Target specific proteochemometric model development for BACE1 - protein flexibility and structural water are critical in virtual screening

Molecular BioSystems

Volumn 11, Issue 7, 2015, Pages 1955-1972

  Manoharan, Prabu ^a   Chennoju, Kiranmai ^b   Ghoshal, Nanda ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

^b NATIONAL INSTITUTE OF PHARMACEUTICAL EDUCATION AND RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC PROTEINASE; BACE1 PROTEIN, HUMAN; LIGAND; PROTEIN BINDING; PROTEINASE INHIBITOR; SECRETASE; WATER;

ALZHEIMER DISEASE; CHEMICAL PHENOMENA; CHEMISTRY; ENZYME ACTIVE SITE; ENZYMOLOGY; HUMAN; HYDROGEN BOND; MOLECULAR DOCKING; MOLECULARLY TARGETED THERAPY; RECEIVER OPERATING CHARACTERISTIC; THERMODYNAMICS;

ALZHEIMER DISEASE; AMYLOID PRECURSOR PROTEIN SECRETASES; ASPARTIC ACID ENDOPEPTIDASES; CATALYTIC DOMAIN; HUMANS; HYDROGEN BONDING; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIGANDS; MOLECULAR DOCKING SIMULATION; MOLECULAR TARGETED THERAPY; PROTEASE INHIBITORS; PROTEIN BINDING; ROC CURVE; THERMODYNAMICS; WATER;

EID: 84934892563     PISSN: 1742206X     EISSN: 17422051     Source Type: Journal    
DOI: 10.1039/c5mb00088b     Document Type: Article

References (77)

1. S. Salloway J. Mintzer M. F. Weiner J. L. Cummings Disease-modifying therapies in Alzheimer's disease Alzheimer's Dementia 2008 4 65 79
2. M. Citron Alzheimer's disease: strategies for disease modification Nat. Rev. Drug Discovery 2010 9 387 398
3. B. De Strooper R. Vassar T. Golde The secretases: enzymes with therapeutic potential in Alzheimer disease Nat. Rev. Neurol. 2010 6 99 107
4. M. Citron beta-Secretase inhibition for the treatment of Alzheimer's disease-promise and challenge Trends Pharmacol. Sci. 2004 25 92 97
5. R. Yan M. J. Bienkowski M. E. Shuck H. Miao M. C. Tory A. M. Pauley J. R. Brashler N. C. Stratman W. R. Mathews A. E. Buhl D. B. Carter A. G. Tomasselli L. A. Parodi R. L. Heinrikson M. E. Gurney Membrane-anchored aspartyl protease with Alzheimer's disease [beta]-secretase activity Nature 1999 402 533 537
6. R. Vassar B. D. Bennett S. Babu-Khan S. Kahn E. A. Mendiaz P. Denis D. B. Teplow S. Ross P. Amarante R. Loeloff Y. Luo S. Fisher J. Fuller S. Edenson J. Lile M. A. Jarosinski A. L. Biere E. Curran T. Burgess J. C. Louis F. Collins J. Treanor G. Rogers M. Citron β-Secretase Cleavage of Alzheimer's Amyloid Precursor Protein by the Transmembrane Aspartic Protease BACE Science 1999 286 735 741
7. S. Sinha J. P. Anderson R. Barbour G. S. Basi R. Caccavello D. Davis M. Doan H. F. Dovey N. Frigon J. Hong K. Jacobson-Croak N. Jewett P. Keim J. Knops I. Lieberburg M. Power H. Tan G. Tatsuno J. Tung D. Schenk P. Seubert S. M. Suomensaari S. Wang D. Walker J. Zhao L. McConlogue V. John Purification and cloning of amyloid precursor protein [beta]-secretase from human brain Nature 1999 402 537 540
8. H. M. Berman J. Westbrook Z. Feng G. Gilliland T. N. Bhat H. Weissig I. N. Shindyalov P. E. Bourne The protein data bank Nucleic Acids Res. 2000 28 235 242
9. A. A. Gorfe A. Caflisch Functional plasticity in the substrate binding site of beta-secretase Structure 2005 13 1487 1498
10. F. A. Quiocho D. K. Wilson N. K. Vyas Substrate specificity and affinity of a protein modulated by bound water molecules Nature 1989 340 404 407
11. T. N. Bhat G. A. Bentley G. Boulot M. I. Greene D. Tello W. Dall'Acqua H. Souchon F. P. Schwarz R. A. Mariuzza R. J. Poljak Bound water molecules and conformational stabilization help mediate an antigen-antibody association Proc. Natl. Acad. Sci. U. S. A. 1994 91 1089 1093
12. J. R. Tame S. H. Sleigh A. J. Wilkinson J. E. Ladbury The role of water in sequence-independent ligand binding by an oligopeptide transporter protein Nat. Struct. Biol. 1996 3 998 1001
13. M. Babor V. Sobolev M. Edelman Conserved Positions for Ribose Recognition: Importance of Water Bridging Interactions Among ATP, ADP and FAD-protein Complexes J. Mol. Biol. 2002 323 523 532
14. N. Huang B. K. Shoichet Exploiting Ordered Waters in Molecular Docking J. Med. Chem. 2008 51 4862 4865
15. Z. Li T. Lazaridis Thermodynamic Contributions of the Ordered Water Molecule in HIV-1 Protease J. Am. Chem. Soc. 2003 125 6636 6637
16. Y. Lu C. Y. Yang S. Wang Binding Free Energy Contributions of Interfacial Waters in HIV-1 Protease/Inhibitor Complexes J. Am. Chem. Soc. 2006 128 11830 11839
17. C. A. Coburn S. J. Stachel Y. M. Li D. M. Rush T. G. Steele E. Chen-Dodson M. K. Holloway M. Xu Q. Huang M. T. Lai J. DiMuzio M. C. Crouthamel X. P. Shi V. Sardana Z. Chen S. Munshi L. Kuo G. M. Makara D. A. Annis P. K. Tadikonda H. M. Nash J. P. Vacca T. Wang Identification of a Small Molecule Nonpeptide Active Site β-Secretase Inhibitor That Displays a Nontraditional Binding Mode for Aspartyl Proteases J. Med. Chem. 2004 47 6117 6119
18. S. Tian H. Sun P. Pan D. Li X. Zhen Y. Li T. Hou Assessing an Ensemble Docking-Based Virtual Screening Strategy for Kinase Targets by Considering Protein Flexibility J. Chem. Inf. Model. 2014 54 2664 2679
19. S. Tian H. Sun Y. Li P. Pan D. Li T. Hou Development and Evaluation of an Integrated Virtual Screening Strategy by Combining Molecular Docking and Pharmacophore Searching Based on Multiple Protein Structures J. Chem. Inf. Model. 2013 53 2743 2756
20. S. Tian Y. Li D. Li X. Xu J. Wang Q. Zhang T. Hou Modeling Compound-Target Interaction Network of Traditional Chinese Medicines for Type II Diabetes Mellitus: Insight for Polypharmacology and Drug Design J. Chem. Inf. Model. 2013 53 1787 1803
21. S. Zhou Y. Li T. Hou Feasibility of Using Molecular Docking-Based Virtual Screening for Searching Dual Target Kinase Inhibitors J. Chem. Inf. Model. 2013 53 982 996
22. T. Hou S. Guo X. Xu Predictions of binding of a diverse set of ligands to gelatinase-A by a combination of molecular dynamics and continuum solvent models J. Phys. Chem. B 2002 106 5527 5535
23. W. Wang P. A. Kollman Computational study of protein specificity: The molecular basis of HIV-1 protease drug resistance Proc. Natl. Acad. Sci. U. S. A. 2001 98 14937 14942
24. M. Lepsik Z. Kriz Z. Havlas Efficiency of a second-generation HIV-1 protease inhibitor studied by molecular dynamics and absolute binding free energy calculations Proteins: Struct., Funct., Bioinf. 2004 57 279 293
25. B. Kuhn P. A. Kollman Binding of a diverse set of ligands to avidin and streptavidin: an accurate quantitative prediction of their relative affinities by a combination of molecular mechanics and continuum solvent models J. Med. Chem. 2000 43 3786 3791
26. S. Huo J. Wang P. Cieplak P. A. Kollman I. D. Kuntz Molecular dynamics and free energy analyses of cathepsin D-inhibitor interactions: insight into structure-based ligand design J. Med. Chem. 2002 45 1412 1419
27. S. P. Brown S. W. Muchmore High-throughput calculation of proteinligand binding affinities: modification and adaptation of the MM-PBSA protocol to enterprise grid computing J. Chem. Inf. Model. 2006 46 999 1005
28. I. Stoica S. K. Sadiq P. V. Coveney Rapid and accurate prediction of binding free energies for saquinavir-bound HIV-1 proteases J. Am. Chem. Soc. 2008 130 2639 2648
29. T. Hou L. Zhu L. Chen X. Xu Mapping the binding site of a large set of quinazoline type EGF-R inhibitors using molecular field analyses and molecular docking studies J. Chem. Inf. Comput. Sci. 2003 43 273 287
30. T. Hou R. Yu Molecular dynamics and free energy studies on the wild-type and double mutant HIV-1 protease complexed with amprenavir and two amprenavir-related inhibitors: mechanism for binding and drug resistance J. Med. Chem. 2007 50 1177 1188
31. T. Hou J. Wang Y. Li W. Wang Assessing the Performance of the MM/PBSA and MM/GBSA Methods. 1, The Accuracy of Binding Free Energy Calculations Based on Molecular Dynamics Simulations J. Chem. Inf. Model. 2011 51 69 82
32. T. Hou J. Wang Y. Li W. Wang Assessing the Performance of the Molecular Mechanics/Poisson Boltzmann Surface Area and Molecular Mechanics/Generalized Born Surface Area Methods. II. The Accuracy of Ranking Poses Generated From Docking J. Comput. Chem. 2011 32 866 877
33. L. Xu H. Sun Y. Li J. Wang T. Hou Assessing the Performance of MM/PBSA and MM/GBSA Methods. 3. The Impact of Force Fields and Ligand Charge Models J. Phys. Chem. B 2013 117 8408 8421
34. H. Sun Y. Li S. Tian L. Xub T. Hou Assessing the performance of MM/PBSA and MM/GBSA methods. 4. Accuracies of MM/PBSA and MM/GBSA methodologies evaluated by various simulation protocols using PDBbind data set Phys. Chem. Chem. Phys. 2014 16 16719 16729
35. H. Sun Y. Li M. Shen S. Tian L. Xu P. Pan Y. Guana T. Hou Assessing the performance of MM/PBSA and MM/GBSA methods. 5, Improved docking performance using high solute dielectric constant MM/GBSA and MM/PBSA rescoring Phys. Chem. Chem. Phys. 2014 16 22035 22045
36. N. Moitessier P. Englebienne D. Lee J. Lawandi C. R. Corbeil Towards the development of universal, fast and highly accurate docking/scoring methods: a long way to go Br. J. Pharmacol. 2008 153 suppl 1 S7 S26
37. R. Taylor P. Jewsbury J. Essex A review of protein-small molecule docking methods J. Comput.-Aided Mol. Des. 2002 16 151 166
38. G. L. Warren C. W. Andrews A. Capelli B. Clarke J. LaLonde M. H. Lambert M. Lindvall N. Nevins S. F. Semus S. Senger G. Tedesco I. D. Wall J. M. Woolven C. E. Peishoff M. S. Head A critical assessment of docking programs and scoring functions J. Med. Chem. 2006 49 5912 5931
39. A. R. Leach B. K. Shoichet C. E. Peishoff Prediction of protein-ligand interactions. Docking and scoring: successes and gaps J. Med. Chem. 2006 49 5851 5855
40. P. Manoharan R. S. Vijayan N. Ghoshal Rationalizing fragment based drug discovery for BACE1: insights from FB-QSAR, FB-QSSR, multi objective (MO-QSPR) and MIF studies J. Comput.-Aided Mol. Des. 2010 24 843 864
41. P. Manoharan N. Ghoshal Rationalizing lead optimization by consensus 2D- CoMFA CoMSIA GRIND (3D) QSAR guided fragment hopping in search of γ-secretase inhibitors Mol. Diversity 2012 3 563 577
42. S. Cosconati L. Marinelli F. S. D. Leva V. L. Pietra A. D. Simone F. Mancini V. Andrisano E. Novellino D. S. Goodsell A. J. Olson Protein Flexibility in Virtual Screening: The BACE-1 Case Study J. Chem. Inf. Model. 2012 52 2697 2704
43. A. F. Nastase D. B. Boyd Simple Structure-Based Approach for Predicting the Activity of Inhibitors of Beta-Secretase (BACE1) Associated with Alzheimer's Disease J. Chem. Inf. Model. 2012 52 3302 3307
44. R. A. Friesner R. B. Murphy M. P. Repasky L. L. Frye J. R. Greenwood T. A. Halgren P. C. Sanschagrin D. T. Mainz Extra precision glide: docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes J. Med. Chem. 2006 49 6177 6196
45. L. Tan J. Batista J. Bajorath Computational methodologies for compound database searching that utilize experimental protein-ligand interaction information Chem. Biol. Drug Des. 2010 76 191 200
46. C. de Graaf C. Rein D. Piwnica F. Giordanetto D. Rognan Structure-based discovery of allosteric modulators of two related class B G-protein-coupled receptors ChemMedChem 2011 6 2159 2169
47. C. de Graaf D. Rognan Selective structure-based virtual screening for full and partial agonists of the beta2 adrenergic receptor J. Med. Chem. 2008 51 4978 4985
48. N. Weill C. Valencia S. Gioria P. Villa M. Hibert D. Rognan Identification of Nonpeptide Oxytocin Receptor Ligands by Receptor-Ligand Fingerprint Similarity Search Mol. Inf. 2011 30 521 526
49. T. Liu Y. Lin X. Wen R. N. Jorissen M. K. Gilson BindingDB: a web-accessible database of experimentally determined protein-ligand binding affinities Nucleic Acids Res. 2007 35 198 201
50. R. A. Laskowski M. B. Swindells LigPlot+: multiple ligand-protein interaction diagrams for drug discovery J. Chem. Inf. Model. 2011 51 2778 2786
51. I. K. McDonald J. M. Thornton Satisfying Hydrogen Bonding Potential in Proteins J. Mol. Biol. 1994 238 777 793
52. Maestro, Version 9.0, Schrodinger, LLC, New York, NY, 2008
53. Molecular Operating Environment (MOE), 2012.10, Chemical Computing Group Inc., 1010 Sherbooke St. West, Suite #910, Montreal, QC, Canada, H3A 2R7, 2012
54. P. Beswick N. Charrier B. Clarke E. Demont C. Dingwall R. Dunsdon A. Faller R. Gleave J. Hawkins I. Hussain C. N. Johnson D. MacPherson G. Maile P. Milner A. Naylor A. O'Brien S. Redshaw D. Riddell P. Rowland J. Skidmore V. Soleil K. Smith S. Stanway G. Stemp A. Stuart P. Theobald D. Vesey D. S. Walter J. Ward G. Wayne BACE-1 inhibitors. Part 3: identification of hydroxyl ethylamines (HEAs) with nanomolar potency in cells Bioorg. Med. Chem. Lett. 2008 18 1022 1026
55. TSAR, Version 3.3, Accelrys Inc., San Diego, CA, 2007
56. A. K. Ghosh N. Kumaragurubarana L. Hong c. S. Kulkarni X. Xu H. B. Miller D. S. Reddy V. Weerasena R. Turner W. Chang G. Koelschb c. J. Tang Potent memapsin 2 (β-secretase) inhibitors: design, synthesis, protein-ligand X-ray structure, and in vivo evaluation Bioorg. Med. Chem. Lett. 2008 18 1031 1036
57. J. N. Cumming T. X. Le S. Babu C. Carroll X. Chen L. Favreau P. Gaspari T. Guo D. W. Hobbs Y. Huang U. Iserloh M. E. Kennedy R. Kuvelkar G. Li J. Lowrie N. A. McHugh L. Ozgur J. Pan E. M. Parker K. Saionz A. W. Stamford C. Strickland D. Tadesse J. Voigt L. Wang Y. Wu L. Zhang Q. Zhang Rational design of novel, potent piperazinone and imidazolidinone BACE1 inhibitors Bioorg. Med. Chem. Lett. 2008 18 3236 3241
58. J. N. Freskos Y. M. Fobian T. E. Benson J. B. Moon M. J. Bienkowski D. L. Brown T. L. Emmons R. Heintz A. Laborde J. J. McDonald B. V. Mischke J. M. Molyneaux P. B. Mullins D. Bryan Prince D. J. Paddock A. G. Tomasselli G. Winterrowd Design of potent inhibitors of human beta-secretase. Part 2 Bioorg. Med. Chem. Lett. 2007 17 78 81
59. Y. S. Wang C. Strickland J. H. Voigt M. E. Kennedy B. M. Beyer M. M. Senior E. M. Smith T. L. Nechuta V. S. Madison M. Czarniecki B. A. McKittrick A. W. Stamford E. M. Parker J. C. Hunter W. J. Greenlee D. F. Wyss Application of Fragment-Based NMR Screening, X-ray Crystallography, Structure-Based Design, and Focused Chemical Library Design to Identify Novel μM Leads for the Development of nM BACE-1 (β-Site APP Cleaving Enzyme 1) Inhibitors J. Med. Chem. 2010 53 942 950
60. L. Hong J. Tang Flap Position of Free Memapsin 2 (β-Secretase), a Model for Flap Opening in Aspartic Protease Catalysis Biochemistry 2004 43 4689 4695
61. S. Patel L. Vuillard A. Cleasby C. W. Murray J. Yon Apo and Inhibitor Complex Structures of BACE (β-secretase J. Mol. Biol. 2004 343 407 416
62. Y. Xu M. J. Li H. Greenblatt W. Chen A. Paz O. Dym Y. Peleg T. Chen X. Shen J. He H. Jiang I. Silman J. L. Sussman Flexibility of the flap in the active site of BACE1 as revealed by crystal structures and molecular dynamics simulations Acta Crystallogr., Sect. D: Biol. Crystallogr. 2012 68 13 25
63. J. Dundas Z. Ouyang J. Tseng A. Binkowski Y. Turpaz J. Liang CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues Nucleic Acids Res. 2006 34 W116 W118
64. P. Labute Probabilistic Receptor Potentials J. Chem. Comput. Group 2001
65. A. L. Hopkins C. R. Groom A. Alex Ligand efficiency: a useful metric for lead selection Drug Discovery Today 2004 9 430 431
66. S. W. Homans Water, water everywhere - except where it matters? Drug Discovery Today 2007 12 534 539
67. C. Barillari J. Taylor R. Viner J. W. Essex Classification of Water Molecules in Protein Binding Sites J. Am. Chem. Soc. 2007 129 2577 2587
68. F. Wångsell K. Gustafsson I. Kvarnström N. Borkakoti M. Edlund K. Jansson J. Lindberg A. Hallberg A. Rosenquist B. Samuelsson Synthesis of potent BACE-1 inhibitors incorporating a hydroxyethylene isostere as central core Eur. J. Med. Chem. 2010 45 870 882
69. C. Björklund S. Oscarson K. Benkestock N. Borkakoti K. Jansson J. Lindberg L. Vrang A. Hallberg A. Rosenquist B. Samuelsson Design and Synthesis of Potent and Selective BACE-1 Inhibitors J. Med. Chem. 2010 53 1458 1464
70. N. Weill D. Rognan Development and validation of a novel protein-ligand fingerprint to mine chemogenomic space: application to G protein-coupled receptors and their ligands J. Chem. Inf. Model. 2009 49 1049 1062
71. H. Geppert J. Humrich D. Stumpfe T. Gartner J. Bajorath Ligand prediction from protein sequence and small molecule information using support vector machines and fingerprint descriptors J. Chem. Inf. Model. 2009 49 767 779
72. J. Yuan S. Venkatraman Y. Zheng B. M. McKeever L. W. Dillard S. B. Singh Structure-Based Design of β-Site APP Cleaving Enzyme 1 (BACE1) Inhibitors for the Treatment of Alzheimer's Disease J. Med. Chem. 2013 56 4156 4180
73. A. Barman R. Prabhakar Protonation States of the Catalytic Dyad of β-Secretase (BACE1) in the Presence of Chemically Diverse Inhibitors: A Molecular Docking Study J. Chem. Inf. Model. 2012 52 1275 1287
74. J. L. Domínguez T. Christopeit M. C. Villaverde T. Gossas J. M. Otero S. Nyström V. Baraznenok E. Lindström U. H. Danielson F. Sussman Effect of the Protonation State of the Titratable Residues on the Inhibitor Affinity to BACE-1 Biochemistry 2010 49 7255 7263
75. T. Fawcett An introduction to ROC analysis Pattern Recognit. Lett. 2006 27 861 874
76. R. S. Vijayan M. Prabu N. M. Mascarenhas N. Ghoshal Hybrid Structure-Based Virtual Screening Protocol for the Identification of Novel BACE1 Inhibitors J. Chem. Inf. Model. 2009 49 647 657
77. N. Huang B. K. Shoichet J. K. Irwin Benchmarking Sets for Molecular Docking J. Med. Chem. 2006 49 6789 6801