Symbiotic bacterial metabolites regulate gastrointestinal barrier function via the xenobiotic sensor PXR and Toll-like receptor 4
Open accessAbstract
Intestinal microbial metabolites are conjectured to affect mucosal integrity through an incompletely characterized mechanism. Here we showed that microbial-specific indoles regulated intestinal barrier function through the xenobiotic sensor, pregnane X receptor (PXR). Indole 3-propionic acid (IPA), in the context of indole, is a ligand for PXR in vivo, and IPA downregulated enterocyte TNF-α while it upregulated junctional protein-coding mRNAs. PXR-deficient (Nr1i2(-/-)) mice showed a distinctly "leaky" gut physiology coupled with upregulation of the Toll-like receptor (TLR) signaling pathway. These defects in the epithelial barrier were corrected in Nr1i2(-/-)Tlr4(-/-) mice. Our results demonstrate that a direct chemical communication between the intestinal symbionts and PXR regulates mucosal integrity through a pathway that involves luminal sensing and signaling by TLR4.
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NR1I2/PXR is a functional receptor for indole-3-propionic acid (IPA).
“the promiscuous nuclear receptor subfamily 1 group I member 2 (NR1I2, also known as pregnane X receptor, PXR) has been identified as a functional receptor for indole-3-propionic acid (IPA)”
From Understanding the Holobiont: How Microbial Metabolites Affect Human Health and Shape the Immune System (2017) · cites this paper as Venkatesh et al., 2014
Nr1i2−/− mice exhibit impaired epithelial barrier function.
“Nr1i2−/− mice exhibit impaired epithelial barrier function”
From Understanding the Holobiont: How Microbial Metabolites Affect Human Health and Shape the Immune System (2017) · cites this paper as Venkatesh et al., 2014
IPA is produced in mice monocolonized with Clostridium sporogenes but is absent in the gut of germ-free mice.
“which is produced in mice monocolonized with Clostridium sporogenes but absent in the gut of germ-free mice (Venkatesh et al., 2014; Wikoff et al., 2009).”
From Understanding the Holobiont: How Microbial Metabolites Affect Human Health and Shape the Immune System (2017) · cites this paper as Venkatesh et al., 2014
Combined knockout of Nr1i2 and Tlr4 can rescue the phenotype of Nr1i2−/− mice, possibly by counteracting accelerated cell death of inflammatory monocytes.
“the combined knockout of Nr1i2 and the gene encoding the LPS sensor toll-like receptor 4 (Tlr4) can rescue the phenotype of Nr1i2−/− mice, possibly because it counteracts the accelerated cell death of inflammatory monocytes observed in NR1I2-deficient mice (Z. Qiu et al., 2016; Venkatesh et al., 2014).”
From Understanding the Holobiont: How Microbial Metabolites Affect Human Health and Shape the Immune System (2017) · cites this paper as Venkatesh et al., 2014
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Goldszmid, R. S., Dzutsev, A., Viaud, S., Zitvogel, L., Restifo, N. P., & Trinchieri, G. (2015) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-14-0225 · Cited by 46 · see citing works
Dietary Protein and Colonic Microbiota
Boudry, G., Le Huërou-Luron, I., & Michel, C. (2016) · The Molecular Nutrition of Amino Acids and Proteins · doi:10.1016/b978-0-12-802167-5.00015-3 · Cited by 5 · see citing works
- Authors
- Venkatesh, M., Mukherjee, S., Wang, H., Li, H., Sun, K., Benechet, A. P., Qiu, Z., Maher, L., Redinbo, M. R., Phillips, R. S., Fleet, J. C., Kortagere, S., Mukherjee, P., Fasano, A., Le Ven, J., Nicholson, J. K., Dumas, M. E., Khanna, K. M., & Mani, S.
- Affiliations
- Albert Einstein College of Medicine (US)
- Montefiore Medical Center (US)
- UConn Health (US)
- University of North Carolina at Chapel Hill (US)
- University of Georgia (US)
- Purdue University West Lafayette (US)
- Drexel University (US)
- Harvard University (US)
- Imperial College London (GB)
- Corresponding author
- Khanna, Kamal M.
- Mani, Sridhar
- ORCID
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2014-08
- Volume
- 41
- Issue
- 2
- Pages
- 296-310
- ISSN
- 1074-7613 (ISSN-L)
- PMC
- PMC4142105
- OpenAlex
- W2073714219
- Cited by
- 1,066
- References
- 50
- Citations by year
- 2026: 130 · 2025: 110 · 2024: 130 · 2023: 101 · 2022: 123 · 2021: 137 · 2020: 103 · 2019: 67 · 2018: 52 · 2017: 41 · 2016: 43 · 2015: 21 · 2014: 6
- FWCI
- 15.16
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Immunity (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- UNC Libraries
- Funders
- Damon Runyon Cancer Research Foundation
- University of Connecticut
- University of Pittsburgh
- European Commission (305312)
- National Institutes of Health
- National Cancer Institute (CA161879, CA 127231, R01CA161879, R01CA127231, P30CA013330)
- National Institute of Allergy and Infectious Diseases (R01AI097375, AI097375)
- FP7 Health (305312)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- indole-3-propionic acid, pregnane X receptor, TLR4, intestinal barrier function, intestinal permeability, mucosal integrity, tight junction proteins
- MeSH terms
- Pregnane X Receptor, Animals, Anti-Inflammatory Agents, Non-Steroidal, Antibodies, Cell Line, Female, Humans, Indoles, Indomethacin, Inflammation, Intestines, Lipopolysaccharides, Mice, Inbred C57BL, Receptors, Steroid, RNA, Messenger, Tumor Necrosis Factor-alpha, Signal Transduction, Reperfusion Injury, CD3 Complex, Caco-2 Cells, Tight Junctions, Adherens Junctions, RNA Interference, RNA, Small Interfering, Toll-Like Receptor 4, Mice, HEK293 Cells, Microbiota
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