Identification of a Signaling Mechanism by Which the Microbiome Regulates Th17 Cell-Mediated Depressive-Like Behaviors in Mice
Open accessAbstract
OBJECTIVE: Microbiota dysbiosis has been linked to major depressive disorder, but the mechanisms whereby the microbiota modulates mood remain poorly understood. The authors tested whether specific changes in the microbiome modulate depressive-like behaviors. METHODS: Stools from learned helpless, non-learned helpless, and non-shocked mice were analyzed by V4 16S RNA sequencing to identify gut bacteria associated with learned helplessness and to quantify the level of the quorum-sensing molecule autoinducer-2 (AI-2). T cells were analyzed by flow cytometry, and serum amyloid proteins (SAA) were analyzed by quantitative real-time polymerase chain reaction. Fecal transfer approach and administration of oleic acid and AI-2 were used to determine the effects of the microbiome and quorum-sensing molecules on depressive-like behaviors. RESULTS: Mice deficient in segmented filamentous bacteria (SFB) were resilient to the induction of depressive-like behavior, and were resensitized when SFB was reintroduced in the gut. SFB produces the quorum-sensing AI-2 and promotes the production of SAA1 and SAA2 by the host, which increases T helper 17 (Th17) cell production. Th17 cells were required to promote depressive-like behaviors by AI-2, as AI-2 administration did not promote susceptibility to depressive-like behaviors or SAA1 and SAA2 production in Th17-deficient mice after stress. Oleic acid, an AI-2 inhibitor, exhibited antidepressant properties, reducing depressive-like behavior, intestinal SAA1 and SAA2 production, and hippocampal Th17 cell accumulation. Stool samples from 10 people with current depressive symptoms and 10 matched healthy control subjects were analyzed as well. Patients with current major depressive disorder exhibited increased fecal interleukin 17A, SAA, and SFB levels. CONCLUSIONS: The study results reveal a novel mechanism by which bacteria alter mood.
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IL-17A-producing Th17 cells mediate the relationship between certain gut microorganisms and development of depression-like symptoms in mice.
“They found a relationship between certain types of gut microorganisms and the development of depression-like symptoms. The primary cells which mediated these processes were IL-17A-producing Th17 cells [146].”
From Selected biomarkers of depression: what are the effects of cytokines and inflammation (2022) · cites this paper as [146]
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Self-citationDectin-1 signaling on colonic γδ T cells promotes psychosocial stress responses
Zhu, X., Sakamoto, S., Ishii, C., Smith, M. D., Ito, K., Obayashi, M., Unger, L., Hasegawa, Y., Kurokawa, S., Kishimoto, T., et al. (2023) · Nature Immunology · doi:10.1038/s41590-023-01447-8 · Cited by 99 · see citing works
Inflamed brain: Targeting immune changes and inflammation for treatment of depression
Sakamoto, S., Zhu, X., Hasegawa, Y., Karma, S., Obayashi, M., Alway, E., & Kamiya, A. (2021) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.13286 · Cited by 51 · see citing works
- Authors
- Medina-Rodriguez, E. M., Madorma, D., O’Connor, G., Mason, B. L., Han, D., Deo, S. K., Oppenheimer, M., Nemeroff, C. B., Trivedi, M. H., Daunert, S., & Beurel, E.
- Affiliations
- University of Miami (US)
- Corresponding author
- Beurel, Eléonore
- ORCID
- Venue
- American Journal of Psychiatry
- Published
- 2020-10-01
- Volume
- 177
- Issue
- 10
- Pages
- 974-990
- ISSN
- 0002-953X (ISSN-L)
- 1535-7228
- PMC
- PMC7647050
- OpenAlex
- W3046220904
- Cited by
- 110
- References
- 83
- Citations by year
- 2026: 13 · 2025: 9 · 2024: 28 · 2023: 19 · 2022: 29 · 2021: 10 · 2020: 2
- FWCI
- 4.86
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- American Journal of Psychiatry (publishedVersion, public-domain)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH104656, R01MH110415)
- National Institute of General Medical Sciences (R01GM127706, R01GM114321, R01GM047915)
- 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 › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- gut microbiota, depression-like behavior, Th17 cells, autoinducer-2, quorum sensing, segmented filamentous bacteria, serum amyloid protein, learned helplessness, oleic acid, antidepressant effects, major depressive disorder, IL-17A, stress resilience, fecal microbiota transplantation
- MeSH terms
- Gastrointestinal Microbiome, Adult, Serum Amyloid A Protein, Animals, Depression, Major Depressive Disorder, Disease Models, Animal, Feces, Female, Flow Cytometry, Helplessness, Learned, Humans, Male, Mice, Inbred C57BL, Middle Aged, RNA, Ribosomal, 16S, Interleukin-17, Mice, Quorum Sensing, Th17 Cells, Real-Time Polymerase Chain Reaction
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