DNA from Porphyromonas gingivalis and Tannerella forsythia induce cytokine production in human monocytic cell lines

Molecular Oral Microbiology

Volumn 25, Issue 2, 2010, Pages 123-135

  Sahingur, S E ^a   Xia, X J ^a   Alamgir, S ^a   Honma, K ^b   Sharma, A ^b   Schenkein, H A ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

Cytokines; P. gingivalis; Periodontitis; T. forsythia; TLR9

Indexed keywords

ALKALINE PHOSPHATASE; BACTERIAL DNA; CHLOROQUINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; LEUKEMIA CELL LINE; MOLECULAR RECOGNITION; MONOCYTE; NONHUMAN; POLYMERASE CHAIN REACTION; PORPHYROMONAS GINGIVALIS; SIGNAL TRANSDUCTION; TANNERELLA FORSYTHENSIS;

BACTEROIDES; CELL LINE, TUMOR; CYTOKINES; DNA, BACTERIAL; GENE EXPRESSION PROFILING; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; INTERLEUKIN-6; KIDNEY; MONOCYTES; NF-KAPPA B; PORPHYROMONAS GINGIVALIS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 9; TRANSFECTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77949395206     PISSN: 20411006     EISSN: 20411014     Source Type: Journal    
DOI: 10.1111/j.2041-1014.2009.00551.x     Document Type: Article

References (71)

1. Abou Fakher, F.H., Rachinel, N., Klimczak, M., Louis, J. and Doyen, N. (2009) TLR9-dependent activation of dendritic cells by DNA from Leishmania major favors Th1 cell development and the resolution of lesions. J Immunol 182: 1386-1396.
2. Akira, S. (2006) TLR signaling. Curr Top Microbiol Immunol 311: 1-16.
3. Akira, S., Uematsu, S. and Takeuchi, O. (2006) Pathogen recognition and innate immunity. Cell 124: 783-801.
4. Albiger, B., Dahlberg, S., Sandgren, A. et al. (2007) Tolllike receptor 9 acts at an early stage in host defence against pneumococcal infection. Cell Microbiol 9: 633-644.
5. Bauer, S., Kirschning, C.J., Hacker, H. et al. (2001) Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc Natl Acad Sci U S A 98: 9237-9242.
6. Beklen, A., Hukkanen, M., Richardson, R. and Konttinen, Y.T. (2008) Immunohistochemical localization of Tolllike receptors 1-10 in periodontitis. Oral Microbiol Immunol 23: 425-431.
7. Burckstummer, T., Baumann, C., Bluml, S. et al. (2009) An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat Immunol 10: 266-272.
8. Cochran, D.L. (2008) Inflammation and bone loss in periodontal disease. J Periodontol 79: 1569-1576.
9. Dalpke, A., Zimmermann, S. and Heeg, K. (2002) Immunopharmacology of CpG DNA. Biol Chem 383: 1491-1500.
10. Dalpke, A., Frank, J., Peter, M. and Heeg, K. (2006) Activation of toll-like receptor 9 by DNA from different bacterial species. Infect Immun 74: 940-946.
11. El Kebir, D., Jozsef, L., Pan, W., Wang, L. and Filep, J.G. (2009) Bacterial DNA activates endothelial cells and promotes neutrophil adherence through TLR9 signaling. J Immunol 182: 4386-4394.
12. Erridge, C., Burdess, A., Jackson, A.J. et al. (2008) Vascular cell responsiveness to Toll-like receptor ligands in carotid atheroma. Eur J Clin Invest 38: 713-720.
13. Fernandes-Alnemri, T., Yu, J.W., Datta, P., Wu, J. and Alnemri, E.S. (2009) AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458: 509-513.
14. Fredheim, E.G., Klingenberg, C., Rohde, H. et al. (2009) Biofilm formation by Staphylococcus haemolyticus. J Clin Microbiol 47: 1172-1180.
15. Fuxman Bass, J.I., Alvarez, M.E., Gabelloni, M.L. et al. (2008a) GM-CSF enhances a CpG-independent pathway of neutrophil activation triggered by bacterial DNA. Mol Immunol 46: 37-44.
16. Fuxman Bass, J.I., Gabelloni, M.L., Alvarez, M.E. et al. (2008b) Characterization of bacterial DNA binding to human neutrophil surface. Lab Invest 88: 926-937.
17. Gibson, F.C. III, Ukai, T. and Genco, C.A. (2008) Engagement of specific innate immune signaling pathways during Porphyromonas gingivalis induced chronic inflammation and atherosclerosis. Front Biosci 13: 2041-2059.
18. Haffajee, A.D. and Socransky, S.S. (1994) Microbial etiological agents of destructive periodontal diseases. Periodontol 2000 5: 78-111.
19. Hajishengallis, G., Wang, M., Bagby, G.J. and Nelson, S. (2008a) Importance of TLR2 in early innate immune response to acute pulmonary infection with Porphyromonas gingivalis in mice. J Immunol 181: 4141-4149.
20. Hajishengallis, G., Wang, M., Liang, S., Triantafilou, M. and Triantafilou, K. (2008b) Pathogen induction of CXCR4/TLR2 cross-talk impairs host defense function. Proc Natl Acad Sci U S A 105: 13532-13537.
21. Hajishengallis, G., Wang, M. and Liang, S. (2009) Induction of distinct TLR2-mediated proinflammatory and proadhesive signaling pathways in response to Porphyromonas gingivalis fimbriae. J Immunol 182: 6690-6696.
22. Hall, J.A., Bouladoux, N., Sun, C.M. et al. (2008) Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses. Immunity 29: 637-649.
23. Haraszthy, V.I., Zambon, J.J., Trevisan, M., Zeid, M. and Genco, R.J. (2000) Identification of periodontal pathogens in atheromatous plaques. J Periodontol 71: 1554-1560.
24. Heeg, K., Dalpke, A., Peter, M. and Zimmermann, S. (2008) Structural requirements for uptake and recognition of CpG oligonucleotides. Int J Med Microbiol 298: 33-38.
25. Hornung, V., Ablasser, A., Charrel-Dennis, M. et al. (2009) AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458: 514-518.
26. Huang, X., Barrett, R.P., McClellan, S.A. and Hazlett, L.D. Silencing Toll-like receptor-9 in Pseudomonas aeruginosa keratitis (2005) Invest Ophthalmol Vis Sci 46: 4209-4216.
27. Imai, K., Takeshita, A. and Hanazawa, S. (1999) TGF-beta inhibits lipopolysaccharide-stimulated activity of c-Jun N-terminal kinase in mouse macrophages. FEBS Lett 456: 375-378.
28. Janeway, C.A. Jr. and Medzhitov, R. (2002) Innate immune recognition. Annu Rev Immunol 20: 197-216.
29. Jurk, M., Kritzler, A., Debelak, H., Vollmer, J., Krieg, A.M. and Uhlmann, E. (2006) Structure-activity relationship studies on the immune stimulatory effects of base-modified CpG toll-like receptor 9 agonists. ChemMedChem 1: 1007-1014.
30. Kajita, K., Honda, T., Amanuma, R. et al. (2007) Quantitative messenger RNA expression of Toll-like receptors and interferon-alpha1 in gingivitis and periodontitis. Oral Microbiol Immunol 22: 398-402.
31. Klaschik, S., Tross, D. and Klinman, D.M. (2009) Inductive and suppressive networks regulate TLR9-dependent gene expression in vivo. J Leukoc Biol 85: 788-795.
32. Komatsuda, A., Wakui, H., Iwamoto, K. et al. (2008) Upregulated expression of Toll-like receptors mRNAs in peripheral blood mononuclear cells from patients with systemic lupus erythematosus. Clin Exp Immunol 152: 482-487.
33. Koutouzis, T., Haber, D., Shaddox, L., Aukhil, I. and Wallet, S.M. (2009) Autoreactivity of serum immunoglobulin to periodontal tissue components: a pilot study. J Periodontol 80: 625-633.
34. Krieg, A.M. (2006) Therapeutic potential of Toll-like receptor 9 activation. Nat Rev Drug Discov 5: 471-484.
35. Krieg, A.M. and Vollmer, J. (2007) Toll-like receptors 7, 8, and 9: linking innate immunity to autoimmunity. Immunol Rev 220: 251-269.
36. Kumagai, Y., Takeuchi, O. and Akira, S. (2008) TLR9 as a key receptor for the recognition of DNA. Adv Drug Deliv Rev 60: 795-804.
37. Liao, F., Li, Z., Wang, Y., Shi, B., Gong, Z. and Cheng, X. (2009) Porphyromonas gingivalis may play an important role in the pathogenesis of periodontitis-associated rheumatoid arthritis. Med Hypotheses 72: 732-735.
38. Loos, T., Dekeyzer, L., Struyf, S. et al. (2006) TLR ligands and cytokines induce CXCR3 ligands in endothelial cells: enhanced CXCL9 in autoimmune arthritis. Lab Invest 86: 902-916.
39. Mahanonda, R. and Pichyangkul, S. (2007) Toll-like receptors and their role in periodontal health and disease. Periodontol 2000 43: 41-55.
40. Mealey, B.L. and Ocampo, G.L. (2007) Diabetes mellitus and periodontal disease. Periodontol 2000 44: 127-153.
41. Michalowicz, B.S. and Durand, R. (2007) Maternal periodontal disease and spontaneous preterm birth. Periodontol 2000 44: 103-112.
42. Mogensen, T.H., Paludan, S.R., Kilian, M. and Ostergaard, L. (2006) Live Streptococcus pneumoniae, Haemophilus influenzae, and Neisseria meningitidis activate the inflammatory response through Toll-like receptors 2, 4, and 9 in species-specific patterns. J Leukoc Biol 80: 267-277.
43. Muruve, D.A., Petrilli, V., Zaiss, A.K. et al. (2008) The inflammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature 452: 103-107.
44. Nakano, S., Morimoto, S., Suzuki, J., Nozawa, K., Amaro, H., Tokano, Y. and Takazaki, Y. (2008) Role of pathogenic auto-antibody production by Toll-like receptor 9 of B cells in active systemic lupus erythematosus. Rheumatology (Oxford) 47: 145-149.
45. Nonnenmacher, C., Dalpke, A., Zimmermann, S., Flores-De-Jacoby, L., Mutters, R. and Heeg, K. (2003) DNA from periodontopathogenic bacteria is immunostimulatory for mouse and human immune cells. Infect Immun 71: 850-856.
46. Onishi, S., Honma, K., Liang, S. et al. (2008) Toll-like receptor 2-mediated interleukin-8 expression in gingival epithelial cells by the Tannerella forsythia leucine-rich repeat protein BspA. Infect Immun 76: 198-205.
47. de Pablo, P., Chapple, I.L., Buckley, C.D. and Dietrich, T. (2009) Periodontitis in systemic rheumatic diseases. Nat Rev Rheumatol 5: 218-224.
48. Paquette, D.W., Brodala, N. and Nichols, T.C. (2007) Cardiovascular disease, inflammation, and periodontal infection. Periodontol 2000 44: 113-126.
49. Petersen, F.C., Tao, L. and Scheie, A.A. (2005) DNA binding-uptake system: a link between cell-to-cell communication and biofilm formation. J Bacteriol 187: 4392-4400.
50. Plitas, G., Burt, B.M., Nguyen, H.M., Bamboat, Z.M. and DeMatteo, R.P. (2008) Toll-like receptor 9 inhibition reduces mortality in polymicrobial sepsis. J Exp Med 205: 1277-1283.
51. Raghavendran, K., Mylotte, J.M. and Scannapieco, F.A. (2007) Nursing home-associated pneumonia, hospitalacquired pneumonia and ventilator-associated pneumonia: the contribution of dental biofilms and periodontal inflammation. Periodontol 2000 44: 164-177.
52. Ramaprakash, H., Ito, T., Standiford, T.J., Kunkel, S.L. and Hogaboam, C.M. (2009) Toll-like receptor 9 modulates immune responses to Aspergillus fumigatus conidia in immunodeficient and allergic mice. Infect Immun 77: 108-119.
53. Roberts, T.L., Idris, A., Dunn, J.A. et al. (2009) HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323: 1057-1060.
54. Rudnicka, W., Burakowski, T., Warnawin, E. et al. (2009) Functional TLR9 modulates bone marrow B cells from rheumatoid arthritis patients. Eur J Immunol 39: 1211-1220.
55. Sacre, S.M., Lo, A., Gregory, B. et al. (2008) Inhibitors of TLR8 reduce TNF production from human rheumatoid synovial membrane cultures. J Immunol 181: 8002-8009.
56. Sahingur, S.E. and Cohen, R.E. (2004) Analysis of host responses and risk for disease progression. Periodontol 2000 34: 57-83.
57. Scardina, G.A. and Messina, P. (2007) Microvascular periodontal alterations: a possible relationship between periodontitis and rheumatoid arthritis. Clin Hemorheol Microcirc 37: 229-235.
58. Schenkein, H.A. (2006) Host responses in maintaining periodontal health and determining periodontal disease. Periodontol 2000 40: 77-93.
59. Schenkein, H.A., Best, A.M., Brooks, C.N. et al. (2007) Anti-cardiolipin and increased serum adhesion molecule levels in patients with aggressive periodontitis. J Periodontol 78: 459-466.
60. Sjolinder, H., Mogensen, T.H., Kilian, M., Jonsson, A.B. and Paludan, S.R. (2008) Important role for Toll-like receptor 9 in host defense against meningococcal sepsis. Infect Immun 76: 5421-5428.
61. Takaoka, A., Wang, Z., Choi, M.K. et al. (2007) DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448: 501-505.
62. Takeshita, A., Imai, K. and Hanazawa, S. (1999) CpG motifs in Porphyromonas gingivalis DNA stimulate interleukin-6 expression in human gingival fibroblasts. Infect Immun 67: 4340-4345.
63. Talati, A.J., Kim, H.J., Kim, Y.I., Yi, A.K. and English B.K. (2008) Role of bacterial DNA in macrophage activation by group B streptococci. Microbes Infect 10: 1106-1113.
64. Taubman, M.A., Valverde, P., Han, X. and Kawai, T. (2005) Immune response: the key to bone resorption in periodontal disease. J Periodontol 76: 2033-2041.
65. Taubman, M.A., Han, X., Larosa, K.B., Socransky, S.S. and Smith, D.J. (2007) Periodontal bacterial DNA suppresses the immune response to mutans streptococcal glucosyltransferase. Infect Immun 75: 4088-4096.
66. Tetz, G.V., Artemenko, N.K. and Tetz, V.V. (2009) Effect of DNase and antibiotics on biofilm characteristics. Antimicrob Agents Chemother 53: 1204-1209.
67. Uehara, A., Imamura, V., Potempa, J., Travis, J. and Takada, H. (2008) Gingipains from Porphyromonas gingivalis synergistically induce the production of proinflammatory cytokines through protease-activated receptors with Toll-like receptor and NOD1/2 ligands in human monocytic cells. Cell Microbiol 10: 1181-1189.
68. Vilain, S., Pretorius, J.M., Theron, J. and Brozel, V.S. (2009) DNA as an adhesin: Bacillus cereus requires extracellular DNA to form biofilms. Appl Environ Microbiol 75: 2861-2868.
69. Wu, O., Chen, G.P., Chen, H. et al. (2009) The expressions of Toll-like receptor 9 and T-bet in circulating B and T cells in newly diagnosed, untreated systemic lupus erythematosus and correlations with disease activity and laboratory data in a Chinese population. Immunobiology 214: 392-402.
70. Zorro, S., Arias, M., Riano, F. et al. (2009) Response to ODN-CpG by B Cells from patients with systemic lupus erythematosus correlates with disease activity. Lupus 18: 718-726.
71. Zucchini, N., Bessou, G., Traub, S. et al. (2008) Cutting edge: overlapping functions of TLR7 and TLR9 for innate defense against a herpesvirus infection. J Immunol 180: 5799-5803.