[en] Type I interferon gene induction relies on IKK-related kinase TBK1 and IKK epsilon-mediated phosphorylations of IRF3/7 through the Toll-like receptor-dependent signaling pathways. The scaffold proteins that assemble these kinase complexes are poorly characterized. We show here that TANK/ITRAF is required for the TBK1- and IKK epsilon-mediated IRF3/7 phosphorylations through some Toll-like receptor-dependent pathways and is part of a TRAF3-containing complex. Moreover, TANK is dispensable for the early phase of double-stranded RNA-mediated IRF3 phosphorylation. Interestingly, TANK is heavily phosphorylated by TBK1-IKK epsilon upon lipopolysaccharide stimulation and is also subject to lipopolysaccharide- and TBK1-IKK epsilon-mediated Lys(63)-linked polyubiquitination, a mechanism that does not require TBK1-IKK epsilon kinase activity. Thus, we have identified TANK as a scaffold protein that assembles some but not all IRF3/7-phosphorylating TBK1-IKK epsilon complexes and demonstrated that these kinases possess two functions, namely the phosphorylation of both IRF3/7 and TANK as well as the recruitment of an E3 ligase for Lys63-linked polyubiquitination of their scaffold protein, TANK.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
GATOT, Jean-Stéphane ; Free University of Brussels > Institute of Molecular Biology and Medicine > Dept. of Applied Genetics
Kato, H., Sato, S., Yoneyama, M., Yamamoto, M., Uematsu, S., Matsui, K., Tsujimura, T., Takeda, K., Fujita, T., Takeuchi, O., and Akira, S. (2005) Immunity 23, 19-28
Honda, K., and Taniguchi, T. (2006) Nat. Rev. Immunol. 6, 644-658
O'Neill, L. A. (2006) Curr. Opin. Immunol. 18, 3-9
Stetson, D. B., and Medzhitov, R. (2006) Immunity 25, 373-381
Akira, S., Uematsu, S., and Takeuchi, O. (2006) Cell 124, 783-801
West, A. P., Koblansky, A. A., and Ghosh, S. (2006) Annu. Rev. Cell Dev. Biol. 22, 409-437
Sato, S., Sanjo, H., Takeda, K., Ninomiya-Tsuji, J., Yamamoto, M., Kawai, T., Matsumoto, K., Takeuchi, O., and Akira, S. (2005) Nat. Immunol. 6, 1087-1095
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., Yamada, G., Akira, S., Matsumoto, K., and Ghosh, S. (2005) Genes Dev. 19, 2668-2681
Hacker, H., Redecke, V., Blagoev, B., Kratchmarova, I., Hsu, L. C., Wang, G. G., Kamps, M. P., Raz, E., Wagner, H., Hacker, G., Mann, M., and Karin, M. (2006) Nature 439, 204-207
Oganesyan, G., Saha, S. K., Guo, B., He, J. Q., Shahangian, A., Zarnegar, B., Perry, A., and Cheng, G. (2006) Nature 439, 208-211
Sasai, M., Oshiumi, H., Matsumoto, M., Inoue, N., Fujita, F., Nakanishi, M., and Seya, T. (2005) J. Immunol. 174, 27-30
Cheng, G., and Baltimore, D. (1996) Genes Dev. 10, 963-973
Peters, R. T., Liao, S. M., and Maniatis, T. (2000) Mol. Cell 5, 513-522
Nomura, F., Kawai, T., Nakanishi, K., and Akira, S. (2000) Genes Cells 5, 191-202
Pomerantz, J. L., and Baltimore, D. (1999) EMBO J. 18, 6694-6704
Kaye, K. M., Devergne, O., Harada, J. N., Izumi, K. M., Yalamanchili, R., Kieff, E., and Mosialos, G. (1996) Proc. Natl. Acad. Sci. U. S. A. 93, 11085-11090
Rothe, M., Xiong, J., Shu, H. B., Williamson, K., Goddard, A., and Goeddel, D. V. (1996) Proc. Natl. Acad. Sci. U. S. A. 93, 8241-8246
Chariot, A., Leonardi, A., Muller, J., Bonif, M., Brown, K., and Siebenlist, U. (2002) J. Biol. Chem. 277, 37029-37036
Adli, M., and Baldwin, A. S. (2006) J. Biol. Chem. 281, 26976-26984
Harris, J., Oliere, S., Sharma, S., Sun, Q., Lin, R., Hiscott, J., and Grandvaux, N. (2006) J. Immunol. 177, 2527-2535
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) Nat. Immunol. 4, 491-496
Sharma, S., tenOever, B. R., Grandvaux, N., Zhou, G. P., Lin, R., and Hiscott, J. (2003) Science 300, 1148-1151
Hemmi, H., Takeuchi, O., Sato, S., Yamamoto, M., Kaisho, T., Sanjo, H., Kawai, T., Hoshino, K., Takeda, K., and Akira, S. (2004) J. Exp. Med. 199, 1641-1650
Karin, M., and Ben-Neriah, Y. (2000) Annu. Rev. Immunol. 18, 621-663
Hayden, M. S., and Ghosh, S. (2004) Genes Dev. 18, 2195-2224
Chen, Z. J. (2005) Nat. Cell Biol. 7, 758-765
Sebban, H., Yamaoka, S., and Courtois, G. (2006) Trends Cell Biol. 16, 569-577
Wang, C., Deng, L., Hong, M., Akkaraju, G. R., Inoue, J., and Chen, Z. J. (2001) Nature 412, 346-351
Israel, A. (2006) Trends Immunol. 27, 395-397
Tang, E. D., Wang, C. Y., Xiong, Y., and Guan, K. L. (2003) J. Biol. Chem. 278, 37297-37305
Wu, C. J., Conze, D. B., Li, T., Srinivasula, S. M., and Ashwell, J. D. (2006) Nat. Cell Biol. 8, 398-406
Zhou, H., Wertz, I., O'Rourke, K., Ultsch, M., Seshagiri, S., Eby, M., Xiao, W., and Dixit, V. M. (2004) Nature 427, 167-171
Abbott, D. W., Wilkins, A., Asara, J. M., and Cantley, L. C. (2004) Curr. Biol. 14, 2217-2227
Yamamoto, M., Okamoto, T., Takeda, K., Sato, S., Sanjo, H., Uematsu, S., Saitoh, T., Yamamoto, N., Sakurai, H., Ishii, K. J., Yamaoka, S., Kawai, T., Matsuura, Y., Takeuchi, O., and Akira, S. (2006) Nat. Immunol. 7, 962-970
Leonardi, A., Chariot, A., Claudio, E., Cunningham, K., and Siebenlist, U. (2000) Proc. Natl. Acad. Sci. U. S. A. 97, 10494-10499
Leonardi, A., Ellinger-Ziegelbauer, H., Franzoso, G., Brown, K., and Siebenlist, U. (2000) J. Biol. Chem. 275, 271-278
Bonif, M., Meuwis, M. A., Close, P., Benoit, V., Heyninck, K., Chapelle, J. P., Bours, V., Merville, M. P., Piette, J., Beyaert, R., and Chariot, A. (2006) Biochem. J. 394, 593-603
Mosesson, Y., Shtiegman, K., Katz, M., Zwang, Y., Vereb, G., Szollosi, J., and Yarden, Y. (2003) J. Biol. Chem. 278, 21323-21326
Rubinson, D. A., Dillon, C. P., Kwiatkowski, A. V., Sievers, C., Yang, L., Kopinja, J., Rooney, D. L., Ihrig, M. M., McManus, M. T., Gertler, F. B., Scott, M. L., and Van Parijs, L. (2003) Nat. Genet. 33, 401-406
Huang, J., Liu, T., Xu, L. G., Chen, D., Zhai, Z., and Shu, H. B. (2005)EMBO J. 24, 4018-4028
Solis, M., Romieu-Mourez, R., Goubau, D., Grandvaux, N., Mesplede, T., Julkunen, I., Nardin, A., Salcedo, M., and Hiscott, J. (2007) Eur. J. Immunol. 37, 528-539
Kawai, T., Sato, S., Ishii, K. J., Coban, C., Hemmi, H., Yamamoto, M., Terai, K., Matsuda, M., Inoue, J., Uematsu, S., Takeuchi, O., and Akira, S. (2004) Nat. Immunol. 5, 1061-1068
Ben-Neriah, Y. (2002) Nat. Immunol. 3, 20-26
Liu, Y. C., Penninger, J., and Karin, M. (2005) Nat. Rev. Immunol. 5, 941-952
Hofmann, R. M., and Pickart, C. M. (1999) Cell 96, 645-653
Sato, S., Sugiyama, M., Yamamoto, M., Watanabe, Y., Kawai, T., Takeda, K., and Akira, S. (2003) J. Immunol. 171, 4304-4310
Fujita, F., Taniguchi, Y., Kato, T., Narita, Y., Furuya, A., Ogawa, T., Sakurai, H., Joh, T., Itoh, M., Delhase, M., Karin, M., and Nakanishi, M. (2003) Mol. Cell. Biol. 23, 7780-7793
Pomerantz, J. L., and Baltimore, D. (2002) Mol. Cell 10, 693-695
Guo, B., and Cheng, G. (2007) J. Biol. Chem. 282, 11817-11826
Zhao, T., Yang, L., Sun, Q., Arguello, M., Ballard, D. W., Hiscott, J., and Lin, R. (2007) Nat. Immunol., in press
O'Neill, L. A. J., and Bowie, A. G. (2007) Nat. Rev. Immunol. 7, 353-364
Lamothe, B., Besse, A., Campos, A. D., Webster, W. K., Wu, H., and Darnay, B. G. (2007) J. Biol. Chem. 282, 4102-4112
He, J. Q., Saha, S. K., Kang, J. R., Zarnegar, B., and Cheng, G. (2007) J. Biol. Chem. 282, 3688-3694
Gack, M. U., Shin, Y. C., Joo, C.-H., Urano, T., Liang, C., Sun, L., Osamu, T., Akira, S., Chen, Z., Inoue, S., and Jung, J. U. (2007) Nature 446, 916-920
Korherr, C., Gille, H., Schafer, R., Koenig-Hoffmann, K., Dixelius, J., Egland, K. A., Pastan, I., and Brinkmann, U. (2006) Proc. Natl. Acad. Sci. U. S. A. 103, 4240-4245
Chien, Y., Kim, S., Bumeister, R., Loo, Y. M., Kwon, S. W., Johnson, C. L., Balakireva, M. G., Romeo, Y., Kopelovich, L., Gale, M., Jr., Yeaman, C., Camonis, J. H., Zhao, Y., and White, M. A. (2006) Cell 127, 157-170
Oshima, K., Takeda, M., Kuranaga, E., Ueda, R., Aigaki, T., Miura, M., and Hayashi, S. (2006) Curr. Biol. 16, 1531-1537
