Selective Sorting of Cargo Proteins into Bacterial Membrane Vesicles
In contrast to the well established multiple cellular roles of membrane vesicles in eukaryotic cell biology, outer membrane vesicles (OMV) produced via blebbing of prokaryotic membranes have frequently been regarded as cell debris or microscopy artifacts. Increasingly, however, bacterial membrane ve...
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Veröffentlicht in: | The Journal of biological chemistry 2011-01, Vol.286 (2), p.1269-1276 |
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description | In contrast to the well established multiple cellular roles of membrane vesicles in eukaryotic cell biology, outer membrane vesicles (OMV) produced via blebbing of prokaryotic membranes have frequently been regarded as cell debris or microscopy artifacts. Increasingly, however, bacterial membrane vesicles are thought to play a role in microbial virulence, although it remains to be determined whether OMV result from a directed process or from passive disintegration of the outer membrane. Here we establish that the human oral pathogen Porphyromonas gingivalis has a mechanism to selectively sort proteins into OMV, resulting in the preferential packaging of virulence factors into OMV and the exclusion of abundant outer membrane proteins from the protein cargo. Furthermore, we show a critical role for lipopolysaccharide in directing this sorting mechanism. The existence of a process to package specific virulence factors into OMV may significantly alter our current understanding of host-pathogen interactions. |
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Florencia ; Aduse-Opoku, Joseph ; Rangarajan, Minnie ; Dorobantu, Loredana ; Gray, Murray R. ; Curtis, Michael A. ; Feldman, Mario F.</creator><creatorcontrib>Haurat, M. Florencia ; Aduse-Opoku, Joseph ; Rangarajan, Minnie ; Dorobantu, Loredana ; Gray, Murray R. ; Curtis, Michael A. ; Feldman, Mario F.</creatorcontrib><description>In contrast to the well established multiple cellular roles of membrane vesicles in eukaryotic cell biology, outer membrane vesicles (OMV) produced via blebbing of prokaryotic membranes have frequently been regarded as cell debris or microscopy artifacts. Increasingly, however, bacterial membrane vesicles are thought to play a role in microbial virulence, although it remains to be determined whether OMV result from a directed process or from passive disintegration of the outer membrane. Here we establish that the human oral pathogen Porphyromonas gingivalis has a mechanism to selectively sort proteins into OMV, resulting in the preferential packaging of virulence factors into OMV and the exclusion of abundant outer membrane proteins from the protein cargo. Furthermore, we show a critical role for lipopolysaccharide in directing this sorting mechanism. The existence of a process to package specific virulence factors into OMV may significantly alter our current understanding of host-pathogen interactions.</description><identifier>ISSN: 0021-9258</identifier><identifier>EISSN: 1083-351X</identifier><identifier>DOI: 10.1074/jbc.M110.185744</identifier><identifier>PMID: 21056982</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Adhesins, Bacterial - genetics ; Adhesins, Bacterial - metabolism ; Bacteria ; Bacterial Outer Membrane Proteins - genetics ; Bacterial Outer Membrane Proteins - metabolism ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Cysteine Endopeptidases - genetics ; Cysteine Endopeptidases - metabolism ; Gingipain Cysteine Endopeptidases ; Lipid ; Lipid A - metabolism ; Lipopolysaccharide (LPS) ; Lipopolysaccharides - metabolism ; Membrane Proteins ; Microbiology ; O Antigens - genetics ; O Antigens - metabolism ; Outer Membrane Vesicles (OMV) ; Porphyromonas gingivalis ; Porphyromonas gingivalis - genetics ; Porphyromonas gingivalis - metabolism ; Porphyromonas gingivalis - pathogenicity ; Protein Cargo Selection ; Protein Sorting ; Protein Transport - physiology ; Secretory Vesicles - metabolism ; Vesicles ; Virulence ; Virulence Factors - genetics ; Virulence Factors - metabolism</subject><ispartof>The Journal of biological chemistry, 2011-01, Vol.286 (2), p.1269-1276</ispartof><rights>2011 © 2011 ASBMB. Currently published by Elsevier Inc; originally published by American Society for Biochemistry and Molecular Biology.</rights><rights>2011 by The American Society for Biochemistry and Molecular Biology, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c544t-88250918bfb4217bf8b1a2e69d3a5951c820c515a4a7edd227b2d9f5e32c5d503</citedby><cites>FETCH-LOGICAL-c544t-88250918bfb4217bf8b1a2e69d3a5951c820c515a4a7edd227b2d9f5e32c5d503</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3020734/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3020734/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27903,27904,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21056982$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Haurat, M. Florencia</creatorcontrib><creatorcontrib>Aduse-Opoku, Joseph</creatorcontrib><creatorcontrib>Rangarajan, Minnie</creatorcontrib><creatorcontrib>Dorobantu, Loredana</creatorcontrib><creatorcontrib>Gray, Murray R.</creatorcontrib><creatorcontrib>Curtis, Michael A.</creatorcontrib><creatorcontrib>Feldman, Mario F.</creatorcontrib><title>Selective Sorting of Cargo Proteins into Bacterial Membrane Vesicles</title><title>The Journal of biological chemistry</title><addtitle>J Biol Chem</addtitle><description>In contrast to the well established multiple cellular roles of membrane vesicles in eukaryotic cell biology, outer membrane vesicles (OMV) produced via blebbing of prokaryotic membranes have frequently been regarded as cell debris or microscopy artifacts. Increasingly, however, bacterial membrane vesicles are thought to play a role in microbial virulence, although it remains to be determined whether OMV result from a directed process or from passive disintegration of the outer membrane. Here we establish that the human oral pathogen Porphyromonas gingivalis has a mechanism to selectively sort proteins into OMV, resulting in the preferential packaging of virulence factors into OMV and the exclusion of abundant outer membrane proteins from the protein cargo. Furthermore, we show a critical role for lipopolysaccharide in directing this sorting mechanism. The existence of a process to package specific virulence factors into OMV may significantly alter our current understanding of host-pathogen interactions.</description><subject>Adhesins, Bacterial - genetics</subject><subject>Adhesins, Bacterial - metabolism</subject><subject>Bacteria</subject><subject>Bacterial Outer Membrane Proteins - genetics</subject><subject>Bacterial Outer Membrane Proteins - metabolism</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Cysteine Endopeptidases - genetics</subject><subject>Cysteine Endopeptidases - metabolism</subject><subject>Gingipain Cysteine Endopeptidases</subject><subject>Lipid</subject><subject>Lipid A - metabolism</subject><subject>Lipopolysaccharide (LPS)</subject><subject>Lipopolysaccharides - metabolism</subject><subject>Membrane Proteins</subject><subject>Microbiology</subject><subject>O Antigens - genetics</subject><subject>O Antigens - metabolism</subject><subject>Outer Membrane Vesicles (OMV)</subject><subject>Porphyromonas gingivalis</subject><subject>Porphyromonas gingivalis - genetics</subject><subject>Porphyromonas gingivalis - metabolism</subject><subject>Porphyromonas gingivalis - pathogenicity</subject><subject>Protein Cargo Selection</subject><subject>Protein Sorting</subject><subject>Protein Transport - physiology</subject><subject>Secretory Vesicles - metabolism</subject><subject>Vesicles</subject><subject>Virulence</subject><subject>Virulence Factors - genetics</subject><subject>Virulence Factors - metabolism</subject><issn>0021-9258</issn><issn>1083-351X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkU1P3DAQhq2KqizQM7c2N04Bjz829qUSLJRWAoG0gHqzHGeyNcrGYGdX4t_XSyiihwpfLMuPZ_zOQ8g-0EOglTi6r93hJWxOSlZCfCAToIqXXMKvLTKhlEGpmVTbZCele5qX0PCJbDOgcqoVm5DTOXboBr_GYh7i4PtFEdpiZuMiFNcxDOj7VPh-CMWJdQNGb7viEpd1tD0Wd5i86zDtkY-t7RJ-ftl3ye33s5vZj_Li6vzn7PiidFKIoVSKSapB1W0tGFR1q2qwDKe64VZqCU4x6iRIK2yFTcNYVbNGtxI5c7KRlO-Sb2Pdh1W9xMZhP0TbmYfolzY-mWC9-fem97_NIqwNp4xWXOQCBy8FYnhcYRrM0ieHXZfThFUymnHQisP0XVLlEYNmusrk0Ui6GFKK2L7-B6jZSDJZktlIMqOk_OLL2xiv_F8rGfg6Aq0Nxi6iT-Z2zihwCppz_RxEjwTmca89RpOcx95h42PWaZrg_9v-D8Fgqfs</recordid><startdate>20110114</startdate><enddate>20110114</enddate><creator>Haurat, M. Florencia</creator><creator>Aduse-Opoku, Joseph</creator><creator>Rangarajan, Minnie</creator><creator>Dorobantu, Loredana</creator><creator>Gray, Murray R.</creator><creator>Curtis, Michael A.</creator><creator>Feldman, Mario F.</creator><general>Elsevier Inc</general><general>American Society for Biochemistry and Molecular Biology</general><scope>6I.</scope><scope>AAFTH</scope><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>7X8</scope><scope>7QL</scope><scope>C1K</scope><scope>5PM</scope></search><sort><creationdate>20110114</creationdate><title>Selective Sorting of Cargo Proteins into Bacterial Membrane Vesicles</title><author>Haurat, M. Florencia ; Aduse-Opoku, Joseph ; Rangarajan, Minnie ; Dorobantu, Loredana ; Gray, Murray R. ; Curtis, Michael A. ; Feldman, Mario F.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c544t-88250918bfb4217bf8b1a2e69d3a5951c820c515a4a7edd227b2d9f5e32c5d503</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Adhesins, Bacterial - genetics</topic><topic>Adhesins, Bacterial - metabolism</topic><topic>Bacteria</topic><topic>Bacterial Outer Membrane Proteins - genetics</topic><topic>Bacterial Outer Membrane Proteins - metabolism</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Cysteine Endopeptidases - genetics</topic><topic>Cysteine Endopeptidases - metabolism</topic><topic>Gingipain Cysteine Endopeptidases</topic><topic>Lipid</topic><topic>Lipid A - metabolism</topic><topic>Lipopolysaccharide (LPS)</topic><topic>Lipopolysaccharides - metabolism</topic><topic>Membrane Proteins</topic><topic>Microbiology</topic><topic>O Antigens - genetics</topic><topic>O Antigens - metabolism</topic><topic>Outer Membrane Vesicles (OMV)</topic><topic>Porphyromonas gingivalis</topic><topic>Porphyromonas gingivalis - genetics</topic><topic>Porphyromonas gingivalis - metabolism</topic><topic>Porphyromonas gingivalis - pathogenicity</topic><topic>Protein Cargo Selection</topic><topic>Protein Sorting</topic><topic>Protein Transport - physiology</topic><topic>Secretory Vesicles - metabolism</topic><topic>Vesicles</topic><topic>Virulence</topic><topic>Virulence Factors - genetics</topic><topic>Virulence Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Haurat, M. 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subjects | Adhesins, Bacterial - genetics Adhesins, Bacterial - metabolism Bacteria Bacterial Outer Membrane Proteins - genetics Bacterial Outer Membrane Proteins - metabolism Bacterial Proteins - genetics Bacterial Proteins - metabolism Cysteine Endopeptidases - genetics Cysteine Endopeptidases - metabolism Gingipain Cysteine Endopeptidases Lipid Lipid A - metabolism Lipopolysaccharide (LPS) Lipopolysaccharides - metabolism Membrane Proteins Microbiology O Antigens - genetics O Antigens - metabolism Outer Membrane Vesicles (OMV) Porphyromonas gingivalis Porphyromonas gingivalis - genetics Porphyromonas gingivalis - metabolism Porphyromonas gingivalis - pathogenicity Protein Cargo Selection Protein Sorting Protein Transport - physiology Secretory Vesicles - metabolism Vesicles Virulence Virulence Factors - genetics Virulence Factors - metabolism |
title | Selective Sorting of Cargo Proteins into Bacterial Membrane Vesicles |
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