Inflammatory Immune Responses and Gut Microbiota Changes Following <i>Campylobacter coli</i> Infection of IL-10<sup>-/-</sup> Mice with Chronic Colitis

Human infections with the food-borne enteropathogens <i>Campylobacter</i> are progressively rising. Recent evidence revealed that pre-existing intestinal inflammation facilitates enteropathogenic infection subsequently exacerbating the underlying disease. Given that only little is known...

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Main Authors: Markus M. Heimesaat, Claudia Genger, Nina Biesemeier, Sigri Klove, Dennis Weschka, Soraya Mousavi, Stefan Bereswill
Format: Article
Language:English
Published: MDPI AG 2020-07-01
Series:Pathogens
Subjects:
Online Access:https://www.mdpi.com/2076-0817/9/7/560
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author Markus M. Heimesaat
Claudia Genger
Nina Biesemeier
Sigri Klove
Dennis Weschka
Soraya Mousavi
Stefan Bereswill
author_facet Markus M. Heimesaat
Claudia Genger
Nina Biesemeier
Sigri Klove
Dennis Weschka
Soraya Mousavi
Stefan Bereswill
author_sort Markus M. Heimesaat
collection DOAJ
description Human infections with the food-borne enteropathogens <i>Campylobacter</i> are progressively rising. Recent evidence revealed that pre-existing intestinal inflammation facilitates enteropathogenic infection subsequently exacerbating the underlying disease. Given that only little is known about <i>C. coli</i>–host interactions and particularly during intestinal inflammation, the aim of the present study was to survey gastrointestinal colonization properties, gut microbiota changes and pro-inflammatory sequelae upon peroral <i>C. coli</i>-infection of IL-10<sup>-/-</sup> mice with chronic colitis. <i>C. coli</i> colonized the gastrointestinal tract of mice with varying efficiencies until day 28 post-infection and induced macroscopic and microscopic inflammatory changes as indicated by shorter colonic lengths, more distinct histopathological changes in the colonic mucosa and higher numbers of apoptotic colonic epithelial cells when compared to mock-infected controls. Furthermore, not only colonic innate and adaptive immune cell responses, but also enhanced systemic TNF-α secretion could be observed following <i>C. coli</i> as opposed to mock challenge. Notably, <i>C. coli</i> induced intestinal inflammatory sequelae were accompanied with gut microbiota shifts towards higher commensal enterobacterial loads in the infected gut lumen. Moreover, the pathogen translocated from the intestinal tract to extra-intestinal tissue sites in some cases, but never to systemic compartments. Hence, <i>C. coli</i> accelerates inflammatory immune responses in IL-10<sup>-/-</sup> mice with chronic colitis.
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spelling doaj.art-f7cb62c97d244a7491d7df97c3a876012023-11-20T06:31:29ZengMDPI AGPathogens2076-08172020-07-019756010.3390/pathogens9070560Inflammatory Immune Responses and Gut Microbiota Changes Following <i>Campylobacter coli</i> Infection of IL-10<sup>-/-</sup> Mice with Chronic ColitisMarkus M. Heimesaat0Claudia Genger1Nina Biesemeier2Sigri Klove3Dennis Weschka4Soraya Mousavi5Stefan Bereswill6Institute of Microbiology, Infectious Diseases and Immunology, Charité—University Medicine Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, 12203 Berlin, GermanyInstitute of Microbiology, Infectious Diseases and Immunology, Charité—University Medicine Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, 12203 Berlin, GermanyInstitute of Microbiology, Infectious Diseases and Immunology, Charité—University Medicine Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, 12203 Berlin, GermanyInstitute of Microbiology, Infectious Diseases and Immunology, Charité—University Medicine Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, 12203 Berlin, GermanyInstitute of Microbiology, Infectious Diseases and Immunology, Charité—University Medicine Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, 12203 Berlin, GermanyInstitute of Microbiology, Infectious Diseases and Immunology, Charité—University Medicine Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, 12203 Berlin, GermanyInstitute of Microbiology, Infectious Diseases and Immunology, Charité—University Medicine Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, 12203 Berlin, GermanyHuman infections with the food-borne enteropathogens <i>Campylobacter</i> are progressively rising. Recent evidence revealed that pre-existing intestinal inflammation facilitates enteropathogenic infection subsequently exacerbating the underlying disease. Given that only little is known about <i>C. coli</i>–host interactions and particularly during intestinal inflammation, the aim of the present study was to survey gastrointestinal colonization properties, gut microbiota changes and pro-inflammatory sequelae upon peroral <i>C. coli</i>-infection of IL-10<sup>-/-</sup> mice with chronic colitis. <i>C. coli</i> colonized the gastrointestinal tract of mice with varying efficiencies until day 28 post-infection and induced macroscopic and microscopic inflammatory changes as indicated by shorter colonic lengths, more distinct histopathological changes in the colonic mucosa and higher numbers of apoptotic colonic epithelial cells when compared to mock-infected controls. Furthermore, not only colonic innate and adaptive immune cell responses, but also enhanced systemic TNF-α secretion could be observed following <i>C. coli</i> as opposed to mock challenge. Notably, <i>C. coli</i> induced intestinal inflammatory sequelae were accompanied with gut microbiota shifts towards higher commensal enterobacterial loads in the infected gut lumen. Moreover, the pathogen translocated from the intestinal tract to extra-intestinal tissue sites in some cases, but never to systemic compartments. Hence, <i>C. coli</i> accelerates inflammatory immune responses in IL-10<sup>-/-</sup> mice with chronic colitis.https://www.mdpi.com/2076-0817/9/7/560<i>Campylobacter coli</i>murine chronic colitishost-pathogen interactionaged IL-10<sup>-/-</sup> miceintestinal immunopathologybacterial colonization
spellingShingle Markus M. Heimesaat
Claudia Genger
Nina Biesemeier
Sigri Klove
Dennis Weschka
Soraya Mousavi
Stefan Bereswill
Inflammatory Immune Responses and Gut Microbiota Changes Following <i>Campylobacter coli</i> Infection of IL-10<sup>-/-</sup> Mice with Chronic Colitis
Pathogens
<i>Campylobacter coli</i>
murine chronic colitis
host-pathogen interaction
aged IL-10<sup>-/-</sup> mice
intestinal immunopathology
bacterial colonization
title Inflammatory Immune Responses and Gut Microbiota Changes Following <i>Campylobacter coli</i> Infection of IL-10<sup>-/-</sup> Mice with Chronic Colitis
title_full Inflammatory Immune Responses and Gut Microbiota Changes Following <i>Campylobacter coli</i> Infection of IL-10<sup>-/-</sup> Mice with Chronic Colitis
title_fullStr Inflammatory Immune Responses and Gut Microbiota Changes Following <i>Campylobacter coli</i> Infection of IL-10<sup>-/-</sup> Mice with Chronic Colitis
title_full_unstemmed Inflammatory Immune Responses and Gut Microbiota Changes Following <i>Campylobacter coli</i> Infection of IL-10<sup>-/-</sup> Mice with Chronic Colitis
title_short Inflammatory Immune Responses and Gut Microbiota Changes Following <i>Campylobacter coli</i> Infection of IL-10<sup>-/-</sup> Mice with Chronic Colitis
title_sort inflammatory immune responses and gut microbiota changes following i campylobacter coli i infection of il 10 sup sup mice with chronic colitis
topic <i>Campylobacter coli</i>
murine chronic colitis
host-pathogen interaction
aged IL-10<sup>-/-</sup> mice
intestinal immunopathology
bacterial colonization
url https://www.mdpi.com/2076-0817/9/7/560
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