Regulation of virulence gene expression resulting from Streptococcus pneumoniae and nontypeable Haemophilus influenzae interactions in chronic disease
Chronic rhinosinusitis (CRS) is a common inflammatory disease of the sinonasal cavity mediated, in part, by polymicrobial communities of bacteria. Recent molecular studies have confirmed the importance of Streptococcus pneumoniae and nontypeable Haemophilus influenzae (NTHi) in CRS. Here, we hypothe...
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| creator | Cope, Emily K Goldstein-Daruech, Natalia Kofonow, Jennifer M Christensen, Lanette McDermott, Bridget Monroy, Fernando Palmer, James N Chiu, Alexander G Shirtliff, Mark E Cohen, Noam A Leid, Jeff G |
| description | Chronic rhinosinusitis (CRS) is a common inflammatory disease of the sinonasal cavity mediated, in part, by polymicrobial communities of bacteria. Recent molecular studies have confirmed the importance of Streptococcus pneumoniae and nontypeable Haemophilus influenzae (NTHi) in CRS. Here, we hypothesize that interaction between S. pneumoniae and NTHi mixed-species communities cause a change in bacterial virulence gene expression. We examined CRS as a model human disease to validate these polymicrobial interactions. Clinical strains of S. pneumoniae and NTHi were grown in mono- and co-culture in a standard biofilm assay. Reverse transcriptase real-time PCR (RTqPCR) was used to measure gene expression of key virulence factors. To validate these results, we investigated the presence of the bacterial RNA transcripts in excised human tissue from patients with CRS. Consequences of physical or chemical interactions between microbes were also investigated. Transcription of NTHi type IV pili was only expressed in co-culture in vitro, and expression could be detected ex vivo in diseased tissue. S. pneumoniae pyruvate oxidase was up-regulated in co-culture, while pneumolysin and pneumococcal adherence factor A were down-regulated. These results were confirmed in excised human CRS tissue. Gene expression was differentially regulated by physical contact and secreted factors. Overall, these data suggest that interactions between H. influenzae and S. pneumoniae involve physical and chemical mechanisms that influence virulence gene expression of mixed-species biofilm communities present in chronically diseased human tissue. These results extend previous studies of population-level virulence and provide novel insight into the importance of S. pneumoniae and NTHi in CRS. |
| doi_str_mv | 10.1371/journal.pone.0028523 |
| format | Article |
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Recent molecular studies have confirmed the importance of Streptococcus pneumoniae and nontypeable Haemophilus influenzae (NTHi) in CRS. Here, we hypothesize that interaction between S. pneumoniae and NTHi mixed-species communities cause a change in bacterial virulence gene expression. We examined CRS as a model human disease to validate these polymicrobial interactions. Clinical strains of S. pneumoniae and NTHi were grown in mono- and co-culture in a standard biofilm assay. Reverse transcriptase real-time PCR (RTqPCR) was used to measure gene expression of key virulence factors. To validate these results, we investigated the presence of the bacterial RNA transcripts in excised human tissue from patients with CRS. Consequences of physical or chemical interactions between microbes were also investigated. Transcription of NTHi type IV pili was only expressed in co-culture in vitro, and expression could be detected ex vivo in diseased tissue. S. pneumoniae pyruvate oxidase was up-regulated in co-culture, while pneumolysin and pneumococcal adherence factor A were down-regulated. These results were confirmed in excised human CRS tissue. Gene expression was differentially regulated by physical contact and secreted factors. Overall, these data suggest that interactions between H. influenzae and S. pneumoniae involve physical and chemical mechanisms that influence virulence gene expression of mixed-species biofilm communities present in chronically diseased human tissue. These results extend previous studies of population-level virulence and provide novel insight into the importance of S. pneumoniae and NTHi in CRS.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0028523</identifier><identifier>PMID: 22162775</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Bacteria ; Bacterial genetics ; Bacterial infections ; Biofilms ; Biology ; Biopsy ; Chemical interactions ; Chronic Disease ; Chronic diseases ; Chronic illnesses ; Coculture Techniques ; Communities ; Culture ; DNA polymerases ; DNA Primers - genetics ; Ear diseases ; Gene Expression ; Gene Expression Regulation ; Genes ; Genes, Bacterial ; Genetic research ; Haemophilus influenzae ; Haemophilus influenzae - metabolism ; Hemophilus infections ; Humans ; Inflammation ; Medicine ; Metabolism ; Models, Statistical ; Otolaryngology ; Oxidases ; Pili ; Pneumolysin ; Pneumonia ; Polymerase chain reaction ; Population studies ; Pseudomonas aeruginosa ; Pyruvate oxidase ; Pyruvic acid ; Rhinosinusitis ; Ribonucleic acid ; RNA ; RNA - metabolism ; RNA, Bacterial - metabolism ; RNA, Ribosomal, 16S - metabolism ; RNA-directed DNA polymerase ; Sinusitis - microbiology ; Sinusitis - physiopathology ; Streptococcus infections ; Streptococcus pneumoniae ; Streptococcus pneumoniae - metabolism ; Studies ; Surgery ; Time Factors ; Transcription ; Vaccines ; Virulence ; Virulence (Microbiology) ; Virulence factors</subject><ispartof>PloS one, 2011-12, Vol.6 (12), p.e28523-e28523</ispartof><rights>COPYRIGHT 2011 Public Library of Science</rights><rights>2011 Cope et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://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>Cope et al. 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c691t-7334a7f319bf788a258ec7a9405a0865ee8003dcd17aec5bbf8056d7be7c02983</citedby><cites>FETCH-LOGICAL-c691t-7334a7f319bf788a258ec7a9405a0865ee8003dcd17aec5bbf8056d7be7c02983</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/PMC3230614/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3230614/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22162775$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Cope, Emily K</creatorcontrib><creatorcontrib>Goldstein-Daruech, Natalia</creatorcontrib><creatorcontrib>Kofonow, Jennifer M</creatorcontrib><creatorcontrib>Christensen, Lanette</creatorcontrib><creatorcontrib>McDermott, Bridget</creatorcontrib><creatorcontrib>Monroy, Fernando</creatorcontrib><creatorcontrib>Palmer, James N</creatorcontrib><creatorcontrib>Chiu, Alexander G</creatorcontrib><creatorcontrib>Shirtliff, Mark E</creatorcontrib><creatorcontrib>Cohen, Noam A</creatorcontrib><creatorcontrib>Leid, Jeff G</creatorcontrib><title>Regulation of virulence gene expression resulting from Streptococcus pneumoniae and nontypeable Haemophilus influenzae interactions in chronic disease</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Chronic rhinosinusitis (CRS) is a common inflammatory disease of the sinonasal cavity mediated, in part, by polymicrobial communities of bacteria. Recent molecular studies have confirmed the importance of Streptococcus pneumoniae and nontypeable Haemophilus influenzae (NTHi) in CRS. Here, we hypothesize that interaction between S. pneumoniae and NTHi mixed-species communities cause a change in bacterial virulence gene expression. We examined CRS as a model human disease to validate these polymicrobial interactions. Clinical strains of S. pneumoniae and NTHi were grown in mono- and co-culture in a standard biofilm assay. Reverse transcriptase real-time PCR (RTqPCR) was used to measure gene expression of key virulence factors. To validate these results, we investigated the presence of the bacterial RNA transcripts in excised human tissue from patients with CRS. Consequences of physical or chemical interactions between microbes were also investigated. Transcription of NTHi type IV pili was only expressed in co-culture in vitro, and expression could be detected ex vivo in diseased tissue. S. pneumoniae pyruvate oxidase was up-regulated in co-culture, while pneumolysin and pneumococcal adherence factor A were down-regulated. These results were confirmed in excised human CRS tissue. Gene expression was differentially regulated by physical contact and secreted factors. Overall, these data suggest that interactions between H. influenzae and S. pneumoniae involve physical and chemical mechanisms that influence virulence gene expression of mixed-species biofilm communities present in chronically diseased human tissue. 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metabolism</subject><subject>RNA, Bacterial - metabolism</subject><subject>RNA, Ribosomal, 16S - metabolism</subject><subject>RNA-directed DNA polymerase</subject><subject>Sinusitis - microbiology</subject><subject>Sinusitis - physiopathology</subject><subject>Streptococcus infections</subject><subject>Streptococcus pneumoniae</subject><subject>Streptococcus pneumoniae - metabolism</subject><subject>Studies</subject><subject>Surgery</subject><subject>Time Factors</subject><subject>Transcription</subject><subject>Vaccines</subject><subject>Virulence</subject><subject>Virulence (Microbiology)</subject><subject>Virulence factors</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNk99r1TAUx4sobk7_A9GCoPhwr_nRpu2LMIa6C4PBpr6GND3tzUiTmqRj8w_x7zXd7cat7EHykHDy-X5PcpKTJK8xWmNa4E9XdnRG6PVgDawRImVO6JPkEFeUrBhB9One-iB54f0VQjktGXueHBCCGSmK_DD5cwHdqEVQ1qS2Ta-VGzUYCWkHBlK4GRx4P23GedRBmS5tne3Ty-BgCFZaKUefDgbG3holIBWmSY014XYAUWtITwX0dtgqHTFlWj2C-R0xZQI4Iae8UzyVWxf1Mm2UB-HhZfKsFdrDq3k-Sn58_fL95HR1dv5tc3J8tpKswmFVUJqJoqW4qtuiLAXJS5CFqDKUC1SyHKBEiDaywYUAmdd1W6KcNUUNhUSkKulR8nbnO2jr-VxSzzHFuKSYEBaJzY5orLjig1O9cLfcCsXvAtZ1XLigpAZOK1I3dZ1VLS2zmrI6I1nT5gTVTVO1OUSvz3O2se6hkWCCE3phutwxass7e80poYjhLBp8mA2c_TWCD7xXXoLWwoAdPa8wjndnDEXy3T_k45ebqU7E88fnsTGtnDz5cVawkmGcT9T6ESqOBnol4_drVYwvBB8XgsgEuAmdGL3nm8uL_2fPfy7Z93vsFoQOW2_1ePeLlmC2A6Wz3jtoH2qMEZ-6574afOoePndPlL3Zf58H0X270L-M3xly</recordid><startdate>20111205</startdate><enddate>20111205</enddate><creator>Cope, Emily K</creator><creator>Goldstein-Daruech, Natalia</creator><creator>Kofonow, Jennifer M</creator><creator>Christensen, Lanette</creator><creator>McDermott, Bridget</creator><creator>Monroy, Fernando</creator><creator>Palmer, James N</creator><creator>Chiu, Alexander G</creator><creator>Shirtliff, Mark E</creator><creator>Cohen, Noam A</creator><creator>Leid, Jeff G</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>AEUYN</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>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20111205</creationdate><title>Regulation of virulence gene expression resulting from Streptococcus pneumoniae and nontypeable Haemophilus influenzae interactions in chronic disease</title><author>Cope, Emily K ; Goldstein-Daruech, Natalia ; Kofonow, Jennifer M ; Christensen, Lanette ; McDermott, Bridget ; Monroy, Fernando ; Palmer, James N ; Chiu, Alexander G ; Shirtliff, Mark E ; Cohen, Noam A ; Leid, Jeff G</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c691t-7334a7f319bf788a258ec7a9405a0865ee8003dcd17aec5bbf8056d7be7c02983</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Analysis</topic><topic>Bacteria</topic><topic>Bacterial genetics</topic><topic>Bacterial infections</topic><topic>Biofilms</topic><topic>Biology</topic><topic>Biopsy</topic><topic>Chemical interactions</topic><topic>Chronic Disease</topic><topic>Chronic diseases</topic><topic>Chronic illnesses</topic><topic>Coculture Techniques</topic><topic>Communities</topic><topic>Culture</topic><topic>DNA polymerases</topic><topic>DNA Primers - 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Recent molecular studies have confirmed the importance of Streptococcus pneumoniae and nontypeable Haemophilus influenzae (NTHi) in CRS. Here, we hypothesize that interaction between S. pneumoniae and NTHi mixed-species communities cause a change in bacterial virulence gene expression. We examined CRS as a model human disease to validate these polymicrobial interactions. Clinical strains of S. pneumoniae and NTHi were grown in mono- and co-culture in a standard biofilm assay. Reverse transcriptase real-time PCR (RTqPCR) was used to measure gene expression of key virulence factors. To validate these results, we investigated the presence of the bacterial RNA transcripts in excised human tissue from patients with CRS. Consequences of physical or chemical interactions between microbes were also investigated. Transcription of NTHi type IV pili was only expressed in co-culture in vitro, and expression could be detected ex vivo in diseased tissue. S. pneumoniae pyruvate oxidase was up-regulated in co-culture, while pneumolysin and pneumococcal adherence factor A were down-regulated. These results were confirmed in excised human CRS tissue. Gene expression was differentially regulated by physical contact and secreted factors. Overall, these data suggest that interactions between H. influenzae and S. pneumoniae involve physical and chemical mechanisms that influence virulence gene expression of mixed-species biofilm communities present in chronically diseased human tissue. These results extend previous studies of population-level virulence and provide novel insight into the importance of S. pneumoniae and NTHi in CRS.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22162775</pmid><doi>10.1371/journal.pone.0028523</doi><tpages>e28523</tpages><oa>free_for_read</oa></addata></record> |
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| language | eng |
| recordid | cdi_plos_journals_1311831226 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Analysis Bacteria Bacterial genetics Bacterial infections Biofilms Biology Biopsy Chemical interactions Chronic Disease Chronic diseases Chronic illnesses Coculture Techniques Communities Culture DNA polymerases DNA Primers - genetics Ear diseases Gene Expression Gene Expression Regulation Genes Genes, Bacterial Genetic research Haemophilus influenzae Haemophilus influenzae - metabolism Hemophilus infections Humans Inflammation Medicine Metabolism Models, Statistical Otolaryngology Oxidases Pili Pneumolysin Pneumonia Polymerase chain reaction Population studies Pseudomonas aeruginosa Pyruvate oxidase Pyruvic acid Rhinosinusitis Ribonucleic acid RNA RNA - metabolism RNA, Bacterial - metabolism RNA, Ribosomal, 16S - metabolism RNA-directed DNA polymerase Sinusitis - microbiology Sinusitis - physiopathology Streptococcus infections Streptococcus pneumoniae Streptococcus pneumoniae - metabolism Studies Surgery Time Factors Transcription Vaccines Virulence Virulence (Microbiology) Virulence factors |
| title | Regulation of virulence gene expression resulting from Streptococcus pneumoniae and nontypeable Haemophilus influenzae interactions in chronic disease |
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