Nonredundant roles of TIRAP and MyD88 in airway response to endotoxin, independent of TRIF, IL-1 and IL-18 pathways

Laboratory Investigation

Volumn 86, Issue 11, 2006, Pages 1126-1135

  Togbe, Dieudonnée ^a   Aurore, Gorse ^a   Noulin, Nicolas ^a,b   Quesniaux, Valérie F J ^a   Schnyder Candrian, Silvia ^a   Schnyder, Bruno ^a   Vasseur, Virginie ^a   Akira, Shizuo ^c   Hoebe, Kasper ^d   Beutler, Bruce ^d   Ryffel, Bernhard ^a   Couillin, Isabelle ^a  

^a CNRS   (France)

^b Key Obs   (France)

^c OSAKA UNIVERSITY   (Japan)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Airways response; Caspase 1; Endotoxin; Innate immunity; TLR signaling

Indexed keywords

ENDOTOXIN; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 18; INTERLEUKIN 18 RECEPTOR; INTERLEUKIN 1BETA CONVERTING ENZYME; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN; PROTEIN TIRAP; TOLL LIKE RECEPTOR 4; TRIF PROTEIN; UNCLASSIFIED DRUG;

AIRWAY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL INJURY; BRONCHOSPASM; CONTROLLED STUDY; MOUSE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; BRONCHI; BRONCHOALVEOLAR LAVAGE FLUID; BRONCHOCONSTRICTION; CELLS, CULTURED; ENDOTOXINS; INTERLEUKIN-1; INTERLEUKIN-18; LIPOPOLYSACCHARIDES; LUNG; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; PEROXIDASE; RECEPTORS, INTERLEUKIN-1;

EID: 33750291430     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.3700473     Document Type: Article

References (52)

1. Schwartz DA, Thorne PS, Yagla SJ, et al. The role of endotoxin in grain dust-induced lung disease. Am J Respir Crit Care Med 1995;152:603-608.
2. Kennedy SM, Christiani DC, Eisen EA, et al. Cotton dust and endotoxin exposure-response relationships in cotton textile workers. Am Rev Respir Dis 1987; 135:194-200.
3. Donham K, Haglind P, Peterson Y, et al. Environmental and health studies of farm workers in Swedish swine confinement buildings. Br J Ind Med 1989;46:31-37.
4. Michel O, Kips J, Duchateau J, et al. Severity of asthma is related to endotoxin in house dust. Am J Respir Crit Care Med 1996;154:1641-1646.
5. Liu AH. Something old, something new: indoor endotoxin, allergens and asthma. Paediatr Respir Rev 2004;5(Suppl A):S65-S71.
6. Kline JN, Cowden JD, Hunninghake GW, et al. Variable airway responsiveness to inhaled lipopolysaccharide. Am J Respir Crit Care Med 1999;160:297-303.
7. Arbour NC, Lorenz E, Schutte BC, et al. TLR4 mutations are associated with endotoxin hyporesponsiveness in humans. Nat Genet 2000;25:187-191.
8. Lefort J, Motreff L, Vargaftig BB. Airway administration of Escherichia coli endotoxin to mice induces glucocorticosteroid-resistant bronchoconstriction and vasopermeation. Am J Respir Cell Mol Biol 2001;24: 345-351.
9. Schnyder-Candrian S, Quesniaux VF, Di Padova F, et al. Dual effects of p38 MAPK on TNF-dependent bronchoconstriction and TNF-independent neutrophil recruitment in lipopolysaccharide-induced acute respiratory distress syndrome. J Immunol 2005;175: 262-269.
10. Andonegui G, Goyert SM, Kubes P. Lipopolysaccharide-induced leukocyte-endothelial cell interactions: a role for CD14 vs toll-like receptor 4 within microvessels. J Immunol 2002;169:2111-2119.
11. Andonegui G, Bonder CS, Green F, et al. Endothelium-derived Toll-like receptor-4 is the key molecule in LPS-induced neutrophil sequestration into lungs. J Clin Invest 2003;112:1264.
12. Lefort J, Singer M, Leduc D, et al. Systemic administration of endotoxin induces bronchopulmonary hyperreactivity dissociated from TNF-alpha formation and neutrophil sequestration into the murine lungs. J Immunol 1998;161:474-480.
13. Togbe D, Schnyder S, Schnyder B, et al. TLR4 gene dosage contributes to endotoxin induced acute respiratory inflammation. J Leukoc Biol 2006;80: (in press).
14. Yamamoto M, Sato S, Mori K, et al. Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-beta promoter in the Toll-like receptor signaling. J Immunol 2002;169: 6668-6672.
15. Hoebe K, Du X, Georgel P, et al. Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 2003;424:743-748.
16. Beutler B, Jiang Z, Georgel P, et al. Genetic analysis of host resistance: toll-like receptor signaling and immunity at large. Annu Rev Immunol 2006;24: 353-389.
17. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006;124:783-801.
18. Kawai T, Adachi O, Ogawa T, et al. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 1999;11:115-122.
19. Yamamoto M, Sato S, Hemmi H, et al. Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4. Nature 2002;420:324-329.
20. Oshiumi H, Sasai M, Shida K, et al. TIR-containing adapter molecule (TICAM)-2, a bridging adapter recruiting to toll-like receptor 4 TICAM-1 that induces interferon-beta. J Biol Chem 2003;278:49751-49762.
21. Horng T, Barton GM, Flavell RA, et al. The adaptor molecule TIRAP provides signalling specificity for Toll-like receptors. Nature 2002;420:329-333.
22. Fitzgerald KA, Palsson-McDermott EM, Bowie AG, et al. Mal (MyD88-adapter-like) is required for Toll-like receptor-4 signal transduction. Nature 2001;413:78-83.
23. Horng T, Barton GM, Medzhitov R. TIRAP: an adapter molecule in the Toll signaling pathway. Nat Immunol 2001;2:835-841.
24. Yamamoto M, Sato S, Hemmi H, et al. TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nat Immunol 2003;4:1144-1150.
25. Yamamoto M, Sato S, Hemmi H, et al. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 2003;301:640-643.
26. Guillot L, Medjane S, Le-Barillec K, et al. Response of human pulmonary epithelial cells to lipopolysaccharide involves Toll-like receptor 4 (TLR4)-dependent signaling pathways: evidence for an intracellular compartmentalization of TLR4. J Biol Chem 2004;279: 2712-2718 (Epub 2003 Nov 2714).
27. Piggott DA, Eisenbarth SC, Xu L, et al. MyD88-dependent induction of allergic Th2 responses to intranasal antigen. J Clin Invest 2005;115:459-467.
28. Noulin N, Quesniaux VF, Schnyder-Candrian S, et al. Both hemopoietic and resident cells are required for MyD88-dependent pulmonary inflammatory response to inhaled endotoxin. J Immunol 2005;175: 6861-6869.
29. Zeisel MB, Druet VA, Sibilia J, et al. Cross talk between MyD88 and focal adhesion kinase pathways. J Immunol 2005;174:7393-7397.
30. Gamero AM, Oppenheim JJ. IL-1 can act as number one. Immunity 2006;24:16-17.
31. Jeyaseelan S, Manzer R, Young SK, et al. Toll-IL-1 receptor domain-containing adaptor protein is critical for early lung immune responses against Escherichia coli lipopolysaccharide and viable Escherichia coli. J Immunol 2005;175:7484-7495.
32. Glaccum MB, Stocking KL, Charrier K, et al. Phenotypic and functional characterization of mice that lack the type I receptor for IL-1. J Immunol 1997;159:3364-3371.
33. Hoshino K, Tsutsui H, Kawai T, et al. Cutting edge: generation of IL-18 receptor-deficient mice: evidence for IL-1 receptor-related protein as an essential IL-18 binding receptor. J Immunol 1999;162:5041-5044.
34. Kuida K, Lippke JA, Ku G, et al. Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 1995;267:2000-2003.
35. Hoshino K, Takeuchi O, Kawai T, et al. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 1999;162:3749-3752.
36. Couillin I, Maillet I, Vargaftig BB, et al. Arthropod-derived histamine-binding protein prevents murine allergic asthma. J Immunol 2004;173:3281-3286.
37. Muller M, Eugster HP, Le Hir M, et al. Correction or transfer of immunodeficiency due to TNF-LT alpha deletion by bone marrow transplantation. Mol Med 1996;2:247-255.
38. Nicolle DM, Pichon X, Bouchot A, et al. Chronic pneumonia despite adaptive immune response to Mycobacterium bovis BCG in MyD88-deficient mice. Lab Invest 2004;84:1305-1321.
39. Vogel SN, Fitzgerald KA, Fenton MJ. TLRs: differential adapter utilization by toll-like receptors mediates TLR-specific patterns of gene expression. Mol Interv 2003;3:466-477.
40. Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol 2004;4:499-511.
41. Hirotani T, Yamamoto M, Kumagai Y, et al. Regulation of lipopolysaccharide-inducible genes by MyD88 and Toll/IL-1 domain containing adaptor inducing IFN-beta. Biochem Biophys Res Commun 2005;328: 383-392.
42. Fitzgerald KA, Rowe DC, Barnes BJ, et al. LPS-TLR4 signaling to IRF-3/7 and NF-kappaB involves the toll adapters TRAM and TRIF. J Exp Med 2003;198:1043-1055.
43. Mansell A, Brint E, Gould JA, et al. Mal interacts with tumor necrosis factor receptor-associated factor (TRAF)-6 to mediate NF-kappaB activation by toll-like receptor (TLR)-2 and TLR4. J Biol Chem 2004;279:37227-37230.
44. Gray P, Dunne A, Brikos C, et al. MyD88 adapter-like (Mal) is phosphorylated by Bruton's tyrosine kinase during TLR2 and TLR4 signal transduction. J Biol Chem 2006;281:10489-10495.
45. McGettrick AF, Brint EK, Palsson-McDermott EM, et al. Trif-related adapter molecule is phosphorylated by PKC{varepsilon} during Toll-like receptor 4 signaling. Proc Natl Acad Sci USA 2006;103: 9196-9201.
46. Doyle SL, Jefferies CA, O'Neill LA. Bruton's tyrosine kinase is involved in p65-mediated transactivation and phosphorylation of p65 on serine 536 during NFkappaB activation by lipopolysaccharide. J Biol Chem 2005;280:23496-23501.
47. Jefferies CA, O'Neill LA. Bruton's tyrosine kinase (Btk)-the critical tyrosine kinase in LPS signalling? Immunol Lett 2004;92:15-22.
48. Gray P, Dunne A, Brikos C, et al. MyD88 adapter-like (Mal) is phosphorylated by Bruton's tyrosine kinase during TLR2 and TLR4 signal transduction. J Biol Chem 2006;281:10489-10495.
49. Brint EK, Xu D, Liu H, et al. ST2 is an inhibitor of interleukin 1 receptor and Toll-like receptor 4 signaling and maintains endotoxin tolerance. Nat Immunol 2004;5:373-379.
50. Kagan JC, Medzhitov R. Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling. Cell 2006;125:943-955.
51. Rowe DC, McGettrick AF, Latz E, et al. The myristoylation of TRIF-related adaptor molecule is essential for Toll-like receptor 4 signal transduction. Proc Natl Acad Sci USA 2006;103:6299-6304.
52. Fitzgerald KA, Chen ZJ. Sorting out Toll signals. Cell 2006;125:834-836.