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Impact of supplementation with a food-derived microbial community on obesity-associated inflammation and gut microbiota composition

BACKGROUND: Obesity is a complex pathology associated with dysbiosis, metabolic alterations, and low-grade chronic inflammation promoted by immune cells, infiltrating and populating the adipose tissue. Probiotic supplementation was suggested to be capable of counteracting obesity-associated immune a...

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Autores principales: Roselli, Marianna, Devirgiliis, Chiara, Zinno, Paola, Guantario, Barbara, Finamore, Alberto, Rami, Rita, Perozzi, Giuditta
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5628415/
https://www.ncbi.nlm.nih.gov/pubmed/29043005
http://dx.doi.org/10.1186/s12263-017-0583-1
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author Roselli, Marianna
Devirgiliis, Chiara
Zinno, Paola
Guantario, Barbara
Finamore, Alberto
Rami, Rita
Perozzi, Giuditta
author_facet Roselli, Marianna
Devirgiliis, Chiara
Zinno, Paola
Guantario, Barbara
Finamore, Alberto
Rami, Rita
Perozzi, Giuditta
author_sort Roselli, Marianna
collection PubMed
description BACKGROUND: Obesity is a complex pathology associated with dysbiosis, metabolic alterations, and low-grade chronic inflammation promoted by immune cells, infiltrating and populating the adipose tissue. Probiotic supplementation was suggested to be capable of counteracting obesity-associated immune and microbial alterations, based on its proven immunomodulatory activity and positive effect on gut microbial balance. Traditional fermented foods represent a natural source of live microbes, including environmental strains with probiotic features, which could transiently colonise the gut. The aim of our work was to evaluate the impact of supplementation with a complex foodborne bacterial consortium on obesity-associated inflammation and gut microbiota composition in a mouse model. METHODS: C57BL/6J mice fed a 45% high fat diet (HFD) for 90 days were supplemented with a mixture of foodborne lactic acid bacteria derived from the traditional fermented dairy product “Mozzarella di Bufala Campana” (MBC) or with the commercial probiotic GG strain of Lactobacillus rhamnosus (LGG). Inflammation was assessed in epididymal white adipose tissue (WAT) following HFD. Faecal microbiota composition was studied by next-generation sequencing. RESULTS: Significant reduction of epididymal WAT weight was observed in MBC-treated, as compared to LGG and control, animals. Serum metabolic profiling showed correspondingly reduced levels of triglycerides and higher levels of HDL cholesterol, as well as a trend toward reduction of LDL-cholesterol levels. Analysis of the principal leucocyte subpopulations in epididymal WAT revealed increased regulatory T cells and CD4(+) cells in MBC microbiota-supplemented mice, as well as decreased macrophage and CD8(+) cell numbers, suggesting anti-inflammatory effects. These results were associated with lower levels of pro-inflammatory cytokines and chemokines in WAT explants. Faecal bacterial profiling demonstrated increased Firmicutes/Bacteroidetes ratio in all mice groups following HFD. CONCLUSIONS: Taken together, these results indicate a protective effect of MBC microbiota supplementation toward HFD-induced fat accumulation and triglyceride and cholesterol levels, as well as inflammation, suggesting a stronger effect of a mixed microbial consortium vs single-strain probiotic supplementation. The immunomodulatory activity exerted by the MBC microbiota could be due to synergistic interactions within the microbial consortium, highlighting the important role of dietary microbes with yet uncharacterised probiotic effect. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12263-017-0583-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-56284152017-10-17 Impact of supplementation with a food-derived microbial community on obesity-associated inflammation and gut microbiota composition Roselli, Marianna Devirgiliis, Chiara Zinno, Paola Guantario, Barbara Finamore, Alberto Rami, Rita Perozzi, Giuditta Genes Nutr Research BACKGROUND: Obesity is a complex pathology associated with dysbiosis, metabolic alterations, and low-grade chronic inflammation promoted by immune cells, infiltrating and populating the adipose tissue. Probiotic supplementation was suggested to be capable of counteracting obesity-associated immune and microbial alterations, based on its proven immunomodulatory activity and positive effect on gut microbial balance. Traditional fermented foods represent a natural source of live microbes, including environmental strains with probiotic features, which could transiently colonise the gut. The aim of our work was to evaluate the impact of supplementation with a complex foodborne bacterial consortium on obesity-associated inflammation and gut microbiota composition in a mouse model. METHODS: C57BL/6J mice fed a 45% high fat diet (HFD) for 90 days were supplemented with a mixture of foodborne lactic acid bacteria derived from the traditional fermented dairy product “Mozzarella di Bufala Campana” (MBC) or with the commercial probiotic GG strain of Lactobacillus rhamnosus (LGG). Inflammation was assessed in epididymal white adipose tissue (WAT) following HFD. Faecal microbiota composition was studied by next-generation sequencing. RESULTS: Significant reduction of epididymal WAT weight was observed in MBC-treated, as compared to LGG and control, animals. Serum metabolic profiling showed correspondingly reduced levels of triglycerides and higher levels of HDL cholesterol, as well as a trend toward reduction of LDL-cholesterol levels. Analysis of the principal leucocyte subpopulations in epididymal WAT revealed increased regulatory T cells and CD4(+) cells in MBC microbiota-supplemented mice, as well as decreased macrophage and CD8(+) cell numbers, suggesting anti-inflammatory effects. These results were associated with lower levels of pro-inflammatory cytokines and chemokines in WAT explants. Faecal bacterial profiling demonstrated increased Firmicutes/Bacteroidetes ratio in all mice groups following HFD. CONCLUSIONS: Taken together, these results indicate a protective effect of MBC microbiota supplementation toward HFD-induced fat accumulation and triglyceride and cholesterol levels, as well as inflammation, suggesting a stronger effect of a mixed microbial consortium vs single-strain probiotic supplementation. The immunomodulatory activity exerted by the MBC microbiota could be due to synergistic interactions within the microbial consortium, highlighting the important role of dietary microbes with yet uncharacterised probiotic effect. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12263-017-0583-1) contains supplementary material, which is available to authorized users. BioMed Central 2017-10-04 /pmc/articles/PMC5628415/ /pubmed/29043005 http://dx.doi.org/10.1186/s12263-017-0583-1 Text en © The Author(s) 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Roselli, Marianna
Devirgiliis, Chiara
Zinno, Paola
Guantario, Barbara
Finamore, Alberto
Rami, Rita
Perozzi, Giuditta
Impact of supplementation with a food-derived microbial community on obesity-associated inflammation and gut microbiota composition
title Impact of supplementation with a food-derived microbial community on obesity-associated inflammation and gut microbiota composition
title_full Impact of supplementation with a food-derived microbial community on obesity-associated inflammation and gut microbiota composition
title_fullStr Impact of supplementation with a food-derived microbial community on obesity-associated inflammation and gut microbiota composition
title_full_unstemmed Impact of supplementation with a food-derived microbial community on obesity-associated inflammation and gut microbiota composition
title_short Impact of supplementation with a food-derived microbial community on obesity-associated inflammation and gut microbiota composition
title_sort impact of supplementation with a food-derived microbial community on obesity-associated inflammation and gut microbiota composition
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5628415/
https://www.ncbi.nlm.nih.gov/pubmed/29043005
http://dx.doi.org/10.1186/s12263-017-0583-1
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