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LPS-TLR4 Signaling to IRF-3/7 and NF-B Involves the Toll Adapters TRAM and TRIF

Katherine A. Fitzgerald¹, Daniel C. Rowe¹, Betsy J. Barnes², Daniel R. Caffrey³, Alberto Visintin¹, Eicke Latz¹, Brian Monks¹, Paula M. Pitha² and Douglas T. Golenbock¹

¹ Division of Infectious Disease and Immunology, Department of Medicine, The University of Massachusetts Medical School, Worcester, MA 01605
² The Sidney Kimmel Comprehensive Cancer Center, Oncology Department, Johns Hopkins School of Medicine, Baltimore, MD 21231
³ Pfizer Discovery Technology Center, Cambridge, MA 02139

Address correspondence to Douglas Golenbock, Div. of Infectious Disease and Immunology, Dept. of Medicine, The University of Massachusetts Medical School, Worcester, MA 01605. Phone: (508) 856-5980; Fax: (508) 856-5463; email: Douglas.Golenbock{at}umassmed.edu

Toll–IL-1–resistance (TIR) domain–containing adaptor-inducing IFN-ß (TRIF)–related adaptor molecule (TRAM) is the fourth TIR domain–containing adaptor protein to be described that participates in Toll receptor signaling. Like TRIF, TRAM activates interferon regulatory factor (IRF)-3, IRF-7, and NF-B-dependent signaling pathways. Toll-like receptor (TLR)3 and 4 activate these pathways to induce IFN-/ß, regulated on activation, normal T cell expressed and secreted (RANTES), and interferon–inducible protein 10 (IP-10) expression independently of the adaptor protein myeloid differentiation factor 88 (MyD88). Dominant negative and siRNA studies performed here demonstrate that TRIF functions downstream of both the TLR3 (dsRNA) and TLR4 (LPS) signaling pathways, whereas the function of TRAM is restricted to the TLR4 pathway. TRAM interacts with TRIF, MyD88 adaptor–like protein (Mal)/TIRAP, and TLR4 but not with TLR3. These studies suggest that TRIF and TRAM both function in LPS-TLR4 signaling to regulate the MyD88-independent pathway during the innate immune response to LPS.

Key Words: innate immunity • endotoxin • interferon • signal transduction • host defense

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• Schneeman, T. A., Bruno, M. E. C., Schjerven, H., Johansen, F.-E., Chady, L., Kaetzel, C. S. (2005). Regulation of the Polymeric Ig Receptor by Signaling through TLRs 3 and 4: Linking Innate and Adaptive Immune Responses. J. Immunol. 175: 376-384 [Abstract] [Full Text]  
• Toshchakov, V. U., Basu, S., Fenton, M. J., Vogel, S. N. (2005). Differential Involvement of BB Loops of Toll-IL-1 Resistance (TIR) Domain-Containing Adapter Proteins in TLR4- versus TLR2-Mediated Signal Transduction. J. Immunol. 175: 494-500 [Abstract] [Full Text]  
• Qin, J., Qian, Y., Yao, J., Grace, C., Li, X. (2005). SIGIRR Inhibits Interleukin-1 Receptor- and Toll-like Receptor 4-mediated Signaling through Different Mechanisms. J. Biol. Chem. 280: 25233-25241 [Abstract] [Full Text]  
• Cho, H.-Y., Jedlicka, A. E., Clarke, R., Kleeberger, S. R. (2005). Role of Toll-like receptor-4 in genetic susceptibility to lung injury induced by residual oil fly ash. Physiol. Genomics 22: 108-117 [Abstract] [Full Text]  
• Miller, Y. I., Viriyakosol, S., Worrall, D. S., Boullier, A., Butler, S., Witztum, J. L. (2005). Toll-Like Receptor 4-Dependent and -Independent Cytokine Secretion Induced by Minimally Oxidized Low-Density Lipoprotein in Macrophages. Arterioscler. Thromb. Vasc. Bio. 25: 1213-1219 [Abstract] [Full Text]  
• Ferreon, J. C., Ferreon, A. C. M., Li, K., Lemon, S. M. (2005). Molecular Determinants of TRIF Proteolysis Mediated by the Hepatitis C Virus NS3/4A Protease. J. Biol. Chem. 280: 20483-20492 [Abstract] [Full Text]  
• Hasan, U. A., Trinchieri, G., Vlach, J. (2005). Toll-like Receptor Signaling Stimulates Cell Cycle Entry and Progression in Fibroblasts. J. Biol. Chem. 280: 20620-20627 [Abstract] [Full Text]  
• Zughaier, S. M., Zimmer, S. M., Datta, A., Carlson, R. W., Stephens, D. S. (2005). Differential Induction of the Toll-Like Receptor 4-MyD88-Dependent and -Independent Signaling Pathways by Endotoxins. Infect. Immun. 73: 2940-2950 [Abstract] [Full Text]  
• Conzelmann, K.-K. (2005). Transcriptional Activation of Alpha/Beta Interferon Genes: Interference by Nonsegmented Negative-Strand RNA Viruses. J. Virol. 79: 5241-5248 [Full Text]  
• Fukata, M., Michelsen, K. S., Eri, R., Thomas, L. S., Hu, B., Lukasek, K., Nast, C. C., Lechago, J., Xu, R., Naiki, Y., Soliman, A., Arditi, M., Abreu, M. T. (2005). Toll-like receptor-4 is required for intestinal response to epithelial injury and limiting bacterial translocation in a murine model of acute colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 288: G1055-G1065 [Abstract] [Full Text]  
• Schoenemeyer, A., Barnes, B. J., Mancl, Margo. E., Latz, E., Goutagny, N., Pitha, P. M., Fitzgerald, K. A., Golenbock, D. T. (2005). The Interferon Regulatory Factor, IRF5, Is a Central Mediator of Toll-like Receptor 7 Signaling. J. Biol. Chem. 280: 17005-17012 [Abstract] [Full Text]  
• Kaiser, W. J., Offermann, M. K. (2005). Apoptosis Induced by the Toll-Like Receptor Adaptor TRIF Is Dependent on Its Receptor Interacting Protein Homotypic Interaction Motif. J. Immunol. 174: 4942-4952 [Abstract] [Full Text]  
• Breiman, A., Grandvaux, N., Lin, R., Ottone, C., Akira, S., Yoneyama, M., Fujita, T., Hiscott, J., Meurs, E. F. (2005). Inhibition of RIG-I-Dependent Signaling to the Interferon Pathway during Hepatitis C Virus Expression and Restoration of Signaling by IKK{varepsilon}. J. Virol. 79: 3969-3978 [Abstract] [Full Text]  
• Stack, J., Haga, I. R., Schroder, M., Bartlett, N. W., Maloney, G., Reading, P. C., Fitzgerald, K. A., Smith, G. L., Bowie, A. G. (2005). Vaccinia virus protein A46R targets multiple Toll-like-interleukin-1 receptor adaptors and contributes to virulence. JEM 201: 1007-1018 [Abstract] [Full Text]  
• Pulendran, B. (2005). Variegation of the Immune Response with Dendritic Cells and Pathogen Recognition Receptors. J. Immunol. 174: 2457-2465 [Abstract] [Full Text]  
• Hasan, U., Chaffois, C., Gaillard, C., Saulnier, V., Merck, E., Tancredi, S., Guiet, C., Briere, F., Vlach, J., Lebecque, S., Trinchieri, G., Bates, E. E. M. (2005). Human TLR10 Is a Functional Receptor, Expressed by B Cells and Plasmacytoid Dendritic Cells, Which Activates Gene Transcription through MyD88. J. Immunol. 174: 2942-2950 [Abstract] [Full Text]  
• Li, K., Foy, E., Ferreon, J. C., Nakamura, M., Ferreon, A. C. M., Ikeda, M., Ray, S. C., Gale, M. Jr., Lemon, S. M. (2005). Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF. Proc. Natl. Acad. Sci. USA 102: 2992-2997 [Abstract] [Full Text]  

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