Interleukin-1 receptor-associated kinase-1 (IRAK-1): A self-regulatory adapter molecule in the signaling cascade of the Toll/IL-1 receptor family

Signal Transduction

Volumn 1, Issue 1-2, 2001, Pages 37-50

  Martin, Michael U ^a   Kollewe, Christian ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

IL 1 receptor family; IL 1 signaling; Innate immunity; IRAK; Kinases; Signal transduction

Indexed keywords

EID: 0000126250     PISSN: 16154053     EISSN: None     Source Type: Journal    
DOI: 10.1002/1615-4061(200111)1:1/2<37::aid-sita37>3.0.co;2-k     Document Type: Article

References (88)

1. O'Neill, L. A., Dinarello, C. A. (2000) The IL-1 receptor/toII-like superfamily: crucial receptors for inflammation and host defense. Immunol. Today 21: 206-209.
2. Schwandner, R., Yamaguchi, K., Cao, Z. (2000) Requirement of tumor necrosis factor receptor-associated factor (TRAF6) in interleukin 17 signal transduction. J. Exp. Med. 191: 1233-1240.
3. Lomaga, M. A., Yeh, W.-C., Sarosi, I., Duncan, G. S., Furlonger, C., Ho, A., Morony, S., Capparelli, C., Van, G., Kaufman, S., van der Heiden, A., Itie, A., Wakeham, A., Khoo, W., Sasaki, T., Cao, Z., Penninger, J. M., Paige, C. J., Lacey, D. L., Dunstan, C. R., Boyle, W. J., Goeddel, D. V., Mak, T. W. (1999) TRAF6 deficiency results in osteopetrosis and defective inferleukin-1, CD40 and LPS signaling. Genes Dev. 13: 1015-1024.
4. Cao, Z., Henzel, W. J., Gao, X. (1996) IRAK: A kinase associated with the Interleukin-1 receptor. Science 271: 1128-1131.
5. Jensen, L. E., Whitehead, A. S. (2001) IRAK1b, a novel alternative splice variant of interleukin-1 receptor associated kinase (IRAK), mediates interleukin-1 signaling and has prolonged stability. J. Biol. Chem. published online June 7, 2001, M103815200.
6. Muzio, M. Ni, J., Feng, P., Dixit, V. (1997) IRAK (Pelle) Family Member IRAK-2 and MyD88 as Proximal Mediators of IL-2 Signaling. Science 278: 1612-1615.
7. Wesche, H., Gao, X., Li, X., Kirschning, C. J., Stark, G. R., Cao, Z. (1999) IRAK-M is a novel member of the Pelle/ Interleukin-1 Receptor-associated Kinase (IRAK) family. J. Biol. Chem. 274: 19403-19410.
8. Rich, T., Allen, R. A., Lucas, A.-M., Stewart, A., Trowsdale, J. (2000) Pellino-related sequences from Caenorhabditis elegans and Homo sapiens. Immunogenetics 52: 145-149.
9. Burns, K., Cladworthy, J., Martin, L., Martinon, F., Plumpton, C., Maschera, B., Lewis, A., Ray, K., Tschopp, J., Volpe, F. (2000) Tollip, a new component of the IL-1RI pathway, links IRAK to the IL-1 receptor. Nature Cell Biology 2: 346-351.
10. Vig, E., Green, M., Liu, Y., Yu, K-Y., Kwon, H-J., Tian, J., Goebl, M. K., Harrington, M. A. (2001) SIMPL is a Tumor Necrosis Factor-specific regulator of nuclear factor-κB activity. J. Biol. Chem. 276: 7859-7866.
11. Malinin, N. L., Boldin, M. P., Kovalenko, A. V., Wallach, D. (1997) MAP3K-related kinase involved in NF-κB induction by TNF, CD95 and IL-1. Nature 385: 540-544.
12. Yin, L., Wu, L., Wesche, H., Arthur, C. D., White, J. M., Goeddel, D. V., Schreiber, R. D. (2001) Defective lymphotoxin-β receptor-induced NF-κB transcriptional activity in NIK-deficient mice. Science 291: 2162-2165.
13. Ling, L., Goeddel, D. V. (2000) T6BP, a TRAF6-interacting protein involved in IL-1 signaling. Proc. Natl. Acad. Sci. U.S.A. 97: 9567-9572.
14. Kopp, E., Medzhitov, R., Carothers, J., Xiao, C., Douglas, I., Janeway, C.A., Ghosh, S. (1999) ECSIT is an evolutionary conserved intermediate in the ToII/IL-1 signal transduction pathway. Genes Dev. 13: 2059-2071.
15. Sanz, L., Diaz-Meco, M. T., Nakano, H., Moscat, J. (2000) The atypical PKC-interacting protein p62 channels NF-κB activation by the IL-1-TRAF6 pathway. EMBO J. 19: 1576-1586.
16. Ninomiya-Tsuji, J., Kishimoto, K., Hiyama, A., Inoue, J., Cao, Z., Matsumoto, K. (1999) The kinase TAK1 can activate the NIK-I κB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature 398: 252-256.
17. Kishimoto, K., Matsumoto, K., Ninomiya-Tsuji, J. (2000) TAK1 mitogen-activated protein kinase kinase kinase is activated by autophosphorylation within its activation loop. J. Biol. Chem. 275: 7359-7364.
18. Takaesu, G., Kisnida, S., Hiyama, A., Yamaguchi, K., Shibuya, H., Irie, K., Ninomiya-Tsuji, J., Matsumoto, K. (2000) TAB2, a novel adaptor protein, mediates activation of TAK1 MAPKKK by linking TAK1 to TRAF6 in the IL-1 signal transduction pathway. Mol. Cell. 5: 649-658.
19. Mochida, Y., Takeda, K., Saitoh, M., Nishitoh, H., Amagasa, T., Ninomiya-Tsuji, J., Matsumoto, K., Ichijo, H. (2000) ASK1 inhibits interleukin-1-induced NF-κB activity through disruption of TRAF6-TAK1 interaction. J. Biol. Chem. 275: 32747-32752.
20. Hanada, M., Ninomiya-Tsuji, J., Komaki, K., Ohnishi, M., Kastura, K., Kanamaru, R., Mastumoto, K, Tamura, S. (2001) Regulation of the TAK1 signaling pathway by protein phosphatase 2C. J. Biol. Chem. 276: 5753-5759.
21. Martin, M., Böl, G. F., Eriksson, A., Resch, K., Brigelius-Flohé, R. (1994) Interleukin-1 induced activation of a protein kinase co-precipitating with the type I IL-1 receptor in T cells. Eur. J. Immunol. 24: 1566-1571.
22. Croston, G. E., Cao, Z., Goeddel, D. V. (1995) NF-κB Activation by Interleukin-1 (IL-1) Requires an IL-1 Receptor-associated Protein Kinase Activity. J. Biol. Chem. 270: 16514-16517.
23. Shelton, C. A., Wasserman, S. A. (1993) Pelle encodes a protein kinase required to establish dorsoventral polarity in Drosophila embryo. Cell 72: 515-525.
24. Großhans, J., Bergmann, A., Haffter, P., Nüsslein-Volhard, G. (1994) Activation of the kinase Pelle by Tube in the dorsoventral signal transduction pathway of Drosophila embryo. Nature 372: 563-566.
25. Trofimova, M., Sprenkle, A. B., Green, M., Sturgill, T. W., Gobel, M. G., Harrington, M. A. (1996) Development and Tissue-specific Expression of Mouse Pelle-like Kinase. J. Biol. Chem. 271: 17609-17612.
26. Loh, Y.-T., Martin, G. B. (1995) The Pto bacterial resistance gene and the Fen insecticide sensitivity gene encode functional protein kinases with serine/threonine specificity. Plant Physiol. 108: 1735-1739.
27. Kimbrell, D. A., Beutler, B. (2001) The evolution and genetics of innate immunity. Nat. Rev. Genet. 2: 256-267.
28. O'Neill, L. A. (2000) The ToII/interleukin-1 receptor domain: a molecular switch for inflammation and host defence. Biochem. Soc. Transaction. 28: 557-563.
29. Sessa, G., Martin, G. B. (2000) Signal recognition and transduction mediated by the tomato Pto kinase: a paradigm of innate immunity in plants. Microbes. Infect. 2: 1591-1597.
30. Khush, R. S., Lemaitre, B. (2000) Genes that fight infection: what the Drosophila genome says about animal immunity. Trends Genet. 26: 442-229.
31. Tauszig, S., Jouanguy, E., Hoffmann, J. A., Imler, J.-L. (2000) ToII-related receptors and the control of antimicrobial peptide expression in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 97: 10520-10525.
32. Brenner, V., Nyakatura, G., Rosenthal, A., Platzer, M. (1997) Genomic organization of the two novel genes on human Xq28: compact head to head arrangement of IDH gamma and TRAP delta is conserved in rat and mouse. Genomics 44: 8-14.
33. Reichwald, K., Thiesen, J., Wiehe, T., Weitzel, J., Strätling, W. H., Kioschis, P., Poustka, A., Rosenthal, A., Platzer, M. (2000) Comparative sequence analysis of the MECP2-locus in human and mouse reveals new transcribed regions. Mamm. Genome. 11: 182-190.
34. Thomas, J. A., Allen, J. L., Tsen, M., Dubnicoff, T., Danao, J., Liao, X. C., Cao, Z., Wasserman, S. A. (1999). Impaired cytokine signaling in mice lacking the IL-1 receptor-associated kinase. J. Immunol. 163: 978-984.
35. Centanni, J. M., de Miguel, M., Gopalan, G., Gilbert, D. J., Copeland, N. G., Jenkins, N. A., Donovan, P. J. (1998) Interleukin-1 receptor-associated kinase gene III1 rak maps to the mouse X chromosome. Mamm. Genome 9: 340-341.
36. Maschera, B., Ray, K., Burns, K., Volpe, F. (1999) Overexpression of an enzymatically inactive interleukin-1 receptor-associated kinase activates nuclear factor-κB. Biochem. J. 339: 227-231.
37. Rechsteiner, M., Rogers, S. W. (1996) PEST sequences and regulation by proteolysis. TIBS 21: 267-271.
38. Yamin, T.-T., Miller, D. K. (1997) The Interleukin-1 Receptor-associated Kinase is degraded by proteasomes following its phosphorylation. J. Biol. Chem. 272: 21540-2547.
39. Li, X., Commane, M., Jiang, Z., Stark, G. (2001) IL-1-induced NFκB and c-Jun N-terminal kinase (JNK) activation diverges at the IL-1 receptor-associated kinase (IRAK). Proc. Natl. Acad. Sci. U.S.A. 98: 4461-4465.
40. Greenfeder, S. A., Nunes, P., Kwee, L., Labow, M., Chizzonite, R. A., Ju, G. (1995) Molecular cloning and characterization of a second subunit of the Interleukin 1 receptor complex. J. Biol. Chem. 270: 13757-13765.
41. Wesche, H., Korherr, C., Kracht, M. Falk, W., Resch, K., Martin, M. U. (1997) The Interleukin-1 receptor accessory protein (IL-IRAcP) is essential for IL-1 induced activation of Interleukin-1 receptor associated protein kinase (IRAK) and stress activated protein kinases (SAP-kinases). J. Biol. Chem. 277: 7727-7731.
42. Korherr, C., Hofmeister, R., Wesche, H., Falk, W. (1997) A critical role for interleukin-1 receptor accessory protein in interleukin-1 signaling. Eur. J. Immunol. 27: 262-267.
43. Huang, J., Gao, X., Li, S., Cao, Z. (1997) Recruitment of IRAK of the interleukin 1 receptor complex requires interleukin 1 receptor accessory protein. Proc. Natl. Acad. Sci. U.S.A. 94: 12829-12832.
44. Cullinan, E. B., Kwee, L., Nunes, P., Shuster, D. J., Ju, G., McIntyre, K. W., Chizzonite, R. A., Labow, M. A. (1998) IL-1 receptor accessory protein is an essential component of the IL-1 receptor. J. Immunol. 161: 5614-5620.
45. Born, T. L., Thomassen, E., Bird, T. A., Sims, J. E. (1998) Cloning of a novel receptor subunit, AcPL, required for interleukin-18 signaling. J. Biol. Chem. 273: 29445-29450.
46. Thomassen, E., Bird, T. A., Renshaw, B. R., Kennedy, M. K., Sims, J. E. (1998) Binding of interleukin-18 to the interleukin-1 receptor homologous receptor IL-1Rrp1 leads to activation of signaling pathways similar to those used by interleukin-1. J. Interferon Cytokine Res. 18: 1077-1088
47. Wyllie, D. H., Kiss-Toth, E., Visitin, A., Smith, S. C., Boussouf, S., Segal, D. M., Duff, G. W., Dower, S. K. (2000) Evidence for an accessory protein function for ToII-like receptor 1 in anti-bacterial responses. J. Immunol. 165: 7125-7132.
48. Hajjar, A. M., O'Mahony, D. S., Ozinsky, A., Underhill, D. M., Aderem, A., Klebanoff, S. J., Wilson, C. B. (2001 ) Functional interactions between ToII-like receptor (TLR) 2 and TLR1 or TLR6 in response to phenol-soluble modulin. J. Immunol. 166: 15-19.
49. Medzhitov, R., Preston-Hurlburt, P., Chaneway Jr., J. (1997) A human homologue of Drosophila ToII protein signals activation of adaptive immunity. Nature 388: 394-397.
50. Gay, N. J., Keith, F. J. (1991) Drosophila ToII and IL-1 receptor. Nature 351: 355-356.
51. Schneider, D. S., Hudson, K. L., Lin, T. Y., Anderson, K. V. (1991) Dominant and recessive mutations define functional domains of ToII, a transmembrane protein required for dorsal-ventral polarity in the Drosophila embryo. Genes. Dev. 5: 797-807.
52. Xu, Y., Tao, X., Shen, B., Horng, T., Medzhitov, R., Manley, J. L., Tong, L. (2000) Structural basis for signal transduction by the ToII/interleukin-1 receptor domains. Nature 408: 111-115.
53. Colotta, F., Dower, S. K., Sims, J. E., Mantovani, A. (1994) The type II 'decoy' receptor: a novel regulatory pathway for interleukin-1. Immunol. Today 15: 562-566.
54. Lang, D., Knop, J., Wesche, H., Raffetseder, U., Kurrle, R., Boraschi, D., Martin, M. U. (1998) The type II IL-1 Receptor interacts with the IL-1 Receptor Acessory Protein: A novel mechanism of regulation of IL-1 responsiveness. J. Immunol. 161: 6871-6877.
55. Wesche, H., Henzel, W. J., Shillinglaw, W., Li, S., Cao, Z. (1997) MyD88: an adapter that recruits IRAK to the IL-1 receptor complex. Immunity 7: 837-847.
56. Burns, K., Martinon, F., Esslinger, C., Pahl, H., Schneider, P., Bodmer, J.-L., Di Marco, F., French, L., Tschopp, J. (1998) MyD88, an adaptor protein involved in interleukin-1 signaling. J. Biol. Chem. 273: 12203-12209.
57. Hultmark, D. (1994) Macrophage differentiation marker MyD88 is a member of the ToII/IL-1 receptor family. Biochem. Biophys. Res. Commun. 199: 144-146.
58. Adachi, O., Kawai, T., Takeda, K., Matsumoto, M., Tsutsui, H., Sakagmi, M., Nakanishi, K., Akira, S. (1998) Targeted disruption of the MyD88 gene results in the loss of IL-1-and IL-18-mediated function. Immunity 9: 143-150.
59. Seki, E., Tsutsui, H., Nakano, H., Tsuji, N., Hoshino, K., Adachi, O., Adachi, K., Futatsugi, S., Kuida, K., Takeuchi, O., Okamura, H., Fujimoto, J., Akira, S., Nakanishi, K. (2001) Lipopolysaccharide-induced IL-18 secretion from murine Kupffer cells independently of myeloid differentiation factor 88 that is critically involved in induction of production of IL-12 and IL-1β. J. Immunol. 166: 2651-2657.
60. Xiao, T., Towb, P., Wasserman, S. A., Sprang, S. R. (1999) Three-dimensional structure of a complex between the death domains of Pelle and Tube. Cell 99: 545-555.
61. Cao, Z., Xiong, J., Takeuchi, M., Kurama, T., Goeddel, D. V. (1996) TRAF6 is a signal transducer for interleukin-1. Nature 383: 443-446.
62. Takaesu, G., Ninomiya-Tsuji, J., Kishida, S., Li, X. Stark, G. R., Matsumoto, K. (2001) Interleukin-1 (il-1) receptor-associated kinase leads to activation of tak1 by inducing tab2 translocation in the il-1 signaling pathway. Mol. Cell. Biol. 7: 2475-2484.
63. Singh, R., Huang, S., Guth, T., Konieczkowski, M., Sedor, J. R. (1997) Cytosolic domain of the type I Interleukin-1 receptor spontaneously recruits signaling molecules to activate a proinflammatory gene. J. Clin. Invest. 100: 419-428.
64. Knop, J., Martin, M. U. (1999) Effects of the IL-1 receptor associated kinase (IRAK) expression on IL-1 signaling are independent of its' kinase activity. FEBS Letters 448: 81-85.
65. Li, X., Commane, M., Burns, C., Vithalani, K., Cao, Z., Stark, G. (1999) Mutant cells that do not respond to Interleukin-1 (IL-1) reveal a novel role for the IL-1 receptor-associated kinase. Mol. Cell. Biol. 19: 4643-4652.
66. Vig, E., Green, M., Liu, Y., Donner, D. B., Mukaida, N., Goebl, M. G., Harrington, M. A. (1999) Modulation of Tumor Necrosis Factor and Interleukin-1 dependent NF-κB activity by mPLK/IRAK. J. Biol. Chem. 274: 13077-13084.
67. Shen, B., Manley, J. L. (1998) Phosphorylation modulates direct interactions between the ToII receptor, Pelle kinase and Tube. Development 125: 4719-4728.
68. Großhans, J., Schnorrer, F., Nüsslein-Volhard, C. (1999) Oligomerisation of Tube and Pelle leads to nuclear localisation of Dorsal. Mech. Dev. 81: 127-138.
69. Knop, J., Wesche, H., Lang, D., Martin, M. U. (1998) Effects of overexpression of IL-1 receptor associated kinase on NFκB activation, IL-2 production and stress-activated protein kinases in the murine T cell line EL-4. Eur. J. Immunol. 28: 3100-3109.
70. Park, Y. C., Burkitt, V., Villa, A. R., Tong, L., Wu, H. (1999) Structural basis for self-association and receptor recognition of human TRAF2. Nature 398: 533-538.
71. Baud, V., Liu, Z-G., Bennett, B., Suzuki. N., Xia, Y., Karin, M. (1999) Signaling by proinflammatory cytokines: oligomerization of TRAF2 and TRAF6 is sufficient for JNK and IKK activation and target gene induction via an amino-terminal effector domain. Genes Dev. 13: 1297-1308.
72. Schmidt, A., Caron, E., Hall, A. (2001) Lipopolysaccharide-induced activation of β2-integrin function in macrophages requires Irak kinase activity, P38 mitogen-activated protein kinase, and the Rap1 GTPase. Mol. Cell. Biol. 21: 438-448.
73. Hanks, S.K., Hunter, T. (1995) The eukaryotic proteinkinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 9: 576-595.
74. Johnson, L. N., Noble, M. E. M., Owen, D. J. (1998) Active and inactive protein kinases: Structrual basis for regulation. Cell 85: 149-158.
75. Deng, L., Wang, C., Spencer, E., Yang, L., Braun, A., You, J., Slaughter, C., Pickart, C., Chen, Z. J. (2000) Activation of the IκB Kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103: 351-361.
76. Guo, F., Wu, S. (2000) IRAK-2 and P13-Kinase synergistically activate NF-κB and AP-1. Inflammation 24: 305-316.
77. Guo, F. K., Li, Y. L., Wu, S. G. (2000) Antisense IRAK-2 oligodeoxynucleotides inhibits interleukin-1-induced nuclear factor-κ B activation in vitro. Acta Pharmacol. Sin. 21: 318-320.
78. O'Neill, L. A., Greene, C. (1998) Signal transduction pathways activated by the IL-1 receptor family: ancient signaling machinery in mammals, insects, and plants. J. Leukoc. Biol. 63: 650-657.
79. Hofmeister, R., Wiegmann K., Korherr, C., Bernardo, K., Krönke, M., Falk, W. (1997) Activation of acid sphingomyelinase by Interleukin-1 requires IL-1 receptor accessory protein. J. Biol. Chem. 272: 27730-22736.
80. Reddy, S. A., Huang, J. H., Liao, W. S. (1997) Phosphatidylinositol 3-kinase in interleukin 1 signaling. Physical interaction with the interleukin-1 receptor and requirement in NFκB and AP-1 activation. J. Biol. Chem. 272: 29167-19173.
81. Sizemore, N., Leung, S., Stark, G. R. (1999) Activation of phosphatidylinositol 3-kinase in response to interleukin-1 leads to phosphorylation and activation of the NF-κB p65/ RelA subunit. Mol. Cell. Biol. 19: 4798-4805.
82. Marmiroli, S., Bavelloni, A., Faenzy, I., Sirri, A., Ognibene, A., Cenni, V., Tsukada, J., Koyama, Y., Ruzzene, M., Ferri, A., Auron, P.E., Toker, A., Maraldi, N.M. (1998) Phosphatidylinositol 3-kinase is recruited to a specific site in the activated IL-1 receptor I. FEBS Lett. 438: 49-54.
83. Bavelloni, A., Santi, S., Sirri, A., Riccio, M., Faenza, I., Zini, N., Cecchi, S., Ferri, A., Auron, P. E., Maraldi, N. M., Marmiroli, S. (1999) Phosphatidylinositol 3-kinase translocation to the nucleus is induced by interleukin-1 and prevented by mutation of interleukin-1 receptor in human osteosarcoma Saos-2 cells. J. Cell Sci. 112: 631-640.
84. Magde, L. A., Pober, J. S. (2000) A phosphatidylinositol 3-kinase/Akt pathway, activated by tumor necrosis factor or interleukin-1, inhibits apoptosis but does not activtae NFκB in human endothelial cells. J. Biol. Chem. 275: 15458-15465.
85. Böl, G. F., Kreuzer, O. J., Brigelius-Flohé, R. (2000) Translocation of the interleukin-1 receptor-associated kinase-1 (IRAK-1) into the nucleus. FEBS Lett. 477: 73-78.
86. Kanakaraj, P., Schafer, P. H., Cavender, D. E., Wu, Y., Ngo, K., Grealish, P. F., Wadsworth, S. A., Peterson, P. A., Siekierka, J. J., Harris, C. A., Fung-Leung, W. P. (1998) Interleukin (IL)-1 receptor-associated kinase (IRAK) requirement for optimal induction of multiple IL-1 signaling pathways and IL-6 production. J. Exp. Med. 187: 2073-2079.
87. Kanakaraj, P., Ngo, K., Wu, Y., Angulo, A., Ghazal, P., Harris, C. A., Siekierka, J. J., Peterson, P. A., Fung-Leung, W. (1999) Defective interieukin (IL)-18-mediated natural killer and T helper cell type 1 responses in IL-1 receptor-asscoiated kinase (IRAK)-deficient mice. J. Exp. Med. 189: 1129-1138.
88. Bowie, A., Kiss-Toth, E., Symons, J. K., Smith, G. L., Dower, S. K., O'Neill L. A. (2000) A46R and A52R from vaccinia virus are antagonists of host IL-1 and toII-like receptor signaling. Proc. Natl. Acad. Sci. U.S.A. 97: 10162-10167.