Interleukin-1 and TRAF6-dependent activation of TAK1 in the absence of TAB2 and TAB3

Biochemical Journal

Volumn 474, Issue 13, 2017, Pages 2235-2248

  Zhang, Jiazhen ^a   Macartney, Thomas ^a   Peggie, Mark ^a   Cohen, Philip ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HETERODIMER; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 8; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE 1; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1 BINDING 2; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1 BINDING 3; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UBIQUITIN CONJUGATING ENZYME 13; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS; MAP KINASE KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; PROTEIN BINDING; SIGNAL PEPTIDE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TAB2 PROTEIN, HUMAN; TAB3 PROTEIN, HUMAN; TIFAB PROTEIN, HUMAN; UBIQUITIN;

ARTICLE; ENZYME ACTIVATION; GENE EDITING; HUMAN; IMMEDIATE EARLY GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; CRISPR CAS SYSTEM; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; METABOLISM; PHOSPHORYLATION; UBIQUITINATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CRISPR-CAS SYSTEMS; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; INTERLEUKIN-1; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAP KINASE KINASE KINASES; PHOSPHORYLATION; PROTEIN BINDING; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED FACTOR 6; UBIQUITIN; UBIQUITINATION;

EID: 85022024657     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BCJ20170288     Document Type: Article

References (44)

1. Garlanda, C., Dinarello, C.A. and Mantovani, A. (2013) The interleukin-1 family: back to the future. Immunity 39, 1003-1018 doi:10.1016/j.immuni. 2013.11.010
2. Lin, S.-C., Lo, Y.-C. and Wu, H. (2010) Helical assembly in the MyD88-IRAK4-IRAK2 complex in TLR/IL-1R signalling. Nature 465, 885-890 doi:10. 1038/nature09121
3. Motshwene, P.G., Moncrieffe, M.C., Grossmann, J.G., Kao, C., Ayaluru, M., Sandercock, A.M. et al. (2009) An oligomeric signaling platform formed by the Toll-like receptor signal transducers MyD88 and IRAK-4. J. Biol. Chem. 284, 25404-25411 doi:10.1074/jbc.M109.022392
4. Ye, H., Arron, J.R., Lamothe, B., Cirilli, M., Kobayashi, T., Shevde, N.K. et al. (2002) Distinct molecular mechanism for initiating TRAF6 signalling. Nature 418, 443-447 doi:10.1038/nature00888
5. Yin, Q., Lin, S.-C., Lamothe, B., Lu, M., Lo, Y.-C., Hura, G. et al. (2009) E2 interaction and dimerization in the crystal structure of TRAF6. Nat. Struct. Mol. Biol. 16, 658-666 doi:10.1038/nsmb.1605
6. Smith, H., Peggie, M., Campbell, D.G., Vandermoere, F., Carrick, E. and Cohen, P. (2009) Identification of the phosphorylation sites on the E3 ubiquitin ligase Pellino that are critical for activation by IRAK1 and IRAK4. Proc. Natl Acad. Sci. U.S.A. 106, 4584-4590 doi:10.1073/pnas.0900774106
7. Ordureau, A., Smith, H., Windheim, M., Peggie, M., Carrick, E., Morrice, N. et al. (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 doi:10.1042/BJ20071365
8. Goh, E.T.H., Arthur, J.S.C., Cheung, P.C.F., Akira, S., Toth, R. and Cohen, P. (2012) Identification of the protein kinases that activate the E3 ubiquitin ligase Pellino 1 in the innate immune system. Biochem. J. 441, 339-346 doi:10.1042/BJ20111415
9. Strickson, S., Emmerich, C.H., Goh, E.T.H., Zhang, J., Kelsall, I.R., Macartney, T. et al. (2017) Roles of the TRAF6 and Pellino E3 ligases in MyD88 and RANKL signaling. Proc. Natl Acad. Sci. U.S.A. 114, E3481-E3489 doi:10.1073/pnas.1702367114
10. Pauls, E., Nanda, S.K., Smith, H., Toth, R., Arthur, J.S.C. and Cohen, P. (2013) Two phases of inflammatory mediator production defined by the study of IRAK2 and IRAK1 knock-in mice. J. Immunol. 191, 2717-2730 doi:10.4049/jimmunol.1203268
11. Xia, Z.-P., Sun, L., Chen, X., Pineda, G., Jiang, X., Adhikari, A. et al. (2009) Direct activation of protein kinases by unanchored polyubiquitin chains. Nature 461, 114-119 doi:10.1038/nature08247
12. Wang, C., Deng, L., Hong, M., Akkaraju, G.R., Inoue, J.-i. and Chen, Z.J. (2001) TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412, 346-351 doi:10.1038/35085597
13. Cheung, P.C.F., Nebreda, A.R. and Cohen, P. (2004) TAB3, a new binding partner of the protein kinase TAK1. Biochem. J. 378, 27-34 doi:10.1042/ bj20031794
14. Kanayama, A., Seth, R.B., Sun, L., Ea, C.-K., Hong, M., Shaito, A. et al. (2004) TAB2 and TAB3 activate the NF-κB pathway through binding to polyubiquitin chains. Mol. Cell 15, 535-548 doi:10.1016/j.molcel.2004.08.008
15. Kulathu, Y., Akutsu, M., Bremm, A., Hofmann, K. and Komander, D. (2009) Two-sided ubiquitin binding explains specificity of the TAB2 NZF domain. Nat. Struct. Mol. Biol. 16, 1328-1330 doi:10.1038/nsmb.1731
16. Tournier, C., Dong, C., Turner, T.K., Jones, S.N., Flavell, R.A. and Davis, R.J. (2001) MKK7 is an essential component of the JNK signal transduction pathway activated by proinflammatory cytokines. Genes Dev. 15, 1419-1426 doi:10.1101/gad.888501
17. Lawler, S., Fleming, Y., Goedert, M. and Cohen, P. (1998) Synergistic activation of SAPK1/JNK1 by two MAP kinase kinases in vitro. Curr. Biol. 8, 1387-1391 doi:10.1016/S0960-9822(98)00019-0
18. Shim, J.-H., Xiao, C., Paschal, A.E., Bailey, S.T., Rao, P., Hayden, M.S. et al. (2005) TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev. 19, 2668-2681 doi:10.1101/gad.1360605
19. Sato, S., Sanjo, H., Takeda, K., Ninomiya-Tsuji, J., Yamamoto, M., Kawai, T. et al. (2005) Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat. Immunol. 6, 1087-1095 doi:10.1038/ni1255
20. Zhang, J., Clark, K., Lawrence, T., Peggie, M.W. and Cohen, P. (2014) An unexpected twist to the activation of IKKβ: TAK1 primes IKKβ for activation by autophosphorylation. Biochem. J. 461, 531-537 doi:10.1042/BJ20140444
21. DiDonato, J.A., Hayakawa, M., Rothwarf, D.M., Zandi, E. and Karin, M. (1997) A cytokine-responsive IκB kinase that activates the transcription factor NF-κB. Nature 388, 548-554 doi:10.1038/41493
22. Lopez-Pelaez, M., Lamont, D.J., Peggie, M., Shpiro, N., Gray, N.S. and Cohen, P. (2014) Protein kinase IKKβ-catalyzed phosphorylation of IRF5 at Ser462 induces its dimerization and nuclear translocation in myeloid cells. Proc. Natl Acad. Sci. U.S.A. 111, 17432-17437 doi:10.1073/pnas.1418399111
23. Ren, J., Chen, X. and Chen, Z.J. (2014) IKKβ is an IRF5 kinase that instigates inflammation. Proc. Natl Acad. Sci. U.S.A. 111, 17438-17443 doi:10. 1073/pnas.1418516111
24. Waterfield, M., Jin, W., Reiley, W., Zhang, M. and Sun, S.-C. (2004) Iκb kinase is an essential component of the Tpl2 signaling pathway. Mol. Cell. Biol. 24, 6040-6048 doi:10.1128/MCB.24.13.6040-6048.2004
25. Beinke, S., Robinson, M.J., Hugunin, M. and Ley, S.C. (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 doi:10.1128/ MCB.24.21.9658-9667.2004
26. Ben-Addi, A., Mambole-Dema, A., Brender, C., Martin, S.R., Janzen, J., Kjaer, S. et al. (2014) Iκb kinase-induced interaction of TPL-2 kinase with 14-3-3 is essential for Toll-like receptor activation of ERK-1 and -2 MAP kinases. Proc. Natl Acad. Sci. U.S.A. 111, E2394-E2403 doi:10.1073/pnas.1320440111
27. Gantke, T., Sriskantharajah, S., Sadowski, M. and Ley, S.C. (2012) Iκb kinase regulation of the TPL-2/ERK MAPK pathway. Immunol. Rev. 246, 168-182 doi:10.1111/j.1600-065X.2012.01104.x
28. Pattison, M.J., Mitchell, O., Flynn, H.R., Chen, C.-S., Yang, H.-T., Ben-Addi, H. et al. (2016) TLR and TNF-R1 activation of the MKK3/MKK6-p38α axis in macrophages is mediated by TPL-2 kinase. Biochem. J. 473, 2845-2861 doi:10.1042/BCJ20160502
29. Emmerich, C.H., Ordureau, A., Strickson, S., Arthur, J.S.C., Pedrioli, P.G.A., Komander, D. et al. (2013) Activation of the canonical IKK complex by K63/ M1-linked hybrid ubiquitin chains. Proc. Natl Acad. Sci. U.S.A. 110, 15247-15252 doi:10.1073/pnas.1314715110
30. Cushing, L., Stochaj, W., Siegel, M., Czerwinski, R., Dower, K., Wright, Q. et al. (2014) Interleukin 1/Toll-like receptor-induced autophosphorylation activates interleukin 1 receptor-associated kinase 4 and controls cytokine induction in a cell type-specific manner. J. Biol. Chem. 289, 10865-10875 doi:10.1074/jbc.M113.544809
31. Vince, J.E., Wong, W.W.-L., Khan, N., Feltham, R., Chau, D., Ahmed, A.U. et al. (2007) IAP antagonists target cIAP1 to induce TNFα-dependent apoptosis. Cell 131, 682-693 doi:10.1016/j.cell.2007.10.037
32. Vince, J.E., Wong, W.W.-L., Gentle, I., Lawlor, K.E., Allam, R., O'Reilly, L. et al. (2012) Inhibitor of apoptosis proteins limit RIP3 kinase-dependent interleukin-1 activation. Immunity 36, 215-227 doi:10.1016/j.immuni.2012.01.012
33. Lawlor, K.E., Khan, N., Mildenhall, A., Gerlic, M., Croker, B.A., D'Cruz, A.A. et al. (2015) RIPK3 promotes cell death and NLRP3 inflammasome activation in the absence of MLKL. Nat. Commun. 6, 6282 doi:10.1038/ncomms7282
34. Singhirunnusorn, P., Suzuki, S., Kawasaki, N., Saiki, I. and Sakurai, H. (2005) Critical roles of threonine 187 phosphorylation in cellular stress-induced rapid and transient activation of transforming growth factor-β-activated kinase 1 (TAK1) in a signaling complex containing TAK1-binding protein TAB1 and TAB2. J. Biol. Chem. 280, 7359-7368 doi:10.1074/jbc.M407537200
35. Deng, L., Wang, C., Spencer, E., Yang, L., Braun, A., You, J. et al. J. (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 doi:10.1016/S0092-8674(00)00126-4
36. Lu, M., Lin, S.-C., Huang, Y., Kang, Y.J., Rich, R., Lo, Y.-C. et al. (2007) XIAP induces NF-κB activation via the BIR1/TAB1 interaction and BIR1 dimerization. Mol. Cell 26, 689-702 doi:10.1016/j.molcel.2007.05.006
37. Gu, M., Ouyang, C., Lin, W., Zhang, T., Cao, X., Xia, Z. et al. (2014) Phosphatase holoenzyme PP1/GADD34 negatively regulates TLR response by inhibiting TAK1 serine 412 phosphorylation. J. Immunol. 192, 2846-2856 doi:10.4049/jimmunol.1302537
38. Ouyang, C., Nie, L., Gu, M., Wu, A., Han, X., Wang, X. et al. (2014) Transforming growth factor (TGF)-β-activated kinase 1 (TAK1) activation requires phosphorylation of serine 412 by protein kinase A catalytic subunit α (PKACα) and X-linked protein kinase (PRKX). J. Biol. Chem. 289, 24226-24237 doi:10.1074/jbc.M114.559963
39. Kim, S.I., Kwak, J.H., Wang, L. and Choi, M.E. (2008) Protein phosphatase 2A is a negative regulator of transforming growth factor-β1-induced TAK1 activation in mesangial cells. J. Biol. Chem. 283, 10753-10763 doi:10.1074/jbc.M801263200
40. Kajino, T., Ren, H., Iemura, S.-i., Natsume, T., Stefansson, B., Brautigan, D.L. et al. (2006) Protein phosphatase 6 down-regulates TAK1 kinase activation in the IL-1 signaling pathway. J. Biol. Chem. 281, 39891-39896 doi:10.1074/jbc.M608155200
41. Ori, D., Kato, H., Sanjo, H., Tartey, S., Mino, T., Akira, S. et al. (2013) Essential roles of K63-linked polyubiquitin-binding proteins TAB2 and TAB3 in B cell activation via MAPKs. J. Immunol. 190, 4037-4045 doi:10.4049/jimmunol.1300173
42. Hubbard, M.J. and Cohen, P. (1993) On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem. Sci. 18, 172-177 doi:10.1016/0968-0004(93)90109-Z
43. Schröfelbauer, B., Polley, S., Behar, M., Ghosh, G. and Hoffmann, A. (2012) NEMO ensures signaling specificity of the pleiotropic IKKβ by directing its kinase activity toward IκBα. Mol. Cell 47, 111-121 doi:10.1016/j.molcel.2012.04.020
44. Clark, K., Nanda, S. and Cohen, P. (2013) Molecular control of the NEMO family of ubiquitin-binding proteins. Nat. Rev. Mol. Cell Biol. 14, 673-685 doi:10.1038/nrm3644