Comparative and phylogenetic analyses of three TIR domain-containing adaptors in metazoans: Implications for evolution of TLR signaling pathways

Developmental and Comparative Immunology

Volumn 35, Issue 7, 2011, Pages 764-773

  Wu, Baojun ^a   Xin, Bo ^a   Jin, Meng ^a   Wei, Tiandi ^a   Bai, Zengliang ^a  

^a SHANDONG UNIVERSITY   (China)

Author keywords

Comparative genomics; Shark; TICAM 1; TICAM 2; TIRAP

Indexed keywords

LIPOPOLYSACCHARIDE; TOLL INTERLEUKIN 1 RECEPTOR DOMAIN CONTAINING ADAPTOR PROTEIN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 22; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 2; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CHORDATA; COMPARATIVE STUDY; CONTROLLED STUDY; GENE; GENETIC ANALYSIS; GRAM POSITIVE BACTERIUM; HUMAN; METAZOON; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; SHARK; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; TICAM 2 GENE;

BACTERIA (MICROORGANISMS); BRANCHIOSTOMA LANCEOLATUM; CHONDRICHTHYES; CHORDATA; MAMMALIA; METAZOA; POSIBACTERIA; VERTEBRATA;

EID: 79954924229     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2011.02.009     Document Type: Article

References (57)

1. Akira S., Takeda K. Toll-like receptor signalling. Nat. Rev. Immunol. 2004, 4:499-511.
2. Alexopoulou L., Holt A.C., Medzhitov R., Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001, 413:732-738.
3. Baoprasertkul P., Peatman E., Somridhivej B., Liu Z. Toll-like receptor 3 and TICAM genes in catfish: species-specific expression profiles following infection with Edwardsiella ictaluri. Immunogenetics 2006, 58:817-830.
4. Choi Y.J., Im E., Pothoulakis C., Rhee S.H. TRIF modulates TLR5-dependent responses by inducing proteolytic degradation of TLR5. J. Biol. Chem. 2010, 285:21382-21390.
5. Devaraj S., Dasu M.R., Rockwood J., Winter W., Griffen S.C., Jialal I. Increased Toll-like receptor (TLR) 2 and TLR4 expression in monocytes from patients with type 1 diabetes: further evidence of a proinflammatory state. J. Clin. Endocrinol. Metab. 2008, 93:578-583.
6. Fan S., Chen S., Liu Y., Lin Y., Liu H., Guo L., Lin B., Huang S., Xu A. Zebrafish TRIF, a Golgi-localized protein, participates in IFN induction and NF-kappaB activation. J. Immunol. 2008, 180:5373-5383.
7. Fiser A., Do R.K., Sali A. Modeling of loops in protein structures. Protein Sci. 2000, 9:1753-1773.
8. Fitzgerald K.A., Rowe D.C., Barnes B.J., Caffrey D.R., Visintin A., Latz E., Monks B., Pitha P.M., Golenbock D.T. LPS-TLR4 signaling to IRF-3/7 and NF-kappaB involves the toll adapters TRAM and TRIF. J. Exp. Med. 2003, 198:1043-1055.
9. Gauthier M.E., Du Pasquier L., Degnan B.M. The genome of the sponge Amphimedon queenslandica provides new perspectives into the origin of Toll-like and interleukin 1 receptor pathways. Evol. Dev. 2010, 12:519-533.
10. Gong J., Wei T., Stark R.W., Jamitzky F., Heckl W.M., Anders H.J., Lech M., Rossle S.C. Inhibition of Toll-like receptors TLR4 and 7 signaling pathways by SIGIRR: a computational approach. J. Struct. Biol. 2010, 169:323-330.
11. Gray P., Dunne A., Brikos C., Jefferies C.A., Doyle S.L., O'Neill L.A. MyD88 adapter-like (Mal) is phosphorylated by Bruton's tyrosine kinase during TLR2 and TLR4 signal transduction. J. Biol. Chem. 2006, 281:10489-10495.
12. Guindon S., Lethiec F., Duroux P., Gascuel O. PHYML Online-a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res. 2005, 33:W557-W559.
13. Horng T., Barton G.M., Medzhitov R. TIRAP: an adapter molecule in the Toll signaling pathway. Nat. Immunol. 2001, 2:835-841.
14. Horng T., Barton G.M., Flavell R.A., Medzhitov R. The adaptor molecule TIRAP provides signalling specificity for Toll-like receptors. Nature 2002, 420:329-333.
15. Huang S., Yuan S., Guo L., Yu Y., Li J., Wu T., Liu T., Yang M., Wu K., Liu H., Ge J., Huang H., Dong M., Yu C., Chen S., Xu A. Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity. Genome Res. 2008, 18:1112-1126.
16. Irazoqui J.E., Urbach J.M., Ausubel F.M. Evolution of host innate defence: insights from Caenorhabditis elegans and primitive invertebrates. Nat. Rev. Immunol. 2010, 10:47-58.
17. Jenkins K.A., Mansell A. TIR-containing adaptors in Toll-like receptor signalling. Cytokine 2010, 49:237-244.
18. Jiang Z., Mak T.W., Sen G., Li X. Toll-like receptor 3-mediated activation of NF-kappaB and IRF3 diverges at Toll-IL-1 receptor domain-containing adapter inducing IFN-beta. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:3533-3538.
19. Kagan J.C., Medzhitov R. Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling. Cell 2006, 125:943-955.
20. Kasamatsu J., Oshiumi H., Matsumoto M., Kasahara M., Seya T. Phylogenetic and expression analysis of Lamprey Toll-like receptors. Dev. Comp. Immunol. 2010.
21. Keestra A.M., van Putten J.P. Unique properties of the chicken TLR4/MD-2 complex: selective lipopolysaccharide activation of the MyD88-dependent pathway. J. Immunol. 2008, 181:4354-4362.
22. Kumar H., Kawai T., Akira S. Toll-like receptors and innate immunity. Biochem. Biophys. Res. Commun. 2009, 388:621-625.
23. Laskowski R.A., Rullmannn J.A., MacArthur M.W., Kaptein R., Thornton J.M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 1996, 8:477-486.
24. Li G., Zhang J., Sun Y., Wang H., Wang Y. The evolutionarily dynamic IFN-inducible GTPase proteins play conserved immune functions in vertebrates and cephalochordates. Mol. Biol. Evol. 2009, 26:1619-1630.
25. Liu Y., Li M., Fan S., Lin Y., Lin B., Luo F., Zhang C., Chen S., Li Y., Xu A. A unique feature of Toll/IL-1 receptor domain-containing adaptor protein is partially responsible for lipopolysaccharide insensitivity in zebrafish with a highly conserved function of Myd88. J. Immunol. 2010, 185:3391-3400.
26. Lobley A., Sadowski M.I., Jones D.T. pGenTHREADER and pDomTHREADER: new methods for improved protein fold recognition and superfamily discrimination. Bioinformatics 2009, 25:1761-1767.
27. Loiarro M., Capolunghi F., Fanto N., Gallo G., Campo S., Arseni B., Carsetti R., Carminati P., De Santis R., Ruggiero V., Sette C. Pivotal advance: inhibition of MyD88 dimerization and recruitment of IRAK1 and IRAK4 by a novel peptidomimetic compound. J. Leukoc. Biol. 2007, 82:801-810.
28. Mansell A., Brint E., Gould J.A., O'Neill L.A., Hertzog P.J. 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.
29. 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.
30. Matsuo A., Oshiumi H., Tsujita T., Mitani H., Kasai H., Yoshimizu M., Matsumoto M., Seya T. Teleost TLR22 recognizes RNA duplex to induce IFN and protect cells from birnaviruses. J. Immunol. 2008, 181:3474-3485.
31. McGettrick A.F., Brint E.K., Palsson-McDermott E.M., Rowe D.C., Golenbock D.T., Gay N.J., Fitzgerald K.A., O'Neill L.A. Trif-related adapter molecule is phosphorylated by PKC{epsilon} during Toll-like receptor 4 signaling. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:9196-9201.
32. McLaughlin S., Wang J., Gambhir A., Murray D. PIP(2) and proteins: interactions, organization, and information flow. Annu. Rev. Biophys. Biomol. Struct. 2002, 31:151-175.
33. Meijer A.H., Gabby Krens S.F., Medina Rodriguez I.A., He S., Bitter W., Ewa Snaar-Jagalska B., Spaink H.P. Expression analysis of the Toll-like receptor and TIR domain adaptor families of zebrafish. Mol. Immunol. 2004, 40:773-783.
34. Meylan E., Burns K., Hofmann K., Blancheteau V., Martinon F., Kelliher M., Tschopp J. RIP1 is an essential mediator of Toll-like receptor 3-induced NF-kappa B activation. Nat. Immunol. 2004, 5:503-507.
35. Nunez Miguel R., Wong J., Westoll J.F., Brooks H.J., O'Neill L.A., Gay N.J., Bryant C.E., Monie T.P. A dimer of the Toll-like receptor 4 cytoplasmic domain provides a specific scaffold for the recruitment of signalling adaptor proteins. PLoS One 2007, 2:e788.
36. Ohnishi H., Tochio H., Kato Z., Orii K.E., Li A., Kimura T., Hiroaki H., Kondo N., Shirakawa M. Structural basis for the multiple interactions of the MyD88 TIR domain in TLR4 signaling. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:10260-10265.
37. Oshiumi H., Matsumoto M., Funami K., Akazawa T., Seya T. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat. Immunol. 2003, 4:161-167.
38. Oshiumi H., Sasai M., Shida K., Fujita T., Matsumoto M., Seya T. 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.
39. Oshiumi H., Matsuo A., Matsumoto M., Seya T. Pan-vertebrate Toll-like receptors during evolution. Curr. Genomics 2008, 9:488-493.
40. Peng J., Yuan Q.A., Lin B., Panneerselvam P., Wang X.W., Luan X.L., Lim S.K., Leung B.P., Ho B., Ding J.L. SARM inhibits both TRIF- and MyD88-mediated AP-1 activation. Eur. J. Immunol. 2010, 40:1738-1747.
41. Phillips J.C., Braun R., Wang W., Gumbart J., Tajkhorshid E., Villa E., Chipot C., Skeel R.D., Kale L., Schulten K. Scalable molecular dynamics with NAMD. J. Comput. Chem. 2005, 26:1781-1802.
42. Putnam N.H., Butts T., Ferrier D.E., Furlong R.F., Hellsten U., Kawashima T., Robinson-Rechavi M., Shoguchi E., Terry A., Yu J.K., Benito-Gutierrez E.L., Dubchak I., Garcia-Fernandez J., Gibson-Brown J.J., Grigoriev I.V., Horton A.C., de Jong P.J., Jurka J., Kapitonov V.V., Kohara Y., Kuroki Y., Lindquist E., Lucas S., Osoegawa K., Pennacchio L.A., Salamov A.A., Satou Y., Sauka-Spengler T., Schmutz J., Shin I.T., Toyoda A., Bronner-Fraser M., Fujiyama A., Holland L.Z., Holland P.W., Satoh N., Rokhsar D.S. The amphioxus genome and the evolution of the chordate karyotype. Nature 2008, 453:1064-1071.
43. Ribeiro C.M., Hermsen T., Taverne-Thiele A.J., Savelkoul H.F., Wiegertjes G.F. Evolution of recognition of ligands from Gram-positive bacteria: similarities and differences in the TLR2-mediated response between mammalian vertebrates and teleost fish. J. Immunol. 2010, 184:2355-2368.
44. Rowe D.C., McGettrick A.F., Latz E., Monks B.G., Gay N.J., Yamamoto M., Akira S., O'Neill L.A., Fitzgerald K.A., Golenbock D.T. The myristoylation of TRIF-related adaptor molecule is essential for Toll-like receptor 4 signal transduction. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:6299-6304.
45. Sasai M., Tatematsu M., Oshiumi H., Funami K., Matsumoto M., Hatakeyama S., Seya T. Direct binding of TRAF2 and TRAF6 to TICAM-1/TRIF adaptor participates in activation of the Toll-like receptor 3/4 pathway. Mol. Immunol. 2010, 47:1283-1291.
46. Seya T., Matsumoto M., Ebihara T., Oshiumi H. Functional evolution of the TICAM-1 pathway for extrinsic RNA sensing. Immunol. Rev. 2009, 227:44-53.
47. Sullivan C., Postlethwait J.H., Lage C.R., Millard P.J., Kim C.H. Evidence for evolving Toll-IL-1 receptor-containing adaptor molecule function in vertebrates. J. Immunol. 2007, 178:4517-4527.
48. Sullivan C., Charette J., Catchen J., Lage C.R., Giasson G., Postlethwait J.H., Millard P.J., Kim C.H. The gene history of zebrafish tlr4a and tlr4b is predictive of their divergent functions. J. Immunol. 2009, 183:5896-5908.
49. Takaki H., Oshiumi H., Sasai M., Kawanishi T., Matsumoto M., Seya T. Oligomerized TICAM-1 (TRIF) in the cytoplasm recruits nuclear BS69 to enhance NF-kappaB activation and type I IFN induction. Eur. J. Immunol. 2009, 39:3469-3476.
50. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
51. Verstak B., Nagpal K., Bottomley S.P., Golenbock D.T., Hertzog P.J., Mansell A. MyD88 adapter-like (Mal)/TIRAP interaction with TRAF6 is critical for TLR2- and TLR4-mediated NF-kappaB proinflammatory responses. J. Biol. Chem. 2009, 284:24192-24203.
52. Yamamoto M., Sato S., Hemmi H., Sanjo H., Uematsu S., Kaisho T., Hoshino K., Takeuchi O., Kobayashi M., Fujita T., Takeda K., Akira S. Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4. Nature 2002, 420:324-329.
53. Yamamoto M., Sato S., Hemmi H., Hoshino K., Kaisho T., Sanjo H., Takeuchi O., Sugiyama M., Okabe M., Takeda K., Akira S. Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science 2003, 301:640-643.
54. Yamamoto M., Sato S., Hemmi H., Uematsu S., Hoshino K., Kaisho T., Takeuchi O., Takeda K., Akira S. TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nat. Immunol. 2003, 4:1144-1150.
55. Yoneyama M., Kikuchi M., Natsukawa T., Shinobu N., Imaizumi T., Miyagishi M., Taira K., Akira S., Fujita T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 2004, 5:730-737.
56. Yoneyama M., Kikuchi M., Matsumoto K., Imaizumi T., Miyagishi M., Taira K., Foy E., Loo Y.M., Gale M., Akira S., Yonehara S., Kato A., Fujita T. Shared and unique functions of the DExD/H-box helicases RIG-I. MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 2005, 175:2851-2858.
57. Zou J., Chang M., Nie P., Secombes C.J. Origin and evolution of the RIG-I like RNA helicase gene family. BMC Evol. Biol. 2009, 9:85.