Anti-inflammatory effects of apigenin on nicotine- and lipopolysaccharide-stimulated human periodontal ligament cells via heme oxygenase-1

International Immunopharmacology

Volumn 9, Issue 12, 2009, Pages 1374-1380

  Jeong, Gil Saeng ^a   Lee, Seoung Hoon ^a   Jeong, Seong Nyum ^a   Kim, Youn Chul ^a   Kim, Eun Cheol ^a  

^a Wonkwang University   (South Korea)

Author keywords

Anti inflammatory; Apigenin; Human periodontal ligament cells; LPS; Nicotine

Indexed keywords

APIGENIN; CYCLOOXYGENASE 2; HEME OXYGENASE 1; HEMIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINE; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROSTAGLANDIN E2; PROTEIN KINASE C INHIBITOR; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; TUMOR NECROSIS FACTOR ALPHA;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL VIABILITY; CHEMICAL STRUCTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; PERIODONTAL LIGAMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; WESTERN BLOTTING;

ANTI-INFLAMMATORY AGENTS; APIGENIN; CELL LINE, TRANSFORMED; CYCLOOXYGENASE 2; CYTOKINES; DENTAL PLAQUE; DINOPROSTONE; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION; HEME OXYGENASE-1; HEMIN; HUMANS; LIPOPOLYSACCHARIDES; NICOTINE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PERIODONTAL DISEASES; PERIODONTAL LIGAMENT; PHOSPHORYLATION; SMOKING;

EID: 70349424713     PISSN: 15675769     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.intimp.2009.08.015     Document Type: Article

References (53)

1. Page R.C., and Schroeder H.E. Pathogenesis of inflammatory periodontal disease. A summary of current work. Lab Invest 34 (1976) 235-249
2. Yamaji Y., Kubota T., Sasaguri K., Sato S., Suzuki Y., and Kumada H. Inflammatory cytokine gene expression in human periodontal ligament fibroblasts treated with bacterial lipopolysaccharide. Infect Immun 63 (1995) 3576-3581
3. Garrison S.W., and Nichols F.C. LPS-elicited secretory responses in monocytes: altered release of PGE2 but not IL-1 beta in patients with adult periodontitis. J Periodontal Res 24 (1989) 88-95
4. Page R.C. The role of inflammatory mediators in the pathogenesis of periodontal disease. Journal of Periodontal Research 26 (1991) 230-242
5. Agarwal S., Baran C., Piesco N.P., Quintero J.C., Langkamp H.H., Johns L.P., et al. Synthesis of proinflammatory cytokines by human gingival fibroblasts in response to lipopolysaccharides and interleukin-1 beta. Journal of Periodontal Research 30 (1995) 382-389
6. McGuire J.R., McQuade M.J., Rossmann J.A., Garnick J.J., Sutherland D.E., Scheidt M.J., et al. Nicotine in saliva and gingival crevicular fluid of smokers with periodontal disease. J Periodontol 60 (1989) 176-181
7. Giannopoulou C., Geinoz A., and Cimason G. Effects of nicotine on periodontal ligament fibroblasts in vitro. J Clin Periodontol 26 (1999) 49-55
8. Chang Y.C., Lii C.K., Tai K.W., and Chou M.Y. Adverse effects of arecoline and nicotine on human periodontal ligament fibroblasts in vitro. J Clin Periodontol 28 (2001) 277-282
9. Chang Y.C., Huang F.M., Tai K.W., Yang L.C., and Chou M.Y. Mechanisms of cytotoxicity of nicotine in human periodontal ligament fibroblast cultures in vitro. J Periodontal Res 37 (2002) 279-285
10. Katono T., Kawato T., Tanabe N., Tanaka H., Suzuki N., Kitami S., et al. Effects of nicotine and lipopolysaccharide on the expression of matrix metalloproteinases, plasminogen activators, and their inhibitors in human osteoblasts. Arch Oral Biol 54 (2009) 146-155
11. Tanaka H., Tanabe N., Shoji M., Suzuki N., Katono T., Sato S., et al. Nicotine and lipopolysaccharide stimulate the formation of osteoclast-like cells by increasing macrophage colony-stimulating factor and prostaglandin E2 production by osteoblasts. Life Sci 78 (2006) 1733-1740
12. Shoji M., Tanabe N., Mitsui N., Suzuki N., Takeichi O., Katono T., et al. Lipopolysaccharide enhances the production of nicotine-induced prostaglandin E2 by an increase in cyclooxygenase-2 expression in osteoblasts. Acta Biochim Biophys Sin (Shanghai) 39 (2007) 163-172
13. Almasri A., Wisithphrom K., Windsor L.J., and Olson B. Nicotine and lipopolysaccharide affect cytokine expression from gingival fibroblasts. J Periodontol 78 (2007) 533-541
14. Wendell K.J., and Stein S.H. Regulation of cytokine production in human gingival fibroblasts following treatment with nicotine and lipopolysaccharide. J Periodontol 72 (2001) 1038-1044
15. Pi S.H., Jeong G.S., Oh H.W., Kim Y.S., Pae H.O., Chung H.T., et al. Heme oxygenase-1 mediates nicotine- and lipopolysaccharide-induced COX-2 and iNOS expression in human periodontal ligament cells. J Periodontal Res (2009) Electronic publication in ahead
16. Lekic P., and McCulloch C.A. Periodontal ligament cell population : the central role of fibroblasts in creating a unique tissue. Anat Rec 245 (1996) 327-341
17. Hou L.T., and Yaeger J.A. Cloning and characterization of human gingival and periodontal ligament fibroblasts. J Periodontol 64 (1993) 1209-1218
18. Ross J.A., and Kasum C.M. Dietary flavonoids: bioavailability, metabolic effects, and safety. Annu Rev Nutr 22 (2002) 19-34
19. Choi J.R., Lee C.M., Jung I.D., Lee J.S., Jeong Y.I., Chang J.H., et al. Apigenin protects ovalbumin-induced asthma through the regulation of GATA-3 gene. Int Immunopharmacol 9 (2009) 918-924
20. Yano S., Umeda D., Yamashita S., Yamada K., and Tachibana H. Dietary apigenin attenuates the development of atopic dermatitis-like skin lesions in NC/Nga mice. J Nutr Biochem (2008) Electronic publication in ahead
21. Conforti F., Rigano D., Menichini F., Loizzo M.R., and Senatore F. Protection against neurodegenerative diseases of Iris pseudopumila extracts and their constituents. Fitoterapia 80 (2008) 62-67
22. Rezai-Zadeh K., Ehrhart J., Bai Y., Sanberg P.R., Bickford P., Tan J., et al. Apigenin and luteolin modulate microglial activation via inhibition of STAT1-induced CD40 expression. J Neuroinflammation 25 (2008) 41
23. Xu L., Zhang L., Bertucci A.M., Pope R.M., and Datta S.K. Apigenin, a dietary flavonoid, sensitizes human T cells for activation-induced cell death by inhibiting PKB/Akt and NF-kappaB activation pathway. Immunol Lett 121 (2008) 74-83
24. Ha S.K., Lee P., Park J.A., Oh H.R., Lee S.Y., Park J.H., et al. Apigenin inhibits the production of NO and PGE2 in microglia and inhibits neuronal cell death in a middle cerebral artery occlusion-induced focal ischemia mice model. Neurochem Int 52 (2008) 878-886
25. Nicholas C., Batra S., Vargo M.A., Voss O.H., Gavrilin M.A., Wewers M.D., et al. Apigenin blocks lipopolysaccharide-induced lethality in vivo and proinflammatory cytokines expression by inactivating NF-kappaB through the suppression of p65 phosphorylation. J Immunol 179 (2007) 7121-7127
26. Maines M.D. The heme oxygenase system: a regulator of second messenger genes. Annu Rev Pharmacol Toxicol 37 (1997) 517-554
27. Min K.S., Hwang Y.H., Ju H.J., Chang H.S., Kang K.H., Pi S.H., et al. Heme oxygenase-1 mediates cytoprotection against nitric oxide-induced cytotoxicity via the cGMP pathway in human pulp cells. Oral Surg Oal Med Oral Pathol Oral Radol Endod 102 (2006) 803-808
28. Min K.S., Kwon Y.Y., Lee H.J., et al. Effects of proinflammatory cytokines on the expression of mineralization markers and heme oxygenase-1 in human pulp cells. J Endod 32 (2006) 39-43
29. Pi S.H., Kim S.C., Kim H.T., Lee H.J., Lee S.K., and Kim E.C. Defense mechanism of heme oxygenase-1 against cytotoxic and receptor activator of NF kappa-B ligand inducing effects of hydrogen peroxide in human periodontal ligament cells. J Periodontal Res 42 (2007) 331-339
30. Lee S.K., Pi S.H., Kim S.H., et al. Substance P regulates macrophage inflammatory protein 3α/CCL20 with heme oxygenase-1 in human periodontal ligament cells. Clin Exp Immunol 150 (2007) 567-575
31. Lee S.K., Min K.S., Kim Y., et al. Mechanical stress activates proinflammatory cytokines and antioxidant defense enzymes in human dental pulp cells. J Endod 34 (2008) 1364-1369
32. Kook Y.A., Lee S.K., Son D.H., et al. Effects of substance P on osteoblastic differentiation and heme oxygenase-1 in human periodontal ligament cells. Cell Biol Int 33 (2009) 424-428
33. Farombi E.O., and Surh Y.J. Heme oxygenase-1 as a potential therapeutic target for hepatoprotection. J Biochem Mol Biol 39 (2006) 479-491
34. Benallaoua M., François M., Batteux F., Thelier N., Shyy J.Y., Fitting C., et al. Pharmacologic induction of heme oxygenase 1 reduces acute inflammatory arthritis in mice. Arthritis Rheum 56 (2007) 2585-2594
35. Ma L.J., You Y., Bai B.X., and Li Y.Z. Therapeutic effects of heme oxygenase-1 on psoriasiform skin lesions in guinea pigs. Arch Dermatol Res 301 (2009) 459-466
36. Syapin P.J. Regulation of haeme oxygenase-1 for treatment of neuroinflammation and brain disorders. Br J Pharmacol 155 (2008) 623-640
37. Naito Y., Takagi T., and Yoshikawa T. Heme oxygenase-1: a new therapeutic target for inflammatory bowel disease. Aliment Pharmacol Ther 20 (2004) 177-184
38. Pi S.H., Lee S.K., Hwang Y.S., Choi M.G., Lee S.K., and 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 42 (2007) 103-114
39. Kutty R.K., and Maines M.D. Oxidation of heme c derivatives by purified heme oxygenase. Evidence for the presence of one molecular species of heme oxygenase in the rat liver. J Biol Chem 257 (1982) 9944-9952
40. Kornman K.S. Host modulation as a therapeutic strategy in the treatment of periodontal disease. Clin Infect Dis 28 (1999) 520-526
41. Bodet C., Chandad F., and Grenier D. Anti-inflammatory activity of a high-molecular-weight cranberry fraction on macrophages stimulated by lipopolysaccharides from periodontopathogens. J. Dental Res 85 (2006) 235-239
42. Zdarilová A., Svobodová A., Simánek V., and Ulrichová J. Prunella vulgaris extract and rosmarinic acid suppress lipopolysaccharide-induced alteration in human gingival fibroblasts. Toxicol In Vitro 23 (2009) 386-392
43. Chen D., Nie M., Fan M.W., and Bian Z. Anti-inflammatory activity of curcumin in macrophages stimulated by lipopolysaccharides from Porphyromonas gingivalis. Pharmacology 82 (2008) 264-269
44. Kowalski J., Samojedny A., Paul M., Pietsz G., and Wilczok T. Effect of apigenin, kaempferol and resveratrol on the expression of interleukin-1beta and tumor necrosis factor-alpha genes in J774.2 macrophages. Pharmacol Rep 57 (2005) 390-394
45. Lee J.H., Zhou H.Y., Cho S.Y., Kim Y.S., Lee Y.S., and Jeong C.S. Anti-inflammatory mechanisms of apigenin: inhibition of cyclooxygenase-2 expression, adhesion of monocytes to human umbilical vein endothelial cells, and expression of cellular adhesion molecules. Arch Pharm Res 30 (2007) 1318-1327
46. Balogun E., Hoque M., Gong P., Killeen E., Green C.J., Foresti R., et al. Curcumin activates the heme oxygenase-1 gene via regulation of Nrf2 and the antioxidant responsive element. Biochem J 371 (2003) 887-895
47. Scapagnini G., Foresti R., Calabrese V., Stella A.M., Green C.J., and Motterlini R. Caffeic acid phenethyl ester and curcumin: a novel class of heme oxygenase-1 inducers. Mol Pharmacol 61 (2002) 554-561
48. Juan S.H., Cheng T.H., Lin H.C., Chu Y.L., and Lee W.S. Mechanism of concentration-dependent induction of heme oxygenase-1 by resveratrol in human aortic smooth muscle cells. Biochem Pharmacol 69 (2005) 41-48
49. Hu C.M., Liu Y.H., Cheah K.P., Li J.S., Lam C.S., Yu W.Y., et al. Heme oxygenase-1 mediates the inhibitory actions of brazilin in RAW264.7 macrophages stimulated with lipopolysaccharide. J Ethnopharmacol 121 (2009) 79-85
50. Abate A., Yang G., Wong R.J., Schroder H., Stevenson D.K., and Dennery P.A. Apigenin decreases hemin-mediated heme oxygenase-1 induction. Free Radic Biol Med 39 (2005) 711-718
51. Hou L.T., Liu C.M., and Rossomando E.F. Crevicular interleukin-1 beta in moderate and severe periodontitis patients and the effect of phase I periodontal treatment. J Clin Periodontol 22 (1995) 162-167
52. Lima V., Vidal F.D., Rocha F.A., Brito G.A., and Ribeiro R.A. Effects of tumor necrosis factor-alpha inhibitors pentoxifylline and thalidomide on alveolar bone loss in short-term experimental periodontal disease in rats. J Periodontol 75 (2004) 162-168
53. Assuma R., Oates T., Cochran D., Amar S., and Graves D.T. IL-1 and TNF antagonists inhibit the inflammatory response and bone loss in experimental periodontitis. J Immunol 160 (1998) 403-409