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SlpB Protein Enhances the Probiotic Potential of L. lactis NCDO 2118 in Colitis Mice Model

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. Ulcerat...

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Autores principales: Belo, Giovanna A., Cordeiro, Bárbara F., Oliveira, Emiliano R., Braga, Marina P., da Silva, Sara H., Costa, Bruno G., Martins, Flaviano dos S., Jan, Gwénaël, Le Loir, Yves, Gala-García, Alfonso, Ferreira, Enio, Azevedo, Vasco, do Carmo, Fillipe L. R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8721164/
https://www.ncbi.nlm.nih.gov/pubmed/34987390
http://dx.doi.org/10.3389/fphar.2021.755825
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author Belo, Giovanna A.
Cordeiro, Bárbara F.
Oliveira, Emiliano R.
Braga, Marina P.
da Silva, Sara H.
Costa, Bruno G.
Martins, Flaviano dos S.
Jan, Gwénaël
Le Loir, Yves
Gala-García, Alfonso
Ferreira, Enio
Azevedo, Vasco
do Carmo, Fillipe L. R.
author_facet Belo, Giovanna A.
Cordeiro, Bárbara F.
Oliveira, Emiliano R.
Braga, Marina P.
da Silva, Sara H.
Costa, Bruno G.
Martins, Flaviano dos S.
Jan, Gwénaël
Le Loir, Yves
Gala-García, Alfonso
Ferreira, Enio
Azevedo, Vasco
do Carmo, Fillipe L. R.
author_sort Belo, Giovanna A.
collection PubMed
description 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.
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spelling pubmed-87211642022-01-04 SlpB Protein Enhances the Probiotic Potential of L. lactis NCDO 2118 in Colitis Mice Model Belo, Giovanna A. Cordeiro, Bárbara F. Oliveira, Emiliano R. Braga, Marina P. da Silva, Sara H. Costa, Bruno G. Martins, Flaviano dos S. Jan, Gwénaël Le Loir, Yves Gala-García, Alfonso Ferreira, Enio Azevedo, Vasco do Carmo, Fillipe L. R. Front Pharmacol Pharmacology 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. Frontiers Media S.A. 2021-12-20 /pmc/articles/PMC8721164/ /pubmed/34987390 http://dx.doi.org/10.3389/fphar.2021.755825 Text en Copyright © 2021 Belo, Cordeiro, Oliveira, Braga, da Silva, Costa, Martins, Jan, Le Loir, Gala-García, Ferreira, Azevedo and do Carmo. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Pharmacology
Belo, Giovanna A.
Cordeiro, Bárbara F.
Oliveira, Emiliano R.
Braga, Marina P.
da Silva, Sara H.
Costa, Bruno G.
Martins, Flaviano dos S.
Jan, Gwénaël
Le Loir, Yves
Gala-García, Alfonso
Ferreira, Enio
Azevedo, Vasco
do Carmo, Fillipe L. R.
SlpB Protein Enhances the Probiotic Potential of L. lactis NCDO 2118 in Colitis Mice Model
title SlpB Protein Enhances the Probiotic Potential of L. lactis NCDO 2118 in Colitis Mice Model
title_full SlpB Protein Enhances the Probiotic Potential of L. lactis NCDO 2118 in Colitis Mice Model
title_fullStr SlpB Protein Enhances the Probiotic Potential of L. lactis NCDO 2118 in Colitis Mice Model
title_full_unstemmed SlpB Protein Enhances the Probiotic Potential of L. lactis NCDO 2118 in Colitis Mice Model
title_short SlpB Protein Enhances the Probiotic Potential of L. lactis NCDO 2118 in Colitis Mice Model
title_sort slpb protein enhances the probiotic potential of l. lactis ncdo 2118 in colitis mice model
topic Pharmacology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8721164/
https://www.ncbi.nlm.nih.gov/pubmed/34987390
http://dx.doi.org/10.3389/fphar.2021.755825
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