Commensal Akkermansia muciniphila Exacerbates Gut Inflammation in Salmonella Typhimurium-Infected Gnotobiotic Mice
Open accessAbstract
Excessive mucin degradation by intestinal bacteria may contribute to inflammatory bowel diseases because access of luminal antigens to the intestinal immune system is facilitated. This study investigated how the presence of a mucin degrading commensal bacterium affects the severity of an intestinal Salmonella enterica Typhimurium-induced gut inflammation. Using a gnotobiotic C3H mouse model with a background microbiota of eight bacterial species (SIHUMI) the impact of the mucin-degrading commensal bacterium Akkermansia muciniphila (SIHUMI-A) on inflammatory and infectious symptoms caused by S. Typhimurium was investigated. Presence of A. muciniphila in S. Typhimurium-infected SIHUMI mice caused significantly increased histopathology scores and elevated mRNA levels of IFN-γ, IP-10, TNF-α, IL-12, IL-17 and IL-6 in cecal and colonic tissue. The increase in pro-inflammatory cytokines was accompanied by 10-fold higher S. Typhimurium cell numbers in mesenteric lymph nodes of SIHUMI mice associated with A. muciniphila and S. Typhimurium (SIHUMI-AS) compared to SIHUMI mice with S. Typhimurium only (SIHUMI-S). The number of mucin filled goblet cells was 2- to 3-fold lower in cecal tissue of SIHUMI-AS mice compared to SIHUMI-S, SIHUMI-A or SIHUMI mice. Reduced goblet cell numbers significantly correlated with increased IFN-γ mRNA levels (r(2) = -0.86, ***P<0.001) in all infected mice. In addition, loss of cecal mucin sulphation was observed in SIHUMI mice containing both A. muciniphila and S. Typhimurium compared to other mouse groups. Concomitant presence of A. muciniphila and S. Typhimurium resulted in a drastic change in microbiota composition of SIHUMI mice: the proportion of B. thetaiotaomicron in SIHUMI-AS mice was 0.02% of total bacteria compared to 78%-88% in the other mouse groups and the proportion of S. Typhimurium was 94% in SIHUMI-AS mice but only 2.2% in the SIHUMI-S mice. These results indicate that A. muciniphila exacerbates S. Typhimurium-induced intestinal inflammation by its ability to disturb host mucus homeostasis.
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g_Akkermansia has a negative correlation with body mass index (BMI) and a protective effect for the mucus layer in pro-inflammation.
“It has been reported that the abundance of g_Akkermansia has a negative correlation with the value of body mass index (BMI) [59] and that g_Akkermansia has a protective effect for the mucus layer in pro-inflammation [60].”
From Preventive Effects and Mechanisms of Garlic on Dyslipidemia and Gut Microbiome Dysbiosis (2019) · cites this paper as [60]
Citation [60] is attached to the claimed protective effect on the mucus layer, not the BMI correlation attributed to [59]. In the Results section, the paper says A. muciniphila interfered with mucus formation and facilitated pathogen translocation in Salmonella-infected mice; the Discussion says its presence aggravated intestinal inflammatory symptoms. That is contrary to the attributed protective effect in this inflammatory setting. (LLM, conf=0.91)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredAkkermansia can degrade mucin, cause intestinal inflammation and permeability, and increase endotoxemia and systemic inflammation, eventually promoting neuropathology.
“The Gram-negative bacteria, Akkermansia, can degrade mucin, cause intestinal inflammation and permeability, and increase endotoxemia and systemic inflammation, eventually promoting neuropathology [53,54,55].”
From Neuroprotective Effects of Sodium Butyrate by Restoring Gut Microbiota and Inhibiting TLR4 Signaling in Mice with MPTP-Induced Parkinson’s Disease (2023) · cites this paper as [55]
Akkermansia muciniphila's mucin degrading activity might damage the gut-barrier, triggering inflammation and promoting gut permeability.
“its mucin degrading activity might also damage the gut-barrier triggering inflammation and promoting gut permeability [83,84]”
From The Interplay between Gut Microbiota and Parkinson’s Disease: Implications on Diagnosis and Treatment (2022) · cites this paper as [84]
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- Authors
- Ganesh, B. P., Klopfleisch, R., Loh, G., & Blaut, M.
- Affiliations
- German Institute of Human Nutrition (DE)
- Freie Universität Berlin (DE)
- Corresponding author
- Loh, Gunnar
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-09-10
- Volume
- 8
- Issue
- 9
- Pages
- e74963
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3769299
- OpenAlex
- W2085991415
- Cited by
- 522
- References
- 60
- Citations by year
- 2026: 27 · 2025: 47 · 2024: 69 · 2023: 56 · 2022: 59 · 2021: 50 · 2020: 46 · 2019: 41 · 2018: 37 · 2017: 27 · 2016: 36 · 2015: 13 · 2014: 11 · 2013: 2 · 2012: 1
- FWCI
- 9.26
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Refubium (Universitätsbibliothek der Freien Universität Berlin) (submittedVersion, cc-by)
- Universitätsbibliothek der FU Berlin Hochschulschriftenstelle u. Dokumentenserver (cc-by)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- Akkermansia muciniphila, Salmonella typhimurium, intestinal inflammation, mucin degradation, commensal bacteria, gnotobiotic mice, goblet cells, Bacteroides thetaiotaomicron, inflammatory cytokines, interferon-gamma, gut microbiota, Salmonella enteritis
- MeSH terms
- Animals, Germ-Free Life, Inflammation, Interferon-gamma, Interleukin-1, Intestines, Lymph Nodes, Macrophages, Mice, Inbred C3H, RNA, Messenger, Salmonella Infections, Salmonella typhimurium, Symbiosis, Tumor Necrosis Factor-alpha, Interleukin-6, Interleukin-12, Mice, Chemokine CXCL10, Mucin-2, Verrucomicrobia
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