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Selected commensals educate the intestinal vascular and immune system for immunocompetence

BACKGROUND: The intestinal microbiota fundamentally guides the development of a normal intestinal physiology, the education, and functioning of the mucosal immune system. The Citrobacter rodentium-carrier model in germ-free (GF) mice is suitable to study the influence of selected microbes on an othe...

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Autores principales: Romero, Rossana, Zarzycka, Agnieszka, Preussner, Mathieu, Fischer, Florence, Hain, Torsten, Herrmann, Jan-Paul, Roth, Katrin, Keber, Corinna U., Suryamohan, Kushal, Raifer, Hartmann, Luu, Maik, Leister, Hanna, Bertrams, Wilhelm, Klein, Matthias, Shams-Eldin, Hosam, Jacob, Ralf, Mollenkopf, Hans-Joachim, Rajalingam, Krishnaraj, Visekruna, Alexander, Steinhoff, Ulrich
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9520927/
https://www.ncbi.nlm.nih.gov/pubmed/36171625
http://dx.doi.org/10.1186/s40168-022-01353-5
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author Romero, Rossana
Zarzycka, Agnieszka
Preussner, Mathieu
Fischer, Florence
Hain, Torsten
Herrmann, Jan-Paul
Roth, Katrin
Keber, Corinna U.
Suryamohan, Kushal
Raifer, Hartmann
Luu, Maik
Leister, Hanna
Bertrams, Wilhelm
Klein, Matthias
Shams-Eldin, Hosam
Jacob, Ralf
Mollenkopf, Hans-Joachim
Rajalingam, Krishnaraj
Visekruna, Alexander
Steinhoff, Ulrich
author_facet Romero, Rossana
Zarzycka, Agnieszka
Preussner, Mathieu
Fischer, Florence
Hain, Torsten
Herrmann, Jan-Paul
Roth, Katrin
Keber, Corinna U.
Suryamohan, Kushal
Raifer, Hartmann
Luu, Maik
Leister, Hanna
Bertrams, Wilhelm
Klein, Matthias
Shams-Eldin, Hosam
Jacob, Ralf
Mollenkopf, Hans-Joachim
Rajalingam, Krishnaraj
Visekruna, Alexander
Steinhoff, Ulrich
author_sort Romero, Rossana
collection PubMed
description BACKGROUND: The intestinal microbiota fundamentally guides the development of a normal intestinal physiology, the education, and functioning of the mucosal immune system. The Citrobacter rodentium-carrier model in germ-free (GF) mice is suitable to study the influence of selected microbes on an otherwise blunted immune response in the absence of intestinal commensals. RESULTS: Here, we describe that colonization of adult carrier mice with 14 selected commensal microbes (OMM(12) + MC(2)) was sufficient to reestablish the host immune response to enteric pathogens; this conversion was facilitated by maturation and activation of the intestinal blood vessel system and the step- and timewise stimulation of innate and adaptive immunity. While the immature colon of C. rodentium-infected GF mice did not allow sufficient extravasation of neutrophils into the gut lumen, colonization with OMM(12) + MC(2) commensals initiated the expansion and activation of the visceral vascular system enabling granulocyte transmigration into the gut lumen for effective pathogen elimination. CONCLUSIONS: Consortium modeling revealed that the addition of two facultative anaerobes to the OMM(12) community was essential to further progress the intestinal development. Moreover, this study demonstrates the therapeutic value of a defined consortium to promote intestinal maturation and immunity even in adult organisms. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01353-5.
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spelling pubmed-95209272022-09-30 Selected commensals educate the intestinal vascular and immune system for immunocompetence Romero, Rossana Zarzycka, Agnieszka Preussner, Mathieu Fischer, Florence Hain, Torsten Herrmann, Jan-Paul Roth, Katrin Keber, Corinna U. Suryamohan, Kushal Raifer, Hartmann Luu, Maik Leister, Hanna Bertrams, Wilhelm Klein, Matthias Shams-Eldin, Hosam Jacob, Ralf Mollenkopf, Hans-Joachim Rajalingam, Krishnaraj Visekruna, Alexander Steinhoff, Ulrich Microbiome Research BACKGROUND: The intestinal microbiota fundamentally guides the development of a normal intestinal physiology, the education, and functioning of the mucosal immune system. The Citrobacter rodentium-carrier model in germ-free (GF) mice is suitable to study the influence of selected microbes on an otherwise blunted immune response in the absence of intestinal commensals. RESULTS: Here, we describe that colonization of adult carrier mice with 14 selected commensal microbes (OMM(12) + MC(2)) was sufficient to reestablish the host immune response to enteric pathogens; this conversion was facilitated by maturation and activation of the intestinal blood vessel system and the step- and timewise stimulation of innate and adaptive immunity. While the immature colon of C. rodentium-infected GF mice did not allow sufficient extravasation of neutrophils into the gut lumen, colonization with OMM(12) + MC(2) commensals initiated the expansion and activation of the visceral vascular system enabling granulocyte transmigration into the gut lumen for effective pathogen elimination. CONCLUSIONS: Consortium modeling revealed that the addition of two facultative anaerobes to the OMM(12) community was essential to further progress the intestinal development. Moreover, this study demonstrates the therapeutic value of a defined consortium to promote intestinal maturation and immunity even in adult organisms. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01353-5. BioMed Central 2022-09-28 /pmc/articles/PMC9520927/ /pubmed/36171625 http://dx.doi.org/10.1186/s40168-022-01353-5 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Romero, Rossana
Zarzycka, Agnieszka
Preussner, Mathieu
Fischer, Florence
Hain, Torsten
Herrmann, Jan-Paul
Roth, Katrin
Keber, Corinna U.
Suryamohan, Kushal
Raifer, Hartmann
Luu, Maik
Leister, Hanna
Bertrams, Wilhelm
Klein, Matthias
Shams-Eldin, Hosam
Jacob, Ralf
Mollenkopf, Hans-Joachim
Rajalingam, Krishnaraj
Visekruna, Alexander
Steinhoff, Ulrich
Selected commensals educate the intestinal vascular and immune system for immunocompetence
title Selected commensals educate the intestinal vascular and immune system for immunocompetence
title_full Selected commensals educate the intestinal vascular and immune system for immunocompetence
title_fullStr Selected commensals educate the intestinal vascular and immune system for immunocompetence
title_full_unstemmed Selected commensals educate the intestinal vascular and immune system for immunocompetence
title_short Selected commensals educate the intestinal vascular and immune system for immunocompetence
title_sort selected commensals educate the intestinal vascular and immune system for immunocompetence
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9520927/
https://www.ncbi.nlm.nih.gov/pubmed/36171625
http://dx.doi.org/10.1186/s40168-022-01353-5
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