LuxS signaling in Porphyromonas gingivalis-host interactions
Dental plaque is a multispecies biofilm in the oral cavity that significantly influences oral health. The presence of the oral anaerobic pathogen Porphyromonas gingivalis is an important determinant in the development of periodontitis. Direct and indirect interactions between P. gingivalis and the h...
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description | Dental plaque is a multispecies biofilm in the oral cavity that significantly influences oral health. The presence of the oral anaerobic pathogen Porphyromonas gingivalis is an important determinant in the development of periodontitis. Direct and indirect interactions between P. gingivalis and the host play a major role in disease development. Transcriptome analysis recently revealed that P. gingivalis gene-expression is regulated by LuxS in both an AI-2-dependent and an AI-2 independent manner. However, little is known about the role of LuxS-signaling in P. gingivalis-host interactions. Here, we investigated the effect of a luxS mutation on the ability of P. gingivalis to induce an inflammatory response in human oral cells in vitro. Primary periodontal ligament (PDL) fibroblasts were challenged with P. gingivalis ΔluxS or the wild-type parental strain and gene-expression of pro-inflammatory mediators IL-1β, IL-6 and MCP-1 was determined by real-time PCR. The ability of P. gingivalis ΔluxS to induce an inflammatory response was severely impaired in PDL-fibroblasts. This phenotype could be restored by providing of LuxS in trans, but not by addition of the AI-2 precursor DPD. A similar phenomenon was observed in a previous transcriptome study showing that expression of PGN_0482 was reduced in the luxS mutant independently of AI-2. We therefore also analyzed the effect of a mutation in PGN_0482, which encodes an immuno-reactive, putative outer-membrane protein. Similar to P. gingivalis ΔluxS, the P. gingivalis Δ0482 mutant had an impaired ability to induce an inflammatory response in PDL fibroblasts. LuxS thus appears to influence the pro-inflammatory responses of host cells to P. gingivalis, likely through regulation of PGN_0482.
•LuxS-signaling in Porphyromonas gingivalis interaction with host cells was studied in vitro.•A luxS mutant was no longer able to induce a response in PDL-fibroblasts.•The luxS defect occurred independent of AI-2 through down-regulation of PGN_0482.•A novel function of luxS in P. gingivalis-host cell interaction is reported. |
doi_str_mv | 10.1016/j.anaerobe.2014.11.011 |
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•LuxS-signaling in Porphyromonas gingivalis interaction with host cells was studied in vitro.•A luxS mutant was no longer able to induce a response in PDL-fibroblasts.•The luxS defect occurred independent of AI-2 through down-regulation of PGN_0482.•A novel function of luxS in P. gingivalis-host cell interaction is reported.</description><identifier>ISSN: 1075-9964</identifier><identifier>EISSN: 1095-8274</identifier><identifier>DOI: 10.1016/j.anaerobe.2014.11.011</identifier><identifier>PMID: 25434960</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Adolescent ; Adult ; Autoinducer-2 ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Bacteroidaceae Infections - genetics ; Bacteroidaceae Infections - immunology ; Bacteroidaceae Infections - microbiology ; Carbon-Sulfur Lyases - genetics ; Carbon-Sulfur Lyases - metabolism ; Chemokine CCL2 - genetics ; Chemokine CCL2 - immunology ; Female ; Fibroblasts - immunology ; Fibroblasts - microbiology ; Gene Expression Regulation, Bacterial ; Gingivitis - genetics ; Gingivitis - immunology ; Gingivitis - microbiology ; Host-Pathogen Interactions ; Humans ; Inflammatory response ; Interleukin-1beta - genetics ; Interleukin-1beta - immunology ; Interleukin-6 - genetics ; Interleukin-6 - immunology ; Male ; Periodontal fibroblast ; PGN_0482 ; Porphyromonas gingivalis ; Porphyromonas gingivalis - genetics ; Porphyromonas gingivalis - immunology ; Porphyromonas gingivalis - metabolism ; Quorum sensing ; Signal Transduction</subject><ispartof>Anaerobe, 2015-10, Vol.35 (Pt A), p.3-9</ispartof><rights>2014 Elsevier Ltd</rights><rights>Copyright © 2014 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c467t-7b87a4874954d855dde8a248ebce39b587bf8ae000363bae999dfceac8b2e2b13</citedby><cites>FETCH-LOGICAL-c467t-7b87a4874954d855dde8a248ebce39b587bf8ae000363bae999dfceac8b2e2b13</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1075996414001711$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3536,27903,27904,65309</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25434960$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Scheres, Nina</creatorcontrib><creatorcontrib>Lamont, Richard J.</creatorcontrib><creatorcontrib>Crielaard, Wim</creatorcontrib><creatorcontrib>Krom, Bastiaan P.</creatorcontrib><title>LuxS signaling in Porphyromonas gingivalis-host interactions</title><title>Anaerobe</title><addtitle>Anaerobe</addtitle><description>Dental plaque is a multispecies biofilm in the oral cavity that significantly influences oral health. The presence of the oral anaerobic pathogen Porphyromonas gingivalis is an important determinant in the development of periodontitis. Direct and indirect interactions between P. gingivalis and the host play a major role in disease development. Transcriptome analysis recently revealed that P. gingivalis gene-expression is regulated by LuxS in both an AI-2-dependent and an AI-2 independent manner. However, little is known about the role of LuxS-signaling in P. gingivalis-host interactions. Here, we investigated the effect of a luxS mutation on the ability of P. gingivalis to induce an inflammatory response in human oral cells in vitro. Primary periodontal ligament (PDL) fibroblasts were challenged with P. gingivalis ΔluxS or the wild-type parental strain and gene-expression of pro-inflammatory mediators IL-1β, IL-6 and MCP-1 was determined by real-time PCR. The ability of P. gingivalis ΔluxS to induce an inflammatory response was severely impaired in PDL-fibroblasts. This phenotype could be restored by providing of LuxS in trans, but not by addition of the AI-2 precursor DPD. A similar phenomenon was observed in a previous transcriptome study showing that expression of PGN_0482 was reduced in the luxS mutant independently of AI-2. We therefore also analyzed the effect of a mutation in PGN_0482, which encodes an immuno-reactive, putative outer-membrane protein. Similar to P. gingivalis ΔluxS, the P. gingivalis Δ0482 mutant had an impaired ability to induce an inflammatory response in PDL fibroblasts. LuxS thus appears to influence the pro-inflammatory responses of host cells to P. gingivalis, likely through regulation of PGN_0482.
•LuxS-signaling in Porphyromonas gingivalis interaction with host cells was studied in vitro.•A luxS mutant was no longer able to induce a response in PDL-fibroblasts.•The luxS defect occurred independent of AI-2 through down-regulation of PGN_0482.•A novel function of luxS in P. gingivalis-host cell interaction is reported.</description><subject>Adolescent</subject><subject>Adult</subject><subject>Autoinducer-2</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Bacteroidaceae Infections - genetics</subject><subject>Bacteroidaceae Infections - immunology</subject><subject>Bacteroidaceae Infections - microbiology</subject><subject>Carbon-Sulfur Lyases - genetics</subject><subject>Carbon-Sulfur Lyases - metabolism</subject><subject>Chemokine CCL2 - genetics</subject><subject>Chemokine CCL2 - immunology</subject><subject>Female</subject><subject>Fibroblasts - immunology</subject><subject>Fibroblasts - microbiology</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Gingivitis - genetics</subject><subject>Gingivitis - immunology</subject><subject>Gingivitis - microbiology</subject><subject>Host-Pathogen Interactions</subject><subject>Humans</subject><subject>Inflammatory response</subject><subject>Interleukin-1beta - genetics</subject><subject>Interleukin-1beta - immunology</subject><subject>Interleukin-6 - genetics</subject><subject>Interleukin-6 - immunology</subject><subject>Male</subject><subject>Periodontal fibroblast</subject><subject>PGN_0482</subject><subject>Porphyromonas gingivalis</subject><subject>Porphyromonas gingivalis - genetics</subject><subject>Porphyromonas gingivalis - immunology</subject><subject>Porphyromonas gingivalis - metabolism</subject><subject>Quorum sensing</subject><subject>Signal Transduction</subject><issn>1075-9964</issn><issn>1095-8274</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkE1LAzEQQIMotlb_QunRy67JbrJJwINS_IKCgnoOSXa2TWk3Ndkt9t-b0urV0wwzb2aYh9CY4JxgUt0sc91qCN5AXmBCc0JyTMgJGhIsWSYKTk_3OWeZlBUdoIsYlzgRlLFzNCgYLams8BDdzvrv90l081avXDufuHby5sNmsQt-7VsdJ_NUddvUjNnCxy4BHQRtO-fbeInOGr2KcHWMI_T5-PAxfc5mr08v0_tZZmnFu4wbwTUVnEpGa8FYXYPQBRVgLJTSMMFNIzRgjMuqNBqklHVjQVthCigMKUfo-rB3E_xXD7FTaxctrFa6Bd9HRTiuCiwElwmtDqgNPsYAjdoEt9ZhpwhWe3NqqX7Nqb05RYhKXtLg-HijN2uo_8Z-VSXg7gBA-nTrIKhoHbQWahfAdqr27r8bP1L-g6M</recordid><startdate>20151001</startdate><enddate>20151001</enddate><creator>Scheres, Nina</creator><creator>Lamont, Richard J.</creator><creator>Crielaard, Wim</creator><creator>Krom, Bastiaan P.</creator><general>Elsevier Ltd</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>7X8</scope></search><sort><creationdate>20151001</creationdate><title>LuxS signaling in Porphyromonas gingivalis-host interactions</title><author>Scheres, Nina ; Lamont, Richard J. ; Crielaard, Wim ; Krom, Bastiaan P.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c467t-7b87a4874954d855dde8a248ebce39b587bf8ae000363bae999dfceac8b2e2b13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Adolescent</topic><topic>Adult</topic><topic>Autoinducer-2</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Bacteroidaceae Infections - genetics</topic><topic>Bacteroidaceae Infections - immunology</topic><topic>Bacteroidaceae Infections - microbiology</topic><topic>Carbon-Sulfur Lyases - genetics</topic><topic>Carbon-Sulfur Lyases - metabolism</topic><topic>Chemokine CCL2 - genetics</topic><topic>Chemokine CCL2 - immunology</topic><topic>Female</topic><topic>Fibroblasts - immunology</topic><topic>Fibroblasts - microbiology</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Gingivitis - genetics</topic><topic>Gingivitis - immunology</topic><topic>Gingivitis - microbiology</topic><topic>Host-Pathogen Interactions</topic><topic>Humans</topic><topic>Inflammatory response</topic><topic>Interleukin-1beta - genetics</topic><topic>Interleukin-1beta - immunology</topic><topic>Interleukin-6 - genetics</topic><topic>Interleukin-6 - immunology</topic><topic>Male</topic><topic>Periodontal fibroblast</topic><topic>PGN_0482</topic><topic>Porphyromonas gingivalis</topic><topic>Porphyromonas gingivalis - genetics</topic><topic>Porphyromonas gingivalis - immunology</topic><topic>Porphyromonas gingivalis - metabolism</topic><topic>Quorum sensing</topic><topic>Signal Transduction</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Scheres, Nina</creatorcontrib><creatorcontrib>Lamont, Richard J.</creatorcontrib><creatorcontrib>Crielaard, Wim</creatorcontrib><creatorcontrib>Krom, Bastiaan P.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Anaerobe</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Scheres, Nina</au><au>Lamont, Richard J.</au><au>Crielaard, Wim</au><au>Krom, Bastiaan P.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>LuxS signaling in Porphyromonas gingivalis-host interactions</atitle><jtitle>Anaerobe</jtitle><addtitle>Anaerobe</addtitle><date>2015-10-01</date><risdate>2015</risdate><volume>35</volume><issue>Pt A</issue><spage>3</spage><epage>9</epage><pages>3-9</pages><issn>1075-9964</issn><eissn>1095-8274</eissn><abstract>Dental plaque is a multispecies biofilm in the oral cavity that significantly influences oral health. The presence of the oral anaerobic pathogen Porphyromonas gingivalis is an important determinant in the development of periodontitis. Direct and indirect interactions between P. gingivalis and the host play a major role in disease development. Transcriptome analysis recently revealed that P. gingivalis gene-expression is regulated by LuxS in both an AI-2-dependent and an AI-2 independent manner. However, little is known about the role of LuxS-signaling in P. gingivalis-host interactions. Here, we investigated the effect of a luxS mutation on the ability of P. gingivalis to induce an inflammatory response in human oral cells in vitro. Primary periodontal ligament (PDL) fibroblasts were challenged with P. gingivalis ΔluxS or the wild-type parental strain and gene-expression of pro-inflammatory mediators IL-1β, IL-6 and MCP-1 was determined by real-time PCR. The ability of P. gingivalis ΔluxS to induce an inflammatory response was severely impaired in PDL-fibroblasts. This phenotype could be restored by providing of LuxS in trans, but not by addition of the AI-2 precursor DPD. A similar phenomenon was observed in a previous transcriptome study showing that expression of PGN_0482 was reduced in the luxS mutant independently of AI-2. We therefore also analyzed the effect of a mutation in PGN_0482, which encodes an immuno-reactive, putative outer-membrane protein. Similar to P. gingivalis ΔluxS, the P. gingivalis Δ0482 mutant had an impaired ability to induce an inflammatory response in PDL fibroblasts. LuxS thus appears to influence the pro-inflammatory responses of host cells to P. gingivalis, likely through regulation of PGN_0482.
•LuxS-signaling in Porphyromonas gingivalis interaction with host cells was studied in vitro.•A luxS mutant was no longer able to induce a response in PDL-fibroblasts.•The luxS defect occurred independent of AI-2 through down-regulation of PGN_0482.•A novel function of luxS in P. gingivalis-host cell interaction is reported.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>25434960</pmid><doi>10.1016/j.anaerobe.2014.11.011</doi><tpages>7</tpages></addata></record> |
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subjects | Adolescent Adult Autoinducer-2 Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacteroidaceae Infections - genetics Bacteroidaceae Infections - immunology Bacteroidaceae Infections - microbiology Carbon-Sulfur Lyases - genetics Carbon-Sulfur Lyases - metabolism Chemokine CCL2 - genetics Chemokine CCL2 - immunology Female Fibroblasts - immunology Fibroblasts - microbiology Gene Expression Regulation, Bacterial Gingivitis - genetics Gingivitis - immunology Gingivitis - microbiology Host-Pathogen Interactions Humans Inflammatory response Interleukin-1beta - genetics Interleukin-1beta - immunology Interleukin-6 - genetics Interleukin-6 - immunology Male Periodontal fibroblast PGN_0482 Porphyromonas gingivalis Porphyromonas gingivalis - genetics Porphyromonas gingivalis - immunology Porphyromonas gingivalis - metabolism Quorum sensing Signal Transduction |
title | LuxS signaling in Porphyromonas gingivalis-host interactions |
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