Vibrio VopQ induces PI3-kinase-independent autophagy and antagonizes phagocytosis
Vibrio parahaemolyticus is a Gram-negative bacterium responsible for gastroenteritis acquired from the consumption of contaminated shellfish. This bacterium harbours two type III secretion systems, one on each chromosome. The type III secretion system on chromosome I induces cell death by a temporal...
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Veröffentlicht in: | Molecular microbiology 2009-08, Vol.73 (4), p.639-649 |
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description | Vibrio parahaemolyticus is a Gram-negative bacterium responsible for gastroenteritis acquired from the consumption of contaminated shellfish. This bacterium harbours two type III secretion systems, one on each chromosome. The type III secretion system on chromosome I induces cell death by a temporally controlled sequence of events that is caspase-independent and first involves induction of autophagy, followed by cellular rounding, and finally cellular lysis. VopQ is a type III secreted effector that is necessary for the induction of autophagy as mutant strains lacking VopQ are attenuated in their ability to induce autophagy during infection. VopQ is sufficient to induce rapid autophagy as demonstrated by microinjection of recombinant VopQ into GFP-LC3 HeLa cells. Our results demonstrate that VopQ is both necessary and sufficient for induction of autophagy during V. parahaemolyticus-mediated cell death and this effect is independent of phosphatidylinositol-3-kinases but requires Atg5. Furthermore, induction of VopQ-mediated autophagy prevents recruitment of the necessary cellular machinery required for phagocytosis of V. parahaemolyticus during infection. These data provide important insights into the mechanism used by V. parahaemolyticus to cause disease. |
doi_str_mv | 10.1111/j.1365-2958.2009.06798.x |
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This bacterium harbours two type III secretion systems, one on each chromosome. The type III secretion system on chromosome I induces cell death by a temporally controlled sequence of events that is caspase-independent and first involves induction of autophagy, followed by cellular rounding, and finally cellular lysis. VopQ is a type III secreted effector that is necessary for the induction of autophagy as mutant strains lacking VopQ are attenuated in their ability to induce autophagy during infection. VopQ is sufficient to induce rapid autophagy as demonstrated by microinjection of recombinant VopQ into GFP-LC3 HeLa cells. Our results demonstrate that VopQ is both necessary and sufficient for induction of autophagy during V. parahaemolyticus-mediated cell death and this effect is independent of phosphatidylinositol-3-kinases but requires Atg5. Furthermore, induction of VopQ-mediated autophagy prevents recruitment of the necessary cellular machinery required for phagocytosis of V. parahaemolyticus during infection. These data provide important insights into the mechanism used by V. parahaemolyticus to cause disease.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/j.1365-2958.2009.06798.x</identifier><identifier>PMID: 19627496</identifier><language>eng</language><publisher>Oxford, UK: Oxford, UK : Blackwell Publishing Ltd</publisher><subject>Autophagy ; Autophagy-Related Protein 5 ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Gene Expression Regulation, Bacterial ; HeLa Cells ; Humans ; Microtubule-Associated Proteins - metabolism ; Phagocytosis ; Phosphatidylinositol 3-Kinases - metabolism ; Vibrio ; Vibrio Infections - microbiology ; Vibrio parahaemolyticus ; Vibrio parahaemolyticus - genetics ; Vibrio parahaemolyticus - metabolism ; Vibrio parahaemolyticus - pathogenicity</subject><ispartof>Molecular microbiology, 2009-08, Vol.73 (4), p.639-649</ispartof><rights>2009 The Authors. 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This bacterium harbours two type III secretion systems, one on each chromosome. The type III secretion system on chromosome I induces cell death by a temporally controlled sequence of events that is caspase-independent and first involves induction of autophagy, followed by cellular rounding, and finally cellular lysis. VopQ is a type III secreted effector that is necessary for the induction of autophagy as mutant strains lacking VopQ are attenuated in their ability to induce autophagy during infection. VopQ is sufficient to induce rapid autophagy as demonstrated by microinjection of recombinant VopQ into GFP-LC3 HeLa cells. Our results demonstrate that VopQ is both necessary and sufficient for induction of autophagy during V. parahaemolyticus-mediated cell death and this effect is independent of phosphatidylinositol-3-kinases but requires Atg5. Furthermore, induction of VopQ-mediated autophagy prevents recruitment of the necessary cellular machinery required for phagocytosis of V. parahaemolyticus during infection. These data provide important insights into the mechanism used by V. parahaemolyticus to cause disease.</description><subject>Autophagy</subject><subject>Autophagy-Related Protein 5</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>HeLa Cells</subject><subject>Humans</subject><subject>Microtubule-Associated Proteins - metabolism</subject><subject>Phagocytosis</subject><subject>Phosphatidylinositol 3-Kinases - metabolism</subject><subject>Vibrio</subject><subject>Vibrio Infections - microbiology</subject><subject>Vibrio parahaemolyticus</subject><subject>Vibrio parahaemolyticus - genetics</subject><subject>Vibrio parahaemolyticus - metabolism</subject><subject>Vibrio parahaemolyticus - pathogenicity</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2009</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNUk1v1DAQtRCIblv-AuTELcEfsWMfQEIVlJValYq24mZNbGfrJRuncQJdfj0OuyrlBJbGHzPvPc3oGaGM4IKk9WZdECZ4ThWXBcVYFVhUShb3T9DiofAULbDiOGeSfj1AhzGuMSYMC_YcHRAlaFUqsUCXN74efMhuQn-Z-c5OxsXs85Ll33wH0eUp5XqXtm7MYBpDfwurbQadTTHCKnT-ZyLM2WC2Y4g-HqNnDbTRvdifR-j644erk0_52cXp8uT9WW44ZTKvgZtSGEJLpTBpagtWgJFCNuCUsyXjklJpcXrSWrlKCiuks9Y0wJQtMTtC73a6_VRvnDWpwwFa3Q9-A8NWB_D670rnb_UqfNe0YkyKMgm83gsM4W5ycdQbH41rW-hcmKIWFVeYl_yfQIoriSs8A-UOaIYQ4-Cah24I1rNxeq1nf_Tsj56N07-N0_eJ-vLxNH-Ie6cS4O0O8MO3bvvfwvr8fDnfEv_Vjt9A0LAafNTXX-j8I4gQrKKM_QI1y7Ne</recordid><startdate>200908</startdate><enddate>200908</enddate><creator>Burdette, Dara L</creator><creator>Seemann, Joachim</creator><creator>Orth, Kim</creator><general>Oxford, UK : Blackwell Publishing Ltd</general><general>Blackwell Publishing Ltd</general><scope>FBQ</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>7T5</scope><scope>C1K</scope><scope>F1W</scope><scope>H94</scope><scope>H95</scope><scope>L.G</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>200908</creationdate><title>Vibrio VopQ induces PI3-kinase-independent autophagy and antagonizes phagocytosis</title><author>Burdette, Dara L ; Seemann, Joachim ; Orth, Kim</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5238-ba5c46c1249901fbdad6ac868fae9ed4358228d0fae2b9e786d68eddcfa39d403</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2009</creationdate><topic>Autophagy</topic><topic>Autophagy-Related Protein 5</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>HeLa Cells</topic><topic>Humans</topic><topic>Microtubule-Associated Proteins - metabolism</topic><topic>Phagocytosis</topic><topic>Phosphatidylinositol 3-Kinases - metabolism</topic><topic>Vibrio</topic><topic>Vibrio Infections - microbiology</topic><topic>Vibrio parahaemolyticus</topic><topic>Vibrio parahaemolyticus - genetics</topic><topic>Vibrio parahaemolyticus - metabolism</topic><topic>Vibrio parahaemolyticus - pathogenicity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Burdette, Dara L</creatorcontrib><creatorcontrib>Seemann, Joachim</creatorcontrib><creatorcontrib>Orth, Kim</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Immunology Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Burdette, Dara L</au><au>Seemann, Joachim</au><au>Orth, Kim</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Vibrio VopQ induces PI3-kinase-independent autophagy and antagonizes phagocytosis</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2009-08</date><risdate>2009</risdate><volume>73</volume><issue>4</issue><spage>639</spage><epage>649</epage><pages>639-649</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Vibrio parahaemolyticus is a Gram-negative bacterium responsible for gastroenteritis acquired from the consumption of contaminated shellfish. This bacterium harbours two type III secretion systems, one on each chromosome. The type III secretion system on chromosome I induces cell death by a temporally controlled sequence of events that is caspase-independent and first involves induction of autophagy, followed by cellular rounding, and finally cellular lysis. VopQ is a type III secreted effector that is necessary for the induction of autophagy as mutant strains lacking VopQ are attenuated in their ability to induce autophagy during infection. VopQ is sufficient to induce rapid autophagy as demonstrated by microinjection of recombinant VopQ into GFP-LC3 HeLa cells. Our results demonstrate that VopQ is both necessary and sufficient for induction of autophagy during V. parahaemolyticus-mediated cell death and this effect is independent of phosphatidylinositol-3-kinases but requires Atg5. Furthermore, induction of VopQ-mediated autophagy prevents recruitment of the necessary cellular machinery required for phagocytosis of V. parahaemolyticus during infection. These data provide important insights into the mechanism used by V. parahaemolyticus to cause disease.</abstract><cop>Oxford, UK</cop><pub>Oxford, UK : Blackwell Publishing Ltd</pub><pmid>19627496</pmid><doi>10.1111/j.1365-2958.2009.06798.x</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Autophagy Autophagy-Related Protein 5 Bacterial Proteins - genetics Bacterial Proteins - metabolism Gene Expression Regulation, Bacterial HeLa Cells Humans Microtubule-Associated Proteins - metabolism Phagocytosis Phosphatidylinositol 3-Kinases - metabolism Vibrio Vibrio Infections - microbiology Vibrio parahaemolyticus Vibrio parahaemolyticus - genetics Vibrio parahaemolyticus - metabolism Vibrio parahaemolyticus - pathogenicity |
title | Vibrio VopQ induces PI3-kinase-independent autophagy and antagonizes phagocytosis |
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