Chronically Elevated Levels of Short-Chain Fatty Acids Induce T Cell–Mediated Ureteritis and Hydronephrosis
Open accessAbstract
Short-chain fatty acids (SCFAs) are major products of gut microbial fermentation and profoundly affect host health and disease. SCFAs generate IL-10+ regulatory T cells, which may promote immune tolerance. However, SCFAs can also induce Th1 and Th17 cells upon immunological challenges and, therefore, also have the potential to induce inflammatory responses. Because of the seemingly paradoxical SCFA activities in regulating T cells, we investigated, in depth, the impact of elevated SCFA levels on T cells and tissue inflammation in mice. Orally administered SCFAs induced effector (Th1 and Th17) and regulatory T cells in ureter and kidney tissues, and they induced T cell–mediated ureteritis, leading to kidney hydronephrosis (hereafter called acetate-induced renal disease, or C2RD). Kidney hydronephrosis in C2RD was caused by ureteral obstruction, which was, in turn, induced by SCFA-induced inflammation in the ureteropelvic junction and proximal ureter. Oral administration of all major SCFAs, such as acetate, propionate, and butyrate, induced the disease. We found that C2RD development is dependent on mammalian target of rapamycin activation, T cell–derived inflammatory cytokines such as IFN-γ and IL-17, and gut microbiota. Young or male animals were more susceptible than old or female animals, respectively. However, SCFA receptor (GPR41 or GPR43) deficiency did not affect C2RD development. Thus, SCFAs, when systemically administered at levels higher than physiological levels, cause dysregulated T cell responses and tissue inflammation in the renal system. The results provide insights into the immunological and pathological effects of chronically elevated SCFAs.
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SCFAs promote the expansion of Tregs but also seem to improve the function of effector T cells.
“These were shown to promote the expansion of Tregs, but they also seem to improve the function of effector T cells10–15.”
From Microbial short-chain fatty acids modulate CD8+ T cell responses and improve adoptive immunotherapy for cancer (2021) · cites this paper as [14]
SCFAs have context-dependent effects, promoting Treg expansion and also improving effector T cell functions.
“SCFAs have context-dependent functions: they can promote the expansion of Treg cells and also improve effector T cell functions133–136.”
From Gut OncoMicrobiome Signatures (GOMS) as next-generation biomarkers for cancer immunotherapy (2023) · cites this paper as [135]
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- Authors
- Park, J., Goergen, C. J., HogenEsch, H., & Kim, C. H.
- Affiliations
- Purdue University West Lafayette (US)
- Corresponding author
- Park, Jeongho
- HogenEsch, Harm
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2016-03-01
- Volume
- 196
- Issue
- 5
- Pages
- 2388-2400
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- PMC
- PMC4761537
- OpenAlex
- W2278335898
- Cited by
- 166
- References
- 55
- Citations by year
- 2026: 8 · 2025: 15 · 2024: 9 · 2023: 25 · 2022: 17 · 2021: 21 · 2020: 22 · 2019: 22 · 2018: 11 · 2017: 12 · 2016: 4
- FWCI
- 8.49
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (R01AI080769, R01AI074745)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK076616)
- National Center for Research Resources (S10RR028293)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Immunology and Microbiology › Immunology › Immunotoxicology and immune responses
- Keywords
- short-chain fatty acids, ureteritis, hydronephrosis, Th1 cells, Th17 cells, regulatory T cells, IL-17, interferon-gamma, mTOR signaling, gut microbiota, ureteral obstruction, GPR41, GPR43
- MeSH terms
- Gastrointestinal Microbiome, Animals, Disease Models, Animal, Fatty Acids, Volatile, Female, Fibrosis, Hydronephrosis, Hyperplasia, Male, Sex Factors, Urethritis, Signal Transduction, Cluster Analysis, T-Lymphocyte Subsets, Cytokines, Mice, Knockout, Th2 Cells, Disease Progression, Inflammation Mediators, Sodium Acetate, Gene Expression Profiling, Mice, Th17 Cells, TOR Serine-Threonine Kinases, Transcriptome
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