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Published online on June 28, 2005, 10.1073/pnas.0504084102
PNAS | July 19, 2005 | vol. 102 | no. 29 | 10321-10326


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From The Cover
MICROBIOLOGY
Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids

Corinne Grangette *, {dagger}, Sophie Nutten * {ddagger}, Emmanuelle Palumbo §, Siegfried Morath ¶, Corinna Hermann ¶, Joelle Dewulf *, Bruno Pot *, Thomas Hartung ¶, Pascal Hols §, and Annick Mercenier * {ddagger}

*Laboratoire de Bactériologie des Ecosytèmes, Institut Pasteur de Lille-Institut de Biologie de Lille, 59019 Lille Cedex, France; §Unité de Génétique, Institut des Sciences de la Vie, Université Catholique de Louvain, B-1348 Louvain-la-Neuve, Belgium; and Department of Biochemical Pharmacology, Konstanz University, 78457 Konstanz, Germany

Communicated by Todd R. Klaenhammer, North Carolina State University, Raleigh, NC, May 18, 2005 (received for review November 19, 2004)

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.

lactic acid bacteria | probiotic | immunonodulation | inflammation | cell-wall mutant

Author contributions: C.G., P.H., and A.M. designed research; C.G., S.N., S.M., C.H., and J.D. performed research; E.P., S.M., T.H., and P.H. contributed new reagents/analytic tools; C.G., S.N., C.H., T.H., and A.M. analyzed data; C.G., S.N., C.H., B.P., P.H., and A.M. wrote the paper; and C.G., T.H., P.H., and A.M. provided collaboration management.

Abbreviations: CFU, colony-forming units; IBD, inflammatory bowel disease; LAB, lactic acid bacteria; LTA, lipoteichoic acid; PBMC, peripheral blood mononuclear cells; TA, teichoic acid; TLR, toll-like receptor; TNBS, 2,4,6-trinitrobenzenesulfonic acid.

{ddagger} Present address: Nutrition and Health Department, Nestle Research Centre, CH 1000 Lausanne, Switzerland.

{dagger} To whom correspondence should be addressed. E-mail: corinne.grangette{at}ibl.fr.

© 2005 by The National Academy of Sciences of the USA


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