Structural insights into tir domain specificity of the bridging adaptor mal in tlr4 signaling

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Lin, Zhijie ^a   Lu, Jing ^a   Zhou, Weihong ^a   Shen, Yuequan ^a  

^a NANKAI UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; DIMER; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR; LUCIFERASE; MEMBRANE PROTEIN; TIRAP PROTEIN, HUMAN;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; ENZYME SPECIFICITY; HUMAN; MUTATIONAL ANALYSIS; NUCLEOTIDE SEQUENCE; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN INTERACTION; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; BIOSYNTHESIS; CELL STRAIN HEK293; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HYDROGEN BOND; METABOLISM; MISSENSE MUTATION; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; REPORTER GENE; STRUCTURAL HOMOLOGY; X RAY CRYSTALLOGRAPHY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; GENES, REPORTER; HEK293 CELLS; HUMANS; HYDROGEN BONDING; LUCIFERASES; MEMBRANE GLYCOPROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; NF-KAPPA B; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RECEPTORS, INTERLEUKIN-1; STRUCTURAL HOMOLOGY, PROTEIN; TOLL-LIKE RECEPTOR 4;

EID: 84859227566     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034202     Document Type: Article

References (52)

1. Barton GM, Kagan JC, (2009) A cell biological view of Toll-like receptor function: regulation through compartmentalization. Nat Rev Immunol 9: 535-542.
2. Akira S, Uematsu S, Takeuchi O, (2006) Pathogen recognition and innate immunity. Cell 124: 783-801.
3. Jin MS, Kim SE, Heo JY, Lee ME, Kim HM, et al. (2007) Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 130: 1071-1082.
4. Liu L, Botos I, Wang Y, Leonard JN, Shiloach J, et al. (2008) Structural basis of toll-like receptor 3 signaling with double-stranded RNA. Science 320: 379-381.
5. Choe J, Kelker MS, Wilson IA, (2005) Crystal structure of human toll-like receptor 3 (TLR3) ectodomain. Science 309: 581-585.
6. O'Neill LA, Bowie AG, (2007) The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat Rev Immunol 7: 353-364.
7. Watters TM, Kenny EF, O'Neill LA, (2007) Structure, function and regulation of the Toll/IL-1 receptor adaptor proteins. Immunol Cell Biol 85: 411-419.
8. Yamamoto M, Sato S, Hemmi H, Sanjo H, Uematsu S, et al. (2002) Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4. Nature 420: 324-329.
9. Fitzgerald KA, Palsson-McDermott EM, Bowie AG, Jefferies CA, Mansell AS, et al. (2001) Mal (MyD88-adapter-like) is required for Toll-like receptor-4 signal transduction. Nature 413: 78-83.
10. Horng T, Barton GM, Medzhitov R, (2001) TIRAP: an adapter molecule in the Toll signaling pathway. Nat Immunol 2: 835-841.
11. Horng T, Barton GM, Flavell RA, Medzhitov R, (2002) The adaptor molecule TIRAP provides signalling specificity for Toll-like receptors. Nature 420: 329-333.
12. Kagan JC, Medzhitov R, (2006) Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling. Cell 125: 943-955.
13. Mansell A, Brint E, Gould JA, O'Neill LA, Hertzog PJ, (2004) 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 279: 37227-37230.
14. Gray P, Dunne A, Brikos C, Jefferies CA, Doyle SL, et al. (2006) MyD88 adapter-like (Mal) is phosphorylated by Bruton's tyrosine kinase during TLR2 and TLR4 signal transduction. J Biol Chem 281: 10489-10495.
15. Piao W, Song C, Chen H, Wahl LM, Fitzgerald KA, et al. (2008) Tyrosine phosphorylation of MyD88 adapter-like (Mal) is critical for signal transduction and blocked in endotoxin tolerance. J Biol Chem 283: 3109-3119.
16. Miggin SM, Palsson-McDermott E, Dunne A, Jefferies C, Pinteaux E, et al. (2007) NF-kappaB activation by the Toll-IL-1 receptor domain protein MyD88 adapter-like is regulated by caspase-1. Proc Natl Acad Sci USA 104: 3372-3377.
17. Xu Y, Tao X, Shen B, Horng T, Medzhitov R, et al. (2000) Structural basis for signal transduction by the Toll/interleukin-1 receptor domains. Nature 408: 111-115.
18. Khan JA, Brint EK, O'Neill LA, Tong L, (2004) Crystal structure of the Toll/interleukin-1 receptor domain of human IL-1RAPL. J Biol Chem 279: 31664-31670.
19. Nyman T, Stenmark P, Flodin S, Johansson I, Hammarstrom M, et al. (2008) The crystal structure of the human toll-like receptor 10 cytoplasmic domain reveals a putative signaling dimer. J Biol Chem 283: 11861-11865.
20. Chan SL, Low LY, Hsu S, Li S, Liu T, et al. (2009) Molecular mimicry in innate immunity: crystal structure of a bacterial TIR domain. J Biol Chem 284: 21386-21392.
21. Bernoux M, Ve T, Williams S, Warren C, Hatters D, et al. (2011) Structural and Functional Analysis of a Plant Resistance Protein TIR Domain Reveals Interfaces for Self-Association, Signaling, and Autoregulation. Cell Host Microbe 9: 200-211.
22. Ohnishi H, Tochio H, Kato Z, Orii KE, Li A, et al. (2009) Structural basis for the multiple interactions of the MyD88 TIR domain in TLR4 signaling. Proc Natl Acad Sci USA 106: 10260-10265.
23. Chan SL, Mukasa T, Santelli E, Low LY, Pascual J, (2010) The crystal structure of a TIR domain from Arabidopsis thaliana reveals a conserved helical region unique to plants. Protein Sci 19: 155-161.
24. Dunne A, Ejdeback M, Ludidi PL, O'Neill LA, Gay NJ, (2003) Structural complementarity of Toll/interleukin-1 receptor domains in Toll-like receptors and the adaptors Mal and MyD88. J Biol Chem 278: 41443-41451.
25. Nunez Miguel R, Wong J, Westoll JF, Brooks HJ, O'Neill LA, et al. (2007) 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.
26. Toshchakov VY, Szmacinski H, Couture LA, Lakowicz JR, Vogel SN, (2011) Targeting TLR4 Signaling by TLR4 Toll/IL-1 Receptor Domain-Derived Decoy Peptides: Identification of the TLR4 Toll/IL-1 Receptor Domain Dimerization Interface. J Immunol 186: 4819-27.
27. Kawamoto T, Ii M, Kitazaki T, Iizawa Y, Kimura H, (2008) TAK-242 selectively suppresses Toll-like receptor 4-signaling mediated by the intracellular domain. Eur J Pharmacol 584: 40-48.
28. Takashima K, Matsunaga N, Yoshimatsu M, Hazeki K, Kaisho T, et al. (2009) Analysis of binding site for the novel small-molecule TLR4 signal transduction inhibitor TAK-242 and its therapeutic effect on mouse sepsis model. Br J Pharmacol 157: 1250-1262.
29. Matsunaga N, Tsuchimori N, Matsumoto T, Ii M, (2010) TAK-242 (Resatorvid), a Small Molecule Inhibitor of Toll-Like Receptor (TLR) 4 Signaling, Binds Selectively to TLR4 and Interferes with Interactions between TLR4 and Its Adaptor Molecules. Mol Pharmacol 79: 34-41.
30. Khor CC, Chapman SJ, Vannberg FO, Dunne A, Murphy C, et al. (2007) A Mal functional variant is associated with protection against invasive pneumococcal disease, bacteremia, malaria and tuberculosis. Nat Genet 39: 523-528.
31. An Y, Ohnishi H, Matsui E, Funato M, Kato Z, et al. (2011) Genetic variations in MyD88 adaptor-like are associated with atopic dermatitis. Int J Mol Med 27: 795-801.
32. Ferwerda B, Alonso S, Banahan K, McCall MB, Giamarellos-Bourboulis EJ, et al. (2009) Functional and genetic evidence that the Mal/TIRAP allele variant 180L has been selected by providing protection against septic shock. Proc Natl Acad Sci USA 106: 10272-10277.
33. George J, Kubarenko AV, Rautanen A, Mills TC, Colak E, et al. (2010) MyD88 Adaptor-Like D96N Is a Naturally Occurring Loss-of-Function Variant of TIRAP. J Immunol 184: 3025-3032.
34. Nagpal K, Plantinga TS, Wong J, Monks BG, Gay NJ, et al. (2009) A TIR domain variant of MYD88 adapter-like (MAL)/TIRAP results in loss of MYD88 binding and reduced TLR2/TLR4 signaling. J Biol Chem 284: 25742-8.
35. Dissanayeke SR, Levin S, Pienaar S, Wood K, Eley B, et al. (2009) Polymorphic variation in TIRAP is not associated with susceptibility to childhood TB but may determine susceptibility to TBM in some ethnic groups. PLoS ONE 4: e6698.
36. Valkov E, Stamp A, Dimaio F, Baker D, Verstak B, et al. (2011) Crystal structure of Toll-like receptor adaptor MAL/TIRAP reveals the molecular basis for signal transduction and disease protection. Proc Natl Acad Sci USA 108: 14879-14884.
37. Toshchakov VU, Basu S, Fenton MJ, Vogel SN, (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.
38. Loiarro M, Sette C, Gallo G, Ciacci A, Fanto N, et al. (2005) Peptide-mediated interference of TIR domain dimerization in MyD88 inhibits interleukin-1-dependent activation of NF-{kappa}B. J Biol Chem 280: 15809-15814.
39. Jiang Z, Georgel P, Li C, Choe J, Crozat K, et al. (2006) Details of Toll-like receptor:adapter interaction revealed by germ-line mutagenesis. Proc Natl Acad Sci USA 103: 10961-10966.
40. Li C, Zienkiewicz J, Hawiger J, (2005) Interactive sites in the MyD88 Toll/interleukin (IL) 1 receptor domain responsible for coupling to the IL1beta signaling pathway. J Biol Chem 280: 26152-26159.
41. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
42. Kumpf O, Giamarellos-Bourboulis EJ, Koch A, Hamann L, Mouktaroudi M, et al. (2010) Influence of genetic variations in TLR4 and TIRAP/Mal on the course of sepsis and pneumonia and cytokine release: an observational study in three cohorts. Crit Care 14: R103.
43. Song Z, Tong C, Sun Z, Shen Y, Yao C, et al. (2010) Genetic variants in the TIRAP gene are associated with increased risk of sepsis-associated acute lung injury. BMC Med Genet 11: 168.
44. Durrani O, Banahan K, Sheedy FJ, McBride L, Ben-Chetrit E, et al. (2011) TIRAP Ser180Leu polymorphism is associated with Behcet's disease. Rheumatology 50: 1760-1765.
45. Nejentsev S, Thye T, Szeszko JS, Stevens H, Balabanova Y, et al. (2008) Analysis of association of the TIRAP (MAL) S180L variant and tuberculosis in three populations. Nat Genet 40: 261-262.
46. Castiblanco J, Varela DC, Castano-Rodriguez N, Rojas-Villarraga A, Hincapie ME, et al. (2008) TIRAP (MAL) S180L polymorphism is a common protective factor against developing tuberculosis and systemic lupus erythematosus. Infect Genet Evol 8: 541-544.
47. Otwinowski Z, Minor W, (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326.
48. Pape T, Schneider TR, (2004) HKL2MAP: a graphical user interface for macromolecular phasing with SHELX programs. J Appl Crystallogr 37: 843-844.
49. Zwart PH, Afonine PV, Grosse-Kunstleve RW, Hung LW, Ioerger TR, et al. (2008) Automated structure solution with the PHENIX suite. Methods Mol Biol 426: 419-435.
50. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
51. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, et al. (1998) Crystallography & NMR system: a new software suite for macro-molecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905-921.
52. McCoy AJ, (2007) Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr D Biol Crystallogr 63: 32-41.