Enterococcus faecium and Pediococcus acidilactici deteriorate Enterobacteriaceae-induced depression and colitis in mice

Abstract Gut dysbiosis is closely associated with the outbreak of inflammatory bowel disease (IBD) and psychiatric disorder. The Enterobacteriaceae population was higher in the feces of patients with inflammatory bowel disease (IBD-F) than in those of healthy control volunteers (HC-F). The Enterococ...

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Main Authors: Hyo-Min Jang, Jeon-Kyung Kim, Min-Kyung Joo, Yoon-Jung Shin, Kyung-Eon Lee, Chang Kyun Lee, Hyo-Jong Kim, Dong-Hyun Kim
Format: Article
Language:English
Published: Nature Portfolio 2022-06-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-022-13629-9
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author Hyo-Min Jang
Jeon-Kyung Kim
Min-Kyung Joo
Yoon-Jung Shin
Kyung-Eon Lee
Chang Kyun Lee
Hyo-Jong Kim
Dong-Hyun Kim
author_facet Hyo-Min Jang
Jeon-Kyung Kim
Min-Kyung Joo
Yoon-Jung Shin
Kyung-Eon Lee
Chang Kyun Lee
Hyo-Jong Kim
Dong-Hyun Kim
author_sort Hyo-Min Jang
collection DOAJ
description Abstract Gut dysbiosis is closely associated with the outbreak of inflammatory bowel disease (IBD) and psychiatric disorder. The Enterobacteriaceae population was higher in the feces of patients with inflammatory bowel disease (IBD-F) than in those of healthy control volunteers (HC-F). The Enterococcaceae and Lactobacillaceae populations were higher in the feces of IBD patients with depression (IBD/D+-F) vs. the feces of IBD patients without depression (IBD/D−-F). Therefore, we examined the effects of Klebsiella oxytoca, Escherichia coli, Cronobacter sakazakii, Enterococcus faecium, and Pediococcus acidolactici overpopulated in IBD/D+-F and their byproducts LPS and exopolysaccharide (EPS) on the occurrence of depression and colitis in mice. Oral gavages of Klebsiella oxytoca, Escherichia coli, and Cronobacter sakazakii belonging to Enterobacteriaceae, singly or together, caused dose-dependently colitis and depression-like behaviors in germ-free and specific-pathogen-free mice. Although Enterococcus faecium and Pediococcus acidolactici did not significantly cause colitis and depression-like behaviors, they significantly deteriorated Klebsiella oxytoca- or Escherichia coli-induced colitis, neuroinflammation, and anxiety/depression-like behaviors and increased blood LPS, corticosterone, and IL-6 levels. The EPSs from Enterococcus faecium and Pediococcus acidolactici also worsened Klebsiella oxytoca LPS-induced colitis, neuroinflammation, and depression-like behaviors in mice and increased the translocation of fluorescein isothiocyanate-conjugated LPS into the hippocampus. However, Bifidobacterium longum, which was lower in IBD/D+-F vs. IBD/D−-F, or its EPS suppressed them. In conclusion, Enterococcus faecium and Pediococcus acidolactici, known as a probiotic strain, and their EPSs may be a risk factor for the outbreak of depression and IBD.
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spelling doaj.art-ba82dd0a9e7c483aa83bd9fc107e09922023-08-13T11:09:08ZengNature PortfolioScientific Reports2045-23222022-06-0112111310.1038/s41598-022-13629-9Enterococcus faecium and Pediococcus acidilactici deteriorate Enterobacteriaceae-induced depression and colitis in miceHyo-Min Jang0Jeon-Kyung Kim1Min-Kyung Joo2Yoon-Jung Shin3Kyung-Eon Lee4Chang Kyun Lee5Hyo-Jong Kim6Dong-Hyun Kim7Neurobiota Research Center, College of Pharmacy, Kyung Hee UniversityNeurobiota Research Center, College of Pharmacy, Kyung Hee UniversityNeurobiota Research Center, College of Pharmacy, Kyung Hee UniversityNeurobiota Research Center, College of Pharmacy, Kyung Hee UniversityNeurobiota Research Center, College of Pharmacy, Kyung Hee UniversityDepartment of Internal Medicine, Kyung Hee University School of MedicineDepartment of Internal Medicine, Kyung Hee University School of MedicineNeurobiota Research Center, College of Pharmacy, Kyung Hee UniversityAbstract Gut dysbiosis is closely associated with the outbreak of inflammatory bowel disease (IBD) and psychiatric disorder. The Enterobacteriaceae population was higher in the feces of patients with inflammatory bowel disease (IBD-F) than in those of healthy control volunteers (HC-F). The Enterococcaceae and Lactobacillaceae populations were higher in the feces of IBD patients with depression (IBD/D+-F) vs. the feces of IBD patients without depression (IBD/D−-F). Therefore, we examined the effects of Klebsiella oxytoca, Escherichia coli, Cronobacter sakazakii, Enterococcus faecium, and Pediococcus acidolactici overpopulated in IBD/D+-F and their byproducts LPS and exopolysaccharide (EPS) on the occurrence of depression and colitis in mice. Oral gavages of Klebsiella oxytoca, Escherichia coli, and Cronobacter sakazakii belonging to Enterobacteriaceae, singly or together, caused dose-dependently colitis and depression-like behaviors in germ-free and specific-pathogen-free mice. Although Enterococcus faecium and Pediococcus acidolactici did not significantly cause colitis and depression-like behaviors, they significantly deteriorated Klebsiella oxytoca- or Escherichia coli-induced colitis, neuroinflammation, and anxiety/depression-like behaviors and increased blood LPS, corticosterone, and IL-6 levels. The EPSs from Enterococcus faecium and Pediococcus acidolactici also worsened Klebsiella oxytoca LPS-induced colitis, neuroinflammation, and depression-like behaviors in mice and increased the translocation of fluorescein isothiocyanate-conjugated LPS into the hippocampus. However, Bifidobacterium longum, which was lower in IBD/D+-F vs. IBD/D−-F, or its EPS suppressed them. In conclusion, Enterococcus faecium and Pediococcus acidolactici, known as a probiotic strain, and their EPSs may be a risk factor for the outbreak of depression and IBD.https://doi.org/10.1038/s41598-022-13629-9
spellingShingle Hyo-Min Jang
Jeon-Kyung Kim
Min-Kyung Joo
Yoon-Jung Shin
Kyung-Eon Lee
Chang Kyun Lee
Hyo-Jong Kim
Dong-Hyun Kim
Enterococcus faecium and Pediococcus acidilactici deteriorate Enterobacteriaceae-induced depression and colitis in mice
Scientific Reports
title Enterococcus faecium and Pediococcus acidilactici deteriorate Enterobacteriaceae-induced depression and colitis in mice
title_full Enterococcus faecium and Pediococcus acidilactici deteriorate Enterobacteriaceae-induced depression and colitis in mice
title_fullStr Enterococcus faecium and Pediococcus acidilactici deteriorate Enterobacteriaceae-induced depression and colitis in mice
title_full_unstemmed Enterococcus faecium and Pediococcus acidilactici deteriorate Enterobacteriaceae-induced depression and colitis in mice
title_short Enterococcus faecium and Pediococcus acidilactici deteriorate Enterobacteriaceae-induced depression and colitis in mice
title_sort enterococcus faecium and pediococcus acidilactici deteriorate enterobacteriaceae induced depression and colitis in mice
url https://doi.org/10.1038/s41598-022-13629-9
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