Assessment of QM/MM scoring functions for molecular docking to HIV-1 protease

Journal of Chemical Information and Modeling

Volumn 49, Issue 4, 2009, Pages 913-924

  Fong, Pedro ^a   McNamara, Jonathan P ^a   Hillier, Ian H ^a   Bryce, Richard A ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMBER; BINDING ENERGY; POLARIZATION; QUANTUM THEORY;

AMBER FORCE-FIELD; ELECTROSTATIC COMPONENTS; GENERALIZED BORN; HIV-1 PROTEASE INHIBITORS; MOLECULAR DOCKING; PROTONATION STATE; QUANTUM MECHANICAL; SCORING FUNCTIONS;

LIGANDS;

PROTEINASE; PROTEINASE INHIBITOR;

ALGORITHM; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; ENZYMOLOGY; HUMAN IMMUNODEFICIENCY VIRUS 1; QUANTUM THEORY; STRUCTURE ACTIVITY RELATION;

ALGORITHMS; CATALYTIC DOMAIN; HIV PROTEASE; HIV PROTEASE INHIBITORS; HIV-1; MODELS, MOLECULAR; QUANTUM THEORY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 66149144253     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci800432s     Document Type: Article

References (59)

1. Bohm, H. J.; Stahl, M. The Use of Scoring Functions in Drug Discovery. In Reviews in Computational Chemistry; Lipkowitz, K. B., Boyd, D. B., Eds.; Wiley-VCH: Indianapolis, IN, 2002; Vol. 18, pp 41-87.
2. Ferrara, P.; Gohlke, H.; Price, D. J.; Klebe, G.; Brooks, C. L. Assessing Scoring Functions for Protein-Ligand Interactions. J. Med. Chem. 2004, 47, 3032-3047.
3. Wang, R. X.; Lu, Y. P.; Wang, S. M. Comparative Evaluation of 11 Scoring Functions for Molecular Docking. J. Med. Chem. 2003, 46, 2287-2303.
4. Muegge, I.; Martin, Y. C. A General and Fast Scoring Function for Protein-Ligand Interactions: A Simplified Potential Approach. J. Med. Chem. 1999, 42, 791-804.
5. Gohlke, H.; Hendlich, M.; Klebe, G. Knowledge-Based Scoring Function to Predict Protein-Ligand Interactions. J. Mol. Biol. 2000, 295, 337-356.
6. Eldridge, M. D.; Murray, C. W.; Auton, T. R.; Paolini, G. V.; Mee, R. P. Empirical Scoring Functions: I. The Development of a Fast Empirical Scoring Function to Estimate the Binding Affinity of Ligands in Receptor Complexes. J. Comput. -Aided Mol. Des. 1997, 11, 425-445.
7. Verdonk, M. L.; Cole, J. C.; Hartshorn, M. J.; Murray, C. W.; Taylor, R. D. Improved Protein-Ligand Docking Using GOLD. Proteins: Struct. Funct., Genet. 2003, 52, 609-623.
8. Case, D. A.; Cheatham, T. E.; Darden, T.; Gohlke, H.; Luo, R.; Merz, K. M.; Onufriev, A.; Simmerling, C.; Wang, B.; Woods, R. J. The Amber Biomolecular Simulation Programs. J. Comput. Chem. 2005, 26, 1668-1688.
9. Brooks, B. R.; Bruccoleri, R. E.; Olafson, B. D.; Swaminathan, S.; Karplus, M. CHARMM: A Program for Macromolecular Energy, Minimization, and Dynamics Calculations. J. Comput. Chem. 1983, 4, 187-217.
10. Beierlein, F.; Lanig, H.; Schurer, G.; Horn, A. H. C.; Clark, T. Quantum Mechanical/Molecular Mechanical (QM/MM) Docking: an Evaluation for Known Test Systems. Mol. Phys. 2003, 101, 2469-2480.
11. Friesner, R. A. Modeling Polarization in Proteins and Protein-Ligand Complexes: Methods and Preliminary Results. Adv. Protein Chem. 2006, 72, 79-104.
12. Grater, F.; Schwarzl, S. M.; Dejaegere, A.; Fischer, S.; Smith, J. C. Protein/Ligand Binding Free Energies Calculated With Quantum Mechanics/Molecular Mechanics. J. Phys. Chem. B 2005, 109, 10474-10483.
13. Khandelwal, A.; Balaz, S. Improved Estimation of Ligand-Macro-molecule Binding Affinities by Linear Response Approach Using a Combination of Multi-Mode MD Simulation and QM/MM Methods. J. Comvut.-Aided. Mol. Des. 2007, 21, 131-137.
14. Khandelwal, A.; Lukacova, V.; Comez, D.; Kroll, D. M.; Raha, S.; Balaz, S. A Combination of Docking, QM/MM Methods, and MD Simulation for Binding Affinity Estimation of Metalloprotein Ligands. J. Med. Chem. 2005, 48, 5437-5447.
15. Patel, S.; Brooks, C. L. CHARMM Fluctuating Charge Force Field for Proteins: I Parameterization and Application to Bulk Organic Liquid Simulations. J. Comput. Chem. 2004, 25, 1-15.
16. Vreven, T.; Byun, K. S.; Komaromi, I.; Dapprich, S.; Montgomery, J. A.; Morokuma, K.; Frisch, M. J. Combining Quantum Mechanics Methods With Molecular Mechanics Methods in ONIOM. J. Chem. Theory Comput. 2006, 2, 815-826.
17. Lin, H.; Truhlar, D. G. QM/MM: What Have We Learned, Where Are We, and Where Do We Go From Here. Theor. Chem. Acc. 2007, 117, 185-199.
18. Hensen, C.; Hermann, J. C.; Nam, K. H.; Ma, S. H.; Gao, J. L.; Holtje, H. D. A Combined QM/MM Approach to Protein-Ligand Interactions: Polarization Effects of the HIV-1 Protease on Selected High Affinity Inhibitors. J. Med. Chem. 2004, 47, 6673-6680.
19. Garcia-Viloca, M.; Alhambra, C.; Truhlar, D. G.; Gao, J. L. Importance of Substrate and Cofactor Polarization in the Active Site of Dihyro-folate Reductase. J. Comput. Chem. 2003, 24, 177-190.
20. * Parameters for Phosphorus, Sulfur and Chlorine. J. Mol. Model. 2003, 9, 408-414.
21. Stewart, J. J. P. Optimisation of Parameters for Semi-Empirical Methods. 2. Applications. J. Comput. Chem. 1989, 10, 221-264.
22. McNamara, J. P.; Hillier, I. H. Semi-Empirical Molecular Orbital Methods Including Dispersion Corrections for the Accurate Prediction of the Full Range of Intermolecular Interactions in Biomolecules. Phys. Chem. Chem. Phys. 2007, 9, 2362-2370.
23. Jones, G.; Willett, P.; Glen, R. C.; Leach, A. R.; Taylor, R. Development and Validation of a Genetic Algorithm for Flexible Docking. J. Mol. Biol. 1997, 267, 727-748.
24. Roche, O.; Kiyama, R.; Brooks, C. L. Ligand-Protein DataBase: Linking Protein-Ligand Complex Structures to Binding Data. J. Med. Chem. 2001, 44, 3592-3598.
25. Ala, P. J.; DeLoskey, R. J.; Huston, E. E.; Jadhav, P. K.; Lam, P. Y. S.; Eyermann, C. J.; Hodge, C. N.; Schadt, M. C.; Lewandowski, F. A.; Weber, P. C.; Mccabe, D. D.; Duke, J. L.; Chang, C. H. Molecular Recognition of Cyclic Urea HIV-1 Protease Inhibitors. J. Biol. Chem. 1998, 273, 12325-12331.
26. Hodge, C. N.; Aldrich, P. E.; Bacheler, L. T.; Chang, C. H.; Eyermann, C. J.; Garber, S.; Grubb, M.; Jackson, D. A.; Jadhav, P. K.; Korant, B.; Lam, P. Y. S.; Maurin, M. B.; Meek, J. L.; Otto, M. J.; Rayner, M. M.; Reid, C.; Sharpe, T. R.; Shum, L.; Winslow, D. L.; EricksonViitanen, S. Improved Cyclic Urea Inhibitors of the HIV-I Protease: Synthesis, Potency, Resistance Profile, Human Pharmaco-kinetics and X-Ray Crystal Structure of DMP 450. Chem. Biol. 1996, 3, 301-314.
27. Ala, P. J.; Huston, E. E.; Klabe, R. M.; Jadhav, P. K.; Lam, P. Y. S.; Chang, C. H. Counteracting HIV-1 Protease Drug Resistance: Structural Analysis of Mutant Proteases Complexed With XV638 and SD146, Cyclic Urea Amides With Broad Specificities. Biochemistry 1998, 37, 15042-15049.
28. Schaal, W.; Karlsson, A.; Ahlsen, G.; Lindberg, J.; Andersson, H. O.; Danielson, U. H.; Classon, B.; Unge, T.; Samuelsson, B.; Hulten, J.; Hallberg, A.; Karlen, A. Synthesis and Comparative Molecular Field Analysis (CoMFA) of Symmetric and Nonsymmetric Cyclic Sulfamide HIV-1 Protease Inhibitors. J. Med. Chem. 2001, 44, 155-169.
29. Thaisrivongs, S.; Skulnick, H. I.; Turner, S. R.; Strohbach, J. W.; Tommasi, R. A.; Johnson, P. D.; Aristoff, P. A.; Judge, T. M.; Gammill, R. B.; Morris, J. K.; Romines, K. R.; Chrusciel, R. A.; Hinshaw, R. R.; Chong, K. T.; Tarpley, W. G.; Poppe, S. M.; Slade, D. E.; Lynn, J. C.; Horng, M. M.; Tomich, P. K.; Seest, E. P.; Dolak, L. A.; Howe, W. J.; Howard, G. M.; Schwende, F. J.; Toth, L. N.; Padbury, G. E.; Wilson, G. J.; Shiou, L. H.; Zipp, G. L.; Wilkinson, K. F.; Rush, B. D.; Ruwart, M. J.; Koeplinger, K. A.; Zhao, Z. Y.; Cole, S.; Zaya, R. M.; Kakuk, T. J.; Janakiraman, M. N.; Watenpaugh, K. D. Structure-Based Design of HIV Protease Inhibitors: Sulfonamide-Containing 5,6-Dihydro-4-Hydroxy-2-Pyrones As Non-Peptidic Inhibitors. J. Med. Chem. 1996, 39, 4349-4353.
30. Smith, R.; Brereton, I. M.; Chai, R. Y.; Kent, S. B. H. Ionization States of the Catalytic Residues in HIV-1 Protease. Nat. Struct. Biol. 1996, 3, 946-950.
31. Yamazaki, T.; Nicholson, L. K.; Torchia, D. A.; Wingfield, P.; Stahl, S. J.; Kaufman, J. D.; Eyermann, C. J.; Hodge, C. N.; Lam, P. Y. S.; Ru, Y.; Jadhav, P. K.; Chang, C. H.; Weber, P. C. Nmr and X-Ray Evidence That the Hiv Protease Catalytic Aspartyl Groups Are Protonated in the Complex Formed by the Protease and A Nonpeptide Cyclic Urea-Based Inhibitor. J. Am. Chem. Soc. 1994, 116, 10791-10792.
32. Czodrowski, P.; Sotriffer, C. A.; Klebe, G. Atypical Protonation States in the Active Site of HIV-1 Protease: A Computational Study. J. Chem. Inf. Model. 2007, 47, 1590-1598.
33. Piana, S.; Sebastiani, D.; Carloni, P.; Parrinello, M. Ab Initio Molecular Dynamics-Based Assignment of the Protonation State of Pepstatin A/HIV-1 Protease Cleavage Site. J. Am. Chem. Soc. 2001, 123, 8730-8737.
34. Brik, A.; Wong, C. H. HIV-1 Protease: Mechanism and Drug Discovery. Org. Biomol. Chem. 2003, 1, 5-14.
35. Lam, P. Y. S.; Jadhav, P. K.; Eyermann, C. J.; Hodge, C. N.; Ru, Y.; Bacheler, L. T.; Meek, J. L.; Otto, M. J.; Rayner, M. M.; Wong, Y. N.; Chang, C. H.; Weber, P. C.; Jackson, D. A.; Sharpe, T. R.; EricksonViitanen, S. Rational Design of Potent, Bioavailable, Nonpeptide Cyclic Ureas As Hiv Protease Inhibitors. Science 1994, 263, 380-384.
36. Hyland, L. J.; Tomaszek, T. A.; Meek, T. D. Human Immunodeficiency Virus-1 Protease. 2. Use of Ph Rate Studies and Solvent Kinetic Isotope Effects to Elucidate Details of Chemical Mechanism. Biochemistry 1991, 30, 8454-8463.
37. Hou, T.; McLaughlin, W. A.; Wang, W. Evaluating the Potency of HIV-1 Protease Drugs to Combat Resistance. Proteins: Struct. Funct., Bioinf. 2008, 71, 1163-1174.
38. Cornell, W. D.; Cieplak, P.; Bayly, C. I.; Gould, I. R.; Merz, K. M.; Ferguson, D. M.; Spellmeyer, D. C.; Fox, T.; Caldwell, J. W.; Kollman, P. A. A 2Nd Generation Force-Field for the Simulation of Proteins, Nucleic-Acids, and Organic-Molecules. J. Comput. Chem. 1995, 117, 5179-5197.
39. Onufriev, A.; Bashford, D.; Case, D. A. Exploring Protein Native States and Large-Scale Conformational Changes With a Modified Generalized Born Model. Proteins: Struct. Funct., Bioinf. 2004, 55, 383-394.
40. Maseras, F.; Morokuma, K. Imomm - A New Integrated Ab-Initio Plus Molecular Mechanics Geometry Optimization Scheme of Equilibrium Structures and Transition-States. J. Comput. Chem. 1995, 16, 1170-1179.
41. Svensson, M.; Humbel, S.; Froese, R. D. J.; Matsubara, T.; Sieber, S.; Morokuma, K. ONIOM: A Multilayered Integrated MO+MM Method for Geometry Optimizations and Single Point Energy Predictions. A Test for Diels-Alder Reactions and Pt(P(t-Bu)(3))(2)+H-2 Oxidative Addition. J. Phys. Chem. 1996, 100, 19357-19363.
42. Waszkowycz, B.; Hillier, I. H.; Gensmantel, N.; Payling, D. W. A Quantum Mechanical/Molecular Mechanical Model of Inhibition of the Enzyme Phospholipase A2. J. Chem. Soc, Perkin Trans. 2 1991, 18199-1832.
43. Grimme, S. Accurate Description of Van Der Waals Complexes by Density Functional Theory Including Empirical Corrections. J. Comput. Chem. 2004, 25, 1463-1473.
44. Mohr, M.; McNamara, J. P.; Wang, H.; Rajeev, S. A.; Ge, J.; Morgado, C. A.; Hillier, I. H. The Use of Methods Involving Semi-Empirical Molecular Orbital Theory to Study the Structure and Reactivity of Transition Metal Complexes. Faraday Discuss. 2003, 124, 413-428.
45. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Montgomery, J. A., Jr.; Vreven, T.; Kudin, K. N.; Burant, J. C.; Millam, J. M.; Iyengar, S. S.; Tomasi, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Ayala, P. Y.; Morokuma, K.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Zakrzewski, V. G.; Dapprich, S.; Daniels, A. D.; Strain, M. C.; Farkas, O.; Malick, D. K.; Rabuck, A. D.; Raghavachari, K.; Foresman, J. B.; Ortiz, J. V.; Cui, Q.; Baboul, A. G.; Clifford, S.; Cioslowski, J.; Stefanov, B. B.; Liu, G.; Liashenko, A.; Piskorz, P.; Komaromi, L.; Martin, R. L.; Fox, D. J.; Keith, T.; Al-Laham, M. A.; Peng, C. Y.; Nanayakkara, A.; Challacombe, M.; Gill, P. M. W.; Johnson, B.; Chen, W.; Wong, M. W.; Gonzalez, C.; Pople, J. A. Gaussian 03; Gaussian, Inc.: Wallingford, CT, 2004.
46. Wang, J. M.; Wang, W.; Kollman, P. A.; Case, D. A. Automatic Atom Type and Bond Type Perception in Molecular Mechanical Calculations. J. Mol. Graphics Modell. 2006, 25, 247-260.
47. Case, D. A.; Cheatham, T. E.; Darden, T.; Gohlke, H.; Luo, R.; Merz, K. M.; Onufriev, A.; Simmerling, C.; Wang, B.; Woods, R. The Amber Biomolecular Simulation Programs. J. Comput. Chem. 2005, 26, 1668-1688.
48. Jakalian, A.; Jack, D. B.; Bayly, C. I. Fast, Efficient Generation of High-Quality Atomic Charges. AM1-BCC Model: II. Parameterization and Validation. J. Comput. Chem. 2002, 23, 1623-1641.
49. Mongan, J.; Simmerling, C.; McCammon, J. A.; Case, D. A.; Onufriev, A. Generalized Born Model With a Simple, Robust Molecular Volume Correction. J. Chem. Theory Comput. 2007, 3, 156-169.
50. Gao, J. L.; Xia, X. F. A Priori Evaluation of Aqueous Polarization Effects Through Monte-Carlo QM-MM Simulations. Science 1992, 258, 631-635.
51. Vieth, M.; Hirst, J. D.; Kolinski, A.; Brooks, C. L. Assessing Energy Functions for Flexible Docking. J. Comput. Chem. 1998, 19, 1612-1622.
52. Chen, H.; Lyne, P. D.; Giordanetto, F.; Lovell, T.; Li, J. On Evaluating Molecular-Docking Methods for Pose Prediction and Enrichment Factors. J. Chem. Inf. Model. 2006, 46, 401-415.
53. Schechter, I.; Berger, A. On Size of Active Site in Proteases. I. Papain. Biochem. Biophys. Res. Commun. 1967, 27, 157-162.
54. Wlodawer, A.; Erickson, J. W. Structure-Based Inhibitors of HIV-1 Protease. Annu. Rev. Biochem. 1993, 62, 543-585.
55. MacKerell, A. D.; Bashford, D.; Bellott, M.; Dunbrack, R. L.; Evanseck, J. D.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S.; Joseph-McCarthy, D.; Kuchnir, L.; Kuczera, K.; Lau, F. T. K.; Mattos, C.; Michnick, S.; Ngo, T.; Nguyen, D. T.; Prodhom, B.; Reiher, W. E.; Roux, B.; Schlenkrich, M.; Smith, J. C.; Stote, R.; Sträub, J.; Watanabe, M.; Wiorkiewicz-Kuczera, J.; Yin, D.; Karplus, M. All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins. J. Phys. Chem. B 1998, 102, 3586-3616.
56. Case, D. A.; Darden, T.; Cheatham, T. E., III; Simmerling, C. L.; Wang, J.; Duke, R.; Luo, R.; Merz, K. M., Jr.; Wang, B.; Pearlman, D. A.; Crowley, M.; Brozell, S.; Tsui, V.; Gohlke, H.; Mongan, J.; Hornak, V.; Cui, G.; Beroza, P.; Schafmeister, C.; Caldwell, J. W.; Ross, W. S.; Kollman, P. A. AMBER 8.0; University of California: San Francisco, CA, 2004.
57. Ewing, T. J. A.; Kuntz, I. D. Critical Evaluation of Search Algorithms for Automated Molecular Docking and Database Screening. J. Comput. Chem. 1997, 18, 1175-1189.
58. Todorov, N. P.; Monthoux, P. H.; Alberts, I. L. The Influence of Variations of Ligand Protonation State and Tautomerism on Protein-Ligand Recognition and Binding Energy Landscape. J. Chem. Inf. Model. 2006, 46, 1134-1142.
59. Pellegrini, E.; Field, M. J. A Generalized-Born Solvation Model for Macromolecular Hybrid-Potential Calculations. J. Phys. Chem. A 2002, 106, 1316-1326.