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Aggregating phenotype in Lactobacillus crispatus determines intestinal colonization and TLR2 and TLR4 modulation in murine colonic mucosa.

ABSTRACT: The colonic microbiota is a major modulator of the mucosal immune system; therefore, its manipulation through supplementation with probiotics may significantly affect the host's immune responses. Since different probiotics seem to exert various effects in vivo, we tested the relevance of the autoaggregation phenotype on the intestinal persistence of lactobacilli and their ability to modulate the host's innate immune responses. After 14 days of diet supplementation, the aggregating strain Lactobacillus crispatus M247 but not aggregation-deficient isogenic mutant MU5 was recovered from the feces and colonic mucosa of mice. This observation was confirmed by strain-specific PCR amplification and by Lactobacillus-specific denaturing gradient gel electrophoresis analysis. Indeed, L. crispatus M247 increased Toll-like receptor 2 (TLR2) mRNA levels, while it reduced TLR4 mRNA and protein levels in the colonic mucosa, whereas MU5 was ineffective. In colonic epithelial cells (CMT-93 cells) L. crispatus M247 but not MU5 induced time-dependent extracellular signal-regulated kinase-1 (ERK1) tyrosine phosphorylation and TLR modulation, which were abolished in the presence of PD98059 (an ERK1 inhibitor). To assess the functional relevance of probiotic-induced TLR modulation, we determined the consequences of L. crispatus preexposure on TLR4 (lipopolysaccharide [LPS]) and TLR2 [Pam3Cys-Ser-(Lys)4] ligand-mediated effects in intestinal epithelial cells. Preexposure to L. crispatus M247 blunted LPS-induced interleukin-6 (IL-6) release and inhibition of CMT-93 migration over a wound edge, whereas it enhanced TLR2-mediated IL-10 up-regulation. In summary, the aggregation phenotype is required for L. crispatus persistence in the colon and for modulation of TLR2/TLR4 expression through an ERK-dependent pathway. We speculate that the aggregation phenotype in L. crispatus M247 is required to temper epithelial cell responsiveness to bacterial endotoxins, which thus affects the evolution of intestinal inflammatory processes.

SUBMITTER: Voltan S

PROVIDER: S-EPMC2043298 | biostudies-literature | 2007 Sep

REPOSITORIES: biostudies-literature

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Aggregating phenotype in Lactobacillus crispatus determines intestinal colonization and TLR2 and TLR4 modulation in murine colonic mucosa.

Voltan Sandra S Castagliuolo Ignazio I Elli Marina M Longo Stefano S Brun Paola P D'Incà Renata R Porzionato Andrea A Macchi Veronica V Palù Giorgio G Sturniolo Giacomo C GC Morelli Lorenzo L Martines Diego D

Clinical and vaccine immunology : CVI 20070718 9

The colonic microbiota is a major modulator of the mucosal immune system; therefore, its manipulation through supplementation with probiotics may significantly affect the host's immune responses. Since different probiotics seem to exert various effects in vivo, we tested the relevance of the autoaggregation phenotype on the intestinal persistence of lactobacilli and their ability to modulate the host's innate immune responses. After 14 days of diet supplementation, the aggregating strain Lactoba ...[more]

PMID: 17634514

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Project description:Several fastidious bacteria have been associated with bacterial vaginosis (BV), but their role in lactobacilli recolonization failure is unknown. We studied the effect of 7 BV-associated bacterial species and 2 Lactobacillus species on vaginal colonization with Lactobacillus crispatus CTV-05 (LACTIN-V).Twenty-four women with BV were given a 5-day course of metronidazole vaginal gel and then randomized 3:1 to receive either LACTIN-V or placebo applied vaginally once daily for 5 initial consecutive days, followed by a weekly application over 2 weeks. Vaginal swabs for L. crispatus CTV-05 culture and 9 bacterium-specific 16S rRNA gene quantitative polymerase chain reaction assays were analyzed on several study visits for the 18 women receiving LACTIN-V.Vaginal colonization with CTV-05 was achieved in 61% of the participants receiving LACTIN-V at either day 10 or day 28 visit and 44% at day 28. Participants not colonized with CTV-05 had generally higher median concentrations of BV-associated bacteria compared to those who colonized. Between enrollment and day 28, the median concentration of Gardnerella vaginalis minimally reduced from 10 to 10 16S rRNA gene copies per swab in women who colonized with CTV-05 but increased from 10 to 10 in those who failed to colonize (P = 0.19). Similarly, the median concentration of Atopobium spp. reduced from 10 16S rRNA gene copies per swab to below limit of detection in women who colonized with CTV-05, but increased from 10 to 10 in those who failed to colonize (P = 0.04). The presence of endogenous L. crispatus at enrollment was found to be significantly associated with a reduced odds of colonization with CTV-05 on day 28 (P = 0.003), and vaginal intercourse during the study significantly impaired successful CTV-05 colonization (P = 0.018).Vaginal concentration of certain BV-associated bacteria, vaginal intercourse during treatment, and the presence of endogenous L. crispatus at enrollment predict colonization with probiotic lactobacilli.

Dataset Information

Aggregating phenotype in Lactobacillus crispatus determines intestinal colonization and TLR2 and TLR4 modulation in murine colonic mucosa.

Publications

Aggregating phenotype in Lactobacillus crispatus determines intestinal colonization and TLR2 and TLR4 modulation in murine colonic mucosa.

Similar Datasets

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