Analysis of water patterns in protein kinase binding sites

Proteins: Structure, Function and Bioinformatics

Volumn 79, Issue 7, 2011, Pages 2109-2121

  Barillari, Caterina ^a,b   Duncan, Anna L ^c   Westwood, Isaac M ^a,b   Blagg, Julian ^a,b   van Montfort, Rob L M ^a,b  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Binding site similarity; Drug design; Kinase; Selectivity; Water molecules

Indexed keywords

ADENOSINE TRIPHOSPHATE; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN KINASE; WATER;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME CONFORMATION; ENZYME INACTIVATION; ENZYME STRUCTURE; HYDROGEN BOND; LIGAND BINDING; PRIORITY JOURNAL; WATER ANALYSIS;

ADENOSINE TRIPHOSPHATE; BINDING SITES; CLUSTER ANALYSIS; DATABASES, PROTEIN; HUMANS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN KINASES; WATER;

EID: 79958765059     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.23032     Document Type: Article

References (45)

1. Zhang J, Yang PL, Gray NS. Targeting cancer with small molecule kinase inhibitors. Nat Rev Cancer 2009; 9: 28-39.
2. Noble ME, Endicott JA, Johnson LN. Protein kinase inhibitors: insights into drug design from structure. Science 2004; 303: 1800-1805.
3. Huse M, Kuriyan J. The conformational plasticity of protein kinases. Cell 2002; 109: 275-282.
4. Liu Y, Gray NS. Rational design of inhibitors that bind to inactive kinase conformations. Nat Chem Biol 2006; 2: 358-364.
5. Nagar B, Bornmann WG, Pellicena P, Schindler T, Veach DR, Miller WT, Clarkson B, Kuriyan J. Crystal structures of the kinase domain of c-Abl in complex with the small molecule inhibitors PD173955 and imatinib (STI-571). Cancer Res 2002; 62: 4236-4243.
6. Knight ZA, Shokat KM. Features of selective kinase inhibitors. Chem Biol 2005; 12: 621-637.
7. Kuhn D, Weskamp N, Hullermeier E, Klebe G. Functional classification of protein kinase binding sites using Cavbase. Chem Med Chem 2007; 2: 1432-1447.
8. Kinnings SL, Jackson RM. Binding site similarity analysis for the functional classification of the protein kinase family. J Chem Inf Model 2009; 49: 318-329.
9. Barillari C, Taylor J, Viner R, Essex JW. Classification of water molecules in protein binding sites. J Am Chem Soc 2007; 129: 2577-2587.
10. Brough PA, Aherne W, Barril X, Borgognoni J, Boxall K, Cansfield JE, Cheung KM, Collins I, Davies NG, Drysdale MJ, Dymock B, Eccles SA, Finch H, Fink A, Hayes A, Howes R, Hubbard RE, James K, Jordan AM, Lockie A, Martins V, Massey A, Matthews TP, McDonald E, Northfield CJ, Pearl LH, Prodromou C, Ray S, Raynaud FI, Roughley SD, Sharp SY, Surgenor A, Walmsley DL, Webb P, Wood M, Workman P, Wright L. 4, 5-diarylisoxazole Hsp90 chaperone inhibitors: potential therapeutic agents for the treatment of cancer. J Med Chem 2008; 51: 196-218.
11. Garcia-Sosa AT, Mancera RL, Dean PM. WaterScore: a novel method for distinguishing between bound and displaceable water molecules in the crystal structure of the binding site of protein-ligand complexes. J Mol Model 2003; 9: 172-182.
12. Poornima CS, Dean PM. Hydration in drug design. 3. Conserved water molecules at the ligand-binding sites of homologous proteins. J Comput Aided Mol Des 1995; 9: 521-531.
13. Poornima CS, Dean PM. Hydration in drug design. 2. Influence of local site surface shape on water binding. J Comput Aided Mol Des 1995; 9: 513-520.
14. Poornima CS, Dean PM. Hydration in drug design. 1. Multiple hydrogen-bonding features of water molecules in mediating protein-ligand interactions. J Comput Aided Mol Des 1995; 9: 500-512.
15. Raymer ML, Sanschagrin PC, Punch WF, Venkataraman S, Goodman ED, Kuhn LA. Predicting conserved water-mediated and polar ligand interactions in proteins using a K-nearest-neighbors genetic algorithm. J Mol Biol 1997; 265: 445-464.
16. Mackman RL, Katz BA, Breitenbucher JG, Hui HC, Verner E, Luong C, Liu L, Sprengeler PA. Exploiting subsite S1 of trypsin-like serine proteases for selectivity: potent and selective inhibitors of urokinase-type plasminogen activator. J Med Chem 2001; 44: 3856-3871.
17. Fernandez A, Sanguino A, Peng Z, Ozturk E, Chen J, Crespo A, Wulf S, Shavrin A, Qin C, Ma J, Trent J, Lin Y, Han HD, Mangala LS, Bankson JA, Gelovani J, Samarel A, Bornmann W, Sood AK, Lopez-Berestein G. An anticancer C-Kit kinase inhibitor is reengineered to make it more active and less cardiotoxic. J Clin Invest 2007; 117: 4044-4054.
18. Myrianthopoulos V, Magiatis P, Ferandin Y, Skaltsounis AL, Meijer L, Mikros E. An integrated computational approach to the phenomenon of potent and selective inhibition of aurora kinases B and C by a series of 7-substituted indirubins. J Med Chem 2007; 50: 4027-4037.
19. Finlay MR, Acton DG, Andrews DM, Barker AJ, Dennis M, Fisher E, Graham MA, Green CP, Heaton DW, Karoutchi G, Loddick SA, Morgentin R, Roberts A, Tucker JA, Weir HM. Imidazole piperazines: SAR and development of a potent class of cyclin-dependent kinase inhibitors with a novel binding mode. Bioorg Med Chem Lett 2008; 18: 4442-4446.
20. Robinson DD, Sherman W, Farid R. Understanding kinase selectivity through energetic analysis of binding site waters. Chem Med Chem 2010; 5: 618-627.
21. Knight JD, Hamelberg D, McCammon JA, Kothary R. The role of conserved water molecules in the catalytic domain of protein kinases. Proteins 2009; 76: 527-535.
22. Kellenberger E, Muller P, Schalon C, Bret G, Foata N, Rognan D. sc-PDB: an annotated database of druggable binding sites from the Protein Data Bank. J Chem Inf Model 2006; 46: 717-727.
23. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. The Protein Data Bank. Nucleic Acids Res 2000; 28: 235-242.
24. Chemical Computing Group, Inc. Molecular Operating Environment (MOE). Montreal, Quebec, Canada 2008.
25. Schalon C, Surgand JS, Kellenberger E, Rognan D. A simple and fuzzy method to align and compare druggable ligand-binding sites. Proteins 2008; 71: 1755-1778.
26. Karypis G. 2009. Last accessed on 11/04/2011.
27. Kuhn D, Weskamp N, Schmitt S, Hullermeier E, Klebe G. From the similarity analysis of protein cavities to the functional classification of protein families using cavbase. J Mol Biol 2006; 359: 1023-1044.
28. Sanschagrin PC, Kuhn LA. Cluster analysis of consensus water sites in thrombin and trypsin shows conservation between serine proteases and contributions to ligand specificity. Protein Sci 1998; 7: 2054-2064.
29. Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 2010; 66: 486-501.
30. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 2010; 66: 213-221.
31. Langer G, Cohen SX, Lamzin VS, Perrakis A. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat Protoc 2008; 3: 1171-1179.
32. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S. The protein kinase complement of the human genome. Science 2002; 298: 1912-1934.
33. The PyMOL Molecular Graphics System VrpS, LLC.
34. Michel J, Tirado-Rives J, Jorgensen WL. Energetics of displacing water molecules from protein binding sites: consequences for ligand optimization. J Am Chem Soc 2009; 131: 15403-15411.
35. Potterton L, McNicholas S, Krissinel E, Gruber J, Cowtan K, Emsley P, Murshudov GN, Cohen S, Perrakis A, Noble M. Developments in the CCP4 molecular-graphics project. Acta Crystallogr D Biol Crystallogr 2004; 60: 2288-2294.
36. Thompson AM, Delaney AM, Hamby JM, Schroeder MC, Spoon TA, Crean SM, Showalter HD, Denny WA. Synthesis and structure-activity relationships of soluble 7-substituted 3-(3, 5-dimethoxyphenyl)-1, 6-naphthyridin-2-amines and related ureas as dual inhibitors of the fibroblast growth factor receptor-1 and vascular endothelial growth factor receptor-2 tyrosine kinases. J Med Chem 2005; 48: 4628-4653.
37. Mohammadi M, Froum S, Hamby JM, Schroeder MC, Panek RL, Lu GH, Eliseenkova AV, Green D, Schlessinger J, Hubbard SR. Crystal structure of an angiogenesis inhibitor bound to the FGF receptor tyrosine kinase domain. EMBO J 1998; 17: 5896-5904.
38. Trumpp-Kallmeyer S, Rubin JR, Humblet C, Hamby JM, Hollis Showalter HD. Development of a binding model to protein tyrosine kinases for substituted pyrido[2, 3-d]pyrimidine inhibitors. J Med Chem 1998; 41: 1752-1763.
39. Hamby JM, Connolly CJ, Schroeder MC, Winters RT, Showalter HD, Panek RL, Major TC, Olsewski B, Ryan MJ, Dahring T, Lu GH, Keiser J, Amar A, Shen C, Kraker AJ, Slintak V, Nelson JM, Fry DW, Bradford L, Hallak H, Doherty AM. Structure-activity relationships for a novel series of pyrido[2, 3-d]pyrimidine tyrosine kinase inhibitors. J Med Chem 1997; 40: 2296-2303.
40. Schroeder MC, Hamby JM, Connolly CJ, Grohar PJ, Winters RT, Barvian MR, Moore CW, Boushelle SL, Crean SM, Kraker AJ, Driscoll DL, Vincent PW, Elliott WL, Lu GH, Batley BL, Dahring TK, Major TC, Panek RL, Doherty AM, Showalter HD. Soluble 2-substituted aminopyrido[2, 3-d]pyrimidin-7-yl ureas. Structure-activity relationships against selected tyrosine kinases and exploration of in vitro and in vivo anticancer activity. J Med Chem 2001; 44: 1915-1926.
41. Fedorov O, Sundstrom M, Marsden B, Knapp S. Insights for the development of specific kinase inhibitors by targeted structural genomics. Drug Discov Today 2007; 12: 365-372.
42. Schindler T, Bornmann W, Pellicena P, Miller WT, Clarkson B, Kuriyan J. Structural mechanism for STI-571 inhibition of abelson tyrosine kinase. Science 2000; 289: 1938-1942.
43. Wan PT, Garnett MJ, Roe SM, Lee S, Niculescu-Duvaz D, Good VM, Jones CM, Marshall CJ, Springer CJ, Barford D, Marais R. Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF. Cell 2004; 116: 855-867.
44. Pargellis C, Tong L, Churchill L, Cirillo PF, Gilmore T, Graham AG, Grob PM, Hickey ER, Moss N, Pav S, Regan J. Inhibition of p38 MAP kinase by utilizing a novel allosteric binding site. Nat Struct Biol 2002; 9: 268-272.
45. Liao JJ. Molecular recognition of protein kinase binding pockets for design of potent and selective kinase inhibitors. J Med Chem 2007; 50: 409-424.