Cited by 214Inflammatory Bowel DiseaseGut microbiota and healthImmune Response and Inflammation

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Shift Towards Pro-inflammatory Intestinal Bacteria Aggravates Acute Murine Colitis via Toll-like Receptors 2 and 4

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Heimesaat, Markus M., Fischer, André, Siegmund, Britta, Kupz, Andreas, Niebergall, Julia, Fuchs, David, Jahn, Hannah-Katharina, Freudenberg, Marina, Loddenkemper, Christoph, Batra, Arvind, Lehr, Hans-Anton, Liesenfeld, Oliver, Blaut, Michael, Göbel, Ulf B., Schumann, Ralf R., Bereswill, Stefan·2007·PLoS ONE

DOI 10.1371/journal.pone.0000662PMC PMC1914380

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Abstract

BACKGROUND: Gut bacteria trigger colitis in animal models and are suspected to aggravate inflammatory bowel diseases. We have recently reported that Escherichia coli accumulates in murine ileitis and exacerbates small intestinal inflammation via Toll-like receptor (TLR) signaling. METHODOLOGY AND PRINCIPAL FINDINGS: Because knowledge on shifts in the intestinal microflora during colitis is limited, we performed a global survey of the colon flora of C57BL/10 wild-type (wt), TLR2(-/-), TLR4(-/-), and TLR2/4(-/-) mice treated for seven days with 3.5% dextrane-sulfate-sodium (DSS). As compared to wt animals, TLR2(-/-), TLR4(-/-), and TLR2/4(-/-) mice displayed reduced macroscopic signs of acute colitis and the amelioration of inflammation was associated with reduced IFN-gamma levels in mesenteric lymph nodes, lower amounts of neutrophils, and less FOXP3-positive T-cells in the colon in situ. During acute colitis E. coli increased in wt and TLR-deficient mice (P<0.05), but the final numbers reached were significantly lower in TLR2(-/-), TLR4(-/-) and TLR2/4(-/-) animals, as compared to wt controls (P<0.01). Concentrations of Bacteroides/ Prevotella spp., and enterococci did not increase during colitis, but their numbers were significantly reduced in the colon of DSS-treated TLR2/4(-/-) animals (P<0.01). Numbers of lactobacilli and clostridia remained unaffected by colitis, irrespective of the TLR-genotype of mice. Culture-independent molecular analyses confirmed the microflora shifts towards enterobacteria during colitis and showed that the gut flora composition was similar in both, healthy wt and TLR-deficient animals. CONCLUSIONS AND SIGNIFICANCE: DSS-induced colitis is characterized by a shift in the intestinal microflora towards pro-inflammatory Gram-negative bacteria. Bacterial products exacerbate acute inflammation via TLR2- and TLR4-signaling and direct the recruitment of neutrophils and regulatory T-cells to intestinal sites. E. coli may serve as a biomarker for colitis severity and DSS-induced barrier damage seems to be a valuable model to further identify bacterial factors involved in maintaining intestinal homeostasis and to test therapeutic interventions based upon anti-TLR strategies.

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Authors: Heimesaat, M. M., Fischer, A., Siegmund, B., Kupz, A., Niebergall, J., Fuchs, D., Jahn, H.-K., Freudenberg, M., Loddenkemper, C., Batra, A., Lehr, H.-A., Liesenfeld, O., Blaut, M., Göbel, U. B., Schumann, R. R., & Bereswill, S.
Affiliations: Charité – Universitätsmedizin Berlin (DE)
Max Planck Society (DE)
Centre Hospitalier Universitaire Vaudois (CH)
Corresponding author: Bereswill, Stefan
ORCID: Heimesaat, Markus M.
Fischer, André
Siegmund, Britta
Kupz, Andreas
Fuchs, David
Freudenberg, Marina
Loddenkemper, Christoph
Lehr, Hans-Anton
Liesenfeld, Oliver
Bereswill, Stefan
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2007-07-25
Volume: 2
Issue: 7
Pages: e662
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0000662
PMC: PMC1914380
OpenAlex: W2065205410
Cited by: 213
References: 36
Citations by year: 2026: 3 · 2025: 2 · 2024: 4 · 2023: 10 · 2022: 6 · 2021: 11 · 2020: 7 · 2019: 12 · 2018: 7 · 2017: 11 · 2016: 8 · 2015: 16 · 2014: 16 · 2013: 16 · 2012: 26
FWCI: 6.09
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS ONE (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
SERVAL (Université de Lausanne) (publishedVersion, other-oa)
ResearchOnline - JCU (James Cook University) (submittedVersion)
IRIS (submittedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Max Planck Digital Library (submittedVersion)
MPG.PuRe (Max Planck Society) (submittedVersion)
Funders: Sonnenfeld Stiftung
Deutsche Forschungsgemeinschaft (KFO104, SFB633, Project 6, SPP1110)
Topics: Health Sciences › Medicine › Gastroenterology › Inflammatory Bowel Disease
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Keywords: acute colitis, gut microbiota, TLR2, TLR4, Escherichia coli, DSS-induced colitis, Gram-negative bacteria, neutrophil recruitment, regulatory T cells, interferon-gamma, Bacteroides-Prevotella, Enterococcus, intestinal barrier injury, inflammatory bowel disease
MeSH terms: Acute Disease, Animals, Bacterial Infections, Colitis, Colon, Humans, Inflammation, Mice, Inbred C57BL, Neutrophils, Inflammatory Bowel Diseases, Signal Transduction, Toll-Like Receptor 2, Toll-Like Receptor 4, Mice

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Shift Towards Pro-inflammatory Intestinal Bacteria Aggravates Acute Murine Colitis via Toll-like Receptors 2 and 4

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