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

Summary: 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-...

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Main Authors: 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, IV, Andrew L. Kau, Dan Knights, Purna C. Kashyap, Matthew A. Ciorba, Rodney D. Newberry, Chyi-Song Hsieh
Format: Article
Language:English
Published: Elsevier 2020-10-01
Series:Cell Reports Medicine
Subjects:
IgA
Online Access:http://www.sciencedirect.com/science/article/pii/S266637912030166X
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spelling doaj-332b58370fdc4d669d7cafa06882bcf22020-11-25T04:01:29ZengElsevierCell Reports Medicine2666-37912020-10-0117100124A Potential Role for Stress-Induced Microbial Alterations in IgA-Associated Irritable Bowel Syndrome with DiarrheaSunaina Rengarajan0Kathryn A. Knoop1Arvind Rengarajan2Jiani N. Chai3Jose G. Grajales-Reyes4Vijay K. Samineni5Emilie V. Russler-Germain6Prabha Ranganathan7Alessio Fasano8Gregory S. Sayuk9Robert W. Gereau, IV10Andrew L. Kau11Dan Knights12Purna C. Kashyap13Matthew A. Ciorba14Rodney D. Newberry15Chyi-Song Hsieh16Department of Internal Medicine, Division of Rheumatology, Washington University School of Medicine, St. Louis, MO 63110, USADepartment of Internal Medicine, Division of Gastroenterology, Washington University School of Medicine, St. Louis, MO 63110, USADepartment of Internal Medicine, Division of Gastroenterology, Washington University School of Medicine, St. Louis, MO 63110, USADepartment of Internal Medicine, Division of Rheumatology, Washington University School of Medicine, St. Louis, MO 63110, USAWashington University Pain Center and Department of Anesthesiology, Washington University School of Medicine, St. Louis, MO 63110, USAWashington University Pain Center and Department of Anesthesiology, Washington University School of Medicine, St. Louis, MO 63110, USADepartment of Internal Medicine, Division of Rheumatology, Washington University School of Medicine, St. Louis, MO 63110, USADepartment of Internal Medicine, Division of Rheumatology, Washington University School of Medicine, St. Louis, MO 63110, USACenter for Celiac Research and Treatment and Division of Pediatric Gastroenterology and Nutrition, Massachusetts General Hospital, Boston, MA 02114, USADepartment of Internal Medicine, Division of Gastroenterology, Washington University School of Medicine, St. Louis, MO 63110, USA; Gastroenterology Section, John Cochran Veterans Affairs Medical Center, St. Louis, MO 63125, USAWashington University Pain Center and Department of Anesthesiology, Washington University School of Medicine, St. Louis, MO 63110, USACenter for Women’s Infectious Disease Research and Department of Internal Medicine, Division of Allergy and Immunology, Washington University School of Medicine, St. Louis, MO 63110, USABiomedical Informatics and Computational Biology, University of Minnesota, Minneapolis, MN 55455, USADivision of Gastroenterology and Hepatology, Mayo Clinic, Rochester, MN 55905, USADepartment of Internal Medicine, Division of Gastroenterology, Washington University School of Medicine, St. Louis, MO 63110, USADepartment of Internal Medicine, Division of Gastroenterology, Washington University School of Medicine, St. Louis, MO 63110, USADepartment of Internal Medicine, Division of Rheumatology, Washington University School of Medicine, St. Louis, MO 63110, USA; Corresponding authorSummary: 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.http://www.sciencedirect.com/science/article/pii/S266637912030166Xstresshost:commensal immunityIgAirritable bowel syndrome
collection DOAJ
language English
format Article
sources DOAJ
author 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, IV
Andrew L. Kau
Dan Knights
Purna C. Kashyap
Matthew A. Ciorba
Rodney D. Newberry
Chyi-Song Hsieh
spellingShingle 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, IV
Andrew L. Kau
Dan Knights
Purna C. Kashyap
Matthew A. Ciorba
Rodney D. Newberry
Chyi-Song Hsieh
A Potential Role for Stress-Induced Microbial Alterations in IgA-Associated Irritable Bowel Syndrome with Diarrhea
Cell Reports Medicine
stress
host:commensal immunity
IgA
irritable bowel syndrome
author_facet 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, IV
Andrew L. Kau
Dan Knights
Purna C. Kashyap
Matthew A. Ciorba
Rodney D. Newberry
Chyi-Song Hsieh
author_sort Sunaina Rengarajan
title A Potential Role for Stress-Induced Microbial Alterations in IgA-Associated Irritable Bowel Syndrome with Diarrhea
title_short A Potential Role for Stress-Induced Microbial Alterations in IgA-Associated Irritable Bowel Syndrome with Diarrhea
title_full A Potential Role for Stress-Induced Microbial Alterations in IgA-Associated Irritable Bowel Syndrome with Diarrhea
title_fullStr A Potential Role for Stress-Induced Microbial Alterations in IgA-Associated Irritable Bowel Syndrome with Diarrhea
title_full_unstemmed A Potential Role for Stress-Induced Microbial Alterations in IgA-Associated Irritable Bowel Syndrome with Diarrhea
title_sort potential role for stress-induced microbial alterations in iga-associated irritable bowel syndrome with diarrhea
publisher Elsevier
series Cell Reports Medicine
issn 2666-3791
publishDate 2020-10-01
description Summary: 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.
topic stress
host:commensal immunity
IgA
irritable bowel syndrome
url http://www.sciencedirect.com/science/article/pii/S266637912030166X
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