{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,20]],"date-time":"2026-09-20T22:27:23Z","timestamp":1789943243626,"version":"4.0.1"},"reference-count":31,"publisher":"Oxford University Press (OUP)","issue":"1","license":[{"start":{"date-parts":[[2014,9,4]],"date-time":"2014-09-04T00:00:00Z","timestamp":1409788800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2014,9,4]]},"abstract":"<jats:title>Summary<\/jats:title>\n               <jats:p>Periodontitis is an inflammatory infectious disease that destroys the tooth-supporting tissues. It is caused by multi-species subgingival biofilms that colonize the tooth surface. Porphyromonas gingivalis, Treponema denticola and Tannerella forsythia (i.e. \u2018red complex\u2019 bacteria) are characteristic subgingival biofilm species. The triggering receptor expressed on myeloid cells 1 (TREM-1) is a cell surface receptor of the immunoglobulin superfamily, with a role in the amplification of proinflammatory cytokine production during infection. This study aimed to investigate TREM-1 mRNA expression in gingival tissues from patients with chronic periodontitis, generalized aggressive periodontitis and healthy subjects and its correlation with the levels of periodontal pathogens in the tissue. A further aim was to investigate the regulation of TREM-1 in human monocytic cells (MM6) challenged with an in-vitro subgingival biofilm model. Gingival tissue TREM-1 expression was increased in both chronic and aggressive periodontitis, compared to health, and correlated with the levels of the \u2018red complex\u2019 species in the tissue. No significant differences were detected between the two forms of periodontitis. Biofilm-challenged MM6 cells exhibited higher TREM-1 expression and secretion compared to controls, with partial involvement of the \u2018red complex\u2019. Engagement or inhibition of TREM-1 affected the capacity of the biofilms to stimulate interleukin (IL)-1\u03b2, but not IL-8, secretion by the cells. In conclusion, this study reveals that TREM-1 tissue expression is enhanced in periodontal disease, and correlates with the level of periodontal pathogens. It also provides a mechanistic insight into the regulation of TREM-1 expression and the associated IL-1\u03b2 production in biofilm-challenged monocytes.<\/jats:p>","DOI":"10.1111\/cei.12397","type":"journal-article","created":{"date-parts":[[2014,6,13]],"date-time":"2014-06-13T10:38:10Z","timestamp":1402655890000},"page":"190-200","source":"Crossref","is-referenced-by-count":34,"title":["Expression and regulation of triggering receptor expressed on myeloid cells 1 in periodontal diseases"],"prefix":"10.1093","volume":"178","author":[{"given":"M","family":"Willi","sequence":"first","affiliation":[{"name":"Section of Oral Translational Research, Institute of Oral Biology, Center of Dental Medicine, University of Z\u00fcrich, Z\u00fcrich, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"G N","family":"Belibasakis","sequence":"additional","affiliation":[{"name":"Section of Oral Microbiology, Institute of Oral Biology, Center of Dental Medicine, University of Z\u00fcrich, Z\u00fcrich, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"N","family":"Bostanci","sequence":"additional","affiliation":[{"name":"Section of Oral Translational Research, Institute of Oral Biology, Center of Dental Medicine, University of Z\u00fcrich, Z\u00fcrich, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2014,9,4]]},"reference":[{"key":"2021122010102389900_cei12397-bib-0001","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1902\/annals.1999.4.1.1","article-title":"Development of a classification system for periodontal diseases and conditions","volume":"4","author":"Armitage","year":"1999","journal-title":"Ann Periodontol"},{"key":"2021122010102389900_cei12397-bib-0002","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1046\/j.0906-6713.2002.003421.x","article-title":"Periodontal diagnoses and classification of periodontal diseases","volume":"34","author":"Armitage","year":"2004","journal-title":"Periodontol 2000"},{"key":"2021122010102389900_cei12397-bib-0003","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1111\/j.1600-051X.1998.tb02419.x","article-title":"Microbial complexes in subgingival plaque","volume":"25","author":"Socransky","year":"1998","journal-title":"J Clin Periodontol"},{"key":"2021122010102389900_cei12397-bib-0004","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1111\/j.1600-0757.2009.00331.x","article-title":"Aggregatibacter (Actinobacillus) actinomycetemcomitans: a triple A* periodontopathogen?","volume":"54","author":"Henderson","year":"2010","journal-title":"Periodontol 2000"},{"key":"2021122010102389900_cei12397-bib-0005","doi-asserted-by":"crossref","first-page":"1165","DOI":"10.1177\/154405910508401214","article-title":"Streptococci dominate the diverse flora within buccal cells","volume":"84","author":"Rudney","year":"2005","journal-title":"J Dent Res"},{"key":"2021122010102389900_cei12397-bib-0006","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1177\/154405910508400110","article-title":"Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, and Tannerella forsythensis are components of a polymicrobial intracellular flora within human buccal cells","volume":"84","author":"Rudney","year":"2005","journal-title":"J Dent Res"},{"key":"2021122010102389900_cei12397-bib-0007","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1016\/j.patbio.2006.07.045","article-title":"[Pathogenic potential of Porphyromonas gingivalis, Treponema denticola and Tannerella forsythia, the red bacterial complex associated with periodontitis]","volume":"55","author":"Bodet","year":"2007","journal-title":"Pathol Biol (Paris)"},{"key":"2021122010102389900_cei12397-bib-0008","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1034\/j.1600-0757.2002.03006.x","article-title":"In or out: the invasiveness of oral bacteria","volume":"30","author":"Lamont","year":"2002","journal-title":"Periodontol 2000"},{"key":"2021122010102389900_cei12397-bib-0009","doi-asserted-by":"crossref","first-page":"1266","DOI":"10.1038\/ni1411","article-title":"The TREM receptor family and signal integration","volume":"7","author":"Klesney-Tait","year":"2006","journal-title":"Nat Immunol"},{"key":"2021122010102389900_cei12397-bib-0010","doi-asserted-by":"crossref","first-page":"3812","DOI":"10.4049\/jimmunol.170.7.3812","article-title":"A role for triggering receptor expressed on myeloid cells-1 in host defense during the early-induced and adaptive phases of the immune response","volume":"170","author":"Bleharski","year":"2003","journal-title":"J Immunol"},{"key":"2021122010102389900_cei12397-bib-0011","doi-asserted-by":"crossref","first-page":"1103","DOI":"10.1038\/35074114","article-title":"TREM-1 amplifies inflammation and is a crucial mediator of septic shock","volume":"410","author":"Bouchon","year":"2001","journal-title":"Nature"},{"key":"2021122010102389900_cei12397-bib-0012","doi-asserted-by":"crossref","first-page":"1768","DOI":"10.1136\/ard.2008.089557","article-title":"Elevated synovial expression of triggering receptor expressed on myeloid cells 1 in patients with septic arthritis or rheumatoid arthritis","volume":"68","author":"Collins","year":"2009","journal-title":"Ann Rheum Dis"},{"key":"2021122010102389900_cei12397-bib-0013","doi-asserted-by":"crossref","first-page":"1419","DOI":"10.1084\/jem.20040708","article-title":"A soluble form of the triggering receptor expressed on myeloid cells-1 modulates the inflammatory response in murine sepsis","volume":"200","author":"Gibot","year":"2004","journal-title":"J Exp Med"},{"key":"2021122010102389900_cei12397-bib-0014","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1056\/NEJMoa031544","article-title":"Soluble triggering receptor expressed on myeloid cells and the diagnosis of pneumonia","volume":"350","author":"Gibot","year":"2004","journal-title":"N Engl J Med"},{"key":"2021122010102389900_cei12397-bib-0015","doi-asserted-by":"crossref","first-page":"975","DOI":"10.1086\/506950","article-title":"Modulation of the triggering receptor expressed on myeloid cells-1 pathway during pneumonia in rats","volume":"194","author":"Gibot","year":"2006","journal-title":"J Infect Dis"},{"key":"2021122010102389900_cei12397-bib-0016","doi-asserted-by":"crossref","first-page":"2823","DOI":"10.1128\/IAI.74.5.2823-2830.2006","article-title":"Modulation of the triggering receptor expressed on the myeloid cell type 1 pathway in murine septic shock","volume":"74","author":"Gibot","year":"2006","journal-title":"Infect Immun"},{"key":"2021122010102389900_cei12397-bib-0017","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1055\/s-2006-933671","article-title":"Soluble triggering receptor expressed on myeloid cells and the diagnosis of pneumonia and severe sepsis","volume":"27","author":"Gibot","year":"2006","journal-title":"Semin Respir Crit Care Med"},{"key":"2021122010102389900_cei12397-bib-0018","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1111\/j.1600-0757.1999.tb00163.x","article-title":"The role of the cell-mediated immune response to Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in periodontitis","volume":"20","author":"Zadeh","year":"1999","journal-title":"Periodontol 2000"},{"key":"2021122010102389900_cei12397-bib-0019","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1016\/j.molimm.2011.09.012","article-title":"Involvement of the TREM-1\/DAP12 pathway in the innate immune responses to Porphyromonas gingivalis","volume":"49","author":"Bostanci","year":"2011","journal-title":"Mol Immunol"},{"key":"2021122010102389900_cei12397-bib-0020","doi-asserted-by":"crossref","first-page":"e75784","DOI":"10.1371\/journal.pone.0075784","article-title":"Porphyromonas gingivalis regulates TREM-1 in human polymorphonuclear neutrophils via its gingipains","volume":"8","author":"Bostanci","year":"2013","journal-title":"PLOS ONE"},{"key":"2021122010102389900_cei12397-bib-0021","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1177\/0022034512470691","article-title":"Elevated oral and systemic levels of soluble triggering receptor expressed on myeloid cells-1 (sTREM-1) in periodontitis","volume":"92","author":"Bostanci","year":"2013","journal-title":"J Dent Res"},{"key":"2021122010102389900_cei12397-bib-0022","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1902\/jop.2013.130144","article-title":"Triggering receptor expressed on myeloid cells (sTREM)-1 in gingival crevicular fluid: association with clinical and microbiological parameters","volume":"85","author":"Belibasakis","year":"2014","journal-title":"J Periodontol"},{"key":"2021122010102389900_cei12397-bib-0023","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1111\/j.1600-0765.2006.00946.x","article-title":"Differential expression of receptor activator of nuclear factor-kappaB ligand and osteoprotegerin mRNA in periodontal diseases","volume":"42","author":"Bostanci","year":"2007","journal-title":"J Periodont Res"},{"key":"2021122010102389900_cei12397-bib-0024","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1111\/jre.12034","article-title":"Validation of a quantitative real-time PCR assay and comparison with fluorescence microscopy and selective agar plate counting for species-specific quantification of an in vitro subgingival biofilm model","volume":"48","author":"Ammann","year":"2013","journal-title":"J Periodont Res"},{"key":"2021122010102389900_cei12397-bib-0025","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.cyto.2011.03.009","article-title":"The RANKL\u2013OPG system is differentially regulated by supragingival and subgingival biofilm supernatants","volume":"55","author":"Belibasakis","year":"2011","journal-title":"Cytokine"},{"key":"2021122010102389900_cei12397-bib-0026","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1111\/j.1574-695X.2011.00863.x","article-title":"Induction of prostaglandin E(2) and interleukin-6 in gingival fibroblasts by oral biofilms","volume":"63","author":"Belibasakis","year":"2011","journal-title":"FEMS Immunol Med Microbiol"},{"key":"2021122010102389900_cei12397-bib-0027","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1177\/1753425912444767","article-title":"Down-regulation of NLRP3 of NLRP3 inflammasome in gingival fibroblasts by subgingival biofilms: involvement of Porphyromonas gingivalis","volume":"19","author":"Belibasakis","year":"2013","journal-title":"Innate Immun"},{"key":"2021122010102389900_cei12397-bib-0028","doi-asserted-by":"crossref","first-page":"4991","DOI":"10.4049\/jimmunol.164.10.4991","article-title":"Cutting edge: inflammatory responses can be triggered by TREM-1, a novel receptor expressed on neutrophils and monocytes","volume":"164","author":"Bouchon","year":"2000","journal-title":"J Immunol"},{"key":"2021122010102389900_cei12397-bib-0029","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1111\/j.1600-0757.2010.00349.x","article-title":"Immunological differences and similarities between chronic periodontitis and aggressive periodontitis","volume":"53","author":"Ford","year":"2010","journal-title":"Periodontol 2000"},{"key":"2021122010102389900_cei12397-bib-0030","doi-asserted-by":"crossref","first-page":"2112","DOI":"10.1902\/jop.2008.080139","article-title":"Transcriptomes in healthy and diseased gingival tissues","volume":"79","author":"Demmer","year":"2008","journal-title":"J Periodontol"},{"key":"2021122010102389900_cei12397-bib-0031","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1111\/j.1574-695X.2012.00982.x","article-title":"Doxycycline inhibits TREM-1 induction by Porphyromonas gingivalis","volume":"66","author":"Bostanci","year":"2012","journal-title":"FEMS Immunol Med Microbiol"}],"container-title":["Clinical and Experimental Immunology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1111%2Fcei.12397","content-type":"unspecified","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/academic.oup.com\/cei\/article-pdf\/178\/1\/190\/41790634\/cei12397.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/cei\/article-pdf\/178\/1\/190\/41790634\/cei12397.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,1,1]],"date-time":"2022-01-01T16:26:34Z","timestamp":1641054394000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/cei\/article\/178\/1\/190\/6421997"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2014,9,4]]},"references-count":31,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2014,9,4]]},"published-print":{"date-parts":[[2014,9,4]]}},"URL":"https:\/\/doi.org\/10.1111\/cei.12397","relation":{},"ISSN":["0009-9104","1365-2249"],"issn-type":[{"value":"0009-9104","type":"print"},{"value":"1365-2249","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2014,10]]},"published":{"date-parts":[[2014,9,4]]}}}