Bridging quantum mechanics and structure-based drug design

Frontiers in Bioscience

Volumn 16, Issue 5, 2011, Pages 1619-1633

  De Vivo, Marco ^a  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

Computational chemistry; Drug discovery; Enzymatic catalysis; Metallo beta lactamases; Metalloenzymes; MM; Modeling; Molecular mechanics; Phosphoryl transfer; QM; Quantum mechanics; Review; Ribonuclease H; SBDD; Soluble epoxide hydrolase; Structure based drug design

Indexed keywords

BETA LACTAMASE; EPOXIDE HYDROLASE; LIGAND; MAGNESIUM; PHOSPHOTRANSFERASE; RIBONUCLEASE H; ZINC;

DRUG DESIGN; METABOLISM; QUANTUM THEORY; REVIEW; STRUCTURE ACTIVITY RELATION;

BETA-LACTAMASES; DRUG DESIGN; EPOXIDE HYDROLASES; LIGANDS; MAGNESIUM; PHOSPHOTRANSFERASES; QUANTUM THEORY; RIBONUCLEASE H; STRUCTURE-ACTIVITY RELATIONSHIP; ZINC;

EID: 79955045990     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/3809     Document Type: Article

References (91)

1. N. H. March and C. C. Matthai: The application of quantum chemistry and condensed matter theory in studying amino-acids, protein folding and anticancer drug technology. Theor. Chem. Acc., 125(3-6), 193-201(2009)
2. W. L. Jorgensen: The many roles of computation in drug discovery. Science, 303(5665), 1813-1818 (2004) (Pubitemid 38374866)
3. T. Zhou, D. Huang and A. Caflisch: Quantum mechanical methods for drug design. Curr Top Med Chem, 10(1), 33-45 (2010)
4. A. Cavalli, P. Carloni and M. Recanatini: Target-related applications of first principles quantum chemical methods in drug design. Chem Rev, 106(9), 3497-519 (2006) (Pubitemid 44560452)
5. M. B. Peters, K. Raha and K. M. Merz: Quantum mechanics in structure-based drug design. Current Opinion in Drug Discovery & Development, 9(3), 370-379 (2006) (Pubitemid 43778684)
6. K. Raha, M. B. Peters, B. Wang, N. Yu, A. M. WollaCott, L. M. Westerhoff and K. M. Merz: The role of quantum mechanics in structure-based drug design. Drug Discov. Today, 12(17-18), 725-731 (2007) (Pubitemid 47364833)
7. E. G. Occhiato, A. Ferrali, G. Menchi, A. Guarna, G. Danza, A. Comerci, R. Mancina, M. Serio, G. Garotta, A. Cavalli, M. De Vivo and M. Recanatini: Synthesis, biological activity, and three-dimensional quantitative structure-activity relationship model for a series of benzo[c]quinolizin-3-ones nonsteroidal inhibitors of human steroid 5 alpha-reductase 1. J. Med. Chem., 47(14), 3546-3560 (2004) (Pubitemid 38822016)
8. P. P. Singh, H. K. Srivastava and F. A. Pasha: DFTbased QSAR study of testosterone and its derivatives. Biorg. Med. Chem., 12(1), 171-177 (2004) (Pubitemid 38096229)
9. A. Khandelwal, V. Lukacova, D. Comez, D. M. Kroll, S. Raha and S. Balaz: A combination of docking, QM/MM methods, and MD simulation for binding affinity estimation of metalloprotein ligands. J. Med. Chem., 48(17), 5437-5447 (2005) (Pubitemid 41209242)
10. F. Grater, S. M. Schwarzl, A. Dejaegere, S. Fischer and J. C. Smith: Protein/ligand binding free energies calculated with quantum mechanics/molecular mechanics. J. Phys. Chem. B, 109(20), 10474-10483 (2005) (Pubitemid 40786114)
11. K. Raha and K. M. Merz: A quantum mechanics-based scoring function: Study of zinc ion-mediated ligand binding. J. Am. Chem. Soc., 126(4), 1020-1021 (2004) (Pubitemid 38140722)
12. V. Vasilyev and A. Bliznyuk: Application of semiempirical quantum chemical methods as a scoring function in docking. Theor. Chem. Acc., 112(4), 313-317 (2004) (Pubitemid 39329354)
13. V. Gogonea, D. Suarez, A. van der Vaart and K. W. Merz: New developments in applying quantum mechanics to proteins. Curr. Opin. Struct. Biol., 11(2), 217-223 (2001) (Pubitemid 32289425)
14. J. Khandogin and D. M. York: Quantum descriptors for biological macromolecules from linear-scaling electronic structure methods. Proteins-Structure Function and Bioinformatics, 56(4), 724-737 (2004) (Pubitemid 39063316)
15. M. Dal Peraro, A. J. Vila and P. Carloni: Structural determinants and hydrogen-bond network of the mononuclear zinc(II)-beta-lactamase active site. J. Biol. Inorg. Chem., 7(7-8), 704-712 (2002) (Pubitemid 36061236)
16. M. Dal Peraro, A. J. Vila and P. Carloni: Protonation state of Asp120 in the binuclear active site of the metallobeta-lactamase from Bacteroides fragilis. Inorg. Chem., 42(14), 4245-4247 (2003)
17. N. Yu, S. A. Hayik, B. Wang, N. Liao, C. H. Reynolds and K. M. Merz: Assigning the protonation states of the key aspartates in beta-secretase using QM/MM X-ray structure refinement. Journal of Chemical Theory and Computation, 2(4), 1057-1069 (2006)
18. V. L. Schramm: Enzymatic transition states and transition state analogues. Curr. Opin. Struct. Biol., 15(6), 604-613 (2005) (Pubitemid 41668515)
19. H. M. Senn and W. Thiel: QM/MM Methods for Biomolecular Systems. Angewandte Chemie-International Edition, 48(7), 1198-1229 (2009)
20. M. Garcia-Viloca, J. Gao, M. Karplus and D. G. Truhlar: How enzymes work: Analysis by modern rate theory and computer simulations. Science, 303(5655), 186-195 (2004) (Pubitemid 38057561)
21. A. Warshel: Computer simulations of enzyme catalysis: Methods, progress, and insights. Annu. Rev. Biophys. Biomol. Struct., 32, 425-443 (2003) (Pubitemid 37056236)
22. A. Warshel and M. Levitt: Theoretical Studies of Enzymic Reactions - Dielectric, Electrostatic and Steric Stabilization of Carbonium-Ion in Reaction of Lysozyme. J. Mol. Biol., 103(2), 227-249 (1976)
23. O. Acevedo and W. L. Jorgensen: Advances in quantum and molecular mechanical (QM/MM) simulations for organic and enzymatic reactions. Acc Chem Res, 43(1), 142-51 (2010)
24. J. L. Gao and D. G. Truhlar: Quantum mechanical methods for enzyme kinetics. Annu. Rev. Phys. Chem., 53, 467-505 (2002)
25. R. A. Friesner and V. Guallar: Ab initio quantum chemical and mixed quantum mechanics/molecular mechanics (QM/MM) methods for studying enzymatic catalysis. Annu. Rev. Phys. Chem., 56, 389-427 (2005) (Pubitemid 41156883)
26. A. J. Mulholland: Modelling enzyme reaction mechanisms, specificity and catalysis. Drug Discov. Today, 10(20), 1393-1402 (2005) (Pubitemid 41501794)
27. P. Carloni, U. Rothlisberger and M. Parrinello: The role and perspective of a initio molecular dynamics in the study of biological systems. Acc. Chem. Res., 35(6), 455-464 (2002)
28. M. Dal Peraro, P. Ruggerone, S. Raugei, F. L. Gervasio and P. Carloni: Investigating biological systems using first principles Car-Parrinello molecular dynamics simulations. Curr Opin Struct Biol, 17(2), 149-56 (2007) (Pubitemid 46575263)
29. A. R. Leach: Molecular modeling. Principles and applications. Addison-Wesley: Reading, MA (1996)
30. F. Jensen: Introduction to computational chemistry. John iley and Sons: New York (1999)
31. C. J. Cramer: Esentials of computational chemistry: theories and models. John Wiley and Sons: New York (2004)
32. C. Moller and M. S. Plesset: Note on an approximation treatment for many-electron systems. Physical Review, 46(7), 0618-0622 (1934)
33. R. Car: Introduction to density-functional theory and abinitio molecular dynamics. Quant. Struct.-Act. Relat., 21(2), 97-104 (2002) (Pubitemid 34847487)
34. P. Hohenberg and W. Kohn: Inhomogeneous electron gas. Physical Review B, 136(3B), B864-& (1964)
35. W. Kohn and L. J. Sham: Self-consistent equations including exchange and correlation effects. Physical Review, 140(4A), 1133-& (1965)
36. A. D. Becke: Density-Functional Exchange-Energy Approximation with Correct Asymptotic-Behavior. Physical Review A, 38(6), 3098-3100 (1988)
37. C. T. Lee, W. T. Yang and R. G. Parr: Development of the Colle-Salvetti Correlation-Energy Formula into a Functional of the Electron-Density. Physical Review B, 37(2), 785-789 (1988)
38. A. D. Becke: A new mixing of hartree-fock and local density-functional theories. J. Chem. Phys., 98(2), 1372-1377 (1993)
39. S. H. Vosko, L. Wilk and M. Nusair: Accurate spindependent electron liquid correlation energies for local spindensity calculations - a critical analysis. Can. J. Phys., 58(8), 1200-1211 (1980)
40. R. Car and M. Parrinello: Unified Approach for Molecular-Dynamics and Density-Functional Theory. Phys. Rev. Lett., 55(22), 2471-2474 (1985)
41. L. N. Johnson and R. J. Lewis: Structural basis for control by phosphorylation. Chem Rev, 101(8), 2209-42 (2001) (Pubitemid 35373017)
42. P. P. Dzeja and A. Terzic: Phosphotransfer networks and cellular energetics. J. Exp. Biol., 206(12), 2039-2047 (2003) (Pubitemid 36761807)
43. J. F. Morrison and E. Heyde: Enzymic Phosphoryl Group Transfer. Annu. Rev. Biochem., 41, 29-& (1972)
44. J. R. Knowles: Enzyme-Catalyzed Phosphoryl Transfer-Reactions. Annu. Rev. Biochem., 49, 877-919 (1980)
45. P. J. Kennelly: Protein phosphatases-a phylogenetic perspective. Chem Rev, 101(8), 2291-312 (2001)
46. M. D. Jackson and J. M. Denu: Molecular reactions of protein phosphatases - Insights from structure and chemistry. Chem. Rev., 101(8), 2313-2340 (2001) (Pubitemid 35373021)
47. S. D. Lahiri, G. F. Zhang, D. Dunaway-Mariano and K. N. Allen: The pentacovalent phosphorus intermediate of a phosphoryl transfer reaction. Science, 299(5615), 2067-2071 (2003) (Pubitemid 36383733)
48. C. M. Dupureur: Roles of metal ions in nucleases. Curr. Opin. Chem. Biol., 12(2), 250-255 (2008)
49. J. A. Cowan: Chemical nucleases. Curr. Opin. Chem. Biol., 5(6), 634-642 (2001) (Pubitemid 33153159)
50. S. Broccoli, F. Rallu, P. Sanscartier, S. M. Cerritelli, R. J. Crouch and M. Drolet: Effects of RNA polymerase modifications on transcription-induced negative supercoiling and associated R-loop formation. Mol Microbiol, 52(6), 1769-79 (2004) (Pubitemid 38822684)
51. W. Yang, J. Y. Lee and M. Nowotny: Making and breaking nucleic acids: two-Mg2+-ion catalysis and substrate specificity. Mol Cell, 22(1), 5-13 (2006)
52. M. Nowotny, S. M. Cerritelli, R. Ghirlando, S. A. Gaidamakov, R. J. Crouch and W. Yang: Specific recognition of RNA/DNA hybrid and enhancement of human RNase H1 activity by HBD. Embo J, 27(7), 1172-81 (2008) (Pubitemid 351508154)
53. M. Nowotny, S. A. Gaidamakov, R. J. Crouch and W. Yang: Crystal structures of RNase H bound to an RNA/DNA hybrid: substrate specificity and metal-dependent catalysis. Cell, 121(7), 1005-16 (2005) (Pubitemid 40884393)
54. M. Nowotny, S. A. Gaidamakov, R. Ghirlando, S. M. Cerritelli, R. J. Crouch and W. Yang: Structure of human RNase H1 complexed with an RNA/DNA hybrid: insight into HIV reverse transcription. Mol Cell, 28(2), 264-76 (2007) (Pubitemid 47599996)
55. M. Nowotny and W. Yang: Stepwise analyses of metal ions in RNase H catalysis from substrate destabilization to product release. Embo J, 25(9), 1924-33 (2006)
56. K. Klumpp, J. Q. Hang, S. Rajendran, Y. Yang, A. Derosier, P. Wong Kai In, H. Overton, K. E. Parkes, N. Cammack and J. A. Martin: Two-metal ion mechanism of RNA cleavage by HIV RNase H and mechanism-based design of selective HIV RNase H inhibitors. Nucleic Acids Res, 31(23), 6852-9 (2003) (Pubitemid 37508792)
57. C. A. Shaw-Reid, B. Feuston, V. Munshi, K. Getty, J. Krueger, D. J. Hazuda, M. A. Parniak, M. D. Miller and D. Lewis: Dissecting the effects of DNA polymerase and ribonuclease H inhibitor combinations on HIV-1 reversetranscriptase activities. Biochemistry, 44(5), 1595-606 (2005) (Pubitemid 40204402)
58. A. Laio, J. VandeVondele and U. Rothlisberger: A Hamiltonian electrostatic coupling scheme for hybrid Car- Parrinello molecular dynamics simulations. J. Chem. Phys., 116(16), 6941-6947 (2002) (Pubitemid 34537077)
59. M. De Vivo, M. Dal Peraro and M. L. Klein: Phosphodiester cleavage in ribonuclease H occurs via an associative two-metal-aided catalytic mechanism. J. Am. Chem. Soc., 130(33), 10955-10962 (2008)
60. B. Elsasser, M. Valiev and J. H. Weare: A Dianionic Phosphorane Intermediate and Transition States in an Associative A(N)+D-N Mechanism for the RibonucleaseA Hydrolysis Reaction. J. Am. Chem. Soc., 131(11), 3869 (2009)
61. M. De Vivo, B. Ensing, M. Dal Peraro, G. A. Gomez, D. W. Christianson and M. L. Klein: Proton shuttles and phosphatase activity in soluble epoxide hydrolase. J. Am. Chem. Soc., 129(2), 387-394 (2007) (Pubitemid 46106639)
62. M. De Vivo, B. Ensing and M. L. Klein: Computational study of phosphatase activity in soluble epoxide hydrolase: High efficiency through a water bridge mediated proton shuttle. J. Am. Chem. Soc., 127(32), 11226-11227 (2005) (Pubitemid 41176867)
63. E. Rosta, H. L. Woodcock, B. R. Brooks and G. Hummer: Artificial Reaction Coordinate "Tunneling" in Free-Energy Calculations: The Catalytic Reaction of RNase H. J. Comput. Chem., 30(11), 1634-1641 (2009)
64. I. Ivanov, J. A. Tainer and J. A. McCammon: Unraveling the three-metal-ion catalytic mechanism of the DNA repair enzyme endonuclease IV. Proc Natl Acad Sci U S A, 104(5), 1465-70 (2007) (Pubitemid 46214613)
65. F. Leclerc and M. Karplus: Two-metal-ion mechanism for hammerhead-ribozyme catalysis. J. Phys. Chem. B, 110(7), 3395-3409 (2006)
66. M. Boero, M. Tateno, K. Terakura and A. Oshiyama: Double-metal-ion/ single-metal-ion mechanisms of the cleavage reaction of ribozymes: First-principles molecular dynamics simulations of a fully hydrated model system. Journal of Chemical Theory and Computation, 1(5), 925-934 (2005)
67. N. C. Horton and J. J. Perona: DNA cleavage by EcoRV endonuclease: Two metal ions in three metal ion binding sites. Biochemistry, 43(22), 6841-6857 (2004) (Pubitemid 38720502)
68. K. R. Schmelzer, L. Kubala, J. W. Newman, I. H. Kim, J. P. Eiserich and B. D. Hammock: Soluble epoxide hydrolase is a therapeutic target for acute inflammation. Proceedings of the National Academy of Sciences of the United States of America, 102(28), 9772-9777 (2005) (Pubitemid 40993644)
69. M. F. Moghaddam, D. F. Grant, J. M. Cheek, J. F. Greene, K. C. Williamson and B. D. Hammock: Bioactivation of leukotoxins to their toxic diols by epoxide hydrolase. Nat. Med., 3(5), 562-566 (1997) (Pubitemid 27198657)
70. K. Node, Y. Q. Huo, X. L. Ruan, B. C. Yang, M. Spiecker, K. Ley, D. C. Zeldin and J. K. Liao: Antiinflammatory properties of cytochrome P450 epoxygenasederived eicosanoids. Science, 285(5431), 1276-1279 (1999) (Pubitemid 29398616)
71. A. Cronin, S. Mowbray, H. Durk, S. Homburg, I. Fleming, B. Fisslthaler, F. Oesch and M. Arand: The Nterminal domain of mammalian soluble epoxide hydrolase is a phosphatase. Proceedings of the National Academy of Sciences of the United States of America, 100(4), 1552-1557 (2003) (Pubitemid 36254485)
72. J. W. Newman, C. Morisseau and B. D. Hammock: Epoxide hydrolases: their roles and interactions with lipid metabolism. Prog. Lipid Res., 44(1), 1-51 (2005) (Pubitemid 40313218)
73. G. A. Gomez, C. Morisseau, B. D. Hammock and D. W. Christianson: Structure of human epoxide hydrolase reveals mechanistic inferences on bifunctional catalysis in epoxide and phosphate ester hydrolysis. Biochemistry, 43(16), 4716-4723 (2004) (Pubitemid 38509092)
74. M. De Vivo, A. Cavalli, P. Carloni and M. Recanatini: Computational study of the phosphoryl transfer catalyzed by a cyclin-dependent kinase. Chemistry, 13(30), 8437-44 (2007) (Pubitemid 47608879)
75. P. Cohen: Protein kinases - the major drug targets of the twenty-first century? Nature Reviews Drug Discovery, 1(4), 309-315 (2002) (Pubitemid 37361447)
76. S. Re, J. Jung, S. Ten-no and Y. Sugita: A twodimensional energy surface of the phosphoryl transfer reaction catalyzed by phosphoserine phosphatase. Chem. Phys. Lett., 480(4-6), 284-288 (2009)
77. V. Lopez-Canut, S. Marti, J. Bertran, V. Moliner and I. Tunon: Theoretical Modeling of the Reaction Mechanism of Phosphate Monoester Hydrolysis in Alkaline Phosphatase. J. Phys. Chem. B, 113(22), 7816-7824 (2009)
78. C. Jardin, A. H. C. Horn, G. Schurer and H. Sticht: Insight into the Phosphoryl Transfer of the Escherichia coli Glucose Phosphotransferase System from QM/MM Simulations. J. Phys. Chem. B, 112(42), 13391-13400 (2008)
79. M. H. Ho, M. De Vivo, M. Dal Peraro and M. L. Klein: Unraveling the Catalytic Pathway of Metalloenzyme Farnesyltransferase through QM/MM Computation. Journal of Chemical Theory and Computation, 5(6), 1657-1666 (2009)
80. M. Klahn, E. Rosta and A. Warshel: On the mechanism of hydrolysis of phosphate monoesters dianions in solutions and proteins. J. Am. Chem. Soc., 128(47), 15310-15323 (2006) (Pubitemid 44853542)
81. A. Cavalli and P. Carloni: Enzymatic GTP hydrolysis: Insights from an ab initio molecular dynamics study. J. Am. Chem. Soc., 124(14), 3763-3768 (2002) (Pubitemid 34407897)
82. B. L. Grigorenko, A. V. Nemukhin, R. E. Cachau, I. A. Topol and S. K. Burt: Computational study of a transition state analog of phosphoryl transfer in the Ras-RasGAP complex: AlFx versus MgF3. J. Mol. Model., 11(6), 503-508 (2005) (Pubitemid 41829672)
83. J. F. Fisher, S. O. Meroueh and S. Mobashery: Bacterial resistance to beta-lactam antibiotics: Compelling opportunism, compelling opportunity. Chem. Rev., 105(2), 395-424 (2005) (Pubitemid 40351628)
84. T. R. Walsh, M. A. Toleman, L. Poirel and P. ordmann: Metallo-beta-lactamases: the quiet before the storm? Clin. Microbiol. Rev., 18(2), 306 (2005)
85. F. Simona, A. Magistrato, M. Dal Peraro, A. Cavalli, A. J. Vila and P. Carloni: Common Mechanistic Features among Metallo-beta-lactamases A computational study of aeromonas hydrophila cpha enzyme. J. Biol. Chem., 284(41), 28164-28171 (2009)
86. J. Moran-Barrio, J. M. Gonzalez, M. N. Lisa, A. L. Costello, M. Dal Peraro, P. Carloni, B. Bennett, D. L. Tierney, A. S. Limansky, A. M. Viale and A. J. Vila: The metallo-ss-lactamase GOB is a mono-Zn(II) enzyme with a novel active site. J. Biol. Chem., 282(25), 18286-18293 (2007) (Pubitemid 47100218)
87. M. Dal Peraro, L. I. Llarrull, U. Rothlisberger, A. J. Vila and P. Carloni: Water-assisted reaction mechanism of monozinc beta-lactamases. J. Am. Chem. Soc., 126(39), 12661-12668 (2004) (Pubitemid 39310535)
88. M. Dal Peraro, A. J. Vila and P. Carloni: Substrate binding to mononuclear metallo-beta-lactamase from Bacillus cereus. Proteins-Structure Function and Genetics, 54(3), 412-423 (2004) (Pubitemid 38202184)
89. M. Dal Peraro, A. J. Vila, P. Carloni and M. L. Klein: Role of zinc content on the catalytic efficiency of B1 metallo beta-lactamases. J. Am. Chem. Soc., 129(10), 2808-2816 (2007) (Pubitemid 46417956)
90. H. Park, E. N. Brothers and K. M. Merz: Hybrid QM/MM and DIFT investigations of the catalytic mechanism and inhibition of the dinuclear zinc metallobeta- lactamase CcrA from Bacteroides fragilis. J. Am. Chem. Soc., 127(12), 4232-4241 (2005) (Pubitemid 40463048)
91. D. Xu, H. Guo and G. Cui: Antibiotic deactivation by a dizinc beta-lactamase: Mechanistic insights from QM/MM and DFT studies. J. Am. Chem. Soc., 129(35), 10814-10822 (2007) (Pubitemid 350067492)