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Antigen Sampling CSF1R-Expressing Epithelial Cells Are the Functional Equivalents of Mammalian M Cells in the Avian Follicle-Associated Epithelium

The follicle-associated epithelium (FAE) is a specialized structure that samples luminal antigens and transports them into mucosa-associated lymphoid tissues (MALT). In mammals, transcytosis of antigens across the gut epithelium is performed by a subset of FAE cells known as M cells. Here we show th...

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Autores principales: Balic, Adam, Chintoan-Uta, Cosmin, Vohra, Prerna, Sutton, Kate M., Cassady-Cain, Robin L., Hu, Tuan, Donaldson, David S., Stevens, Mark P., Mabbott, Neil A., Hume, David A., Sang, Helen M., Vervelde, Lonneke
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6817575/
https://www.ncbi.nlm.nih.gov/pubmed/31695701
http://dx.doi.org/10.3389/fimmu.2019.02495
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author Balic, Adam
Chintoan-Uta, Cosmin
Vohra, Prerna
Sutton, Kate M.
Cassady-Cain, Robin L.
Hu, Tuan
Donaldson, David S.
Stevens, Mark P.
Mabbott, Neil A.
Hume, David A.
Sang, Helen M.
Vervelde, Lonneke
author_facet Balic, Adam
Chintoan-Uta, Cosmin
Vohra, Prerna
Sutton, Kate M.
Cassady-Cain, Robin L.
Hu, Tuan
Donaldson, David S.
Stevens, Mark P.
Mabbott, Neil A.
Hume, David A.
Sang, Helen M.
Vervelde, Lonneke
author_sort Balic, Adam
collection PubMed
description The follicle-associated epithelium (FAE) is a specialized structure that samples luminal antigens and transports them into mucosa-associated lymphoid tissues (MALT). In mammals, transcytosis of antigens across the gut epithelium is performed by a subset of FAE cells known as M cells. Here we show that colony-stimulating factor 1 receptor (CSF1R) is expressed by a subset of cells in the avian bursa of Fabricius FAE. Expression was initially detected using a CSF1R-reporter transgene that also label subsets of bursal macrophages. Immunohistochemical detection using a specific monoclonal antibody confirmed abundant expression of CSF1R on the basolateral membrane of FAE cells. CSF1R-transgene expressing bursal FAE cells were enriched for expression of markers previously reported as putative M cell markers, including annexin A10 and CD44. They were further distinguished from a population of CSF1R-transgene negative epithelial cells within FAE by high apical F-actin expression and differential staining with the lectins jacalin, PHA-L and SNA. Bursal FAE cells that express the CSF1R-reporter transgene were responsible for the bulk of FAE transcytosis of labeled microparticles in the size range 0.02–0.1 μm. Unlike mammalian M cells, they did not readily take up larger bacterial sized microparticles (0.5 μm). Their role in uptake of bacteria was tested using Salmonella, which can enter via M cells in mammals. Labeled Salmonella enterica serovar Typhimurium entered bursal tissue via the FAE. Entry was partially dependent upon Type III secretion system-1. However, the majority of invading bacteria were localized to CSF1R-negative FAE cells and in resident phagocytes that express the phosphatidylserine receptor TIM4. CSF1R-expressing FAE cells in infected follicles showed evidence of cell death and shedding into the bursal lumen. In mammals, CSF1R expression in the gut is restricted to macrophages which only indirectly control M cell differentiation. The novel expression of CSF1R in birds suggests that these functional equivalents to mammalian M cells may have different ontological origins and their development and function are likely to be regulated by different growth factors.
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spelling pubmed-68175752019-11-06 Antigen Sampling CSF1R-Expressing Epithelial Cells Are the Functional Equivalents of Mammalian M Cells in the Avian Follicle-Associated Epithelium Balic, Adam Chintoan-Uta, Cosmin Vohra, Prerna Sutton, Kate M. Cassady-Cain, Robin L. Hu, Tuan Donaldson, David S. Stevens, Mark P. Mabbott, Neil A. Hume, David A. Sang, Helen M. Vervelde, Lonneke Front Immunol Immunology The follicle-associated epithelium (FAE) is a specialized structure that samples luminal antigens and transports them into mucosa-associated lymphoid tissues (MALT). In mammals, transcytosis of antigens across the gut epithelium is performed by a subset of FAE cells known as M cells. Here we show that colony-stimulating factor 1 receptor (CSF1R) is expressed by a subset of cells in the avian bursa of Fabricius FAE. Expression was initially detected using a CSF1R-reporter transgene that also label subsets of bursal macrophages. Immunohistochemical detection using a specific monoclonal antibody confirmed abundant expression of CSF1R on the basolateral membrane of FAE cells. CSF1R-transgene expressing bursal FAE cells were enriched for expression of markers previously reported as putative M cell markers, including annexin A10 and CD44. They were further distinguished from a population of CSF1R-transgene negative epithelial cells within FAE by high apical F-actin expression and differential staining with the lectins jacalin, PHA-L and SNA. Bursal FAE cells that express the CSF1R-reporter transgene were responsible for the bulk of FAE transcytosis of labeled microparticles in the size range 0.02–0.1 μm. Unlike mammalian M cells, they did not readily take up larger bacterial sized microparticles (0.5 μm). Their role in uptake of bacteria was tested using Salmonella, which can enter via M cells in mammals. Labeled Salmonella enterica serovar Typhimurium entered bursal tissue via the FAE. Entry was partially dependent upon Type III secretion system-1. However, the majority of invading bacteria were localized to CSF1R-negative FAE cells and in resident phagocytes that express the phosphatidylserine receptor TIM4. CSF1R-expressing FAE cells in infected follicles showed evidence of cell death and shedding into the bursal lumen. In mammals, CSF1R expression in the gut is restricted to macrophages which only indirectly control M cell differentiation. The novel expression of CSF1R in birds suggests that these functional equivalents to mammalian M cells may have different ontological origins and their development and function are likely to be regulated by different growth factors. Frontiers Media S.A. 2019-10-22 /pmc/articles/PMC6817575/ /pubmed/31695701 http://dx.doi.org/10.3389/fimmu.2019.02495 Text en Copyright © 2019 Balic, Chintoan-Uta, Vohra, Sutton, Cassady-Cain, Hu, Donaldson, Stevens, Mabbott, Hume, Sang and Vervelde. 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 Immunology
Balic, Adam
Chintoan-Uta, Cosmin
Vohra, Prerna
Sutton, Kate M.
Cassady-Cain, Robin L.
Hu, Tuan
Donaldson, David S.
Stevens, Mark P.
Mabbott, Neil A.
Hume, David A.
Sang, Helen M.
Vervelde, Lonneke
Antigen Sampling CSF1R-Expressing Epithelial Cells Are the Functional Equivalents of Mammalian M Cells in the Avian Follicle-Associated Epithelium
title Antigen Sampling CSF1R-Expressing Epithelial Cells Are the Functional Equivalents of Mammalian M Cells in the Avian Follicle-Associated Epithelium
title_full Antigen Sampling CSF1R-Expressing Epithelial Cells Are the Functional Equivalents of Mammalian M Cells in the Avian Follicle-Associated Epithelium
title_fullStr Antigen Sampling CSF1R-Expressing Epithelial Cells Are the Functional Equivalents of Mammalian M Cells in the Avian Follicle-Associated Epithelium
title_full_unstemmed Antigen Sampling CSF1R-Expressing Epithelial Cells Are the Functional Equivalents of Mammalian M Cells in the Avian Follicle-Associated Epithelium
title_short Antigen Sampling CSF1R-Expressing Epithelial Cells Are the Functional Equivalents of Mammalian M Cells in the Avian Follicle-Associated Epithelium
title_sort antigen sampling csf1r-expressing epithelial cells are the functional equivalents of mammalian m cells in the avian follicle-associated epithelium
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6817575/
https://www.ncbi.nlm.nih.gov/pubmed/31695701
http://dx.doi.org/10.3389/fimmu.2019.02495
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