Distinct Immunomodulation of Bone Marrow-Derived Dendritic Cell Responses to Lactobacillus plantarum WCFS1 by Two Different Polysaccharides Isolated from Lactobacillus rhamnosus LOCK 0900

Górska, Sabina; Schwarzer, Martin; Jachymek, Wojciech; Šrůtková, Dagmar; Brzozowska, Ewa; Kozáková, Hana; Gamian, Andrzej

doi:10.1128/aem.02104-14

Cited by 39 publications

(40 citation statements)

References 56 publications

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“…The repeating-unit structures of a number of different strains of the Lactobacillus casei group of species (i.e., L. casei, L. paracasei, and Lactobacillus rhamnosus) have been published previously (22)(23)(24)(25)(26)(27)(28), and the repeating-unit structure reported here is different. Moreover, it is also different from the published structures of the EPSs characterized for a range of LAB (20,29).…”

Section: Discussionmentioning

confidence: 81%

A Novel Rhamnose-Rich Hetero-exopolysaccharide Isolated from Lactobacillus paracasei DG Activates THP-1 Human Monocytic Cells

Balzaretti

Taverniti

Guglielmetti

et al. 2017

Appl Environ Microbiol

118

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Lactobacillus paracasei DG is a bacterial strain with recognized probiotic properties and is used in commercial probiotic products. However, the mechanisms underlying its probiotic properties are mainly unknown. In this study, we tested the hypothesis that the ability of strain DG to interact with the host is at least partly associated with its ability to synthesize a surface-associated exopolysaccharide (EPS). Comparative genomics revealed the presence of putative EPS gene clusters in the DG genome; accordingly, EPS was isolated from the surface of the bacterium. A sample of the pure EPS from strain DG (DG-EPS), upon nuclear magnetic resonance (NMR) and chemical analyses, was shown to be a novel branched hetero-EPS with a repeat unit composed of L-rhamnose, D-galactose, and N-acetyl-D-galactosamine in a ratio of 4:1:1. Subsequently, we demonstrated that DG-EPS displays immunostimulating properties by enhancing the gene expression of the proinflammatory cytokines tumor necrosis factor alpha (TNF-␣) and interleukin 6 (IL-6), and particularly that of the chemokines IL-8 and CCL20, in the human monocytic cell line THP-1. In contrast, the expression of the cyclooxygenase enzyme COX-2 was not affected. In conclusion, DG-EPS is a bacterial macromolecule with the ability to boost the immune system either as a secreted molecule released from the bacterium or as a capsular envelope on the bacterial cell wall. This study provides additional information about the mechanisms supporting the cross talk between L. paracasei DG and the host. IMPORTANCEThe consumption of food products and supplements called probiotics (i.e., containing live microbial cells) to potentially prevent or treat specific diseases is constantly gaining popularity. The lack of knowledge on the precise mechanisms supporting their potential health-promoting properties, however, greatly limits a more appropriate use of each single probiotic strain. In this context, we studied a well-known probiotic, Lactobacillus paracasei DG, in order to identify the constitutive molecules that can explain the documented health-promoting properties of this bacterium. We found a novel polysaccharide molecule, named DG-EPS, that is secreted by and covers the bacterium. We demonstrated that this molecule, which has a chemical structure never identified before, has immunostimulatory properties and therefore may contribute to the ability of the probiotic L. paracasei DG to interact with the immune system. KEYWORDS

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Section: Discussionmentioning

confidence: 81%

A Novel Rhamnose-Rich Hetero-exopolysaccharide Isolated from Lactobacillus paracasei DG Activates THP-1 Human Monocytic Cells

Balzaretti

Taverniti

Guglielmetti

et al. 2017

Appl Environ Microbiol

118

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“…Both polymers were negatively charged, but E116n (=E148) contained a phosphomonoester, whereas E116 (=E148c) contained a phosphodiester in its backbone chain. The structure of E116n (=E148) was previously reported6, while that of E116 (=E148c) is new. Polymer E116 (=E148c) is a branched heteropolysaccharide with a repeating unit that comprises six monosaccharide residues (three Gal and three Glc) and phosphorus.…”

Section: Discussionmentioning

confidence: 92%

“…The polysaccharide antigens are highly diversified, varying in their component sugar monomers, linkages, chemical substitutions, branching and molecular mass. Recent studies have shown that these polymers have immunomodulatory properties and provide health benefits to the host678, and that they can be recognized by the dendritic cell (DC) and macrophage that are involved in bacterial recognition or antigen capture9.…”

mentioning

confidence: 99%

Structural and immunomodulatory differences among lactobacilli exopolysaccharides isolated from intestines of mice with experimentally induced inflammatory bowel disease

Górska

Sandström

Wojas-Turek

et al. 2016

Sci Rep

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Characteristic changes in the microbiota biostructure and a decreased tolerance to intestinal bacteria have been associated with inflammatory bowel disease (IBD). However, few studies have examined the constituents of the intestinal microbiota, including the surface molecules of the bacteria, in healthy and IBD subsets. Here, we compare the chemical structures and immunomodulatory properties of the exopolysaccharides (EPS) of lactobacilli isolated from mice with induced IBD (IBD “+”) versus those of healthy mice (IBD “−”). Classical structural analyses were performed using nuclear magnetic resonance spectroscopy and mass spectrometry. Immunomodulatory properties were assessed by stimulation of dendritic cells derived from mouse bone marrow or human peripheral mononuclear blood cells. Our results revealed that EPS produced by IBD “+” species are structurally different from those isolated from IBD “−”. Moreover, the structurally different EPS generate different immune responses by dendritic cells. We speculate that resident strains could, upon gut inflammation, switch to producing EPS with specific motifs that are absent from lactobacilli IBD “−”, and/or that bacteria with a particular EPS structure might inhabit the inflamed intestinal mucosa. This study may shed light on the role of EPS in IBD and help the development of a specific probiotic therapy for this disease.

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“…This argument is supported by our recent finding that EPS produced by the L. rhamnosus LOCK0900 strain can modulate the cytokine production of BM-DCs induced by another bacteria. 56 In conclusion, we have shown that the three lactobacillus strains in Lmix, L. rhamnosus LOCK0900, L. rhamnosus LOCK0908 and L. casei LOCK0919, were able to reduce sensitization to Bet v 1. The specific serum IgE and IgG levels as well as the production of the pro-allergic cytokines IL-4 and IL-5 by splenocytes and MLN cells were also reduced.…”

Section: Discussionmentioning

confidence: 96%

Colonization of germ-free mice with a mixture of three lactobacillus strains enhances the integrity of gut mucosa and ameliorates allergic sensitization

et al. 2015

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Increasing numbers of clinical trials and animal experiments have shown that probiotic bacteria are promising tools for allergy prevention. Here, we analyzed the immunomodulatory properties of three selected lactobacillus strains and the impact of their mixture on allergic sensitization to Bet v 1 using a gnotobiotic mouse model. We showed that Lactobacillus (L.) rhamnosus LOCK0900, L. rhamnosus LOCK0908 and L. casei LOCK0919 are recognized via Toll-like receptor 2 (TLR2) and nucleotide-binding oligomerization domain-containing protein 2 (NOD2) receptors and stimulate bone marrow-derived dendritic cells to produce cytokines in species-and strain-dependent manners. Colonization of germ-free (GF) mice with a mixture of all three strains (Lmix) improved the intestinal barrier by strengthening the apical junctional complexes of enterocytes and restoring the structures of microfilaments extending into the terminal web. Mice colonized with Lmix and sensitized to the Bet v 1 allergen showed significantly lower levels of allergen-specific IgE, IgG1 and IgG2a and an elevated total IgA level in the sera and intestinal lavages as well as an increased transforming growth factor (TGF)-b level compared with the sensitized GF mice. Splenocytes and mesenteric lymph node cells from the Lmix-colonized mice showed the significant upregulation of TGF-b after in vitro stimulation with Bet v 1. Our results show that Lmix colonization improved the gut epithelial barrier and reduced allergic sensitization to Bet v 1. Furthermore, these findings were accompanied by the increased production of circulating and secretory IgA and the regulatory cytokine TGF-b. Thus, this mixture of three lactobacillus strains shows potential for use in the prevention of increased gut permeability and the onset of allergies in humans. Cellular & Molecular Immunology

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Distinct Immunomodulation of Bone Marrow-Derived Dendritic Cell Responses to Lactobacillus plantarum WCFS1 by Two Different Polysaccharides Isolated from Lactobacillus rhamnosus LOCK 0900

Cited by 39 publications

References 56 publications

A Novel Rhamnose-Rich Hetero-exopolysaccharide Isolated from Lactobacillus paracasei DG Activates THP-1 Human Monocytic Cells

A Novel Rhamnose-Rich Hetero-exopolysaccharide Isolated from Lactobacillus paracasei DG Activates THP-1 Human Monocytic Cells

Structural and immunomodulatory differences among lactobacilli exopolysaccharides isolated from intestines of mice with experimentally induced inflammatory bowel disease

Colonization of germ-free mice with a mixture of three lactobacillus strains enhances the integrity of gut mucosa and ameliorates allergic sensitization

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