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The Bile Acid Receptor GPBAR-1 (TGR5) Modulates Integrity of Intestinal Barrier and Immune Response to Experimental Colitis
Open accessAbstract
BACKGROUND: GP-BAR1, a member G protein coupled receptor superfamily, is a cell surface bile acid-activated receptor highly expressed in the ileum and colon. In monocytes, ligation of GP-BAR1 by secondary bile acids results in a cAMP-dependent attenuation of cytokine generation. AIMS: To investigate the role GP-BAR1 in regulating intestinal homeostasis and inflammation-driven immune dysfunction in rodent models of colitis. METHODS: Colitis was induced in wild type and GP-BAR1(-/-) mice by DSS and TNBS administration. Potential GP-BAR1 agonists were identified by in silico screening and computational docking studies. RESULTS: GP-BAR1(-/-) mice develop an abnormal morphology of colonic mucous cells and an altered molecular architecture of epithelial tight junctions with increased expression and abnormal subcellular distribution of zonulin 1 resulting in increased intestinal permeability and susceptibility to develop severe colitis in response to DSS at early stage of life. By in silico screening and docking studies we identified ciprofloxacin as a GP-BAR1 ligand. In monocytes, ciprofloxacin increases cAMP concentrations and attenuates TNFα release induced by TLR4 ligation in a GP-BAR1 dependent manner. Treating mice rendered colitic by TNBS with ciprofloxacin and oleanolic acid, a well characterized GP-BAR1 ligand, abrogates signs and symptoms of colitis. Colonic expression of GP-BAR1 mRNA increases in rodent models of colitis and tissues from Crohn's disease patients. Flow cytometry analysis demonstrates that ≈90% of CD14+ cells isolated from the lamina propria of TNBS-treated mice stained positively for GP-BAR1. CONCLUSIONS: GP-BAR1 regulates intestinal barrier structure. Its expression increases in rodent models of colitis and Crohn's disease. Ciprofloxacin is a GP-BAR1 ligand.
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“changes in the composition of the bile acid pool, an increase in colonic expression of GPBAR1 and a decrease in ileal activity of BAR have all been detected in patients suffering from IBD (Cipriani et al., 2011; Duboc et al., 2013; Lenz et al., 1976; Nijmeijer et al., 2011; Rutgeerts et al., 1979).”
From Understanding the Holobiont: How Microbial Metabolites Affect Human Health and Shape the Immune System (2017) · cites this paper as Cipriani et al., 2011
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“Gpbar1−/− mice, like their Nr1h4−/− counterparts, develop more severe disease than wildtype controls in several animal models of inflammatory disorder, including colitis, hepatitis and gastritis (Cipriani et al., 2011; C. Guo et al., 2015; Y.-D. Wang et al., 2011).”
From Understanding the Holobiont: How Microbial Metabolites Affect Human Health and Shape the Immune System (2017) · cites this paper as Cipriani et al., 2011
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“Mice treated with GP-BAR1 agonists (ciprofloxacin and oleanolic acid) abrogated the signs and symptoms of TNBS-induced colitis.117”
From Regulation of Intestinal Barrier Function by Microbial Metabolites (2021) · cites this paper as [117]
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“Importantly these mice were more susceptible to DSS- or TNBS-induced colitis.117”
From Regulation of Intestinal Barrier Function by Microbial Metabolites (2021) · cites this paper as [117]
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Metadata
- Authors
- Cipriani, S., Mencarelli, A., Chini, M. G., Distrutti, E., Renga, B., Bifulco, G., Baldelli, F., Donini, A., & Fiorucci, S.
- Affiliations
- University of Perugia (IT)
- University of Salerno (IT)
- Azienda Ospedaliera di Perugia (IT)
- Corresponding author
- Fiorucci, Stefano
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-10-27
- Volume
- 6
- Issue
- 10
- Pages
- e25637
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3203117
- OpenAlex
- W1970465623
- Cited by
- 382
- References
- 30
- Citations by year
- 2026: 20 · 2025: 19 · 2024: 30 · 2023: 34 · 2022: 45 · 2021: 49 · 2020: 31 · 2019: 29 · 2018: 25 · 2017: 14 · 2016: 16 · 2015: 17 · 2014: 23 · 2013: 19 · 2012: 11
- FWCI
- 10.58
- Type
- journal article
- Language
- en
- Update notices
- correction (2013-01-29)
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- National University of Singapore (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Archivio Istituzionale della Ricerca - Università degli Studi del Molise (submittedVersion)
- Topics
- Health Sciences › Medicine › Gastroenterology › Inflammatory Bowel Disease
- Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- TGR5, bile acid receptors, colitis, intestinal barrier integrity, tight junctions, intestinal permeability, ciprofloxacin, oleanolic acid, cAMP signaling, TNF-α, TLR4, monocytes, Crohn's disease, DSS-induced colitis, TNBS-induced colitis, lamina propria
- MeSH terms
- Animals, Cholera Toxin, Ciprofloxacin, Colitis, Haptoglobins, Immunity, Intestinal Mucosa, Ligands, Permeability, Protein Precursors, Mice, Knockout, Tight Junctions, Receptors, G-Protein-Coupled, Mice
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