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Porphyromonas gingivalis Components/Secretions Synergistically Enhance Pneumonia Caused by Streptococcus pneumoniae in Mice
is an important causative organism of respiratory tract infections. Although periodontal bacteria have been shown to influence respiratory infections such as aspiration pneumonia, the synergistic effect of and , a periodontopathic bacterium, on pneumococcal infections is unclear. To investigate whet...
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Published in: | International journal of molecular sciences 2021-11, Vol.22 (23), p.12704 |
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creator | Okabe, Teppei Kamiya, Yosuke Kikuchi, Takeshi Goto, Hisashi Umemura, Masayuki Suzuki, Yuki Sugita, Yoshihiko Naiki, Yoshikazu Hasegawa, Yoshiaki Hayashi, Jun-Ichiro Kawamura, Shotaro Sawada, Noritaka Takayanagi, Yuhei Fujimura, Takeki Higuchi, Naoya Mitani, Akio |
description | is an important causative organism of respiratory tract infections. Although periodontal bacteria have been shown to influence respiratory infections such as aspiration pneumonia, the synergistic effect of
and
, a periodontopathic bacterium, on pneumococcal infections is unclear. To investigate whether
accelerates pneumococcal infections, we tested the effects of inoculating
culture supernatant (PgSup) into
-infected mice. Mice were intratracheally injected with
and PgSup to induce pneumonia, and lung histopathological sections and the absolute number and frequency of neutrophils and macrophages in the lung were analyzed. Proinflammatory cytokine/chemokine expression was examined by qPCR and ELISA. Inflammatory cell infiltration was observed in
-infected mice and
and PgSup mixed-infected mice, and mixed-infected mice showed more pronounced inflammation in lung. The ratios of monocytes/macrophages and neutrophils were not significantly different between the lungs of
-infected mice and those of mixed-infected mice. PgSup synergistically increased TNF-α expression/production and IL-17 production compared with
infection alone. We demonstrated that PgSup enhanced inflammation in pneumonia caused by
, suggesting that virulence factors produced by
are involved in the exacerbation of respiratory tract infections such as aspiration pneumonia. |
doi_str_mv | 10.3390/ijms222312704 |
format | article |
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and
, a periodontopathic bacterium, on pneumococcal infections is unclear. To investigate whether
accelerates pneumococcal infections, we tested the effects of inoculating
culture supernatant (PgSup) into
-infected mice. Mice were intratracheally injected with
and PgSup to induce pneumonia, and lung histopathological sections and the absolute number and frequency of neutrophils and macrophages in the lung were analyzed. Proinflammatory cytokine/chemokine expression was examined by qPCR and ELISA. Inflammatory cell infiltration was observed in
-infected mice and
and PgSup mixed-infected mice, and mixed-infected mice showed more pronounced inflammation in lung. The ratios of monocytes/macrophages and neutrophils were not significantly different between the lungs of
-infected mice and those of mixed-infected mice. PgSup synergistically increased TNF-α expression/production and IL-17 production compared with
infection alone. We demonstrated that PgSup enhanced inflammation in pneumonia caused by
, suggesting that virulence factors produced by
are involved in the exacerbation of respiratory tract infections such as aspiration pneumonia.</description><identifier>ISSN: 1422-0067</identifier><identifier>ISSN: 1661-6596</identifier><identifier>EISSN: 1422-0067</identifier><identifier>DOI: 10.3390/ijms222312704</identifier><identifier>PMID: 34884507</identifier><language>eng</language><publisher>Switzerland: MDPI AG</publisher><subject>Animals ; Bacteria ; Bacterial infections ; Bacteroidaceae Infections - complications ; Bacteroidaceae Infections - microbiology ; Cell culture ; Chemokines ; Chemokines - metabolism ; Coronaviruses ; COVID-19 ; Cytokines ; Cytokines - metabolism ; Gene expression ; Inflammation ; Inflammation - etiology ; Inflammation - pathology ; Interleukin 17 ; Leukocytes (neutrophilic) ; Lung - immunology ; Lung - metabolism ; Lung - microbiology ; Lung - pathology ; Lungs ; Macrophages ; Mice ; Mice, Inbred C57BL ; Monocytes ; Mortality ; Neutrophil Infiltration - immunology ; Oral hygiene ; Pathogens ; Pneumonia ; Pneumonia, Pneumococcal - epidemiology ; Pneumonia, Pneumococcal - metabolism ; Pneumonia, Pneumococcal - microbiology ; Pneumonia, Pneumococcal - pathology ; Porphyromonas gingivalis ; Porphyromonas gingivalis - physiology ; Respiratory tract diseases ; Secretions ; Streptococcus infections ; Streptococcus pneumoniae ; Streptococcus pneumoniae - physiology ; Synergistic effect ; Tumor necrosis factor-TNF ; Tumor necrosis factor-α ; Virulence ; Virulence factors</subject><ispartof>International journal of molecular sciences, 2021-11, Vol.22 (23), p.12704</ispartof><rights>2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2021 by the authors. 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c547t-31422823017d6319ca5572d03a61f6b25a52a2e31c84cdfd7a692d3544ef4d143</citedby><cites>FETCH-LOGICAL-c547t-31422823017d6319ca5572d03a61f6b25a52a2e31c84cdfd7a692d3544ef4d143</cites><orcidid>0000-0001-5427-411X ; 0000-0003-0310-5302 ; 0000-0003-2640-2860 ; 0000-0002-5433-6998 ; 0000-0001-9742-5184 ; 0000-0003-3660-6867</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2608123263/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2608123263?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,38516,43895,44590,53791,53793,74412,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34884507$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Okabe, Teppei</creatorcontrib><creatorcontrib>Kamiya, Yosuke</creatorcontrib><creatorcontrib>Kikuchi, Takeshi</creatorcontrib><creatorcontrib>Goto, Hisashi</creatorcontrib><creatorcontrib>Umemura, Masayuki</creatorcontrib><creatorcontrib>Suzuki, Yuki</creatorcontrib><creatorcontrib>Sugita, Yoshihiko</creatorcontrib><creatorcontrib>Naiki, Yoshikazu</creatorcontrib><creatorcontrib>Hasegawa, Yoshiaki</creatorcontrib><creatorcontrib>Hayashi, Jun-Ichiro</creatorcontrib><creatorcontrib>Kawamura, Shotaro</creatorcontrib><creatorcontrib>Sawada, Noritaka</creatorcontrib><creatorcontrib>Takayanagi, Yuhei</creatorcontrib><creatorcontrib>Fujimura, Takeki</creatorcontrib><creatorcontrib>Higuchi, Naoya</creatorcontrib><creatorcontrib>Mitani, Akio</creatorcontrib><title>Porphyromonas gingivalis Components/Secretions Synergistically Enhance Pneumonia Caused by Streptococcus pneumoniae in Mice</title><title>International journal of molecular sciences</title><addtitle>Int J Mol Sci</addtitle><description>is an important causative organism of respiratory tract infections. Although periodontal bacteria have been shown to influence respiratory infections such as aspiration pneumonia, the synergistic effect of
and
, a periodontopathic bacterium, on pneumococcal infections is unclear. To investigate whether
accelerates pneumococcal infections, we tested the effects of inoculating
culture supernatant (PgSup) into
-infected mice. Mice were intratracheally injected with
and PgSup to induce pneumonia, and lung histopathological sections and the absolute number and frequency of neutrophils and macrophages in the lung were analyzed. Proinflammatory cytokine/chemokine expression was examined by qPCR and ELISA. Inflammatory cell infiltration was observed in
-infected mice and
and PgSup mixed-infected mice, and mixed-infected mice showed more pronounced inflammation in lung. The ratios of monocytes/macrophages and neutrophils were not significantly different between the lungs of
-infected mice and those of mixed-infected mice. PgSup synergistically increased TNF-α expression/production and IL-17 production compared with
infection alone. We demonstrated that PgSup enhanced inflammation in pneumonia caused by
, suggesting that virulence factors produced by
are involved in the exacerbation of respiratory tract infections such as aspiration pneumonia.</description><subject>Animals</subject><subject>Bacteria</subject><subject>Bacterial infections</subject><subject>Bacteroidaceae Infections - complications</subject><subject>Bacteroidaceae Infections - microbiology</subject><subject>Cell culture</subject><subject>Chemokines</subject><subject>Chemokines - metabolism</subject><subject>Coronaviruses</subject><subject>COVID-19</subject><subject>Cytokines</subject><subject>Cytokines - metabolism</subject><subject>Gene expression</subject><subject>Inflammation</subject><subject>Inflammation - etiology</subject><subject>Inflammation - pathology</subject><subject>Interleukin 17</subject><subject>Leukocytes (neutrophilic)</subject><subject>Lung - immunology</subject><subject>Lung - metabolism</subject><subject>Lung - microbiology</subject><subject>Lung - pathology</subject><subject>Lungs</subject><subject>Macrophages</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Monocytes</subject><subject>Mortality</subject><subject>Neutrophil Infiltration - immunology</subject><subject>Oral hygiene</subject><subject>Pathogens</subject><subject>Pneumonia</subject><subject>Pneumonia, Pneumococcal - epidemiology</subject><subject>Pneumonia, Pneumococcal - metabolism</subject><subject>Pneumonia, Pneumococcal - microbiology</subject><subject>Pneumonia, Pneumococcal - pathology</subject><subject>Porphyromonas gingivalis</subject><subject>Porphyromonas gingivalis - physiology</subject><subject>Respiratory tract diseases</subject><subject>Secretions</subject><subject>Streptococcus infections</subject><subject>Streptococcus pneumoniae</subject><subject>Streptococcus pneumoniae - physiology</subject><subject>Synergistic effect</subject><subject>Tumor necrosis factor-TNF</subject><subject>Tumor necrosis factor-α</subject><subject>Virulence</subject><subject>Virulence factors</subject><issn>1422-0067</issn><issn>1661-6596</issn><issn>1422-0067</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>COVID</sourceid><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNpdkk1r3DAQhk1padK0x16LoJdc3OjTsi-FsiRpIKWBbc9CK429WmzJleyA6Z-vNpuEbE8S0sMzekdTFB8J_sJYgy_cbkiUUkaoxPxVcUo4pSXGlXz9Yn9SvEtphzFlVDRvixPG65oLLE-Lv3chjtslhiF4nVDnfOfude8SWoVhDB78lC7WYCJMLviE1ouH2Lk0OaP7fkGXfqu9AXTnYc4Kp9FKzwks2ixoPUUYp2CCMXNC4xMByHn0wxl4X7xpdZ_gw-N6Vvy-uvy1-l7e_ry-WX27LY3gcirZPkZNGSbSVow0RgshqcVMV6StNlRoQTUFRkzNjW2t1FVDLROcQ8st4eysuDl4bdA7NUY36LiooJ16OAixUzrmQD2ojbSYmoYIQQjHtWgYrnN9bk1TsdaI7Pp6cI3zZgBrcn-i7o-kxzfebVUX7lVdCSmbveD8URDDnxnSpAaXDPS99hDmpGiVyzIhCcvo5__QXZijz616oEj-zWpPlQfKxJBShPb5MQSr_YiooxHJ_KeXCZ7pp5lg_wBYg7jf</recordid><startdate>20211124</startdate><enddate>20211124</enddate><creator>Okabe, Teppei</creator><creator>Kamiya, Yosuke</creator><creator>Kikuchi, Takeshi</creator><creator>Goto, Hisashi</creator><creator>Umemura, Masayuki</creator><creator>Suzuki, Yuki</creator><creator>Sugita, Yoshihiko</creator><creator>Naiki, Yoshikazu</creator><creator>Hasegawa, Yoshiaki</creator><creator>Hayashi, Jun-Ichiro</creator><creator>Kawamura, Shotaro</creator><creator>Sawada, Noritaka</creator><creator>Takayanagi, Yuhei</creator><creator>Fujimura, Takeki</creator><creator>Higuchi, Naoya</creator><creator>Mitani, Akio</creator><general>MDPI AG</general><general>MDPI</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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>COVID</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>MBDVC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-5427-411X</orcidid><orcidid>https://orcid.org/0000-0003-0310-5302</orcidid><orcidid>https://orcid.org/0000-0003-2640-2860</orcidid><orcidid>https://orcid.org/0000-0002-5433-6998</orcidid><orcidid>https://orcid.org/0000-0001-9742-5184</orcidid><orcidid>https://orcid.org/0000-0003-3660-6867</orcidid></search><sort><creationdate>20211124</creationdate><title>Porphyromonas gingivalis Components/Secretions Synergistically Enhance Pneumonia Caused by Streptococcus pneumoniae in Mice</title><author>Okabe, Teppei ; Kamiya, Yosuke ; Kikuchi, Takeshi ; Goto, Hisashi ; Umemura, Masayuki ; Suzuki, Yuki ; Sugita, Yoshihiko ; Naiki, Yoshikazu ; Hasegawa, Yoshiaki ; Hayashi, Jun-Ichiro ; Kawamura, Shotaro ; Sawada, Noritaka ; Takayanagi, Yuhei ; Fujimura, Takeki ; Higuchi, Naoya ; Mitani, Akio</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c547t-31422823017d6319ca5572d03a61f6b25a52a2e31c84cdfd7a692d3544ef4d143</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animals</topic><topic>Bacteria</topic><topic>Bacterial infections</topic><topic>Bacteroidaceae Infections - 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microbiology</topic><topic>Pneumonia, Pneumococcal - pathology</topic><topic>Porphyromonas gingivalis</topic><topic>Porphyromonas gingivalis - physiology</topic><topic>Respiratory tract diseases</topic><topic>Secretions</topic><topic>Streptococcus infections</topic><topic>Streptococcus pneumoniae</topic><topic>Streptococcus pneumoniae - physiology</topic><topic>Synergistic effect</topic><topic>Tumor necrosis factor-TNF</topic><topic>Tumor necrosis factor-α</topic><topic>Virulence</topic><topic>Virulence factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Okabe, Teppei</creatorcontrib><creatorcontrib>Kamiya, Yosuke</creatorcontrib><creatorcontrib>Kikuchi, Takeshi</creatorcontrib><creatorcontrib>Goto, Hisashi</creatorcontrib><creatorcontrib>Umemura, Masayuki</creatorcontrib><creatorcontrib>Suzuki, Yuki</creatorcontrib><creatorcontrib>Sugita, Yoshihiko</creatorcontrib><creatorcontrib>Naiki, Yoshikazu</creatorcontrib><creatorcontrib>Hasegawa, Yoshiaki</creatorcontrib><creatorcontrib>Hayashi, Jun-Ichiro</creatorcontrib><creatorcontrib>Kawamura, Shotaro</creatorcontrib><creatorcontrib>Sawada, Noritaka</creatorcontrib><creatorcontrib>Takayanagi, Yuhei</creatorcontrib><creatorcontrib>Fujimura, Takeki</creatorcontrib><creatorcontrib>Higuchi, Naoya</creatorcontrib><creatorcontrib>Mitani, Akio</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>Coronavirus Research Database</collection><collection>ProQuest Central</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>Research Library</collection><collection>Research Library (Corporate)</collection><collection>Publicly Available Content Database</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><collection>ProQuest Central Basic</collection><collection>MEDLINE - 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Although periodontal bacteria have been shown to influence respiratory infections such as aspiration pneumonia, the synergistic effect of
and
, a periodontopathic bacterium, on pneumococcal infections is unclear. To investigate whether
accelerates pneumococcal infections, we tested the effects of inoculating
culture supernatant (PgSup) into
-infected mice. Mice were intratracheally injected with
and PgSup to induce pneumonia, and lung histopathological sections and the absolute number and frequency of neutrophils and macrophages in the lung were analyzed. Proinflammatory cytokine/chemokine expression was examined by qPCR and ELISA. Inflammatory cell infiltration was observed in
-infected mice and
and PgSup mixed-infected mice, and mixed-infected mice showed more pronounced inflammation in lung. The ratios of monocytes/macrophages and neutrophils were not significantly different between the lungs of
-infected mice and those of mixed-infected mice. PgSup synergistically increased TNF-α expression/production and IL-17 production compared with
infection alone. We demonstrated that PgSup enhanced inflammation in pneumonia caused by
, suggesting that virulence factors produced by
are involved in the exacerbation of respiratory tract infections such as aspiration pneumonia.</abstract><cop>Switzerland</cop><pub>MDPI AG</pub><pmid>34884507</pmid><doi>10.3390/ijms222312704</doi><orcidid>https://orcid.org/0000-0001-5427-411X</orcidid><orcidid>https://orcid.org/0000-0003-0310-5302</orcidid><orcidid>https://orcid.org/0000-0003-2640-2860</orcidid><orcidid>https://orcid.org/0000-0002-5433-6998</orcidid><orcidid>https://orcid.org/0000-0001-9742-5184</orcidid><orcidid>https://orcid.org/0000-0003-3660-6867</orcidid><oa>free_for_read</oa></addata></record> |
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source | Publicly Available Content Database; PubMed Central; Coronavirus Research Database |
subjects | Animals Bacteria Bacterial infections Bacteroidaceae Infections - complications Bacteroidaceae Infections - microbiology Cell culture Chemokines Chemokines - metabolism Coronaviruses COVID-19 Cytokines Cytokines - metabolism Gene expression Inflammation Inflammation - etiology Inflammation - pathology Interleukin 17 Leukocytes (neutrophilic) Lung - immunology Lung - metabolism Lung - microbiology Lung - pathology Lungs Macrophages Mice Mice, Inbred C57BL Monocytes Mortality Neutrophil Infiltration - immunology Oral hygiene Pathogens Pneumonia Pneumonia, Pneumococcal - epidemiology Pneumonia, Pneumococcal - metabolism Pneumonia, Pneumococcal - microbiology Pneumonia, Pneumococcal - pathology Porphyromonas gingivalis Porphyromonas gingivalis - physiology Respiratory tract diseases Secretions Streptococcus infections Streptococcus pneumoniae Streptococcus pneumoniae - physiology Synergistic effect Tumor necrosis factor-TNF Tumor necrosis factor-α Virulence Virulence factors |
title | Porphyromonas gingivalis Components/Secretions Synergistically Enhance Pneumonia Caused by Streptococcus pneumoniae in Mice |
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