Multiple ligand docking by Glide: Implications for virtual second-site screening

Journal of Computer-Aided Molecular Design

Volumn 26, Issue 7, 2012, Pages 821-834

  Vass, Márton ^a   Tarcsay, Ákos ^a   Keserű, György M ^a  

^a GEDEON RICHTER LTD   (Hungary)

Author keywords

Cooperative binding; Cytochrome P450; Docking; Fragment screening; Molecular modeling; Multiple ligand binding

Indexed keywords

BINDING ENERGY; COMPLEXATION; LIGANDS; MOLECULES; PROTEINS;

BINDING-SITES; COOPERATIVE BINDING; CYTOCHROMES P450; DOCKING; E-MODEL; FRAGMENT SCREENING; LIGAND BINDING; LIGAND DOCKING; MULTIPLE LIGAND BINDING; MULTIPLE LIGANDS;

BINDING SITES;

1 (3 METHYLPHENYL) 1H BENZIMIDAZOL 5 AMINE; 1 (BIPHENYL 4 YLMETHYL) 1H IMIDAZOLE; 2 HYDROXYNAPHTHOQUINONE; 9 AMINOPHENANTHRENE; AMINE; ANDROSTENEDIONE; CARRIER PROTEIN; CHROMOPYRROLIC ACID; CYTOCHROME P450; FLAVIOLIN; HEAT SHOCK PROTEIN 90; IMIDAZOLE DERIVATIVE; KETOCONAZOLE; LIGAND; NAPHTHOQUINONE; PHENANTHRENE DERIVATIVE; RETINOIC ACID; UNCLASSIFIED DRUG; WATER;

ACCURACY; ARTICLE; BINDING SITE; CHEMICAL STRUCTURE; COMPUTER PROGRAM; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; LIGAND BINDING; MOLECULAR DOCKING; PHARMACOKINETICS; PREDICTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; SCORING SYSTEM;

EID: 84865114760     PISSN: 0920654X     EISSN: 15734951     Source Type: Journal    
DOI: 10.1007/s10822-012-9578-6     Document Type: Article

References (66)

1. Whitty A (2008) Cooperativity and biological complexity. Nat Chem Biol 4:435-439 (Pubitemid 352019765)
2. Denisov IG, Frank DJ, Sligar SG (2009) Cooperative properties of cytochromes P450. Pharmacol Ther 124:151-167
3. Guengerich FP (2008) Cytochrome P450 and chemical toxicology. Chem Res Toxicol 21:70-83 (Pubitemid 351219709)
4. Wong H, Tong V, Riggs KW, Rurak DW, Abbott FS, Kumar S (2007) Kinetics of valproic acid glucuronidation: evidence for in vivo autoactivation. Drug Metab Dispos 35:1380-1386 (Pubitemid 47121779)
5. Uchaipichat V, Galetin A, Houston JB, Mackenzie PI, Williams JA, Miners JO (2008) Kinetic modeling of the interactions between 4-methylumbelliferone, 1-naphthol, and zidovudine glucuronidation by UDP-glucuronosyltransferase 2B7 (UGT2B7) provides evidence for multiple substrate binding and effector sites. Mol Pharmacol 74:1152-1162
6. Caccuri AM, Antonini G, Ascenzi P, Nicotra M, Nuccetelli M, Mazzetti AP, Federici G, Lo Bello M, Ricci G (1999) Temperature adaptation of glutathione S-transferase P1-1. A case for homotropic regulation of substrate binding. J Biol Chem 274:19276-19280
7. Martin C, Berridge G, Higgins CF, Mistry P, Charlton P, Callaghan R (2000) Communication between multiple drug binding sites on P-glycoprotein. Mol Pharmacol 58:624-632
8. Kondratov RV, Komarov PG, Becker Y, Ewenson A, Gudkov AV (2001) Small molecules that dramatically alter multidrug resistance phenotype by modulating the substrate specificity of P-glycoprotein. Proc Natl Acad Sci USA 98:14078-14083 (Pubitemid 33116027)
9. Higgins CF (2007) Multiple molecular mechanisms for multidrug resistance transporters. Nature 446:749-757 (Pubitemid 46582024)
10. Sterz K, Möllmann L, Jacobs A, Baumert D, Wiese M (2009) Activators of P-glycoprotein: structure-activity relationships and investigation of their mode of action. Chem Med Chem 4:1897-1911
11. Harlow GR, Halpert JR (1998) Analysis of human cytochrome P450 3A4 cooperativity: construction and characterization of a site-directed mutant that displays hyperbolic steroid hydroxylation kinetics. Proc Natl Acad Sci USA 95:6636-6641 (Pubitemid 28278032)
12. Domanski TL, He YA, Khan KK, Roussel F, Wang Q, Halpert JR (2001) Phenylalanine and tryptophan scanning mutagenesis of CYP3A4 substrate recognition site residues and effect on substrate oxidation and cooperativity. Biochemistry 40:10150-10160 (Pubitemid 32800121)
13. Khan KK, He YQ, Domanski TL, Halpert JR (2002) Midazolam oxidation by cytochrome P450 3A4 and active-site mutants: an evaluation of multiple binding sites and of the metabolic pathway that leads to enzyme inactivation. Mol Pharmacol 61:495-506 (Pubitemid 34171915)
14. Harrelson JP, Atkins WM, Nelson SD (2008) Multiple-ligand binding in CYP2A6: probing mechanisms of cytochrome P450 cooperativity by assessing substrate dynamics. Biochemistry 47:2978-2988 (Pubitemid 351328851)
15. Hummel MA, Gannett PM, Aguilar JS, Tracy TS (2004) Effector-mediated alteration of substrate orientation in cytochrome P450 2C9. Biochemistry 43:7207-7214 (Pubitemid 38720538)
16. Roberts AG, Díaz MD, Lampe JN, Shireman LM, Grinstead JS, Dabrowski MJ, Pearson JT, Bowman MK, Atkins WM, Campbell AP (2006) NMR studies of ligand binding to P450eryF provides insight into the mechanism of cooperativity. Biochemistry 45:1673-1684 (Pubitemid 43222111)
17. Cameron MD, Wen B, Allen KE, Roberts AG, Schuman JT, Campbell AP, Kunze KL, Nelson SD (2005) Cooperative binding of midazolam with testosterone and alpha-naphthoflavone within the CYP3A4 active site: a NMR T1 paramagnetic relaxation study. Biochemistry 44:14143-14151 (Pubitemid 41533039)
18. Cameron MD, Wen B, Roberts AG, Atkins WM, Campbell AP, Nelson SD (2007) Cooperative binding of acetaminophen and caffeine within the P450 3A4 active site. Chem Res Toxicol 20:1434-1441 (Pubitemid 350057212)
19. Schoch GA, Yano JK, Sansen S, Dansette PM, Stout CD, Johnson EF (2008) Determinants of cytochrome P450 2C8 substrate binding: structures of complexes with montelukast, troglitazone, felodipine, and 9-cis-retinoic acid. J Biol Chem 283:17227-17237
20. Schumacher MA, Miller MC, Brennan RG (2004) Structural mechanism of the simultaneous binding of two drugs to a multidrug-binding protein. EMBO J 23:2923-2930 (Pubitemid 39093587)
21. Ekroos M, Sjögren T (2006) Structural basis for ligand promiscuity in cytochrome P450 3A4. Proc Natl Acad Sci USA 103:13682-13687 (Pubitemid 44413967)
22. Aller S, Yu J, Ward A, Weng Y, Chittaboina S, Zhuo R, Harrell PM, Trinh YT, Zhang Q, Urbatsch IL, Chang G (2009) Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323:1718-1722
23. Congreve M, Chessari G, Tisi D, Woodhead AJ (2008) Recent developments in fragment-based drug discovery. J Med Chem 51:3661-3680 (Pubitemid 351956496)
24. Petros AM, Dinges J, Augeri DJ, Baumeister SA, Betebenner DA, Bures MG, Elmore SW, Hajduk PJ, Joseph MK, Landis SK, Nettesheim DG, Rosenberg SH, Shen W, Thomas S, Wang X, Zanze I, Zhang H, Fesik SW (2006) Discovery of a potent inhibitor of the antiapoptotic protein Bcl-xL from NMR and parallel synthesis. J Med Chem 49:656-663 (Pubitemid 43157495)
25. Huth JR, Park C, Petros AM, Kunzer AR, Wendt MD, Wang X, Lynch CL, Mack JC, Swift KM, Judge RA, Chen J, Richardson PL, Jin S, Tahir SK, Matayoshi ED, Dorwin SA, Ladror US, Severin JM, Walter KA, Bartley DM, Fesik SW, Elmore SW, Hajduk PJ (2007) Discovery and design of novel HSP90 inhibitors using multiple fragment-based design strategies. Chem Biol Drug Des 70:1-12 (Pubitemid 47057425)
26. Sandor M, Kiss R, Keseru GM (2010) Virtual fragment docking by Glide: a validation study on 190 protein-fragment complexes. J Chem Inf Model 50:1165-1172
27. Li H, Li C (2010) Multiple ligand simultaneous docking: orchestrated dancing of ligands in binding sites of protein. J Comput Chem 31:2014-2022
28. Li H, Liu A, Zhao Z, Xu Y, Lin J, Jou D, Li C (2011) Fragment-based drug design and drug repositioning using multiple ligand simultaneous docking (MLSD): identifying celecoxib and template compounds as novel inhibitors of signal transducer and activator of transcription 3 (STAT3). J Med Chem 54:5592-5596
29. SiteMap, version 2.4, Schrödinger, LLC, New York, NY, 2010
30. Schrödinger Suite 2010 Protein Preparation Wizard;
31. Epik version 2.1, Schrödinger, LLC, New York, NY, 2010;
32. Impact version 5.6, Schrödinger, LLC, New York, NY, 2010;
33. Prime version 2.2, Schrödinger, LLC, New York, NY, 2010
34. Roughley SD, Hubbard RE (2011) How well can fragments explore accessed chemical space? A case study from heat shock protein 90. J Med Chem 54:3989-4005
35. Molecule File Converter, version 5.4.1.1, 1999-2011 ChemAxon Ltd
36. LigPrep, version 2.4, Schrödinger, LLC, New York, NY, 2010
37. Epik, version 2.1, Schrödinger, LLC, New York, NY, 2010
38. Shelley JC, Cholleti A, Frye LL, Greenwood JR, Timlin MR, Uchiyama M (2007) Epik: a software program for pKa prediction and protonation state generation for druglike molecules. J Comput Aided Mol Des 21:681-691
39. Greenwood JR, Calkins D, Sullivan AP, Shelley JC (2010) Towards the comprehensive, rapid, and accurate prediction of the favorable tautomeric states of drug-like molecules in aqueous solution. J Comput Aided Mol Des 24:591-604
40. Calculator, version 5.4.1.1, 1998-2011 ChemAxon Ltd
41. SiteMap 2.4 User Manual, http://www.schrodinger.com/supportdocs/18/20/
42. Glide, version 5.6, Schrödinger, LLC, New York, NY, 2010
43. Friesner RA, Banks JL, Murphy RB, Halgren TA, Klicic JJ, Mainz DT, Repasky MP, Knoll EH, Shelley M, Perry JK, Shaw DE, Francis P, Shenkin PS (2004) Glide: a new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. J Med Chem 47:1739-1749 (Pubitemid 38380917)
44. Halgren TA, Murphy RB, Friesner RA, Beard HS, Frye LL, Pollard WT, Banks JL (2004) Glide: a new approach for rapid, accurate docking and scoring. 2. Enrichment factors in database screening. J Med Chem 47:1750-1759 (Pubitemid 38380918)
45. Friesner RA, Murphy RB, Repasky MP, Frye LL, Greenwood JR, Halgren TA, Sanschagrin PC, Mainz DT (2006) Extra precision Glide: docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes. J Med Chem 49:6177-6196 (Pubitemid 44595196)
46. Cross JB, Thompson DC, Rai BK, Baber JC, Fan KY, Hu Y, Humblet C (2009) Comparison of several molecular docking programs: pose prediction and virtual screening accuracy. J Chem Inf Model 49:1455-1474
47. Cupp-Vickery J, Anderson R, Hatziris Z (2000) Crystal structures of ligand complexes of P450eryF exhibiting homotropic cooperativity. Proc Natl Acad Sci USA 97:3050-3055 (Pubitemid 30183253)
48. Podust LM, Ouellet H, von Kries JP, de Montellano PR (2009) Interaction of Mycobacterium tuberculosis CYP130 with heterocyclic arylamines. J Biol Chem 284:25211-25219
49. Zhao B, Guengerich FP, Voehler M, Waterman MR (2005) Role of active site water molecules and substrate hydroxyl groups in oxygen activation by cytochrome P450 158A2: a new mechanism of proton transfer. J Biol Chem 280:42188-42197 (Pubitemid 43023189)
50. Zhao B, Guengerich FP, Bellamine A, Lamb DC, Izumikawa M, Lei L, Podust LM, Sundaramoorthy M, Kalaitzis JA, Reddy LM, Kelly SL, Moore BS, Stec D, Voehler M, Falck JR, Shimada T, Waterman MR (2005) Binding of two flaviolin substrate molecules, oxidative coupling, and crystal structure of Streptomyces coelicolor A3(2) cytochrome P450 158A2. J Biol Chem 280: 11599-11607 (Pubitemid 40418473)
51. Makino M, Sugimoto H, Shiro Y, Asamizu S, Onaka H, Nagano S (2007) Crystal structures and catalytic mechanism of cyto-chrome P450 StaP that produces the indolocarbazole skeleton. Proc Natl Acad Sci USA 104:11591-11596 (Pubitemid 47175057)
52. Gay SC, Sun L, Maekawa K, Halpert JR, Stout CD (2009) Crystal structures of cytochrome P450 2B4 in complex with the inhibitor 1-biphenyl-4-methyl-1H- imidazole: ligand induced structural response through a-helical repositioning. Biochemistry 48:4762-4771
53. Atkins WM (2005) Non-Michaelis-Menten kinetics in cytochrome P450-catalyzed reactions. Annu Rev Pharmacol Toxicol 45:291-310 (Pubitemid 40261807)
54. Houston JB, Galetin A (2005) Modelling atypical CYP3A4 kinetics: principles and pragmatism. Arch Biochem Biophys 433:351-360 (Pubitemid 39610415)
55. Zhou SF, Zhou ZW, Yang LP, Cai JP (2009) Substrates, inducers, inhibitors and structure-activity relationships of human cyto-chrome P450 2C9 and implications in drug development. Curr Med Chem 16:3480-3675
56. Sohl CD, Isin EM, Eoff RL, Marsch GA, Stec DF, Guengerich FP (2008) Cooperativity in oxidation reactions catalyzed by cyto-chrome P450 1A2: highly cooperative pyrene hydroxylation and multiphasic kinetics of ligand binding. J Biol Chem 283:7293-7308
57. Khan KK, Liu H, Halpert JR (2003) Homotropic versus hetero-topic cooperativity of cytochrome P450eryF: a substrate oxidation and spectral titration study. Drug Metab Dispos 31:356-359 (Pubitemid 36378512)
58. Lasker JM, Huang MT, Conney AH (1984) In vitro and in vivo activation of oxidative drug metabolism by flavonoids. J Pharmacol Exp Ther 229:162-170 (Pubitemid 14082926)
59. Tang W, Stearns RA, Kwei GY, Iliff SA, Miller RR, Egan MA, Yu NX, Dean DC, Kumar S, Shou M, Lin JH, Baillie TA (1999) Interaction of diclofenac and quinidine in monkeys: stimulation of diclofenac metabolism. J Pharmacol Exp Ther 291:1068-1074
60. Hutzler JM, Frye RF, Korzekwa KR, Branch RA, Huang SM, Tracy TS (2001) Minimal in vivo activation of CYP2C9-mediated flurbiprofen metabolism by dapsone. Eur J Pharm Sci 14:47-52 (Pubitemid 32655414)
61. Egnell AC, Houston B, Boyer S (2003) In vivo CYP3A4 heteroactivation is a possible mechanism for the drug interaction between felbamate and carbamazepine. J Pharmacol Exp Ther 305:1251-1262 (Pubitemid 36618005)
62. Egnell AC, Eriksson C, Albertson N, Houston B, Boyer S (2003) Generation and evaluation of a CYP2C9 heteroactivation pharmacophore. J Pharmacol Exp Ther 307:878-887 (Pubitemid 37494204)
63. Egnell AC, Houston JB, Boyer CS (2005) Predictive models of CYP3A4 Heteroactivation: in vitro-in vivo scaling and pharmacophore modeling. J Pharmacol Exp Ther 312:926-937 (Pubitemid 40293750)
64. Locuson CW, Gannett PM, Ayscue R, Tracy TS (2007) Use of simple docking methods to screen a virtual library for heteroactivators of cytochrome P450 2C9. J Med Chem 50:1158-1165 (Pubitemid 46496316)
65. Barker JJ, Barker O, Courtney SM, Gardiner M, Hesterkamp T, Ichihara O, Mather O, Montalbetti CA, Muller A, Varasi M, Whittaker M, Yarnold CJ (2010) Discovery of a novel Hsp90 inhibitor by fragment linking. Chem Med Chem 5:1697-1700
66. Murray CW, Carr MG, Callaghan O, Chessari G, Congreve M, Cowan S, Coyle JE, Downham R, Figueroa E, Frederickson M, Graham B, McMenamin R, O'Brien MA, Patel S, Phillips TR, Williams G, Woodhead AJ, Woolford AJ (2010) Fragment based drug discovery applied to Hsp90. Discovery of two lead series with high ligand efficiency. J Med Chem 53:5942-5955