ramos, L., Ramadan, Z., Antolín, M., Martínez, C., Rezzi, S., Saperas, E., Kochhar, S., et al. (2008) · Gastroenterology · doi:10.1053/j.gastro.2008.03.036 · Cited by 128 · see citing works
Toward Effective Probiotics for Autism and Other Neurodevelopmental Disorders
Gilbert, J. A., Krajmalnik‐Brown, R., Porazinska, D. L., Weiss, S. J., & Knight, R. D. (2013) · Cell · doi:10.1016/j.cell.2013.11.035 · Cited by 120 · see citing works
Intestinal microbiota and immune function in the pathogenesis of irritable bowel syndrome
Ringel, Y., & Maharshak, N. (2013) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00207.2012 · Cited by 115 · see citing works
Contrasting effects of Bifidobacterium breve NCIMB 702258 and Bifidobacterium breve DPC 6330 on the composition of murine brain fatty acids and gut microbiota
Wall, R., Marques, T. M., O’Sullivan, Ó., Ross, R. P., Shanahan, F., Quigley, E. M. M., Dinan, T. G., Kiely, B., Fitzgerald, G. F., Cotter, P. D., et al. (2012) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.026435 · Cited by 112 · see citing works
Sensitization of Peripheral Sensory Nerves by Mediators From Colonic Biopsies of Diarrhea-Predominant Irritable Bowel Syndrome Patients: A Role for PAR2
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Corticotropin-releasing factor receptor 1 mediates acute and delayed stress-induced visceral hyperalgesia in maternally separated Long-Evans rats
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Intestinal inflammation in a murine model of autism spectrum disorders
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Authors: Mayer, E. A., Tillisch, K., & Gupta, A.
Affiliations: University of California, Los Angeles (US)
VA Greater Los Angeles Healthcare System (US)
Corresponding author: Mayer, Emeran A.
ORCID: Mayer, Emeran A.
Tillisch, Kirsten
Gupta, Arpana
Venue: Journal of Clinical Investigation
Publisher: American Society for Clinical Investigation
Published: 2015-02-17
Volume: 125
Issue: 3
Pages: 926-938
ISSN: 0021-9738 (ISSN-L)
DOI: 10.1172/jci76304
PMC: PMC4362231
OpenAlex: W2001339909
Cited by: 1,503
References: 141
Citations by year: 2026: 144 · 2025: 143 · 2024: 133 · 2023: 128 · 2022: 169 · 2021: 165 · 2020: 160 · 2019: 126 · 2018: 122 · 2017: 90 · 2016: 81 · 2015: 41
FWCI: 10.79
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Clinical Investigation (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: National Institutes of Health (DK 48351)
National Institute of Diabetes and Digestive and Kidney Diseases (DK-48351, DK 64539, R01DK048351, P50DK064539)
National Center for Complementary and Integrative Health (AT007137, R01AT007137)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Keywords: gut-brain axis, gut microbiota, enteric nervous system, emotional behavior, stress response, pain modulation, neurotransmitter systems, probiotics, antibiotics, hormone signaling, autonomic nervous system, irritable bowel syndrome, autism spectrum disorder, anxiety, depression, Parkinson's disease
MeSH terms: Animals, Behavior, Brain, Cell Membrane Permeability, Diet, Emotions, Humans, Hypothalamo-Hypophyseal System, Intestinal Mucosa, Pituitary-Adrenal System, Gastrointestinal Tract, Microbiota

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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

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Gut/brain axis and the microbiota

Abstract

Integrity signals

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