Abstract
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.
MeSH Terms
Animals
Clostridium/immunology
Enterobacteriaceae/immunology
Female
Germinal Center
Intestinal Mucosa/immunology
Lymph Nodes/immunology
Mesentery
Mice
Mice, Inbred BALB C
Mice, Inbred C3H
Spleen/immunology
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Talham G L
Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA.
Jiang H Q
Bos N A
Cebra J J
References (22)
22 references, click to expand
-
The influence of exogenous antigenic stimulation on the specificity repertoire of background immunoglobulin-secreting cells of different isotypes.
Cell Immunol. 1988 Apr 1;112(2):371-80
PMID: 2451571
-
Comparison of 16S rRNA sequences of segmented filamentous bacteria isolated from mice, rats, and chickens and proposal of "Candidatus Arthromitus".
Int J Syst Bacteriol. 1995 Oct;45(4):780-2
PMID: 7547299
-
Commensal enteric bacteria engender a self-limiting humoral mucosal immune response while permanently colonizing the gut.
Infect Immun. 1995 Oct;63(10):3904-13
PMID: 7558298
-
CD4+ T cells reactive to enteric bacterial antigens in spontaneously colitic C3H/HeJBir mice: increased T helper cell type 1 response and ability to transfer disease.
J Exp Med. 1998 Mar 16;187(6):855-64
PMID: 9500788
-
Apathogenic, intestinal, segmented, filamentous bacteria stimulate the mucosal immune system of mice.
Infect Immun. 1993 Jan;61(1):303-6
PMID: 8418051
-
Segmented filamentous bacteria in the rodent small intestine: Their colonization of growing animals and possible role in host resistance toSalmonella.
Microb Ecol. 1982 Oct;8(2):181-90
PMID: 24225812
-
Mono-association of mice with non-cultivable, intestinal, segmented, filamentous bacteria.
Arch Microbiol. 1991;156(2):148-51
PMID: 1838241
-
Patterns of isotype expression by B cell clones responding to thymus-dependent and thymus-independent antigens in vitro.
Eur J Immunol. 1982 Apr;12(4):342-8
PMID: 6980124
-
The preference for switching to IgA expression by Peyer's patch germinal center B cells is likely due to the intrinsic influence of their microenvironment.
J Immunol. 1991 Dec 15;147(12):4126-35
PMID: 1753088
-
Mucosal immunology: new frontiers.
Immunol Today. 1996 Feb;17(2):57-9
PMID: 8808050
-
Use of Peyer's patch and lymph node fragment cultures to compare local immune responses to Morganella morganii.
Infect Immun. 1991 Mar;59(3):1024-31
PMID: 1825484
-
Long-term CD4+ memory T cells from the spleen lack MEL-14, the lymph node homing receptor.
J Immunol. 1992 Jan 15;148(2):324-31
PMID: 1345918
-
Habitat, succession, attachment, and morphology of segmented, filamentous microbes indigenous to the murine gastrointestinal tract.
Infect Immun. 1974 Oct;10(4):948-56
PMID: 4426712
-
Increase in the population of duodenal immunoglobulin A plasmocytes in axenic mice associated with different living or dead bacterial strains of intestinal origin.
Infect Immun. 1978 Aug;21(2):532-9
PMID: 357289
-
Interactions between gut-associated lymphoid tissue and colonization levels of indigenous, segmented, filamentous bacteria in the small intestine of mice.
Can J Microbiol. 1998 Dec;44(12):1177-82
PMID: 10347864
-
Functional and ontogenetic analysis of murine CD45Rhi and CD45Rlo CD4+ T cells.
J Immunol. 1990 May 1;144(9):3288-95
PMID: 1970350
-
Monoclonal immunoglobulin A derived from peritoneal B cells is encoded by both germ line and somatically mutated VH genes and is reactive with commensal bacteria.
Infect Immun. 1996 Feb;64(2):616-23
PMID: 8550216
-
Actin accumulation at sites of attachment of indigenous apathogenic segmented filamentous bacteria to mouse ileal epithelial cells.
Infect Immun. 1993 Sep;61(9):4001-4
PMID: 8359925
-
Role of maternal antibody in the induction of virus specific and bystander IgA responses in Peyer's patches of suckling mice.
Int Immunol. 1995 Jun;7(6):911-8
PMID: 7577799
-
Intestinal, segmented, filamentous bacteria.
FEMS Microbiol Rev. 1992 Jun;8(3-4):165-80
PMID: 1515159
-
Segmented filamentous bacteria are indigenous intestinal bacteria that activate intraepithelial lymphocytes and induce MHC class II molecules and fucosyl asialo GM1 glycolipids on the small intestinal epithelial cells in the ex-germ-free mouse.
Microbiol Immunol. 1995;39(8):555-62
PMID: 7494493
-
Relationship between expression of IgA by Peyer's patch cells and functional IgA memory cells.
J Exp Med. 1987 Nov 1;166(5):1405-18
PMID: 3500260