Baicalin Downregulates Porphyromonas gingivalis Lipopolysaccharide-Upregulated IL-6 and IL-8 Expression in Human Oral Keratinocytes by Negative Regulation of TLR Signaling

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Luo, Wei ^a   Wang, Cun Yu ^b   Jin, Lijian ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; BAICALIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR;

ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; DRUG MECHANISM; ENZYME LINKED IMMUNOSORBENT ASSAY; GAMMA INTERFERON INDUCIBLE PROTEIN 10 GENE; GENE EXPRESSION REGULATION; GENETIC ANALYSIS; GENETIC ASSOCIATION; GRANULOCYTE COLONY STIMULATING FACTOR GENE; HUMAN; HUMAN CELL; KERATINOCYTE; MONOCYTE CHEMOTACTIC PROTEIN 1 GENE; MOUTH MUCOSA; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING;

EID: 84871121476     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051008     Document Type: Article

References (77)

1. Jin LJ, Armitage GC, Klinge B, Lang NP, Tonetti M, et al. (2011) Global oral health inequalities: Task group-periodontal disease. Adv Dent Res 23: 221-226.
2. Parahitiyawa NB, Jin LJ, Leung WK, Yam WC, Samaranayake LP, (2009) Microbiology of odontogenic bacteraemia: beyond endocarditis. Clin Microbiol Rev 22: 46-64.
3. Li X, Tse HF, Jin LJ, (2011) Novel endothelial biomarkers: implications for periodontal disease and CVD. J Dent Res 90: 1062-1069.
4. Lalla E, Papapanou PN, (2011) Diabetes mellitus and periodontitis: a tale of two common interrelated diseases. Nat Rev Endocrinol 7: 738-748.
5. Darveau RP, (2010) Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol 8: 481-490.
6. Yilmaz O, (2008) The chronicles of Porphyromonas gingivalis: the microbium, the human oral epithelium and their interplay. Microbiology 154: 2897-2903.
7. Jain S, Darveau RP, (2010) Contribution of Porphyromonas gingivalis lipopolysaccharide to periodontitis. Periodontol 2000 54: 53-70.
8. Herath TDK, Wang Y, Seneviratne CJ, Lu Q, Darveau RP, et al. (2011) Porphyromonas gingivalis lipopolysaccharide lipid A heterogeneity differentially modulates the expression of IL-6 and IL-8 in human gingival fibroblasts. J Clin Periodontol 38: 694-701.
9. Souza PP, Palmqvist P, Lundgren I, Lie A, Costa-Neto CM, et al. (2010) Stimulation of IL-6 cytokines in fibroblasts by toll-like receptors 2. J Periodontal Res 89: 802-807.
10. Seo T, Cha S, Kim TI, Lee JS, Woo KM, (2012) Porphyromonas gingivalis-derived lipopolysaccharide-mediated activation of MAPK signaling regulates inflammatory response and differentiation in human periodontal ligament fibroblasts. J Microbiol 50: 311-319.
11. Akira S, Takeda K, (2004) Toll-like receptor signalling. Nat Rev Immunol 4: 499-511.
12. Wesche H, Henzel WJ, Shillinglaw W, Li S, Cao Z, (1997) MyD88: an adapter that recruits IRAK to the IL-1 receptor complex. Immunity 7: 837-847.
13. Medzhitov R, Preston-Hurlburt P, Kopp E, Stadlen A, Chen C, et al. (1998) MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol Cell 2: 253-258.
14. Kawai T, Adachi O, Ogawa T, Takeda K, Akira S, (1999) Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11: 115-122.
15. Kawai T, Takeuchi O, Fujita T, Inoue J, Mühlradt PF, et al. (2001) Lipopolysaccharide stimulates the MyD88-independent pathway and results in activation of IFN-regulatory factor 3 and the expression of a subset of lipopolysaccharide-inducible genes. J Immunol 167: 5887-5894.
16. Hoshino K, Kaisho T, Iwabe T, Takeuchi O, Akira S, (2002) Differential involvement of IFN-β in Toll-like receptor stimulated dendritic cell activation. Int Immunol 14: 1225-1231.
17. Yamamoto M, Sato S, Hemmi H, Hoshino K, Kaisho T, et al. (2003) Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science 301: 640-643.
18. Sakaguchi S, Negishi H, Asagiri M, Nakajima C, Mizutani T, et al. (2003) Essential role of IRF-3 in lipopolysaccharide-induced interferon-beta gene expression and endotoxin shock. Biochem Biophys Res Commun 306: 860-866.
19. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, et al. (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282: 2085-2088.
20. Ogawa T, Asai Y, Hashimoto M, Takeuchi O, Kurita T, et al. (2002) Cell activation by Porphyromonas gingivalis lipid A molecule through Toll-like receptor 4- and myeloid differentiation factor 88-dependent signaling pathway. Int Immunol 14: 1325-1332.
21. Sawada N, Ogawa T, Asai Y, Makimura Y, Sugiyama A, (2007) Toll-like receptor 4-dependent recognition of structurally different forms of chemically synthesized lipid As of Porphyromonas gingivalis. Clin Exp Immunol 148: 529-536.
22. Hirschfeld M, Weis JJ, Toshchakov V, Salkowski CA, Cody MJ, et al. (2001) Signaling by toll-like receptor 2 and 4 agonists results in differential gene expression in murine macrophages. Infect Immun 69: 1477-1482.
23. Yoshimura A, Kaneko T, Kato Y, Golenbock DT, Hara Y, (2002) Lipopolysaccharides from periodontopathic bacteria Porphyromonas gingivalis and Capnocytophaga ochracea are antagonists for human toll-like receptor 4. Infect Immun 70: 218-225.
24. Burns E, Bachrach G, Shapira L, Nussbaum G, (2006) Cutting edge: TLR2 is required for the innate response to Porphyromonas gingivalis: activation leads to bacterial persistence and TLR2 deficiency attenuates induced alveolar bone resorption. J Immunol 177: 8296-8300.
25. Netea MG, van Deuren M, Kullberg BJ, Cavaillon JM, Van der Meer JW, (2002) Does the shape of lipid A determine the interaction of LPS with Toll-like receptors? Trends Immunol 23: 135-139.
26. Darveau RP, Pham TT, Lemley K, Reife RA, Bainbridge BW, et al. (2004) Porphyromonas gingivalis lipopolysaccharide contains multiple lipid A species that functionally interact with both toll-like receptors 2 and 4. Infect Immun 72: 5041-5051.
27. Hirschfeld M, Ma Y, Weis JH, Vogel SN, Weis JJ, (2000) Cutting edge: repurification of lipopolysaccharide eliminates signaling through both human and murine Toll-like receptor 2. J Immunol 165: 618-622.
28. Ogawa T, Asai Y, Makimura Y, Tamai R, (2007) Chemical structure and immunobiological activity of Porphyromonas gingivalis lipid A. Front Biosci. 12: 3795-3812.
29. Kumada H, Haishima Y, Watanabe K, Hasegawa C, Tsuchiya T, et al. (2008) Biological properties of the native and synthetic lipid A of Porphyromonas gingivalis lipopolysaccharide. Oral Microbiol Immunol 23: 60-69.
30. Oringer RJ, Research Science, (2002) Therapy Committee of the American Academy of Periodontology (2002) Modulation of the host response in periodontal therapy. J Periodontol 73: 460-470.
31. Bhatavadekar NB, Williams RC, (2009) Modulation of the host inflammatory response in periodontal disease management: exciting new directions. Int Dent J 59: 305-308.
32. Serhan CN, Jain A, Marleau S, Clish C, Kantarci A, et al. (2003) Reduced inflammation and tissue damage in transgenic rabbits overexpressing 15-lipoxygenase and endogenous anti-inflammatory lipid mediators. J Immunol 171: 6856-6865.
33. Preshaw PM, Hefti AF, Jepsen S, Etienne D, Walker C, et al. (2004) Subantimicrobial dose doxycycline as adjunctive treatment for periodontitis. A review. J Clin Periodontol 31: 697-707.
34. Hasturk H, Kantarci A, Goguet-Surmenian E, Blackwood A, Andry C, et al. (2007) Resolvin E1 regulates inflammation at the cellular and tissue level and restores tissue homeostasis in vivo. J Immunol 179: 7021-7029.
35. Ikemoto S, Sugimura K, Yoshida N, Yasumoto R, Wada S, et al. (2000) Antitumor effects of Scutellariae radix and its components baicalein, baicalin, and wogonin on bladder cancer cell lines. Urology 55: 951-955.
36. Zhu G, Li C, Cao Z, (2007) Inhibitory effect of flavonoid baicalin on degranulation of human polymorphonuclear leukocytes induced by interleukin-8: potential role in periodontal diseases. J Ethnopharmacol 109: 325-330.
37. Wang GF, Wu ZF, Wan L, Wang QT, Chen FM, (2006) Influence of baicalin on the expression of receptor activator of nuclear factor-kappaB ligand in cultured human periodontal ligament cells. Pharmacology 77: 71-77.
38. Cai X, Li C, Du G, Cao Z, (2008) Protective effects of baicalin on the ligature-induced periodontitis in rats. J Periodontal Res 43: 14-21.
39. Cao Z, Li C, Zhu G, (2010) Inhibitory effects of baicalin on IL-1beta- induced MMP-1/TIMP-1 and its stimulated effect on collagen-I production in human periodontal ligament cells. Eur J Pharmacoly 641: 1-6.
40. Koga T, Nishihara T, Fujiwara T, Nisizawa T, Okahashi N, et al. (1985) Biochemical and immunobiological properties of lipopolysaccharide (LPS) from Bacteroides gingivalis and comparison with LPS from Escherichia coli. Infect Immun 47: 638-647.
41. Maruyama M, Hayakawa M, Zhang L, Shibata Y, Abiko Y, (2009) Monoclonal antibodies produced against lipopolysaccharide from fimA Type II Porphyromonas gingivalis. Hybridoma 28: 431-434.
42. Peirson SN, Butler JN, Foster RG, (2003) Experimental validation of novel and conventional approaches to quantitative real-time PCR data analysis. Nucleic Acids Res 31: 73-80.
43. Karin M, Ben-Neriah Y, (2000) Phosphorylation meets ubiquitination: the control of NF-kB activity. Annu Rev Immunol 18: 621-663.
44. Carayol N, Chen J, Yang F, Jin T, Jin LJ, et al. (2006) A Dominant Function of IKK/NF-kB Signaling in Global Lipopolysaccharide-induced Gene Expression. J Biol Chem 281: 31142-31151.
45. Chang L, Karin M, (2001) Mammalian MAP kinase signalling cascades. Nature 410: 37-40.
46. Garlet GP, (2010) Destructive and protective roles of cytokines in periodontitis: a re-appraisal from host defense and tissue destruction viewpoints. J Dent Res 89: 1349-1363.
47. Liu YC, Lerner UH, Teng YT, (2010) Cytokine responses against periodontal infection: protective and destructive roles. Periodontol 2000 52: 163-120.
48. Baggiolini M, Walz A, Kunkel SL, (1989) Neutrophil-activating peptide- 1/interleukin-8, a novel cytokine that activates neutrophils. J Clin Invest 84: 1045-1049.
49. Palmqvist P, Persson E, Conaway HH, Lerner UH, (2002) IL-6, leukemia inhibitory factor, and oncostatin M stimulate bone resorption and regulate the expression of receptor activator of NF-kappa B ligand, osteoprotegerin, and receptor activator of NF-kappa B in mouse calvariae. J Immunol 169: 3353-3362.
50. Berman KS, Verma UN, Harburg G, Minna JD, Cobb MH, et al. (2002) Sulindac enhances tumor necrosis factor-α-mediated apoptosis of lung cancer cell lines by inhibition of nuclear factor-κB. Clin Cancer Res 8: 354-360.
51. Burke JR, Pattoli MA, Gregor KR, Brassil PJ, MacMaster JF, et al. (2003) BMS-345541 is a highly selective inhibitor of IκB kinase that binds at an allosteric site of the enzyme and blocks NF-κB-dependent transcription in mice. J Biol Chem 278: 1450-1456.
52. Kishore N, Sommers C, Mathialagan S, Guzova J, Yao M, et al. (2003) A selective IKK-2 inhibitor blocks NF-κBdependent gene expression in IL-1β stimulated synovial fibroblasts. J Biol Chem 278: 32861-32871.
53. Park HJ, Jeong SK, Kim SR, Bae SK, Kim WS, et al. (2009) Resveratrol inhibits Porphyromonas gingivalis lipopolysaccharideinduced endothelial adhesion molecule expression by suppressing NF-kappaB activation. Arch Pharm Res 32: 583-591.
54. Rogers JE, Li F, Coatney DD, Otremba J, Kriegl JM, et al. (2007) A p38 mitogen-activated protein kinase inhibitor arrests active alveolar bone loss in a rat periodontitis model. J Periodontol 78: 1992-1998.
55. Saporito MS, Brown EM, Miller MS, Carswell S, (1999) CEP-1347/KT-7515, an inhibitor of c-jun N-terminal kinase activation, attenuates the 1-methyl-4-phenyl tetrahydropyridine-mediated loss of nigrostriatal dopaminergic neurons In vivo. J Pharmacol Exp Ther 288: 421-427.
56. Carboni S, Hiver A, Szyndralewiez C, Gaillard P, Gotteland JP, et al. (2004) AS601245 (1,3-benzothiazol-2-yl (2-[[2-(3-pyridinyl) ethyl] amino]-4 pyrimidinyl) acetonitrile): a c-Jun NH2-terminal protein kinase inhibitor with neuroprotective properties. J Pharmacol Exp Ther 310: 25-32.
57. Yamaguchi K, Shirakabe K, Shibuya H, Irie K, Oishi I, et al. (1995) Identification of a member of the MAPKKK family as a potential mediator of TGF-beta signal transduction. Science 270: 2008-2011.
58. Lee J, Mira-Arbibe L, Ulevitch RJ, (2000) TAK1 regulates multiple protein kinase cascades activated by bacterial lipopolysaccharide. J Leukoc Biol 68: 909-915.
59. Wang C, Deng L, Hong M, Akkaraju GR, Inoue J, et al. (2001) TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412: 346-351.
60. Cao Z, Henzel WJ, Gao X, (1996) IRAK: a kinase associated with the interleukin-1 receptor. Science 271: 1128-1131.
61. Li S, Strelow A, Fontana EJ, Wesche H, (2002) IRAK-4: a novel member of the IRAK family with the properties of an IRAK-kinase. Proc Natl Acad Sci USA 99: 5567-5572.
62. Janssens S, Beyaert R, (2003) Functional diversity and regulation of different interleukin-1 receptor-associated kinase (IRAK) family members. Mol Cell 11: 293-302.
63. Deshmane SL, Kremlev S, Amini S, Sawaya BE, (2009) Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res 29: 313-326.
64. Demetri GD, Griffin JD, (1991) Granulocyte colony-stimulating factor and its receptor. Blood 78: 2791-2808.
65. Lieschke GJ, Grail D, Hodgson G, Metcalf D, Stanley E, et al. (1994) Mice lacking granulocyte colony-stimulating factor have chronic neutropenia, granulocyte and macrophage progenitor cell deficiency, and impaired neutrophil mobilization. Blood 84: 1737-1746.
66. Liu M, Guo S, Hibbert JM, Jain V, Singh N, et al. (2011) CXCL10/IP-10 in infectious diseases pathogenesis and potential therapeutic implications. Cytokine Growth Factor Rev 22: 121-130.
67. Ueda A, Ishigatsubo Y, Okubo T, Yoshimura T, (1997) Transcriptional regulation of the human monocyte chemoattractant protein-1 gene. Cooperation of two NF-kappaB sites and NF-kappaB/Rel subunit specificity. J Biol Chem 272: 31092-31099.
68. Campbell IK, van Nieuwenhuijze A, Segura E, O'Donnell K, Coghill E, et al. (2011) Differentiation of inflammatory dendritic cells is mediated by NF-κB1-dependent GM-CSF production in CD4 T cells. J Immunol 186: 5468-5477.
69. Doyle S, Vaidya S, O'Connell R, Dadgostar H, Dempsey P, et al. (2002) IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity 17: 251-263.
70. Toshchakov V, Jones BW, Perera PY, Thomas K, Cody MJ, et al. (2003) TLR4, but not TLR2, mediates IFN-beta-induced STAT1alpha/beta-dependent gene expression in macrophages. Nat Immunol 3: 392-398.
71. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, et al. (2003) IKKε and TBK1 are essential components of the IRF3 signaling pathway. Nature Immunol 4: 491-496.
72. Hajishengallis G, (2009) Toll gates to periodontal host modulation and vaccine therapy. Periodontol 2000 51: 181-207.
73. Macagno A, Molteni M, Rinaldi A, Bertoni F, Lanzavecchia A, et al. (2006) A cyanobacterial LPS antagonist prevents endotoxin shock and blocks sustained TLR4 stimulation required for cytokine expression. J Exp Med 203: 1481-1492.
74. Kim HM, Park BS, Kim JI, Kim SE, Lee J, et al. (2007) Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist Eritoran. Cell 130: 906-917.
75. Toshchakov VY, Fenton MJ, Vogel SN, (2007) Cutting edge: differential inhibition of TLR signaling pathways by cell permeable peptides representing BB loops of TLRs. J Immunol 178: 2655-2660.
76. Benakanakere MR, Li Q, Eskan MA, Singh AV, Zhao J, et al. (2009) Modulation of TLR2 protein expression by miR-105 in human oral keratinocytes. J Biol Chem 284: 23107-23115.
77. Dominguez C, Powers DA, Tamayo N, (2005) p38 MAP kinase inhibitors: many are made, but few are chosen. Curr Opin Drug Discov Devel 8: 421-430.