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)

Journal of Biological Chemistry

Volumn 289, Issue 35, 2014, Pages 24226-24237

  Ouyang, Chuan ^a   Nie, Li ^b   Gu, Meidi ^c   Wu, Ailing ^a   Han, Xu ^a   Wang, Xiaojian ^c   Shao, Jianzhong ^b   Xia, Zongping ^a  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CHEMICAL ACTIVATION; ENZYMES; PHOSPHORYLATION; PROTEINS; SIGNALING;

AUTOPHOSPHORYLATION; CATALYTIC SUBUNITS; DOMAIN-MEDIATED DIMERIZATION; MOLECULAR MECHANISM; PRO-INFLAMMATORY STIMULI; PROINFLAMMATORY CYTOKINES; TOLL-LIKE RECEPTORS; TRANSFORMING GROWTH FACTORS;

MOLECULAR INTERACTIONS;

CYCLIC AMP DEPENDENT PROTEIN KINASE CATALYTIC SUBUNIT; CYCLIC AMP DEPENDENT PROTEIN KINASE CATALYTIC SUBUNIT ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; PROTEIN KINASE; SERINE; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; X LINKED PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE; MAP KINASE KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; PROTEIN SERINE THREONINE KINASE;

ARTICLE; AUTOPHOSPHORYLATION; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DIMERIZATION; EMBRYO; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; GENETIC TRANSFECTION; IN VITRO STUDY; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ZEBRA FISH; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; CHEMISTRY; ENZYME ACTIVE SITE; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE; PHOSPHORYLATION; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; ANIMALS; CATALYTIC DOMAIN; CELL LINE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DIMERIZATION; ENZYME ACTIVATION; HUMANS; MAP KINASE KINASE KINASES; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SEQUENCE HOMOLOGY, AMINO ACID; ZEBRAFISH;

EID: 84906880166     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.559963     Document Type: Article

References (35)

1. 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) TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev. 19, 2668-2681 (Pubitemid 41627934)
2. Jadrich, J. L., O'Connor, M. B., and Coucouvanis, E. (2006) The TGF β activated kinase TAK1 regulates vascular development in vivo. Development 133, 1529-1541 (Pubitemid 43732966)
3. Ajibade, A. A., Wang, H. Y., and Wang, R. F. (2013) Cell type-specific function of TAK1 in innate immune signaling. Trends Immunol. 34, 307-316
4. Chen, Z. J. (2005) Ubiquitin signalling in the NF-κB pathway. Nat. Cell Biol. 7, 758-765
5. Ghosh, S., and Hayden, M. S. (2012) Celebrating 25 years of NF-κB research. Immunol. Rev. 246, 5-13
6. 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 (Pubitemid 41541786)
7. Ishitani, T., Takaesu, G., Ninomiya-Tsuji, J., Shibuya, H., Gaynor, R. B., and Matsumoto, K. (2003) Role of the TAB2-related protein TAB3 in IL-1 and TNF signaling. EMBO J. 22, 6277-6288 (Pubitemid 37522585)
8. Kanayama, A., Seth, R. B., Sun, L., Ea, C. K., Hong, M., Shaito, A., Chiu, Y. H., Deng, L., and Chen, Z. J. (2004) TAB2 and TAB3 activate the NF-κB pathway through binding to polyubiquitin chains. Mol. Cell 15, 535-548 (Pubitemid 39141781)
9. Inagaki, M., Omori, E., Kim, J. Y., Komatsu, Y., Scott, G., Ray, M. K., Yamada, G., Matsumoto, K., Mishina, Y., and Ninomiya-Tsuji, J. (2008) TAK1-binding protein 1, TAB1, mediates osmotic stress-induced TAK1 activation but is dispensable for TAK1-mediated cytokine signaling. J. Biol. Chem. 283, 33080-33086
10. 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 (Pubitemid 40341294)
11. Scholz, R., Sidler, C. L., Thali, R. F., Winssinger, N., Cheung, P. C., and Neumann, D. (2010) Autoactivation of transforming growth factor β-activated kinase 1 is a sequential bimolecular process. J. Biol. Chem. 285, 25753-25766
12. Yu, Y., Ge, N., Xie, M., Sun, W., Burlingame, S., Pass, A. K., Nuchtern, J. G., Zhang, D., Fu, S., Schneider, M. D., Fan, J., and Yang, J. (2008) Phosphorylation of Thr-178 and Thr-184 in the TAK1 T-loop is required for interleukin (IL)-1-mediated optimal NFκB and AP-1 activation as well as IL-6 gene expression. J. Biol. Chem. 283, 24497-24505
13. Sakurai, H., Nishi, A., Sato, N., Mizukami, J., Miyoshi, H., and Sugita, T. (2002) TAK1-TAB1 fusion protein: a novel constitutively active mitogen-activated protein kinase kinase kinase that stimulates AP-1 and NF-κB signaling pathways. Biochem. Biophys. Res. Commun. 297, 1277-1281 (Pubitemid 35216385)
14. Sakurai, H., Miyoshi, H., Mizukami, J., and Sugita, T. (2000) Phosphorylation-dependent activation of TAK1 mitogen-activated protein kinase kinase kinase by TAB1. FEBS Lett. 474, 141-145 (Pubitemid 30330823)
15. Kishimoto, K., Matsumoto, K., and Ninomiya-Tsuji, J. (2000)TAK1 mitogen-activated protein kinase kinase kinase is activated by autophosphorylation within its activation loop. J. Biol. Chem. 275, 7359-7364 (Pubitemid 30146289)
16. Kobayashi, Y., Mizoguchi, T., Take, I., Kurihara, S., Udagawa, N., and Takahashi, N. (2005) Prostaglandin E2 enhances osteoclastic differentiation of precursor cells through protein kinase A-dependent phosphorylation of TAK1. J. Biol. Chem. 280, 11395-11403 (Pubitemid 40418448)
17. 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
18. Prickett, T. D., Ninomiya-Tsuji, J., Broglie, P., Muratore-Schroeder, T. L., Shabanowitz, J., Hunt, D. F., and Brautigan, D. L. (2008) TAB4 stimulates TAK1-TAB1 phosphorylation and binds polyubiquitin to direct signaling to NF-κB. J. Biol. Chem. 283, 19245-19254
19. Taylor, S. S., Keshwani, M. M., Steichen, J. M., and Kornev, A. P. (2012) Evolution of the eukaryotic protein kinases as dynamic molecular switches. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 2517-2528
20. Pearce, L. R., Komander, D., and Alessi, D. R. (2010) The nuts and bolts of AGC protein kinases. Nat. Rev. Mol. Cell Biol. 11, 9-22
21. Dulin, N. O., Niu, J., Browning, D. D., Ye, R. D., and Voyno-Yasenetskaya, T. (2001) Cyclic AMP-independent activation of protein kinase A by vasoactive peptides. J. Biol. Chem. 276, 20827-20830
22. Zieger, M., Tausch, S., Henklein, P., Nowak, G., and Kaufmann, R. (2001) A novel PAR-1-type thrombin receptor signaling pathway: cyclic AMP-independent activation of PKA in SNB-19 glioblastoma cells. Biochem. Biophys. Res. Commun. 282, 952-957 (Pubitemid 32924587)
23. Gerlo, S., Kooijman, R., Beck, I. M., Kolmus, K., Spooren, A., and Haegeman, G. (2011) Cyclic AMP: a selective modulator of NF-κB action. Cell. Mol. Life Sci. 68, 3823-3841
24. Mosenden, R., and Taskén, K. (2011) Cyclic AMP-mediated immune regulation: overview of mechanisms of action in T cells. Cell. Signal. 23, 1009-1016
25. Zhong, H., Voll, R. E., and Ghosh, S. (1998) Phosphorylation of NF-κB p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol. Cell 1, 661-671 (Pubitemid 128379244)
26. Wall, E. A., Zavzavadjian, J. R., Chang, M. S., Randhawa, B., Zhu, X., Hsueh, R. C., Liu, J., Driver, A., Bao, X. R., Sternweis, P. C., Simon, M. I., and Fraser, I. D. (2009) Suppression of LPS-induced TNF-α production in macrophages by cAMP is mediated by PKA-AKAP95-p105. Sci. Signal. 2, ra28
27. Trede, N. S., Langenau, D. M., Traver, D., Look, A. T., and Zon, L. I. (2004) The use of zebrafish to understand immunity. Immunity 20, 367-379 (Pubitemid 38482116)
28. van der Vaart, M., Spaink, H. P., and Meijer, A. H. (2012) Pathogen recognition and activation of the innate immune response in zebrafish. Adv. Hematol. 2012, 159807
29. Stein, C., Caccamo, M., Laird, G., and Leptin, M. (2007) Conservation and divergence of gene families encoding components of innate immune response systems in zebrafish. Genome Biol. 8, R251
30. Gu, M., Ouyang, C., Lin, W., Zhang, T., Cao, X., Xia, Z., and Wang, X. (2014) Phosphatase holoenzyme PP1/GADD34 negatively regulates TLR response by inhibiting TAK1 serine 412 phosphorylation. J. Immunol. 192, 2846-2856
31. An, H., Zhao, W., Hou, J., Zhang, Y., Xie, Y., Zheng, Y., Xu, H., Qian, C., Zhou, J., Yu, Y., Liu, S., Feng, G., and Cao, X. (2006) SHP-2 phosphatase negatively regulates the TRIF adaptor protein-dependent type I interferon and proinflammatory cytokine production. Immunity 25, 919-928 (Pubitemid 44894946)
32. Xiong, R., Nie, L., Xiang, L. X., and Shao, J. Z. (2012) Characterization of a PIAS4 homologue from zebrafish: insights into its conserved negative regulatory mechanism in the TRIF, MAVS, and IFN signaling pathways during vertebrate evolution. J. Immunol. 188, 2653-2668
33. Takaesu, G., Kishida, S., Hiyama, A., Yamaguchi, K., Shibuya, H., Irie, K., Ninomiya-Tsuji, J., and Matsumoto, K. (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
34. Xia, Z. P., Sun, L., Chen, X., Pineda, G., Jiang, X., Adhikari, A., Zeng, W., and Chen, Z. J. (2009) Direct activation of protein kinases by unanchored polyubiquitin chains. Nature 461, 114-119
35. Tachibana, M., Ueda, J., Fukuda, M., Takeda, N., Ohta, T., Iwanari, H., Sakihama, T., Kodama, T., Hamakubo, T., and Shinkai, Y. (2005) Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3-K9. Genes Dev. 19, 815-826