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Infection and Immunity, April 1999, p. 1992-2000, Vol. 67, No. 4
0019-9567/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

Segmented Filamentous Bacteria Are Potent Stimuli of a Physiologically Normal State of the Murine Gut Mucosal Immune System

Gwen L. Talham,1,dagger Han-Qing Jiang,1 Nicolaas A. Bos,2 and John J. Cebra1,*

Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104,1 and Department of Histology and Cell Biology, University of Groningen, 9713EZ Groningen, The Netherlands2

Received 10 August 1998/Returned for modification 29 October 1998/Accepted 27 January 1999

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.

* Corresponding author. Mailing address: Department of Biology, University of Pennsylvania, Philadelphia, PA 19104-6018. Phone: (215) 898-5599. Fax: (215) 898-9786. E-mail: jcebra{at}sas.upenn.edu.

dagger Present address: University Laboratory Animal Resources, University of Pennsylvania, Philadelphia, PA 19104-6021.

Infection and Immunity, April 1999, p. 1992-2000, Vol. 67, No. 4
0019-9567/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.


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