Specific inhibition of MyD88-independent signaling pathways of TLR3 and TLR4 by resveratrol: Molecular targets are TBK1 and RIP1 in TRIF complex

Journal of Immunology

Volumn 175, Issue 5, 2005, Pages 3339-3346

  Youn, Hyung S ^a   Lee, Joo Y ^a,e   Fitzgerald, Katherine A ^b   Young, Howard A ^c   Akira, Shizuo ^d   Hwang, Daniel H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d OSAKA UNIVERSITY   (Japan)

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

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; BETA INTERFERON; CYCLOOXYGENASE 2; CYTOKINE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERFERON; INTERFERON REGULATORY FACTOR 3; LIPOPOLYSACCHARIDE; MYELOID DIFFERENTIATION FACTOR 88; PHOSPHOTRANSFERASE; POLYINOSINIC POLYCYTIDYLIC ACID; PROTEIN RIP1; PROTEIN TRIF; REGULATOR PROTEIN; RESVERATROL; TANK BINDING KINASE 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL LINE; CHRONIC INFLAMMATION; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; EMBRYO CELL; ENZYME INHIBITION; FIBROBLAST; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; INFECTION; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

EID: 23844478190     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.175.5.3339     Document Type: Article

References (61)

1. Medzhitov, R., P. Preston-Hurlburt, and C. A. Janeway, Jr. 1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388: 394-397.
2. O'Neill, L. A. 2004. TLRs: Professor Mechnikov, sit on your hat. Trends Immunol. 25: 687-693.
3. Takeda, K., T. Kaisho, and S. Akira. 2003. Toll-like receptors. Annu. Rev. Immunol. 21: 335-376.
4. Zhang, D., G. Zhang, M. S. Hayden, M. B. Greenblatt, C. Bussey, R. A. Flavell, and S. Ghosh. 2004. A Toll-like receptor that prevents infection by uropathogenic bacteria. Science 303: 1522-1526.
5. Hayashi, F., K. D. Smith, A. Ozinsky, T. R. Hawn, E. C. Yi, D. R. Goodlett, J. K. Eng, S. Akira, D. M. Underhill, and A. Aderem. 2001. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410: 1099-1103.
6. Hemmi, H., O. Takeuchi, T. Kawai, T. Kaisho, S. Sato, H. Sanjo, M. Matsumoto, K. Hoshino, H. Wagner, K. Takeda, and S. Akira. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408: 740-745.
7. Rhee, S. H., and D. Hwang. 2000. Murine Toll-like receptor 4 confers lipopolysaccharide responsiveness as determined by activation of NFκB and expression of the inducible cyclooxygenase. J. Biol. Chem. 275: 34035-34040.
8. Poltorak, A., X. He, I. Smirnova, M. Y. Liu, C. Van Huffel, X. Du, D. Birdwell, E. Alejos, M, Silva, C. Galanos, et al. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282: 2085-2088.
9. Heil, F., H. Hemmi, H. Hochrein, F. Ampenberger, C. Kirschning, S. Akira, G. Lipford, H. Wagner, and S. Bauer. 2004. Species-specific recognition of single-stranded RNA via Toll-like receptor 7 and 8. Science 303: 1526-1529.
10. Diebold, S. S., T. Kaisho, H. Hemmi, S. Akira, and C. Reis e Sousa. 2004. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303: 1529-1531.
11. Alexopoulou, L., A. C. Holt, R. Medzhitov, and R. A. Flavell. 2001. Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 413: 732-738.
12. Lien, E., T. J. Sellati, A. Yoshimura, T. H. Flo, G. Rawadi, R. W. Finberg, J. D. Carroll, T. Espevik, R. R. Ingalls, J. D. Radolf, and D. T. Golenbock. 1999. Toll-like receptor 2 functions as a pattern recognition receptor for diverse bacterial products. J. Biol. Chem. 274: 33419-33425.
13. Ohashi, K., V. Burkart, S. Flohe, and H. Kolb. 2000. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the Toll-like receptor-4 complex. J. Immunol. 164: 558-561.
14. Okamura, Y., M. Watari, E. S. Jerud, D. W. Young, S. T. Ishizaka, J. Rose, J. C. Chow, and J. F. Strauss, III. 2001. The extra domain A of fibronectin activates Toll-like receptor 4. J. Biol. Chem. 276: 10229-10233.
15. Kurt-Jones, E. A., L. Popova, L. Kwinn, L. M. Haynes, L. P. Jones, R. A. Tripp, E. E. Walsh, M. W. Freeman, D. T. Golenbock, L. J. Anderson, and R. W. Finberg. 2000. Pattern recognition receptors TLR4 and CDI4 mediate response to respiratory syncytial virus. Nat. Immunol. 1: 398-401.
16. Lee, J. Y., K. H, Sohn, S. H. Rhee, and D. Hwang. 2001. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J. Biol. Chem. 276: 16683-16689.
17. Byrd-Leifer, C. A., E. F. Block, K. Takeda, S. Akira, and A. Ding. 2001. The role of MyD88 and TLR4 in the LPS-mimetic activity of Taxol. Eur. J. Immunol. 31: 2448-2457.
18. Lee, J. Y., J. Ye, Z. Gao, H. S. Youn, W. H. Lee, L. Zhao, N. Sizemore, and D. H. Hwang. 2003. Reciprocal modulation of Toll-like receptor-4 signaling pathways involving MyD88 and phosphatidylinositol 3-kinase/AKT by saturated and polyunsaturated fatty acids. J. Biol Chem. 278: 37041-37051.
19. Medzhitov, R., P. Preston-Hurlburt, E. Kopp, A. Stadlen, C. Chen, S. Ghosh, and C. A. Janeway, Jr. 1998. MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol Cell 2: 253-258.
20. Muzio, M., G. Natoli, S. Saccani, M. Levrero, and A. Mantovani. 1998. The human Toll signaling pathway: divergence of nuclear factor κB and JNK/SAPK activation upstream of tumor necrosis factor receptor-associated factor 6 (TRAF6). J. Exp. Med. 187: 2097-2101.
21. Wesche, H., W. J. Henzel, W. Shillinglaw, S. Li, and Z. Cao. 1997. MyD88: an adapter that recruits IRAK to the IL-1 receptor complex. Immunity 7: 837-847.
22. Barton, G. M., and R. Medzhitov. 2003. Toll-like receptor signaling pathways. Science 300: 1524-1525.
23. Oshiumi, H., M. Matsumoto, K. Funami, T. Akazawa, and T. Seya. 2003. TI-CAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-β induction. Nat. Immunol. 4: 161-167.
24. Yamamoto, M., S. Sato, K. Mori, K. Hoshino, O. Takeuchi, K. Takeda, and S. Akira. 2002. Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-β promoter in the Toll-like receptor signaling. J. Immunol. 169: 6668-6672.
25. Fitzgerald, K. A., S. M. McWhirter, K. L. Faia, D. C. Rowe, E. Latz, D. T. Golenbock, A. J. Coyle, S. M. Liao, and T. Maniatis. 2003. IKKε and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4: 491-496.
26. Toshchakov, V., B. W. Jones, P. Y. Perera, K. Thomas, M. J. Cody, S. Zhang, B. R. Williams, J. Major, T. A. Hamilton, M. J. Fenton, and S. N. Vogel. 2002. TLR4, but not TLR2, mediates IFN-β-induced STATl α/β- dependent gene ex-pression in macrophages. Nat. Immunol. 3: 392-398.
27. Cook, D. N., D. S. Pisetsky, and D. A. Schwartz. 2004. Toll-like receptors in the pathogenesis of human disease. Nat. Immunol. 5: 975-979.
28. Michelsen, K. S., M. H. Wong, P. K. Shah, W. Zhang, J. Yano, T. M. Doherty, S. Akira, T. B. Rajavashisth, and M. Arditi. 2004. Lack of Toll-like receptor 4 or myeloid differentiation factor 88 reduces atherosclerosis and alters plaque phenotype in mice deficient in apolipoprotein E. Proc. Natl. Acad. Sci. USA 101: 10679-10684.
29. Björkbacka, H., V. V. Kunjathoor, K. J. Moore, S. Koehn, C. M. Ordija, M. A. Lee, T. Means, K. Halmen, A. D. Luster, D. T. Golenbock, and M. W. Freeman. 2004. Reduced atherosclerosis in MyD88-null mice links elevated serum cholesterol levels to activation of innate immunity signaling pathways. Nat. Med. 10: 416-421.
30. Hain, R., H. J. Reif, E. Krause, R. Langebartels, H. Kindl, B. Vornam, W. Wiese, E. Schmelzer, P. H. Schreier, R. H. Stocker, et al. 1993. Disease resistance results from foreign phytoalexin expression in a novel plant. Nature 361: 153-156.
31. Hain, R., B. Bieseler, H. Kindl, G. Schroder, and R. Stocker. 1990. Expression of a stilbene synthase gene in Nicotiana tabacum results in synthesis of the phy-toalexin resveratrol. Plant Mol. Biol. 15: 325-335.
32. Jang, M., L. Cai, G. O. Udeani, K. V. Slowing, C. F. Thomas, C. W. Beecher, H. H. Fong, N. R. Farnsworth, A. D. Kinghorn, R. G. Mehta, et al. 1997. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 275: 218-220.
33. Surh, Y. J. 2003. Cancer chemoprevention with dietary phytochemicals. Nat. Rev. Cancer 3: 768-780.
34. Pervaiz, S. 2003. Resveratrol: from grapevines to mammalian biology. FASEB J. 17: 1975-1985.
35. Bhat, K. P., and J. M. Pezzuto. 2002. Cancer chemopreventive activity of resveratrol. Ann. NY Acad. Sci. 957: 210-229.
36. Karin, M., Y. Yamamoto, and Q. M. Wang. 2004. The IKK NF-κB system: a treasure trove for drug development. Nat. Rev. Drug Discov. 3: 17-26.
37. Holmes-McNary, M., and A. S. Baldwin, Jr. 2000. Chemopreventive properties of trans-resveratrol are associated with inhibition of activation of the ÉêÂkinase. Cancer Res. 60: 3477-3483.
38. Manna, S. K., A. Mukhopadhyay, and B. B. Aggarwal. 2000. Resveratrol suppresses TNF-induced activation of nuclear transcription factors NF-κB, activator protein-1, and apoptosis: potential role of reactive oxygen intermediates and lipid peroxidation. J. Immunol. 164:6509-6519.
39. Li, Z. W., R. C. Ricken, and M. Karin. 2004. Genetic dissection of antigen receptor induced-NF-ê activation. Mol. Immunol 41: 701-714.
40. Lee, S. H., E. Soyoola, P. Chanmugam, S. Hart, W. Sun, H. Zhong, S. Liou, D. Simmons, and D. Hwang. 1992. Selective expression of mitogen-inducible cyclooxygenase in macrophages stimulated with lipopolysaccharide. J. Biol. Chem. 267: 25934-25938.
41. Yamamoto, M., S. Sato, H. Hemmi, K. Hoshino, T. Kaisho, H. Sanjo, O. Takeuchi, M. Sugiyama, M. Okabe, K. Takeda, and S. Akira. 2003. Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science 301: 640-643.
42. Blasi, E., D. Radzioch, L. Merletti, and L. Varesio. 1989. Generation of macrophage cell line from fresh bone marrow cells with a myc/raf recombinant retrovirus. Cancer Biochem. Biophys. 10: 303-317.
43. Sharma, S., B. R. tenOever, N. Grandvaux, G. P. Zhou, R. Lin, and J. Hiscott. 2003. Triggering the Interferon antiviral response through an IKK-related pathway. Science 300: 1148-1151.
44. Hwang, D., B. C. Jang, G. Yu, and M. Boudreau. 1997. Expression of mitogen-inducible cyclooxygenase induced by lipopolysaccharide: mediation through both mitogen-activated protein kinase and NF-κB signaling pathways in macrophages. Biochem. Pharmacol. 54: 87-96.
45. Paik, J. H., J. H. Ju, J. Y. Lee, M. D. Boudreau, and D. H. Hwang. 2000. Two opposing effects of non-steroidal anti-inflammatory drugs on the expression of the inducible cyclooxygenase: mediation through different signaling pathways. J. Biol. Chem. 275: 28173-28179.
46. Lee, J. Y., L. Zhao, H. S. Youn, A. R. Weatherill, R. Tapping, L. Feng, W. H. Lee, K. A. Fitzgerald, and D. H. Hwang. 2004. Saturated fatty acid activates but polyunsaturated fatty acid inhibits Toll-like receptor 2 dimerized with Toll-like receptor 6 or 1, J. Biol. Chem. 279: 16971-16979.
47. Qin, B. Y., C. Liu, S. S. Lam, H. Srinath, R. Delston, J. J. Correia, R. Derynck, and K. Lin. 2003. Crystal structure of IRF-3 reveals mechanism of autoinhibition and virus-induced phosphoactivation. Nat. Struct. Biol. 10: 913-921.
48. Hiscott, J., N. Grandvaux, S. Sharma, B. R. Tenoever, M. J. Servant, and R. Lin. 2003. Convergence of the NF-κB and interferon signaling pathways in the regulation of antiviral defense and apoptosis. Ann. NY Acad. Sci. 1010: 237-248.
49. Meylan, E., K. Burns, K. Hofmann, V. Blancheteau, F. Martinen, M. Kelliher, and J. Tschopp. 2004. RIP1 is an essential mediator of Toll-like receptor 3-induced NF-xB activation. Nat. Immunol. 5: 503-507.
50. Björkbacka, H., K. A. Fitzgerald, F. Huet, X. Li, J. A. Gregory, M. A. Lee, C. M. Ordija, N. E. Dowley, D. T. Golenbock, and M. W. Freeman. 2004. The induction of macrophage gene expression by LPS predominantly utilizes Myd88-independent signaling cascades. Physiol. Genomics 19: 319-330.
51. Karaghiosoff, M., R. Steinbom, P. Kovarik, G. Kriegshauser, M. Baccarini, B. Donabauer, U. Reichart, T. Kolbe, C. Bogdan, T. Leanderson, et al. 2003. Central role for type 1 interferons and Tyk2 in lipopolysaccharide-induced endotoxin shock. Nat. Immunol. 4: 471-477.
52. Tsai, S. H., Y. C. Liang, S. Y. Lin-Shiau, and J. K. Lin. 1999. Suppression of TNFα-mediated NFκB activity by myricetin and other flavonoids through down-regulating the activity of IKK in ECV304 cells. J. Cell. Biochem. 74: 606-615.
53. Murakami, A., K. Matsumoto, K. Koshimizu, and H. Ohigashi. 2003. Effects of selected food factors with chemopreventive properties on combined lipopolysaccharide- and interferon-γ-induced IκB degradation in RAW264.7 macrophages. Cancer Lett. 195: 17-25.
54. Sato, S., M. Sugiyama, M. Yamamoto, Y. Watanabe, T. Kawai, K. Takeda, and S. Akira. 2003. Toll/IL-1 receptor domain-containing adaptor inducing IFN-β (TRIF) associates with TNF receptor-associated factor 6 and TANK-binding kinase 1, and activates two distinct transcription factors, NF-κB and IFN-regulatory factor-3, in the Toll-like receptor signaling. J. Immunol. 171: 4304-4310.
55. Jiang, Z., T. W. Mak, G. Sen, and X. Li. 2004. Toll-like receptor 3-mediated activation of NF-κB and IRF3 diverges at Toll-IL-1 receptor domain-containing adapter inducing IFN-β. Proc. Natl. Acad. Sci. USA 101: 3533-3538.
56. Gohda, J., T. Matsumura, and J. Inoue. 2004. Cutting edge: TNFR-associated factor (TRAF) 6 is essential for MyD88-dependent pathway but not Toll/IL-1 receptor domain-containing adaptor-inducing IFN-β (TRIF)-dependem pathway in TLR signaling, J. Immunol. 173: 2913-2917.
57. Bonnard, M., C. Mirtsos, S. Suzuki, K. Graham, J. Huang, M. Ng, A. Itie, A. Wakeham, A. Shahinian, W. J. Henzel, et al. 2000. Deficiency of T2K leads to apoptotic liver degeneration and impaired NF-κB-dependent gene transcrip-tion. EMBO J. 19: 4976-4985.
58. Howitz, K. T., K. J. Bitterman, H. Y. Cohen, D. W. Lamming, S. Lavu, J. G. Wood, R. E. Zipkin, P. Chung, A. Kisielewski, L. L. Zhang, et al. 2003. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 425: 191-196.
59. Yeung, F., J. E. Hoberg, C. S. Ramsey, M. D. Keller, D. R. Jones, R. A. Frye, and M. W. Mayo. 2004. Modulation of NF-κB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 23: 2369-2380.
60. Ashikawa, K., S. Majumdar, S. Banerjee, A. C. Bharti, S. Shishodia, and B. B. Aggarwal. 2002. Piceatannol inhabits TNF-induced NF-κB activation and NF-κB-mediated gene expression through suppression of IκBa kinase and p65 phosphorylation. J. Immunol. 169: 6490-6497.
61. Mutoh, M., M. Takahashi, K. Fukuda, Y. Matsushima-Hibiya, H. Mutoh, T. Sugimura, and K. Wakabayashi. 2000. Suppression of cyclooxygenase-2 promoter-dependent transcriptional activity in colon cancer cells by chemopreventive agents with a resorcin-type structure. Carcinogenesis 21: 959-963.