Mutants of protein kinase A that mimic the ATP-binding site of Aurora kinase

Biochemical Journal

Volumn 440, Issue 1, 2011, Pages 85-93

  Pflug, Alexander ^a   De Oliveira, Taiańa Maia ^a   Bossemeyer, Dirk ^b   Engh, Richard A ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Aurora kinase; Chimaera; JNJ 7706621; Protein kinase A (PKA); VX 680

Indexed keywords

AMINO ACID; AURORA KINASE INHIBITOR; CHIMERIC PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIN DEPENDENT KINASE INHIBITOR; MUTANT PROTEIN; TOZASERTIB;

ALPHA CHAIN; ARTICLE; BINDING AFFINITY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; HUMAN; PRIORITY JOURNAL; X RAY ANALYSIS;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLIN-DEPENDENT KINASES; ENZYME INHIBITORS; HUMANS; KINETICS; MOLECULAR SEQUENCE DATA; PIPERAZINES; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; TRIAZOLES;

EID: 80054943801     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20110592     Document Type: Article

References (44)

1. Lapenna, S. and Giordano, A. (2009) Cell cycle kinases as therapeutic targets for cancer. Nat. Rev. Drug Discovery 8, 547-566
2. Torkamani, A., Verkhivker, G. and Schork, N. J. (2009) Cancer driver mutations in protein kinase genes. Cancer Lett. 281, 117-127
3. Karaman, M. W., Herrgard, S., Treiber, D. K., Gallant, P., Atteridge, C. E., Campbell, B. T., Chan, K. W., Ciceri, P., Davis, M. I., Edeen, P. T. et al. (2008) A quantitative analysis of kinase inhibitor selectivity. Nat. Biotechnol. 26, 127-132
4. Pollard, J. R. and Mortimore, M. (2009) Discovery and development of Aurora kinase inhibitors as anticancer agents. J. Med. Chem. 52, 2629-2651
5. Sasai, K., Katayama, H., Stenoien, D. L., Fujii, S., Honda, R., Kimura, M., Okano, Y., Tatsuka, M., Suzuki, F., Nigg, E. A. et al. (2004) Aurora-C kinase is a novel chromosomal passenger protein that can complement Aurora-B kinase function in mitotic cells. Cell Motil. Cytoskeleton 59, 249-263 (Pubitemid 40012993)
6. Bolanos-Garcia, V. M. (2005) Aurora kinases. Int. J. Biochem. Cell Biol. 37, 1572-1577
7. Gassel, M., Breitenlechner, C. B., Rüger, P., Jucknischke, U., Schneider, T., Huber, R., Bossemeyer, D. and Engh, R. A. (2003) Mutants of protein kinase A that mimic the ATP-binding site of protein kinase B (AKT). J. Mol. Biol. 329, 1021-1034 (Pubitemid 36683158)
8. 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 (Pubitemid 44274255)
9. Davies, T. G., Verdonk, M. L., Graham, B., Saalau-Bethell, S., Hamlett, C. C., McHardy, T., Collins, I., Garrett, M. D., Workman, P., Woodhead, S. J. et al. (2007) A structural comparison of inhibitor binding to PKB, PKA and PKA-PKB chimera. J. Mol. Biol. 367, 882-894 (Pubitemid 46335912)
10. Caldwell, J. J., Davies, T. G., Donald, A., McHardy, T., Rowlands, M. G., Aherne, G. W., Hunter, L. K., Taylor, K., Ruddle, R., Raynaud, F. I. et al. (2008) Identification of 4-(4-aminopiperidin-1-yl)-7H-pyrrolo[2,3-d]pyrimidines as selective inhibitors of protein kinase B through fragment elaboration. J. Med. Chem. 51, 2147-2157 (Pubitemid 351503270)
11. Davies, T. G., Woodhead, S. J. and Collins, I. (2009) Fragment-based discovery of inhibitors of protein kinase B. Curr. Top. Med. Chem. 13, 1705-1717
12. Braman, J., Papworth, C. and Greener, A. (2000) Site-directed mutagenesis using double-stranded plasmid DNA templates. In The Nucleic Acid Protocols Handbook (Rapley, R., ed.), pp. 835-844, Humana Press, New York
13. Studier, F. W. (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41, 207-234
14. Engh, R. A., Girod, A., Kinzel, V., Huber, R. and Bossemeyer, D. (1996) Crystal structures of catalytic subunit of cAMP-dependent protein kinase in complex with isoquinolinesulfonyl protein kinase inhibitors H7, H8, and H89. Structural implications for selectivity. J. Biol. Chem. 271, 26157-26164 (Pubitemid 26347460)
15. Leslie, A. G. W. (1992) Recent changes to the MOSFLM package for processing film and image plate data. CCP4 ESF-EAMCB Newslett. Protein Crystallogr. 26, 27-33
16. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. Sect. D Biol. Crystallogr. 50 760-763
17. Schüttelkopf, A. W. and van Aalten, D. M. F. (2004) PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr. Sect. D Biol. Crystallogr. 60, 1355-1363 (Pubitemid 41079731)
18. Cook, P. F., Neville, M. E., Vrana, K. E., Hartl, F. T. and Roskoski, R. (1982) Adenosine cyclic 3′,5′-monophosphate dependent protein kinase: kinetic mechanism for the bovine skeletal muscle catalytic subunit. Biochemistry 21, 5794-5799
19. Zhang, Q., Liu, Y., Gao, F., Ding, Q., Cho, C., Hur, W., Jin, Y., Uno, T., Joazeiro, C. A. P. and Gray, N. (2006) Discovery of EGFR selective 4,6-disubstituted pyrimidines from a combinatorial kinase-directed heterocycle library. J. Am. Chem. Soc. 128, 2182-2183
20. Emanuel, S., Rugg, C. A., Gruninger, R. H., Lin, R., Fuentes-Pesquera, A., Connolly, P. J., Wetter, S. K., Hollister, B., Kruger, W. W., Napier, C. et al. (2005) The in vitro and in vivo effects of JNJ-7706621: a dual inhibitor of cyclin-dependent kinases and Aurora kinases. Cancer Res. 65, 9038-9046 (Pubitemid 41377396)
21. Harrington, E. A., Bebbington, D., Moore, J., Rasmussen, R. K., Ajose-Adeogun, A. O., Nakayama, T., Graham, J. A., Demur, C., Hercend, T., Diu-Hercend, A. et al. (2004) VX-680, a potent and selective small-molecule inhibitor of the Aurora kinases, suppresses tumor growth in vivo. Nat. Med. 10, 262-267 (Pubitemid 38667616)
22. Kornev, A. P., Taylor, S. S. and Ten Eyck, L. F. (2008) A helix scaffold for the assembly of active protein kinases. Proc. Natl. Acad. Sci. U.S.A. 105, 14377-14382
23. Yonemoto, W., McGlone, M. L., Grant, B. and Taylor, S. S. (1997) Autophosphorylation of the catalytic subunit of cAMP-dependent protein kinase in Escherichia coli. Protein Eng. 10, 915-925 (Pubitemid 27491648)
24. Davies, S. P., Reddy, H., Caivano, M. and Cohen, P. (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351, 95-105
25. Breitenlechner, C., Engh, R. A., Huber, R., Kinzel, V., Bossemeyer, D. and Gassel, M. (2004) The typically disordered N-terminus of PKA can fold as a helix and project the myristoylation site into solution. Biochemistry 43, 7743-7749 (Pubitemid 38787682)
26. Wu, J., Yang, J., Kannan, N., Madhusudan, Xuong, N., Ten Eyck, L. F. and Taylor, S. S. (2005) Crystal structure of the E230Q mutant of cAMP-dependent protein kinase reveals an unexpected apoenzyme conformation and an extended N-terminal A helix. Protein Sci. 14, 2871-2879 (Pubitemid 41577266)
27. Yang, J., Ten Eyck, L. F., Xuong, N. and Taylor, S. S. (2004) Crystal structure of a cAMP-dependent protein kinase mutant at 1.26 Å: new insights into the catalytic mechanism. J. Mol. Biol. 336, 473-487 (Pubitemid 38147641)
28. Seifert, M. H. J., Breitenlechner, C. B., Bossemeyer, D., Huber, R., Holak, T. A. and Engh, R. A. (2002) Phosphorylation and flexibility of cyclic-AMP-dependent protein kinase (PKA) using 31P NMR spectroscopy. Biochemistry 41, 5968-77 (Pubitemid 34498902)
29. Bossemeyer, D., Engh, R. A., Kinzel, V., Ponstingl, H. and Huber, R. (1993) Phosphotransferase and substrate binding mechanism of the cAMP-dependent protein kinase catalytic subunit from porcine heart as deduced from the 2.0 Å structure of the complex with Mn2+ adenylyl imidodiphosphate and inhibitor peptide PKI(5-24). EMBO J. 12, 849-859 (Pubitemid 23095833)
30. Pepperkok, R., Hotz-Wagenblatt, A., König, N., Girod, A., Bossemeyer, D. and Kinzel, V. (2000) Intracellular distribution of mammalian protein kinase A catalytic subunit altered by conserved Asn2 deamidation. J. Cell. Biol. 148, 715-726
31. Rubin, E. H., Shapiro, G. I., Stein, M. N., Watson, P., Bergstrom, D., Xiao, A., Clark, J. B., Freedman, S. J. and Eder, J. P. (2006) A phase I clinical and pharmacokinetic (PK) trial of the aurora kinase (AK) inhibitor MK-0457 in cancer patients. J. Clin. Oncol. 24, 3009
32. Lin, Z., Hsu, H., Hsu, C., Yeh, P., Huang, C. F., Huang, Y., Chen, T., Kuo, S., Hsu, C., Hu, F. et al. (2009) The Aurora kinase inhibitor VE-465 has anticancer effects in pre-clinical studies of human hepatocellular carcinoma. J. Hepatol. 50, 518-527
33. Young, M. A., Shah, N. P., Chao, L. H., Seeliger, M., Milanov, Z. V., Biggs, W. H., Treiber, D. K., Patel, H. K., Zarrinkar, P. P., Lockhart, D. J. et al. (2006) Structure of the kinase domain of an imatinib-resistant Abl mutant in complex with the Aurora kinase inhibitor VX-680. Cancer Res. 66, 1007-1014 (Pubitemid 43168337)
34. Cheetham, G., Charlton, P., Golec, J. and Pollard, J. (2007) Structural basis for potent inhibition of the Aurora kinases and a T315I multi-drug resistant mutant form of Abl kinase by VX-680. Cancer Lett. 251, 323-329 (Pubitemid 46669805)
35. Zhao, B., Smallwood, A., Yang, J., Koretke, K., Nurse, K., Calamari, A., Kirkpatrick, R. B. and Lai, Z. (2008) Modulation of kinase-inhibitor interactions by auxiliary protein binding: crystallography studies on Aurora A interactions with VX-680 and with TPX2. Protein Sci. 17, 1791-1797
36. Oliveira, T., Ahmad, R. and Engh, R. (2011) VX680 binding in Aurora A: π-π interactions involving the conserved aromatic amino acid of the flexible glycine-rich loop. J. Phys. Chem. A 115, 3895-3904
37. Sobolev, V., Sorokine, A., Prilusky, J., Abola, E. E. and Edelman, M. (1999) Automated analysis of interatomic contacts in proteins. Bioinformatics 15, 327-332 (Pubitemid 29213759)
38. Malumbres, M., Pevarello, P., Barbacid, M. and Bischoff, J. R. (2008) CDK inhibitors in cancer therapy: what is next? Trends Pharmacol. Sci. 29, 16-21
39. Lochner, A. and Moolman, J. A. (2006) The many faces of H89: a review. Cardiovasc. Drug Rev. 24, 261-274 (Pubitemid 46435008)
40. Tari, L. W., Hoffman, I. D., Bensen, D. C., Hunter, M. J., Nix, J., Nelson, K. J., McRee, D. E. and Swanson, R. V. (2007) Structural basis for the inhibition of Aurora A kinase by a novel class of high affinity disubstituted pyrimidine inhibitors. Bioorg. Med. Chem. Lett. 17, 688-691 (Pubitemid 46127641)
41. Prime, M., Courtney, S., Brookfield, F., Marston, R., Walker, V., Warne, J., Boyd, A., Kairies, N., von der Saal, W., Limberg, A. et al. (2010) Phthalazinone pyrazoles as potent, selective, and orally bioavailable inhibitors of Aurora-A kinase. J. Med. Chem., doi: 10.1021/jm101346r
42. Cohen, M. S., Zhang, C., Shokat, K. M. and Taunton, J. (2005) Structural bioinformatics-based design of selective, irreversible kinase inhibitors. Science 308, 1318-1321 (Pubitemid 40746129)
43. Smith, C., Radzio-Andzelm, E., Madhusudan, Akamine, P. and Taylor, S. (1999) The catalytic subunit of cAMP-dependent protein kinase: prototype for an extended network of communication. Prog. Biophys. Mol. Biol. 71, 313-341 (Pubitemid 29156305)
44. Thompson, E. E., Kornev, A. P., Kannan, N., Kim, C., Ten Eyck, L. F. and Taylor, S. S. (2009) Comparative surface geometry of the protein kinase family. Protein Sci. 18, 2016-2026