Interleukin-1 receptor-associated kinase (IRAK) -1-mediated NF-κB activation requires cytosolic and nuclear activity

FASEB Journal

Volumn 22, Issue 7, 2008, Pages 2285-2296

  Liu, Gang ^a   Park, Young Jun ^a   Abraham, Edward ^a,b  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

Author keywords

Histone H3; Nuclear translocation; Toll like receptor; Transcription

Indexed keywords

EXPORTIN 1; HISTONE H3; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; LIPOPOLYSACCHARIDE; SERINE; TOLL LIKE RECEPTOR;

ARTICLE; CELL STIMULATION; CONTROLLED STUDY; ENZYME BINDING; ENZYME INDUCTION; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION;

ANIMALS; BASE SEQUENCE; BREAST NEOPLASMS; CELL LINE; CELL LINE, TUMOR; CELL NUCLEUS; CYTOSOL; DNA PRIMERS; FEMALE; HUMANS; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; KIDNEY; MACROPHAGES; MICE; MOLECULAR SEQUENCE DATA; NF-KAPPA B; RNA, MESSENGER;

EID: 46749110737     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.07-101816     Document Type: Article

References (59)

1. Gan, L., and Li, L. (2006) Regulations and roles of the interleukin-1 receptor associated kinases (IRAKs) in innate and adaptive immunity. Immunol. Res. 35, 295-302
2. Janssens, S., and Beyaert, R. (2003) Functional diversity and regulation of different interleukin-1 receptor-associated kinase (IRAK) family members. Mol. Cell 11, 293-302
3. O'Neill, L. (2000) The Toll/interleukin-1 receptor domain: a molecular switch for inflammation and host defence. Biochem. Soc. Trans. 28, 557-563
4. O'Neill, L. A. (2006) How Toll-like receptors signal: what we know and what we don't know. Curr. Opin. Immunol. 18, 3-9
5. Yamamoto, M., Takeda, K., and Akira, S. (2004) TIR domain-containing adaptors define the specificity of TLR signaling. Mol. Immunol. 40, 861-868
6. Akira, S., Uematsu, S., and Takeuchi, O. (2006) Pathogen recognition and innate immunity. Cell 124, 783-801
7. Honda, K., and Taniguchi, T. (2006) IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat. Rev. Immunol. 6, 644-658
8. Medzhitov, R. (2001) Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1, 135-145
9. Moynagh, P. N. (2005) TLR signalling and activation of IRFs: revisiting old friends from the NF-κB pathway. Trends Immunol. 26, 469-476
10. Trinchieri, G., and Sher, A. (2007) Cooperation of Toll-like receptor signals in innate immune defence. Nat. Rev. Immunol. 7, 179-190
11. Burns, K., Clatworthy, J., Martin, L., Martinon, F., Plumpton, C., Maschera, B., Lewis, A., Ray, K., Tschopp, J., and Volpe, F. (2000) Tollip, a new component of the IL-1RI pathway, links IRAK to the IL-1 receptor. Nat. Cell Biol. 2, 346-351
12. Burns, K., Martinon, F., Esslinger, C., Pahl, H., Schneider, P., Bodmer, J. L., Di Marco, F., French, L., and Tschopp, J. (1998) MyD88, an adapter protein involved in interleukin-1 signaling. J. Biol. Chem. 273, 12203-12209
13. Huang, J., Gao, X., Li, S., and Cao, Z. (1997) Recruitment of IRAK to the interleukin 1 receptor complex requires interleukin 1 receptor accessory protein. Proc. Natl. Acad. Sci. U. S. A. 94, 12829-12832
14. Medzhitov, R., Preston-Hurlburt, P., Kopp, E., Stadlen, A., Chen, C., Ghosh, S., and Janeway, C. A., Jr. (1998) MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol. Cell 2, 253-258
15. Muzio, M., Ni, J., Feng, P., and Dixit, V. M. (1997) IRAK (Pelle) family member IRAK-2 and MyD88 as proximal mediators of IL-1 signaling. Science 278, 1612-1615
16. Wesche, H., Henzel, W. J., Shillinglaw, W., Li, S., and Cao, Z. (1997) MyD88: an adapter that recruits IRAK to the IL-1 receptor complex. Immunity 7, 837-847
17. Burns, K., Janssens, S., Brissoni, B., Olivos, N., Beyaert, R., and Tschopp, J. (2003) Inhibition of interleukin 1 receptor/Toll-like receptor signaling through the alternatively spliced, short form of MyD88 is due to its failure to recruit IRAK-4. J. Exp. Med. 197, 263-268
18. Li, S., Strelow, A., Fontana, E. J., and Wesche, H. (2002) IRAK-4: a novel member of the IRAK family with the properties of an IRAK-kinase. Proc. Natl. Acad. Sci. U. S. A. 99, 5567-5572
19. Suzuki, N., Suzuki, S., and Yeh, W. C. (2002) IRAK-4 as the central TIR signaling mediator in innate immunity. Trends Immunol. 23, 503-506
20. Chen, Z. J. (2005) Ubiquitin signalling in the NF-κB pathway. Nat. Cell Biol. 7, 758-765
21. Li, X., Commane, M., Jiang, Z., and Stark, G. R. (2001) IL-1-induced NF-κB and c-Jun N-terminal kinase (JNK) activation diverge at IL-1 receptor-associated kinase (IRAK). Proc. Natl. Acad. Sci. U. S. A. 98, 4461-4465
22. Qian, Y., Commane, M., Ninomiya-Tsuji, J., Matsumoto, K., and Li, X. (2001) IRAK-mediated translocation of TRAF6 and TAB2 in the interleukin-1- induced activation of NF-κB. J. Biol. Chem. 276, 41661-41667
23. Takaesu, G., Ninomiya-Tsuji, J., Kishida, S., Li, X., Stark, G. R., and 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. 21, 2475-2484
24. Takaesu, G., Kishida, S., Hiyama, A., Yamaguchi, K., Shibuya, H., Irie, K., Ninomiya-Tsuji, J., and 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
25. Hoffmann, A., Natoli, G., and Ghosh, G. (2006) Transcriptional regulation via the NF-κB signaling module. Oncogene 25, 6706-6716
26. Natoli, G., Saccani, S., Bosisio, D., and Marazzi, I. (2005) Interactions of NF-κB with chromatin: the art of being at the right place at the right time. Nat. Immunol. 6, 439-445
27. Sanjabi, S., Williams, K. J., Saccani, S., Zhou, L., Hoffmann, A., Ghosh, G., Gerondakis, S., Natoli, G., and Smale, S. T. (2005) A c-Rel subdomain responsible for enhanced DNA-binding affinity and selective gene activation. Genes Dev. 19, 2138-2151
28. Chen, L. F., and Greene, W. C. (2004) Shaping the nuclear action of NF-κB. Nat. Rev. Mol. Cell. Biol. 5, 392-401
29. Quivy, V., and Van Lint, C. (2004) Regulation at multiple levels of NF-κB-mediated transactivation by protein acetylation. Biochem. Pharmacol. 68, 1221-1229
30. Vermeulen, L., De Wilde, G., Van Damme, P., Vanden Berghe, W., and Haegeman, G. (2003) Transcriptional activation of the NF-kappaB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J. 22, 1313-1324
31. Viatour, P., Bentires-Alj, M., Chariot, A., Deregowski, V., de Leval, L., Merville, M. P., and Bours, V. (2003) NF-κB2/p100 induces Bcl-2 expression. Leukemia 17, 1349-1356
32. Perkins, N. D. (2006) Post-translational modifications regulating the activity and function of the nuclear factor-κB pathway. Oncogene 25, 6717-6730
33. Bol, G., Kreuzer, O. J., and Brigelius-Flohe, R. (2000) Translocation of the interleukin-1 receptor-associated kinase-1 (IRAK-1) into the nucleus. FEBS Lett. 477, 73-78
34. Li, L., Cousart, S., Hu, J., and McCall, C. E. (2000) Characterization of interleukin-1 receptor-associated kinase in normal and endotoxin-tolerant cells. J. Biol. Chem. 275, 23340-23345
35. Su, J., Richter, K., Zhang, C., Gu, Q., and Li, L. (2007) Differential regulation of interleukin-1 receptor associated kinase 1 (IRAK1) splice variants. Mol. Immunol. 44, 900-905
36. Huang, Y., Li, T., Sane, D. C., and Li, L. (2004) IRAK1 serves as a novel regulator essential for lipopolysaccharide-induced interleukin-10 gene expression. J. Biol. Chem. 279, 51697-51703
37. Li, X., Commane, M., Burns, C., Vithalani, K., Cao, Z., and Stark, G. R. (1999) Mutant cells that do not respond to interleukin-1 (IL-1) reveal a novel role for IL-1 receptor-associated kinase. Mol. Cell. Biol. 19, 4643-4652
38. Knop, J., and Martin, M. U. (1999) Effects of IL-1 receptor-associated kinase (IRAK) expression on IL-1 signaling are independent of its kinase activity. FEBS Lett. 448, 81-85
39. Knop, J., Wesche, H., Lang, D., and Martin, M. U. (1998) Effects of overexpression of IL-1 receptor-associated kinase on NF-κB activation, IL-2 production and stress-activated protein kinases in the murine T cell line EL4. Eur. J. Immunol. 28, 3100-3109
40. Maschera, B., Ray, K., Burns, K., and Volpe, F. (1999) Overexpression of an enzymically inactive interleukin-1-receptor-associated kinase activates nuclear factor-κB. Biochem. J. 339, 227-231
41. Kollewe, C., Mackensen, A. C., Neumann, D., Knop, J., Cao, P., Li, S., Wesche, H., and Martin, M. U. (2004) Sequential autophosphorylation steps in the interleukin-1 receptor-associated kinase-1 regulate its availability as an adapter in interleukin-1 signaling. J. Biol. Chem. 279, 5227-5236
42. Yamin, T. T., and Miller, D. K. (1997) The interleukin-1 receptor-associated kinase is degraded by proteasomes following its phosphorylation. J. Biol. Chem. 272, 21540-21547
43. Dong, Z., and Bode, A. M. (2006) The role of histone H3 phosphorylation (Ser10 and Ser28) in cell growth and cell transformation. Mol Carcinog. 45, 416-421
44. Nowak, S. J., and Corces, V. G. (2004) Phosphorylation of histone H3: a balancing act between chromosome condensation and transcriptional activation. Trends Genet. 20, 214-220
45. Prigent, C., and Dimitrov, S. (2003) Phosphorylation of serine 10 in histone H3, what for? J. Cell Sci. 116, 3677-3685
46. Asehnoune, K., Strassheim, D., Mitra, S., Kim, J. Y., and Abraham, E. (2004) Involvement of reactive oxygen species in Toll-like receptor 4-dependent activation of NF-κB. J. Immunol. 172, 2522-2529
47. Jacinto, R., Hartung, T., McCall, C., and Li, L. (2002) Lipopolysaccharide-and lipoteichoic acid-induced tolerance and cross-tolerance: distinct alterations in IL-1 receptor-associated kinase. J. Immunol. 168, 6136-6141
48. 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., and 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
49. Swantek, J. L., Tsen, M. F., Cobb, M. H., and Thomas, J. A. (2000) IL-1 receptor-associated kinase modulates host responsiveness to endotoxin. J. Immunol. 164, 4301-4306
50. Thomas, J. A., Allen, J. L., Tsen, M., Dubnicoff, T., Danao, J., Liao, X. C., Cao, Z., and Wasserman, S. A. (1999) Impaired cytokine signaling in mice lacking the IL-1 receptor-associated kinase. J. Immunol. 163, 978-984
51. Arcaroli, J., Silva, E., Maloney, J. P., He, Q., Svetkauskaite, D., Murphy, J. R., and Abraham, E. (2006) Variant IRAK-1 haplotype is associated with increased nuclear factor-κB activation and worse outcomes in sepsis. Am. J. Respir. Crit. Care Med. 173, 1335-1341
52. Haglund, K., and Dikic, I. (2005) Ubiquitylation and cell signaling. EMBO J. 24, 3353-3359
53. Ordureau, A., Smith, H., Windheim, M., Peggie, M., Carrick, E., Morrice, N., and Cohen, P. (2008) The IRAK-catalysed activation of the E3 ligase function of Pellino isoforms induces the Lys63-linked polyubiquitination of IRAK1. Biochem. J. 409, 43-52
54. Geetha, T., Kenchappa, R. S., Wooten, M. W., and Carter, B. D. (2005) TRAF6-mediated ubiquitination regulates nuclear translocation of NRIF, the p75 receptor interactor. EMBO J. 24, 3859-3868
55. Emerson, B. M. (2002) Specificity of gene regulation. Cell 109, 267-270
56. Cheung, P., Allis, C. D., and Sassone-Corsi, P. (2000) Signaling to chromatin through histone modifications. Cell 103, 263-271
57. Kadam, S., and Emerson, B. M. (2002) Mechanisms of chromatin assembly and transcription. Curr. Opin. Cell Biol. 14, 262-268
58. Anest, V., Hanson, J. L., Cogswell, P. C., Steinbrecher, K. A., Strahl, B. D., and Baldwin, A. S. (2003) A nucleosomal function for IκB kinase-alpha in NF-κB-dependent gene expression. Nature 423, 659-663
59. Yamamoto, Y., Verma, U. N., Prajapati, S., Kwak, Y. T., and Gaynor, R. B. (2003) Histone H3 phosphorylation by IKK-alpha is critical for cytokine-induced gene expression. Nature 423, 655-659