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Immune Response to Mycoplasma pulmonis in Nasal Mucosa Is Modulated by the Normal Microbiota

Departments of Clinical Sciences and of Otorhinolaryngology, Karolinska Institute, Huddinge University Hospital, Huddinge, Sweden; Laboratory for Immunohistochemistry and Immunopathology (LIIPAT), Institute of Pathology, Rikshospitalet University Hospital, University of Oslo, Oslo, Norway; and Department of Medical Microbial Ecology, Karolinska Institute, Stockholm, Sweden

Address correspondence to: Prof. Per Brandtzaeg, Institute of Pathology, Rikshospitalet University Hospital, N-0027 Oslo, Norway. E-mail: per.brandtzaeg{at}medisin.uio.no

The impact of commensal bacteria on lymphocyte responses in the upper airways was studied in rat nasal mucosa after infection with the pathogen Mycoplasma pulmonis. Phenotyping was performed in situ by paired immunofluorescence staining in germ-free (GF) and conventional (CV) rats before and 3 wk after the monoinfection. Intraepithelial lymphocytes had expanded significantly in GF (P = 0.02) but not in CV rats. Furthermore, a striking proportional increase of T-cell receptor (TCR)ß⁺CD4⁺ cells was observed both in the lamina propria and epithelium of GF (P < 0.01) but not of CV rats. Notably, in contrast to the pre-infection state, both mucosal compartments showed a percentage of TCRß⁺CD4⁺ cells that was significantly higher in GF (P = 0.03–P < 0.01) than in CV rats after the monoinfection. In parallel, both compartments displayed a percentage of TCRß⁺ CD8⁺ cells that was decreased in GF (P < 0.01) but not in CV rats. The small fraction of TCR⁺ T cells observed (< 5%) did not change quantitatively or phenotypically after infection. The size of organized nose-associated lymphoid tissue was, on average, increased 5.2-fold in GF rats versus 2.6-fold in CV rats. Collectively, our results demonstrated that the normal microbiota modulated markedly the nasal immune response elicited by monoinfection with M. pulmonis.

Abbreviations: antigen-presenting cell, APC • conventional, CV • dendritic cell, DC • germ free, GF • intraepithelial lymphocyte, IEL • lamina propria lymphocyte, LPL • monoclonal antibodies, mAb • nose-associated lymphoid tissue, NALT • natural killer, NK • pattern recognition receptor, PRR • T-cell receptor, TCR • regulatory T cells, T_reg cells