Functional Advantages of Porphyromonas gingivalis Vesicles
Porphyromonas gingivalis is a keystone pathogen of periodontitis. Outer membrane vesicles (OMVs) have been considered as both offense and defense components of this bacterium. Previous studies indicated that like their originating cells, P. gingivalis vesicles, are able to invade oral epithelial cel...
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| description | Porphyromonas gingivalis is a keystone pathogen of periodontitis. Outer membrane vesicles (OMVs) have been considered as both offense and defense components of this bacterium. Previous studies indicated that like their originating cells, P. gingivalis vesicles, are able to invade oral epithelial cells and gingival fibroblasts, in order to promote aggregation of some specific oral bacteria and to induce host immune responses. In the present study, we investigated the invasive efficiency of P. gingivalis OMVs and compared results with that of the originating cells. Results revealed that 70-90% of human primary oral epithelial cells, gingival fibroblasts, and human umbilical vein endothelial cells carried vesicles from P. gingivalis 33277 after being exposed to the vesicles for 1 h, while 20-50% of the host cells had internalized P. gingivalis cells. We also detected vesicle-associated DNA and RNA and a vesicle-mediated horizontal gene transfer in P. gingivalis strains, which represents a novel mechanism for gene transfer between P. gingivalis strains. Moreover, purified vesicles of P. gingivalis appear to have a negative impact on biofilm formation and the maintenance of Streptococcus gordonii. Our results suggest that vesicles are likely the best offence weapon of P. gingivalis for bacterial survival in the oral cavity and for induction of periodontitis. |
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Outer membrane vesicles (OMVs) have been considered as both offense and defense components of this bacterium. Previous studies indicated that like their originating cells, P. gingivalis vesicles, are able to invade oral epithelial cells and gingival fibroblasts, in order to promote aggregation of some specific oral bacteria and to induce host immune responses. In the present study, we investigated the invasive efficiency of P. gingivalis OMVs and compared results with that of the originating cells. Results revealed that 70-90% of human primary oral epithelial cells, gingival fibroblasts, and human umbilical vein endothelial cells carried vesicles from P. gingivalis 33277 after being exposed to the vesicles for 1 h, while 20-50% of the host cells had internalized P. gingivalis cells. We also detected vesicle-associated DNA and RNA and a vesicle-mediated horizontal gene transfer in P. gingivalis strains, which represents a novel mechanism for gene transfer between P. gingivalis strains. Moreover, purified vesicles of P. gingivalis appear to have a negative impact on biofilm formation and the maintenance of Streptococcus gordonii. Our results suggest that vesicles are likely the best offence weapon of P. gingivalis for bacterial survival in the oral cavity and for induction of periodontitis.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0123448</identifier><identifier>PMID: 25897780</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Atherosclerosis ; Bacteria ; Bacteroidaceae Infections - microbiology ; Biofilms ; Candida albicans ; Cell Membrane ; Cells, Cultured ; Dentistry ; Deoxyribonucleic acid ; DNA ; Endothelial cells ; Extracellular Vesicles - physiology ; Fibroblasts ; Fibroblasts - microbiology ; Fibroblasts - physiology ; Gene Transfer, Horizontal ; Genes, Bacterial ; Gram-negative bacteria ; Host-Pathogen Interactions ; Human Umbilical Vein Endothelial Cells - microbiology ; Human Umbilical Vein Endothelial Cells - physiology ; Humans ; Immune response ; Keratinocytes - microbiology ; Keratinocytes - physiology ; Pathogens ; Periodontics ; Periodontitis - microbiology ; Porphyromonas gingivalis ; Porphyromonas gingivalis - physiology ; Proteins ; Pseudomonas aeruginosa ; Ribonucleic acid ; RNA ; Vesicles</subject><ispartof>PloS one, 2015-04, Vol.10 (4), p.e0123448-e0123448</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Ho et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2015 Ho et al 2015 Ho et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c758t-a5e8fe99bcd183eb9b4a3092d10f0974c894b2d93740540fd1a80f359d3a363b3</citedby><cites>FETCH-LOGICAL-c758t-a5e8fe99bcd183eb9b4a3092d10f0974c894b2d93740540fd1a80f359d3a363b3</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/PMC4405273/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4405273/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25897780$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Kreth, Jens</contributor><creatorcontrib>Ho, Meng-Hsuan</creatorcontrib><creatorcontrib>Chen, Chin-Ho</creatorcontrib><creatorcontrib>Goodwin, J Shawn</creatorcontrib><creatorcontrib>Wang, Bing-Yan</creatorcontrib><creatorcontrib>Xie, Hua</creatorcontrib><title>Functional Advantages of Porphyromonas gingivalis Vesicles</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Porphyromonas gingivalis is a keystone pathogen of periodontitis. Outer membrane vesicles (OMVs) have been considered as both offense and defense components of this bacterium. Previous studies indicated that like their originating cells, P. gingivalis vesicles, are able to invade oral epithelial cells and gingival fibroblasts, in order to promote aggregation of some specific oral bacteria and to induce host immune responses. In the present study, we investigated the invasive efficiency of P. gingivalis OMVs and compared results with that of the originating cells. Results revealed that 70-90% of human primary oral epithelial cells, gingival fibroblasts, and human umbilical vein endothelial cells carried vesicles from P. gingivalis 33277 after being exposed to the vesicles for 1 h, while 20-50% of the host cells had internalized P. gingivalis cells. We also detected vesicle-associated DNA and RNA and a vesicle-mediated horizontal gene transfer in P. gingivalis strains, which represents a novel mechanism for gene transfer between P. gingivalis strains. Moreover, purified vesicles of P. gingivalis appear to have a negative impact on biofilm formation and the maintenance of Streptococcus gordonii. Our results suggest that vesicles are likely the best offence weapon of P. gingivalis for bacterial survival in the oral cavity and for induction of periodontitis.</description><subject>Atherosclerosis</subject><subject>Bacteria</subject><subject>Bacteroidaceae Infections - microbiology</subject><subject>Biofilms</subject><subject>Candida albicans</subject><subject>Cell Membrane</subject><subject>Cells, Cultured</subject><subject>Dentistry</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>Endothelial cells</subject><subject>Extracellular Vesicles - physiology</subject><subject>Fibroblasts</subject><subject>Fibroblasts - microbiology</subject><subject>Fibroblasts - physiology</subject><subject>Gene Transfer, Horizontal</subject><subject>Genes, Bacterial</subject><subject>Gram-negative bacteria</subject><subject>Host-Pathogen Interactions</subject><subject>Human Umbilical Vein Endothelial Cells - microbiology</subject><subject>Human Umbilical Vein Endothelial Cells - physiology</subject><subject>Humans</subject><subject>Immune response</subject><subject>Keratinocytes - microbiology</subject><subject>Keratinocytes - physiology</subject><subject>Pathogens</subject><subject>Periodontics</subject><subject>Periodontitis - microbiology</subject><subject>Porphyromonas gingivalis</subject><subject>Porphyromonas gingivalis - physiology</subject><subject>Proteins</subject><subject>Pseudomonas aeruginosa</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Vesicles</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNkl1v0zAUhiMEYqPwDxBEQkJw0WLHjj-4QKomBpUmDfGxW8uxndSVGxc7qbZ_P2fNpgbtAvnC1vFz3nOO_WbZawgWEFH4aeP70Eq32PnWLAAsEMbsSXYKOSrmpADo6dH5JHsR4waAEjFCnmcnRck4pQycZp_P-1Z11ielfKn3su1kY2Lu6_yHD7v1TfDbdBfzxraN3UtnY35lolXOxJfZs1q6aF6N-yz7c_7199n3-cXlt9XZ8mKuaMm6uSwNqw3nldKQIVPxCksEeKEhqAGnWDGOq0JzRDEoMag1lAzUqOQaSURQhWbZ24PuzvkoxrGjgIRiwhBL482y1YHQXm7ELtitDDfCSyvuAj40QoZuaFpwXpISpvIAQEw14ZxRxbTBqTPEqExaX8ZqfbU1Wpm2C9JNRKc3rV2Lxu8FTu0XFCWBD6NA8H97EzuxtVEZ52RrfH_Xd8kIpwgm9N0_6OPTjVQj0wC2rX2qqwZRscRFKkkKzhO1eIRKS5utVckjtU3xScLHSUJiOnPdNbKPUax-_fx_9vJqyr4_YtdGum4dvesHk8UpiA-gCj7GYOqHR4ZADBa_fw0xWFyMFk9pb44_6CHp3tPoFlaE9IM</recordid><startdate>20150421</startdate><enddate>20150421</enddate><creator>Ho, Meng-Hsuan</creator><creator>Chen, Chin-Ho</creator><creator>Goodwin, J Shawn</creator><creator>Wang, Bing-Yan</creator><creator>Xie, Hua</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20150421</creationdate><title>Functional Advantages of Porphyromonas gingivalis Vesicles</title><author>Ho, Meng-Hsuan ; Chen, Chin-Ho ; Goodwin, J Shawn ; Wang, Bing-Yan ; Xie, Hua</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c758t-a5e8fe99bcd183eb9b4a3092d10f0974c894b2d93740540fd1a80f359d3a363b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Atherosclerosis</topic><topic>Bacteria</topic><topic>Bacteroidaceae Infections - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ho, Meng-Hsuan</au><au>Chen, Chin-Ho</au><au>Goodwin, J Shawn</au><au>Wang, Bing-Yan</au><au>Xie, Hua</au><au>Kreth, Jens</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Functional Advantages of Porphyromonas gingivalis Vesicles</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-04-21</date><risdate>2015</risdate><volume>10</volume><issue>4</issue><spage>e0123448</spage><epage>e0123448</epage><pages>e0123448-e0123448</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Porphyromonas gingivalis is a keystone pathogen of periodontitis. Outer membrane vesicles (OMVs) have been considered as both offense and defense components of this bacterium. Previous studies indicated that like their originating cells, P. gingivalis vesicles, are able to invade oral epithelial cells and gingival fibroblasts, in order to promote aggregation of some specific oral bacteria and to induce host immune responses. In the present study, we investigated the invasive efficiency of P. gingivalis OMVs and compared results with that of the originating cells. Results revealed that 70-90% of human primary oral epithelial cells, gingival fibroblasts, and human umbilical vein endothelial cells carried vesicles from P. gingivalis 33277 after being exposed to the vesicles for 1 h, while 20-50% of the host cells had internalized P. gingivalis cells. We also detected vesicle-associated DNA and RNA and a vesicle-mediated horizontal gene transfer in P. gingivalis strains, which represents a novel mechanism for gene transfer between P. gingivalis strains. Moreover, purified vesicles of P. gingivalis appear to have a negative impact on biofilm formation and the maintenance of Streptococcus gordonii. Our results suggest that vesicles are likely the best offence weapon of P. gingivalis for bacterial survival in the oral cavity and for induction of periodontitis.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25897780</pmid><doi>10.1371/journal.pone.0123448</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Atherosclerosis Bacteria Bacteroidaceae Infections - microbiology Biofilms Candida albicans Cell Membrane Cells, Cultured Dentistry Deoxyribonucleic acid DNA Endothelial cells Extracellular Vesicles - physiology Fibroblasts Fibroblasts - microbiology Fibroblasts - physiology Gene Transfer, Horizontal Genes, Bacterial Gram-negative bacteria Host-Pathogen Interactions Human Umbilical Vein Endothelial Cells - microbiology Human Umbilical Vein Endothelial Cells - physiology Humans Immune response Keratinocytes - microbiology Keratinocytes - physiology Pathogens Periodontics Periodontitis - microbiology Porphyromonas gingivalis Porphyromonas gingivalis - physiology Proteins Pseudomonas aeruginosa Ribonucleic acid RNA Vesicles |
| title | Functional Advantages of Porphyromonas gingivalis Vesicles |
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