Bone Marrow Dendritic Cells from Mice with an Altered Microbiota Provide Interleukin 17A-Dependent Protection against <named-content content-type="genus-species">Entamoeba histolytica</named-content> Colitis

ABSTRACT There is an emerging paradigm that the human microbiome is central to many aspects of health and may have a role in preventing enteric infection. Entamoeba histolytica is a major cause of amebic diarrhea in developing countries. It colonizes the colon lumen in close proximity to the gut mic...

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Autores principales:	Stacey L. Burgess, Erica Buonomo, Maureen Carey, Carrie Cowardin, Caitlin Naylor, Zannatun Noor, Marsha Wills-Karp, William A. Petri
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f76923db21fb432abd9d18ac44d2080a
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spelling	oai:doaj.org-article:f76923db21fb432abd9d18ac44d2080a2021-11-15T15:47:03ZBone Marrow Dendritic Cells from Mice with an Altered Microbiota Provide Interleukin 17A-Dependent Protection against <named-content content-type="genus-species">Entamoeba histolytica</named-content> Colitis10.1128/mBio.01817-142150-7511https://doaj.org/article/f76923db21fb432abd9d18ac44d2080a2014-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01817-14https://doaj.org/toc/2150-7511ABSTRACT There is an emerging paradigm that the human microbiome is central to many aspects of health and may have a role in preventing enteric infection. Entamoeba histolytica is a major cause of amebic diarrhea in developing countries. It colonizes the colon lumen in close proximity to the gut microbiota. Interestingly, not all individuals are equally susceptible to E. histolytica infection. Therefore, as the microbiota is highly variable within individuals, we sought to determine if a component of the microbiota could regulate susceptibility to infection. In studies utilizing a murine model, we demonstrated that colonization of the gut with the commensal Clostridia-related bacteria known as segmented filamentous bacteria (SFB) is protective during E. histolytica infection. SFB colonization in this model was associated with elevated cecal levels of interleukin 17A (IL-17A), dendritic cells, and neutrophils. Bone marrow-derived dendritic cells (BMDCs) from SFB-colonized mice had higher levels of IL-23 production in response to stimulation with trophozoites. Adoptive transfer of BMDCs from an SFB+ to an SFB− mouse was sufficient to provide protection against E. histolytica. IL-17A induction during BMDC transfer was necessary for this protection. This work demonstrates that intestinal colonization with a specific commensal bacterium can provide protection during amebiasis in a murine model. Most importantly, this work demonstrates that the microbiome can mediate protection against an enteric infection via extraintestinal effects on bone marrow-derived dendritic cells. IMPORTANCE Entamoeba histolytica is the causative agent of amebiasis, an infectious disease that contributes significantly to morbidity and mortality due to diarrhea in the developing world. We showed in a murine model that colonization with the commensal members of the Clostridia known as SFB provides protection against E. histolytica and that dendritic cells from SFB-colonized mice alone can recapitulate protection. Understanding interactions between enteropathogens, commensal intestinal bacteria, and the mucosal immune response, including dendritic cells, will help in the development of effective treatments for this disease and other infectious and inflammatory diseases. The demonstration of immune-mediated protection due to communication from the microbiome to the bone marrow represents an emerging field of study that will yield unique approaches to the development of these treatments.Stacey L. BurgessErica BuonomoMaureen CareyCarrie CowardinCaitlin NaylorZannatun NoorMarsha Wills-KarpWilliam A. PetriAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 6 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Stacey L. Burgess Erica Buonomo Maureen Carey Carrie Cowardin Caitlin Naylor Zannatun Noor Marsha Wills-Karp William A. Petri Bone Marrow Dendritic Cells from Mice with an Altered Microbiota Provide Interleukin 17A-Dependent Protection against <named-content content-type="genus-species">Entamoeba histolytica</named-content> Colitis
description	ABSTRACT There is an emerging paradigm that the human microbiome is central to many aspects of health and may have a role in preventing enteric infection. Entamoeba histolytica is a major cause of amebic diarrhea in developing countries. It colonizes the colon lumen in close proximity to the gut microbiota. Interestingly, not all individuals are equally susceptible to E. histolytica infection. Therefore, as the microbiota is highly variable within individuals, we sought to determine if a component of the microbiota could regulate susceptibility to infection. In studies utilizing a murine model, we demonstrated that colonization of the gut with the commensal Clostridia-related bacteria known as segmented filamentous bacteria (SFB) is protective during E. histolytica infection. SFB colonization in this model was associated with elevated cecal levels of interleukin 17A (IL-17A), dendritic cells, and neutrophils. Bone marrow-derived dendritic cells (BMDCs) from SFB-colonized mice had higher levels of IL-23 production in response to stimulation with trophozoites. Adoptive transfer of BMDCs from an SFB+ to an SFB− mouse was sufficient to provide protection against E. histolytica. IL-17A induction during BMDC transfer was necessary for this protection. This work demonstrates that intestinal colonization with a specific commensal bacterium can provide protection during amebiasis in a murine model. Most importantly, this work demonstrates that the microbiome can mediate protection against an enteric infection via extraintestinal effects on bone marrow-derived dendritic cells. IMPORTANCE Entamoeba histolytica is the causative agent of amebiasis, an infectious disease that contributes significantly to morbidity and mortality due to diarrhea in the developing world. We showed in a murine model that colonization with the commensal members of the Clostridia known as SFB provides protection against E. histolytica and that dendritic cells from SFB-colonized mice alone can recapitulate protection. Understanding interactions between enteropathogens, commensal intestinal bacteria, and the mucosal immune response, including dendritic cells, will help in the development of effective treatments for this disease and other infectious and inflammatory diseases. The demonstration of immune-mediated protection due to communication from the microbiome to the bone marrow represents an emerging field of study that will yield unique approaches to the development of these treatments.
format	article
author	Stacey L. Burgess Erica Buonomo Maureen Carey Carrie Cowardin Caitlin Naylor Zannatun Noor Marsha Wills-Karp William A. Petri
author_facet	Stacey L. Burgess Erica Buonomo Maureen Carey Carrie Cowardin Caitlin Naylor Zannatun Noor Marsha Wills-Karp William A. Petri
author_sort	Stacey L. Burgess
title	Bone Marrow Dendritic Cells from Mice with an Altered Microbiota Provide Interleukin 17A-Dependent Protection against <named-content content-type="genus-species">Entamoeba histolytica</named-content> Colitis
title_short	Bone Marrow Dendritic Cells from Mice with an Altered Microbiota Provide Interleukin 17A-Dependent Protection against <named-content content-type="genus-species">Entamoeba histolytica</named-content> Colitis
title_full	Bone Marrow Dendritic Cells from Mice with an Altered Microbiota Provide Interleukin 17A-Dependent Protection against <named-content content-type="genus-species">Entamoeba histolytica</named-content> Colitis
title_fullStr	Bone Marrow Dendritic Cells from Mice with an Altered Microbiota Provide Interleukin 17A-Dependent Protection against <named-content content-type="genus-species">Entamoeba histolytica</named-content> Colitis
title_full_unstemmed	Bone Marrow Dendritic Cells from Mice with an Altered Microbiota Provide Interleukin 17A-Dependent Protection against <named-content content-type="genus-species">Entamoeba histolytica</named-content> Colitis
title_sort	bone marrow dendritic cells from mice with an altered microbiota provide interleukin 17a-dependent protection against <named-content content-type="genus-species">entamoeba histolytica</named-content> colitis
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/f76923db21fb432abd9d18ac44d2080a
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Bone Marrow Dendritic Cells from Mice with an Altered Microbiota Provide Interleukin 17A-Dependent Protection against <named-content content-type="genus-species">Entamoeba histolytica</named-content> Colitis

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