DHA suppresses Prevotella intermedia lipopolysaccharide-induced production of proinflammatory mediators in murine macrophages

British Journal of Nutrition

Volumn 111, Issue 7, 2014, Pages 1221-1230

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

^a Silla University   (South Korea)

^b Pusan National University   (South Korea)

Author keywords

DHA; Lipopolysaccharide; Prevotella intermedia; Proinflammatory mediators

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; DOCOSAHEXAENOIC ACID; HEME OXYGENASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; NITRIC OXIDE; PROTOPORPHYRIN TIN; STAT1 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; AUTACOID; ENZYME INHIBITOR; HMOX1 PROTEIN, MOUSE; IL1B PROTEIN, MOUSE; INTERLEUKIN 6, MOUSE; INTERLEUKIN-6, MOUSE; LIPOPOLYSACCHARIDE; MEMBRANE PROTEIN; METALLOPORPHYRIN; NONSTEROID ANTIINFLAMMATORY AGENT; NOS2 PROTEIN, MOUSE; PROTOPORPHYRIN;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DNA BINDING; GENE EXPRESSION; GENETIC TRANSCRIPTION; MACROPHAGE; NONHUMAN; PREVOTELLA INTERMEDIA; PROTEIN PHOSPHORYLATION; ANIMAL; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; FAT INTAKE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; ISOLATION AND PURIFICATION; MACROPHAGE ACTIVATION; METABOLISM; MICROBIOLOGY; MOUSE; PERIODONTITIS; SIGNAL TRANSDUCTION; TRANSFORMED CELL LINE;

MURINAE; PREVOTELLA INTERMEDIA;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CELL LINE, TRANSFORMED; DIETARY FATS; DOCOSAHEXAENOIC ACIDS; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; HEME OXYGENASE-1; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MACROPHAGE ACTIVATION; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MEMBRANE PROTEINS; METALLOPORPHYRINS; MICE; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PERIODONTITIS; PREVOTELLA INTERMEDIA; PROTOPORPHYRINS;

EID: 84900497061     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114513003681     Document Type: Article

References (54)

1. Williams RC (1990) Periodontal disease. N Engl J Med 322, 373-381.
2. Teng YT, Taylor GW, Scannapieco F, et al. (2002) Periodontal health and systemic disorders. J Can Dent Assoc 68, 188-192.
3. Seymour GJ, Ford PJ, Cullinan MP, et al. (2007) Relationship between periodontal infections and systemic disease. Clin Microbiol Infect 13, 3-10.
4. Sosroseno W, Barid I, Herminajeng E, et al. (2002) Nitric oxide production by a murine macrophage cell line (RAW264.7) stimulated with lipopolysaccharide from Actinobacillus actinomycetemcomitans. Oral Microbiol Immunol 17, 72-78.
5. Kim SJ, Ha MS, Choi EY, et al. (2004) Prevotella intermedia lipopolysaccharide stimulates release of nitric oxide by inducing expression of inducible nitric oxide synthase. J Periodontal Res 39, 424-431.
6. Kim SJ, Ha MS, Choi EY, et al. (2005) Nitric oxide production and inducible nitric oxide synthase expression induced by Prevotella nigrescens lipopolysaccharide. FEMS Immunol Med Microbiol 43, 51-58.
7. Kim SJ, Choi EY, Kim EG, et al. (2007) Prevotella intermedia lipopolysaccharide stimulates release of tumor necrosis factor-α through mitogen-activated protein kinase signaling pathways in monocyte-derived macrophages. FEMS Immunol Med Microbiol 51, 407-413.
8. Calder PC (2006) n-3 Polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr 83, Suppl., 1505S-1519S.
9. Leeb BF, Sautner J, Andel I, et al. (2006) Intravenous application of omega-3 fatty acids in patients with active rheumatoid arthritis. The ORA-1 trial. An open pilot study. Lipids 41, 29-34.
10. Geusens P, Wouters C, Nijs J, et al. (1994) Long-term effect of omega-3 fatty acid supplementation in active rheumatoid arthritis. A 12-month, double-blind, controlled study. Arthritis Rheum 37, 824-829.
11. Kesavalu L, Vasudevan B, Raghu B, et al. (2006) Omega-3 fatty acid effect on alveolar bone loss in rats. J Dent Res 85, 648-652.
12. Naqvi AZ, Buettner C, Phillips RS, et al. (2010) n-3 Fatty acids and periodontitis in US adults. J Am Diet Assoc 110, 1669-1675.
13. Iwasaki M, Yoshihara A, Moynihan P, et al. (2010) Longitudinal relationship between dietary ω-3 fatty acids and periodontal disease. Nutrition 26, 1105-1109.
14. Green LC, Wagner DA, Glogowski J, et al. (1982) Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem 126, 131-138.
15. Choi EY, Jin JY, Lee JY, et al. (2011) Melatonin inhibits Prevotella intermedia lipopolysaccharide-induced production of nitric oxide and interleukin-6 in murine macrophages by suppressing NF-κB and STAT1 activity. J Pineal Res 50, 197-206.
16. Slots J, Bragd L, Wikström M, et al. (1986) The occurrence of Actinobacillus actinomycetemcomitans, Bacteroides gingivalis and Bacteroides intermedius in destructive periodontal disease in adults. J Clin Periodontol 13, 570-577.
17. Tanner AC, Haffer C, Bratthall GT, et al. (1979) A study of the bacteria associated with advancing periodontitis in man. J Clin Periodontol 6, 278-307.
18. Chung CP, Nisengard RJ, Slots J, et al. (1983) Bacterial IgG and IgM antibody titers in acute necrotizing ulcerative gingivitis. J Periodontol 54, 557-562.
19. Kornman KS & Loesche WJ (1980) The subgingival microbial flora during pregnancy. J Periodontal Res 15, 111-122.
20. Pelt P, Zimmermann B, Ulbrich N, et al. (2002) 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 47, 859-866.
21. Sosroseno W, Herminajeng E, Bird PS, et al. (2004) L-Argininedependent nitric oxide production of a murine macrophagelike RAW264.7 cell line stimulated with Porphyromonas gingivalis lipopolysaccharide. Oral Microbiol Immunol 19, 65-70.
22. Shapira L, Champagne C, Van Dyke TE, et al. (1998) Straindependent activation of monocytes and inflammatory macrophages by lipopolysaccharide of Porphyromonas gingivalis. Infect Immun 66, 2736-2742.
23. Zappa U, Reinking-Zappa M, Graf H, et al. (1991) Cell populations and episodic periodontal attachment loss in humans. J Clin Periodontol 18, 508-515.
24. Kornman KS, Page RC & Tonetti MS (1997) The host response to the microbial challenge in periodontitis: assembling the players. Periodontol 2000 14, 33-53.
25. Hamada S, Takada H, Ogawa T, et al. (1990) Lipopolysaccharides of oral anaerobes associated with chronic inflammation: chemical and immunomodulating properties. Int Rev Immunol 6, 247-261.
26. Kirikae T, Nitta T, Kirikae F, et al. (1999) 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 67, 1736-1742.
27. Matejka M, Partyka L, Ulm C, et al. (1998) Nitric oxide synthesis is increased in periodontal disease. J Periodontal Res 33, 517-518.
28. Batista AC, Silva TA, Chun JH, et al. (2002) Nitric oxide synthesis and severity of human periodontal disease. Oral Dis 8, 254-260.
29. Stashenko P, Fujiyoshi P, Obernesser MS, et al. (1991) Levels of interleukin 1β in tissues from sites of active periodontal disease. J Clin Periodontol 18, 567-575.
30. 2-microglobulin, and transforming growth factor-a in gingival crevicular fluid from human periodontal disease. Arch Oral Biol 44, 535-539.
31. Geivelis M, Turner DW, Pederson ED, et al. (1993) Measurements of interleukin-6 in gingival crevicular fluid from adults with destructive periodontal disease. J Periodontol 64, 980-983.
32. Tatakis DN (1993) Interleukin-1 and bone metabolism: a review. J Periodontol 64, 416-431.
33. 2 signaling systems results in enhancement of osteoclastogenesis through effects on the osteoprotegerin/receptor activator of NF-κB (RANK) ligand/RANK system. Endocrinology 146, 1991-1998.
34. Ryter SW, Alam J & Choi AM (2006) Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86, 583-650.
35. Otterbein LE, Soares MP, Yamashita K, et al. (2003) Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 24, 449-455.
36. Morse D & Choi AM (2002) Heme oxygenase-1: the "emerging molecule" has arrived. Am J Respir Cell Mol Biol 27, 8-16.
37. Poss KD & Tonegawa S (1997) Reduced stress defense in heme oxygenase 1-deficient cells. Proc Natl Acad Sci U S A 94, 10925-10930.
38. Otterbein LE, Bach FH, Alam J, et al. (2000) Carbon monoxide has anti-inflammatory effects involving the mitogenactivated protein kinase pathway. Nat Med 6, 422-428.
39. Morse D, Pischke SE, Zhou Z, et al. (2003) Suppression of inflammatory cytokine production by carbon monoxide involves the JNK pathway and AP-1. J Biol Chem 278, 36993-36998.
40. Sarady-Andrews JK, Liu F, Gallo D, et al. (2005) Biliverdin administration protects against endotoxin-induced acute lung injury in rats. Am J Physiol Lung Cell Mol Physiol 289, L1131-L1137.
41. Baeuerle PA & Henkel T (1994) Function and activation of NF-κB in the immune system. Annu Rev Immunol 12, 141-179.
42. Rothwarf DM & Karin M (1999) The NF-κB activation pathway: a paradigm in information transfer from membrane to nucleus. Sci STKE 1999, RE1.
43. Karin M & Ben-Neriah Y (2000) Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu Rev Immunol 18, 621-663.
44. Covert MW, Leung TH, Gaston JE, et al. (2005) Achieving stability of lipopolysaccharide-induced NF-κB activation. Science 309, 1854-1857.
45. Li Q & Verma IM (2002) NF-κB regulation in the immune system. Nat Rev Immunol 2, 725-734.
46. Hayden MS & Ghosh S (2004) Signaling to NF-κB. Genes Dev 18, 2195-2224.
47. Ghosh S, May MJ & Kopp EB (1998) NF-κB and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 16, 225-260.
48. Pfitzner E, Kliem S, Baus D, et al. (2004) The role of STATs in inflammation and inflammatory diseases. Curr Pharm Des 10, 2839-2850.
49. Schindler C & Darnell JE Jr (1995) Transcriptional responses to polypeptide ligands: the JAK-STAT pathway. Annu Rev Biochem 64, 621-651.
50. Schindler C, Levy DE & Decker T (2007) JAK-STAT signaling: from interferons to cytokines. J Biol Chem 282, 20059-20063.
51. Gao JJ, Filla MB, Fultz MJ, et al. (1998) Autocrine/paracrine IFN-αβ mediates the lipopolysaccharide-induced activation of transcription factor Stat1α in mouse macrophages: pivotal role of Stat1α in induction of the inducible nitric oxide synthase gene. J Immunol 161, 4803-4810.
52. Requirand P, Gibert P, Tramini P, et al. (2000) Serum fatty acid imbalance in bone loss: example with periodontal disease. Clin Nutr 19, 271-276.
53. Ramirez-Tortosa MC, Quiles JL, Battino M, et al. (2010) Periodontitis is associated with altered plasma fatty acids and cardiovascular risk markers. Nutr Metab Cardiovasc Dis 20, 133-139.
54. Figueredo CM, Martinez GL, Koury JC, et al. (2013) Serum levels of long-chain polyunsaturated fatty acids in patients with periodontal disease. J Periodontol 84, 675-685.