71
Views
185
CrossRef citations to date
0
Altmetric
Article

Lys63-Linked Polyubiquitination of IRAK-1 Is Required for Interleukin-1 Receptor- and Toll-Like Receptor-Mediated NF-κB Activation

, , , &
Pages 3538-3547 | Received 23 Nov 2007, Accepted 10 Mar 2008, Published online: 27 Mar 2023

REFERENCES

  • Akira, S., and K. Takeda. 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4:499–511.
  • Burns, K., S. Janssens, B. Brissoni, N. Olivos, R. Beyaert, and J. Tschopp. 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.
  • Burns, K., F. Martinon, C. Esslinger, H. Pahl, P. Schneider, J. L. Bodmer, F. Di Marco, L. French, and J. Tschopp. 1998. MyD88, an adapter protein involved in interleukin-1 signaling. J. Biol. Chem. 273:12203–12209.
  • Cao, Z., W. J. Henzel, and X. Gao. 1996. IRAK: a kinase associated with the interleukin-1 receptor. Science 271:1128–1131.
  • Cao, Z., J. Xiong, M. Takeuchi, T. Kurama, and D. V. Goeddel. 1996. TRAF6 is a signal transducer for interleukin-1. Nature 383:443–446.
  • Deng, L., C. Wang, E. Spencer, L. Yang, A. Braun, J. You, C. Slaughter, C. Pickart, and Z. J. Chen. 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.
  • Dinarello, C. A. 1996. Biologic basis for interleukin-1 in disease. Blood 87:2095–2147.
  • Doffinger, R., A. Smahi, C. Bessia, F. Geissmann, J. Feinberg, A. Durandy, C. Bodemer, S. Kenwrick, S. Dupuis-Girod, S. Blanche, P. Wood, S. H. Rabia, D. J. Headon, P. A. Overbeek, F. Le Deist, S. M. Holland, K. Belani, D. S. Kumararatne, A. Fischer, R. Shapiro, M. E. Conley, E. Reimund, H. Kalhoff, M. Abinun, A. Munnich, A. Israel, G. Courtois, and J. L. Casanova. 2001. X-linked anhidrotic ectodermal dysplasia with immunodeficiency is caused by impaired NF-κB signaling. Nat. Genet. 27:277–285.
  • Ea, C. K., L. Deng, Z. P. Xia, G. Pineda, and Z. J. Chen. 2006. Activation of IKK by TNFα requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol. Cell 22:245–257.
  • Filipe-Santos, O., J. Bustamante, M. H. Haverkamp, E. Vinolo, C. L. Ku, A. Puel, D. M. Frucht, K. Christel, H. von Bernuth, E. Jouanguy, J. Feinberg, A. Durandy, B. Senechal, A. Chapgier, G. Vogt, L. de Beaucoudrey, C. Fieschi, C. Picard, M. Garfa, J. Chemli, M. Bejaoui, M. N. Tsolia, N. Kutukculer, A. Plebani, L. Notarangelo, C. Bodemer, F. Geissmann, A. Israel, M. Veron, M. Knackstedt, R. Barbouche, L. Abel, K. Magdorf, D. Gendrel, F. Agou, S. M. Holland, and J. L. Casanova. 2006. X-linked susceptibility to mycobacteria is caused by mutations in NEMO impairing CD40-dependent IL-12 production. J. Exp. Med. 203:1745–1759.
  • Janssens, S., and R. Beyaert. 2003. Functional diversity and regulation of different interleukin-1 receptor-associated kinase (IRAK) family members. Mol. Cell 11:293–302.
  • Jiang, Z., J. Ninomiya-Tsuji, Y. Qian, K. Matsumoto, and X. Li. 2002. Interleukin-1 (IL-1) receptor-associated kinase-dependent IL-1-induced signaling complexes phosphorylate TAK1 and TAB2 at the plasma membrane and activate TAK1 in the cytosol. Mol. Cell. Biol. 22:7158–7167.
  • Kanakaraj, P., P. H. Schafer, D. E. Cavender, Y. Wu, K. Ngo, P. F. Grealish, S. A. Wadsworth, P. A. Peterson, J. J. Siekierka, C. A. Harris, and W. P. Fung-Leung. 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.
  • Kanayama, A., R. B. Seth, L. Sun, C. K. Ea, M. Hong, A. Shaito, Y. H. Chiu, L. Deng, and Z. J. Chen. 2004. TAB2 and TAB3 activate the NF-κB pathway through binding to polyubiquitin chains. Mol. Cell 15:535–548.
  • Kawagoe, T., S. Sato, A. Jung, M. Yamamoto, K. Matsui, H. Kato, S. Uematsu, O. Takeuchi, and S. Akira. 2007. Essential role of IRAK-4 protein and its kinase activity in Toll-like receptor-mediated immune responses but not in TCR signaling. J. Exp. Med. 204:1013–1024.
  • Kim, T. W., K. Staschke, K. Bulek, J. Yao, K. Peters, K. H. Oh, Y. Vandenburg, H. Xiao, W. Qian, T. Hamilton, B. Min, G. Sen, R. Gilmour, and X. Li. 2007. A critical role for IRAK4 kinase activity in Toll-like receptor-mediated innate immunity. J. Exp. Med. 204:1025–1036.
  • Knop, J., and M. U. Martin. 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.
  • Koziczak-Holbro, M., C. Joyce, A. Gluck, B. Kinzel, M. Muller, C. Tschopp, J. C. Mathison, C. N. Davis, and H. Gram. 2007. IRAK-4 kinase activity is required for interleukin-1 (IL-1) receptor- and toll-like receptor 7-mediated signaling and gene expression. J. Biol. Chem. 282:13552–13560.
  • Lamothe, B., A. Besse, A. D. Campos, W. K. Webster, H. Wu, and B. G. Darnay. 2007. Site-specific Lys-63-linked tumor necrosis factor receptor-associated factor 6 auto-ubiquitination is a critical determinant of I kappa B kinase activation. J. Biol. Chem. 282:4102–4112.
  • Li, H., M. Kobayashi, M. Blonska, Y. You, and X. Lin. 2006. Ubiquitination of RIP is required for tumor necrosis factor alpha-induced NF-κB activation. J. Biol. Chem. 281:13636–13643.
  • Li, S., A. Strelow, E. J. Fontana, and H. Wesche. 2002. IRAK-4: a novel member of the IRAK family with the properties of an IRAK-kinase. Proc. Natl. Acad. Sci. USA 99:5567–5572.
  • Li, X., M. Commane, C. Burns, K. Vithalani, Z. Cao, and G. R. Stark. 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.
  • Li, X., M. Commane, Z. Jiang, and G. R. Stark. 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. USA 98:4461–4465.
  • Lomaga, M. A., W. C. Yeh, I. Sarosi, G. S. Duncan, C. Furlonger, A. Ho, S. Morony, C. Capparelli, G. Van, S. Kaufman, A. van der Heiden, A. Itie, A. Wakeham, W. Khoo, T. Sasaki, Z. Cao, J. M. Penninger, C. J. Paige, D. L. Lacey, C. R. Dunstan, W. J. Boyle, D. V. Goeddel, and T. W. Mak. 1999. TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev. 13:1015–1024.
  • Maschera, B., K. Ray, K. Burns, and F. Volpe. 1999. Overexpression of an enzymically inactive interleukin-1-receptor-associated kinase activates nuclear factor-κB. Biochem. J. 339:227–231.
  • Medzhitov, R., P. Preston-Hurlburt, E. Kopp, A. Stadlen, C. Chen, S. Ghosh, and C. A. J. Janeway. 1998. MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol. Cell 2:253–258.
  • Naito, A., S. Azuma, S. Tanaka, T. Miyazaki, S. Takaki, K. Takatsu, K. Nakao, K. Nakamura, M. Katsuki, T. Yamamoto, and J. Inoue. 1999. Severe osteopetrosis, defective interleukin-1 signalling and lymph node organogenesis in TRAF6-deficient mice. Genes Cells 4:353–362.
  • Oeckinghaus, A., E. Wegener, V. Welteke, U. Ferch, S. C. Arslan, J. Ruland, C. Scheidereit, and D. Krappmann. 2007. Malt1 ubiquitination triggers NF-κB signaling upon T-cell activation. EMBO J. 26:4634–4645.
  • O'Neill, L. A. 8 August 2000, posting date. The interleukin-1 receptor/Toll-like receptor superfamily: signal transduction during inflammation and host defense. Sci. STKE. doi:10.1126/stke.2999.44.re1.
  • Ordureau, A., H. Smith, M. Windheim, M. Peggie, E. Carrick, N. Morrice, and P. Cohen. 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.
  • Pandey, S., and D. K. Agrawal. 2006. Immunobiology of Toll-like receptors: emerging trends. Immunol. Cell Biol. 84:333–341.
  • Petrak, D., S. A. Memon, M. J. Birrer, J. D. Ashwell, and C. M. Zacharchuk. 1994. Dominant negative mutant of c-Jun inhibits NF-AT transcriptional activity and prevents IL-2 gene transcription. J. Immunol. 153:2046–2051.
  • Picard, C., A. Puel, M. Bonnet, C. L. Ku, J. Bustamante, K. Yang, C. Soudais, S. Dupuis, J. Feinberg, C. Fieschi, C. Elbim, R. Hitchcock, D. Lammas, G. Davies, A. Al-Ghonaium, H. Al-Rayes, S. Al-Jumaah, S. Al-Hajjar, I. Z. Al-Mohsen, H. H. Frayha, R. Rucker, T. R. Hawn, A. Aderem, H. Tufenkeji, S. Haraguchi, N. K. Day, R. A. Good, M. A. Gougerot-Pocidalo, A. Ozinsky, and J. L. Casanova. 2003. Pyogenic bacterial infections in humans with IRAK-4 deficiency. Science 299:2076–2079.
  • Qin, J., Z. Jiang, Y. Qian, J. L. Casanova, and X. Li. 2004. IRAK4 kinase activity is redundant for interleukin-1 (IL-1) receptor-associated kinase phosphorylation and IL-1 responsiveness. J. Biol. Chem. 279:26748–26753.
  • Rincon, M., B. Derijard, C. W. Chow, R. J. Davis, and R. A. Flavell. 1997. Reprogramming the signalling requirement for AP-1 (activator protein-1) activation during differentiation of precursor CD4+ T-cells into effector Th1 and Th2 cells. Genes Funct. 1:51–68.
  • Rothwarf, D. M., and M. Karin. 1999. The NF-kappa B activation pathway: a paradigm in information transfer from membrane to nucleus. Sci. STKE. doi:10.1126/stke.1999.5.re1.
  • Rudolph, D., W. C. Yeh, A. Wakeham, B. Rudolph, D. Nallainathan, J. Potter, A. J. Elia, and T. W. Mak. 2000. Severe liver degeneration and lack of NF-κB activation in NEMO/IKKγ-deficient mice. Genes Dev. 14:854–862.
  • Sato, S., H. Sanjo, K. Takeda, J. Ninomiya-Tsuji, M. Yamamoto, T. Kawai, K. Matsumoto, O. Takeuchi, and S. Akira. 2005. Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat. Immunol. 6:1087–1095.
  • Schauvliege, R., S. Janssens, and R. Beyaert. 2006. Pellino proteins are more than scaffold proteins in TLR/IL-1R signalling: a role as novel RING E3-ubiquitin-ligases. FEBS Lett. 580:4697–4702.
  • Schmidt-Supprian, M., W. Bloch, G. Courtois, K. Addicks, A. Israel, K. Rajewsky, and M. Pasparakis. 2000. NEMO/IKK gamma-deficient mice model incontinentia pigmenti. Mol. Cell 5:981–992.
  • Schnare, M., G. M. Barton, A. C. Holt, K. Takeda, S. Akira, and R. Medzhitov. 2001. Toll-like receptors control activation of adaptive immune responses. Nat. Immunol. 2:947–950.
  • Schreiber, E., P. Matthias, M. M. Muller, and W. Schaffner. 1989. Rapid detection of octamer binding proteins with ‘mini-extracts’, prepared from a small number of cells. Nucleic Acids Res. 17:6419.
  • Suzuki, N., S. Suzuki, G. S. Duncan, D. G. Millar, T. Wada, C. Mirtsos, H. Takada, A. Wakeham, A. Itie, S. Li, J. M. Penninger, H. Wesche, P. S. Ohashi, T. W. Mak, and W. C. Yeh. 2002. Severe impairment of interleukin-1 and Toll-like receptor signalling in mice lacking IRAK-4. Nature 416:750–756.
  • Swantek, J. L., M. F. Tsen, M. H. Cobb, and J. A. Thomas. 2000. IL-1 receptor-associated kinase modulates host responsiveness to endotoxin. J. Immunol. 164:4301–4306.
  • Takaesu, G., S. Kishida, A. Hiyama, K. Yamaguchi, H. Shibuya, K. Irie, J. Ninomiya-Tsuji, and K. Matsumoto. 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.
  • Thomas, J. A., J. L. Allen, M. Tsen, T. Dubnicoff, J. Danao, X. C. Liao, Z. Cao, and S. A. Wasserman. 1999. Impaired cytokine signaling in mice lacking the IL-1 receptor-associated kinase. J. Immunol. 163:978–984.
  • Tugores, A., M. A. Alonso, F. Sanchez-Madrid, and M. O. de Landazuri. 1992. Human T cell activation through the activation-inducer molecule/CD69 enhances the activity of transcription factor AP-1. J. Immunol. 148:2300–2306.
  • Wang, C., L. Deng, M. Hong, G. R. Akkaraju, J. Inoue, and Z. J. Chen. 2001. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412:346–351.
  • Wesche, H., W. J. Henzel, W. Shillinglaw, S. Li, and Z. Cao. 1997. MyD88: an adapter that recruits IRAK to the IL-1 receptor complex. Immunity 7:837–847.
  • West, A. P., A. A. Koblansky, and S. Ghosh. 2006. Recognition and signaling by Toll-like receptors. Annu. Rev. Cell Dev. Biol. 22:409–437.
  • Wu, C. J., and J. D. Ashwell. 2008. NEMO recognition of polyubiquitinated Bcl10 is required for T cell receptor-mediated NF- 239 B activation. Proc. Natl. Acad. Sci. USA 105:3023–3028.
  • Wu, C. J., D. B. Conze, T. Li, S. M. Srinivasula, and J. D. Ashwell. 2006. NEMO is a sensor of Lys 63-linked polyubiquitination and functions in NF-κB activation. Nat. Cell Biol. 8:398–406.
  • Yamin, T. T., and D. K. Miller. 1997. The interleukin-1 receptor-associated kinase is degraded by proteasomes following its phosphorylation. J. Biol. Chem. 272:21540–21547.
  • Yao, J., T. W. Kim, J. Qin, Z. Jiang, Y. Qian, H. Xiao, Y. Lu, W. Qian, M. F. Gulen, N. Sizemore, J. DiDonato, S. Sato, S. Akira, B. Su, and X. Li. 2007. Interleukin-1 (IL-1)-induced TAK1-dependent versus MEKK3-dependent NF-κB activation pathways bifurcate at IL-1 receptor-associated kinase modification. J. Biol. Chem. 282:6075–6089.
  • Ye, H., J. R. Arron, B. Lamothe, M. Cirilli, T. Kobayashi, N. K. Shevde, D. Segal, O. K. Dzivenu, M. Vologodskaia, M. Yim, K. Du, S. Singh, J. W. Pike, B. G. Darnay, Y. Choi, and H. Wu. 2002. Distinct molecular mechanism for initiating TRAF6 signalling. Nature 418:443–447.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.