Suppression of Toll-like receptor 4 activation by caffeic acid phenethyl ester is mediated by interferenceof LPS binding to MD2

British Journal of Pharmacology

Volumn 168, Issue 8, 2013, Pages 1933-1945

  Kim, So Young ^b   Koo, Jung Eun ^a   Seo, Yun Jee ^b   Tyagi, Nisha ^b   Jeong, Eunshil ^a   Choi, Jaeyoung ^c   Lim, Kyung Min ^d   Park, Zee Yong ^b   Lee, Joo Young ^a  

^a The Catholic University of Korea   (South Korea)

^b Gwangju Institute of Science and Technology (GIST)   (South Korea)

^c AmorePacific Corporation   (South Korea)

^d Ewha Womans University   (South Korea)

Author keywords

caffeic acid phenethyl ester; cysteine133; LPS; MD2; Toll like receptor

Indexed keywords

BETA INTERFERON; CAFFEIC ACID PHENETHYL ESTER; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; RANTES; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; ANTIINFLAMMATORY AGENT; CAFFEIC ACID DERIVATIVE; LY96 PROTEIN, HUMAN; LY96 PROTEIN, MOUSE; PHENETHYL ALCOHOL; PROTEIN MD 2; TLR4 PROTEIN, HUMAN; TLR4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DERMATITIS; DOWN REGULATION; DRUG EFFICACY; DRUG MECHANISM; DRUG TARGETING; HUMAN; HUMAN CELL; IMMUNOSUPPRESSIVE TREATMENT; MACROPHAGE; MALE; MOUSE; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; SKIN EDEMA; TRANSCRIPTION INITIATION; TREATMENT RESPONSE; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL LINE; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; GAS CHROMATOGRAPHY; GENE EXPRESSION REGULATION; HEK293 CELL LINE; INFLAMMATION; METABOLISM; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CAFFEIC ACIDS; CELL LINE; CHROMATOGRAPHY, GAS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; INFLAMMATION; INTERFERON REGULATORY FACTOR-3; LIPOPOLYSACCHARIDES; LYMPHOCYTE ANTIGEN 96; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NF-KAPPA B; PHENYLETHYL ALCOHOL; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; TOLL-LIKE RECEPTOR 4;

EID: 84875472803     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12091     Document Type: Article

References (33)

1. Akira S, Uematsu S, Takeuchi O, (2006). Pathogen recognition and innate immunity. Cell 124: 783-801.
2. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, Golenbock DT, et al. (2003). IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4: 491-496.
3. Frenkel K, Wei H, Bhimani R, Ye J, Zadunaisky JA, Huang MT, et al. (1993). Inhibition of tumor promoter-mediated processes in mouse skin and bovine lens by caffeic acid phenethyl ester. Cancer Res 53: 1255-1261.
4. Gobert AP, Bambou JC, Werts C, Balloy V, Chignard M, Moran AP, et al. (2004). Helicobacter pylori heat shock protein 60 mediates interleukin-6 production by macrophages via a toll-like receptor (TLR)-2-, TLR-4-, and myeloid differentiation factor 88-independent mechanism. J Biol Chem 279: 245-250.
5. Gradisar H, Keber MM, Pristovsek P, Jerala R, (2007). MD-2 as the target of curcumin in the inhibition of response to LPS. J Leukoc Biol 82: 968-974.
6. Ishihara S, Rumi MA, Kadowaki Y, Ortega-Cava CF, Yuki T, Yoshino N, et al. (2004). Essential role of MD-2 in TLR4-dependent signaling during Helicobacter pylori-associated gastritis. J Immunol 173: 1406-1416.
7. Joung SM, Park ZY, Rani S, Takeuchi O, Akira S, Lee JY, (2011). Akt contributes to activation of the TRIF-dependent signaling pathways of TLRs by interacting with TANK-binding kinase 1. J Immunol 186: 499-507.
8. Jung WK, Choi I, Lee DY, Yea SS, Choi YH, Kim MM, et al. (2008). Caffeic acid phenethyl ester protects mice from lethal endotoxin shock and inhibits lipopolysaccharide-induced cyclooxygenase-2 and inducible nitric oxide synthase expression in RAW 264.7 macrophages via the p38/ERK and NF-kappaB pathways. Int J Biochem Cell Biol 40: 2572-2582.
9. Kanzler H, Barrat FJ, Hessel EM, Coffman RL, (2007). Therapeutic targeting of innate immunity with Toll-like receptor agonists and antagonists. Nat Med 13: 552-559.
10. Kawai T, Adachi O, Ogawa T, Takeda K, Akira S, (1999). Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11: 115-122.
11. Keogh B, Parker AE, (2011). Toll-like receptors as targets for immune disorders. Trends Pharmacol Sci 32: 435-442.
12. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). NC3Rs Reporting Guidelines Working Group. Br J Pharmacol 160: 1577-1579.
13. Kim HM, Park BS, Kim JI, Kim SE, Lee J, Oh SC, et al. (2007). Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist Eritoran. Cell 130: 906-917.
14. Koksel O, Ozdulger A, Tamer L, Cinel L, Ercil M, Degirmenci U, et al. (2006). Effects of caffeic acid phenethyl ester on lipopolysaccharide-induced lung injury in rats. Pulm Pharmacol Ther 19: 90-95.
15. Lee JK, Kim SY, Kim YS, Lee WH, Hwang DH, Lee JY, (2009). Suppression of the TRIF-dependent signaling pathway of Toll-like receptors by luteolin. Biochem Pharmacol 77: 1391-1400.
16. Lee JY, Hwang DH, (2006). The modulation of inflammatory gene expression by lipids: mediation through Toll-like receptors. Mol Cells 21: 174-185.
17. Lee Y, Shin DH, Kim JH, Hong S, Choi D, Kim YJ, et al. (2010). Caffeic acid phenethyl ester-mediated Nrf2 activation and IkappaB kinase inhibition are involved in NFkappaB inhibitory effect: structural analysis for NFkappaB inhibition. Eur J Pharmacol 643: 21-28.
18. Mancek-Keber M, Gradisar H, Inigo Pestana M, Martinez De Tejada G, Jerala R, (2009). Free thiol group of MD-2 as the target for inhibition of the lipopolysaccharide-induced cell activation. J Biol Chem 284: 19493-19500.
19. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
20. Meylan E, Burns K, Hofmann K, Blancheteau V, Martinon F, Kelliher M, et al. (2004). RIP1 is an essential mediator of Toll-like receptor 3-induced NF-kappa B activation. Nat Immunol 5: 503-507.
21. Michaluart P, Masferrer JL, Carothers AM, Subbaramaiah K, Zweifel BS, Koboldt C, et al. (1999). Inhibitory effects of caffeic acid phenethyl ester on the activity and expression of cyclooxygenase-2 in human oral epithelial cells and in a rat model of inflammation. Cancer Res 59: 2347-2352.
22. Miyake K, (2006). Roles for accessory molecules in microbial recognition by Toll-like receptors. J Endotoxin Res 12: 195-204.
23. Mullen GE, Kennedy MN, Visintin A, Mazzoni A, Leifer CA, Davies DR, et al. (2003). The role of disulfide bonds in the assembly and function of MD-2. Proc Natl Acad Sci U S A 100: 3919-3924.
24. Natarajan K, Singh S, Burke TR, JR, Grunberger D, Aggarwal BB, (1996). Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B. Proc Natl Acad Sci U S A 93: 9090-9095.
25. Oshiumi H, Matsumoto M, Funami K, Akazawa T, Seya T, (2003). TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat Immunol 4: 161-167.
26. Park BS, Song DH, Kim HM, Choi BS, Lee H, Lee JO, (2009). The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458: 1191-1195.
27. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, et al. (1998). Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282: 2085-2088.
28. Re F, Strominger JL, (2003). Separate functional domains of human MD-2 mediate Toll-like receptor 4-binding and lipopolysaccharide responsiveness. J Immunol 171: 5272-5276.
29. Saitoh S, Akashi S, Yamada T, Tanimura N, Kobayashi M, Konno K, et al. (2004). Lipid A antagonist, lipid IVa, is distinct from lipid A in interaction with Toll-like receptor 4 (TLR4)-MD-2 and ligand-induced TLR4 oligomerization. Int Immunol 16: 961-969.
30. Schromm AB, Lien E, Henneke P, Chow JC, Yoshimura A, Heine H, et al. (2001). Molecular genetic analysis of an endotoxin nonresponder mutant cell line: a point mutation in a conserved region of MD-2 abolishes endotoxin-induced signaling. J Exp Med 194: 79-88.
31. Toyoda T, Tsukamoto T, Takasu S, Shi L, Hirano N, Ban H, et al. (2009). Anti-inflammatory effects of caffeic acid phenethyl ester (CAPE), a nuclear factor-kappaB inhibitor, on Helicobacter pylori-induced gastritis in Mongolian gerbils. Int J Cancer 125: 1786-1795.
32. Wang LC, Lin YL, Liang YC, Yang YH, Lee JH, Yu HH, et al. (2009). The effect of caffeic acid phenethyl ester on the functions of human monocyte-derived dendritic cells. BMC Immunol 10: 39.
33. Youn HS, Kim YS, Park ZY, Kim SY, Choi NY, Joung SM, et al. (2010). Sulforaphane suppresses oligomerization of TLR4 in a thiol-dependent manner. J Immunol 184: 411-419.