A Potential Role for Stress-Induced Microbial Alterations in IgA-Associated Irritable Bowel Syndrome with Diarrhea

Sunaina Rengarajan; Kathryn A. Knoop; Arvind Rengarajan; Jiani N. Chai; Jose G. Grajales-Reyes; Vijay K. Samineni; Emilie V. Russler-Germain; Prabha Ranganathan; Alessio Fasano; Gregory S. Sayuk; Robert W. Gereau; Andrew L. Kau; Dan Knights; Purna C. Kashyap; Matthew A. Ciorba; Rodney D. Newberry; Chyi Song Hsieh

doi:10.1016/j.xcrm.2020.100124

A Potential Role for Stress-Induced Microbial Alterations in IgA-Associated Irritable Bowel Syndrome with Diarrhea

Sunaina Rengarajan, Kathryn A. Knoop, Arvind Rengarajan, Jiani N. Chai, Jose G. Grajales-Reyes, Vijay K. Samineni, Emilie V. Russler-Germain, Prabha Ranganathan, Alessio Fasano, Gregory S. Sayuk, Robert W. Gereau, Andrew L. Kau, Dan Knights, Purna C. Kashyap, Matthew A. Ciorba, Rodney D. Newberry, Chyi Song Hsieh

Research output: Contribution to journal › Article › peer-review

1 Scopus citations

Abstract

Stress is a known trigger for flares of inflammatory bowel disease (IBD) and irritable bowel syndrome (IBS); however, this process is not well understood. Here, we find that restraint stress in mice leads to signs of diarrhea, fecal dysbiosis, and a barrier defect via the opening of goblet-cell associated passages. Notably, stress increases host immunity to gut bacteria as assessed by immunoglobulin A (IgA)-bound gut bacteria. Stress-induced microbial changes are necessary and sufficient to elicit these effects. Moreover, similar to mice, many diarrhea-predominant IBS (IBS-D) patients from two cohorts display increased antibacterial immunity as assessed by IgA-bound fecal bacteria. This antibacterial IgA response in IBS-D correlates with somatic symptom severity and was distinct from healthy controls or IBD patients. These findings suggest that stress may play an important role in patients with IgA-associated IBS-D by disrupting the intestinal microbial community that alters gastrointestinal function and host immunity to commensal bacteria.

Original language	English (US)
Article number	100124
Journal	Cell Reports Medicine
Volume	1
Issue number	7
DOIs	https://doi.org/10.1016/j.xcrm.2020.100124
State	Published - Oct 20 2020

Keywords

IgA
host:commensal immunity
irritable bowel syndrome
stress

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.xcrm.2020.100124

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Rengarajan, S., Knoop, K. A., Rengarajan, A., Chai, J. N., Grajales-Reyes, J. G., Samineni, V. K., Russler-Germain, E. V., Ranganathan, P., Fasano, A., Sayuk, G. S., Gereau, R. W., Kau, A. L., Knights, D., Kashyap, P. C., Ciorba, M. A., Newberry, R. D., & Hsieh, C. S. (2020). A Potential Role for Stress-Induced Microbial Alterations in IgA-Associated Irritable Bowel Syndrome with Diarrhea. Cell Reports Medicine, 1(7), Article 100124. https://doi.org/10.1016/j.xcrm.2020.100124

Rengarajan, S, Knoop, KA, Rengarajan, A, Chai, JN, Grajales-Reyes, JG, Samineni, VK, Russler-Germain, EV, Ranganathan, P, Fasano, A, Sayuk, GS, Gereau, RW, Kau, AL, Knights, D, Kashyap, PC, Ciorba, MA, Newberry, RD & Hsieh, CS 2020, 'A Potential Role for Stress-Induced Microbial Alterations in IgA-Associated Irritable Bowel Syndrome with Diarrhea', Cell Reports Medicine, vol. 1, no. 7, 100124. https://doi.org/10.1016/j.xcrm.2020.100124

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abstract = "Stress is a known trigger for flares of inflammatory bowel disease (IBD) and irritable bowel syndrome (IBS); however, this process is not well understood. Here, we find that restraint stress in mice leads to signs of diarrhea, fecal dysbiosis, and a barrier defect via the opening of goblet-cell associated passages. Notably, stress increases host immunity to gut bacteria as assessed by immunoglobulin A (IgA)-bound gut bacteria. Stress-induced microbial changes are necessary and sufficient to elicit these effects. Moreover, similar to mice, many diarrhea-predominant IBS (IBS-D) patients from two cohorts display increased antibacterial immunity as assessed by IgA-bound fecal bacteria. This antibacterial IgA response in IBS-D correlates with somatic symptom severity and was distinct from healthy controls or IBD patients. These findings suggest that stress may play an important role in patients with IgA-associated IBS-D by disrupting the intestinal microbial community that alters gastrointestinal function and host immunity to commensal bacteria.",

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AU - Ranganathan, Prabha

AU - Fasano, Alessio

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AU - Gereau, Robert W.

AU - Kau, Andrew L.

AU - Knights, Dan

AU - Kashyap, Purna C.

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AU - Newberry, Rodney D.

AU - Hsieh, Chyi Song

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AB - Stress is a known trigger for flares of inflammatory bowel disease (IBD) and irritable bowel syndrome (IBS); however, this process is not well understood. Here, we find that restraint stress in mice leads to signs of diarrhea, fecal dysbiosis, and a barrier defect via the opening of goblet-cell associated passages. Notably, stress increases host immunity to gut bacteria as assessed by immunoglobulin A (IgA)-bound gut bacteria. Stress-induced microbial changes are necessary and sufficient to elicit these effects. Moreover, similar to mice, many diarrhea-predominant IBS (IBS-D) patients from two cohorts display increased antibacterial immunity as assessed by IgA-bound fecal bacteria. This antibacterial IgA response in IBS-D correlates with somatic symptom severity and was distinct from healthy controls or IBD patients. These findings suggest that stress may play an important role in patients with IgA-associated IBS-D by disrupting the intestinal microbial community that alters gastrointestinal function and host immunity to commensal bacteria.

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A Potential Role for Stress-Induced Microbial Alterations in IgA-Associated Irritable Bowel Syndrome with Diarrhea

Abstract

Keywords

ASJC Scopus subject areas

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