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The Cheese Matrix Modulates the Immunomodulatory Properties of Propionibacterium freudenreichii CIRM-BIA 129 in Healthy Piglets

Propionibacterium freudenreichii is a beneficial bacterium, used as a cheese starter, which presents versatile probiotic properties. These properties are strain-dependent. We hypothesized they may also be delivery vehicle-dependent. In this study, we thus explored in healthy piglets how the cheese m...

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Autores principales: Rabah, Houem, Ferret-Bernard, Stéphanie, Huang, Song, Le Normand, Laurence, Cousin, Fabien J., Gaucher, Floriane, Jeantet, Romain, Boudry, Gaëlle, Jan, Gwénaël
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6215859/
https://www.ncbi.nlm.nih.gov/pubmed/30420848
http://dx.doi.org/10.3389/fmicb.2018.02584
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author Rabah, Houem
Ferret-Bernard, Stéphanie
Huang, Song
Le Normand, Laurence
Cousin, Fabien J.
Gaucher, Floriane
Jeantet, Romain
Boudry, Gaëlle
Jan, Gwénaël
author_facet Rabah, Houem
Ferret-Bernard, Stéphanie
Huang, Song
Le Normand, Laurence
Cousin, Fabien J.
Gaucher, Floriane
Jeantet, Romain
Boudry, Gaëlle
Jan, Gwénaël
author_sort Rabah, Houem
collection PubMed
description Propionibacterium freudenreichii is a beneficial bacterium, used as a cheese starter, which presents versatile probiotic properties. These properties are strain-dependent. We hypothesized they may also be delivery vehicle-dependent. In this study, we thus explored in healthy piglets how the cheese matrix affects the immunomodulatory properties of P. freudenreichii. During 2 weeks, three groups of weaned piglets consumed, respectively, P. freudenreichii as a liquid culture (PF-culture), P. freudenreichii under the form of a cheese (PF-cheese), or a control sterile cheese matrix (Cheese-matrix). The in vivo metabolic activity of P. freudenreichii was assessed by determining short chain fatty acids (SCFA) concentration and bifidobacteria population in feces. Whatever the delivery vehicle, P. freudenreichii was metabolically active in piglets’ colon and enhanced both bifidobacteria and SCFA in feces. P. freudenreichii consumption decreased the secretion of TNFα and of IL-10 by peripheral blood mononuclear cells (PBMC). It did not alter IL-10, IFNγ, IL-17, and TNFα secretion in mesenteric lymph node immune cells (MLNC). PF-cheese enhanced significantly Treg phenotype, while PF-culture decreased significantly Th17 phenotype in PBMC and MLNC. Remarkably, only PF-cheese induced an increase of Th2 phenotype in PBMC and MLNC. Ex vivo stimulation of PBMC and MLNC by Lipopolysaccharides and Concanavalin A emphasized the difference in the immunomodulatory responses between PF-culture and PF-cheese group, as well as between PBMC and MLNC. This study shows the importance to consider the delivery vehicle for probiotic administration. It confirms the anti-inflammatory potential of P. freudenreichii. It opens new perspectives for the use propionibacteria-fermented products as preventive agents for inflammatory bowel diseases and intestinal infectious diseases.
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spelling pubmed-62158592018-11-12 The Cheese Matrix Modulates the Immunomodulatory Properties of Propionibacterium freudenreichii CIRM-BIA 129 in Healthy Piglets Rabah, Houem Ferret-Bernard, Stéphanie Huang, Song Le Normand, Laurence Cousin, Fabien J. Gaucher, Floriane Jeantet, Romain Boudry, Gaëlle Jan, Gwénaël Front Microbiol Microbiology Propionibacterium freudenreichii is a beneficial bacterium, used as a cheese starter, which presents versatile probiotic properties. These properties are strain-dependent. We hypothesized they may also be delivery vehicle-dependent. In this study, we thus explored in healthy piglets how the cheese matrix affects the immunomodulatory properties of P. freudenreichii. During 2 weeks, three groups of weaned piglets consumed, respectively, P. freudenreichii as a liquid culture (PF-culture), P. freudenreichii under the form of a cheese (PF-cheese), or a control sterile cheese matrix (Cheese-matrix). The in vivo metabolic activity of P. freudenreichii was assessed by determining short chain fatty acids (SCFA) concentration and bifidobacteria population in feces. Whatever the delivery vehicle, P. freudenreichii was metabolically active in piglets’ colon and enhanced both bifidobacteria and SCFA in feces. P. freudenreichii consumption decreased the secretion of TNFα and of IL-10 by peripheral blood mononuclear cells (PBMC). It did not alter IL-10, IFNγ, IL-17, and TNFα secretion in mesenteric lymph node immune cells (MLNC). PF-cheese enhanced significantly Treg phenotype, while PF-culture decreased significantly Th17 phenotype in PBMC and MLNC. Remarkably, only PF-cheese induced an increase of Th2 phenotype in PBMC and MLNC. Ex vivo stimulation of PBMC and MLNC by Lipopolysaccharides and Concanavalin A emphasized the difference in the immunomodulatory responses between PF-culture and PF-cheese group, as well as between PBMC and MLNC. This study shows the importance to consider the delivery vehicle for probiotic administration. It confirms the anti-inflammatory potential of P. freudenreichii. It opens new perspectives for the use propionibacteria-fermented products as preventive agents for inflammatory bowel diseases and intestinal infectious diseases. Frontiers Media S.A. 2018-10-29 /pmc/articles/PMC6215859/ /pubmed/30420848 http://dx.doi.org/10.3389/fmicb.2018.02584 Text en Copyright © 2018 Rabah, Ferret-Bernard, Huang, Le Normand, Cousin, Gaucher, Jeantet, Boudry and Jan. http://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 Microbiology
Rabah, Houem
Ferret-Bernard, Stéphanie
Huang, Song
Le Normand, Laurence
Cousin, Fabien J.
Gaucher, Floriane
Jeantet, Romain
Boudry, Gaëlle
Jan, Gwénaël
The Cheese Matrix Modulates the Immunomodulatory Properties of Propionibacterium freudenreichii CIRM-BIA 129 in Healthy Piglets
title The Cheese Matrix Modulates the Immunomodulatory Properties of Propionibacterium freudenreichii CIRM-BIA 129 in Healthy Piglets
title_full The Cheese Matrix Modulates the Immunomodulatory Properties of Propionibacterium freudenreichii CIRM-BIA 129 in Healthy Piglets
title_fullStr The Cheese Matrix Modulates the Immunomodulatory Properties of Propionibacterium freudenreichii CIRM-BIA 129 in Healthy Piglets
title_full_unstemmed The Cheese Matrix Modulates the Immunomodulatory Properties of Propionibacterium freudenreichii CIRM-BIA 129 in Healthy Piglets
title_short The Cheese Matrix Modulates the Immunomodulatory Properties of Propionibacterium freudenreichii CIRM-BIA 129 in Healthy Piglets
title_sort cheese matrix modulates the immunomodulatory properties of propionibacterium freudenreichii cirm-bia 129 in healthy piglets
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6215859/
https://www.ncbi.nlm.nih.gov/pubmed/30420848
http://dx.doi.org/10.3389/fmicb.2018.02584
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