Cited by 405Gut microbiota and healthBacterial biofilms and quorum sensingGastrointestinal motility and disorders

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Commensal Bacteria-Dependent Indole Production Enhances Epithelial Barrier Function in the Colon

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Shimada, Yosuke, Kinoshita, Makoto, Harada, Kazuo, Mizutani, Masafumi, Masahata, Kazunori, Kayama, Hisako, Takeda, Kiyoshi·2013·PLoS ONE

DOI 10.1371/journal.pone.0080604PMC PMC3835565

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Abstract

Microbiota have been shown to have a great influence on functions of intestinal epithelial cells (ECs). The role of indole as a quorum-sensing (QS) molecule mediating intercellular signals in bacteria has been well appreciated. However, it remains unknown whether indole has beneficial effects on maintaining intestinal barriers in vivo. In this study, we analyzed the effect of indole on ECs using a germ free (GF) mouse model. GF mice showed decreased expression of junctional complex molecules in colonic ECs. The feces of specific pathogen-free (SPF) mice contained a high amount of indole; however the amount was significantly decreased in the feces of GF mice by 27-fold. Oral administration of indole-containing capsules resulted in increased expression of both tight junction (TJ)- and adherens junction (AJ)-associated molecules in colonic ECs in GF mice. In accordance with the increased expression of these junctional complex molecules, GF mice given indole-containing capsules showed higher resistance to dextran sodium sulfate (DSS)-induced colitis. A similar protective effect of indole on DSS-induced epithelial damage was also observed in mice bred in SPF conditions. These findings highlight the beneficial role of indole in establishing an epithelial barrier in vivo.

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Additional file 3 of Indoleacrylic acid produced by Parabacteroides distasonis alleviates type 2 diabetes via activation of AhR to repair intestinal barrier
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Additional file 9 of Indoleacrylic acid produced by Parabacteroides distasonis alleviates type 2 diabetes via activation of AhR to repair intestinal barrier
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Additional file 2 of Gut microbiota-derived 3-phenylpropionic acid promotes intestinal epithelial barrier function via AhR signaling
Hu, J., Chen, J., Xu, X., Hou, Q., Ren, J., & Yan, X. (2023) · Figshare · doi:10.6084/m9.figshare.22790384
Additional file 7 of Gut microbiota-derived 3-phenylpropionic acid promotes intestinal epithelial barrier function via AhR signaling
Hu, J., Chen, J., Xu, X., Hou, Q., Ren, J., & Yan, X. (2023) · Figshare · doi:10.6084/m9.figshare.22790399
Additional file 6 of Indoleacrylic acid produced by Parabacteroides distasonis alleviates type 2 diabetes via activation of AhR to repair intestinal barrier
Liu, D., Zhang, S., Li, S., Zhang, Q., Cai, Y., Li, P., Li, H., Shen, B., Liao, Q., Hong, Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26583225
Additional file 4 of Indoleacrylic acid produced by Parabacteroides distasonis alleviates type 2 diabetes via activation of AhR to repair intestinal barrier
Liu, D., Zhang, S., Li, S., Zhang, Q., Cai, Y., Li, P., Li, H., Shen, B., Liao, Q., Hong, Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26583219
Additional file 14 of Gut microbiota-derived 3-phenylpropionic acid promotes intestinal epithelial barrier function via AhR signaling
Hu, J., Chen, J., Xu, X., Hou, Q., Ren, J., & Yan, X. (2023) · Figshare · doi:10.6084/m9.figshare.22790420
Additional file 6 of Gut microbiota-derived 3-phenylpropionic acid promotes intestinal epithelial barrier function via AhR signaling
Hu, J., Chen, J., Xu, X., Hou, Q., Ren, J., & Yan, X. (2023) · Figshare · doi:10.6084/m9.figshare.22790396
Additional file 1 of Gut microbiota-derived 3-phenylpropionic acid promotes intestinal epithelial barrier function via AhR signaling
Hu, J., Chen, J., Xu, X., Hou, Q., Ren, J., & Yan, X. (2023) · Figshare · doi:10.6084/m9.figshare.22790381
Additional file 5 of Indoleacrylic acid produced by Parabacteroides distasonis alleviates type 2 diabetes via activation of AhR to repair intestinal barrier
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Additional file 7 of Indoleacrylic acid produced by Parabacteroides distasonis alleviates type 2 diabetes via activation of AhR to repair intestinal barrier
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Additional file 11 of Gut microbiota-derived 3-phenylpropionic acid promotes intestinal epithelial barrier function via AhR signaling
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Additional file 8 of Indoleacrylic acid produced by Parabacteroides distasonis alleviates type 2 diabetes via activation of AhR to repair intestinal barrier
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Additional file 8 of Gut microbiota-derived 3-phenylpropionic acid promotes intestinal epithelial barrier function via AhR signaling
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Additional file 2 of Metabolites mediate the causal associations between gut microbiota and NAFLD: a Mendelian randomization study
Ouyang, C., Liu, P., Liu, Y., Lan, J., & Liu, Q. (2024) · Figshare · doi:10.6084/m9.figshare.26420546
Additional file 2 of Indoleacrylic acid produced by Parabacteroides distasonis alleviates type 2 diabetes via activation of AhR to repair intestinal barrier
Liu, D., Zhang, S., Li, S., Zhang, Q., Cai, Y., Li, P., Li, H., Shen, B., Liao, Q., Hong, Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26583213
Additional file 10 of Gut microbiota-derived 3-phenylpropionic acid promotes intestinal epithelial barrier function via AhR signaling
Hu, J., Chen, J., Xu, X., Hou, Q., Ren, J., & Yan, X. (2023) · Figshare · doi:10.6084/m9.figshare.22790408
Additional file 4 of Gut microbiota-derived 3-phenylpropionic acid promotes intestinal epithelial barrier function via AhR signaling
Hu, J., Chen, J., Xu, X., Hou, Q., Ren, J., & Yan, X. (2023) · Figshare · doi:10.6084/m9.figshare.22790390
Additional file 13 of Gut microbiota-derived 3-phenylpropionic acid promotes intestinal epithelial barrier function via AhR signaling
Hu, J., Chen, J., Xu, X., Hou, Q., Ren, J., & Yan, X. (2023) · Figshare · doi:10.6084/m9.figshare.22790417
Additional file 9 of Gut microbiota-derived 3-phenylpropionic acid promotes intestinal epithelial barrier function via AhR signaling
Hu, J., Chen, J., Xu, X., Hou, Q., Ren, J., & Yan, X. (2023) · Figshare · doi:10.6084/m9.figshare.22790405
Additional file 10 of Indoleacrylic acid produced by Parabacteroides distasonis alleviates type 2 diabetes via activation of AhR to repair intestinal barrier
Liu, D., Zhang, S., Li, S., Zhang, Q., Cai, Y., Li, P., Li, H., Shen, B., Liao, Q., Hong, Y., et al. (2023) · Figshare · doi:10.6084/m9.figshare.26583237
Additional file 1 of Indoleacrylic acid produced by Parabacteroides distasonis alleviates type 2 diabetes via activation of AhR to repair intestinal barrier
Liu, D., Zhang, S., Li, S., Zhang, Q., Cai, Y., Li, P., Li, H., Shen, B., Liao, Q., Hong, Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26583210
Additional file 12 of Gut microbiota-derived 3-phenylpropionic acid promotes intestinal epithelial barrier function via AhR signaling
Hu, J., Chen, J., Xu, X., Hou, Q., Ren, J., & Yan, X. (2023) · Figshare · doi:10.6084/m9.figshare.22790414
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Authors: Shimada, Y., Kinoshita, M., Harada, K., Mizutani, M., Masahata, K., Kayama, H., & Takeda, K.
Affiliations: Immunology Frontier Research Center, The University of Osaka (JP)
Japan Science and Technology Agency (JP)
The University of Osaka (JP)
Morishita Jintan (Japan) (JP)
Corresponding author: Takeda, Kiyoshi
ORCID: Kinoshita, Makoto
Harada, Kazuo
Masahata, Kazunori
Kayama, Hisako
Takeda, Kiyoshi
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2013-11-20
Volume: 8
Issue: 11
Pages: e80604
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0080604
PMC: PMC3835565
OpenAlex: W2040501063
Cited by: 404
References: 41
Citations by year: 2026: 23 · 2025: 43 · 2024: 50 · 2023: 53 · 2022: 44 · 2021: 47 · 2020: 34 · 2019: 27 · 2018: 24 · 2017: 23 · 2016: 15 · 2015: 15 · 2014: 6
FWCI: 5.37
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/3.0/ (vor)
Locations: PLoS ONE (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Figshare (submittedVersion, cc-by)
Funders: Ministry of Education, Culture, Sports, Science and Technology
Ministry of Health, Labour and Welfare
Japan Society for the Promotion of Science (24390120)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Keywords: indole, commensal bacteria, intestinal epithelial barrier, tight junctions, adherens junctions, quorum sensing, germ-free mice, DSS-induced colitis, colonic epithelial cells, gut microbiota, epithelial permeability
MeSH terms: Animals, Bacteria, Chromatography, High Pressure Liquid, Colon, Germ-Free Life, Indoles, Intestinal Mucosa, Mice, Tandem Mass Spectrometry, Real-Time Polymerase Chain Reaction

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Commensal Bacteria-Dependent Indole Production Enhances Epithelial Barrier Function in the Colon

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