Trafficking of endosomal Toll-like receptors

Trends in Cell Biology

Volumn 24, Issue 6, 2014, Pages 360-369

  Lee, Bettina L ^a,b   Barton, Gregory M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b GENENTECH INC   (United States)

Author keywords

AP complex; Autoimmunity; Innate immunity; Type I interferon; UNC93B1

Indexed keywords

DNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; RNA; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9;

CYTOKINE PRODUCTION; CYTOLOGY; DENDRITIC CELL; ENDOPLASMIC RETICULUM; ENDOSOME; HUMAN; INNATE IMMUNITY; INTERFERON PRODUCTION; NONHUMAN; PATTERN RECOGNITION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVIEW; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UBIQUITINATION; ANIMAL; METABOLISM;

ANIMALS; ENDOPLASMIC RETICULUM; ENDOSOMES; HUMANS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 84901446294     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2013.12.002     Document Type: Review

References (99)

1. Janeway C.A. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol. 1989, 54:1-13.
2. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 2010, 11:373-384.
3. Kawai T., Akira S. Toll-like receptor and RIG-I-like receptor signaling. Ann. N. Y. Acad. Sci. 2008, 1143:1-20.
4. Brunette R.L., et al. Extensive evolutionary and functional diversity among mammalian AIM2-like receptors. J. Exp. Med. 2012, 209:1969-1983.
5. Wen H., et al. Mechanisms of NOD-like receptor-associated inflammasome activation. Immunity 2013, 39:432-441.
6. Geijtenbeek T.B., Gringhuis S.I. Signalling through C-type lectin receptors: shaping immune responses. Nat. Rev. Immunol. 2009, 9:465-479.
7. Iwasaki A., Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 2004, 5:987-995.
8. Marshak-Rothstein A. Toll-like receptors in systemic autoimmune disease. Nat. Rev. Immunol. 2006, 6:823-835.
9. Choe J. Crystal structure of human Toll-Like receptor 3 (TLR3) ectodomain. Science 2005, 309:581-585.
10. Jin M.S., et al. Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 2007, 130:1071-1082.
11. Kang J.Y., et al. Recognition of lipopeptide patterns by Toll-like receptor 2-Toll-like receptor 6 heterodimer. Immunity 2009, 31:873-884.
12. Liu L., et al. Structural basis of Toll-Like receptor 3 signaling with double-stranded RNA. Science 2008, 320:379-381.
13. Lu J., Sun P.D. The structure of the TLR5-flagellin complex: a new mode of pathogen detection, conserved receptor dimerization for signaling. Sci. Signal. 2012, 5:pe11.
14. Park B.S., et al. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 2009, 458:1191-1195.
15. Tanji H., et al. Structural reorganization of the Toll-like receptor 8 dimer induced by agonistic ligands. Science 2013, 339:1426-1429.
16. Jin M.S., Lee J.O. Structures of the toll-like receptor family and its ligand complexes. Immunity 2008, 29:182-191.
17. Barton G.M. Viral recognition by Toll-like receptors. Semin. Immunol. 2007, 19:33-40.
18. Alexopoulou L., et al. Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 2001, 413:732-738.
19. Lund J.M., et al. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:5598-5603.
20. Hemmi H., et al. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat. Immunol. 2002, 3:196-200.
21. Heil F. Species-specific recognition of single-stranded RNA via Toll-like receptor 7 and 8. Science 2004, 303:1526-1529.
22. Forsbach A., et al. Identification of RNA sequence motifs stimulating sequence-specific TLR8-dependent immune responses. J. Immunol. 2008, 180:3729-3738.
23. Hemmi H., et al. A Toll-like receptor recognizes bacterial DNA. Nature 2000, 408:740-745.
24. Li X.D., Chen Z.J. Sequence specific detection of bacterial 23S ribosomal RNA by TLR13. eLife 2012, 1:e00102.
25. Oldenburg M., et al. TLR13 recognizes bacterial 23S rRNA devoid of erythromycin resistance-forming modification. Science 2012, 337:1111-1115.
26. Shi Z., et al. A novel Toll-like receptor that recognizes vesicular stomatitis virus. J. Biol. Chem. 2011, 286:4517-4524.
27. Gorden K.B., et al. Synthetic TLR agonists reveal functional differences between human TLR7 and TLR8. J. Immunol. 2005, 174:1259-1268.
28. Jurk M., et al. Human TLR7 or TLR8 independently confer responsiveness to the antiviral compound R-848. Nat. Immunol. 2002, 3:499.
29. Rutz M., et al. Toll-like receptor 9 binds single-stranded CpG-DNA in a sequence- and pH-dependent manner. Eur. J. Immunol. 2004, 34:2541-2550.
30. Krieg A.M. CpG motifs in bacterial DNA and their immune effects. Annu. Rev. Immunol. 2002, 20:709-760.
31. Bauer S., et al. Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:9237-9242.
32. Yasuda K., et al. CpG motif-independent activation of TLR9 upon endosomal translocation of 'natural' phosphodiester DNA. Eur. J. Immunol. 2006, 36:431-436.
33. Haas T., et al. The DNA sugar backbone 2 deoxyribose determines Toll-like receptor 9 activation. Immunity 2008, 28:315-323.
34. Brinkmann V., et al. Neutrophil extracellular traps kill bacteria. Science 2004, 303:1532-1535.
35. Fuchs T.A., et al. Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 2007, 176:231-241.
36. Barbalat R., et al. Nucleic acid recognition by the innate immune system. Annu. Rev. Immunol. 2011, 29:185-214.
37. Garcia-Romo G.S., et al. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci. Transl. Med. 2011, 3:73ra20.
38. Yoshida H., et al. Lethal anemia caused by interferon-beta produced in mouse embryos carrying undigested DNA. Nat. Immunol. 2005, 6:49-56.
39. Barton G.M., Kagan J.C. A cell biological view of Toll-like receptor function: regulation through compartmentalization. Nat. Rev. Immunol. 2009, 9:535-542.
40. Pifer R., et al. UNC93B1 Is essential for TLR11 activation and IL-12-dependent host resistance to Toxoplasma gondii. J. Biol. Chem. 2011, 286:3307-3314.
41. Andrade W.A., et al. Combined action of nucleic acid-sensing Toll-like receptors and TLR11/TLR12 heterodimers imparts resistance to Toxoplasma gondii in mice. Cell Host Microbe 2013, 13:42-53.
42. Yi A.K., et al. CpG motifs in bacterial DNA activate leukocytes through the pH-dependent generation of reactive oxygen species. J. Immunol. 1998, 160:4755-4761.
43. Kagan J.C., et al. TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-β. Nat. Immunol. 2008, 9:361-368.
44. Honda K., et al. Spatiotemporal regulation of MyD88-IRF-7 signalling for robust type-I interferon induction. Nature 2005, 434:1035-1040.
45. Means T.K., et al. Human lupus autoantibody-DNA complexes activate DCs through cooperation of CD32 and TLR9. J. Clin. Invest. 2005, 115:407-417.
46. Leadbetter E.A., et al. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 2002, 416:603-607.
47. Chaturvedi A. The B cell receptor governs the subcellular location of Toll-like receptor 9 leading to hyperresponses to DNA-containing antigens. Immunity 2008, 28:799-809.
48. Lande R., et al. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 2007, 449:564-569.
49. Ivanov S., et al. A novel role for HMGB1 in TLR9-mediated inflammatory responses to CpG-DNA. Blood 2007, 110:1970-1981.
50. Tian J., et al. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat. Immunol. 2007, 8:487-496.
51. Yanai H., et al. HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature 2009, 461:99-103.
52. Ewald S.E., et al. The ectodomain of Toll-like receptor 9 is cleaved to generate a functional receptor. Nature 2008, 456:658-662.
53. Park B., et al. Proteolytic cleavage in an endolysosomal compartment is required for activation of Toll-like receptor 9. Nat. Immunol. 2008, 9:1407-1414.
54. Sepulveda F.E., et al. Critical role for asparagine endopeptidase in endocytic Toll-like receptor signaling in dendritic cells. Immunity 2009, 31:737-748.
55. Ewald S.E., et al. Nucleic acid recognition by Toll-like receptors is coupled to stepwise processing by cathepsins and asparagine endopeptidase. J. Exp. Med. 2011, 208:643-651.
56. Latz E., et al. Ligand-induced conformational changes allosterically activate Toll-like receptor 9. Nat. Immunol. 2007, 8:772-779.
57. Peter M.E., et al. Identification of an N-Terminal recognition site in TLR9 that contributes to CpG-DNA-mediated receptor activation. J. Immunol. 2009, 182:7690-7697.
58. Fukuda K., et al. Modulation of double-stranded RNA recognition by the N-terminal histidine-rich region of the human Toll-like receptor 3. J. Biol. Chem. 2008, 283:22787-22794.
59. Bell J.K., et al. The dsRNA binding site of human Toll-like receptor 3. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:8792-8797.
60. Botos I., et al. The Toll-like receptor 3:dsRNA signaling complex. Biochim. Biophys. Acta 2009, 1789:667-674.
61. Toscano F., et al. Cleaved/associated TLR3 represents the primary form of the signaling receptor. J. Immunol. 2013, 190:764-773.
62. Barton G.M. Intracellular localization of Toll-like receptor 9 prevents recognition of self DNA but facilitates access to viral DNA. Nat. Immunol. 2006, 7:49-56.
63. Mouchess M.L., et al. Transmembrane mutations in Toll-like receptor 9 bypass the requirement for ectodomain proteolysis and induce fatal inflammation. Immunity 2011, 35:721-732.
64. Subramanian S., et al. A Tlr7 translocation accelerates systemic autoimmunity in murine lupus. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:9970-9975.
65. Pisitkun P. Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science 2006, 312:1669-1672.
66. Deane J.A., et al. Control of Toll-like receptor 7 expression is essential to restrict autoimmunity and dendritic cell proliferation. Immunity 2007, 27:801-810.
67. Kim Y-M., et al. UNC93B1 delivers nucleotide-sensing toll-like receptors to endolysosomes. Nature 2008, 452:234-238.
68. Tabeta K., 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.
69. Lee B.L., et al. UNC93B1 mediates differential trafficking of endosomal TLRs. eLife 2013, 2:e00291.
70. Brinkmann M.M., et al. 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.
71. Kim J., et al. Acidic amino acid residues in the juxtamembrane region of the nucleotide-sensing TLRs are important for UNC93B1 binding and signaling. J. Immunol. 2013, 190:5287-5295.
72. Nishiya T., et al. TLR3 and TLR7 are targeted to the same intracellular compartments by distinct regulatory elements. J. Biol. Chem. 2005, 280:37107-37117.
73. Funami K., et al. The cytoplasmic 'linker region' in Toll-like receptor 3 controls receptor localization and signaling. Int. Immunol. 2004, 16:1143-1154.
74. Kajita E., et al. The transmembrane domain directs TLR9 to intracellular compartments that contain TLR3. Biochem. Biophys. Res. Commun. 2006, 343:578-584.
75. Nishiya T., DeFranco A.L. Ligand-regulated chimeric receptor approach reveals distinctive subcellular localization and signaling properties of the Toll-like receptors. J. Biol. Chem. 2004, 279:19008-19017.
76. Leifer C.A., et al. Cytoplasmic targeting motifs control localization of toll-like receptor 9. J. Biol. Chem. 2006, 281:35585-35592.
77. Lee C.C. Accessory molecules for Toll-like receptors and their function. Nat. Rev. Immunol. 2012, 12:168-179.
78. Yang Y., et al. 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.
79. Takahashi K., 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.
80. Liu B., et al. Folding of Toll-like receptors by the HSP90 paralogue gp96 requires a substrate-specific cochaperone. Nat. Commun. 2010, 1:1-10.
81. Chockalingam A., et al. TLR9 traffics through the Golgi complex to localize to endolysosomes and respond to CpG DNA. Immunol. Cell Biol. 2009, 87:209-217.
82. Chiang C-Y., et al. Cofactors required for TLR7- and TLR9-dependent innate immune responses. Cell Host Microbe 2012, 11:306-318.
83. Christensen S.R., et al. Toll-like receptor 7 and TLR9 dictate autoantibody specificity and have opposing inflammatory and regulatory roles in a murine model of lupus. Immunity 2006, 25:417-428.
84. Nickerson K.M., et al. TLR9 regulates TLR7- and MyD88-dependent autoantibody production and disease in a murine model of lupus. J. Immunol. 2010, 184:1840-1848.
85. Wang J., et al. The functional effects of physical interactions among Toll-like receptors 7, 8, and 9. J. Biol. Chem. 2006, 281:37427-37434.
86. Fukui R., et al. 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.
87. Fukui R., et al. Unc93B1 Restricts systemic lethal inflammation by orchestrating Toll-like receptor 7 and 9 trafficking. Immunity 2011, 35:69-81.
88. Kawai T., 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.
89. Hoshino K., et al. IkappaB kinase-alpha is critical for interferon-alpha production induced by Toll-like receptors 7 and 9. Nature 2006, 440:949-953.
90. Honda K., et al. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 2005, 434:772-777.
91. Kerkmann M., et al. Activation with CpG-A and CpG-B oligonucleotides reveals two distinct regulatory pathways of type I IFN synthesis in human plasmacytoid dendritic cells. J. Immunol. 2003, 170:4465-4474.
92. Guiducci C. Properties regulating the nature of the plasmacytoid dendritic cell response to Toll-like receptor 9 activation. J. Exp. Med. 2006, 203:1999-2008.
93. Vollmer J., et al. Characterization of three CpG oligodeoxynucleotide classes with distinct immunostimulatory activities. Eur. J. Immunol. 2004, 34:251-262.
94. Sasai M. Bifurcation of Toll-like receptor 9 signaling by adaptor protein 3. Science 2010, 329:1530-1534.
95. Blasius A.L., et al. Slc15a4, AP-3, and Hermansky-Pudlak syndrome proteins are required for Toll-like receptor signaling in plasmacytoid dendritic cells. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:19973-19978.
96. Henault J., et al. Noncanonical autophagy is required for type I interferon secretion in response to DNA-immune complexes. Immunity 2012, 37:986-997.
97. Lee H.K., et al. Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science 2007, 315:1398-1401.
98. Menke D.B. Engineering subtle targeted mutations into the mouse genome. Genesis 2013, 51:605-618.
99. Mali P., et al. Cas9 as a versatile tool for engineering biology. Nat. Methods 2013, 10:957-963.