Structural analysis of ARC-type inhibitor (ARC-1034) binding to protein kinase A catalytic subunit and rational design of bisubstrate analogue inhibitors of basophilic protein kinases

Journal of Medicinal Chemistry

Volumn 52, Issue 2, 2009, Pages 308-321

  Lavogina, Darja ^a   Lust, Marje ^a   Viil, Indrek ^a   König, Norbert ^b   Raidaru, Gerda ^a   Rogozina, Jevgenia ^a   Enkvist, Erki ^a   Uri, Asko ^a   Bossemeyer, Dirk ^b  

^a Institute of Chemistry   (Estonia)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE 4' DEHYDROXYMETHYL 4' CARBOXYLIC ACID DERIVATIVE; ADENOSINE DERIVATIVE; ARC 1034; ARGININE DERIVATIVE; CYCLIC AMP DEPENDENT PROTEIN KINASE; ENZYME INHIBITOR; UNCLASSIFIED DRUG; ADENOSINE; DIPEPTIDE; DRUG DERIVATIVE; PROTEIN KINASE INHIBITOR;

ARTICLE; BASOPHIL; CRYSTAL STRUCTURE; DRUG BINDING SITE; DRUG DESIGN; DRUG POTENCY; DRUG PROTEIN BINDING; DRUG SELECTIVITY; DRUG STRUCTURE; ENZYME ACTIVE SITE; ENZYME ASSAY; ENZYME INHIBITION; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY; AMINO ACID SEQUENCE; ANIMAL; CATTLE; CHEMICAL STRUCTURE; CHEMISTRY; CRYSTALLOGRAPHY; ENZYMOLOGY; FLUORESCENCE POLARIZATION; METABOLISM; MOLECULAR GENETICS; SEQUENCE HOMOLOGY;

ADENOSINE; AMINO ACID SEQUENCE; ANIMALS; BASOPHILS; CATALYTIC DOMAIN; CATTLE; CRYSTALLOGRAPHY; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DIPEPTIDES; FLUORESCENCE POLARIZATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN KINASE INHIBITORS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 60549099993     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm800797n     Document Type: Article

References (54)

1. Manning, G.; Whyte, D. B.; Martinez, R.; Hunter, T.; Sudarsanam, S. The protein kinase complement of the human genome. Science 2002, 298, 1912-1934.
2. Breitenlechner, C.; Gassel, M.; Engh, R.; Bossenmeyer, D. Structural insights into AGC kinase inhibition. Oncol. Res. 2004, 14, 267-278.
3. Cohen, P. Protein kinases-the major drug targets of the twenty-first century. Nat. Rev. Drug Discovery 2002, 1, 309-315.
4. Noble, M. E.; Endicott, J. A.; Johnson, L. N. Protein kinase inhibitors: insights into drug design from structure. Science 2004, 303, 1800-1805.
5. Pelech, S. Tracking cell signaling protein expression and phosphory-lation by innovative proteomic solutions. Curr. Pharm. Biotechnol. 2004, 5, 69-77.
6. Gill, A. L.; Verdonk, M.; Boyle, R. G.; Taylor, R. A comparison of physicochemical property profiles of marketed oral drugs and orally bioavailable anti-cancer protein kinase inhibitors in clinical development. Curr. Toy. Med. Chem. 2007, 7, 1408-1422.
7. Enkvist, E.; Lavogina, D.; Raidaru, G.; Vaasa, A.; Viil, I.; Lust, M.; Viht, K.; Uri, A. Conjugation of adenosine and hexa-(D-arginine) leads to a nanomolar bisubstrate-analog inhibitor of basophilic protein kinases. J. Med. Chem. 2006, 49, 7150-7159.
8. Nam, N.-H.; Lee, S.; Ye, G.; Sun, G.; Parang, K. ATP-phosphopeptide conjugates as inhibitors of Src tyrosine kinases. Bioorg. Med. Chem. 2004, 12, 5753-5766.
9. Shen, K.; Cole, P. A. Conversion of a tyrosine kinase protein substrate to a high affinity ligand by ATP linkage. J. Am. Chem. Soc. 2003, 125, 16172-16173.
10. Fischer, P. M. The design of drug candidate molecules as selective inhibitors of therapeutically relevant protein kinases. Curr. Med. Chem. 2004, 11, 1563-1583.
11. Knight, Z. A.; Shokat, K. M. Features of selective kinase inhibitors. Chem. Biol. 2005, 12, 621-637.
12. Parang, K.; Cole, P. A. Designing bisubstrate analog inhibitors for protein kinases. Pharm. Ther. 2002, 93, 145-157.
13. Bogoyevitch, M. A.; Barr, R. K.; Ketterman, A. J. Peptide inhibitors of protein kinases-discovery, characterisation and use. Biochim. Biophys. Acta 2005, 1754, 79-99.
14. Lawrence, D. S. New design strategies for ligands that target protein kinase-mediated protein-protein interactions. In Handbook of Experimental pharmacology, Inhibitors of Protein Kinases and Protein Phosphatases; Pinna, A. L., Cohen, P. T. W., Eds.; Springer-Verlag: Berlin, 2005; Vol. 167, pp 11-44.
15. Lienhard, G. E.; Secemski, I.I. P1, P5-Di(adenosine-5′) pentaphosphate, a potent multisubstrate inhibitor of adenylate kinase. J. Biol. Chem. 1973, 248, 1121-1123.
16. Parang, K.; Till, J. H.; Ablooglu, A. J.; Kohanski, R. A.; Hubbard, S. R.; Cole, P. A. Mechanism-based design of a protein kinase inhibitor. Nat. Struct. Biol. 2001, 8, 37-41.
17. Jencks, W. P. On the attribution and additivity of binding energies. Proc. Natl. Acad. Sci. U.S.A. 1981, 78, 4046-4050.
18. Ricouart, A.; Gesquiere, J. C.; Tartar, A.; Sergheraert, C. Design of potent protein kinase inhibitors using the bisubstrate approach. J. Med. Chem. 1991, 34, 73-78.
19. Garber, K. The second wave in kinase cancer drugs. Nat. Biotechnol. 2006, 24, 127-130.
20. Enkvist, E.; Raidaru, G.; Vaasa, A.; Pehk, T.; Lavogina, D.; Uri, A. Carbocyclic 3'-deoxyadenosine-based highly potent bisubstrate-analog inhibitor of basophilic protein kinases. Bioorg. Med. Chem. Lett. 2007, 17, 5336-5339.
21. Viht, K.; Schweinsberg, S.; Lust, M.; Vaasa, A.; Raidaru, G.; Lavogina, D.; Uri, A.; Herberg, F. W. Surface-plasmon-resonance-based biosensor with immobilized bisubstrate analog inhibitor for the determination of affinities of ATP- and protein-competitive ligands of cAMP- dependent protein kinase. Anal. Biochem. 2007, 362, 268-277.
22. Taylor, S. S.; Yang, J.; Wu, J.; Haste, N. M.; Radzio-Andzelm, E.; Anand, G. PKA: a portrait of protein kinase dynamics. Biochim. Biophys. Acta 2004, 1697, 259-269.
23. Taylor, S. S.; Kim, C.; Vigil, D.; Haste, N. M.; Yang, J.; Wu, J.; Anand, G. S. Dynamics of signaling by PKA. Biochim. Biophys. Acta 2005, 1754, 25-37.
24. Bonn, S.; Herrero, S.; Breitenlechner, C. B.; Elbruch, A.; Lehmann, W.; Engh, R. A.; Gassel, M.; Bossemeyer, D. Structural analysis of protein kinase A mutants with Rho-kinase inhibitor specificity. J. Biol. Chem. 2006, 281, 24818-24830.
25. Gassel, M.; Breitenlechner, B. C.; Ruger, P.; Jucknischke, U.; Schneider, T.; Huber, R.; Bossemeyer, D.; Engh, R. A. Mutants of protein kinase A that mimic the ATP-binding site of protein kinase B (AKT). J. Mol. Biol. 2003, 329, 1021-1034.
26. Gassel, M.; Breitenlechner, C. B.; Konig, N.; Huber, R.; Engh, R. A.; Bossemeyer, D. The protein kinase C inhibitor bisindolyl maleimide 2 binds with reversed orientations to different conformations of protein kinase A. J. Biol. Chem. 2004, 279, 23679-23690.
27. Breitenlechner, C.; Gassel, M.; Hidaka, H.; Kinzel, V.; Huber, R.; Engh, R. A.; Bossenmeyer, D. Protein kinase A in complex with Rhokinase inhibitors Y-27632, Fasudil, and H-1152P: structural basis of selectivity. Structure 2003, 11, 1595-1607.
28. Prade, L.; Engh, R. A.; Girod, A.; Kinzel, V.; Huber, R.; Bossemeyer, D. Staurosporine-induced conformational changes of cAMP-dependent protein kinase catalytic subunit explain inhibitory potential. Structure 1997, 5, 1627-1637.
29. Engh, R. A.; Girod, A.; Kinzel, V.; Huber, R.; Bossemeyer, D. 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. 1996, 271, 26157-26164.
30. Akamine, P.; Madhusudan; Brunton, L. L.; Ou, H. D.; Canaves, J. M.; Xuong, N. H.; Taylor, S. S. Balanol analogues probe specificity determinants and the conformational malleability of the cyclic 3′,5′- adenosine monophosphate-dependent protein kinase catalytic subunit. Biochemistry 2004, 43, 85-96.
31. Breitenlechner, C. B.; Wegge, T.; Berillon, L.; Graul, K.; Marzenell, K.; Friebe, W. G.; Thomas, U.; Schumacher, R.; Huber, R.; Engh, R. A.; Masjost, B. Structure-based optimization of novel azepane derivatives as PKB inhibitors. J. Med. Chem. 2004, 47, 1375-1390.
32. Zhang, X.; Gureasko, J.; Shen, K.; Cole, P. A.; Kuriyan, J. An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell. 2006, 125, 1137-1149.
33. Levinson, N. M.; Kuchment, O.; Shen, K.; Young, M. A.; Koldobskiy, M.; Karplus, M.; Cole, P. A.; Kuriyan, J. A Src-like inactive conformation in the abl tyrosine kinase domain. PLoS Biol. 2006, 4, 753-767.
34. Cheng, K. Y.; Noble, M. E.; Skamnaki, V.; Brown, N. R.; Lowe, E. D.; Kontogiannis, L.; Shen, K.; Cole, P. A.; Siligardi, G.; Johnson, L. N. The role of the phospho-CDK2/cyclin A recruitment site in substrate recognition. J. Biol. Chem. 2006, 281, 23167-23179.
35. Viht, K.; Vaasa, A.; Raidaru, G.; Enkvist, E.; Uri, A. Fluorometric TLC assay for evaluation of protein kinase inhibitors. Anal. Biochem. 2005, 340, 165-170.
36. 2+ adenylyl imidodiphosphate and inhibitor peptide PKI(5-24). EMBO J. 1993, 12, 849-859.
37. Zheng, J.; Knighton, D. R.; ten Eyck, L. F.; Karlsson, R.; Xuong, N.; Taylor, S. S.; Sowadski, J. M. Crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with MgATP and peptide inhibitor. Biochemistry 1993, 32, 2154-2161.
38. Gibbs, C. S.; Zoller, M. J. Rational scanning mutagenesis of a protein kinase identifies functional regions involved in catalysis and substrate interactions. J. Biol. Chem. 1991, 266, 8923-8931.
39. Yang, J.; Ten Eyck, L. F.; Xuong, N. H.; Taylor, S. S. Crystal structure of a cAMP-dependent protein kinase mutant at 1.26A: new insights into the catalytic mechanism. J. Mol. Biol. 2004, 336, 473-487.
40. Vaasa, A.; Viil, I.; Enkvist, E.; Viht, K.; Raidaru, G.; Lavogina, D.; Uri, A. High-affinity bisubstrate probe for fluorescence anisotropy binding/displacement assays with protein kinases PKA and ROCK. Anal. Biochem. 2008, in press, doi:, 10.1016/j.ab.2008.10.030.
41. Knighton, D. R.; Zheng, J. H.; Ten Eyck, L. F.; Xuong, N. H.; Taylor, S. S.; Sowadski, J. M. Structure of a peptide inhibitor bound to the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 1991, 253, 414-420.
42. Schneider, T. L.; Mathew, R. S.; Rice, K. P.; Tamaki, K.; Wood, J. L.; Schepartz, A. Increasing the kinase specificity of k252a by protein surface recognition. Org. Lett. 2005, 7, 1695-1698.
43. Lee, J. H.; Kumar, S.; Lawrence, D. S. Stepwise combinatorial evolution of Akt bisubstrate inhibitors. ChemBioChem. 2008, 9, 507-509.
44. Miick, S. M.; Jalali, S.; Dwyer, B. P.; Havens, J.; Thomas, D.; Jimenez, M. A.; Simpson, M. T.; Zile, B.; Huss, K. L.; Campbell, R. M. Development of a microplate-based, electrophoretic fluorescent protein kinase A assay: comparison with filter-binding and fluorescence polarization assay formats. J. Biomol. Screening 2005, 10, 329-338.
45. Chijiwa, T.; Mishima, A.; Hagiwara, M.; Sano, M.; Hayashi, K.; Inoue, T.; Naito, K.; Toshioka, T.; Hidaka, H. Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(p- bromocinnamylamino)ethyl]-5- isoquinolinesulfonamide (H-89), of PC12D pheochromocytoma cells. J. Biol. Chem. 1990, 265, 5267-5272.
46. Nakagawa, O.; Fujisawa, K.; Ishizaki, T.; Saito, Y.; Nakao, K.; Narumiya, S. ROCK-I and ROCK-II, two isoforms of Rho-associated coiled-coil forming protein serine/threonine kinase in mice. FEBS Lett. 1996, 392, 189-193.
47. Shi, J.; Wei, L. Rho kinase in the regulation of cell death and survival. Arch. Immunol. Ther. Exp. 2007, 55, 61-75.
48. Kang, J. H.; Jiang, Y.; Toita, R.; Oishi, J.; Kawamura, K.; Han, A.; Mori, T.; Niidome, T.; Ishida, M.; Tatematsu, K.; Tanizawa, K.; Katayama, Y. Phosphorylation of Rho-associated kinase (Rho-kinase/ROCK/ROK) substrates by protein kinases A and C. Biochimie 2007, 89, 39-47.
49. Collins, I.; Caldwell, J.; Fonseca, T.; Donald, A.; Bavetsias, V.; Hunter, L. J.; Garrett, M. D.; Rowlands, M. G.; Aherne, G. W.; Davies, T. G.; Berdini, V.; Woodhead, S. J.; Davis, D.; Seavers, L. C.; Wyatt, P. G.; Workman, P.; McDonald, E. Structure-based design of isoquinoline-5-sulfonamide inhibitors of protein kinase B. Bioorg. Med. Chem. 2006, 14, 1255-1273.
50. Laine, J.; Kunstle, G.; Obata, T.; Noguchi, M. Differential Regulation of Akt Kinase Isoforms by the Members of the TCL1 Oncogene Family. J. Biol. Chem. 2002, 277, 3743-3751.
51. 50) of an enzymatic reaction. Biochem. Pharmacol. 1973, 22, 3099-3108.
52. Zhang, X.; Zhang, S.; Yamane, H.; Wahl, R.; Ali, A.; Lofgren, J. A.; Kendall, R. L. Kinetic mechanism of AKT/PKB enzyme family. J. Biol. Chem. 2006, 281, 13949-13956.
53. Ito, K.; Shimomura, E.; Iwanaga, T.; Shiraishi, M.; Shindo, K.; Nakamura, J.; Nagumo, H.; Seto, M.; Sasaki, Y.; Takuwa, Y. J. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). Physiology 2003, 546, 823-836.
54. Nikolovska-Coleska, Z.; Wang, R.; Fang, X.; Pan, H.; Tomita, Y.; Li, P.; Roller, P. P.; Krajewski, K.; Saito, N.; Stuckey, J.; Wang, S. Development and optimization of a binding assay for the XIAP BIR3 domain using fluorescence polarization. Anal. Biochem. 2004, 332, 261-273.