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Segmented Filamentous Bacteria Are Potent Stimuli of a Physiologically Normal State of the Murine Gut Mucosal Immune System
Open accessAbstract
Segmented filamentous bacteria (SFB) are autochthonous bacteria inhabiting the intestinal tracts of many species, including humans. We studied the effect of SFB on the mucosal immune system by monoassociating formerly germfree C3H/HeN mice with SFB. At various time points during 190 days of colonization, fragment cultures of small intestine and Peyer's patches (PP) were analyzed for total immunoglobulin A (IgA) and SFB-specific IgA production. Also, phenotypic changes indicating germinal center reactions (GCRs) and the activation of CD4(+) T cells in PP were determined by using fluorescence-activated cell sorter analyses. A second group of SFB-monoassociated mice was colonized with a gram-negative commensal, Morganella morganii, to determine if the mucosal immune system was again stimulated and to evaluate the effect of prior colonization with SFB on the ability of M. morganii to translocate to the spleen and mesenteric lymph nodes. We found that SFB stimulated GCRs in PP from day 6 after monoassociation, that GCRs only gradually waned over the entire length of colonization, that natural IgA production was increased to levels 24 to 63% of that of conventionally reared mice, and that SFB-specific IgA was produced but accounted for less than 1.4% of total IgA. Also, the proportion of CD4(+), CD45RBlow T cells, indicative of activated cells, gradually increased in the PP to the level found in conventionally reared mice. Secondary colonization with M. morganii was able to stimulate GCRs anew, leading to a specific IgA antibody response. Previous stimulation of mucosal immunity by SFB did not prevent the translocation of M. morganii in the double-colonized mice. Our findings generally indicate that SFB are one of the single most potent microbial stimuli of the gut mucosal immune system.
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“segmented filamentous bacteria are critical promoters of intestinal mucosal IgA production (39, 40)and Th17 cell induction (41, 42)”
From Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. (2018) · cites this paper as [40]
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Self-citation
Metadata
- Authors
- Talham, G. L., Jiang, H.-Q., Bos, N. A., & Cebra, J. J.
- Affiliations
- University of Pennsylvania (US)
- University of Groningen (NL)
- ORCID
- Bos, Nicolaas A.
- Venue
- Infection and Immunity
- Publisher
- American Society for Microbiology
- Published
- 1999-04
- Volume
- 67
- Issue
- 4
- Pages
- 1992-2000
- ISSN
- 0019-9567 (ISSN-L)
- 1098-5522
- PMC
- PMC96557
- OpenAlex
- W2106689062
- Cited by
- 408
- References
- 23
- Citations by year
- 2026: 8 · 2025: 16 · 2024: 14 · 2023: 16 · 2022: 15 · 2021: 22 · 2020: 21 · 2019: 13 · 2018: 17 · 2017: 12 · 2016: 24 · 2015: 22 · 2014: 30 · 2013: 29 · 2012: 25
- FWCI
- 1.72
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Infection and Immunity (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Funders
- National Institutes of Health (5r01ai035936-04)
- National Institute of Allergy and Infectious Diseases (AI37108, R37AI037108, R01AI037108, AI-35936)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- segmented filamentous bacteria, gut mucosal immunity, immunoglobulin A, Peyer's patches, germinal center reaction, CD4+ T cell activation, Morganella morganii, commensal bacteria, bacterial translocation, germ-free mice, secondary colonization, small intestine
- MeSH terms
- Animals, Clostridium, Enterobacteriaceae, Female, Intestinal Mucosa, Lymph Nodes, Mesentery, Mice, Inbred BALB C, Mice, Inbred C3H, Spleen, Germinal Center, Mice
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