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Anti-inflammatory effects of Lactococcus lactis NCDO 2118 during the remission period of chemically induced colitis.

Luerce TD, Gomes-Santos AC, Rocha CS, Moreira TG, Cruz DN, Lemos L, Sousa AL, Pereira VB, de Azevedo M, Moraes K, Cara DC, LeBlanc JG, Azevedo V, Faria AM, Miyoshi A - Gut Pathog (2014)

Bottom Line: Only one strain, L. lactis NCDO 2118, was able to reduce IL-1β-induced IL-8 secretion in Caco-2 cells, suggesting a potential anti-inflammatory effect.This protective effect was not attributable to changes in secretory IgA (sIgA); however, NCDO 2118 administration was associated with an early increase in IL-6 production and sustained IL-10 production in colonic tissue.Here, we identified a new probiotic strain with a potential role in the treatment of IBD, and we elucidated some of the mechanisms underlying its anti-inflammatory effect.

View Article: PubMed Central - HTML - PubMed

Affiliation: Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627 - 31270-901 Belo Horizonte, MG, Brazil.

ABSTRACT

Background: Many probiotic bacteria have been described as promising tools for the treatment and prevention of inflammatory bowel diseases (IBDs). Most of these bacteria are lactic acid bacteria, which are part of the healthy human microbiota. However, little is known about the effects of transient bacteria present in normal diets, including Lactococcus lactis.

Methods: In the present study, we analysed the immunomodulatory effects of three L. lactis strains in vitro using intestinal epithelial cells. L. lactis NCDO 2118 was administered for 4 days to C57BL/6 mice during the remission period of colitis induced by dextran sodium sulphate (DSS).

Results: Only one strain, L. lactis NCDO 2118, was able to reduce IL-1β-induced IL-8 secretion in Caco-2 cells, suggesting a potential anti-inflammatory effect. Oral treatment using L. lactis NCDO 2118 resulted in a milder form of recurrent colitis than that observed in control diseased mice. This protective effect was not attributable to changes in secretory IgA (sIgA); however, NCDO 2118 administration was associated with an early increase in IL-6 production and sustained IL-10 production in colonic tissue. Mice fed L. lactis NCDO 2118 had an increased number of regulatory CD4(+) T cells (Tregs) bearing surface TGF-β in its latent form (Latency-associated peptide-LAP) in the mesenteric lymph nodes and spleen.

Conclusions: Here, we identified a new probiotic strain with a potential role in the treatment of IBD, and we elucidated some of the mechanisms underlying its anti-inflammatory effect.

No MeSH data available.


Related in: MedlinePlus

Schematic model for the immunomodulatory effects of Lactococcus lactis NCDO 2118 in DSS-induced colitis. Orally administered Lactococcus lactis NCDO 2118 is able to induce an early increase in IL-6 production and to sustain IL-10 secretion in colonic tissue of the dextran sulphate sodium (DSS)-induced murine model of ulcerative colitis. It also increases the number of local tolerogenic dendritic cells (CD11c+CD11b-CD103+). These cells migrate to the mesenteric lymph nodes and stimulate the expansion of CD4+CD25+LAP+ cells, a regulatory type of T cell (Treg), leading ultimately to downmodulation of colitis.
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Figure 7: Schematic model for the immunomodulatory effects of Lactococcus lactis NCDO 2118 in DSS-induced colitis. Orally administered Lactococcus lactis NCDO 2118 is able to induce an early increase in IL-6 production and to sustain IL-10 secretion in colonic tissue of the dextran sulphate sodium (DSS)-induced murine model of ulcerative colitis. It also increases the number of local tolerogenic dendritic cells (CD11c+CD11b-CD103+). These cells migrate to the mesenteric lymph nodes and stimulate the expansion of CD4+CD25+LAP+ cells, a regulatory type of T cell (Treg), leading ultimately to downmodulation of colitis.

Mentions: Because dendritic cells modulate T cell differentiation into effector or regulatory T cells [47], the profile of DCs was evaluated. It has been shown previously that CD103+ DCs can induce CD4 + CD25 + Foxp3+ Treg cells in the intestinal mucosa [48]. In the chemically induced colitis model, we found increased numbers of CD11c+CD103+ DCs in mice treated with DSS. However, oral administration of L. lactis NCDO 2118 enhanced the numbers of CD11c+CD103+ DCs to a greater extent. Gyu Jeon et al.[49] recently showed that Bifidobacterium breve induced the development of IL-10-producing T cells and that this effect was mediated by CD103+ DCs. Thus, L. lactis NCDO 2118 may trigger a regulatory phenotype in DCs that drives the expansion of induced regulatory T cells such as CD4+LAP+. Therefore, we propose a working model for L. lactis NCDO 2118 activity in vivo, which is depicted in Figure 7.


Anti-inflammatory effects of Lactococcus lactis NCDO 2118 during the remission period of chemically induced colitis.

Luerce TD, Gomes-Santos AC, Rocha CS, Moreira TG, Cruz DN, Lemos L, Sousa AL, Pereira VB, de Azevedo M, Moraes K, Cara DC, LeBlanc JG, Azevedo V, Faria AM, Miyoshi A - Gut Pathog (2014)

Schematic model for the immunomodulatory effects of Lactococcus lactis NCDO 2118 in DSS-induced colitis. Orally administered Lactococcus lactis NCDO 2118 is able to induce an early increase in IL-6 production and to sustain IL-10 secretion in colonic tissue of the dextran sulphate sodium (DSS)-induced murine model of ulcerative colitis. It also increases the number of local tolerogenic dendritic cells (CD11c+CD11b-CD103+). These cells migrate to the mesenteric lymph nodes and stimulate the expansion of CD4+CD25+LAP+ cells, a regulatory type of T cell (Treg), leading ultimately to downmodulation of colitis.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4126083&req=5

Figure 7: Schematic model for the immunomodulatory effects of Lactococcus lactis NCDO 2118 in DSS-induced colitis. Orally administered Lactococcus lactis NCDO 2118 is able to induce an early increase in IL-6 production and to sustain IL-10 secretion in colonic tissue of the dextran sulphate sodium (DSS)-induced murine model of ulcerative colitis. It also increases the number of local tolerogenic dendritic cells (CD11c+CD11b-CD103+). These cells migrate to the mesenteric lymph nodes and stimulate the expansion of CD4+CD25+LAP+ cells, a regulatory type of T cell (Treg), leading ultimately to downmodulation of colitis.
Mentions: Because dendritic cells modulate T cell differentiation into effector or regulatory T cells [47], the profile of DCs was evaluated. It has been shown previously that CD103+ DCs can induce CD4 + CD25 + Foxp3+ Treg cells in the intestinal mucosa [48]. In the chemically induced colitis model, we found increased numbers of CD11c+CD103+ DCs in mice treated with DSS. However, oral administration of L. lactis NCDO 2118 enhanced the numbers of CD11c+CD103+ DCs to a greater extent. Gyu Jeon et al.[49] recently showed that Bifidobacterium breve induced the development of IL-10-producing T cells and that this effect was mediated by CD103+ DCs. Thus, L. lactis NCDO 2118 may trigger a regulatory phenotype in DCs that drives the expansion of induced regulatory T cells such as CD4+LAP+. Therefore, we propose a working model for L. lactis NCDO 2118 activity in vivo, which is depicted in Figure 7.

Bottom Line: Only one strain, L. lactis NCDO 2118, was able to reduce IL-1β-induced IL-8 secretion in Caco-2 cells, suggesting a potential anti-inflammatory effect.This protective effect was not attributable to changes in secretory IgA (sIgA); however, NCDO 2118 administration was associated with an early increase in IL-6 production and sustained IL-10 production in colonic tissue.Here, we identified a new probiotic strain with a potential role in the treatment of IBD, and we elucidated some of the mechanisms underlying its anti-inflammatory effect.

View Article: PubMed Central - HTML - PubMed

Affiliation: Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627 - 31270-901 Belo Horizonte, MG, Brazil.

ABSTRACT

Background: Many probiotic bacteria have been described as promising tools for the treatment and prevention of inflammatory bowel diseases (IBDs). Most of these bacteria are lactic acid bacteria, which are part of the healthy human microbiota. However, little is known about the effects of transient bacteria present in normal diets, including Lactococcus lactis.

Methods: In the present study, we analysed the immunomodulatory effects of three L. lactis strains in vitro using intestinal epithelial cells. L. lactis NCDO 2118 was administered for 4 days to C57BL/6 mice during the remission period of colitis induced by dextran sodium sulphate (DSS).

Results: Only one strain, L. lactis NCDO 2118, was able to reduce IL-1β-induced IL-8 secretion in Caco-2 cells, suggesting a potential anti-inflammatory effect. Oral treatment using L. lactis NCDO 2118 resulted in a milder form of recurrent colitis than that observed in control diseased mice. This protective effect was not attributable to changes in secretory IgA (sIgA); however, NCDO 2118 administration was associated with an early increase in IL-6 production and sustained IL-10 production in colonic tissue. Mice fed L. lactis NCDO 2118 had an increased number of regulatory CD4(+) T cells (Tregs) bearing surface TGF-β in its latent form (Latency-associated peptide-LAP) in the mesenteric lymph nodes and spleen.

Conclusions: Here, we identified a new probiotic strain with a potential role in the treatment of IBD, and we elucidated some of the mechanisms underlying its anti-inflammatory effect.

No MeSH data available.


Related in: MedlinePlus