Porphyromonas gingivalis lipopolysaccharide regulates interleukin (IL)-17 and IL-23 expression via SIRT1 modulation in human periodontal ligament cells

Cytokine

Volumn 60, Issue 1, 2012, Pages 284-293

  Park, Yong Duk ^a   Kim, Young Suk ^a   Jung, Yu Mi ^a   Lee, Sang Im ^a   Lee, Young Man ^a   Bang, Jae Beum ^a   Kim, Eun Cheol ^a  

^a Kyung Hee University   (South Korea)

Author keywords

IL 17; IL 23; LPS; P. gingivalis; SIRT1

Indexed keywords

ALKALINE PHOSPHATASE; BACTERIUM LIPOPOLYSACCHARIDE; BONE SIALOPROTEIN; COLONY STIMULATING FACTOR 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 17; INTERLEUKIN 23; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; NEUTRALIZING ANTIBODY; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPONTIN; PHOSPHATIDYLINOSITOL 3 KINASE; SIRTINOL; SIRTUIN 1; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; GENE EXPRESSION; HUMAN; HUMAN CELL; NONHUMAN; PERIODONTAL LIGAMENT; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION;

ALKALINE PHOSPHATASE; ANTIBODIES, NEUTRALIZING; BENZAMIDES; BLOTTING, WESTERN; CELLS, CULTURED; ENZYME INHIBITORS; HUMANS; INTERLEUKIN-17; INTERLEUKIN-23; LIPOPOLYSACCHARIDES; MITOGEN-ACTIVATED PROTEIN KINASES; NAPHTHOLS; NF-KAPPA B; PERIODONTAL LIGAMENT; PHOSPHATIDYLINOSITOL 3-KINASES; PORPHYROMONAS GINGIVALIS; RANK LIGAND; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SIRTUIN 1; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

PORPHYROMONAS GINGIVALIS;

EID: 84865404292     PISSN: 10434666     EISSN: 10960023     Source Type: Journal    
DOI: 10.1016/j.cyto.2012.05.021     Document Type: Article

References (57)

1. Haffajee A.D., Socransky S.S. Microbial etiological agents of destructive periodontal diseases. Periodontol 2000, 1994(5):78-111.
2. Choi J.I., Nakagawa T., Yamada S., Takazoe I., Okuda K. Clinical, microbiological and immunological studies on recurrent periodontal disease. J Clin Periodontol 1990, 17:426-434.
3. Darveau R.P., Belton C.M., Reife R.A., Lamont R.J. Local chemokine paralysis, a novel pathogenic mechanism for Porphyromonas gingivalis. Infect Immun 1998, 66:1660-1665.
4. Sandros J., Karlsson C., Lappin D.F., Madianos P.N., Kinane D.F., Papapanou P.N. Cytokine responses of oral epithelial cells to Porphyromonas gingivalis infection. J Dent Res 2000, 79:1808-1814.
5. Agarwal S., Piesco N.P., Johns L.P., Riccelli A.E. Differential expression of IL-1 beta, TNF-alpha, IL-6, and IL-8 in human monocytes in response to lipopolysaccharides from different microbes. J Dent Res 1995, 74:1057-1065.
6. Baqui A.A., Meiller T.F., Falkler W.A. Enhanced interleukin-8 production in THP-1 human monocytic cells by lipopolysaccharide from oral microorganisms and granulocyte-macrophage colony-stimulating factor. Oral Microbiol Immun 1999, 14:275-280.
7. Yamaji Y., Kubota T., Sasaguri K., Sato S., Suzuki Y., Kumada H., et al. Inflammatory cytokine gene expression in human periodontal ligament fibroblasts stimulated with bacterial lipopolysaccharides. Infect Immun 1995, 63:3576-3581.
8. Chang Y.C., Yang S.F., Lai C.C., Liu J.Y., Hsieh Y.S. Regulation of matrix metalloproteinase production by cytokines, pharmacological agents and periodontal ligament fibroblast cultures. J Periodont Res 2002, 37:196-203.
9. Lee H.J., Cho J.W., Kim S.C., Kang K.H., Lee S.K., Pi S.H., et al. Roles of p38 and ERK MAP kinases in IL-8 expression in TNF-a- and dexamethasone-stimulated human periodontal ligament cells. Cytokine 2006, 35:67-76.
10. Lee S.K., Pi S.H., Kim S.H., Min K.S., Lee H.J., Chang H.S., et al. Substance p regulates macrophage inflammatory protein 3/CCL20 with heme oxygenase-1 in human periodontal ligament cells. Clin Exp Immunol 2007, 150:566-575.
11. Lee H.J., Pi S.H., Kim Y., Kim H.S., Kim S.J., Kim Y.S., et al. Effects of nicotine on antioxidant defense enzymes and RANKL expression in human periodontal ligament cells. J Periodontol 2009, 80:1281-1288.
12. Jeong G.S., Lee S.H., Jeong S.N., Kim Y.C., Kim E.C. Anti-inflammatory effects of apigenin on nicotine- and lipopolysaccharide-stimulated human periodontal ligament cells via heme oxygenase-1. Int Immunopharmacol 2009, 9:1374-1380.
13. Kim Y.S., Pi S.H., Lee Y.M., Lee S.I., Kim E.C. The anti-inflammatory role of heme oxygenase-1 in lipopolysaccharide and cytokine-stimulated inducible nitric oxide synthase and nitric oxide production in human periodontal ligament cells. J Periodontol 2009, 80:2045-2055.
14. Lee H.J., Jeong G.S., Pi S.H., Lee S.I., Bae W.J., Kim S.J., et al. Heme oxygenase-1 protects human periodontal ligament cells against substance P-induced RANKL expression. J Periodontal Res 2010, 45:367-374.
15. Aarvak T., Chabaud M., Miossec P., Natvig J.B. IL-17 is produced by some proinflammatory Th1/Th0 cells but not by Th2 cells. J Immunol 1999, 162:1246-1251.
16. Ohyama H., Kato-Kogoe N., Kuhara A., Nishimura F., Nakasho K., Yamanegi K., et al. The involvement of IL-23 and the Th17 pathway in periodontitis. J Dent Res 2009, 88:633-638.
17. Weaver C.T., Hatton R.D., Mangan P.R., Harrington L.E. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol 2007, 25:821-852.
18. Kim K.W., Cho M.L., Park M.K., Yoon C.H., Park S.H., Lee S.H., et al. Increased interleukin-17 production via a phosphoinositide 3-kinase/Akt and nuclear factor kappaB-dependent pathway in patients with rheumatoid arthritis. Arthritis Res Ther 2005, 7:R139-R148.
19. Van Bezooijen R., Farih-Sips H.C., Papapoulos S.E., Löwik C.W. Interleukin-17: a new bone acting cytokine in vitro. J Bone Miner Res 1999, 9:1513-1521.
20. Chen L., Wei X.Q., Evans B., Jiang W., Aeschlimann D. IL-23 promotes osteoclast formation by up-regulation of receptor activator of NF-kappaB (RANK) expression in myeloid precursor cells. Eur J Immunol 2008, 38:2845-2854.
21. Beklen A., Ainola M., Hukkanen M., Gürgan C., Sorsa T., Konttinen Y.T. MMPs, IL-1, and TNF are regulated by IL-17 in periodontitis. J Dent Res 2007, 86:347-351.
22. Vernal R., Dutzan N., Chaparro A., Puente J., Antonieta Valenzuela M., Gamonal J. Levels of interleukin-17 in gingival crevicular fluid and in supernatants of cellular cultures of gingival tissue from persons with chronic periodontitis. J Clin Periodontol 2005, 32:383-389.
23. Buduneli N., Buduneli E., Kütükçüler N. Interleukin-17, RANKL, and osteoprotegerin levels in gingival crevicular fluid from smoking and non-smoking patients with chronic periodontitis during initial periodontal treatment. J Periodontol 2009, 80:1274-1280.
24. Yu J.J., Ruddy M.J., Wong G.C., Sfintescu C., Baker P.J., Smith J.B., et al. An essential role for IL-17 in preventing pathogen-initiated bone destruction: recruitment of neutrophils to inflamed bone requires IL-17 receptor-dependent signals. Blood 2007, 109:3794-3802.
25. Oppmann B., Lesley R., Blom B., Timans J.C., Xu Y., Hunte B., et al. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 2000, 13:715-725.
26. Langrish C.L., Chen Y., Blumenschein W.M., Mattson J., Basham B., Sedgwick J.D., et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 2005, 201:233-240.
27. Hölttä V., Klemetti P., Sipponen T., Westerholm-Ormio M., Kociubinski G., Salo H., et al. IL-23/IL-17 immunity as a hallmark of Crohn's disease. Inflamm Bowel Dis 2008, 14:1175-1184.
28. Chi W., Zhu X., Yang P., Liu X., Lin X., Zhou H., et al. Upregulated IL-23 and IL-17 in Behçet Patients with active uveitis. Invest Ophthalmol Vis Sci 2008, 49:3058-3064.
29. Zhang Z., Kyttaris V.C., Tsokos G.C. The role of IL-23/IL-17 axis in lupus nephritis. J Immunol 2009, 183:3160-3169.
30. Anastasiou D., Krek W. SIRT1 linking adaptive cellular responses to aging-associated changes in organismal physiology. Physiology 2006, 21:404-410.
31. Lee Y.M., Shin S.I., Shin K.S., Lee Y.R., Park B.H., Kim E.C. The role of sirtuin1 in osteoblastic differentiation in human periodontal ligament cells. J Periodontal Res 2011, 46:712-721.
32. Lee S.I., Park K.H., Kim S.J., Kang Y.G., Lee Y.M., Kim E.C. Mechanical stress-activated immune response genes via Sirtuin 1 expression in human periodontal ligament cells. Clin Exp Immunol 2012, 168:113-124.
33. Lee S.I., Min K.S., Bae W.J., Lee Y.M., Lee S.Y., Lee E.S., et al. Role of SIRT1 in heat stress- and lipopolysaccharide-induced immune and defense gene expression in human dental pulp cells. J Endod 2011, 37:1525-1530.
34. Kim Y.S., Lee Y.M., Park J.S., Lee S.K., Kim E.C. SIRT1 modulates high-mobility group box 1-induced osteoclastogenic cytokines in human periodontal ligament cells. J Cell Biochem 2010, 111:1310-1320.
35. Yeung F., Hoberg J.E., Ramsey C.S., Keller M.D., Jones D.R., Frye R.A., et al. Modulation of NF-κB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J 2004, 23:2369-2380.
36. Kitagawa M., Kudo Y., Iizuka S., Ogawa I., Abiko Y., Miyauchi M., et al. Effect of F-spondin on cementoblastic differentiation of human periodontal ligament cells. Biochem Biophys Res Commun 2006, 349:1050-1056.
37. Mahanonda R., Jitprasertwong P., Sa-Ard-Iam N., Rerkyen P., Charatkulangkun O., Jansisyanont P., et al. Effects of IL-17 on human gingival fibroblasts. J Dent Res 2008, 87:267-272.
38. Kotake S., Udagawa N., Takahashi N., Matsuzaki K., Itoh K., Ishiyama S., et al. IL-17 in synovial fl uids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 1999, 103:1345-1352.
39. Aggarwal S., Ghilardi N., Xie M.H., de Sauvage F.J., Gurney A.L. Interleukin- 23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J Biol Chem 2003, 278:1910-1914.
40. Kamiya S., Nakamura C., Fukawa T., Ono K., Ohwaki T., Yoshimoto T., et al. Effects of IL-23 and IL-27 on osteoblasts and steoclasts: inhibitory effects on osteoclast differentiation. J Bone Miner Metab 2007, 25:277-285.
41. Phipps R.P., Borrello M.A., Blieden T.M. Fibroblast heterogeneity in the periodontium and other tissues. J Periodontal Res 1997, 32:159-165.
42. Fujii S., Maeda H., Wada N., Kano Y., Akamine A. Establishing and characterizing human periodontal ligament fibroblasts immortalized by SV40T-antigen and hTERT gene transfer. Cell Tissue Res 2006, 324:117-125.
43. Hari A., Flach T., Shi Y., Mydlarski R. Toll-like receptors: role in dermatological disease. Mediators Inflamm 2010, 2010:1-16.
44. Sun Y., Shu R., Li C.L., Zhang M.Z. Gram-negative periodontal bacteria induce the activation of Toll-like receptors 2 and 4, and cytokine production in human periodontal ligament cells. J Periodontol 2010, 81:1488-1496.
45. Jeong G.S., Lee D.S., Li B., Kim J.J., Kim E.C., Kim Y.C. Anti-inflammatory effects of lindenenyl acetate via heme oxygenase-1 and AMPK in human periodontal ligament cells. Eur J Pharmacol 2011, 670:295-303.
46. Akira S., Takeda K. Toll-like receptor signalling. Nat Rev Immunol 2004, 4:499-511.
47. Underhill D.M., Ozinsky A. Toll-like receptors: key mediators of microbe detection. Curr Opin Immunol 2002, 14:103-110.
48. Tabeta K., Yamzaki K., Akashi S., Miyake K., Kumada H., Umemoto T., et al. Toll-like receptors confer responsiveness to lipopolysaccharide from Porphyromonas gingivalis in human gingival fibroblasts. Infect Immun 2000, 68:3731-3735.
49. Zhang D., Chen L., Li S., Gu Z., Yan J. Lipopolysaccharide (LPS) of Porphyromonas gingivalis induces IL-1beta, TNF-alpha and IL-6 production by THP-1 cells in a way different from that of Escherichia coli LPS. Innate Immun 2008, 14:99-107.
50. Lee J.H., Song M.Y., Song E.K., Kim E.K., Moon W.S., Han M.K., et al. Overexpression of SIRT1 protects pancreatic beta-cells against cytokine toxicity by suppressing the nuclear factor-kappaB signaling pathway. Diabetes 2009, 58:344-351.
51. Rajendrasozhan S., Yang S.R., Kinnula V.L., Rahman I. SIRT1, an antiinflammatory and antiaging protein, is decreased in lungs of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2008, 177:861-870.
52. Kim S.R., Lee K.S., Park S.J., Min K.H., Choe Y.H., Moon H. Et al. Involvement of sirtuin 1 in airway inflammation and hyperresponsiveness of allergic airway disease. J Allergy Clin Immunol 2010, 125:449-460.
53. Liu F.C., Day Y.J., Liou J.T., Lau Y.T., Yu H.P. Sirtinol attenuates hepatic injury and pro-inflammatory cytokine production following trauma-hemorrhage in male Sprague-Dawley rats. Acta Anaesthesiol Scand 2008, 52:635-640.
54. Orecchia A., Scarponi C., Di Felice F., Cesarini E., Avitabile S., Mai A., et al. Sirtinol treatment reduces inflammation in human dermal microvascular endothelial cells. PLoS One 2011, 6:e24307.
55. Pi S.H., Lee S.K., Hwang Y.S., Choi M.G., Lee S.K., Kim E.C. Differential expression of periodontal ligament-specific markers and osteogenic differentiation in HPV16-immortalized human gingival fibroblasts and periodontal ligament cells. J Periodontal Res 2007, 42:104-113.
56. Reddi D., Bostanci N., Hashim A., Aduse-Opoku J., Curtis M.A., Hughes F.J., et al. Porphyromonas gingivalis regulates the RANKL-OPG system in bone marrow stromal cells. Microbes Infect 2008, 10:1459-1468.
57. Loomer P.M., Sigusch B., Sukhu B., Ellen R.P., Tenenbaum H.C. Direct effects of metabolic products and sonicated extracts of Porphyromonas gingivalis 2561 on osteogenesis in vitro. Infect Immun 1994, 62:1289-1297.