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Fimbriae‐mediated outer membrane vesicle production and invasion of P orphyromonas gingivalis
P orphyromonas gingivalis is a keystone periopathogen that plays an essential role in the progress of periodontitis. Like other gram‐negative bacteria, the ability of P . gingivalis to produce outer membrane vesicles is a strategy used to interact with, and survive within its biological niches. Here...
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Published in: | MicrobiologyOpen (Weinheim) 2015-02, Vol.4 (1), p.53-65 |
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creator | Mantri, Chinmay K. Chen, Chin‐Ho Dong, Xinhong Goodwin, Jeffery Shawn Pratap, Siddharth Paromov, Victor Xie, Hua |
description | P
orphyromonas gingivalis
is a keystone periopathogen that plays an essential role in the progress of periodontitis. Like other gram‐negative bacteria, the ability of
P
. gingivalis
to produce outer membrane vesicles is a strategy used to interact with, and survive within its biological niches. Here we compared the protein components associated with vesicles derived from a fimbriated strain (33277) and an afimbriated strain (W83) of
P
. gingivalis
using proteomic analyses. Some well‐known virulence factors were identified in vesicles from both strains, such as gingipains and hemagglutinin. In contrast, FimC, FimD, and FimE, minor components of long fimbriae were found exclusively in 33277 vesicles, while proteins with a tetratricopeptide repeat (
TPR
) domain were unique to W83 vesicles. We found that significantly more 33277 than W83 vesicles were internalized into human oral keratinocytes and gingival fibroblasts. Interestingly, FimA, a well‐known adhesin responsible for the attachment and invasion of
P
. gingivalis
into host cells, was not essential for the invasive capabilities of
P
. gingivalis
vesicles. Rather minor components of long fimbriae were required for an efficient invasive activity of vesicles. The most striking finding was that
P
. gingivalis
strains lacking or having a reduced FimA expression showed a significant reduction in vesiculation. These results suggest that production and pathogenicity of
P
. gingivalis
vesicles may largely depend on expression of the
fim
locus, and that the integration of vesicle production and pathogenicity with fimbrial expression may allow
P. gingivalis
to confer upon itself certain functional advantages. |
doi_str_mv | 10.1002/mbo3.221 |
format | article |
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orphyromonas gingivalis
is a keystone periopathogen that plays an essential role in the progress of periodontitis. Like other gram‐negative bacteria, the ability of
P
. gingivalis
to produce outer membrane vesicles is a strategy used to interact with, and survive within its biological niches. Here we compared the protein components associated with vesicles derived from a fimbriated strain (33277) and an afimbriated strain (W83) of
P
. gingivalis
using proteomic analyses. Some well‐known virulence factors were identified in vesicles from both strains, such as gingipains and hemagglutinin. In contrast, FimC, FimD, and FimE, minor components of long fimbriae were found exclusively in 33277 vesicles, while proteins with a tetratricopeptide repeat (
TPR
) domain were unique to W83 vesicles. We found that significantly more 33277 than W83 vesicles were internalized into human oral keratinocytes and gingival fibroblasts. Interestingly, FimA, a well‐known adhesin responsible for the attachment and invasion of
P
. gingivalis
into host cells, was not essential for the invasive capabilities of
P
. gingivalis
vesicles. Rather minor components of long fimbriae were required for an efficient invasive activity of vesicles. The most striking finding was that
P
. gingivalis
strains lacking or having a reduced FimA expression showed a significant reduction in vesiculation. These results suggest that production and pathogenicity of
P
. gingivalis
vesicles may largely depend on expression of the
fim
locus, and that the integration of vesicle production and pathogenicity with fimbrial expression may allow
P. gingivalis
to confer upon itself certain functional advantages.</description><identifier>ISSN: 2045-8827</identifier><identifier>EISSN: 2045-8827</identifier><identifier>DOI: 10.1002/mbo3.221</identifier><language>eng</language><publisher>Bognor Regis: John Wiley & Sons, Inc</publisher><subject>Adhesives ; Bacteria ; Fibroblasts ; Gram-negative bacteria ; Hemagglutinins ; Keratinocytes ; Membrane vesicles ; Pathogenicity ; Pathogens ; Peptides ; Periodontitis ; Pili ; Proteins ; Proteomics ; Strains (organisms) ; Vesicles ; Virulence ; Virulence factors</subject><ispartof>MicrobiologyOpen (Weinheim), 2015-02, Vol.4 (1), p.53-65</ispartof><rights>2015. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c1006-8b167ee61b240199b01b6b31deb1b7bb5f49ec4e6010af7bbcee6b055eb574623</citedby><cites>FETCH-LOGICAL-c1006-8b167ee61b240199b01b6b31deb1b7bb5f49ec4e6010af7bbcee6b055eb574623</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2289742326/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2289742326?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>314,780,784,25752,27923,27924,37011,44589,74897</link.rule.ids></links><search><creatorcontrib>Mantri, Chinmay K.</creatorcontrib><creatorcontrib>Chen, Chin‐Ho</creatorcontrib><creatorcontrib>Dong, Xinhong</creatorcontrib><creatorcontrib>Goodwin, Jeffery Shawn</creatorcontrib><creatorcontrib>Pratap, Siddharth</creatorcontrib><creatorcontrib>Paromov, Victor</creatorcontrib><creatorcontrib>Xie, Hua</creatorcontrib><title>Fimbriae‐mediated outer membrane vesicle production and invasion of P orphyromonas gingivalis</title><title>MicrobiologyOpen (Weinheim)</title><description>P
orphyromonas gingivalis
is a keystone periopathogen that plays an essential role in the progress of periodontitis. Like other gram‐negative bacteria, the ability of
P
. gingivalis
to produce outer membrane vesicles is a strategy used to interact with, and survive within its biological niches. Here we compared the protein components associated with vesicles derived from a fimbriated strain (33277) and an afimbriated strain (W83) of
P
. gingivalis
using proteomic analyses. Some well‐known virulence factors were identified in vesicles from both strains, such as gingipains and hemagglutinin. In contrast, FimC, FimD, and FimE, minor components of long fimbriae were found exclusively in 33277 vesicles, while proteins with a tetratricopeptide repeat (
TPR
) domain were unique to W83 vesicles. We found that significantly more 33277 than W83 vesicles were internalized into human oral keratinocytes and gingival fibroblasts. Interestingly, FimA, a well‐known adhesin responsible for the attachment and invasion of
P
. gingivalis
into host cells, was not essential for the invasive capabilities of
P
. gingivalis
vesicles. Rather minor components of long fimbriae were required for an efficient invasive activity of vesicles. The most striking finding was that
P
. gingivalis
strains lacking or having a reduced FimA expression showed a significant reduction in vesiculation. These results suggest that production and pathogenicity of
P
. gingivalis
vesicles may largely depend on expression of the
fim
locus, and that the integration of vesicle production and pathogenicity with fimbrial expression may allow
P. gingivalis
to confer upon itself certain functional advantages.</description><subject>Adhesives</subject><subject>Bacteria</subject><subject>Fibroblasts</subject><subject>Gram-negative bacteria</subject><subject>Hemagglutinins</subject><subject>Keratinocytes</subject><subject>Membrane vesicles</subject><subject>Pathogenicity</subject><subject>Pathogens</subject><subject>Peptides</subject><subject>Periodontitis</subject><subject>Pili</subject><subject>Proteins</subject><subject>Proteomics</subject><subject>Strains (organisms)</subject><subject>Vesicles</subject><subject>Virulence</subject><subject>Virulence factors</subject><issn>2045-8827</issn><issn>2045-8827</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><recordid>eNpNUMtOwzAQtBBIVKUSn2CJC5cU23Gc5IgqCkiV4ABny5tsiqvGLnZSqTc-gW_kS3BVDuxlXzO7oyHkmrM5Z0zc9eDzuRD8jEwEk0VWVaI8_1dfklmMG5aiZEJJPiF6aXsI1uDP13ePrTUDttSPAwbaY9oYh3SP0TZbpLvg27EZrHfUuJZatzfx2PiOvlIfdh-H4HvvTKRr69Z2b7Y2XpGLzmwjzv7ylLwvH94WT9nq5fF5cb_KmiRcZRVwVSIqDkIyXtfAOCjIeYvAoQQoOlljI1ExzkyXBk0CAysKhKKUSuRTcnO6m0R-jhgHvfFjcOmlFqKqSylyoRLq9oRqgo8xYKd3wfYmHDRn-uigPjqYGDz_BRw-ZZU</recordid><startdate>201502</startdate><enddate>201502</enddate><creator>Mantri, Chinmay K.</creator><creator>Chen, Chin‐Ho</creator><creator>Dong, Xinhong</creator><creator>Goodwin, Jeffery Shawn</creator><creator>Pratap, Siddharth</creator><creator>Paromov, Victor</creator><creator>Xie, Hua</creator><general>John Wiley & Sons, Inc</general><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QL</scope><scope>7T7</scope><scope>7X7</scope><scope>7XB</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope></search><sort><creationdate>201502</creationdate><title>Fimbriae‐mediated outer membrane vesicle production and invasion of P orphyromonas gingivalis</title><author>Mantri, Chinmay K. ; Chen, Chin‐Ho ; Dong, Xinhong ; Goodwin, Jeffery Shawn ; Pratap, Siddharth ; Paromov, Victor ; Xie, Hua</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c1006-8b167ee61b240199b01b6b31deb1b7bb5f49ec4e6010af7bbcee6b055eb574623</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Adhesives</topic><topic>Bacteria</topic><topic>Fibroblasts</topic><topic>Gram-negative bacteria</topic><topic>Hemagglutinins</topic><topic>Keratinocytes</topic><topic>Membrane vesicles</topic><topic>Pathogenicity</topic><topic>Pathogens</topic><topic>Peptides</topic><topic>Periodontitis</topic><topic>Pili</topic><topic>Proteins</topic><topic>Proteomics</topic><topic>Strains (organisms)</topic><topic>Vesicles</topic><topic>Virulence</topic><topic>Virulence factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Mantri, Chinmay K.</creatorcontrib><creatorcontrib>Chen, Chin‐Ho</creatorcontrib><creatorcontrib>Dong, Xinhong</creatorcontrib><creatorcontrib>Goodwin, Jeffery Shawn</creatorcontrib><creatorcontrib>Pratap, Siddharth</creatorcontrib><creatorcontrib>Paromov, Victor</creatorcontrib><creatorcontrib>Xie, Hua</creatorcontrib><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection (Proquest) (PQ_SDU_P3)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biological Sciences</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database (Proquest) (PQ_SDU_P3)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><jtitle>MicrobiologyOpen (Weinheim)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Mantri, Chinmay K.</au><au>Chen, Chin‐Ho</au><au>Dong, Xinhong</au><au>Goodwin, Jeffery Shawn</au><au>Pratap, Siddharth</au><au>Paromov, Victor</au><au>Xie, Hua</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Fimbriae‐mediated outer membrane vesicle production and invasion of P orphyromonas gingivalis</atitle><jtitle>MicrobiologyOpen (Weinheim)</jtitle><date>2015-02</date><risdate>2015</risdate><volume>4</volume><issue>1</issue><spage>53</spage><epage>65</epage><pages>53-65</pages><issn>2045-8827</issn><eissn>2045-8827</eissn><abstract>P
orphyromonas gingivalis
is a keystone periopathogen that plays an essential role in the progress of periodontitis. Like other gram‐negative bacteria, the ability of
P
. gingivalis
to produce outer membrane vesicles is a strategy used to interact with, and survive within its biological niches. Here we compared the protein components associated with vesicles derived from a fimbriated strain (33277) and an afimbriated strain (W83) of
P
. gingivalis
using proteomic analyses. Some well‐known virulence factors were identified in vesicles from both strains, such as gingipains and hemagglutinin. In contrast, FimC, FimD, and FimE, minor components of long fimbriae were found exclusively in 33277 vesicles, while proteins with a tetratricopeptide repeat (
TPR
) domain were unique to W83 vesicles. We found that significantly more 33277 than W83 vesicles were internalized into human oral keratinocytes and gingival fibroblasts. Interestingly, FimA, a well‐known adhesin responsible for the attachment and invasion of
P
. gingivalis
into host cells, was not essential for the invasive capabilities of
P
. gingivalis
vesicles. Rather minor components of long fimbriae were required for an efficient invasive activity of vesicles. The most striking finding was that
P
. gingivalis
strains lacking or having a reduced FimA expression showed a significant reduction in vesiculation. These results suggest that production and pathogenicity of
P
. gingivalis
vesicles may largely depend on expression of the
fim
locus, and that the integration of vesicle production and pathogenicity with fimbrial expression may allow
P. gingivalis
to confer upon itself certain functional advantages.</abstract><cop>Bognor Regis</cop><pub>John Wiley & Sons, Inc</pub><doi>10.1002/mbo3.221</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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source | Open Access: PubMed Central; Publicly Available Content Database (Proquest) (PQ_SDU_P3); Wiley Online Library Open Access |
subjects | Adhesives Bacteria Fibroblasts Gram-negative bacteria Hemagglutinins Keratinocytes Membrane vesicles Pathogenicity Pathogens Peptides Periodontitis Pili Proteins Proteomics Strains (organisms) Vesicles Virulence Virulence factors |
title | Fimbriae‐mediated outer membrane vesicle production and invasion of P orphyromonas gingivalis |
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