Structure and Ubiquitination-Dependent Activation of TANK-Binding Kinase 1

Cell Reports

Volumn 3, Issue 3, 2013, Pages 747-758

  Tu, Daqi ^a,b   Zhu, Zehua ^a,c   Zhou, Alicia Y ^a,c   Yun, Cai hong ^a,b   Lee, Kyung Eun ^d   Toms, Angela V ^a,b   Li, Yiqun ^a   Dunn, Gavin P ^a,c   Chan, Edmond ^a,c   Thai, Tran ^a,c   Yang, Shenghong ^a,c   Ficarro, Scott B ^a,b   Marto, Jarrod A ^a,b   Jeon, Hyesung ^d   Hahn, William C ^a,c   Barbie, David A ^a,c   Eck, Michael J ^a,b  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d Korea Institute of Science and Technology   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B KINASE BETA; I KAPPA B KINASE EPSILON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 3; LYSINE; PROTEIN SERINE THREONINE KINASE; TANK BINDING KINASE 1; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UBIQUITINATION;

AMINO ACID SEQUENCE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; HUMANS; I-KAPPA B KINASE; INTERFERON REGULATORY FACTOR-3; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; UBIQUITINATION;

EID: 84875808591     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.01.033     Document Type: Article

References (53)

1. Abbott D.W., Wilkins A., Asara J.M., Cantley L.C. The Crohn's disease protein, NOD2, requires RIP2 in order to induce ubiquitinylation of a novel site on NEMO. Curr. Biol. 2004, 14:2217-2227.
2. Ashkenazy H., Erez E., Martz E., Pupko T., Ben-Tal N. ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res. 2010, 38(Web Server issue):W529-W533.
3. Barbie D.A., Tamayo P., Boehm J.S., Kim S.Y., Moody S.E., Dunn I.F., Schinzel A.C., Sandy P., Meylan E., Scholl C., et al. Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1. Nature 2009, 462:108-112.
4. Bianchi K., Meier P. A tangled web of ubiquitin chains: breaking news in TNF-R1 signaling. Mol. Cell 2009, 36:736-742.
5. Boehm J.S., Zhao J.J., Yao J., Kim S.Y., Firestein R., Dunn I.F., Sjostrom S.K., Garraway L.A., Weremowicz S., Richardson A.L., et al. Integrative genomic approaches identify IKBKE as a breast cancer oncogene. Cell 2007, 129:1065-1079.
6. Bonnard M., Mirtsos C., Suzuki S., Graham K., Huang J., Ng M., Itié A., Wakeham A., Shahinian A., Henzel W.J., et al. Deficiency of T2K leads to apoptotic liver degeneration and impaired NF-kappaB-dependent gene transcription. EMBO J. 2000, 19:4976-4985.
7. Chariot A., Leonardi A., Muller J., Bonif M., Brown K., Siebenlist U. 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. 2002, 277:37029-37036.
8. Chau T.L., Gioia R., Gatot J.S., Patrascu F., Carpentier I., Chapelle J.P., O'Neill L., Beyaert R., Piette J., Chariot A. Are the IKKs and IKK-related kinases TBK1 and IKK-epsilon similarly activated?. Trends Biochem. Sci. 2008, 33:171-180.
9. Chen H., Sun H., You F., Sun W., Zhou X., Chen L., Yang J., Wang Y., Tang H., Guan Y., et al. Activation of STAT6 by STING is critical for antiviral innate immunity. Cell 2011, 147:436-446.
10. Chiang S.H., Bazuine M., Lumeng C.N., Geletka L.M., Mowers J., White N.M., Ma J.T., Zhou J., Qi N., Westcott D., et al. The protein kinase IKKepsilon regulates energy balance in obese mice. Cell 2009, 138:961-975.
11. Chien Y., Kim S., Bumeister R., Loo Y.M., Kwon S.W., Johnson C.L., Balakireva M.G., Romeo Y., Kopelovich L., Gale M., et al. RalB GTPase-mediated activation of the IkappaB family kinase TBK1 couples innate immune signaling to tumor cell survival. Cell 2006, 127:157-170.
12. Clark K., Plater L., Peggie M., Cohen P. Use of the pharmacological inhibitor BX795 to study the regulation and physiological roles of TBK1 and IkappaB kinase epsilon: a distinct upstream kinase mediates Ser-172 phosphorylation and activation. J. Biol. Chem. 2009, 284:14136-14146.
13. Clark K., Peggie M., Plater L., Sorcek R.J., Young E.R., Madwed J.B., Hough J., McIver E.G., Cohen P. Novel cross-talk within the IKK family controls innate immunity. Biochem. J. 2011, 434:93-104.
14. Clark K., Takeuchi O., Akira S., Cohen P. The TRAF-associated protein TANK facilitates cross-talk within the IkappaB kinase family during Toll-like receptor signaling. Proc. Natl. Acad. Sci. USA 2011, 108:17093-17098.
15. Dolcet X., Llobet D., Pallares J., Matias-Guiu X. NF-kB in development and progression of human cancer. Virchows Arch. 2005, 446:475-482.
16. Feldman R.I., Wu J.M., Polokoff M.A., Kochanny M.J., Dinter H., Zhu D., Biroc S.L., Alicke B., Bryant J., Yuan S., et al. Novel small molecule inhibitors of 3-phosphoinositide-dependent kinase-1. J. Biol. Chem. 2005, 280:19867-19874.
17. Friedman C.S., O'Donnell M.A., Legarda-Addison D., Ng A., Cárdenas W.B., Yount J.S., Moran T.M., Basler C.F., Komuro A., Horvath C.M., et al. The tumour suppressor CYLD is a negative regulator of RIG-I-mediated antiviral response. EMBO Rep. 2008, 9:930-936.
18. Gleason C.E., Ordureau A., Gourlay R., Arthur J.S., Cohen P. Polyubiquitin binding to optineurin is required for optimal activation of TANK-binding kinase 1 and production of interferon β. J. Biol. Chem. 2011, 286:35663-35674.
19. Goncalves A., Bürckstümmer T., Dixit E., Scheicher R., Górna M.W., Karayel E., Sugar C., Stukalov A., Berg T., Kralovics R., et al. Functional dissection of the TBK1 molecular network. PLoS ONE 2011, 6:e23971.
20. Häcker H., Karin M. Regulation and function of IKK and IKK-related kinases. Sci. STKE 2006, 2006:re13.
21. Hayden M.S., Ghosh S. Signaling to NF-kappaB. Genes Dev. 2004, 18:2195-2224.
22. Hou F., Sun L., Zheng H., Skaug B., Jiang Q.X., Chen Z.J. MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell 2011, 146:448-461.
23. Hutti J.E., Shen R.R., Abbott D.W., Zhou A.Y., Sprott K.M., Asara J.M., Hahn W.C., Cantley L.C. Phosphorylation of the tumor suppressor CYLD by the breast cancer oncogene IKKepsilon promotes cell transformation. Mol. Cell 2009, 34:461-472.
24. Ishikawa H., Barber G.N. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 2008, 455:674-678.
25. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature 2006, 441:431-436.
26. Kishore N., Huynh Q.K., Mathialagan S., Hall T., Rouw S., Creely D., Lange G., Caroll J., Reitz B., Donnelly A., et al. IKK-i and TBK-1 are enzymatically distinct from the homologous enzyme IKK-2: comparative analysis of recombinant human IKK-i, TBK-1, and IKK-2. J. Biol. Chem. 2002, 277:13840-13847.
27. Li Q., Van Antwerp D., Mercurio F., Lee K.F., Verma I.M. Severe liver degeneration in mice lacking the IkappaB kinase 2 gene. Science 1999, 284:321-325.
28. Li S., Wang L., Berman M., Kong Y.Y., Dorf M.E. Mapping a dynamic innate immunity protein interaction network regulating type I interferon production. Immunity 2011, 35:426-440.
29. Li J., Li J., Miyahira A., Sun J., Liu Y., Cheng G., Liang H. Crystal structure of the ubiquitin-like domain of human TBK1. Protein Cell 2012, 3:383-391.
30. Ma X., Helgason E., Phung Q.T., Quan C.L., Iyer R.S., Lee M.W., Bowman K.K., Starovasnik M.A., Dueber E.C. Molecular basis of Tank-binding kinase 1 activation by transautophosphorylation. Proc. Natl. Acad. Sci. USA 2012, 109:9378-9383.
31. Morton S., Hesson L., Peggie M., Cohen P. Enhanced binding of TBK1 by an optineurin mutant that causes a familial form of primary open angle glaucoma. FEBS Lett. 2008, 582:997-1002.
32. Ou Y.H., Torres M., Ram R., Formstecher E., Roland C., Cheng T., Brekken R., Wurz R., Tasker A., Polverino T., et al. TBK1 directly engages Akt/PKB survival signaling to support oncogenic transformation. Mol. Cell 2011, 41:458-470.
33. Parvatiyar K., Barber G.N., Harhaj E.W. TAX1BP1 and A20 inhibit antiviral signaling by targeting TBK1-IKKi kinases. J. Biol. Chem. 2010, 285:14999-15009.
34. Peters R.T., Liao S.M., Maniatis T. IKKepsilon is part of a novel PMA-inducible IkappaB kinase complex. Mol. Cell 2000, 5:513-522.
35. Pomerantz J.L., Baltimore D. NF-kappaB activation by a signaling complex containing TRAF2, TANK and TBK1, a novel IKK-related kinase. EMBO J. 1999, 18:6694-6704.
36. Radtke A.L., Delbridge L.M., Balachandran S., Barber G.N., O'Riordan M.X. TBK1 protects vacuolar integrity during intracellular bacterial infection. PLoS Pathog. 2007, 3:e29.
37. Shen R.R., Hahn W.C. Emerging roles for the non-canonical IKKs in cancer. Oncogene 2011, 30:631-641.
38. Shen R.R., Zhou A.Y., Kim E., Lim E., Habelhah H., Hahn W.C. IκB kinase ε phosphorylates TRAF2 to promote mammary epithelial cell transformation. Mol. Cell. Biol. 2012, 32:4756-4768.
39. Shimada T., Kawai T., Takeda K., Matsumoto M., Inoue J., Tatsumi Y., Kanamaru A., Akira S. IKK-i, a novel lipopolysaccharide-inducible kinase that is related to IkappaB kinases. Int. Immunol. 1999, 11:1357-1362.
40. Tanaka Y., Chen Z.J. STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci. Signal. 2012, 5:ra20.
41. Tang E.D., Wang C.Y., Xiong Y., Guan K.L. A role for NF-kappaB essential modifier/IkappaB kinase-gamma (NEMO/IKKgamma) ubiquitination in the activation of the IkappaB kinase complex by tumor necrosis factor-alpha. J. Biol. Chem. 2003, 278:37297-37305.
42. Tenoever B.R., Ng S.L., Chua M.A., McWhirter S.M., García-Sastre A., Maniatis T. Multiple functions of the IKK-related kinase IKKepsilon in interferon-mediated antiviral immunity. Science 2007, 315:1274-1278.
43. Thurston T.L., Ryzhakov G., Bloor S., von Muhlinen N., Randow F. The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat. Immunol. 2009, 10:1215-1221.
44. Wang C., Chen T., Zhang J., Yang M., Li N., Xu X., Cao X. The E3 ubiquitin ligase Nrdp1 'preferentially' promotes TLR-mediated production of type I interferon. Nat. Immunol. 2009, 10:744-752.
45. Wang L., Li S., Dorf M.E. NEMO binds ubiquitinated TANK-binding kinase 1 (TBK1) to regulate innate immune responses to RNA viruses. PLoS ONE 2012, 7:e43756.
46. Weidberg H., Elazar Z. TBK1 mediates crosstalk between the innate immune response and autophagy. Sci. Signal. 2011, 4:pe39.
47. Wild P., Farhan H., McEwan D.G., Wagner S., Rogov V.V., Brady N.R., Richter B., Korac J., Waidmann O., Choudhary C., et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 2011, 333:228-233.
48. Xie X., Zhang D., Zhao B., Lu M.K., You M., Condorelli G., Wang C.Y., Guan K.L. IkappaB kinase epsilon and TANK-binding kinase 1 activate AKT by direct phosphorylation. Proc. Natl. Acad. Sci. USA 2011, 108:6474-6479.
49. Xu G., Lo Y.C., Li Q., Napolitano G., Wu X., Jiang X., Dreano M., Karin M., Wu H. Crystal structure of inhibitor of κB kinase β. Nature 2011, 472:325-330.
50. Yun C.H., Boggon T.J., Li Y., Woo M.S., Greulich H., Meyerson M., Eck M.J. Structures of lung cancer-derived EGFR mutants and inhibitor complexes: mechanism of activation and insights into differential inhibitor sensitivity. Cancer Cell 2007, 11:217-227.
51. Zeng W., Xu M., Liu S., Sun L., Chen Z.J. Key role of Ubc5 and lysine-63 polyubiquitination in viral activation of IRF3. Mol. Cell 2009, 36:315-325.
52. Zhou A.Y., Shen R.R., Kim E., Lock Y.J., Xu M., Chen Z.J., Hahn W.C. IKKε-mediated tumorigenesis requires K63-linked polyubiquitination by a cIAP1/cIAP2/TRAF2 E3 ubiquitin ligase complex. Cell Rep. 2013, 3. Published online February 28, 2013. 10.1016/j.celrep.2013.01.031.
53. Zhou H., Wertz I., O'Rourke K., Ultsch M., Seshagiri S., Eby M., Xiao W., Dixit V.M. Bcl10 activates the NF-kappaB pathway through ubiquitination of NEMO. Nature 2004, 427:167-171.