The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation

Tarun Bansal, Robert C. Alaniz, Thomas K. Wood, Arul Jayaraman

Research output: Contribution to journalArticle

232 Citations (Scopus)

Abstract

Interkingdom signaling is established in the gastrointestinal tract in that human hormones trigger responses in bacteria; here, we show that the corollary is true, that a specific bacterial signal, indole, is recognized as a beneficial signal in intestinal epithelial cells. Our prior work has shown that indole, secreted by commensal Escherichia coli and detected in human feces, reduces pathogenic E. coli chemotaxis, motility, and attachment to epithelial cells. However, the effect of indole on intestinal epithelial cells is not known. Because intestinal epithelial cells are likely to be exposed continuously to indole, we hypothesized that indole may be beneficial for these cells, and investigated changes in gene expression with the human enterocyte cell line HCT-8 upon exposure to indole. Exposure to physiologically relevant amounts of indole increased expression of genes involved in strengthening the mucosal barrier and mucin production, which were consistent with an increase in the transepithelial resistance of HCT-8 cells. Indole also decreased TNF-α-mediated activation of NF-κB, expression of the proinflammatory chemokine IL-8, and the attachment of pathogenic E. coli to HCT-8 cells, as well as increased expression of the antiinflammatory cytokine IL-10. The changes in transepithelial resistance and NF-κB activation were specific to indole: other indole-like molecules did not elicit a similar response. Our results are similar to those observed with probiotic strains and suggest that indole could be important in the intestinal epithelial cells response to gastrointestinal tract pathogens.

Original languageEnglish (US)
Pages (from-to)228-233
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume107
Issue number1
DOIs
StatePublished - Feb 15 2010

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Intercellular Junctions
Tight Junctions
Epithelial Cells
Inflammation
Escherichia coli
Gastrointestinal Tract
indole
Gene Expression
Enterocytes
Probiotics
Mucins
Chemotaxis
Interleukin-8
Chemokines
Feces
Interleukin-10
Anti-Inflammatory Agents
Hormones
Cytokines
Bacteria

All Science Journal Classification (ASJC) codes

  • General

Cite this

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abstract = "Interkingdom signaling is established in the gastrointestinal tract in that human hormones trigger responses in bacteria; here, we show that the corollary is true, that a specific bacterial signal, indole, is recognized as a beneficial signal in intestinal epithelial cells. Our prior work has shown that indole, secreted by commensal Escherichia coli and detected in human feces, reduces pathogenic E. coli chemotaxis, motility, and attachment to epithelial cells. However, the effect of indole on intestinal epithelial cells is not known. Because intestinal epithelial cells are likely to be exposed continuously to indole, we hypothesized that indole may be beneficial for these cells, and investigated changes in gene expression with the human enterocyte cell line HCT-8 upon exposure to indole. Exposure to physiologically relevant amounts of indole increased expression of genes involved in strengthening the mucosal barrier and mucin production, which were consistent with an increase in the transepithelial resistance of HCT-8 cells. Indole also decreased TNF-α-mediated activation of NF-κB, expression of the proinflammatory chemokine IL-8, and the attachment of pathogenic E. coli to HCT-8 cells, as well as increased expression of the antiinflammatory cytokine IL-10. The changes in transepithelial resistance and NF-κB activation were specific to indole: other indole-like molecules did not elicit a similar response. Our results are similar to those observed with probiotic strains and suggest that indole could be important in the intestinal epithelial cells response to gastrointestinal tract pathogens.",
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The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation. / Bansal, Tarun; Alaniz, Robert C.; Wood, Thomas K.; Jayaraman, Arul.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 107, No. 1, 15.02.2010, p. 228-233.

Research output: Contribution to journalArticle

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