This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Jiang, H.-Q.
Right arrow Articles by Cebra, J. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Jiang, H.-Q.
Right arrow Articles by Cebra, J. J.

 Previous Article  |  Next Article 

Infection and Immunity, June 2001, p. 3611-3617, Vol. 69, No. 6
0019-9567/01/$04.00+0   DOI: 10.1128/IAI.69.6.3611-3617.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Timing, Localization, and Persistence of Colonization by Segmented Filamentous Bacteria in the Neonatal Mouse Gut Depend on Immune Status of Mothers and Pups

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 7 December 2000/Returned for modification 2 February 2001/Accepted 5 March 2001

As a member of the indigenous gut mucosal microbiota, segmented filamentous bacteria (SFB) colonize the guts of a variety of vertebrates and invertebrates. They are potent microbial stimuli of the gut mucosal immune system. In the small intestines of mice and rats, it has been observed that SFB are absent during the suckling period and appear in high numbers shortly after weaning, then quickly retreat to the cecum and large intestine. In this study, we explored whether this microecological phenomenon resulted from the interaction between SFB and the passively acquired maternal mucosal immunity and/or the actively acquired mucosal immunity. We set up a mouse model by reciprocal crossings and backcrossings of SFB-monoassociated, formerly germ-free, immunocompetent (+/+) BALB/c mice and immunodeficient (scid/scid) mice to produce pups which are either immunocompetent (scid/+) or immunodeficient (scid/scid) and are born either to immunocompetent (scid/+) mothers or to immunodeficient (scid/scid) mothers. We monitored the number of SFB on the mucosa of the small intestine in the four different groups of mice after birth, as well as the level of passively acquired antibodies, the active gut mucosal immune responses, and immunoglobulin A (IgA) coating of SFB in the gut. The results showed that, irrespective of whether the pups were scid/scid or scid/+, SFB could be found earlier on the mucosa of the small intestine in pups born to scid/scid mothers, appearing from day 13 and rapidly reaching a climax around weaning time on day 28, compared to the significantly delayed colonization in the pups of scid/+ mothers, starting from day 16 and peaking around days 28 to 32. After the climax, SFB quickly declined to very low levels in the small intestines of scid/+ pups of either scid/scid mothers or scid/+ mothers, whereas they remained at high levels in scid/scid pups at least until day 70, the last observation time in this study. The dynamic changes in SFB colonization of the small intestines of the different groups of pups may be related to the dynamic changes in the levels of SFB coated with secretory IgA (sIgA), which resulted from the significantly different levels of sIgA obtained from the mothers' milk during the suckling period and, later, of self-produced sIgA in the small intestine. Nevertheless, it is evident that the timing, localization, and persistence of colonization of the neonatal gut by SFB depends on the immune status of both mothers and pups.

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

Infection and Immunity, June 2001, p. 3611-3617, Vol. 69, No. 6
0019-9567/01/$04.00+0   DOI: 10.1128/IAI.69.6.3611-3617.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Zola, T. A., Lysenko, E. S., Weiser, J. N. (2009). Natural Antibody to Conserved Targets of Haemophilus influenzae Limits Colonization of the Murine Nasopharynx. Infect. Immun. 77: 3458-3465 [Abstract] [Full Text]  
  • Croswell, A., Amir, E., Teggatz, P., Barman, M., Salzman, N. H. (2009). Prolonged Impact of Antibiotics on Intestinal Microbial Ecology and Susceptibility to Enteric Salmonella Infection. Infect. Immun. 77: 2741-2753 [Abstract] [Full Text]  
  • Butler, J. E., Francis, D. H., Freeling, J., Weber, P., Krieg, A. M. (2005). Antibody Repertoire Development in Fetal and Neonatal Piglets. IX. Three Pathogen-Associated Molecular Patterns Act Synergistically to Allow Germfree Piglets to Respond to Type 2 Thymus-Independent and Thymus-Dependent Antigens. J. Immunol. 175: 6772-6785 [Abstract] [Full Text]  
  • Diaz, R. L., Hoang, L., Wang, J., Vela, J. L., Jenkins, S., Aranda, R., Martin, M. G. (2004). Maternal Adaptive Immunity Influences the Intestinal Microflora of Suckling Mice. J. Nutr. 134: 2359-2364 [Abstract] [Full Text]  
  • Suzuki, K., Meek, B., Doi, Y., Muramatsu, M., Chiba, T., Honjo, T., Fagarasan, S. (2004). Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proc. Natl. Acad. Sci. USA 101: 1981-1986 [Abstract] [Full Text]  
  • Ramsburg, E., Tigelaar, R., Craft, J., Hayday, A. (2003). Age-dependent Requirement for {gamma}{delta} T Cells in the Primary but Not Secondary Protective Immune Response against an Intestinal Parasite. JEM 198: 1403-1414 [Abstract] [Full Text]  
  • Thurnheer, M. C., Zuercher, A. W., Cebra, J. J., Bos, N. A. (2003). B1 Cells Contribute to Serum IgM, But Not to Intestinal IgA, Production in Gnotobiotic Ig Allotype Chimeric Mice. J. Immunol. 170: 4564-4571 [Abstract] [Full Text]  
  • Sait, L., Galic, M., Strugnell, R. A., Janssen, P. H. (2003). Secretory Antibodies Do Not Affect the Composition of the Bacterial Microbiota in the Terminal Ileum of 10-Week-Old Mice. Appl. Environ. Microbiol. 69: 2100-2109 [Abstract] [Full Text]  
  • Ibnou-Zekri, N., Blum, S., Schiffrin, E. J., von der Weid, T. (2003). Divergent Patterns of Colonization and Immune Response Elicited from Two Intestinal Lactobacillus Strains That Display Similar Properties In Vitro. Infect. Immun. 71: 428-436 [Abstract] [Full Text]  
  • Meyerholz, D. K., Stabel, T. J., Cheville, N. F. (2002). Segmented Filamentous Bacteria Interact with Intraepithelial Mononuclear Cells. Infect. Immun. 70: 3277-3280 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»