Interactions between the microbiota, immune and nervous systems in health and disease

Fung, Thomas C; Olson, Christine A; Hsiao, Elaine Y

doi:10.1038/nn.4476

Cited by 1,900Gut microbiota and healthTryptophan and brain disordersNeuroinflammation and Neurodegeneration Mechanisms

Interactions between the microbiota, immune and nervous systems in health and disease

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Fung, Thomas C, Olson, Christine A, Hsiao, Elaine Y·2017·Nature Neuroscience

DOI 10.1038/nn.4476PMC PMC6960010

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Abstract

The diverse collection of microorganisms that inhabit the gastrointestinal tract, collectively called the gut microbiota, profoundly influences many aspects of host physiology, including nutrient metabolism, resistance to infection and immune system development. Studies investigating the gut–brain axis demonstrate a critical role for the gut microbiota in orchestrating brain development and behavior, and the immune system is emerging as an important regulator of these interactions. Intestinal microbes modulate the maturation and function of tissue-resident immune cells in the CNS. Microbes also influence the activation of peripheral immune cells, which regulate responses to neuroinflammation, brain injury, autoimmunity and neurogenesis. Accordingly, both the gut microbiota and immune system are implicated in the etiopathogenesis or manifestation of neurodevelopmental, psychiatric and neurodegenerative diseases, such as autism spectrum disorder, depression and Alzheimer's disease. In this review, we discuss the role of CNS-resident and peripheral immune pathways in microbiota–gut–brain communication during health and neurological disease.

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Modulation of gut physiology by the central nervous system and its effects on gut function such as motility, secretion, blood flow, nociception, and immune function during neurological stressors are well-documented.
“The modulation of gut physiology by the CNS and its effects on gut function such as motility, secretion, blood flow, nociception, and immune function during neurological stressors are well-documented (17, 29, 30).”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [17]
The Neuroendocrine pathways section says stress-related CNS signaling can alter intestinal motility, mucus production, and immune responses. The Neuronal signaling section also describes CNS control of motility and the intestinal immune environment. These passages do not establish the claimed effects on gut blood flow or nociception, or secretion generally; page numbers are unavailable in our copy. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Several bacterial strains can modify levels of neurotransmitter precursors in the gut lumen and even independently synthesize or modulate the synthesis of neurotransmitters including GABA, serotonin, dopamine, and noradrenaline.
“several bacterial strains can modify levels of neurotransmitter precursors in the gut lumen and even independently synthesize (or modulate the synthesis of) a number of neurotransmitters, including γ-aminobutyric acid (GABA), serotonin (5-HT), dopamine (DA), and noradrenaline (NA) (16–18).”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [17]
The “Bacteria-derived and host-derived products” section (page not provided) says that particular gut microbes can synthesize neurotransmitters de novo and that microbiota regulate serotonin, GABA, norepinephrine and dopamine pathways. It does not say that bacterial strains alter neurotransmitter precursor levels in the gut lumen, or that they independently synthesize each of the four named neurotransmitters. (LLM, conf=0.87)
Experimental — accuracy not yet measured
The gut microbiota can interact with the central nervous system via gut modulation or directly via metabolites and endotoxin translocation from the lumen to the circulation.
“the gut microbiota can interact with the CNS via gut modulation or directly via metabolites and endotoxin translocation from the lumen to the circulation (9, 17, 21).”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [17]
The ‘Bacteria-derived and host-derived products’ section (page unavailable) says gut bacteria influence brain function through gut signaling and that circulating metabolites can enter the CNS. It also reports systemic detection of microbiota-derived TLR ligands during chronic inflammatory disorders, but does not establish the claimed direct route of endotoxin translocation from the gut lumen to the circulation and onward to the CNS; it says evidence for microbiota-derived products triggering CNS inflammation is limited. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Butyrate is capable of inducing T regulatory cell differentiation and controlling inflammation.
“butyrate is capable of inducing Treg differentiation and controlling inflammation (17, 23, 24, 87).”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [17]
The “CNS inflammation and injury” section reports that treating mice with short-chain fatty acids reduced EAE and axonal damage through increased Treg differentiation. It does not identify butyrate specifically as responsible for those effects; the “Microglia” section lists butyrate as an SCFA but calls for further study of particular SCFAs. Page numbers were not available in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Short-chain fatty acids that cross into the central nervous system have neuroactive properties.
“Accumulating evidence suggests that SCFAs that cross into the CNS have neuroactive properties.”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [17]
The ‘Bacteria-derived and host-derived products’ section (page unavailable) says circulating metabolites can enter the CNS and directly affect neuroactivity. But it does not identify those metabolites as SCFAs; the ‘Microglia’ section (page unavailable) says whether SCFAs act through direct signaling remains unclear. The source therefore supports the general mechanism, not the SCFA-specific claim. (LLM, conf=0.86)
Experimental — accuracy not yet measured

The microbiota is altered in CNS diseases, which aggravates the condition, and/or its modulation might prevent or improve the development and progression of CNS pathologies.
“The central hypothesis is supported by experimental and clinical evidence that the microbiota is altered in such diseases, which aggravates the condition, and/or its modulation might prevent or improve the development and progression of CNS pathologies (17, 19, 29, 33–37).”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [17]
The review reports altered microbiota in people with depression and Parkinson’s disease (Associations with endophenotypes of neurological diseases; page unavailable), and describes mouse stroke experiments in which microbiota transfer worsened injury while transfer from healthy animals reduced lesions (CNS inflammation and injury; page unavailable). These findings support the proposed link and the possibility that modulation could help, but they do not establish that altered microbiota generally aggravates CNS diseases or that modulation prevents their progression in patients. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Several brain disorders have been linked to imbalances in the microbial composition of the gut.
“several brain disorders have been linked to imbalances in the microbial composition of the gut (17, 19, 29, 33–37)”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [17]
Brain-to-gut signaling can directly affect the microbiota via the immune system or gut functions such as motility, release of neurotransmitters, and intestinal immune tone.
“brain to gut signaling can directly affect the microbiota, either via immune system or gut functions such as motility, release of neurotransmitters and intestinal immune tone (12, 17, 21, 31).”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [17]
Growing evidence supports that short-chain fatty acids exert crucial physiological effects on several organs, including the brain.
“growing evidence supports the idea that SCFAs also exert crucial physiological effects on several organs, including the brain (17, 20, 21).”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [17]
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 Fung et al., 2017
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 Fung et al., 2017
Gut microbiota can influence the state of peripheral inflammation through interactions with nearby immune cells.
“Along with affecting the level of permeability along the intestinal tract, gut microbiota can influence the state of peripheral inflammation through interactions with nearby immune cells.”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Fung et al., 2017
When microbe-associated molecular patterns produced by pathogenic invaders bind to pattern recognition receptors such as TLRs on host cells, they influence the production of both pro- and anti-inflammatory cytokines.
“When microbe-associated molecular patterns produced by pathogenic invaders bind to pattern recognition receptors, such as TLRs, on host cells, they influence the production of both pro- and anti-inflammatory cytokines (Fung et al., 2017).”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Fung et al., 2017
The number of microbes inhabiting the human body is roughly equal to the number of human cells.
“the number of microbes that inhabit the human body (roughly equal to the number of human cells)”
From The microbiome and human cancer (2021) · cites this paper as [29]
The microbial gene count exceeds the human genome's gene count by about 100-fold and enables diverse metabolic programming.
“their gene count that exceeds the human genome’s gene count by ~100-fold and enables diverse metabolic programming”
From The microbiome and human cancer (2021) · cites this paper as [29]
Microbes affect host immune system development and activity, including antitumor immunosurveillance.
“their effects on host immune system development and activity, including antitumor immunosurveillance (27–31).”
From The microbiome and human cancer (2021) · cites this paper as [29]
The intestinal microbiota is involved in immune response and prevention of pathogenic invasions.
“The intestinal microbiota is involved in immune response and prevention of pathogenic invasions [33].”
From Microalgae n-3 PUFAs Production and Use in Food and Feed Industries (2021) · cites this paper as [33]
Altered SCFA production is demonstrated in a variety of neuropathologies.
“Altered SCFA production has also been demonstrated in a variety of neuropathologies (42, 116, 127, 130, 132, 292–295).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [127]
The gut microbiome likely alters brain functions through various mechanisms including environmental factors, host genetics, host immune response regulation, excretion of metabolites, regulation of neurotransmitters, or neuroactive compounds.
“the gut microbiome likely alters brain functions through various other mechanisms, including environmental factors (e.g. in utero exposure to infection, maternal conditions, and medications), host genetics, host immune response regulation [12, 57, 58], excretion of metabolites such as tyrosine analogues, p-cresol, 4-ethylphenylsulfate, indoles, lipopolysaccharides and free amino acids [59-62],”
From Gut microbiota changes in children with autism spectrum disorder: a systematic review (2020) · cites this paper as [57]

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The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication
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“One of the best-documented effects of SCFAs is on the immune system since butyrate is capable of inducing Treg differentiation and controlling inflammation (17, 23, 24, 87).”
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Gut microbiome alterations in Alzheimer’s disease
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GABA-modulating bacteria of the human gut microbiota
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Altered Microbiomes Distinguish Alzheimer’s Disease from Amnestic Mild Cognitive Impairment and Health in a Chinese Cohort
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Transfer of a healthy microbiota reduces amyloid and tau pathology in an Alzheimer’s disease animal model
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Combined effects of host genetics and diet on human gut microbiota and incident disease in a single population cohort
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“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).”
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A gut bacterial amyloid promotes α-synuclein aggregation and motor impairment in mice
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Microalgae n-3 PUFAs Production and Use in Food and Feed Industries
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Dysbiosis of microbiome and probiotic treatment in a genetic model of autism spectrum disorders
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Th17 cells in depression
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Blockade of interleukin-6 receptor in the periphery promotes rapid and sustained antidepressant actions: a possible role of gut–microbiota–brain axis
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Intestinal Microbiota Influences Non-intestinal Related Autoimmune Diseases
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Microbiota-gut-brain axis in health and disease: Is NLRP3 inflammasome at the crossroads of microbiota-gut-brain communications?
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Key role of gut microbiota in anhedonia-like phenotype in rodents with neuropathic pain
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Time to test antibacterial therapy in Alzheimer’s disease
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Gut Microbiota Dysbiosis Is Associated with Elevated Bile Acids in Parkinson’s Disease
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The gut microbiome: a key player in the complexity of amyotrophic lateral sclerosis (ALS)
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Fluoxetine ameliorates dysbiosis in a depression model induced by chronic unpredicted mild stress in mice
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Authors: Fung, T. C., Olson, C. A., & Hsiao, E. Y.
Affiliations: University of California, Los Angeles (US)
Corresponding author: Hsiao, Elaine Y
ORCID: Fung, Thomas C
Olson, Christine A
Hsiao, Elaine Y
Venue: Nature Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2017-01-16
Volume: 20
Issue: 2
Pages: 145-155
ISSN: 1097-6256 (ISSN-L)
1546-1726
DOI: 10.1038/nn.4476
PMC: PMC6960010
OpenAlex: W2572551054
Semantic Scholar: 48f698ab29a167efa4c1bbd22c3c7c185b485eb0
Cited by: 1,900
References: 157
Citations by year: 2026: 156 · 2025: 238 · 2024: 222 · 2023: 212 · 2022: 264 · 2021: 275 · 2020: 205 · 2019: 171 · 2018: 93 · 2017: 62 · 2013: 1
FWCI: 13.58
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature Neuroscience (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (DP5OD017924)
National Institute of Mental Health (F31MH090749)
National Institute of General Medical Sciences (T32GM065823)
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 › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: gut microbiota, gut-brain axis, microbiota-immune interactions, neuroinflammation, neurodevelopmental disorders, autism spectrum disorder, depression, Alzheimer's disease, neurodegenerative diseases, neurogenesis, brain injury, autoimmunity, peripheral immune cells, mental illness
MeSH terms: Autism Spectrum Disorder, Animals, Brain, Humans, Nervous System Diseases, Autoimmunity, Gastrointestinal Tract, Microbiota

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