Characterization of WZ4003 and HTH-01-015 as selective inhibitors of the LKB1-tumour-suppressor-activated NUAK kinases

Biochemical Journal

Volumn 457, Issue 1, 2014, Pages 215-225

  Banerjee, Sourav ^a   Buhrlage, Sara J ^b,c   Huang, Hai Tsang ^b,c   Deng, Xianming ^b,c   Zhou, Wenjun ^b,c   Wang, Jinhua ^b,c   Traynor, Ryan ^b,c   Prescott, Alan R ^a   Alessi, Dario R ^a   Gray, Nathanael S ^b,c  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

AMP activated protein kinase (AMPK); AMPK related kinase 5 (ARK5); Kinase inhibitor; Kinase profiling; Liver kinase B1 (LKB1); Myosin phosphate targeting subunit 1(MYPT1); Sucrose non fermenting protein kinase AMPKrelated protein kinase (SNARK)

Indexed keywords

HTH 01 015; MYPT1 PROTEIN; PROTEIN; PROTEIN KINASE INHIBITOR; PROTEIN KINASE LKB1; SERINE; UNCLASSIFIED DRUG; WZ 4003;

ANIMAL CELL; ARTICLE; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DRUG SELECTIVITY; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; GENE MUTATION; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IC 50; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; WILD TYPE;

ANILIDES; ANIMALS; BENZODIAZEPINONES; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; DRUG EVALUATION, PRECLINICAL; ENZYME ACTIVATION; HEK293 CELLS; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; HUMANS; MICE; NEOPLASMS; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; PYRIMIDINES; REPRESSOR PROTEINS; SUBSTRATE SPECIFICITY; TUMOR SUPPRESSOR PROTEINS;

EID: 84890070290     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20131152     Document Type: Article

References (36)

1. Lizcano, J. M., Goransson, O., Toth, R., Deak, M., Morrice, N. A., Boudeau, J., Hawley, S. A., Udd, L., Makela, T. P., Hardie, D. G. and Alessi, D. R. (2004) LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J. 23, 833-843
2. Alessi, D. R., Sakamoto, K. and Bayascas, J. R. (2006) LKB1-dependent signaling pathways. Annu. Rev. Biochem. 75, 137-163
3. Jaleel, M., McBride, A., Lizcano, J. M., Deak, M., Toth, R., Morrice, N. A. and Alessi, D. R. (2005) Identification of the sucrose non-fermenting related kinase SNRK, as a novel LKB1 substrate. FEBS Lett. 579, 1417-1423
4. Hardie, D. G., Ross, F. A. and Hawley, S. A. (2012) AMPK: A nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell Biol. 13, 251-262
5. Matenia, D. and Mandelkow, E. M. (2009) The tau of MARK: A polarized view of the cytoskeleton. Trends Biochem. Sci. 34, 332-342
6. Kishi, M., Pan, Y. A., Crump, J. G. and Sanes, J. R. (2005) Mammalian SAD kinases are required for neuronal polarization. Science 307, 929-932
7. Screaton, R. A., Conkright, M. D., Katoh, Y., Best, J. L., Canettieri, G., Jeffries, S., Guzman, E., Niessen, S., Yates, III., J. R., Takemori, H. et al. (2004) The CREB coactivator TORC2 functions as a calcium- and cAMP-sensitive coincidence detector. Cell 119, 61-74
8. Clark, K., MacKenzie, K. F., Petkevicius, K., Kristariyanto, Y., Zhang, J., Choi, H. G., Peggie, M., Plater, L., Pedrioli, P. G., McIver, E. et al. (2012) Phosphorylation of CRTC3 by the salt-inducible kinases controls the interconversion of classically activated and regulatory macrophages. Proc. Natl. Acad. Sci. U.S.A. 109, 16986-16991
9. Vallenius, T., Vaahtomeri, K., Kovac, B., Osiceanu, A. M., Viljanen, M. and Makela, T. P. (2011) An association between NUAK2 and MRIP reveals a novel mechanism for regulation of actin stress fibers. J. Cell Sci. 124, 384-393
10. Zagorska, A., Deak, M., Campbell, D. G., Banerjee, S., Hirano, M., Aizawa, S., Prescott, A. R. and Alessi, D. R. (2010) New roles for the LKB1-NUAK pathway in controlling myosin phosphatase complexes and cell adhesion. Sci. Signaling 3, ra25
11. Bell, R. E., Khaled, M., Netanely, D., Schubert, S., Golan, T., Buxbaum, A., Janas, M. M., Postolsky, B., Goldberg, M. S., Shamir, R. and Levy, C. (2013) Transcription factor/microRNA axis blocks melanoma invasion program by miR-211 targeting NUAK1. J. Invest. Dermatol., doi:10.1038/jid.2013.340
12. Kusakai, G., Suzuki, A., Ogura, T., Kaminishi, M. and Esumi, H. (2004) Strong association of ARK5 with tumor invasion and metastasis. J. Exp. Clin. Cancer Res. 23, 263-268
13. Lu, S., Niu, N., Guo, H., Tang, J., Guo, W., Liu, Z., Shi, L., Sun, T., Zhou, F., Li, H. et al. (2013) ARK5 promotes glioma cell invasion, and its elevated expression is correlated with poor clinical outcome. Eur. J. Cancer 49, 752-763
14. Hirano, M., Kiyonari, H., Inoue, A., Furushima, K., Murata, T., Suda, Y. and Aizawa, S. (2006) A new serine/threonine protein kinase, Omphk1, essential to ventral body wall formation. Dev. Dyn. 235, 2229-2237
15. Ohmura, T., Shioi, G., Hirano, M. and Aizawa, S. (2012) Neural tube defects by NUAK1 and NUAK2 double mutation. Dev. Dyn. 241, 1350-1364
16. Humbert, N., Navaratnam, N., Augert, A., Da Costa, M., Martien, S., Wang, J., Martinez, D., Abbadie, C., Carling, D., de Launoit, Y. et al. (2010) Regulation of ploidy and senescence by the AMPK-related kinase NUAK1. EMBO J. 29, 376-386
17. Hou, X., Liu, J. E., Liu, W., Liu, C. Y., Liu, Z. Y. and Sun, Z. Y. (2011) A new role of NUAK1: directly phosphorylating p53 and regulating cell proliferation. Oncogene 30, 2933-2942
18. Courchet, J., Lewis, Jr, T. L., Lee, S., Courchet, V., Liou, D. Y., Aizawa, S. and Polleux, F. (2013) Terminal axon branching is regulated by the LKB1-NUAK1 kinase pathway via presynaptic mitochondrial capture. Cell 153, 1510-1525
19. Liu, L., Ulbrich, J., Muller, J., Wustefeld, T., Aeberhard, L., Kress, T. R., Muthalagu, N., Rycak, L., Rudalska, R., Moll, R. et al. (2012) Deregulated MYC expression induces dependence upon AMPK-related kinase 5. Nature 483, 608-612
20. Yu, P. B., Hong, C. C., Sachidanandan, C., Babitt, J. L., Deng, D. Y., Hoyng, S. A., Lin, H. Y., Bloch, K. D. and Peterson, R. T. (2008) Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat. Chem. Biol. 4, 33-41
21. Clark, K., Plater, L., Peggie, M. and Cohen, P. (2009) Use of the pharmacological inhibitor BX795 to study the regulation and physiological roles of TBK1 and IκB kinase ε: A distinct upstream kinase mediates Ser-172 phosphorylation and activation. J. Biol. Chem. 284, 14136-14146
22. Clark, K., Peggie, M., Plater, L., Sorcek, R. J., Young, E. R., Madwed, J. B., Hough, J., McIver, E. G. and Cohen, P. (2011) Novel cross-talk within the IKK family controls innate immunity. Biochem. J. 434, 93-104
23. MacKenzie, K. F., Clark, K., Naqvi, S., McGuire, V. A., Noehren, G., Kristariyanto, Y., van den Bosch, M., Mudaliar, M., McCarthy, P. C., Pattison, M. J. et al. (2013) PGE2 induces macrophage IL-10 production and a regulatory-like phenotype via a protein kinase A-SIK-CRTC3 pathway. J. Immunol. 190, 565-577
24. Durocher, Y., Perret, S. and Kamen, A. (2002) High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucleic Acids Res. 30, E9
25. Sommer, E. M., Dry, H., Cross, D., Guichard, S., Davies, B. R. and Alessi, D. R. (2013) Elevated SGK1 predicts resistance of breast cancer cells to Akt inhibitors. Biochem. J. 452, 499-508
26. Bain, J., Plater, L., Elliott, M., Shpiro, N., Hastie, C. J., McLauchlan, H., Klevernic, I., Arthur, J. S., Alessi, D. R. and Cohen, P. (2007) The selectivity of protein kinase inhibitors: A further update. Biochem. J. 408, 297-315
27. Najafov, A., Sommer, E. M., Axten, J. M., Deyoung, M. P. and Alessi, D. R. (2011) Characterization of GSK2334470, a novel and highly specific inhibitor of PDK1. Biochem. J. 433, 357-369
28. 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. (2005) Novel small molecule inhibitors of 3-phosphoinositide-dependent kinase-1. J. Biol. Chem. 280, 19867-19874
29. McIver, E. G., Bryans, J., Birchall, K., Chugh, J., Drake, T., Lewis, S. J., Osborne, J., Smiljanic-Hurley, E., Tsang, W., Kamal, A. et al. (2012) Synthesis and structure-activity relationships of a novel series of pyrimidines as potent inhibitors of TBK1/IKKepsilon kinases. Bioorg. Med. Chem. Lett. 22, 7169-7173
30. Zhou, W., Ercan, D., Chen, L., Yun, C. H., Li, D., Capelletti, M., Cortot, A. B., Chirieac, L., Iacob, R. E., Padera, R. et al. (2009) Novel mutant-selective EGFR kinase inhibitors against EGFR T790M. Nature 462, 1070-1074
31. Deng, X., Dzamko, N., Prescott, A., Davies, P., Liu, Q., Yang, Q., Lee, J. D., Patricelli, M. P., Nomanbhoy, T. K., Alessi, D. R. and Gray, N. S. (2011) Characterization of a selective inhibitor of the Parkinson's disease kinase LRRK2. Nat. Chem. Biol. 7, 203-205
32. Miduturu, C. V., Deng, X., Kwiatkowski, N., Yang, W., Brault, L., Filippakopoulos, P., Chung, E., Yang, Q., Schwaller, J., Knapp, S. et al. (2011) High-throughput kinase profiling: A more efficient approach toward the discovery of new kinase inhibitors. Chem. Biol. 18, 868-879
33. Bonn, S., Herrero, S., Breitenlechner, C. B., Erlbruch, A., Lehmann, W., Engh, R. A., Gassel, M. and Bossemeyer, D. (2006) Structural analysis of protein kinase A mutants with Rho-kinase inhibitor specificity. J. Biol. Chem. 281, 24818-24830
34. Nichols, R. J., Dzamko, N., Hutti, J. E., Cantley, L. C., Deak, M., Moran, J., amborough, P., Reith, A. D. and Alessi, D. R. (2009) Substrate specificity and inhibitors of LRRK2, a protein kinase mutated in Parkinson's disease. Biochem. J. 424, 47-60
35. Ha, J., Daniel, S., Broyles, S. S. and Kim, K. H. (1994) Critical phosphorylation sites for acetyl-CoA carboxylase activity. J. Biol. Chem. 269, 22162-22168
36. Albini, A. (1998) Tumor and endothelial cell invasion of basement membranes. The matrigel chemoinvasion assay as a tool for dissecting molecular mechanisms. Pathol. Oncol. Res. 4, 230-241