Abstract
Bacteria used in the production of fermented food products have been investigated for their potential role as modulators of inflammation in gastrointestinal tract disorders such as inflammatory bowel diseases (IBD) that cause irreversible changes in the structure and function of gut tissues. Ulcerative colitis (UC) is the most prevalent IBD in the population of Western countries, and it is marked by symptoms such as weight loss, rectal bleeding, diarrhea, shortening of the colon, and destruction of the epithelial layer. The strain Propionibacterium freudenreichii CIRM-BIA 129 recently revealed promising immunomodulatory properties that greatly rely on surface-layer proteins (Slp), notably SlpB. We, thus, cloned the sequence encoding the SlpB protein into the pXIES-SEC expression and secretion vector, and expressed the propionibacterial protein in the lactic acid bacterium Lactococcus lactis NCDO 2118. The probiotic potential of L. lactis NCDO 2118 harboring pXIES-SEC:slpB (L. lactis-SlpB) was evaluated in a UC-mice model induced by Dextran Sulfate Sodium (DSS). During colitis induction, mice receiving L. lactis-SlpB exhibited reduced severity of colitis, with lower weight loss, lower disease activity index, limited shortening of the colon length, and reduced histopathological score, with significant differences, compared with the DSS group and the group treated with L. lactis NCDO 2118 wild-type strain. Moreover, L. lactis-SlpB administration increased the expression of genes encoding tight junction proteins zo-1, cln-1, cln-5, ocln, and muc-2 in the colon, increased IL-10 and TGF-β, and decreased IL-17, TNF-α, and IL-12 cytokines in the colon. Therefore, this work demonstrates that SlpB recombinant protein is able to increase the probiotic potential of the L. lactis strain to alleviate DSS-induced colitis in mice. This opens perspectives for the development of new approaches to enhance the probiotic potential of strains by the addition of SlpB protein.
Highlights
Propionibacterium freudenreichii (Pf) is a dairy propionic acid bacterium (PAB) that has gained prominence as a potential probiotic, after studies have shown primitive characteristics, such as the production of short-chain fatty acids and conjugated linoleic acid, in addition to producing vitamin 12 at an industrial scale (Thierry et al, 2011; Deptula et al, 2017)
Expression of the P. freudenreichii SlpB protein by L. lactis NCDO 2118 was first verified by Western blotting (Supplementary Figure S2)
We investigated the ability of such expression to enhance the probiotic properties of the L. lactis in the context of Dextran Sulfate Sodium (DSS)-colitis
Summary
Propionibacterium freudenreichii (Pf) is a dairy propionic acid bacterium (PAB) that has gained prominence as a potential probiotic, after studies have shown primitive characteristics, such as the production of short-chain fatty acids and conjugated linoleic acid, in addition to producing vitamin 12 at an industrial scale (Thierry et al, 2011; Deptula et al, 2017). Pf has been listed in the Immunomodulatory SlpB Protein qualified presumption of safety (QPS) list by the European food safety authority and has a GRAS (Generally Recognized As Safe) status for its use in cheese. Mutation of the gene encoding SlpB, a surface protein present at the surface of the probiotic strain P. freudenreichii CIRM-BIA 129 (Pf 129), drastically alters its immunomodulatory effects in vitro and in vivo, its adhesion to HT-29, its physicochemical properties, its ability to survive stress, and its surface and whole-cell proteome. The purified Pf 129 SlpB protein was able to increase IL-10 gene expression in HT-29 cells. It is very important to know whether the immunomodulatory effects of the Pf 129 SlpB protein can be observed in other organisms, such as lactic acid bacteria
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