TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-β

Nature Immunology

Volumn 9, Issue 4, 2008, Pages 361-368

  Kagan, Jonathan C ^a,c   Su, Tian ^a   Horng, Tiffany ^a,d   Chow, Amy ^a,c,e   Akira, Shizuo ^b   Medzhitov, Ruslan ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b OSAKA UNIVERSITY   (Japan)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d CENTER FOR BLOOD RESEARCH   (United States)

^e ROCHESTER INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; BETA INTERFERON; BINDING PROTEIN; MYELOID DIFFERENTIATION FACTOR 88; TOLL INTERLEUKIN 1 RECEPTOR ADAPTOR PROTEIN; TOLL LIKE RECEPTOR 4; TOLL RECEPTOR ASSOCIATED ACTIVATOR OF INTERFERON; TOLL RECEPTOR ASSOCIATED ACTIVATOR OF INTERFERON RELATED ADAPTOR MOLECULE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN RECOGNITION; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; HUMAN; HUMAN CELL; INNATE IMMUNITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CELL LINE; DOWN-REGULATION; ENDOCYTOSIS; HUMANS; INTERFERON-BETA; INTRACELLULAR FLUID; MEMBRANE GLYCOPROTEINS; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; MYELOID DIFFERENTIATION FACTOR 88; RECEPTORS, INTERLEUKIN-1; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 40949134086     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni1569     Document Type: Article

References (50)

1. Akira, S., Uematsu, S. & Takeuchi, O. Pathogen recognition and innate immunity. Cell 124, 783-801 (2006).
2. Janeway, C.A. Jr & Medzhitov, R. Innate immune recognition. Annu. Rev. Immunol. 20, 197-216 (2002).
3. Hiratani, T. et al. Regulabon at lipopolysaccharide-inducible genes by MyD88 and Toll/IL-1 domain containing adaptor inducing IFN-β. Biochem. Biophys. Res. Commun. 328, 383-392 (2005).
4. Yamamoto, M. et al. Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science 301, 640-643 (2003).
5. Yamamoto, M. et al. TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nat. Immunol. 4, 1144-1150 (2003).
6. Yamamoto, M. et al. Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4. Nature 420, 324-329 (2002).
7. Horng, T., Barton, G.M., Flavell, R.A. & Medzhitov, R. The adaptor molecule TIRAP provides signalling specificity for Toll-like receptors. Nature 420, 329-333 (2002).
8. Barton, G.M., Kagan, J.C. & Medzhitov, R. Intracellular localization of Toll-like receptor 9 prevents recognition of self DNA but facilitates access to viral DNA. Nat. Immunol. 7, 49-56 (2006).
9. Latz, E. et al. TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat. Immunol. 5, 190-198 (2004).
10. Hayashi, F. et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410, 1099-1103 (2001).
11. Toshchakov, V. et al. TLR4, but nut TLR2, mediates IFN-β-induced STAT1α/β-dependent gene expression in macrophages. Nat. Immunol. 3, 392-398 (2002).
12. Alexopoulou, L., Holt, A.C., Medzhitov, R. & Flavell, R.A. Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 413, 732-738 (2001).
13. Lund, J.M. et al. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. USA 101, 5598-5603 (2004).
14. Diebold, S.S., Kaisho, T., Hemmi, H., Akira, S. & Reis e Sousa, C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303, 1529-1531 (2004).
15. Kawai, T. & Akira, S. Antiviral signaling through pattern recognition receptors. J. Biochem. 141, 137-145 (2007).
16. Honda, K. et al. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434, 772-777 (2005).
17. Kawai, T. et al. Interferon-α induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat. Immunol. 5, 1061-1068 (2004).
18. Doyle, S. et al. IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity 17, 251-263 (2002).
19. Oshiumi, H., Matsumoto, M., Funami, K., Akazawa, T. & Seya, T. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-β induction. Nat. Immunol. 4, 161-167 (2003).
20. Barton, G.M. & Medzhitov, R. Toll-like receptor signaling pathways. Science 300, 1524-1525 (2003).
21. Takaoka, A. et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448, 501-505 (2007).
22. Kato, H. et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441, 101-105 (2006).
23. O'Neill, L.A. & Bowie, A.G. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat Rev. Immunol. 7 353-364 (2007).
24. Kagan, J.C. & Medzhitov, R. Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling. Cell 125, 943-955 (2006).
25. Ulrichts, P., Peelman, F., Beyaert, R. & Tavernier, J. MAPPIT analysis of TLR adaptor complexes. FEBS Lett. 581, 629-636 (2007).
26. Oshiumi, H. et al. TIR-containing adapter molecule (TICAM)-2, a bridging adapter recruiting to toll-like receptor 4 TICAM-1 that induces interferon-β. J. Biol. Chem. 278, 49751-49762 (2003).
27. Rowe, D.C. et al. The myristoylation of TRIF-related adaptor molecule is essential for Toll-like receptor 4 signal transduction. Proc. Natl. Acad. Sci. USA 103, 6299-6304 (2006).
28. Husebye, H. et al. Endocytic pathways regulate Toll-like receptor 4 signaling and link innate and adaptive immunity. EMBO J. 25 683-692 (2006).
29. Praefcke, G.J. & McMahon, H.T. The dynamin superfamily: Universal membrane tubulation and fission molecules? Nat. Rev. Mol. Cell Biol. 5, 133-147 (2004).
30. Akashi, S. et al. Lipopolysaccharide interaction with cell surface. Toll-like receptor 4-MD-2 higher affinity than that with MD-2 or CD14. J. Exp. Med. 198, 1035-1042 (2003).
31. Macia, E. et al. Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 10, 839-850 (2006).
32. Boll, W., Ehrlich, M., Collier, R.J. & Kirchhausen, T. Effects of dynamin inactivation on pathways of anthrax toxin uptake. Eur. J. Cell Biol. 83, 281-288 (2004).
33. Damke, H., Baba, T., van der Bliek, A.M. & Schmid, S.L. Clathrin-independent pinocytosis is induced in cells overexpressing a temperature-sensitive mutant of dynamin. J. Cell Biol. 131, 69-80 (1995).
34. Seeger, M. & Payne, G.S. A role for clathrin in the sorting of vacuolar proteins in the Golgi complex of yeast. EMBO J. 11, 2811-2818 (1992).
35. Racoosin, E.L. & Swanson, J.A. Macropinosome maturation and fusion with tubular lysosomes in macrophages. J. Cell Biol. 121, 1011-1020 (1993).
36. Radhakrishna, H. & Donaldson, J.G. ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J. Cell Biol. 139, 49-61 (1997).
37. McDonald, P.H. et al. β-arrestin 2: A receptor-regulated MAPK scaffold for the activation of JNK3. Science 290, 1574-1577 (2000).
38. Sandilands, E., Brunton, V.G. & Frame, M.C. The membrane targeting and spatial activation of Src, Yes and Fyn is influenced by palmitoylation and distinct RhoB/RhoD endosome requirements. J. Cell Sci. 120 2555-2564 (2007).
39. Martin, T.F. Phosphoinositide lipids as signaling molecules: Common themes for signal transduction, cytoskeletal regulation, and membrane trafficking. Annu. Rev. Cell Dev. Biol. 14, 231-264 (1998).
40. Oganesyan, G. et al. Critical role of TRAF3 in the Toll-like receptor-dependent and -independent antiviral response. Nature 439, 208-211 (2006).
41. Hacker, H. et al. Specificity in Toll-like receptor signalling through distinct effector functions of TRAF3 and TRAF6. Nature 439, 204-207 (2006).
42. Rothe, M., Sarma, V., Dixit, V.M. & Goeddel, D.V. TRAF2-mediated activation of NF-κB by TNF receptor 2 and CD40. Science 269 1424-1427 (1995).
43. Botelho, R.J. et al. Localized biphasic changes in phosphatidylinositol-4,5-bisphosphate at sites of phagocytosis. J. Cell Biol. 151, 1353-1368 (2000).
44. Nunez Miguel, R. et al. A dimer of the Toll-like receptor 4 cytoplasmic domain provides a specific scaffold for the recruitment of signalling adaptor proteins. PLoS ONE 2, e788 (2007).
45. Vieira, A.V., Lamaze, C. & Schmid, S.L. Control of EGF receptor signaling by clathrin-mediated endocytosis. Science 274, 2086-2089 (1996).
46. Schneider-Brachert, W. et al. Compartmentalization of TNF receptor 1 signaling: Internalized TNF receptosomes as death signaling vesicles. Immunity 21, 415-428 (2004).
47. Xu, Y., Cheng, G. & Baltimore, D. Targeted disruption of TRAF3 leads to postnatal lethality and defective T-dependent immune responses. Immunity 5, 407-415 (1996).
48. Hostager, B.S., Catlett, I.M. & Bishop, G.A. Recruit pent of CD40 and tumor necrosis factor receptor-associated factors 2 and 3 to membrane microdomains during CD40 signaling. J. Biol. Chem. 275, 15392-15398 (2000).
49. Kagan, J.C. & Roy, C.R. Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat. Cell Biol. 4, 945-954 (2002).
50. Horng, T., Barton, G.M. & Medzhitov, R. TIRAP: An adapter molecule in the Toll signaling pathway. Nat. Immunol. 2, 835-841 (2001).