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Salmonella detoxifying enzymes are sufficient to cope with the host oxidative burst
Summary The oxidative burst produced by the NADPH oxidase (Phox) is an essential weapon used by host cells to eradicate engulfed pathogens. In Salmonella typhimurium, oxidative stress resistance has been previously proposed to be mediated by the pathogenicity island 2 type III secretion system (T3SS...
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Published in: | Molecular microbiology 2011-05, Vol.80 (3), p.628-640 |
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creator | Aussel, Laurent Zhao, Weidong Hébrard, Magali Guilhon, Aude‐Agnès Viala, Julie P. M. Henri, Sandrine Chasson, Lionel Gorvel, Jean‐Pierre Barras, Frédéric Méresse, Stéphane |
description | Summary
The oxidative burst produced by the NADPH oxidase (Phox) is an essential weapon used by host cells to eradicate engulfed pathogens. In Salmonella typhimurium, oxidative stress resistance has been previously proposed to be mediated by the pathogenicity island 2 type III secretion system (T3SS‐2), periplasmic superoxide dismutases and cytoplasmic catalases/peroxidases. Here, we fused an OxyR‐dependent promoter to the gfp to build the ahpC‐gfp transcriptional fusion. This reporter was used to monitor hydrogen peroxide levels as sensed by Salmonella during the course of an infection. We showed that the expression of this fusion was under the exclusive control of reactive oxygen species produced by the host. The ahpC‐gfp expression was noticeably modified in the absence of bacterial periplasmic superoxide dismutases or cytoplasmic catalases/peroxidases. Surprisingly, inactivation of the T3SS‐2 had no effect on the ahpC‐gfp expression. All together, these results led to a model in which Salmonella resistance relies on its arsenal of detoxifying enzymes to cope with Phox‐mediated oxidative stress. |
doi_str_mv | 10.1111/j.1365-2958.2011.07611.x |
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The oxidative burst produced by the NADPH oxidase (Phox) is an essential weapon used by host cells to eradicate engulfed pathogens. In Salmonella typhimurium, oxidative stress resistance has been previously proposed to be mediated by the pathogenicity island 2 type III secretion system (T3SS‐2), periplasmic superoxide dismutases and cytoplasmic catalases/peroxidases. Here, we fused an OxyR‐dependent promoter to the gfp to build the ahpC‐gfp transcriptional fusion. This reporter was used to monitor hydrogen peroxide levels as sensed by Salmonella during the course of an infection. We showed that the expression of this fusion was under the exclusive control of reactive oxygen species produced by the host. The ahpC‐gfp expression was noticeably modified in the absence of bacterial periplasmic superoxide dismutases or cytoplasmic catalases/peroxidases. Surprisingly, inactivation of the T3SS‐2 had no effect on the ahpC‐gfp expression. All together, these results led to a model in which Salmonella resistance relies on its arsenal of detoxifying enzymes to cope with Phox‐mediated oxidative stress.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/j.1365-2958.2011.07611.x</identifier><identifier>PMID: 21362067</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Animals ; Artificial Gene Fusion ; Bacteriology ; Biological and medical sciences ; Cells, Cultured ; Disease Models, Animal ; Enzymes ; Fundamental and applied biological sciences. Psychology ; Gene expression ; Gene Expression Profiling ; Genes, Reporter ; Green Fluorescent Proteins - genetics ; Green Fluorescent Proteins - metabolism ; Hydrogen Peroxide - metabolism ; Immunology ; Inactivation, Metabolic ; Life Sciences ; Macrophages - microbiology ; Mice ; Mice, Inbred C57BL ; Microbial Viability - drug effects ; Microbiology ; Miscellaneous ; Oxidative stress ; Phagosomes - metabolism ; Phagosomes - microbiology ; Reactive Oxygen Species - metabolism ; Respiratory Burst ; Salmonella ; Salmonella Infections, Animal - immunology ; Salmonella Infections, Animal - microbiology ; Salmonella typhimurium ; Salmonella typhimurium - drug effects ; Salmonella typhimurium - physiology ; Spleen - microbiology ; Superoxides - metabolism</subject><ispartof>Molecular microbiology, 2011-05, Vol.80 (3), p.628-640</ispartof><rights>2011 Blackwell Publishing Ltd</rights><rights>2015 INIST-CNRS</rights><rights>2011 Blackwell Publishing Ltd.</rights><rights>Copyright Blackwell Publishing Ltd. May 2011</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5411-f604f780bf42a19a81ddbcbd7c0ef4fa2b830a6d1dcf5f47f1e2a57b272994a03</citedby><cites>FETCH-LOGICAL-c5411-f604f780bf42a19a81ddbcbd7c0ef4fa2b830a6d1dcf5f47f1e2a57b272994a03</cites><orcidid>0000-0003-4083-626X ; 0000-0002-8980-9193 ; 0000-0003-3458-2574 ; 0000-0002-2829-9804 ; 0000-0001-6578-5177</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,778,782,883,27907,27908</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=24128332$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21362067$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-00611571$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Aussel, Laurent</creatorcontrib><creatorcontrib>Zhao, Weidong</creatorcontrib><creatorcontrib>Hébrard, Magali</creatorcontrib><creatorcontrib>Guilhon, Aude‐Agnès</creatorcontrib><creatorcontrib>Viala, Julie P. M.</creatorcontrib><creatorcontrib>Henri, Sandrine</creatorcontrib><creatorcontrib>Chasson, Lionel</creatorcontrib><creatorcontrib>Gorvel, Jean‐Pierre</creatorcontrib><creatorcontrib>Barras, Frédéric</creatorcontrib><creatorcontrib>Méresse, Stéphane</creatorcontrib><title>Salmonella detoxifying enzymes are sufficient to cope with the host oxidative burst</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Summary
The oxidative burst produced by the NADPH oxidase (Phox) is an essential weapon used by host cells to eradicate engulfed pathogens. In Salmonella typhimurium, oxidative stress resistance has been previously proposed to be mediated by the pathogenicity island 2 type III secretion system (T3SS‐2), periplasmic superoxide dismutases and cytoplasmic catalases/peroxidases. Here, we fused an OxyR‐dependent promoter to the gfp to build the ahpC‐gfp transcriptional fusion. This reporter was used to monitor hydrogen peroxide levels as sensed by Salmonella during the course of an infection. We showed that the expression of this fusion was under the exclusive control of reactive oxygen species produced by the host. The ahpC‐gfp expression was noticeably modified in the absence of bacterial periplasmic superoxide dismutases or cytoplasmic catalases/peroxidases. Surprisingly, inactivation of the T3SS‐2 had no effect on the ahpC‐gfp expression. All together, these results led to a model in which Salmonella resistance relies on its arsenal of detoxifying enzymes to cope with Phox‐mediated oxidative stress.</description><subject>Animals</subject><subject>Artificial Gene Fusion</subject><subject>Bacteriology</subject><subject>Biological and medical sciences</subject><subject>Cells, Cultured</subject><subject>Disease Models, Animal</subject><subject>Enzymes</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Genes, Reporter</subject><subject>Green Fluorescent Proteins - genetics</subject><subject>Green Fluorescent Proteins - metabolism</subject><subject>Hydrogen Peroxide - metabolism</subject><subject>Immunology</subject><subject>Inactivation, Metabolic</subject><subject>Life Sciences</subject><subject>Macrophages - microbiology</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Microbial Viability - drug effects</subject><subject>Microbiology</subject><subject>Miscellaneous</subject><subject>Oxidative stress</subject><subject>Phagosomes - metabolism</subject><subject>Phagosomes - microbiology</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Respiratory Burst</subject><subject>Salmonella</subject><subject>Salmonella Infections, Animal - immunology</subject><subject>Salmonella Infections, Animal - microbiology</subject><subject>Salmonella typhimurium</subject><subject>Salmonella typhimurium - drug effects</subject><subject>Salmonella typhimurium - physiology</subject><subject>Spleen - microbiology</subject><subject>Superoxides - metabolism</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><recordid>eNqN0U2P1CAYB3BiNO64-hUMMTEbDx0fXgrtwcNmo-4ms_GwmngjlILDpC0jtLszfnqpM46JF4WENvB7CPBHCBNYktzebpaEibKgdVktKRCyBCnyuHuEFqeFx2gBdQkFq-jXM_QspQ0AYSDYU3RGs6Ig5ALd3emuD4PtOo1bO4add3s_fMN2-LHvbcI6Wpwm57zxdhjxGLAJW4sf_LjG49ridUgjzlWtHv29xc0U0_gcPXG6S_bF8XuOvnx4__nqulh9-nhzdbkqTMkJKZwA7mQFjeNUk1pXpG0b07TSgHXcadpUDLRoSWtc6bh0xFJdyoZKWtdcAztHbw77rnWnttH3Ou5V0F5dX67UPAeQX6WU5J5ke3Gw2xi-TzaNqvfJzNcebJiSqkESwXjN_ymrzGiGIstXf8lNmOKQr5yRKHOHKqPqgEwMKUXrTicloOYw1UbNmak5MzWHqX6FqXa59OVx_6npbXsq_J1eBq-PQCejOxf1YHz64zihFWM0u3cH9-A7u__vA6jb25v5j_0Esxq5kw</recordid><startdate>201105</startdate><enddate>201105</enddate><creator>Aussel, Laurent</creator><creator>Zhao, Weidong</creator><creator>Hébrard, Magali</creator><creator>Guilhon, Aude‐Agnès</creator><creator>Viala, Julie P. M.</creator><creator>Henri, Sandrine</creator><creator>Chasson, Lionel</creator><creator>Gorvel, Jean‐Pierre</creator><creator>Barras, Frédéric</creator><creator>Méresse, Stéphane</creator><general>Blackwell Publishing Ltd</general><general>Blackwell</general><general>Wiley</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0003-4083-626X</orcidid><orcidid>https://orcid.org/0000-0002-8980-9193</orcidid><orcidid>https://orcid.org/0000-0003-3458-2574</orcidid><orcidid>https://orcid.org/0000-0002-2829-9804</orcidid><orcidid>https://orcid.org/0000-0001-6578-5177</orcidid></search><sort><creationdate>201105</creationdate><title>Salmonella detoxifying enzymes are sufficient to cope with the host oxidative burst</title><author>Aussel, Laurent ; Zhao, Weidong ; Hébrard, Magali ; Guilhon, Aude‐Agnès ; Viala, Julie P. 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Psychology</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Genes, Reporter</topic><topic>Green Fluorescent Proteins - genetics</topic><topic>Green Fluorescent Proteins - metabolism</topic><topic>Hydrogen Peroxide - metabolism</topic><topic>Immunology</topic><topic>Inactivation, Metabolic</topic><topic>Life Sciences</topic><topic>Macrophages - microbiology</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Microbial Viability - drug effects</topic><topic>Microbiology</topic><topic>Miscellaneous</topic><topic>Oxidative stress</topic><topic>Phagosomes - metabolism</topic><topic>Phagosomes - microbiology</topic><topic>Reactive Oxygen Species - metabolism</topic><topic>Respiratory Burst</topic><topic>Salmonella</topic><topic>Salmonella Infections, Animal - immunology</topic><topic>Salmonella Infections, Animal - microbiology</topic><topic>Salmonella typhimurium</topic><topic>Salmonella typhimurium - drug effects</topic><topic>Salmonella typhimurium - physiology</topic><topic>Spleen - microbiology</topic><topic>Superoxides - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Aussel, Laurent</creatorcontrib><creatorcontrib>Zhao, Weidong</creatorcontrib><creatorcontrib>Hébrard, Magali</creatorcontrib><creatorcontrib>Guilhon, Aude‐Agnès</creatorcontrib><creatorcontrib>Viala, Julie P. 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M.</au><au>Henri, Sandrine</au><au>Chasson, Lionel</au><au>Gorvel, Jean‐Pierre</au><au>Barras, Frédéric</au><au>Méresse, Stéphane</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Salmonella detoxifying enzymes are sufficient to cope with the host oxidative burst</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2011-05</date><risdate>2011</risdate><volume>80</volume><issue>3</issue><spage>628</spage><epage>640</epage><pages>628-640</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Summary
The oxidative burst produced by the NADPH oxidase (Phox) is an essential weapon used by host cells to eradicate engulfed pathogens. In Salmonella typhimurium, oxidative stress resistance has been previously proposed to be mediated by the pathogenicity island 2 type III secretion system (T3SS‐2), periplasmic superoxide dismutases and cytoplasmic catalases/peroxidases. Here, we fused an OxyR‐dependent promoter to the gfp to build the ahpC‐gfp transcriptional fusion. This reporter was used to monitor hydrogen peroxide levels as sensed by Salmonella during the course of an infection. We showed that the expression of this fusion was under the exclusive control of reactive oxygen species produced by the host. The ahpC‐gfp expression was noticeably modified in the absence of bacterial periplasmic superoxide dismutases or cytoplasmic catalases/peroxidases. Surprisingly, inactivation of the T3SS‐2 had no effect on the ahpC‐gfp expression. All together, these results led to a model in which Salmonella resistance relies on its arsenal of detoxifying enzymes to cope with Phox‐mediated oxidative stress.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>21362067</pmid><doi>10.1111/j.1365-2958.2011.07611.x</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0003-4083-626X</orcidid><orcidid>https://orcid.org/0000-0002-8980-9193</orcidid><orcidid>https://orcid.org/0000-0003-3458-2574</orcidid><orcidid>https://orcid.org/0000-0002-2829-9804</orcidid><orcidid>https://orcid.org/0000-0001-6578-5177</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Artificial Gene Fusion Bacteriology Biological and medical sciences Cells, Cultured Disease Models, Animal Enzymes Fundamental and applied biological sciences. Psychology Gene expression Gene Expression Profiling Genes, Reporter Green Fluorescent Proteins - genetics Green Fluorescent Proteins - metabolism Hydrogen Peroxide - metabolism Immunology Inactivation, Metabolic Life Sciences Macrophages - microbiology Mice Mice, Inbred C57BL Microbial Viability - drug effects Microbiology Miscellaneous Oxidative stress Phagosomes - metabolism Phagosomes - microbiology Reactive Oxygen Species - metabolism Respiratory Burst Salmonella Salmonella Infections, Animal - immunology Salmonella Infections, Animal - microbiology Salmonella typhimurium Salmonella typhimurium - drug effects Salmonella typhimurium - physiology Spleen - microbiology Superoxides - metabolism |
title | Salmonella detoxifying enzymes are sufficient to cope with the host oxidative burst |
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