Intracellular Toll-like Receptors

Immunity

Volumn 32, Issue 3, 2010, Pages 305-315

  Blasius, Amanda L ^a   Beutler, Bruce ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CPG OLIGODEOXYNUCLEOTIDE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FC RECEPTOR; GLYCOPROTEIN GP 96; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE; MYELOID DIFFERENTIATION FACTOR 88; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6;

AUTOIMMUNITY; CELLULAR DISTRIBUTION; CYTOKINE PRODUCTION; DENDRITIC CELL; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; HOST RESISTANCE; INFECTION RESISTANCE; INTERNALIZATION; NONHUMAN; PHAGOCYTOSIS; PINOCYTOSIS; PRIORITY JOURNAL; RETROPOSON; REVIEW; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; VIRUS DETECTION;

ANIMALS; CYTOKINES; ENDOCYTOSIS; HUMANS; INTRACELLULAR SPACE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 77949940198     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2010.03.012     Document Type: Review

References (115)

1. Asagiri M., Hirai T., Kunigami T., Kamano S., Gober H.J., Okamoto K., Nishikawa K., Latz E., Golenbock D.T., Aoki K., et al. Cathepsin K-dependent toll-like receptor 9 signaling revealed in experimental arthritis. Science 2008, 319:624-627.
2. Bafica A., Santiago H.C., Goldszmid R., Ropert C., Gazzinelli R.T., Sher A. Cutting edge: TLR9 and TLR2 signaling together account for MyD88-dependent control of parasitemia in Trypanosoma cruzi infection. J. Immunol. 2006, 177:3515-3519.
3. Barbalat R., Lau L., Locksley R.M., Barton G.M. Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat. Immunol. 2009, 10:1200-1207.
4. 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. 2006, 7:49-56.
5. Bell J.K., Botos I., Hall P.R., Askins J., Shiloach J., Segal D.M., Davies D.R. The molecular structure of the Toll-like receptor 3 ligand-binding domain. Proc. Natl. Acad. Sci. USA 2005, 102:10976-10980.
6. Beutler B., Moresco E.M. The forward genetic dissection of afferent innate immunity. Curr. Top. Microbiol. Immunol. 2008, 321:3-26.
7. Beutler B., Jiang Z., Georgel P., Crozat K., Croker B., Rutschmann S., Du X., Hoebe K. Genetic analysis of host resistance: Toll-like receptor signaling and immunity at large. Annu. Rev. Immunol. 2006, 24:353-389.
8. Boulé M.W., Broughton C., Mackay F., Akira S., Marshak-Rothstein A., Rifkin I.R. Toll-like receptor 9-dependent and -independent dendritic cell activation by chromatin-immunoglobulin G complexes. J. Exp. Med. 2004, 199:1631-1640.
9. Brinkmann M.M., Spooner E., Hoebe K., Beutler B., Ploegh H.L., Kim Y.M. The interaction between the ER membrane protein UNC93B and TLR3, 7, and 9 is crucial for TLR signaling. J. Cell Biol. 2007, 177:265-275.
10. Chockalingam A., Brooks J.C., Cameron J.L., Blum L.K., Leifer C.A. TLR9 traffics through the Golgi complex to localize to endolysosomes and respond to CpG DNA. Immunol. Cell Biol. 2009, 87:209-217.
11. Conner S.D., Schmid S.L. Regulated portals of entry into the cell. Nature 2003, 422:37-44.
12. Crow Y.J., Hayward B.E., Parmar R., Robins P., Leitch A., Ali M., Black D.N., van Bokhoven H., Brunner H.G., Hamel B.C., et al. Mutations in the gene encoding the 3′-5′ DNA exonuclease TREX1 cause Aicardi-Goutières syndrome at the AGS1 locus. Nat. Genet. 2006, 38:917-920.
13. Di Domizio J., Blum A., Gallagher-Gambarelli M., Molens J.P., Chaperot L., Plumas J. TLR7 stimulation in human plasmacytoid dendritic cells leads to the induction of early IFN-inducible genes in the absence of type I IFN. Blood 2009, 114:1794-1802.
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 2004, 303:1529-1531.
15. Ding C., Cai Y., Marroquin J., Ildstad S.T., Yan J. Plasmacytoid dendritic cells regulate autoreactive B cell activation via soluble factors and in a cell-to-cell contact manner. J. Immunol. 2009, 183:7140-7149.
16. Dunne A., Ejdeback M., Ludidi P.L., O'Neill L.A., Gay N.J. Structural complementarity of Toll/Interleukin1 receptor identity regions in toll-like receptors and the adaptors Mal and MyD88. J. Biol. Chem. 2003, 278:41443-41451.
17. Eberle F., Sirin M., Binder M., Dalpke A.H. Bacterial RNA is recognized by different sets of immunoreceptors. Eur. J. Immunol. 2009, 39:2537-2547.
18. Ermolaeva M.A., Michallet M.C., Papadopoulou N., Utermöhlen O., Kranidioti K., Kollias G., Tschopp J., Pasparakis M. Function of TRADD in tumor necrosis factor receptor 1 signaling and in TRIF-dependent inflammatory responses. Nat. Immunol. 2008, 9:1037-1046.
19. Ewald S.E., Lee B.L., Lau L., Wickliffe K.E., Shi G.P., Chapman H.A., Barton G.M. The ectodomain of Toll-like receptor 9 is cleaved to generate a functional receptor. Nature 2008, 456:658-662.
20. Ferrandon D., Imler J.L., Hetru C., Hoffmann J.A. The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat. Rev. Immunol. 2007, 7:862-874.
21. Fitzgerald K.A., McWhirter S.M., Faia K.L., Rowe D.C., Latz E., Golenbock D.T., Coyle A.J., Liao S.M., Maniatis T. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 2003, 4:491-496.
22. Fukui R., Saitoh S., Matsumoto F., Kozuka-Hata H., Oyama M., Tabeta K., Beutler B., Miyake K. Unc93B1 biases Toll-like receptor responses to nucleic acid in dendritic cells toward DNA- but against RNA-sensing. J. Exp. Med. 2009, 206:1339-1350.
23. Funami K., Matsumoto M., Oshiumi H., Akazawa T., Yamamoto A., Seya T. The cytoplasmic 'linker region' in Toll-like receptor 3 controls receptor localization and signaling. Int. Immunol. 2004, 16:1143-1154.
24. Gavin A.L., Hoebe K., Duong B., Ota T., Martin C., Beutler B., Nemazee D. Adjuvant-enhanced antibody responses in the absence of toll-like receptor signaling. Science 2006, 314:1936-1938.
25. Groves E., Dart A.E., Covarelli V., Caron E. Molecular mechanisms of phagocytic uptake in mammalian cells. Cell. Mol. Life Sci. 2008, 65:1957-1976.
26. Guiducci C., Ott G., Chan J.H., Damon E., Calacsan C., Matray T., Lee K.D., Coffman R.L., Barrat F.J. Properties regulating the nature of the plasmacytoid dendritic cell response to Toll-like receptor 9 activation. J. Exp. Med. 2006, 203:1999-2008.
27. Haas T., Metzger J., Schmitz F., Heit A., Müller T., Latz E., Wagner H. The DNA sugar backbone 2′ deoxyribose determines toll-like receptor 9 activation. Immunity 2008, 28:315-323.
28. Häcker H., Mischak H., Miethke T., Liptay S., Schmid R., Sparwasser T., Heeg K., Lipford G.B., Wagner H. CpG-DNA-specific activation of antigen-presenting cells requires stress kinase activity and is preceded by non-specific endocytosis and endosomal maturation. EMBO J. 1998, 17:6230-6240.
29. Häcker H., Redecke V., Blagoev B., Kratchmarova I., Hsu L.C., Wang G.G., Kamps M.P., Raz E., Wagner H., Häcker G., et al. Specificity in Toll-like receptor signalling through distinct effector functions of TRAF3 and TRAF6. Nature 2006, 439:204-207.
30. Heil F., Hemmi H., Hochrein H., Ampenberger F., Kirschning C., Akira S., Lipford G., Wagner H., Bauer S. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 2004, 303:1526-1529.
31. Hoebe K., Du X., Georgel P., Janssen E., Tabeta K., Kim S.O., Goode J., Lin P., Mann N., Mudd S., et al. Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 2003, 424:743-748.
32. Hoebe K., Georgel P., Rutschmann S., Du X., Mudd S., Crozat K., Sovath S., Shamel L., Hartung T., Zähringer U., Beutler B. CD36 is a sensor of diacylglycerides. Nature 2005, 433:523-527.
33. Honda K., Ohba Y., Yanai H., Negishi H., Mizutani T., Takaoka A., Taya C., Taniguchi T. Spatiotemporal regulation of MyD88-IRF-7 signalling for robust type-I interferon induction. Nature 2005, 434:1035-1040.
34. Honda K., Yanai H., Negishi H., Asagiri M., Sato M., Mizutani T., Shimada N., Ohba Y., Takaoka A., Yoshida N., Taniguchi T. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 2005, 434:772-777.
35. Hornung V., Guenthner-Biller M., Bourquin C., Ablasser A., Schlee M., Uematsu S., Noronha A., Manoharan M., Akira S., de Fougerolles A., et al. Sequence-specific potent induction of IFN-alpha by short interfering RNA in plasmacytoid dendritic cells through TLR7. Nat. Med. 2005, 11:263-270.
36. Husebye H., Halaas O., Stenmark H., Tunheim G., Sandanger O., Bogen B., Brech A., Latz E., Espevik T. Endocytic pathways regulate Toll-like receptor 4 signaling and link innate and adaptive immunity. EMBO J. 2006, 25:683-692.
37. Jiang Z., Georgel P., Li C., Choe J., Crozat K., Rutschmann S., Du X., Bigby T., Mudd S., Sovath S., et al. Details of Toll-like receptor:adapter interaction revealed by germ-line mutagenesis. Proc. Natl. Acad. Sci. USA 2006, 103:10961-10966.
38. Jurk M., Heil F., Vollmer J., Schetter C., Krieg A.M., Wagner H., Lipford G., Bauer S. Human TLR7 or TLR8 independently confer responsiveness to the antiviral compound R-848. Nat. Immunol. 2002, 3:196-200.
39. Kagan J.C., Su T., Horng T., Chow A., Akira S., Medzhitov R. TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-beta. Nat. Immunol. 2008, 9:361-368.
40. Kawagoe T., Sato S., Matsushita K., Kato H., Matsui K., Kumagai Y., Saitoh T., Kawai T., Takeuchi O., Akira S. Sequential control of Toll-like receptor-dependent responses by IRAK1 and IRAK2. Nat. Immunol. 2008, 9:581-582.
41. Kawai T., Akira S. The roles of TLRs, RLRs and NLRs in pathogen recognition. Int. Immunol. 2009, 21:317-337.
42. Kawai T., Sato S., Ishii K.J., Coban C., Hemmi H., Yamamoto M., Terai K., Matsuda M., Inoue J., Uematsu S., et al. Interferon-alpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat. Immunol. 2004, 5:1061-1068.
43. Kawane K., Ohtani M., Miwa K., Kizawa T., Kanbara Y., Yoshioka Y., Yoshikawa H., Nagata S. Chronic polyarthritis caused by mammalian DNA that escapes from degradation in macrophages. Nature 2006, 443:998-1002.
44. Kerkmann M., Costa L.T., Richter C., Rothenfusser S., Battiany J., Hornung V., Johnson J., Englert S., Ketterer T., Heckl W., et al. Spontaneous formation of nucleic acid-based nanoparticles is responsible for high interferon-alpha induction by CpG-A in plasmacytoid dendritic cells. J. Biol. Chem. 2005, 280:8086-8093.
45. Kim Y.M., Brinkmann M.M., Paquet M.E., Ploegh H.L. UNC93B1 delivers nucleotide-sensing toll-like receptors to endolysosomes. Nature 2008, 452:234-238.
46. Kobayashi K., Hernandez L.D., Galán J.E., Janeway C.A., Medzhitov R., Flavell R.A. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 2002, 110:191-202.
47. Krug A., French A.R., Barchet W., Fischer J.A., Dzionek A., Pingel J.T., Orihuela M.M., Akira S., Yokoyama W.M., Colonna M. TLR9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function. Immunity 2004, 21:107-119.
48. Krug A., Luker G.D., Barchet W., Leib D.A., Akira S., Colonna M. Herpes simplex virus type 1 activates murine natural interferon-producing cells through toll-like receptor 9. Blood 2004, 103:1433-1437.
49. Kumar H., Kawai T., Akira S. Toll-like receptors and innate immunity. Biochem. Biophys. Res. Commun. 2009, 388:621-625.
50. Lande R., Gregorio J., Facchinetti V., Chatterjee B., Wang Y.H., Homey B., Cao W., Wang Y.H., Su B., Nestle F.O., et al. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 2007, 449:564-569.
51. Latz E., Schoenemeyer A., Visintin A., Fitzgerald K.A., Monks B.G., Knetter C.F., Lien E., Nilsen N.J., Espevik T., Golenbock D.T. TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat. Immunol. 2004, 5:190-198.
52. Latz E., Verma A., Visintin A., Gong M., Sirois C.M., Klein D.C., Monks B.G., McKnight C.J., Lamphier M.S., Duprex W.P., et al. Ligand-induced conformational changes allosterically activate Toll-like receptor 9. Nat. Immunol. 2007, 8:772-779.
53. Lau C.M., Broughton C., Tabor A.S., Akira S., Flavell R.A., Mamula M.J., Christensen S.R., Shlomchik M.J., Viglianti G.A., Rifkin I.R., Marshak-Rothstein A. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J. Exp. Med. 2005, 202:1171-1177.
54. Leadbetter E.A., Rifkin I.R., Hohlbaum A.M., Beaudette B.C., Shlomchik M.J., Marshak-Rothstein A. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 2002, 416:603-607.
55. Lee M.S., Kim Y.J. Signaling pathways downstream of pattern-recognition receptors and their cross talk. Annu. Rev. Biochem. 2007, 76:447-480.
56. Lee H.K., Lund J.M., Ramanathan B., Mizushima N., Iwasaki A. Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science 2007, 315:1398-1401.
57. Lee-Kirsch M.A., Chowdhury D., Harvey S., Gong M., Senenko L., Engel K., Pfeiffer C., Hollis T., Gahr M., Perrino F.W., et al. A mutation in TREX1 that impairs susceptibility to granzyme A-mediated cell death underlies familial chilblain lupus. J. Mol. Med. 2007, 85:531-537.
58. Lee-Kirsch M.A., Gong M., Chowdhury D., Senenko L., Engel K., Lee Y.A., de Silva U., Bailey S.L., Witte T., Vyse T.J., et al. Mutations in the gene encoding the 3′-5′ DNA exonuclease TREX1 are associated with systemic lupus erythematosus. Nat. Genet. 2007, 39:1065-1067.
59. Leifer C.A., Kennedy M.N., Mazzoni A., Lee C., Kruhlak M.J., Segal D.M. TLR9 is localized in the endoplasmic reticulum prior to stimulation. J. Immunol. 2004, 173:1179-1183.
60. Lemaitre B., Nicolas E., Michaut L., Reichhart J.M., Hoffmann J.A. The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 1996, 86:973-983.
61. Li C., Zienkiewicz J., Hawiger J. Interactive sites in the MyD88 Toll/interleukin (IL) 1 receptor domain responsible for coupling to the IL1beta signaling pathway. J. Biol. Chem. 2005, 280:26152-26159.
62. Liu L., Botos I., Wang Y., Leonard J.N., Shiloach J., Segal D.M., Davies D.R. Structural basis of toll-like receptor 3 signaling with double-stranded RNA. Science 2008, 320:379-381.
63. Lund J., Sato A., Akira S., Medzhitov R., Iwasaki A. Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells. J. Exp. Med. 2003, 198:513-520.
64. Lund J.M., Alexopoulou L., Sato A., Karow M., Adams N.C., Gale N.W., Iwasaki A., Flavell R.A. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. USA 2004, 101:5598-5603.
65. Mancuso G., Gambuzza M., Midiri A., Biondo C., Papasergi S., Akira S., Teti G., Beninati C. Bacterial recognition by toll-like receptor 7 in the lysosomes of conventional dendritic cells. Nat. Immunol. 2009, in press.
66. Marshak-Rothstein A. Toll-like receptors in systemic autoimmune disease. Nat. Rev. Immunol. 2006, 6:823-835.
67. Martinon F., Gaide O., Pétrilli V., Mayor A., Tschopp J. NALP inflammasomes: a central role in innate immunity. Semin. Immunopathol. 2007, 29:213-229.
68. Matsumoto M., Funami K., Tanabe M., Oshiumi H., Shingai M., Seto Y., Yamamoto A., Seya T. Subcellular localization of Toll-like receptor 3 in human dendritic cells. J. Immunol. 2003, 171:3154-3162.
69. Matsumoto F., Saitoh S., Fukui R., Kobayashi T., Tanimura N., Konno K., Kusumoto Y., Akashi-Takamura S., Miyake K. Cathepsins are required for Toll-like receptor 9 responses. Biochem. Biophys. Res. Commun. 2008, 367:693-699.
70. Maxfield F.R., McGraw T.E. Endocytic recycling. Nat. Rev. Mol. Cell Biol. 2004, 5:121-132.
71. Mellman I. Endocytosis and molecular sorting. Annu. Rev. Cell Dev. Biol. 1996, 12:575-625.
72. Mellman I., Steinman R.M. Dendritic cells: specialized and regulated antigen processing machines. Cell 2001, 106:255-258.
73. Miyake K. Innate immune sensing of pathogens and danger signals by cell surface Toll-like receptors. Semin. Immunol. 2007, 19:3-10.
74. Morita M., Stamp G., Robins P., Dulic A., Rosewell I., Hrivnak G., Daly G., Lindahl T., Barnes D.E. Gene-targeted mice lacking the Trex1 (DNase III) 3′->5′ DNA exonuclease develop inflammatory myocarditis. Mol. Cell. Biol. 2004, 24:6719-6727.
75. Napirei M., Karsunky H., Zevnik B., Stephan H., Mannherz H.G., Möröy T. Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat. Genet. 2000, 25:177-181.
76. Negishi H., Fujita Y., Yanai H., Sakaguchi S., Ouyang X., Shinohara M., Takayanagi H., Ohba Y., Taniguchi T., Honda K. Evidence for licensing of IFN-gamma-induced IFN regulatory factor 1 transcription factor by MyD88 in Toll-like receptor-dependent gene induction program. Proc. Natl. Acad. Sci. USA 2006, 103:15136-15141.
77. Nishiya T., Kajita E., Miwa S., Defranco A.L. TLR3 and TLR7 are targeted to the same intracellular compartments by distinct regulatory elements. J. Biol. Chem. 2005, 280:37107-37117.
78. Okabe Y., Kawane K., Akira S., Taniguchi T., Nagata S. Toll-like receptor-independent gene induction program activated by mammalian DNA escaped from apoptotic DNA degradation. J. Exp. Med. 2005, 202:1333-1339.
79. Palsson-McDermott E.M., Doyle S.L., McGettrick A.F., Hardy M., Husebye H., Banahan K., Gong M., Golenbock D., Espevik T., O'Neill L.A. TAG, a splice variant of the adaptor TRAM, negatively regulates the adaptor MyD88-independent TLR4 pathway. Nat. Immunol. 2009, 10:579-586.
80. Park B., Brinkmann M.M., Spooner E., Lee C.C., Kim Y.M., Ploegh H.L. Proteolytic cleavage in an endolysosomal compartment is required for activation of Toll-like receptor 9. Nat. Immunol. 2008, 9:1407-1414.
81. Parroche P., Lauw F.N., Goutagny N., Latz E., Monks B.G., Visintin A., Halmen K.A., Lamphier M., Olivier M., Bartholomeu D.C., et al. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc. Natl. Acad. Sci. USA 2007, 104:1919-1924.
82. Petzke M.M., Brooks A., Krupna M.A., Mordue D., Schwartz I. Recognition of Borrelia burgdorferi, the Lyme disease spirochete, by TLR7 and TLR9 induces a type I IFN response by human immune cells. J. Immunol. 2009, 183:5279-5292.
83. Pobezinskaya Y.L., Kim Y.S., Choksi S., Morgan M.J., Li T., Liu C., Liu Z. The function of TRADD in signaling through tumor necrosis factor receptor 1 and TRIF-dependent Toll-like receptors. Nat. Immunol. 2008, 9:1047-1054.
84. Poltorak A., He X., Smirnova I., Liu M.Y., Van Huffel C., Du X., Birdwell D., Alejos E., Silva M., Galanos C., et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998, 282:2085-2088.
85. Pryor P.R., Luzio J.P. Delivery of endocytosed membrane proteins to the lysosome. Biochim. Biophys. Acta 2009, 1793:615-624.
86. Randow F., Seed B. Endoplasmic reticulum chaperone gp96 is required for innate immunity but not cell viability. Nat. Cell Biol. 2001, 3:891-896.
87. Saha S.K., Cheng G. TRAF3: a new regulator of type I interferons. Cell Cycle 2006, 5:804-807.
88. Sepulveda F.E., Maschalidi S., Colisson R., Heslop L., Ghirelli C., Sakka E., Lennon-Duménil A.M., Amigorena S., Cabanie L., Manoury B. Critical role for asparagine endopeptidase in endocytic Toll-like receptor signaling in dendritic cells. Immunity 2009, 31:737-748.
89. Sharma S., tenOever B.R., Grandvaux N., Zhou G.P., Lin R., Hiscott J. Triggering the interferon antiviral response through an IKK-related pathway. Science 2003, 300:1148-1151.
90. Shinohara M.L., Lu L., Bu J., Werneck M.B., Kobayashi K.S., Glimcher L.H., Cantor H. Osteopontin expression is essential for interferon-alpha production by plasmacytoid dendritic cells. Nat. Immunol. 2006, 7:498-506.
91. Siggs O.M., Berger M., Krebs P., Arnold C.N., Eidenschenk C., Huber C., Pirie E., Smart N.G., Khovananth K., Xia Y., et al. A mutation of Ikbkg causes immune deficiency without impairing degradation of IkappaB alpha. Proc. Natl. Acad. Sci. USA 2010, 107:3046-3051.
92. Skaug B., Jiang X., Chen Z.J. The role of ubiquitin in NF-kappaB regulatory pathways. Annu. Rev. Biochem. 2009, 78:769-796.
93. Slack E., Hapfelmeier S., Stecher B., Velykoredko Y., Stoel M., Lawson M.A., Geuking M.B., Beutler B., Tedder T.F., Hardt W.D., et al. Innate and adaptive immunity cooperate flexibly to maintain host-microbiota mutualism. Science 2009, 325:617-620.
94. Stetson D.B., Ko J.S., Heidmann T., Medzhitov R. Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 2008, 134:587-598.
95. Suzuki N., Suzuki S., Duncan G.S., Millar D.G., Wada T., Mirtsos C., Takada H., Wakeham A., Itie A., Li S., et al. Severe impairment of interleukin-1 and Toll-like receptor signalling in mice lacking IRAK-4. Nature 2002, 416:750-756.
96. Tabeta K., Georgel P., Janssen E., Du X., Hoebe K., Crozat K., Mudd S., Shamel L., Sovath S., Goode J., et al. Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc. Natl. Acad. Sci. USA 2004, 101:3516-3521.
97. Tabeta K., Hoebe K., Janssen E.M., Du X., Georgel P., Crozat K., Mudd S., Mann N., Sovath S., Goode J., et al. The Unc93b1 mutation 3d disrupts exogenous antigen presentation and signaling via Toll-like receptors 3, 7 and 9. Nat. Immunol. 2006, 7:156-164.
98. Takahashi K., Shibata T., Akashi-Takamura S., Kiyokawa T., Wakabayashi Y., Tanimura N., Kobayashi T., Matsumoto F., Fukui R., Kouro T., et al. A protein associated with Toll-like receptor (TLR) 4 (PRAT4A) is required for TLR-dependent immune responses. J. Exp. Med. 2007, 204:2963-2976.
99. Takaoka A., Yanai H., Kondo S., Duncan G., Negishi H., Mizutani T., Kano S., Honda K., Ohba Y., Mak T.W., Taniguchi T. Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 2005, 434:243-249.
100. Takeuchi O., Hoshino K., Akira S. Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. J. Immunol. 2000, 165:5392-5396.
101. Tanimura N., Saitoh S., Matsumoto F., Akashi-Takamura S., Miyake K. Roles for LPS-dependent interaction and relocation of TLR4 and TRAM in TRIF-signaling. Biochem. Biophys. Res. Commun. 2008, 368:94-99.
102. Wagner H. The sweetness of the DNA backbone drives Toll-like receptor 9. Curr. Opin. Immunol. 2008, 20:396-400.
103. Wang T., Town T., Alexopoulou L., Anderson J.F., Fikrig E., Flavell R.A. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat. Med. 2004, 10:1366-1373.
104. Wang J., Shao Y., Bennett T.A., Shankar R.A., Wightman P.D., Reddy L.G. The functional effects of physical interactions among Toll-like receptors 7, 8, and 9. J. Biol. Chem. 2006, 281:37427-37434.
105. Wang J.P., Liu P., Latz E., Golenbock D.T., Finberg R.W., Libraty D.H. Flavivirus activation of plasmacytoid dendritic cells delineates key elements of TLR7 signaling beyond endosomal recognition. J. Immunol. 2006, 177:7114-7121.
106. Weber F., Wagner V., Rasmussen S.B., Hartmann R., Paludan S.R. Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J. Virol. 2006, 80:5059-5064.
107. Yang Y., Liu B., Dai J., Srivastava P.K., Zammit D.J., Lefrançois L., Li Z. Heat shock protein gp96 is a master chaperone for toll-like receptors and is important in the innate function of macrophages. Immunity 2007, 26:215-226.
108. Yang Y.G., Lindahl T., Barnes D.E. Trex1 exonuclease degrades ssDNA to prevent chronic checkpoint activation and autoimmune disease. Cell 2007, 131:873-886.
109. Yasuda K., Yu P., Kirschning C.J., Schlatter B., Schmitz F., Heit A., Bauer S., Hochrein H., Wagner H. Endosomal translocation of vertebrate DNA activates dendritic cells via TLR9-dependent and -independent pathways. J. Immunol. 2005, 174:6129-6136.
110. Yasuda K., Rutz M., Schlatter B., Metzger J., Luppa P.B., Schmitz F., Haas T., Heit A., Bauer S., Wagner H. CpG motif-independent activation of TLR9 upon endosomal translocation of " natural" phosphodiester DNA. Eur. J. Immunol. 2006, 36:431-436.
111. Yasutomo K., Horiuchi T., Kagami S., Tsukamoto H., Hashimura C., Urushihara M., Kuroda Y. Mutation of DNASE1 in people with systemic lupus erythematosus. Nat. Genet. 2001, 28:313-314.
112. Yoneyama M., Fujita T. RNA recognition and signal transduction by RIG-I-like receptors. Immunol. Rev. 2009, 227:54-65.
113. Yoshida H., Okabe Y., Kawane K., Fukuyama H., Nagata S. Lethal anemia caused by interferon-beta produced in mouse embryos carrying undigested DNA. Nat. Immunol. 2005, 6:49-56.
114. Zhang S.Y., Jouanguy E., Ugolini S., Smahi A., Elain G., Romero P., Segal D., Sancho-Shimizu V., Lorenzo L., Puel A., et al. TLR3 deficiency in patients with herpes simplex encephalitis. Science 2007, 317:1522-1527.
115. Zheng L., Dai H., Zhou M., Li M., Singh P., Qiu J., Tsark W., Huang Q., Kernstine K., Zhang X., et al. Fen1 mutations result in autoimmunity, chronic inflammation and cancers. Nat. Med. 2007, 13:812-819.