Interleukin-1 (IL-1) Induces the Lys63-Linked Polyubiquitination of IL-1 Receptor-Associated Kinase 1 To Facilitate NEMO Binding and the Activation of IκBα Kinase

REFERENCES

• Alessi, D. R., P. Cohen, A. Ashworth, S. Cowley, S. J. Leevers, and C. J. Marshall. 1995. Assay and expression of mitogen-activated protein kinase, MAP kinase kinase, and Raf. Methods Enzymol. 255:279–290.
   PubMed Web of Science ®Google Scholar
• Beinke, S., M. J. Robinson, M. Hugunin, and S. C. Ley. 2004. Lipopolysaccharide activation of the TPL-2/MEK/extracellular signal-regulated kinase mitogen-activated protein kinase cascade is regulated by IκB kinase-induced proteolysis of NF-κB1 p105. Mol. Cell. Biol. 24:9658–9667.
   PubMedGoogle Scholar
• Butler, M. P., J. A. Hanly, and P. N. Moynagh. 2007. Kinase-active interleukin-1 receptor-associated kinases promote polyubiquitination and degradation of the Pellino family: direct evidence for PELLINO proteins being ubiquitin-protein isopeptide ligases. J. Biol. Chem. 282:29729–29737.
   PubMedGoogle Scholar
• Chen, Z. J. 2005. Ubiquitin signalling in the NF-κB pathway. Nat. Cell Biol. 7:758–765.
   PubMed Web of Science ®Google Scholar
• Cheung, P. C., D. G. Campbell, A. R. Nebreda, and P. Cohen. 2003. Feedback control of the protein kinase TAK1 by SAPK2a/p38α. EMBO J. 22:5793–5805.
   PubMed Web of Science ®Google Scholar
• Cooke, E. L., I. J. Uings, C. L. Xia, P. Woo, and K. P. Ray. 2001. Functional analysis of the interleukin-1-receptor-associated kinase (IRAK-1) in interleukin-1β-stimulated nuclear factor κB (NF-κB) pathway activation: IRAK-1 associates with the NF-κB essential modulator (NEMO) upon receptor stimulation. Biochem. J. 359:403–410.
   PubMedGoogle Scholar
• Das, S., J. Cho, I. Lambertz, M. A. Kelliher, A. G. Eliopoulos, K. Du, and P. N. Tsichlis. 2005. Tpl2/Cot signals activate ERK, JNK, and NF-κB in a cell-type and stimulus-specific manner. J. Biol. Chem. 280:23748–23757.
   PubMedGoogle Scholar
• Döffinger, 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.
   PubMed Web of Science ®Google Scholar
• Dumitru, C. D., J. D. Ceci, C. Tsatsanis, D. Kontoyiannis, K. Stamatakis, J. H. Lin, C. Patriotis, N. A. Jenkins, N. G. Copeland, G. Kollias, and P. N. Tsichlis. 2000. TNF-α induction by LPS is regulated posttranscriptionally via a Tpl2/ERK-dependent pathway. Cell 103:1071–1083.
   PubMed Web of Science ®Google Scholar
• Durocher, Y., S. Perret, and A. Kamen. 2002. High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucleic Acids Res. 30:E9.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Hu, J., R. Jacinto, C. McCall, and L. Li. 2002. Regulation of IL-1 receptor-associated kinases by lipopolysaccharide. J. Immunol. 168:3910–3914.
   PubMedGoogle Scholar
• Jiang, Z., H. J. Johnson, H. Nie, J. Qin, T. A. Bird, and X. Li. 2003. Pellino 1 is required for interleukin-1 (IL-1)-mediated signaling through its interaction with the IL-1 receptor-associated kinase 4 (IRAK4)-IRAK-tumor necrosis factor receptor-associated factor 6 (TRAF6) complex. J. Biol. Chem. 278:10952–10956.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Kobayashi, N., Y. Kadono, A. Naito, K. Matsumoto, T. Yamamoto, S. Tanaka, and J. Inoue. 2001. Segregation of TRAF6-mediated signaling pathways clarifies its role in osteoclastogenesis. EMBO J. 20:1271–1280.
   PubMed Web of Science ®Google Scholar
• Lang, V., A. Symons, S. J. Watton, J. Janzen, Y. Soneji, S. Beinke, S. Howell, and S. C. Ley. 2004. ABIN-2 forms a ternary complex with TPL-2 and NF-κ B1 p105 and is essential for TPL-2 protein stability. Mol. Cell. Biol. 24:5235–5248.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• Li, X., M. Commane, Z. Jiang, and G. R. Stark. 2001. IL-1-induced NFκB and c-Jun N-terminal kinase (JNK) activation diverge at IL-1 receptor-associated kinase (IRAK). Proc. Natl. Acad. Sci. USA 98:4461–4465.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Mendoza, H., D. G. Campbell, K. Burness, J. Hastie, N. Ronkina, J. H. Shim, J. S. Arthur, R. J. Davis, M. Gaestel, G. L. Johnson, S. Ghosh, and P. Cohen. 2008. Roles for TAB1 in regulating the IL-1-dependent phosphorylation of the TAB3 regulatory subunit and activity of the TAK1 complex. Biochem. J. 409:711–722.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Rodríguez, C., M. Pozo, E. Nieto, M. Fernandez, and S. Alemany. 2006. TRAF6 and Src kinase activity regulates Cot activation by IL-1. Cell. Signal. 18:1376–1385.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Schauvliege, R., S. Janssens, and R. Beyaert. 2007. Pellino proteins: novel players in TLR and IL-1R signalling. J. Cell. Mol. Med. 11:453–461.
   PubMed Web of Science ®Google Scholar
• Shim, J. H., C. Xiao, A. E. Paschal, S. T. Bailey, P. Rao, M. S. Hayden, K. Y. Lee, C. Bussey, M. Steckel, N. Tanaka, G. Yamada, S. Akira, K. Matsumoto, and S. Ghosh. 2005. TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev. 19:2668–2681.
   PubMed Web of Science ®Google Scholar
• Strelow, A., C. Kollewe, and H. Wesche. 2003. Characterization of Pellino2, a substrate of IRAK1 and IRAK4. FEBS Lett. 547:157–161.
   PubMedGoogle Scholar
• Takaesu, G., J. Ninomiya-Tsuji, S. Kishida, X. Li, G. R. Stark, and K. Matsumoto. 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Waterfield, M., W. Jin, W. Reiley, M. Zhang, and S. C. Sun. 2004. IκB kinase is an essential component of the Tpl2 signaling pathway. Mol. Cell. Biol. 24:6040–6048.
   PubMedGoogle Scholar
• Waterfield, M. R., M. Zhang, L. P. Norman, and S. C. Sun. 2003. NF-κB1/p105 regulates lipopolysaccharide-stimulated MAP kinase signaling by governing the stability and function of the Tpl2 kinase. Mol. Cell 11:685–694.
   PubMed Web of Science ®Google Scholar
• Wu, C. J., D. B. Conze, T. Li, S. M. Srinivasula, and J. D. Ashwell. 2006. Sensing of Lys 63-linked polyubiquitination by NEMO is a key event in NF-κB activation. Nat. Cell Biol. 8:398–406.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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 NFκB activation pathways bifurcate at IL-1 receptor-associated kinase modification. J. Biol. Chem. 282:6075–6089.
   PubMed Web of Science ®Google Scholar