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Strain-specific alterations in gut microbiome and host immune responses elicited by tolerogenic Bifidobacterium pseudolongum

The beneficial effects attributed to Bifidobacterium are largely attributed to their immunomodulatory capabilities, which are likely to be species- and even strain-specific. However, their strain-specificity in direct and indirect immune modulation remain largely uncharacterized. We have shown that...

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Autores principales: Ma, Bing, Gavzy, Samuel J., Saxena, Vikas, Song, Yang, Piao, Wenji, Lwin, Hnin Wai, Lakhan, Ram, Iyyathurai, Jegan, Li, Lushen, France, Michael, Paluskievicz, Christina, Shirkey, Marina W., Hittle, Lauren, Munawwar, Arshi, Mongodin, Emmanuel F., Bromberg, Jonathan S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9852428/
https://www.ncbi.nlm.nih.gov/pubmed/36658194
http://dx.doi.org/10.1038/s41598-023-27706-0
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author Ma, Bing
Gavzy, Samuel J.
Saxena, Vikas
Song, Yang
Piao, Wenji
Lwin, Hnin Wai
Lakhan, Ram
Iyyathurai, Jegan
Li, Lushen
France, Michael
Paluskievicz, Christina
Shirkey, Marina W.
Hittle, Lauren
Munawwar, Arshi
Mongodin, Emmanuel F.
Bromberg, Jonathan S.
author_facet Ma, Bing
Gavzy, Samuel J.
Saxena, Vikas
Song, Yang
Piao, Wenji
Lwin, Hnin Wai
Lakhan, Ram
Iyyathurai, Jegan
Li, Lushen
France, Michael
Paluskievicz, Christina
Shirkey, Marina W.
Hittle, Lauren
Munawwar, Arshi
Mongodin, Emmanuel F.
Bromberg, Jonathan S.
author_sort Ma, Bing
collection PubMed
description The beneficial effects attributed to Bifidobacterium are largely attributed to their immunomodulatory capabilities, which are likely to be species- and even strain-specific. However, their strain-specificity in direct and indirect immune modulation remain largely uncharacterized. We have shown that B. pseudolongum UMB-MBP-01, a murine isolate strain, is capable of suppressing inflammation and reducing fibrosis in vivo. To ascertain the mechanism driving this activity and to determine if it is specific to UMB-MBP-01, we compared it to a porcine tropic strain B. pseudolongum ATCC25526 using a combination of cell culture and in vivo experimentation and comparative genomics approaches. Despite many shared features, we demonstrate that these two strains possess distinct genetic repertoires in carbohydrate assimilation, differential activation signatures and cytokine responses signatures in innate immune cells, and differential effects on lymph node morphology with unique local and systemic leukocyte distribution. Importantly, the administration of each B. pseudolongum strain resulted in major divergence in the structure, composition, and function of gut microbiota. This was accompanied by markedly different changes in intestinal transcriptional activities, suggesting strain-specific modulation of the endogenous gut microbiota as a key to immune modulatory host responses. Our study demonstrated a single probiotic strain can influence local, regional, and systemic immunity through both innate and adaptive pathways in a strain-specific manner. It highlights the importance to investigate both the endogenous gut microbiome and the intestinal responses in response to probiotic supplementation, which underpins the mechanisms through which the probiotic strains drive the strain-specific effect to impact health outcomes.
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spelling pubmed-98524282023-01-21 Strain-specific alterations in gut microbiome and host immune responses elicited by tolerogenic Bifidobacterium pseudolongum Ma, Bing Gavzy, Samuel J. Saxena, Vikas Song, Yang Piao, Wenji Lwin, Hnin Wai Lakhan, Ram Iyyathurai, Jegan Li, Lushen France, Michael Paluskievicz, Christina Shirkey, Marina W. Hittle, Lauren Munawwar, Arshi Mongodin, Emmanuel F. Bromberg, Jonathan S. Sci Rep Article The beneficial effects attributed to Bifidobacterium are largely attributed to their immunomodulatory capabilities, which are likely to be species- and even strain-specific. However, their strain-specificity in direct and indirect immune modulation remain largely uncharacterized. We have shown that B. pseudolongum UMB-MBP-01, a murine isolate strain, is capable of suppressing inflammation and reducing fibrosis in vivo. To ascertain the mechanism driving this activity and to determine if it is specific to UMB-MBP-01, we compared it to a porcine tropic strain B. pseudolongum ATCC25526 using a combination of cell culture and in vivo experimentation and comparative genomics approaches. Despite many shared features, we demonstrate that these two strains possess distinct genetic repertoires in carbohydrate assimilation, differential activation signatures and cytokine responses signatures in innate immune cells, and differential effects on lymph node morphology with unique local and systemic leukocyte distribution. Importantly, the administration of each B. pseudolongum strain resulted in major divergence in the structure, composition, and function of gut microbiota. This was accompanied by markedly different changes in intestinal transcriptional activities, suggesting strain-specific modulation of the endogenous gut microbiota as a key to immune modulatory host responses. Our study demonstrated a single probiotic strain can influence local, regional, and systemic immunity through both innate and adaptive pathways in a strain-specific manner. It highlights the importance to investigate both the endogenous gut microbiome and the intestinal responses in response to probiotic supplementation, which underpins the mechanisms through which the probiotic strains drive the strain-specific effect to impact health outcomes. Nature Publishing Group UK 2023-01-19 /pmc/articles/PMC9852428/ /pubmed/36658194 http://dx.doi.org/10.1038/s41598-023-27706-0 Text en © The Author(s) 2023, corrected publication 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Ma, Bing
Gavzy, Samuel J.
Saxena, Vikas
Song, Yang
Piao, Wenji
Lwin, Hnin Wai
Lakhan, Ram
Iyyathurai, Jegan
Li, Lushen
France, Michael
Paluskievicz, Christina
Shirkey, Marina W.
Hittle, Lauren
Munawwar, Arshi
Mongodin, Emmanuel F.
Bromberg, Jonathan S.
Strain-specific alterations in gut microbiome and host immune responses elicited by tolerogenic Bifidobacterium pseudolongum
title Strain-specific alterations in gut microbiome and host immune responses elicited by tolerogenic Bifidobacterium pseudolongum
title_full Strain-specific alterations in gut microbiome and host immune responses elicited by tolerogenic Bifidobacterium pseudolongum
title_fullStr Strain-specific alterations in gut microbiome and host immune responses elicited by tolerogenic Bifidobacterium pseudolongum
title_full_unstemmed Strain-specific alterations in gut microbiome and host immune responses elicited by tolerogenic Bifidobacterium pseudolongum
title_short Strain-specific alterations in gut microbiome and host immune responses elicited by tolerogenic Bifidobacterium pseudolongum
title_sort strain-specific alterations in gut microbiome and host immune responses elicited by tolerogenic bifidobacterium pseudolongum
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9852428/
https://www.ncbi.nlm.nih.gov/pubmed/36658194
http://dx.doi.org/10.1038/s41598-023-27706-0
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