Cysteine mapping in conformationally distinct kinase nucleotide binding sites: Application to the design of selective covalent inhibitors

Journal of Medicinal Chemistry

Volumn 54, Issue 5, 2011, Pages 1347-1355

  Leproult, Emeline ^a   Barluenga, Sofia ^a   Moras, Dino ^a   Wurtz, Jean Marie ^a   Winssinger, Nicolas ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; ADENOSINE TRIPHOSPHATE; CYSTEINE; IMATINIB; NUCLEOTIDE; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN KINASE; PROTEIN KINASE INHIBITOR; STEM CELL FACTOR;

AMINO ACID ANALYSIS; ARTICLE; BINDING SITE; DRUG DESIGN; DRUG STRUCTURE; ENZYME CONFORMATION; ENZYME INHIBITION; IC 50; PREDICTION; VALIDATION PROCESS;

ADENOSINE TRIPHOSPHATE; CATALYTIC DOMAIN; CYSTEINE; DRUG DESIGN; HUMANS; MODELS, MOLECULAR; PIPERAZINES; PROTEIN CONFORMATION; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-ABL; PROTO-ONCOGENE PROTEINS C-KIT; PYRIMIDINES; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 79952269716     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm101396q     Document Type: Article

References (51)

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 (Pubitemid 35425239)
2. Bennett, B. L. c-Jun N-terminal kinase-dependent mechanisms in respiratory disease Eur. Respir. J. 2006, 28, 651-661 (Pubitemid 44794682)
3. Dhillon, A. S.; Hagan, S.; Rath, O.; Kolch, W. MAP kinase signalling pathways in cancer Oncogene 2007, 26, 3279-3290 (Pubitemid 46763021)
4. Wang, Y. Mitogen-Activated Protein Kinases in Heart Development and Diseases Circulation 2007, 116, 1413-1423 (Pubitemid 47417568)
5. Cuenda, A.; Rousseau, S. p38 MAP-kinases pathway regulation, function and role in human diseases Biochim. Biophys. Acta 2007, 1773, 1358-1375 (Pubitemid 47125981)
6. Pandya, N.; Santani, D.; Jain, S. Role of mitogen-activated protein (MAP) kinases in cardiovascular diseases Cardiovasc. Drug Rev. 2005, 23, 247-254 (Pubitemid 41572016)
7. Zuccotto, F.; Ardini, E.; Casale, E.; Angiolini, M. Through the "Gatekeeper Door": Exploiting the Active Kinase Conformation J. Med. Chem. 2010, 53, 2681-2694
8. Zhang, J.; Yang, P. L.; Gray, N. S. Targeting cancer with small molecule kinase inhibitors Nat. Rev. Cancer 2009, 9, 28-39
9. Scaltriti, M.; Verma, C.; Guzman, M.; Jimenez, J.; Parra, J. L.; Pedersen, K.; Smith, D. J.; Landolfi, S.; Ramon y Cajal, S.; Arribas, J.; Baselga, J. Lapatinib, a HER2 tyrosine kinase inhibitor, induces stabilization and accumulation of HER2 and potentiates trastuzumab-dependent cell cytotoxicity Oncogene 2009, 28, 803-814
10. Buchdunger, E.; Zimmermann, J.; Mett, H.; Meyer, T.; Müller, M.; Druker, B. J.; Lydon, N. B. Inhibition of the Abl protein-tyrosine kinase in vitro and in vivo by a 2-phenylaminopyrimidine derivative Cancer Res. 1996, 56, 100-104
11. Andzelm, E. R.; Lew, J.; Taylor, S. Bound to activate: Conformational consequences of cyclin binding to CDK2 Structure 1995, 3, 1135-1141 (Pubitemid 3001433)
12. Nagar, B.; Hantschel, O.; Young, M. A.; Scheffzek, K.; Veach, D.; Bornmann, W.; Clarkson, B.; Superti-Furga, G.; Kuriyan, J. Structural Basis for the Autoinhibition of c-Abl Tyrosine Kinase Cell 2003, 112, 859-871 (Pubitemid 36378887)
13. Liao, J. J. Molecular Recognition of Protein Kinase Binding Pockets for Design of Potent and Selective Kinase Inhibitors J. Med. Chem. 2007, 50, 409-424 (Pubitemid 46239775)
14. Cohen, M. S.; Zhang, C.; Shokat, K. M.; Taunton, J. Structural Bioinformatics-Based Design of Selective, Irreversible Kinase Inhibitors Science 2005, 308, 1318-1321 (Pubitemid 40746129)
15. Potashman, M. H.; Duggan, M. E. Covalent Modifiers: An Orthogonal Approach to Drug Design J. Med. Chem. 2009, 52, 1231-1246
16. Yun, C.; Mengwasser, K. E.; Toms, A. V.; Woo, M. S.; Greulich, H.; Wong, K.; Meyerson, M.; Eck, M. J. The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 2070-2075 (Pubitemid 351439466)
17. Allen, L. F.; Eiseman, I. A.; Fry, D. W.; Lenehan, P. F. CI-1033, an irreversible pan-erbB receptor inhibitor and its potential application for the treatment of breast cancer Semin. Oncol. 2003, 30, 65-78 (Pubitemid 37433398)
18. Laheru, D.; Croghan, G.; Bukowski, R.; Rudek, M.; Messersmith, W.; Erlichman, C.; Pelley, R.; Jimeno, A.; Donehower, R.; Boni, J.; Abbas, R.; Martins, P.; Zacharchuk, C.; Hidalgo, M. A Phase I Study of EKB-569 in Combination with Capecitabine in Patients with Advanced Colorectal Cancer Clin. Cancer Res. 2008, 14, 5602-5609
19. Spicer, J.; Rudman, S. EGFR inhibitors in non-small cell lung cancer (NSCLC): The emerging role of the dual irreversible EGFR/HER2 inhibitor BIBW 2992 Targeted Oncol. 2010, 5, 245-255
20. For another example (structure undisclosed), see Engelman, J. A.; Zejnullahu, K.; Gale, C.; Lifshits, E.; Gonzales, A. J.; Shimamura, T.; Zhao, F.; Vincent, P. W.; Naumov, G. N.; Bradner, J. E.; Althaus, I. W.; Gandhi, L.; Shapiro, G. I.; Nelson, J. M.; Heymach, J. V.; Meyerson, M.; Wong, K.; Jänne, P. A. PF00299804, an Irreversible Pan-ERBB Inhibitor, Is Effective in Lung Cancer Models with EGFR and ERBB2Mutations that Are Resistant to Gefitinib Cancer Res. 2007, 67, 11924-11932
21. Cha, M. Y.; Lee, K.; Kim, J. W.; Lee, C. G.; Song, J. Y.; Kim, Y. H.; Lee, G. S.; Park, S. B.; Kim, M. S. Discovery of A Novel Her-1/Her-2 Dual Tyrosine Kinase Inhibitor for the Treatment of Her-1 Selective Inhibitor-Resistant Non-small Cell Lung Cancer J. Med. Chem. 2009, 52, 6880-6888
22. Rabindran, S. K.; Discafani, C. M.; Rosfjord, E. C.; Baxter, M.; Floyd, M. B.; Golas, J.; Hallett, W. A.; Johnson, B. D.; Nilakantan, R.; Overbeek, E.; Reich, M. F.; Shen, R.; Shi, X.; Tsou, H.; Wang, Y.; Wissner, A. Antitumor Activity of HKI-272, an Orally Active, Irreversible Inhibitor of the HER-2 Tyrosine Kinase Cancer Res. 2004, 64, 3958-3965 (Pubitemid 38697310)
23. Blair, J. A.; Rauh, D.; Kung, C.; Yun, C.; Fan, Q.; Rode, H.; Zhang, C.; Eck, M. J.; Weiss, W. A.; Shokat, K. M. Structure-guided development of affinity probes for tyrosine kinases using chemical genetics Nat. Chem. Biol. 2007, 3, 229-238 (Pubitemid 46440537)
24. Zhou, W.; Ercan, D.; Chen, L.; Yun, C.; Li, D.; Capelletti, M.; Cortot, A. B.; Chirieac, L.; Iacob, R. E.; Padera, R.; Engen, J. R.; Wong, K.; Eck, M. J.; Gray, N. S.; Janne, P. A. Novel mutant-selective EGFR kinase inhibitors against EGFR T790M Nature 2009, 462, 1070-1074
25. Fry, D. W.; Bridges, A. J.; Denny, W. A.; Doherty, A.; Greis, K. D.; Hicks, J. L.; Hook, K. E.; Keller, P. R.; Leopold, W. R.; Loo, J. A.; McNamara, D. J.; Nelson, J. M.; Sherwood, V.; Smaill, J. B.; Trumpp-Kallmeyer, S.; Dobrusin, E. M. Specific, irreversible inactivation of the epidermal growth factor receptor and erbB2, by a new class of tyrosine kinase inhibitor Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 12022-12027 (Pubitemid 28460532)
26. Wood, E. R.; Shewchuk, L. M.; Ellis, B.; Brignola, P.; Brashear, R. L.; Caferro, T. R.; Dickerson, S. H.; Dickson, H. D.; Donaldson, K. H.; Gaul, M.; Griffin, R. J.; Hassell, A. M.; Keith, B.; Mullin, R.; Petrov, K. G.; Reno, M. J.; Rusnak, D. W.; Tadepalli, S. M.; Ulrich, J. C.; Wagner, C. D.; Vanderwall, D. E.; Waterson, A. G.; Williams, J. D.; White, W. L.; Uehling, D. E. 6-Ethynylthieno[3,2-d]- and 6-ethynylthieno[2,3-d]pyrimidin-4-anilines as tunable covalent modifiers of ErbB kinases Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 2773-2778 (Pubitemid 351723619)
27. Pan, Z.; Scheerens, H.; Li, S.; Schultz, B. E.; Sprengeler, P. A.; Burrill, L. C.; Mendonca, R. V.; Sweeney, M. D.; Scott, K. C. K.; Grothaus, P. G.; Jeffery, D. A.; Spoerke, J. M.; Honigberg, L. A.; Young, P. R.; Dalrymple, S. A.; Palmer, J. T. Discovery of selective irreversible inhibitors for Bruton's tyrosine kinase ChemMedChem 2007, 2, 58-61
28. Ohori, M.; Kinoshita, T.; Yoshimura, S.; Warizaya, M.; Nakajima, H.; Miyake, H. Role of a cysteine residue in the active site of ERK and the MAPKK family Biochim. Biophys. Res. Commun. 2007, 353, 633-637 (Pubitemid 46048715)
29. Jogireddy, R.; Dakas, P.; Valot, G.; Barluenga, S.; Winssinger, N. Synthesis of a Resorcylic Acid Lactone (RAL) Library Using Fluorous-Mixture Synthesis and Profile of its Selectivity Against a Panel of Kinases Chem. - Eur. J. 2009, 15, 11498-11506
30. Dakas, P.-Y.; Barluenga, S.; Totzke, F.; Zirrgiebel, U.; Winssinger, N. Modular Synthesis of Radicicol A and Related Resorcylic Acid Lactones, Potent Kinase Inhibitors Angew. Chem., Int. Ed. 2007, 6899-6902 (Pubitemid 47425814)
31. Rastelli, G.; Rosenfeld, R.; Reid, R.; Santi, D. V. Molecular modeling and crystal structure of ERK2-hypothemycin complexes J. Struct. Biol. 2008, 164, 18-23
32. Schirmer, A.; Kennedy, J.; Murli, S.; Reid, R.; Santi, D. V. Targeted covalent inactivation of protein kinases by resorcylic acid lactone polyketides Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 4234-4239
33. Zhou, W.; Hur, W.; McDermott, U.; Dutt, A.; Xian, W.; Ficarro, S. B.; Zhang, J.; Sharma, S. V.; Brugge, J.; Meyerson, M.; Settleman, J.; Gray, N. S. A structure-guided approach to creating covalent FGFR inhibitors Chem. Biol. 2010, 17, 285-295
34. 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.; Faraoni, R.; Floyd, M.; Hunt, J. P.; Lockhart, D. J.; Milanov, Z. V.; Morrison, M. J.; Pallares, G.; Patel, H. K.; Pritchard, S.; Wodicka, L. M.; Zarrinkar, P. P. A quantitative analysis of kinase inhibitor selectivity Nat. Biotechnol. 2008, 26, 127-132
35. Santarius, T.; Shipley, J.; Brewer, D.; Stratton, M. R.; Cooper, C. S. A census of amplified and overexpressed human cancer genes Nat. Rev. Cancer 2010, 10, 59-64
36. Berman, H. M.; Westbrook, J.; Feng, Z.; Gilliland, G.; Bhat, T. N.; Weissig, H.; Shindyalov, I. N.; Bourne, P. E. The Protein Data Bank Nucleic Acids Res. 2000, 28, 235-242 (Pubitemid 30047768)
37. Aleksandrov, A.; Simonson, T. A molecular mechanics model for imatinib and imatinib:kinase binding J. Comput. Chem. 2010, 31, 1550-1560
38. Fabian, M. A.; Biggs, W. H.; Treiber, D. K.; Atteridge, C. E.; Azimioara, M. D.; Benedetti, M. G.; Carter, T. A.; Ciceri, P.; Edeen, P. T.; Floyd, M.; Ford, J. M.; Galvin, M.; Gerlach, J. L.; Grotzfeld, R. M.; Herrgard, S.; Insko, D. E.; Insko, M. A.; Lai, A. G.; Lelias, J.; Mehta, S. A.; Milanov, Z. V.; Velasco, A. M.; Wodicka, L. M.; Patel, H. K.; Zarrinkar, P. P.; Lockhart, D. J. A small molecule-kinase interaction map for clinical kinase inhibitors Nat. Biotechnol. 2005, 23, 329-336 (Pubitemid 41094421)
39. Michalczyk, A.; Klüter, S.; Rode, H. B.; Simard, J. R.; Grütter, C.; Rabiller, M.; Rauh, D. Structural insights into how irreversible inhibitors can overcome drug resistance in EGFR Bioorg. Med. Chem. 2008, 16, 3482-3488 (Pubitemid 351484056)
40. Blencke, S.; Zech, B.; Engkvist, O.; Greff, Z.; Orfi, L.; Horváth, Z.; Kéri, G.; Ullrich, A.; Daub, H. Characterization of a Conserved Structural Determinant Controlling Protein Kinase Sensitivity to Selective Inhibitors Chem. Biol. 2004, 11, 691-701 (Pubitemid 38708838)
41. Rossi, A.; Kapahi, P.; Natoli, G.; Takahashi, T.; Chen, Y.; Karin, M.; Santoro, M. G. Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of I[kappa]B kinase Nature 2000, 403, 103-118
42. Copeland, R. A.; Pompliano, D. L.; Meek, T. D. Drug-target residence time and its implications for lead optimization Nat. Rev. Drug Discovery 2006, 5, 730-739 (Pubitemid 44323700)
43. Smith, A. J. T.; Zhang, X.; Leach, A. G.; Houk, K. N. Beyond Picomolar Affinities: Quantitative Aspects of Noncovalent and Covalent Binding of Drugs to Proteins J. Med. Chem. 2009, 52, 225-233
44. Knight, Z. A.; Shokat, K. M. Features of Selective Kinase Inhibitors Chem. Biol. 2005, 12, 621-637 (Pubitemid 43142039)
45. Toursel, T.; Bard, N.; Bolze, R.; Caron, E.; Desprez, F.; Heymann, M.; Friedrich, A.; Moulinier, L.; Nguyen, N. H.; Poch, O. Décrypthon grid-grid resources dedicated to neuromuscular disorders Stud. Health Technol. Inform. 2010, 159, 124-133
46. BIRD 2010; http://alnitak.u-strasbg.fr/wikili/index.php/BIRD.
47. Dolinsky, T. J.; Nielsen, J. E.; McCammon, J. A.; Baker, N. A. PDB2PQR: An automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations Nucleic Acids Res. 2004, 32, W665-W667
48. Albou, L.; Schwarz, B.; Poch, O.; Wurtz, J. M.; Moras, D. Defining and characterizing protein surface using alpha shapes Proteins: Struct., Funct., Bioinf. 2009, 76, 1-12
49. Edelsbrunner, H.; Facello, M.; Liang, J. On the definition and the construction of pockets in macromolecules Pac. Symp. Biocomput. 1996, 272-287
50. Liang, J.; Edelsbrunner, H.; Woodward, C. Anatomy of protein pockets and cavities: Measurement of binding site geometry and implications for ligand design Protein Sci. 1998, 7, 1884-1897 (Pubitemid 28432430)
51. Kabsch, W.; Sander, C. Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features Biopolymers 1983, 22, 2577-2637