A role for the adaptor proteins TRAM and TRIF in toll-like receptor 2 signaling

Journal of Biological Chemistry

Volumn 290, Issue 6, 2015, Pages 3209-3222

  Nilsen, Nadra J ^a   Vladimer, Gregory I ^c   Stenvik, Jørgen ^a   Orning, M Pontus A ^a,b   Zeid Kilani, Maria V ^a   Bugge, Marit ^a   Bergstroem, Bjarte ^a   Conlon, Joseph ^b   Husebye, Harald ^a   Hise, Amy G ^a   Fitzgerald, Katherine A ^a,b   Espevik, Terje ^a   Lien, Egil ^a,b,d  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Program in Innate Immunity Division of Infectious Diseases   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; CHEMICAL ACTIVATION; GLYCOPROTEINS; INTERFERONS; LIPIDS; LIPOPROTEINS; MOLECULAR BIOLOGY; PROTEINS; SIGNAL TRANSDUCTION; SIGNALING;

ADAPTOR PROTEINS; INNATE IMMUNITY; INTERFERON REGULATORY FACTORS; INTRACELLULAR COMPARTMENTS; LIPOPOLYSACCHARIDES; NOVEL FUNCTIONS; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTORS;

RAILROAD ROLLING STOCK;

BETA INTERFERON; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 1 RECEPTOR; KINASE TBK 1; LIPOPOLYSACCHARIDE; LIPOPROTEIN; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MYELOID DIFFERENTIATION FACTOR 88; PHOSPHOTRANSFERASE; POLYINOSINIC POLYCYTIDYLIC ACID; RANTES; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 2; UNCLASSIFIED DRUG; INTERLEUKIN RECEPTOR; IRF1 PROTEIN, MOUSE; IRF3 PROTEIN, MOUSE; MYD88 PROTEIN, MOUSE; PROTEIN SERINE THREONINE KINASE; TBK1 PROTEIN, MOUSE; TICAM-1 PROTEIN, MOUSE; TIRP PROTEIN, MOUSE; TLR2 PROTEIN, MOUSE; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENDOCYTOSIS; ENDOSOME; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; INNATE IMMUNITY; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROVOCATION TEST; SIGNAL TRANSDUCTION; UPREGULATION; AGONISTS; ANIMAL; CELL CULTURE; GENETICS; HEK293 CELL LINE; METABOLISM;

BACTERIA (MICROORGANISMS);

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CELLS, CULTURED; CHEMOKINE CCL4; CHEMOKINE CCL5; ENDOCYTOSIS; ENDOSOMES; HEK293 CELLS; HUMANS; INTERFERON REGULATORY FACTOR-1; INTERFERON REGULATORY FACTOR-3; INTERFERON-BETA; LIPOPOLYSACCHARIDES; MACROPHAGES, PERITONEAL; MICE; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, INTERLEUKIN; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2;

EID: 84922311613     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.593426     Document Type: Article

References (50)

1. Kawai, T., and Akira, S. (2007) TLR signaling. Semin. Immunol. 19, 24-32
2. Kawai, T., and Akira, S. (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11, 373-384
3. Lien, E., Sellati, T. J., Yoshimura, A., Flo, T. H., Rawadi, G., Finberg, R. W., Carroll, J. D., Espevik, T., Ingalls, R. R., Radolf, J. D., and Golenbock, D. T. (1999) Toll-like receptor 2 functions as a pattern recognition receptor for diverse bacterial products. J. Biol. Chem. 274, 33419-33425
4. Brightbill, H. D., Libraty, D. H., Krutzik, S. R., Yang, R. B., Belisle, J. T., Bleharski, J. R., Maitland, M., Norgard, M. V., Plevy, S. E., Smale, S. T., Brennan, P. J., Bloom, B. R., Godowski, P. J., and Modlin, R. L. (1999) Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science 285, 732-736
5. Aliprantis, A. O., Yang, R. B., Mark, M. R., Suggett, S., Devaux, B., Radolf, J. D., Klimpel, G. R., Godowski, P., and Zychlinsky, A. (1999) Cell activation and apoptosis by bacterial lipoproteins through toll-like receptor-2. Science 285, 736-739
6. Kang, D. C., Gopalkrishnan, R. V., Wu, Q., Jankowsky, E., Pyle, A. M., and Fisher, P. B. (2002) mda-5: An interferon-inducible putative RNA helicase with double-stranded RNA-dependent ATPase activity and melanoma growth-suppressive properties. Proc. Natl. Acad. Sci. U.S.A. 99, 637-642
7. Kato, H., Takeuchi, O., Sato, S., Yoneyama, M., Yamamoto, M., Matsui, K., Uematsu, S., Jung, A., Kawai, T., Ishii, K. J., Yamaguchi, O., Otsu, K., Tsujimura, T., Koh, C. S., Reis e Sousa, C., Matsuura, Y., Fujita, T., and Akira, S. (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441, 101-105
8. Yoneyama, M., Kikuchi, M., Natsukawa, T., Shinobu, N., Imaizumi, T., Miyagishi, M., Taira, K., Akira, S., and Fujita, T. (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5, 730-737
9. Fitzgerald, K. A., Rowe, D. C., Barnes, B. J., Caffrey, D. R., Visintin, A., Latz, E., Monks, B., Pitha, P. M., and Golenbock, D. T. (2003) LPS-TLR4 signaling to IRF-3/7 and NF-κB involves the toll adapters TRAM and TRIF. J. Exp. Med. 198, 1043-1055
10. Hoebe, K., Janssen, E. M., Kim, S. O., Alexopoulou, L., Flavell, R. A., Han, J., and Beutler, B. (2003) Upregulation of co-stimulatory molecules induced by lipopolysaccharide and double-strandedRNAoccurs by Trif-dependent and Trif-independent pathways. Nat. Immunol. 4, 1223-1229
11. Hirschfield, G. M., Herbert, J., Kahan, M. C., and Pepys, M. B. (2003) Human C-reactive protein does not protect against acute lipopolysaccharide challenge in mice. J. Immunol. 171, 6046-6051
12. Montminy, S. W., Khan, N., McGrath, S., Walkowicz, M. J., Sharp, F., Conlon, J. E., Fukase, K., Kusumoto, S., Sweet, C., Miyake, K., Akira, S., Cotter, R. J., Goguen, J. D., and Lien, E. (2006) Virulence factors of Yersinia pestis are overcome by a strong lipopolysaccharide response. Nat. Immunol. 7, 1066-1073
13. Morath, S., Geyer, A., and Hartung, T. (2001) Structure-function relationship of cytokine induction by lipoteichoic acid from Staphylococcus aureus. J. Exp. Med. 193, 393-397
14. Nilsen, N., Nonstad, U., Khan, N., Knetter, C. F., Akira, S., Sundan, A., Espevik, T., and Lien, E. (2004) Lipopolysaccharide and double-stranded RNA up-regulate toll-like receptor 2 independently of myeloid differentiation factor 88. J. Biol. Chem. 279, 39727-39735
15. Latz, E., Visintin, A., Lien, E., Fitzgerald, K. A., Monks, B. G., Kurt-Jones, E. A., Golenbock, D. T., and Espevik, T. (2002) Lipopolysaccharide rapidly traffics to and from the Golgi apparatus with the toll-like receptor 4-MD-2-CD14 complex in a process that is distinct from the initiation of signal transduction. J. Biol. Chem. 277, 47834-47843
16. Heine, H., Kirschning, C. J., Lien, E., Monks, B. G., Rothe, M., and Golenbock, D. T. (1999) Cutting edge: cells that carry A null allele for toll-like receptor 2 are capable of responding to endotoxin. J. Immunol. 162, 6971-6975
17. Fitzgerald, K. A., McWhirter, S. M., Faia, K. L., Rowe, D. C., Latz, E., Golenbock, D. T., Coyle, A. J., Liao, S. M., and Maniatis, T. (2003) IKKε and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4, 491-496
18. Yamamoto, M., Sato, S., Mori, K., Hoshino, K., Takeuchi, O., Takeda, K., and Akira, S. (2002) Cutting edge: a novel Toll/IL-1 receptor domaincontaining adapter that preferentially activates the IFN-β promoter in the Toll-like receptor signaling. J. Immunol. 169, 6668-6672
19. McBride, H. M., Rybin, V., Murphy, C., Giner, A., Teasdale, R., and Zerial, M. (1999) Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and syntaxin 13. Cell 98, 377-386
20. Barabitskaja, O., Foulke, J. S., Jr., Pati, S., Bodor, J., and Reitz, M. S., Jr. (2006) Suppression of MIP-1β transcription in human T cells is regulated by inducible cAMP early repressor (ICER). J. Leukocyte Biol. 79, 378-387
21. Adachi, O., Kawai, T., Takeda, K., Matsumoto, M., Tsutsui, H., Sakagami, M., Nakanishi, K., and Akira, S. (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9, 143-150
22. Takeuchi, O., Kawai, T., Sanjo, H., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., Takeda, K., and Akira, S. (1999) TLR6: A novel member of an expanding toll-like receptor family. Gene 231, 59-65
23. Yamamoto, M., Sato, S., Hemmi, H., Sanjo, H., Uematsu, S., Kaisho, T., Hoshino, K., Takeuchi, O., Kobayashi, M., Fujita, T., Takeda, K., and Akira, S. (2002) Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4. Nature 420, 324-329
24. Yamamoto, M., Sato, S., Hemmi, H., Hoshino, K., Kaisho, T., Sanjo, H., Takeuchi, O., Sugiyama, M., Okabe, M., Takeda, K., and Akira, S. (2003) Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 301, 640-643
25. Hoebe, K., Du, X., Georgel, P., Janssen, E., Tabeta, K., Kim, S. O., Goode, J., Lin, P., Mann, N., Mudd, S., Crozat, K., Sovath, S., Han, J., and Beutler, B. (2003) Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 424, 743-748
26. Bonnard, M., Mirtsos, C., Suzuki, S., Graham, K., Huang, J., Ng, M., Itié, A., Wakeham, A., Shahinian, A., Henzel, W. J., Elia, A. J., Shillinglaw, W., Mak, T. W., Cao, Z., and Yeh, W. C. (2000) Deficiency of T2K leads to apoptotic liver degeneration and impaired NF-κB-dependent gene transcription. EMBO J. 19, 4976-4985
27. Halle, A., Hornung, V., Petzold, G. C., Stewart, C. R., Monks, B. G., Reinheckel, T., Fitzgerald, K. A., Latz, E., Moore, K. J., and Golenbock, D. T. (2008) The NALP3 inflammasome is involved in the innate immune response to amyloid-β. Nat. Immunol. 9, 857-865
28. Roberson, S. M., and Walker, W. S. (1988) Immortalization of cloned mouse splenic macrophages with a retrovirus containing the v-raf/mil and v-myc oncogenes. Cell. Immunol. 116, 341-351
29. Wang, Y. C., Zhou, Y., Fang, H., Lin, S., Wang, P. F., Xiong, R. P., Chen, J., Xiong, X. Y., Lv, F. L., Liang, Q. L., and Yang, Q. W. (2014) Toll-like receptor 2/4 heterodimer mediates inflammatory injury in intracerebral hemorrhage. Ann. Neurol. 75, 876-889
30. Nilsen, N. J., Deininger, S., Nonstad, U., Skjeldal, F., Husebye, H., Rodionov, D., von Aulock, S., Hartung, T., Lien, E., Bakke, O., and Espevik, T. (2008) Cellular trafficking of lipoteichoic acid and Toll-like receptor 2 in relation to signaling: role of CD14 and CD36. J. Leukocyte Biol. 84, 280-291
31. Génin, P., Algarté, M., Roof, P., Lin, R., and Hiscott, J. (2000) Regulation of RANTES chemokine gene expression requires cooperativity between NF-κB and IFN-regulatory factor transcription factors. J. Immunol. 164, 5352-5361
32. Lin, R., Heylbroeck, C., Genin, P., Pitha, P. M., and Hiscott, J. (1999) Essential role of interferon regulatory factor 3 in direct activation of RANTES chemokine transcription. Mol. Cell. Biol. 19, 959-966
33. Kawai, T., Takeuchi, O., Fujita, T., Inoue, J., Mühlradt, P. F., Sato, S., Hoshino, K., and Akira, S. (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
34. Wathelet, M. G., Lin, C. H., Parekh, B. S., Ronco, L. V., Howley, P. M., and Maniatis, T. (1998) Virus infection induces the assembly of coordinately activated transcription factors on the IFN-β enhancer in vivo. Mol. Cell 1, 507-518
35. Yang, H., Lin, C. H., Ma, G., Orr, M., Baffi, M. O., and Wathelet, M. G. (2002) Transcriptional activity of interferon regulatory factor (IRF)-3 depends on multiple protein-protein interactions. Eur. J. Biochem./FEBS 269, 6142-6151
36. Colonna, M. (2007) TLR pathways and IFN-regulatory factors: to each its own. Eur. J. Immunol. 37, 306-309
37. Schmitz, F., Heit, A., Guggemoos, S., Krug, A., Mages, J., Schiemann, M., Adler, H., Drexler, I., Haas, T., Lang, R., and Wagner, H. (2007) Interferon-regulatory-factor 1 controls Toll-like receptor 9-mediated IFN-β production in myeloid dendritic cells. Eur. J. Immunol. 37, 315-327
38. McWhirter, S. M., Barbalat, R., Monroe, K. M., Fontana, M. F., Hyodo, M., Joncker, N. T., Ishii, K. J., Akira, S., Colonna, M., Chen, Z. J., Fitzgerald, K. A., Hayakawa, Y., and Vance, R. E. (2009) A host type I interferon response is induced by cytosolic sensing of the bacterial second messenger cyclic-di-GMP. J. Exp. Med. 206, 1899-1911
39. Gatot, J. S., Gioia, R., Chau, T. L., Patrascu, F., Warnier, M., Close, P., Chapelle, J. P., Muraille, E., Brown, K., Siebenlist, U., Piette, J., Dejardin, E., and Chariot, A. (2007) Lipopolysaccharide-mediated interferon regulatory factor activation involves TBK1-IKKε-dependent Lys(63)-linked polyubiquitination and phosphorylation of TANK/I-TRAF. J. Biol. Chem. 282, 31131-31146
40. Solis, M., Romieu-Mourez, R., Goubau, D., Grandvaux, N., Mesplede, T., Julkunen, I., Nardin, A., Salcedo, M., and Hiscott, J. (2007) Involvement of TBK1 and IKKε in lipopolysaccharide-induced activation of the interferon response in primary human macrophages. Eur. J. Immunol. 37, 528-539
41. Barbalat, R., Lau, L., Locksley, R. M., and Barton, G. M. (2009) Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat. Immunol. 10, 1200-1207
42. Hirotani, T., Yamamoto, M., Kumagai, Y., Uematsu, S., Kawase, I., Takeuchi, O., and Akira, S. (2005) Regulation of lipopolysaccharide-inducible genes by MyD88 and Toll/IL-1 domain containing adaptor inducing IFN-β. Biochem. Biophys. Res. Commun. 328, 383-392
43. Dietrich, N., Lienenklaus, S., Weiss, S., and Gekara, N. O. (2010) Murine toll-like receptor 2 activation induces type I interferon responses from endolysosomal compartments. PLoS One 5, e10250
44. Rowe, D. C., McGettrick, A. F., Latz, E., Monks, B. G., Gay, N. J., Yamamoto, M., Akira, S., O'Neill, L. A., Fitzgerald, K. A., and Golenbock, D. T. (2006) The myristoylation of TRIF-related adaptor molecule is essential for Toll-like receptor 4 signal transduction. Proc. Natl. Acad. Sci. U.S.A. 103, 6299-6304
45. Schjetne, K. W., Thompson, K. M., Nilsen, N., Flo, T. H., Fleckenstein, B., Iversen, J. G., Espevik, T., and Bogen, B. (2003) Cutting edge: link between innate and adaptive immunity: Toll-like receptor 2 internalizes antigen for presentation to CD4+ T cells and could be an efficient vaccine target. J. Immunol. 171, 32-36
46. Kagan, J. C., Su, T., Horng, T., Chow, A., Akira, S., and Medzhitov, R. (2008) TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-β. Nat. Immunol. 9, 361-368
47. Petnicki-Ocwieja, T., Chung, E., Acosta, D. I., Ramos, L. T., Shin, O. S., Ghosh, S., Kobzik, L., Li, X., and Hu, L. T. (2013) TRIF mediates Toll-like receptor 2-dependent inflammatory responses to Borrelia burgdorferi. Infect. Immun. 81, 402-410
48. Husebye, H., Halaas, Ø., Stenmark, H., Tunheim, G., Sandanger, Ø., Bogen, B., Brech, A., Latz, E., and Espevik, T. (2006) Endocytic pathways regulate Toll-like receptor 4 signaling and link innate and adaptive immunity. EMBO J. 25, 683-692
49. Choi, Y. J., Im, E., Chung, H. K., Pothoulakis, C., and Rhee, S. H. (2010) TRIF mediates Toll-like receptor 5-induced signaling in intestinal epithelial cells. J. Biol. Chem. 285, 37570-37578
50. Aubry, C., Corr, S. C., Wienerroither, S., Goulard, C., Jones, R., Jamieson, A. M., Decker, T., O'Neill, L. A., Dussurget, O., and Cossart, P. (2012) Both TLR2 and TRIF contribute to interferon-β production during Listeria infection. PLoS One 7, e33299