Involvement of the TREM-1/DAP12 pathway in the innate immune responses to Porphyromonas gingivalis

Molecular Immunology

Volumn 49, Issue 1-2, 2011, Pages 387-394

  Bostanci, Nagihan ^a   Thurnheer, Thomas ^a   Belibasakis, Georgios N ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Cytokines; DAP12; Inflammation; Innate immunity; LP17; MonoMac 6; Periodontal disease; Porphyromonas gingivalis; TREM 1

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 6; KILLER CELL ACTIVATING RECEPTOR ASSOCIATED PROTEIN; LP 17; PROTEIN INHIBITOR; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 1; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 1 ANTAGONIST; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL IMMUNITY; BACTERIAL VIABILITY; CELL LINE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNOPOTENTIATION; INNATE IMMUNITY; MONOCYTE; MOUSE; NONHUMAN; PERIODONTAL DISEASE; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL LINE; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; HUMANS; IMMUNITY, INNATE; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; MONOCYTES; PORPHYROMONAS GINGIVALIS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PORPHYROMONAS GINGIVALIS;

EID: 82455218964     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2011.09.012     Document Type: Article

References (69)

1. Allcock R.J., Barrow A.D., Forbes S., Beck S., Trowsdale J. The human TREM gene cluster at 6p21.1 encodes both activating and inhibitory single IgV domain receptors and includes NKp44. Eur. J. Immunol. 2003, 33:567-577.
2. Aoki N., Zganiacz A., Margetts P., Xing Z. Differential regulation of DAP12 and molecules associated with DAP12 during host responses to mycobacterial infection. Infect. Immun. 2004, 72:2477-2483.
3. Arts R.J., Joosten L.A., Dinarello C.A., Kullberg B.J., van der Meer J.W., Netea M.G. TREM-1 interaction with the LPS/TLR4 receptor complex. Eur. Cytokine Netw. 2011, 22:11-14.
4. Begum N.A., Ishii K., Kurita-Taniguchi M., Tanabe M., Kobayashi M., Moriwaki Y., Matsumoto M., Fukumori Y., Azuma I., Toyoshima K., Seya T. Mycobacterium bovis BCG cell wall-specific differentially expressed genes identified by differential display and cDNA subtraction in human macrophages. Infect. Immun. 2004, 72:937-948.
5. Bleharski J.R., Kiessler V., Buonsanti C., Sieling P.A., Stenger S., Colonna M., Modlin R.L. A role for triggering receptor expressed on myeloid cells-1 in host defense during the early-induced and adaptive phases of the immune response. J. Immunol. 2003, 170:3812-3818.
6. Bostanci N., Allaker R., Johansson U., Rangarajan M., Curtis M.A., Hughes F.J., McKay I.J. Interleukin-1alpha stimulation in monocytes by periodontal bacteria: antagonistic effects of Porphyromonas gingivalis. Oral Microbiol. Immunol. 2007, 22:52-60.
7. Bostanci N., Allaker R.P., Belibasakis G.N., Rangarajan M., Curtis M.A., Hughes F.J., McKay I.J. Porphyromonas gingivalis antagonises Campylobacter rectus induced cytokine production by human monocytes. Cytokine 2007, 39:147-156.
8. Bouchon A., Dietrich J., Colonna M. Cutting edge: inflammatory responses can be triggered by TREM-1, a novel receptor expressed on neutrophils and monocytes. J. Immunol. 2000, 164:4991-4995.
9. Bouchon A., Facchetti F., Weigand M.A., Colonna M. TREM-1 amplifies inflammation and is a crucial mediator of septic shock. Nature 2001, 410:1103-1107.
10. Brodala N., Merricks E.P., Bellinger D.A., Damrongsri D., Offenbacher S., Beck J., Madianos P., Sotres D., Chang Y.L., Koch G., Nichols T.C. Porphyromonas gingivalis bacteremia induces coronary and aortic atherosclerosis in normocholesterolemic and hypercholesterolemic pigs. Arterioscler. Thromb. Vasc. Biol. 2005, 25:1446-1451.
11. Buckland K.F., Ramaprakash H., Murray L.A., Carpenter K.J., Choi E.S., Kunkel S.L., Lukacs N.W., Xing Z., Aoki N., Hartl D., Hogaboam C.M. Triggering receptor expressed on myeloid cells-1 (TREM-1) modulates immune responses to Aspergillus fumigatus during fungal asthma in mice. Immunol. Invest. 2011.
12. Burns E., Bachrach G., Shapira L., Nussbaum G. Cutting Edge: TLR2 is required for the innate response to Porphyromonas gingivalis: activation leads to bacterial persistence and TLR2 deficiency attenuates induced alveolar bone resorption. J. Immunol. 2006, 177:8296-8300.
13. Cappelli D., Steffen M.J., Holt S.C., Ebersole J.L. Periodontitis in pregnancy: clinical and serum antibody observations from a baboon model of ligature-induced disease. J. Periodontol. 2009, 80:1154-1165.
14. Cavaillon J.M. Monocyte TREM-1 membrane expression in non-infectious inflammation. Crit. Care 2009, 13:152.
15. Collins C.E., La D.T., Yang H.T., Massin F., Gibot S., Faure G., Stohl W. Elevated synovial expression of triggering receptor expressed on myeloid cells 1 in patients with septic arthritis or rheumatoid arthritis. Ann. Rheum. Dis. 2009, 68:1768-1774.
16. Colonna M., Facchetti F. TREM-1 (triggering receptor expressed on myeloid cells): a new player in acute inflammatory responses. J. Infect. Dis. 2003, 187(Suppl. 2):S397-S401.
17. Curtis M.A., Aduse-Opoku J., Rangarajan M. Cysteine proteases of Porphyromonas gingivalis. Crit. Rev. Oral Biol. Med. 2001, 12:192-216.
18. Darveau R.P. Periodontitis: a polymicrobial disruption of host homeostasis. Nat. Rev. Microbiol. 2011, 8:481-490.
19. del Fresno C., Gomez-Pina V., Lores V., Soares-Schanoski A., Fernandez-Ruiz I., Rojo B., Alvarez-Sala R., Caballero-Garrido E., Garcia F., Veliz T., Arnalich F., Fuentes-Prior P., Garcia-Rio F., Lopez-Collazo E. Monocytes from cystic fibrosis patients are locked in an LPS tolerance state: down-regulation of TREM-1 as putative underlying mechanism. PLoS One 2008, 3:e2667.
20. Dower K., Ellis D.K., Saraf K., Jelinsky S.A., Lin L.L. Innate immune responses to TREM-1 activation: overlap, divergence, and positive and negative cross-talk with bacterial lipopolysaccharide. J. Immunol. 2008, 180:3520-3534.
21. El Mezayen R., El Gazzar M., Seeds M.C., McCall C.E., Dreskin S.C., Nicolls M.R. Endogenous signals released from necrotic cells augment inflammatory responses to bacterial endotoxin. Immunol. Lett. 2007, 111:36-44.
22. Ferat-Osorio E., Wong-Baeza I., Esquivel-Callejas N., Figueroa-Figueroa S., Duarte-Rojo A., Guzman-Valdivia-Gomez G., Rodea-Rosas H., Torres-Gonzalez R., Sanchez-Fernandez P., Arriaga-Pizano L., Lopez-Macias C., Robles-Diaz G., Isibasi A. Triggering receptor expressed on myeloid cells-1 expression on monocytes is associated with inflammation but not with infection in acute pancreatitis. Crit. Care 2009, 13:R69.
23. Ford J.W., McVicar D.W. TREM and TREM-like receptors in inflammation and disease. Curr. Opin. Immunol. 2009, 21:38-46.
24. Gibot S., Cravoisy A. Soluble form of the triggering receptor expressed on myeloid cells-1 as a marker of microbial infection. Clin. Med. Res. 2004, 2:181-187.
25. Gibot S., Cravoisy A., Kolopp-Sarda M.N., Bene M.C., Faure G., Bollaert P.E., Levy B. Time-course of sTREM (soluble triggering receptor expressed on myeloid cells)-1, procalcitonin, and C-reactive protein plasma concentrations during sepsis. Crit. Care Med. 2005, 33:792-796.
26. Gibot S., Cravoisy A., Levy B., Bene M.C., Faure G., Bollaert P.E. Soluble triggering receptor expressed on myeloid cells and the diagnosis of pneumonia. N. Engl. J. Med. 2004, 350:451-458.
27. Gibot S., Kolopp-Sarda M.N., Bene M.C., Bollaert P.E., Lozniewski A., Mory F., Levy B., Faure G.C. A soluble form of the triggering receptor expressed on myeloid cells-1 modulates the inflammatory response in murine sepsis. J. Exp. Med. 2004, 200:1419-1426.
28. Gibot S., Kolopp-Sarda M.N., Bene M.C., Cravoisy A., Levy B., Faure G.C., Bollaert P.E. Plasma level of a triggering receptor expressed on myeloid cells-1: its diagnostic accuracy in patients with suspected sepsis. Ann. Intern. Med. 2004, 141:9-15.
29. Gingras M.C., Lapillonne H., Margolin J.F. TREM-1 MDL-1, and DAP12 expression is associated with a mature stage of myeloid development. Mol. Immunol. 2002, 38:817-824.
30. Gomez-Pina V., Soares-Schanoski A., Rodriguez-Rojas A., Del Fresno C., Garcia F., Vallejo-Cremades M.T., Fernandez-Ruiz I., Arnalich F., Fuentes-Prior P., Lopez-Collazo E. Metalloproteinases shed TREM-1 ectodomain from lipopolysaccharide-stimulated human monocytes. J. Immunol. 2007, 179:4065-4073.
31. Guggenheim B., Gmur R., Galicia J.C., Stathopoulou P.G., Benakanakere M.R., Meier A., Thurnheer T., Kinane D.F. In vitro modeling of host-parasite interactions: the 'subgingival' biofilm challenge of primary human epithelial cells. BMC Microbiol. 2009, 9:280.
32. Guo Y., Nguyen K.A., Potempa J. Dichotomy of gingipains action as virulence factors: from cleaving substrates with the precision of a surgeon's knife to a meat chopper-like brutal degradation of proteins. Periodontology 2000 2010, 54:15-44.
33. Hajishengallis G. Porphyromonas gingivalis-host interactions: open war or intelligent guerilla tactics?. Microbes Infect. 2009, 11:637-645.
34. Hajishengallis G., Sharma A., Russell M.W., Genco R.J. Interactions of oral pathogens with toll-like receptors: possible role in atherosclerosis. Ann. Periodontol. 2002, 7:72-78.
35. Hajishengallis G., Wang M., Liang S., Shakhatreh M.A., James D., Nishiyama S., Yoshimura F., Demuth D.R. Subversion of innate immunity by periodontopathic bacteria via exploitation of complement receptor-3. Adv. Exp. Med. Biol. 2008, 632:203-219.
36. Hajishengallis G., Wang M., Liang S., Triantafilou M., Triantafilou K. Pathogen induction of CXCR4/TLR2 cross-talk impairs host defense function. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:13532-13537.
37. Hamedi M., Belibasakis G.N., Cruchley A.T., Rangarajan M., Curtis M.A., Bostanci N. Porphyromonas gingivalis culture supernatants differentially regulate interleukin-1beta and interleukin-18 in human monocytic cells. Cytokine 2009, 45:99-104.
38. Harokopakis E., Albzreh M.H., Martin M.H., Hajishengallis G. TLR2 transmodulates monocyte adhesion and transmigration via Rac1- and PI3K-mediated inside-out signaling in response to Porphyromonas gingivalis fimbriae. J. Immunol. 2006, 176:7645-7656.
39. How C.K., Hou S.K., Shih H.C., Yen D.H., Huang C.I., Lee C.H., Tang G.J. Usefulness of triggering receptor expressed on myeloid cells-1 in differentiating between typical and atypical community-acquired pneumonia. Am. J. Emerg. Med. 2011.
40. Ingersoll M.A., Spanbroek R., Lottaz C., Gautier E.L., Frankenberger M., Hoffmann R., Lang R., Haniffa M., Collin M., Tacke F., Habenicht A.J., Ziegler-Heitbrock L., Randolph G.J. Comparison of gene expression profiles between human and mouse monocyte subsets. Blood 2010, 115:e10-e19.
41. Klesney-Tait J., Colonna M. Uncovering the TREM-1-TLR connection. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007, 293:L1374-L1376.
42. Klesney-Tait J., Turnbull I.R., Colonna M. The TREM receptor family and signal integration. Nat. Immunol. 2006, 7:1266-1273.
43. Klinke T., Guggenheim B., Klimm W., Thurnheer T. Dental caries in rats associated with Candida albicans. Caries Res. 2011, 45:100-106.
44. Knapp S., Gibot S., de Vos A., Versteeg H.H., Colonna M., van der Poll T. Cutting edge: expression patterns of surface and soluble triggering receptor expressed on myeloid cells-1 in human endotoxemia. J. Immunol. 2004, 173:7131-7134.
45. Kusanovic J.P., Romero R., Chaiworapongsa T., Mittal P., Mazaki-Tovi S., Vaisbuch E., Erez O., Gotsch F., Than N.G., Edwin S.S., Pacora P., Jodicke C., Yeo L., Hassan S.S. Amniotic fluid sTREM-1 in normal pregnancy, spontaneous parturition at term and preterm, and intra-amniotic infection/inflammation. J. Matern. Fetal Neonatal Med. 2011, 23:34-47.
46. Liang S., Domon H., Hosur K.B., Wang M., Hajishengallis G. Age-related alterations in innate immune receptor expression and ability of macrophages to respond to pathogen challenge in vitro. Mech. Ageing Dev. 2009, 130:538-546.
47. Liao F., Li Z., Wang Y., Shi B., Gong Z., Cheng X. Porphyromonas gingivalis may play an important role in the pathogenesis of periodontitis-associated rheumatoid arthritis. Med. Hypotheses 2009, 72:732-735.
48. Lin D., Smith M.A., Champagne C., Elter J., Beck J., Offenbacher S. Porphyromonas gingivalis infection during pregnancy increases maternal tumor necrosis factor alpha, suppresses maternal interleukin-10, and enhances fetal growth restriction and resorption in mice. Infect. Immun. 2003, 71:5156-5162.
49. Maekawa T., Takahashi N., Tabeta K., Aoki Y., Miyashita H., Miyauchi S., Miyazawa H., Nakajima T., Yamazaki K. Chronic oral infection with Porphyromonas gingivalis accelerates atheroma formation by shifting the lipid profile. PLoS One 2011, 6:e20240.
50. Murakami Y., Kohsaka H., Kitasato H., Akahoshi T. Lipopolysaccharide-induced up-regulation of triggering receptor expressed on myeloid cells-1 expression on macrophages is regulated by endogenous prostaglandin E2. J. Immunol. 2007, 178:1144-1150.
51. Netea M.G., Azam T., Ferwerda G., Girardin S.E., Kim S.H., Dinarello C.A. Triggering receptor expressed on myeloid cells-1 (TREM-1) amplifies the signals induced by the NACHT-LRR (NLR) pattern recognition receptors. J. Leukoc. Biol. 2006, 80:1454-1461.
52. Ornatowska M., Azim A.C., Wang X., Christman J.W., Xiao L., Joo M., Sadikot R.T. Functional genomics of silencing TREM-1 on TLR4 signaling in macrophages. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007, 293:L1377-L1384.
53. Pathirana R.D., O'Brien-Simpson N.M., Reynolds E.C. Host immune responses to Porphyromonas gingivalis antigens. Periodontology 2000 2010, 52:218-237.
54. Pussinen P.J., Mattila K. Periodontal infections and atherosclerosis: mere associations?. Curr. Opin. Lipidol. 2004, 15:583-588.
55. Ramanathan B., Minton J.E., Ross C.R., Blecha F. Cloning of porcine triggering receptor expressed on myeloid cells-1 (TREM-1) and its induction by lipopolysaccharide, peptidoglycan, and Salmonella enterica serovar Typhimurium infection. Dev. Comp. Immunol. 2005, 29:1-7.
56. Richeldi L., Mariani M., Losi M., Maselli F., Corbetta L., Buonsanti C., Colonna M., Sinigaglia F., Panina-Bordignon P., Fabbri L.M. Triggering receptor expressed on myeloid cells: role in the diagnosis of lung infections. Eur. Respir. J. 2004, 24:247-250.
57. Salvi G.E., Yalda B., Collins J.G., Jones B.H., Smith F.W., Arnold R.R., Offenbacher S. Inflammatory mediator response as a potential risk marker for periodontal diseases in insulin-dependent diabetes mellitus patients. J. Periodontol. 1997, 68:127-135.
58. Schenk M., Bouchon A., Birrer S., Colonna M., Mueller C. Macrophages expressing triggering receptor expressed on myeloid cells-1 are underrepresented in the human intestine. J. Immunol. 2005, 174:517-524.
59. Schenk M., Bouchon A., Seibold F., Mueller C. TREM-1-expressing intestinal macrophages crucially amplify chronic inflammation in experimental colitis and inflammatory bowel diseases. J. Clin. Invest. 2007, 117:3097-3106.
60. Schmausser B., Endrich S., Beier D., Moran A.P., Burek C.J., Rosenwald A., Rieckmann P., Muller-Hermelink H.K., Eck M. Triggering receptor expressed on myeloid cells-1 (TREM-1) expression on gastric epithelium: implication for a role of TREM-1 in Helicobacter pylori infection. Clin. Exp. Immunol. 2008, 152:88-94.
61. Socransky S.S., Smith C., Haffajee A.D. Subgingival microbial profiles in refractory periodontal disease. J. Clin. Periodontol. 2002, 29:260-268.
62. Tomasello E., Vivier E. KARAP/DAP12/TYROBP: three names and a multiplicity of biological functions. Eur. J. Immunol. 2005, 35:1670-1677.
63. Turnbull I.R., McDunn J.E., Takai T., Townsend R.R., Cobb J.P., Colonna M. DAP12 (KARAP) amplifies inflammation and increases mortality from endotoxemia and septic peritonitis. J. Exp. Med. 2005, 202:363-369.
64. Wang M., Krauss J.L., Domon H., Hosur K.B., Liang S., Magotti P., Triantafilou M., Triantafilou K., Lambris J.D., Hajishengallis G. Microbial hijacking of complement-toll-like receptor crosstalk. Sci. Signal. 2010, 3:ra11.
65. Wong-Baeza I., Gonzalez-Roldan N., Ferat-Osorio E., Esquivel-Callejas N., Aduna-Vicente R., Arriaga-Pizano L., Astudillo-de la Vega H., Villasis-Keever M.A., Torres-Gonzalez R., Estrada-Garcia I., Lopez-Macias C., Isibasi A. Triggering receptor expressed on myeloid cells (TREM-1) is regulated post-transcriptionally and its ligand is present in the sera of some septic patients. Clin. Exp. Immunol. 2006, 145:448-455.
66. Ximenez-Fyvie L.A., Haffajee A.D., Socransky S.S. Microbial composition of supra- and subgingival plaque in subjects with adult periodontitis. J. Clin. Periodontol. 2000, 27:722-732.
67. Yamazaki K., Ueki-Maruayama K., Honda T., Nakajima T., Seymour G.J. Effect of periodontal treatment on the serum antibody levels to heat shock proteins. Clin. Exp. Immunol. 2004, 135:478-482.
68. Zeng H., Ornatowska M., Joo M.S., Sadikot R.T. TREM-1 expression in macrophages is regulated at transcriptional level by NF-kappaB and PU.1. Eur. J. Immunol. 2007, 37:2300-2308.
69. Zijnge V., van Leeuwen M.B., Degener J.E., Abbas F., Thurnheer T., Gmur R., Harmsen H.J. Oral biofilm architecture on natural teeth. PLoS One 2010, 5:e9321.