Kaempferol inhibits P. intermedia lipopolysaccharide-induced production of nitric oxide through translational regulation in murine macrophages: Critical role of heme oxygenase-1-mediated ROS reduction

Journal of Periodontology

Volumn 84, Issue 4, 2013, Pages 545-555

  Choi, In Soon ^a   Choi, Eun Young ^a   Jin, Ji Young ^a   Park, Hae Ryoun ^b   Choi, Jeom Il ^b,c   Kim, Sung Jo ^b,c  

^a Silla University   (South Korea)

^b Pusan National University   (South Korea)

^c Pusan National University School of Medicine   (South Korea)

Author keywords

Heme oxygenase 1; Kaempferol; Lipopolysaccharides; Nitric oxide; Prevotella intermedia; Reactive oxygen species

Indexed keywords

HEME OXYGENASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; KAEMPFEROL; KAEMPFEROL DERIVATIVE; LIPOPOLYSACCHARIDE; NITRIC OXIDE; NOS2 PROTEIN, MOUSE; REACTIVE OXYGEN METABOLITE;

ANIMAL; ARTICLE; BIOSYNTHESIS; CELL LINE; DRUG ANTAGONISM; DRUG EFFECT; MACROPHAGE; METABOLISM; MOUSE; PHYSIOLOGY; PREVOTELLA INTERMEDIA; PROTEIN PROCESSING;

ANIMALS; CELL LINE; HEME OXYGENASE-1; KAEMPFEROLS; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PREVOTELLA INTERMEDIA; PROTEIN MODIFICATION, TRANSLATIONAL; REACTIVE OXYGEN SPECIES;

EID: 84876125385     PISSN: 00223492     EISSN: None     Source Type: Journal    
DOI: 10.1902/jop.2012.120180     Document Type: Article

References (50)

1. Preshaw PM. Host response modulation in periodontics. Periodontol 2000 2008;48:92-110.
2. Reddy MS, Geurs NC, Gunsolley JC. Periodontal host modulation with antiproteinase, anti-inflammatory, and bone-sparing agents. A systematic review. Ann Periodontol 2003;8:12-37.
3. Moncada S, Palmer RMJ, Higgs EA. Nitric oxide: Physiology, pathophysiology, and pharmacology. Pharmacol Rev 1991;43:109-142.
4. Southey A, Tanaka S, Murakami T, et al. Pathophysiological role of nitric oxide in rat experimental colitis. Int J Immunopharmacol 1997;19:669-676.
5. Weinberg JB, Granger DL, Pisetsky DS, et al. The role of nitric oxide in the pathogenesis of spontaneous J Periodontol • April 2013 Choi, Choi, Jin, Park, Choi, Kim murine autoimmune disease: Increased nitric oxide production and nitric oxide synthase expression in MRL-lpr/lpr mice, and reduction of spontaneous glomerulonephritis and arthritis by orally administered NGmonomethyl- L-arginine. J ExpMed 1994;179:651-660.
6. Matejka M, Partyka L, Ulm C, Solar P, Sinzinger H. Nitric oxide synthesis is increased in periodontal disease. J Periodontal Res 1998;33:517-518.
7. Batista AC, Silva TA, Chun JH, Lara VS. Nitric oxide synthesis and severity of human periodontal disease. Oral Dis 2002;8:254-260.
8. Hirose M, Ishihara K, Saito A, Nakagawa T, Yamada S, Okuda K. Expression of cytokines and inducible nitric oxide synthase in inflamed gingival tissue. J Periodontol 2001;72:590-597.
9. Kendall HK, Haase HR, Li H, Xiao Y, Bartold PM. Nitric oxide synthase type-II is synthesized by human gingival tissue and cultured human gingival fibroblasts. J Periodontal Res 2000;35:194-200.
10. Lappin DF, Kjeldsen M, Sander L, Kinane DF. Inducible nitric oxide synthase expression in periodontitis. J Periodontal Res 2000;35:369-373.
11. Sosroseno W, Barid I, Herminajeng E, Susilowati H. Nitric oxide production by a murine macrophage cell line (RAW264.7) stimulated with lipopolysaccharide from Actinobacillus actinomycetemcomitans. Oral Microbiol Immunol 2002;17:72-78.
12. Kim SJ, Ha MS, Choi EY, Choi JI, Choi IS. Prevotella intermedia lipopolysaccharide stimulates release of nitric oxide by inducing expression of inducible nitric oxide synthase. J Periodontal Res 2004;39:424-431.
13. Kim SJ, Ha MS, Choi EY, Choi JI, Choi IS. Nitric oxide production and inducible nitric oxide synthase expression induced by Prevotella nigrescens lipopolysaccharide. FEMS Immunol Med Microbiol 2005;43:51-58.
14. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/ carbon monoxide: From basic science to therapeutic applications. Physiol Rev 2006;86:583-650.
15. Otterbein LE, Soares MP, Yamashita K, Bach FH. Heme oxygenase-1: Unleashing the protective properties of heme. Trends Immunol 2003;24:449-455.
16. Rushworth SA, Chen XL, Mackman N, Ogborne RM, O'Connell MA. Lipopolysaccharide-induced heme oxygenase-1 expression in human monocytic cells is mediated via Nrf2 and protein kinase C. J Immunol 2005;175:4408-4415.
17. Kutty RK, Kutty G, Wiggert B, Chader GJ, Darrow RM, Organisciak DT. Induction of heme oxygenase 1 in the retina by intense visible light: Suppression by the antioxidant dimethylthiourea. Proc Natl Acad Sci USA 1995;92:1177-1181.
18. Poss KD, Tonegawa S. Reduced stress defense in heme oxygenase 1-deficient cells. Proc Natl Acad Sci USA 1997;94:10925-10930.
19. Wiesel P, Foster LC, Pellacani A, et al. Thioredoxin facilitates the induction of heme oxygenase-1 in response to inflammatory mediators. J Biol Chem 2000; 275:24840-24846.
20. Oh GS, Pae HO, Lee BS, et al. Hydrogen sulfide inhibits nitric oxide production and nuclear factor-kB via heme oxygenase-1 expression in RAW264.7 macrophages stimulated with lipopolysaccharide. Free RadicBiol Med 2006;41:106-119.
21. Skaleric U, Manthey CM, Mergenhagen SE, Gaspirc B, Wahl SM. Superoxide release and superoxide dismutase expression by human gingival fibroblasts. Eur J Oral Sci 2000;108:130-135.
22. Petti S, Scully C. Polyphenols, oral health and disease: A review. J Dent 2009;37:413-423.
23. Slots J, Bragd L, Wikström M, Dahlén G. The occurrence of Actinobacillus actinomycetemcomitans, Bacteroides gingivalis and Bacteroides intermedius in destructive periodontal disease in adults. J Clin Periodontol 1986;13:570-577.
24. Tanner AC, Haffer C, Bratthall GT, Visconti RA, Socransky SS. A study of the bacteria associated with advancing periodontitis in man. J Clin Periodontol 1979;6:278-307.
25. Chung CP, Nisengard RJ, Slots J, Genco RJ. Bacterial IgG and IgM antibody titers in acute necrotizing ulcerative gingivitis. J Periodontol 1983;54:557-562.
26. Kornman KS, Loesche WJ. The subgingival microbial flora during pregnancy. J Periodontal Res 1980;15: 111-122.
27. Morrison DC, Ryan JL. Endotoxins and disease mechanisms. Annu Rev Med 1987;38:417-432.
28. Geller DA, Nussler AK, Di Silvio M, et al. Cytokines, endotoxin, and glucocorticoids regulate the expression of inducible nitric oxide synthase in hepatocytes. Proc Natl Acad Sci USA 1993;90:522-526.
29. Nathan C, Xie QW. Regulation of biosynthesis of nitric oxide. J Biol Chem 1994;269:13725-13728.
30. Fotsis T, Pepper MS, Aktas E, et al. Flavonoids, dietaryderived inhibitors of cell proliferation and in vitro angiogenesis. Cancer Res 1997;57:2916-2921.
31. Middleton E Jr., Kandaswami C, Theoharides TC. The effects of plant flavonoids on mammalian cells: Implications for inflammation, heart disease, and cancer. Pharmacol Rev 2000;52:673-751.
32. Calderón-Montaño JM, Burgos-Morón E, Pérez- Guerrero C, López-Lázaro M. A review on the dietary flavonoid kaempferol. Mini Rev Med Chem 2011;11: 298-344.
33. Lin MK, Yu YL, Chen KC, et al. Kaempferol from Semen cuscutae attenuates the immune function of dendritic cells. Immunobiology 2011;216:1103-1109.
34. Kowalski J, Samojedny A, Paul M, Pietsz G, Wilczok T. Effect of kaempferol on the production and gene expression of monocyte chemoattractant protein-1 in J774.2 macrophages. Pharmacol Rep 2005;57:107-112.
35. Park SE, Sapkota K, Kim S, Kim H, Kim SJ. Kaempferol acts through mitogen-activated protein kinases and protein kinase B/AKT to elicit protection in a model of neuroinflammation in BV2 microglial cells. Br J Pharmacol 2011;164:1008-1025.
36. Choi EY, Jin JY, Lee JY, Choi JI, Choi IS, Kim SJ. Melatonin inhibits Prevotella intermedia lipopolysaccharide- induced production of nitric oxide and interleukin-6 in murine macrophages by suppressing NF-kB and STAT1 activity. J Pineal Res 2011;50:197-206.
37. Markwell MA, Haas SM, Bieber LL, Tolbert NE. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 1978;87:206-210.
38. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem 1982;126:131-138.
39. Kim SJ, Choi EY, Kim EG, et al. Prevotella intermedia lipopolysaccharide stimulates release of tumor necrosis factor-alpha through mitogen-activated protein kinase signaling pathways in monocyte-derived macrophages. FEMS Immunol Med Microbiol 2007;51: 407-413.
40. Hamada S, Takada H, Ogawa T, Fujiwara T, Mihara J. Lipopolysaccharides of oral anaerobes associated with chronic inflammation: Chemical and immunomodulating properties. Int Rev Immunol 1990;6:247-261.
41. Kirikae T, Nitta T, Kirikae F, et al. Lipopolysaccharides (LPS) of oral black-pigmented bacteria induce tumor necrosis factor production by LPS-refractory C3H/HeJ macrophages in a way different from that of Salmonella LPS. Infect Immun 1999;67:1736-1742.
42. Hashimoto M, Asai Y, Tamai R, Jinno T, Umatani K, Ogawa T. Chemical structure and immunobiological activity of lipid A from Prevotella intermedia ATCC 25611 lipopolysaccharide. FEBS Lett 2003;543:98-102.
43. Sosroseno W, Herminajeng E, Bird PS, Seymour GJ. Larginine- dependent nitric oxide production of a murine macrophage-like RAW 264.7 cell line stimulated with Porphyromonas gingivalis lipopolysaccharide. Oral Microbiol Immunol 2004;19:65-70.
44. Shapira L, Champagne C, VanDyke TE,Amar S. Straindependent activation of monocytes and inflammatory macrophages by lipopolysaccharide of Porphyromonas gingivalis. Infect Immun 1998;66:2736-2742.
45. Pelt P, Zimmermann B, Ulbrich N, Bernimoulin JP. Effects of lipopolysaccharide extracted from Prevotella intermedia on bone formation and on the release of osteolytic mediators by fetal mouse osteoblasts in vitro. Arch Oral Biol 2002;47:859-866.
46. Uǧar-Cankal D, Ozmeric N. A multifaceted molecule, nitric oxide in oral and periodontal diseases. Clin Chim Acta 2006;366:90-100.
47. Choi EY, Jin JY, Choi JI, Choi IS, Kim SJ. Effects of luteolin on the release of nitric oxide and interleukin-6 by macrophages stimulated with lipopolysaccharide from Prevotella intermedia. J Periodontol 2011;82: 1509-1517.
48. Choi EY, Jin JY, Lee JY, Choi JI, Choi IS, Kim SJ. Anti-inflammatory effects and the underlying mechanisms of action of daidzein in murine macrophages stimulated with Prevotella intermedia lipopolysaccharide. J Periodontal Res 2012;47: 204-211.
49. Lu Y, Wahl LM. Oxidative stress augments the production ofmatrixmetalloproteinase-1, cyclooxygenase- 2, and prostaglandin E2 through enhancement of NF-kB activity in lipopolysaccharide-activated human primary monocytes. J Immunol 2005;175: 5423-5429.
50. Hsu HY, Wen MH. Lipopolysaccharide-mediated reactive oxygen species and signal transduction in the regulation of interleukin-1 gene expression. J Biol Chem 2002;277:22131-22139.