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Lymphoid Tissue–Resident Alcaligenes Establish an Intracellular Symbiotic Environment by Creating a Unique Energy Shift in Dendritic Cells

Lymphoid-tissue–resident commensal bacteria (LRCs), including Alcaligenes faecalis, are present in intestinal lymphoid tissue including the Peyer’s patches (PPs) of mammals and modulate the host immune system. Although LRCs can colonize within dendritic cells (DCs), the mechanisms through which LRCs...

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Autores principales: Hosomi, Koji, Shibata, Naoko, Shimoyama, Atsushi, Uto, Tomoya, Nagatake, Takahiro, Tojima, Yoko, Nishino, Tomomi, Takeyama, Haruko, Fukase, Koichi, Kiyono, Hiroshi, Kunisawa, Jun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7545135/
https://www.ncbi.nlm.nih.gov/pubmed/33101234
http://dx.doi.org/10.3389/fmicb.2020.561005
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author Hosomi, Koji
Shibata, Naoko
Shimoyama, Atsushi
Uto, Tomoya
Nagatake, Takahiro
Tojima, Yoko
Nishino, Tomomi
Takeyama, Haruko
Fukase, Koichi
Kiyono, Hiroshi
Kunisawa, Jun
author_facet Hosomi, Koji
Shibata, Naoko
Shimoyama, Atsushi
Uto, Tomoya
Nagatake, Takahiro
Tojima, Yoko
Nishino, Tomomi
Takeyama, Haruko
Fukase, Koichi
Kiyono, Hiroshi
Kunisawa, Jun
author_sort Hosomi, Koji
collection PubMed
description Lymphoid-tissue–resident commensal bacteria (LRCs), including Alcaligenes faecalis, are present in intestinal lymphoid tissue including the Peyer’s patches (PPs) of mammals and modulate the host immune system. Although LRCs can colonize within dendritic cells (DCs), the mechanisms through which LRCs persist in DCs and the symbiotic relationships between LRCs and DCs remain to be investigated. Here, we show an intracellular symbiotic system in which the LRC Alcaligenes creates a unique energy shift in DCs. Whereas DCs showed low mitochondrial respiration when they were co-cultured with Escherichia coli, DCs carrying A. faecalis maintained increased mitochondrial respiration. Furthermore, E. coli induced apoptosis of DCs but A. faecalis did not. Regarding an underlying mechanism, A. faecalis—unlike E. coli—did not induce intracellular nitric oxide (NO) production in DCs due to the low activity of its lipopolysaccharide (LPS). Therefore, A. faecalis, an example of LRCs, may persist within intestinal lymphoid tissue because they elicit little NO production in DCs. In addition, the symbiotic DCs exhibit characteristic physiologic changes, including a low rate of apoptosis and increased mitochondrial respiration.
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spelling pubmed-75451352020-10-22 Lymphoid Tissue–Resident Alcaligenes Establish an Intracellular Symbiotic Environment by Creating a Unique Energy Shift in Dendritic Cells Hosomi, Koji Shibata, Naoko Shimoyama, Atsushi Uto, Tomoya Nagatake, Takahiro Tojima, Yoko Nishino, Tomomi Takeyama, Haruko Fukase, Koichi Kiyono, Hiroshi Kunisawa, Jun Front Microbiol Microbiology Lymphoid-tissue–resident commensal bacteria (LRCs), including Alcaligenes faecalis, are present in intestinal lymphoid tissue including the Peyer’s patches (PPs) of mammals and modulate the host immune system. Although LRCs can colonize within dendritic cells (DCs), the mechanisms through which LRCs persist in DCs and the symbiotic relationships between LRCs and DCs remain to be investigated. Here, we show an intracellular symbiotic system in which the LRC Alcaligenes creates a unique energy shift in DCs. Whereas DCs showed low mitochondrial respiration when they were co-cultured with Escherichia coli, DCs carrying A. faecalis maintained increased mitochondrial respiration. Furthermore, E. coli induced apoptosis of DCs but A. faecalis did not. Regarding an underlying mechanism, A. faecalis—unlike E. coli—did not induce intracellular nitric oxide (NO) production in DCs due to the low activity of its lipopolysaccharide (LPS). Therefore, A. faecalis, an example of LRCs, may persist within intestinal lymphoid tissue because they elicit little NO production in DCs. In addition, the symbiotic DCs exhibit characteristic physiologic changes, including a low rate of apoptosis and increased mitochondrial respiration. Frontiers Media S.A. 2020-09-24 /pmc/articles/PMC7545135/ /pubmed/33101234 http://dx.doi.org/10.3389/fmicb.2020.561005 Text en Copyright © 2020 Hosomi, Shibata, Shimoyama, Uto, Nagatake, Tojima, Nishino, Takeyama, Fukase, Kiyono and Kunisawa. 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
Hosomi, Koji
Shibata, Naoko
Shimoyama, Atsushi
Uto, Tomoya
Nagatake, Takahiro
Tojima, Yoko
Nishino, Tomomi
Takeyama, Haruko
Fukase, Koichi
Kiyono, Hiroshi
Kunisawa, Jun
Lymphoid Tissue–Resident Alcaligenes Establish an Intracellular Symbiotic Environment by Creating a Unique Energy Shift in Dendritic Cells
title Lymphoid Tissue–Resident Alcaligenes Establish an Intracellular Symbiotic Environment by Creating a Unique Energy Shift in Dendritic Cells
title_full Lymphoid Tissue–Resident Alcaligenes Establish an Intracellular Symbiotic Environment by Creating a Unique Energy Shift in Dendritic Cells
title_fullStr Lymphoid Tissue–Resident Alcaligenes Establish an Intracellular Symbiotic Environment by Creating a Unique Energy Shift in Dendritic Cells
title_full_unstemmed Lymphoid Tissue–Resident Alcaligenes Establish an Intracellular Symbiotic Environment by Creating a Unique Energy Shift in Dendritic Cells
title_short Lymphoid Tissue–Resident Alcaligenes Establish an Intracellular Symbiotic Environment by Creating a Unique Energy Shift in Dendritic Cells
title_sort lymphoid tissue–resident alcaligenes establish an intracellular symbiotic environment by creating a unique energy shift in dendritic cells
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7545135/
https://www.ncbi.nlm.nih.gov/pubmed/33101234
http://dx.doi.org/10.3389/fmicb.2020.561005
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