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Comparative Study
. 2005 Jul 19;102(29):10321-6.
doi: 10.1073/pnas.0504084102. Epub 2005 Jun 28.

Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids

Corinne Grangette  1 , Sophie Nutten, Emmanuelle Palumbo, Siegfried Morath, Corinna Hermann, Joelle Dewulf, Bruno Pot, Thomas Hartung, Pascal Hols, Annick Mercenier
Affiliations
Comparative Study

Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids

Corinne Grangette et al. Proc Natl Acad Sci U S A. .

Abstract

Teichoic acids (TAs), and especially lipoteichoic acids (LTAs), are one of the main immunostimulatory components of pathogenic Gram-positive bacteria. Their contribution to the immunomodulatory properties of commensal bacteria and especially of lactic acid bacteria has not yet been investigated in detail. To evaluate the role of TAs in the interaction between lactic acid bacteria and the immune system, we analyzed the antiinflammatory properties of a mutant of Lactobacillus plantarum NCIMB8826 affected in the TA biosynthesis pathway both in vitro (mononuclear cells stimulation) and in vivo (murine model of colitis). This Dlt- mutant was found to incorporate much less D-Ala in its TAs than the WT strain. This defect significantly impacted the immunomodulation reactions induced by the bacterium, as shown by a dramatically reduced secretion of proinflammatory cytokines by peripheral blood mononuclear cells and monocytes stimulated by the Dlt- mutant as compared with the parental strain. Concomitantly, a significant increase in IL-10 production was stimulated by the Dlt- mutant in comparison with the WT strain. Moreover, the proinflammatory capacity of L. plantarum-purified LTA was found to be Toll-like receptor 2-dependent. Consistent with the in vitro results, the Dlt- mutant was significantly more protective in a murine colitis model than its WT counterpart. The results indicated that composition of LTA within the whole-cell context of L. plantarum can modulate proinflammatory or antiinflammatory immune responses.

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Figures

Fig. 1.
Fig. 1.
Cytokine response of human PBMC to stimulation with L. plantarum NCIMB8826 WT, the isogenic Dlt- mutant, E. coli TG1, and Streptococcus gordonii LMG 17843 strains. Bacteria were collected after 48 h (lactobacilli) or 24 h (E. coli and Streptococcus gordonii) of growth. Results represent the mean ± SEM for the response of 11 blood samples (individual donors).
Fig. 2.
Fig. 2.
Cytokine response of human PBMC to stimulation with 1 or 10 μg/ml of LTAs purified from the L. plantarum NCIMB8826 WT (filled bars) or the isogenic Dlt- mutant (hatched bars). Results represent the mean ± SEM for the response of six blood samples (individual donors).
Fig. 3.
Fig. 3.
TNF-α response of bone marrow cells derived from TLR-2+/+ (black bars) and TLR-2-/- (gray bars) mice to stimulation by 10 μg/ml purified bacterial LTA (A) or whole bacteria (5 × 104 CFU) (B). Results represent the mean ± SEM (n = 4). *, P < 0.05 represents significant differences.
Fig. 4.
Fig. 4.
Effect of preventive administration of L. plantarum NCIMB8826 WT and Dlt- mutant strains on acute colitis induced in BALB/c mice by intrarectal administration of TNBS. (A) Weight variation between day 5 (TNBS administration) and day 7 (death). (B and C) Wallace (B) and Ameho (C) inflammation scores. Results are means ± SEM of one representative experiment (eight or nine mice per group). Significant P < 0.05 (**) or < 0.1 (*), as compared with the TNBS control group.
Fig. 5.
Fig. 5.
Representative histological sections of colonic tissues of BALB/c mice obtained 2 days after intrarectal TNBS/ethanol administration. Shown are colon sections of mice receiving no LAB and ethanol 40% (A), TNBS-treated mice receiving no LAB (B), TNBS-treated mice gavaged with L. plantarum NCIMB8826 WT strain (C), or TNBS-treated mice gavaged with the Dlt- mutant (D). (Magnification: ×100.)
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