Tank binding kinase 1 is a centrosome-associated kinase necessary for microtubule dynamics and mitosis

Nature Communications

Volumn 6, Issue , 2015, Pages

  Pillai, Smitha ^a   Nguyen, Jonathan ^a   Johnson, Joseph ^a   Haura, Eric ^a   Coppola, Domenico ^a   Chellappan, Srikumar ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; PHOSPHOTRANSFERASE; TANK BINDING KINASE 1; UNCLASSIFIED DRUG; PROTEIN BINDING; PROTEIN SERINE THREONINE KINASE; TBK1 PROTEIN, HUMAN;

CHEMICAL BINDING; EXPERIMENTAL STUDY; MAMMAL; MEMBRANE;

ARTICLE; CENTROSOME; ENZYME ACTIVITY; ENZYME BINDING; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; MAMMAL CELL; MICROTUBULE; MITOSIS; MITOSIS SPINDLE; PROTEIN BINDING; CELL LINE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

MAMMALIA;

CELL LINE; CENTROSOME; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MICROTUBULES; MITOSIS; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES;

EID: 84949673157     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10072     Document Type: Article

References (59)

1. Chau, T. L. et al. Are the IKKs and IKK-related kinases TBK1 and IKK-epsilon similarly activated? Trends Biochem. Sci. 33, 171-180 (2008).
2. Clement, J. F., Meloche, S. & Servant, M. J. The IKK-related kinases: from innate immunity to oncogenesis. Cell Res. 18, 889-899 (2008).
3. Kawai, T. & Akira, S. Signaling to NF-kappaB by Toll-like receptors. Trends Mol. Med. 13, 460-469 (2007).
4. Tojima, Y. et al. NAK is an IkappaB kinase-activating kinase. Nature 404, 778-782 (2000).
5. Fitzgerald, K. A. et al. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4, 491-496 (2003).
6. Hemmi, H. et al. The roles of two IkappaB kinase-related kinases in lipopolysaccharide and double stranded RNA signaling and viral infection. J. Exp. Med. 199, 1641-1650 (2004).
7. Ou, Y. H. et al. TBK1 directly engages Akt/PKB survival signaling to support oncogenic transformation. Mol. Cell 41, 458-470 (2011).
8. Chien, Y. et al. RalB GTPase-mediated activation of the IkappaB family kinase TBK1 couples innate immune signaling to tumor cell survival. Cell 127, 157-170 (2006).
9. Balakireva, M. et al. The Ral/exocyst effector complex counters c-Jun N-terminal kinase-dependent apoptosis in Drosophila melanogaster. Mol. Cell Biol. 26, 8953-8963 (2006).
10. Barbie, D. A. et al. Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1. Nature 462, 108-112 (2009).
11. Shen, R. R. & Hahn, W. C. Emerging roles for the non-canonical IKKs in cancer. Oncogene 30, 631-641 (2011).
12. Kim, J. K. et al. TBK1 regulates prostate cancer dormancy through mTOR inhibition. Neoplasia 15, 1064-1074 (2013).
13. Kim, J. Y. et al. Dissection of TBK1 signaling via phosphoproteomics in lung cancer cells. Proc. Natl Acad. Sci. USA 110, 12414-12419 (2013).
14. Guarguaglini, G. et al. The forkhead-associated domain protein Cep170 interacts with Polo-like kinase 1 and serves as a marker for mature centrioles. Mol. Biol. Cell 16, 1095-1107 (2005).
15. Radulescu, A. E. & Cleveland, D. W. NuMA after 30 years: the matrix revisited. Trends Cell Biol. 20, 214-222 (2010).
16. Reber, S. Isolation of centrosomes from cultured cells. Methods Mol. Biol. 777, 107-116 (2011).
17. Hsu, L. C. & White, R. L. BRCA1 is associated with the centrosome during mitosis. Proc. Natl Acad. Sci. USA 95, 12983-12988 (1998).
18. Nigg, E. A. & Stearns, T. The centrosome cycle: centriole biogenesis, duplication and inherent asymmetries. Nat. Cell Biol. 13, 1154-1160 (2011).
19. Nigg, E. A. Origins and consequences of centrosome aberrations in human cancers. Int. J. Cancer 119, 2717-2723 (2006).
20. Welburn, J. P. & Cheeseman, I. M. The microtubule-binding protein Cep170 promotes the targeting of the kinesin-13 depolymerase Kif2b to the mitotic spindle. Mol. Biol. Cell 23, 4786-4795 (2012).
21. Jarvius, M. et al. In situ detection of phosphorylated platelet-derived growth factor receptor beta using a generalized proximity ligation method. Mol. Cell. Proteom. 6, 1500-1509 (2007).
22. Soderberg, O. et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995-1000 (2006).
23. Asthana, J., Kapoor, S., Mohan, R. & Panda, D. Inhibition of HDAC6 deacetylase activity increases its binding with microtubules and suppresses microtubule dynamic instability in MCF-7 cells. J. Biol. Chem. 288, 22516-22526 (2013).
24. Goold, R. G., Owen, R. & Gordon-Weeks, P. R. Glycogen synthase kinase 3beta phosphorylation of microtubule-associated protein 1B regulates the stability of microtubules in growth cones. J. Cell Sci. 112(Pt 19): 3373-3384 (1999).
25. Hung, L. Y., Chen, H. L., Chang, C. W., Li, B. R. & Tang, T. K. Identification of a novel microtubule-destabilizing motif in CPAP that binds to tubulin heterodimers and inhibits microtubule assembly. Mol. Biol. Cell 15, 2697-2706 (2004).
26. Mian, I. et al. LKB1 destabilizes microtubules in myoblasts and contributes to myoblast differentiation. PLoS ONE 7, e31583 (2012).
27. Welburn, J. P. The molecular basis for kinesin functional specificity during mitosis. Cytoskeleton 70, 476-493 (2013).
28. Koonce, M. P. et al. Dynein motor regulation stabilizes interphase microtubule arrays and determines centrosome position. EMBO J. 18, 6786-6792 (1999).
29. Hendricks, A. G. et al. Dynein tethers and stabilizes dynamic microtubule plus ends. Curr. Biol. 22, 632-637 (2012).
30. Manning, A. L. et al. The kinesin-13 proteins Kif2a, Kif2b, and Kif2c/MCAK have distinct roles during mitosis in human cells. Mol. Biol. Cell 18, 2970-2979 (2007).
31. Wei, C., Bhattaram, V. K., Igwe, J. C., Fleming, E. & Tirnauer, J. S. The LKB1 tumor suppressor controls spindle orientation and localization of activated AMPK in mitotic epithelial cells. PLoS ONE 7, e41118 (2012).
32. Derossi, D. et al. Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent. J. Biol. Chem. 271, 18188-18193 (1996).
33. Dasgupta, P. et al. Disruption of the Rb-Raf-1 interaction inhibits tumor growth and angiogenesis. Mol. Cell Biol. 24, 9527-9541 (2004).
34. Foley, E. A. & Kapoor, T. M. Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nat. Rev. Mol. Cell. Biol. 14, 25-37 (2013).
35. Storchova, Z. et al. Genome-wide genetic analysis of polyploidy in yeast. Nature 443, 541-547 (2006).
36. Torres, E. M., Williams, B. R. & Amon, A. Aneuploidy: cells losing their balance. Genetics 179, 737-746 (2008).
37. Storchova, Z. & Pellman, D. From polyploidy to aneuploidy, genome instability and cancer. Nat. Rev. Mol. Cell. Biol. 5, 45-54 (2004).
38. Storchova, Z. & Kuffer, C. The consequences of tetraploidy and aneuploidy. J. Cell. Sci. 121, 3859-3866 (2008).
39. Alexander, J. et al. Spatial exclusivity combined with positive and negative selection of phosphorylation motifs is the basis for context-dependent mitotic signaling. Sci. Signal. 4, ra42 (2011).
40. Johnson, L. N. Substrates of mitotic kinases. Sci. Signal. 4, pe31 (2011).
41. Nigg, E. A. Mitotic kinases as regulators of cell division and its checkpoints. Nat. Rev. Mol. Cell Biol. 2, 21-32 (2001).
42. Merdes, A., Heald, R., Samejima, K., Earnshaw, W. C. & Cleveland, D. W. Formation of spindle poles by dynein/dynactin-dependent transport of NuMA. J. Cell Biol. 149, 851-862 (2000).
43. Basith, S., Manavalan, B., Yoo, T. H., Kim, S. G. & Choi, S. Roles of toll-like receptors in cancer: a double-edged sword for defense and offense. Arch. Pharm. Res. 35, 1297-1316 (2012).
44. Clark, K. et al. Novel cross-talk within the IKK family controls innate immunity. Biochem. J. 434, 93-104 (2011).
45. Lei, C. Q. et al. Glycogen synthase kinase 3beta regulates IRF3 transcription factor-mediated antiviral response via activation of the kinase TBK1. Immunity 33, 878-889 (2010).
46. Hirota, T. et al. Aurora-A and an interacting activator, the LIM protein Ajuba, are required for mitotic commitment in human cells. Cell 114, 585-598 (2003).
47. Luo, J. et al. A genome-wide RNAi screen identifies multiple synthetic lethal interactions with the Ras oncogene. Cell 137, 835-848 (2009).
48. Kawai, T. & Akira, S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34, 637-650 (2011).
49. Gonzalez-Reyes, S. et al. Study of TLR3, TLR4, and TLR9 in prostate carcinomas and their association with biochemical recurrence. Cancer Immunol. Immunother. 60, 217-226 (2011).
50. Greulich, H. et al. Oncogenic transformation by inhibitor-sensitive and -resistant EGFR mutants. PLoS Med. 2, e313 (2005).
51. Pedrali-Noy, G. et al. Synchronization of HeLa cell cultures by inhibition of DNA polymerase alpha with aphidicolin. Nucleic Acids Res. 8, 377-387 (1980).
52. Bostock, C. J., Prescott, D. M. & Kirkpatrick, J. B. An evaluation of the double thymidine block for synchronizing mammalian cells at the G1-S border. Exp. Cell Res. 68, 163-168 (1971).
53. Matsumura, S. & Toyoshima, F. ABL1 joins the cadre of spindle orientation machinery. Cell Struct. Funct. 37, 81-87 (2012).
54. Wang, S., Ghosh, R. N. & Chellappan, S. P. Raf-1 physically interacts with Rb and regulates its function: a link between mitogenic signaling and cell cycle regulation. Mol. Cell Biol. 18, 7487-7498 (1998).
55. Juan, G. & Darzynkiewicz, Z. Detection of mitotic cells. Curr. Protoc. Cytom. Chapter 7, Unit 7 24 (2004).
56. Dasgupta, P. et al. Nicotine induces cell proliferation, invasion and epithelial mesenchymal transition in a variety of human cancer cell lines. Int. J. Cancer 124, 36-45 (2009).
57. Dasgupta, P. et al. Nicotine induces cell proliferation by beta-arrestinmediated activation of Src and Rb-Raf-1 pathways. J. Clin. Invest. 116, 2208-2217 (2006).
58. Yates, 3rd J. R., Eng, J. K., McCormack, A. L. & Schieltz, D. Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal. Chem. 67, 1426-1436 (1995).
59. Perkins, D. N., Pappin, D. J., Creasy, D. M. & Cottrell, J. S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567 (1999).