TNFα- and IKKβ-mediated TANK/I-TRAF phosphorylation: Implications for interaction with NEMO/IKKγ and NF-κB activation

Biochemical Journal

Volumn 394, Issue 3, 2006, Pages 593-603

  Bonif, Marianne ^a   Meuwis, Marie Alice ^a   Close, Pierre ^a   Benoit, Valérie ^a   Heyninck, Karen ^b   Chapelle, Jean Paul ^a   Bours, Vincent ^a   Merville, Marie Paule ^a   Piette, Jacques ^a   Beyaert, Rudi ^b   Chariot, Alain ^a,c  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Nuclear factor B (NF B); p65; RNA interference; TNF receptor associated factor (TRAF); TRAF family member associated NF B activator (TANK); Tumour necrosis factor (TNF)

Indexed keywords

DEGRADATION; GENES; PHOSPHORUS COMPOUNDS; PROTEINS; RNA;

NUCLEAR FACTOR ΚB (NF-ΚB); RNA INTERFERENCE; TNF RECEPTOR-ASSOCIATED FACTOR (TRAF); TUMOUR NECROSIS FACTOR (TNF);

TUMORS;

I KAPPA B KINASE BETA; I KAPPA B KINASE GAMMA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MEMBRANE PROTEIN; PROTEIN TANK; SYNAPTOTAGMIN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; I KAPPA B KINASE; MULTIPROTEIN COMPLEX; RNA BINDING PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TANK PROTEIN, HUMAN; TUMOR NECROSIS FACTOR RECEPTOR 1;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; RNA INTERFERENCE; TRANSACTIVATION; ANIMAL; CELL LINE; CHEMISTRY; DRUG EFFECT; ENZYME SPECIFICITY; GENE EXPRESSION REGULATION; METABOLISM; MOUSE; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL LINE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; I-KAPPA B KINASE; MICE; MULTIPROTEIN COMPLEXES; NF-KAPPA B; PHOSPHORYLATION; PROTEIN BINDING; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; TUMOR NECROSIS FACTOR-ALPHA; ZINC FINGERS;

EID: 33644956702     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20051659     Document Type: Article

References (57)

1. Tracey, K. J. and Cerami, A. (1993) Tumor necrosis factor, other cytokines and disease. Annu. Rev. Cell Biol. 9, 317-343
2. Karin, M. and Ben-Neriah, Y. (2000) Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu. Rev. Immunol. 18, 621-663
3. Hayden, M. S. and Ghosh, S. (2004) Signaling to NF-kappaB. Genes Dev. 18, 2195-2224
4. Hsu, H., Xiong, J. and Goeddel, D. V. (1995) The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell (Cambridge, Mass.) 81, 495-504
5. Devin, A., Cook, A., Lin, Y., Rodriguez, Y., Kelliher, M. and Liu, Z. (2000) The distinct roles of TRAF2 and RIP in IKK activation by TNF-R1: TRAF2 recruits IKK to TNF-R1 while RIP mediates IKK activation. Immunity 12, 419-429
6. Rothwarf, D. M., Zandi, E., Natoli, G. and Karin, M. (1998) IKK-gamma is an essential regulatory subunit of the IkappaB kinase complex. Nature (London) 395, 297-300
7. Yamaoka, S., Courtois, G., Bessia, C., Whiteside, S. T., Weil, R., Agou, F., Kirk, H. E., Kay, R. J. and Israel, A. (1998) Complementation cloning of NEMO, a component of the IkappaB kinase complex essential for NF-kappaB activation. Cell (Cambridge, Mass.) 93, 1231-1240
8. Takaesu, G., Surabhi, R. M., Park, K. J., Ninomiya-Tsuji, J., Matsumoto, K. and Gaynor, R. B. (2003) TAK1 is critical for IkappaB kinase-mediated activation of the NF-kappaB pathway. J. Mol. Biol. 326, 105-115
9. Sato, S., Sanjo, H., Takeda, K., Ninomiya-Tsuji, J., Yamamoto, M., Kawai, T., Matsumoto, K., Takeuchi, O. and Akira, S. (2005) Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat. Immunol. 6, 1087-1095
10. Shim, J. H., Xiao, C., Paschal, A. E., Bailey, S. T., Rao, P., Hayden, M. S., Lee, K. Y., Bussey, C., Steckel, M., Tanaka, N. et al. (2005) TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev. 19, 2668-2681
11. Yang, J., Lin, Y., Guo, Z., Cheng, J., Huang, J., Deng, L., Liao, W., Chen, Z., Liu, Z. and Su, B. (2001) The essential role of MEKK3 in TNF-induced NF-kappaB activation. Nat. Immunol. 2, 620-624
12. Prajapati, S. and Gaynor, R. B. (2002) Regulation of Ikappa B kinase (IKK)gamma/NEMO function by IKKbeta -mediated phosphorylation. J. Biol. Chem. 277, 24331-24339
13. Tarassishin, L. and Horwitz, M. S. (2001) Sites on FIP-3 (NEMO/IKKgamma) essential for its phosphorylation and NF-kappaB modulating activity. Biochem. Biophys. Res. Commun. 285, 555-560
14. Chariot, A., Meuwis, M. A., Bonif, M., Leonardi, A., Merville, M. P., Gielen, J., Piette, J., Siebenlist, U. and Bours, V. (2003) NF-kappaB activating scaffold proteins as signaling molecules and putative therapeutic targets. Curr. Med. Chem. 10, 593-602
15. Vermeulen, L., De Wilde, G., Notebaert, S., Vanden Berghe, W. and Haegeman, G. (2002) Regulation of the transcriptional activity of the nuclear factor-kappaB p65 subunit. Biochem. Pharmacol. 64, 963-970
16. Anest, V., Hanson, J. L., Cogswell, P. C., Steinbrecher, K. A., Strahl, B. D. and Baldwin, A. S. (2003) A nucleosomal function for IkappaB kinase-alpha in NF-kappaB-dependent gene expression. Nature (London) 423, 659-663
17. 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 (London) 423, 655-659
18. Sakurai, H., Chiba, H., Miyoshi, H., Sugita, T. and Toriumi, W. (1999) IkappaB kinases phosphorylate NF-kappaB p65 subunit on serine 536 in the transactivation domain. J. Biol. Chem. 274, 30353-30356
19. Cheng, G. and Baltimore, D. (1996) TANK, a co-inducer with TRAF2 of TNF- and CD 40L-mediated NF-kappaB activation. Genes Dev. 10, 963-973
20. Nomura, F., Kawai, T., Nakanishi, K. and Akira, S. (2000) NF-kappaB activation through IKK-i-dependent I-TRAF/TANK phosphorylation. Genes Cells 5, 191-202
21. Pomerantz, J. L. and Baltimore, D. (1999) NF-kappaB activation by a signaling complex containing TRAF2, TANK and TBK1, a novel IKK-related kinase. EMBO J. 18, 6694-6704
22. Kaye, K. M., Devergne, O., Harada, J. N., Izumi, K. M., Yalamanchili, R., Kieff, E. and Mosialos, G. (1996) Tumor necrosis factor receptor associated factor 2 is a mediator of NF-kappa B activation by latent infection membrane protein 1, the Epstein-Barr virus transforming protein. Proc. Natl. Acad. Sci. U.S.A. 93, 11085-11090
23. Rothe, M., Xiong, J., Shu, H. B., Williamson, K., Goddard, A. and Goeddel, D. V. (1996) I-TRAF is a novel TRAF-interacting protein that regulates TRAF-mediated signal transduction. Proc. Natl. Acad. Sci. U.S.A. 93, 8241-8246
24. Chariot, A., Leonardi, A., Muller, J., Bonif, M., Brown, K. and Siebenlist, U. (2002) Association of the adaptor TANK with the I kappa B kinase (IKK) regulator NEMO connects IKK complexes with IKK epsilon and TBK1 kinases. J. Biol. Chem. 277, 37029-37036
25. Leonardi, A., Chariot, A., Claudio, E., Cunningham, K. and Siebenlist, U. (2000) CIKS, a connection to Ikappa B kinase and stress-activated protein kinase. Proc. Natl. Acad. Sci. U.S.A. 97, 10494-10499
26. Leonardi, A., Ellinger-Ziegelbauer, H., Franzoso, G., Brown, K. and Siebenlist, U. (2000) Physical and functional interaction of filamin (actin-binding protein-280) and tumor necrosis factor receptor-associated factor 2. J. Biol. Chem. 275, 271-278
27. Ting, A. T., Pimentel-Muinos, F. X. and Seed, B. (1996) RIP mediates tumor necrosis factor receptor 1 activation of NF-kappaB but not Fas/APO-1-initiated apoptosis. EMBO J. 15, 6189-6196
28. Viatour, P., Dejardin, E., Warnier, M., Lair, F., Claudio, E., Bureau, F., Marine, J. C., Merville, M. P., Maurer, U., Green, D. et al. (2004) GSK3-mediated BCL-3 phosphorylation modulates its degradation and its oncogenicity. Mol. Cell 16, 35-45
29. Chin, A. I., Shu, J., Shan Shi, C., Yao, Z., Kehrl, J. H. and Cheng, G. (1999) TANK potentiates tumor necrosis factor receptor-associated factor-mediated c-Jun N-terminal kinase/stress-activated protein kinase activation through the germinal center kinase pathway. Mol. Cell. Biol. 19, 6665-6672
30. Pierce, J. W., Schoenleber, R., Jesmok, G., Best, J., Moore, S. A., Collins, T. and Gerritsen, M. E. (1997) Novel inhibitors of cytokine-induced IkappaBalpha phosphorylation and endothelial cell adhesion molecule expression show anti-inflammatory effects in vivo. J. Biol. Chem. 272, 21096-21103
31. Tada, K., Okazaki, T., Sakon, S., Kobarai, T., Kurosawa, K., Yamaoka, S., Hashimoto, H., Mak, T. W., Yagita, H., Okumura, K. et al. (2001) Critical roles of TRAF2 and TRAF5 in tumor necrosis factor-induced NF-kappa B activation and protection from cell death. J. Biol. Chem. 276, 36530-36534
32. Hsu, H., Huang, J., Shu, H. B., Baichwal, V. and Goeddel, D. V. (1996) TNF-dependent recruitment of the protein kinase RIP to the TNF receptor-1 signaling complex. Immunity 4, 387-396
33. Brown, K., Gerstberger, S., Carlson, L., Franzoso, G. and Siebenlist, U. (1995) Control of I kappa B-alpha proteolysis by site-specific, signal-induced phosphorylation. Science 267, 1485-1488
34. Gao, Z., Hwang, D., Bataille, F., Lefevre, M., York, D., Quon, M. J. and Ye, J. (2002) Serine phosphorylation of insulin receptor substrate 1 by inhibitor kappa B kinase complex. J. Biol. Chem. 277, 48115-48121
35. Bonnard, M., Mirtsos, C., Suzuki, S., Graham, K., Huang, J., Ng, M., Itie, A., Wakeham, A., Shahinian, A., Henzel, W. J. et al. (2000) Deficiency of T2K leads to apoptotic liver degeneration and impaired NF-kappaB-dependent gene transcription. EMBO J. 19, 4976-4985
36. Das, S., Cho, J., Lambertz, I., Kelliher, M. A., Eliopoulos, A. G., Du, K. and Tsichlis, P. N. (2005) Tpl2/cot signals activate ERK, JNK, and NF-kappaB in a cell-type and stimulus-specific manner. J. Biol. Chem. 280, 23748-23757
37. Wang, D., Westerheide, S. D., Hanson, J. L. and Baldwin, Jr, A. S. (2000) Tumor necrosis factor alpha-induced phosphorylation of RelA/p65 on Ser529 is controlled by casein kinase II. J. Biol. Chem. 275, 32592-32597
38. Kuai, J., Wooters, J., Hall, J. P., Rao, V. R., Nickbarg, E., Li, B., Chatterjee-Kishore, M., Qiu, Y. and Lin, L. L. (2004) NAK is recruited to the TNFR1 complex in a TNFalpha-dependent manner and mediates the production of RANTES: identification of endogenous TNFR-interacting proteins by a proteomic approach. J. Biol. Chem. 279, 53266-53271
39. Beg, A. A., Sha, W. C., Bronson, R. T., Ghosh, S. and Baltimore, D. (1995) Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappa B. Nature (London) 376, 167-170
40. Li, Q., Van Antwerp, D., Mercurio, F., Lee, K. F. and Verma, I. M. (1999) Severe liver degeneration in mice lacking the IkappaB kinase 2 gene. Science 284, 321-325
41. Li, Z. W., Chu, W., Hu, Y., Delhase, M., Deerinck, T., Ellisman, M., Johnson, R. and Karin, M. (1999) The IKKbeta subunit of IkappaB kinase (IKK) is essential for nuclear factor kappaB activation and prevention of apoptosis. J. Exp. Med. 189, 1839-1845
42. Tanaka, M., Fuentes, M. E., Yamaguchi, K., Durnin, M. H., Dalrymple, S. A., Hardy, K. L. and Goeddel, D. V. (1999) Embryonic lethality, liver degeneration, and impaired NF-kappa B activation in IKK-beta-deficient mice. Immunity 10, 421-429
43. Rudolph, D., Yen, W. C., Wakeham, A., Rudolph, B., Nallainathan, D., Potter, J., Elia, A. J. and Mak, T. W. (2000) Severe liver degeneration and lack of NF-kappaB activation in NEMO/IKKgamma-deficient mice. Genes Dev. 14, 854-862
44. Hemmi, H., Takeuchi, O., Sato, S., Yamamoto, M., Kaisho, T., Sanjo, H., Kawai, T., Hoshino, K., Takeda, K. and Akira, S. (2004) The roles of two IkappaB kinase-related kinases in lipopolysaccharide and double stranded RNA signaling and viral infection. J. Exp. Med. 199, 1641-1650
45. Fujita, F., Taniguchi, Y., Kato, T., Narita, Y., Furuya, A., Ogawa, T., Sakurai, H., Joh, T., Itoh, M., Delhase, M. et al. (2003) Identification of NAP1, a regulatory subunit of IkappaB kinase-related kinases that potentiates NF-kappaB signaling. Mol. Cell. Biol. 23, 7780-7793
46. Buss, H., Dorrie, A., Schmitz, M. L., Hoffmann, E., Resch, K. and Kracht, M. (2004) Constitutive and interleukin-1-inducible phosphorylation of p65 NF-{kappa}B at serine 536 is mediated by multiple protein kinases including I{kappa}B kinase (IKK)-{alpha}, IKK{beta}, IKK{epsilon}, TRAF family member-associated (TANK)-binding kinase 1 (TBK1), and an unknown kinase and couples p65 to TATA-binding protein-associated factor II31-mediated interleukin-8 transcription. J. Biol. Chem. 279, 55633-55643
47. McWhirter, S. M., Fitzgerald, K. A., Rosains, J., Rowe, D. C., Golenbock, D. T. and Maniatis, T. (2004) IFN-regulatory factor 3-dependent gene expression is defective in Tbk1-deficient mouse embryonic fibroblasts. Proc. Natl. Acad. Sci. U.S.A. 101, 233-238
48. Leitges, M., Sanz, L., Martin, P., Duran, A., Braun, U., Garcia, J. F., Camacho, F., Diaz-Meco, M. T., Rennert, P. D. and Moscat, J. (2001) Targeted disruption of the zetaPKC gene results in the impairment of the NF-kappaB pathway. Mol. Cell 8, 771-780
49. Shimada, T., Kawai, T., Takeda, K., Matsumoto, M., Inoue, J., Tatsumi, Y., Kanamaru, A. and Akira, S. (1999) IKK-i, a novel lipopolysacoharide- inducible kinase that is related to IkappaB kinases. Int. Immunol. 11, 1357-1362
50. Weiss, T., Grell, M., Hessabi, B., Bourteele, S., Muller, G., Scheurich, P. and Wajant, H. (1997) Enhancement of TNF receptor p60-mediated cytotoxicity by TNF receptor p80: requirement of the TNF receptor-associated factor-2 binding site. J. Immunol. 158, 2398-2404
51. Chan, F. K. and Lenardo, M. J. (2000) A crucial role for p80 TNF-R2 in amplifying p60 TNF-R1 apoptosis signals in T lymphocytes. Eur. J. Immunol. 30, 652-660
52. Fotin-Mleczek, M., Henkier, F., Samel, D., Reichwein, M., Hausser, A., Parmryd, I., Scheurich, P., Schmid, J. A. and Wajant, H. (2002) Apoptotic crosstalk of TNF receptors: TNF-R2-induces depletion of TRAF2 and IAP proteins and accelerates TNF-R1-dependent activation of caspase-8. J. Cell Sci. 115, 2757-2770
53. 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). EMBOJ. 22, 1313-1324
54. Beyaert, R., Cuenda, A., Vanden Berghe, W., Plaisance, S., Lee, J. C., Haegeman, G., Cohen, P. and Fiers, W. (1996) The p38/RK mitogen-activated protein kinase pathway regulates interleukin-6 synthesis response to tumor necrosis factor. EMBO J. 15, 1914-1923
55. Banno, T., Gazel, A. and Blumenberg, M. (2005) Pathway-specific profiling identifies the NF-kappa B-dependent tumor necrosis factor alpha-regulated genes in epidermal keratinocytes. J. Biol. Chem. 280, 18973-18980
56. Fitzgerald, K. A., McWhirter, S. M., Faia, K. L., Rowe, D. C., Latz, E., Golenbock, D. T., Coyle, A. J., Liao, S. M. and Maniatis, T. (2003) IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4, 491-496
57. Sharma, S., tenOever, B. R., Grandvaux, N., Zhou, G. P., Lin, R. and Hiscott, J. (2003) Triggering the interferon antiviral response through an IKK-related pathway. Science 300, 1148-1151