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A species-specific activation of Toll-like receptor signaling in bovine and sheep bronchial epithelial cells triggered by Mycobacterial infections

•A differentiated bovine bronchial epithelial air–liquid interface model was established.•A species-specific TLR-mediated PAMP recognition in bovine and sheep airway epithelial cells was determined.•Mycobacteria triggered a species-specific TLR signaling in bovine and sheep airway epithelial cells.•...

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Published in:Molecular immunology 2016-03, Vol.71, p.23-33
Main Authors: Ma, Yan, Han, Fei, Liang, Jinping, Yang, Jiali, Shi, Juan, Xue, Jing, Yang, Li, Li, Yong, Luo, Meihui, Wang, Yujiong, Wei, Jun, Liu, Xiaoming
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description •A differentiated bovine bronchial epithelial air–liquid interface model was established.•A species-specific TLR-mediated PAMP recognition in bovine and sheep airway epithelial cells was determined.•Mycobacteria triggered a species-specific TLR signaling in bovine and sheep airway epithelial cells.•Mycobacteria infections induced a species-specific inflammatory response in bovine and sheep airway epithelial cells. Pulmonary tuberculosis caused by a Mycobacterium infection remains a major public health problem in most part of the world, in part owing to the transmission of its pathogens between hosts including human, domestic and wild animals. To date, molecular mechanisms of the pathogenesis of TB are still incompletely understood. In addition to alveolar macrophages, airway epithelial cells have also been recently recognized as main targets for Mycobacteria infections. In an effort to understand the pathogen-host interaction between Mycobacteria and airway epithelial cells in domestic animals, in present study, we investigated the Toll-like receptor (TLR) signaling in bovine and sheep airway epithelial cells in response to an infection of Mycobacterium tuberculosis avirulent H37Ra stain or Mycobacterium bovis BCG vaccine strain, using primary air–liquid interface (ALI) bronchial epithelial culture models. Our results revealed a host and pathogen species-specific TLR-mediated recognition of pathogen-associated molecular patterns (PAMPs), induction and activation of TLR signaling pathways, and substantial induction of inflammatory response in bronchial epithelial cells in response to Mycobacteria infections between these two species. Interestingly, the activation TLR signaling in bovine bronchial epithelial cells induced by Mycobacteria infection was mainly through a myeloid differentiation factor 88 (MyD88)-independent TLR signaling pathway, while both MyD88-dependent and independent TLR signaling cascades could be induced in sheep epithelial cells. Equally noteworthy, a BCG infection was able to induce both MyD88-dependent and independent signaling in sheep and bovine airway epithelial cells, but more robust inflammatory responses were induced in sheep epithelial cells relative to the bovines; whereas an H37Ra infection displayed an ability to mainly trigger a MyD88-independent TLR signaling cascade in these two host species, and induce a more extent expression of inflammatory cytokines in bovine cells in comparison with that in sheep. These data thus pro
doi_str_mv 10.1016/j.molimm.2016.01.004
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Pulmonary tuberculosis caused by a Mycobacterium infection remains a major public health problem in most part of the world, in part owing to the transmission of its pathogens between hosts including human, domestic and wild animals. To date, molecular mechanisms of the pathogenesis of TB are still incompletely understood. In addition to alveolar macrophages, airway epithelial cells have also been recently recognized as main targets for Mycobacteria infections. In an effort to understand the pathogen-host interaction between Mycobacteria and airway epithelial cells in domestic animals, in present study, we investigated the Toll-like receptor (TLR) signaling in bovine and sheep airway epithelial cells in response to an infection of Mycobacterium tuberculosis avirulent H37Ra stain or Mycobacterium bovis BCG vaccine strain, using primary air–liquid interface (ALI) bronchial epithelial culture models. Our results revealed a host and pathogen species-specific TLR-mediated recognition of pathogen-associated molecular patterns (PAMPs), induction and activation of TLR signaling pathways, and substantial induction of inflammatory response in bronchial epithelial cells in response to Mycobacteria infections between these two species. Interestingly, the activation TLR signaling in bovine bronchial epithelial cells induced by Mycobacteria infection was mainly through a myeloid differentiation factor 88 (MyD88)-independent TLR signaling pathway, while both MyD88-dependent and independent TLR signaling cascades could be induced in sheep epithelial cells. Equally noteworthy, a BCG infection was able to induce both MyD88-dependent and independent signaling in sheep and bovine airway epithelial cells, but more robust inflammatory responses were induced in sheep epithelial cells relative to the bovines; whereas an H37Ra infection displayed an ability to mainly trigger a MyD88-independent TLR signaling cascade in these two host species, and induce a more extent expression of inflammatory cytokines in bovine cells in comparison with that in sheep. These data thus provide an evidence for a host and pathogen species-specific response in bovine and sheep airway epithelial cells in response to Mycobacteria infections, which also suggest there is a need to consider in the interpretation of data generated using a species other than the primary host for analysis of a function role or mechanism of ligands or pathogens.</description><identifier>ISSN: 0161-5890</identifier><identifier>EISSN: 1872-9142</identifier><identifier>DOI: 10.1016/j.molimm.2016.01.004</identifier><identifier>PMID: 26802731</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Airway epithelial cells ; Animals ; Blotting, Western ; Bovine ; Bronchi - immunology ; Bronchi - metabolism ; Bronchi - microbiology ; Cattle ; Disease Models, Animal ; Fluorescent Antibody Technique ; Microscopy, Electron ; Mycobacterium bovis ; Mycobacterium infection ; Mycobacterium tuberculosis ; Real-Time Polymerase Chain Reaction ; Respiratory Mucosa - immunology ; Respiratory Mucosa - metabolism ; Respiratory Mucosa - microbiology ; Sheep ; Signal Transduction - immunology ; Species Specificity ; Species-specific recognition ; Toll-like receptor signaling ; Toll-Like Receptors - immunology ; Toll-Like Receptors - metabolism ; Tuberculosis, Pulmonary - immunology ; Tuberculosis, Pulmonary - metabolism</subject><ispartof>Molecular immunology, 2016-03, Vol.71, p.23-33</ispartof><rights>2016 Elsevier Ltd</rights><rights>Copyright © 2016 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c395t-24f47996e2c12396273f289ce17b27bde37a043267e6de3b1d70d94a296376363</citedby><cites>FETCH-LOGICAL-c395t-24f47996e2c12396273f289ce17b27bde37a043267e6de3b1d70d94a296376363</cites><orcidid>0000-0001-8006-1409</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26802731$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ma, Yan</creatorcontrib><creatorcontrib>Han, Fei</creatorcontrib><creatorcontrib>Liang, Jinping</creatorcontrib><creatorcontrib>Yang, Jiali</creatorcontrib><creatorcontrib>Shi, Juan</creatorcontrib><creatorcontrib>Xue, Jing</creatorcontrib><creatorcontrib>Yang, Li</creatorcontrib><creatorcontrib>Li, Yong</creatorcontrib><creatorcontrib>Luo, Meihui</creatorcontrib><creatorcontrib>Wang, Yujiong</creatorcontrib><creatorcontrib>Wei, Jun</creatorcontrib><creatorcontrib>Liu, Xiaoming</creatorcontrib><title>A species-specific activation of Toll-like receptor signaling in bovine and sheep bronchial epithelial cells triggered by Mycobacterial infections</title><title>Molecular immunology</title><addtitle>Mol Immunol</addtitle><description>•A differentiated bovine bronchial epithelial air–liquid interface model was established.•A species-specific TLR-mediated PAMP recognition in bovine and sheep airway epithelial cells was determined.•Mycobacteria triggered a species-specific TLR signaling in bovine and sheep airway epithelial cells.•Mycobacteria infections induced a species-specific inflammatory response in bovine and sheep airway epithelial cells. Pulmonary tuberculosis caused by a Mycobacterium infection remains a major public health problem in most part of the world, in part owing to the transmission of its pathogens between hosts including human, domestic and wild animals. To date, molecular mechanisms of the pathogenesis of TB are still incompletely understood. In addition to alveolar macrophages, airway epithelial cells have also been recently recognized as main targets for Mycobacteria infections. In an effort to understand the pathogen-host interaction between Mycobacteria and airway epithelial cells in domestic animals, in present study, we investigated the Toll-like receptor (TLR) signaling in bovine and sheep airway epithelial cells in response to an infection of Mycobacterium tuberculosis avirulent H37Ra stain or Mycobacterium bovis BCG vaccine strain, using primary air–liquid interface (ALI) bronchial epithelial culture models. 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Equally noteworthy, a BCG infection was able to induce both MyD88-dependent and independent signaling in sheep and bovine airway epithelial cells, but more robust inflammatory responses were induced in sheep epithelial cells relative to the bovines; whereas an H37Ra infection displayed an ability to mainly trigger a MyD88-independent TLR signaling cascade in these two host species, and induce a more extent expression of inflammatory cytokines in bovine cells in comparison with that in sheep. 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Pulmonary tuberculosis caused by a Mycobacterium infection remains a major public health problem in most part of the world, in part owing to the transmission of its pathogens between hosts including human, domestic and wild animals. To date, molecular mechanisms of the pathogenesis of TB are still incompletely understood. In addition to alveolar macrophages, airway epithelial cells have also been recently recognized as main targets for Mycobacteria infections. In an effort to understand the pathogen-host interaction between Mycobacteria and airway epithelial cells in domestic animals, in present study, we investigated the Toll-like receptor (TLR) signaling in bovine and sheep airway epithelial cells in response to an infection of Mycobacterium tuberculosis avirulent H37Ra stain or Mycobacterium bovis BCG vaccine strain, using primary air–liquid interface (ALI) bronchial epithelial culture models. Our results revealed a host and pathogen species-specific TLR-mediated recognition of pathogen-associated molecular patterns (PAMPs), induction and activation of TLR signaling pathways, and substantial induction of inflammatory response in bronchial epithelial cells in response to Mycobacteria infections between these two species. Interestingly, the activation TLR signaling in bovine bronchial epithelial cells induced by Mycobacteria infection was mainly through a myeloid differentiation factor 88 (MyD88)-independent TLR signaling pathway, while both MyD88-dependent and independent TLR signaling cascades could be induced in sheep epithelial cells. Equally noteworthy, a BCG infection was able to induce both MyD88-dependent and independent signaling in sheep and bovine airway epithelial cells, but more robust inflammatory responses were induced in sheep epithelial cells relative to the bovines; whereas an H37Ra infection displayed an ability to mainly trigger a MyD88-independent TLR signaling cascade in these two host species, and induce a more extent expression of inflammatory cytokines in bovine cells in comparison with that in sheep. These data thus provide an evidence for a host and pathogen species-specific response in bovine and sheep airway epithelial cells in response to Mycobacteria infections, which also suggest there is a need to consider in the interpretation of data generated using a species other than the primary host for analysis of a function role or mechanism of ligands or pathogens.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>26802731</pmid><doi>10.1016/j.molimm.2016.01.004</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0001-8006-1409</orcidid></addata></record>
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ispartof Molecular immunology, 2016-03, Vol.71, p.23-33
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source ScienceDirect Journals
subjects Airway epithelial cells
Animals
Blotting, Western
Bovine
Bronchi - immunology
Bronchi - metabolism
Bronchi - microbiology
Cattle
Disease Models, Animal
Fluorescent Antibody Technique
Microscopy, Electron
Mycobacterium bovis
Mycobacterium infection
Mycobacterium tuberculosis
Real-Time Polymerase Chain Reaction
Respiratory Mucosa - immunology
Respiratory Mucosa - metabolism
Respiratory Mucosa - microbiology
Sheep
Signal Transduction - immunology
Species Specificity
Species-specific recognition
Toll-like receptor signaling
Toll-Like Receptors - immunology
Toll-Like Receptors - metabolism
Tuberculosis, Pulmonary - immunology
Tuberculosis, Pulmonary - metabolism
title A species-specific activation of Toll-like receptor signaling in bovine and sheep bronchial epithelial cells triggered by Mycobacterial infections
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