Mixed quantum mechanics and molecular mechanics methods: Looking inside proteins

Wiley Interdisciplinary Reviews: Computational Molecular Science

Volumn 1, Issue 2, 2011, Pages 315-322

  Wallrapp, Frank H ^a   Guallar, Victor ^a  

^a BARCELONA SUPERCOMPUTING CENTER   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AB INITIO; ACTIVE SITE; CHEMICAL PROCESS; CONFORMATIONAL SAMPLINGS; MIXED QUANTUM MECHANICS; MOLECULAR MECHANICS METHOD;

ENZYMES; MOLECULAR MECHANICS; PROTEINS;

QUANTUM THEORY;

EID: 84860269412     PISSN: 17590876     EISSN: 17590884     Source Type: Journal    
DOI: 10.1002/wcms.27     Document Type: Review

References (75)

1. Warshel A, Levitt MA. Theoretical studies of enzymic reactions: dielectric, electrostatic and steric stabilization of the carbonium ion in the reaction of lysozyme. J Mol Biol 1976, 103: 227-249.
2. Warshel A, Karplus M. Calculation of ground and excited state potential surfaces of conjugated molecules. I. Formulation and parametrization. J Am Chem Soc 1972, 94: 5612-5625. doi:10.1021/ja00771a014.
3. Brooks B, Karplus M. Harmonic dynamics of proteins: normal modes and fluctuations in bovine pancreatic trypsin inhibitor. PNAS 1983, 80: 6571-6575.
4. Klepeis JL, Lindorff-Larsen K, Dror RO, Shaw DE. Long-timescale molecular dynamics simulations of protein structure and function. Curr Opin Struc Biol 2009, 19: 120-127. doi:10.1016/j.sbi.2009.03.004.
5. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kalé L, Schulten K. Scalable molecular dynamics with NAMD. J Comput Chem 2005, 26: 1781-1802.
6. Hess B, Kutzner C, Van Der Spoel D, Lindahl E. GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theory Comput 2008, 4: 435-447, doi:10.1021/ct700301q.
7. Li ZQ, Scheraga HA. Monte Carlo -minimization approach to the multiple-minima problem in protein folding. Proc Natl Acad Sci U S A 1987, 84: 2633-2636.
8. Ulmschneider JP, Jorgensen WL. Monte Carlo backbone sampling for polypeptides with variable bond angles and dihedral angles using concerted rotations and a Gaussian bias. J Chem Phys 2003, 118: 4261-4271.
9. Evans DA, Wales DJ. Free energy landscapes of model peptides and proteins. J Chem Phys 2003, 118: 3891-3897.
10. Borrelli KW, Vitalis A, Alcantara R, Guallar V. PELE: protein energy landscape exploration. A novel Monte Carlo based technique. J Chem Theory Comput 2005, 1: 1304-1311.
11. Jacobson MP, Pincus DL, Rapp CS, Tyler JF, Honig B, Shaw DE, Friesner RA. A hierarchical approach to all-atom protein loop prediction. Proteins 2004, 55: 351-367.
12. Ruiz-Pernia JJ, Silla E, Tunon I, Marti S, Moliner V. Hybrid QM/MM potentials of mean force with interpolated corrections. J Phys Chem B 2004, 108: 8427-8433, doi:10.1021/jp049633g.
13. Hu H, Lu ZY, Yang WT. QM/MM minimum free-energy path: methodology and application to triosephosphate isomerase. J Chem Theory Comput 2007, 3: 390-406, doi:10.1021/ct600240y.
14. Solt I, Kulhanek P, Simon I, Winfield S, Payne MC, Csanyi G, Fuxreiter M. Evaluating boundary dependent errors in QM/MM simulations. J Phys Chem B 2009, 113: 5728-5735, doi:10.1021/jp807277r.
15. Sumowski CV, Ochsenfeld CA. Convergence study of QM/MM isomerization energies with the selected size of the QM region for peptidic systems. J Phys Chem A 2009, 113: 11734-11741.
16. Schwartz SD, Schramm VL. Enzymatic transition states and dynamic motion in barrier crossing. Nat Chem Biol 2009, 5: 551-558.
17. Sgrignani J, Bonaccini C, Grazioso G, Chioccioli M, Cavalli A, Gratteri P. Insights into docking and scoring neuronal alpha 4 beta 2 nicotinic receptor agonists using molecular dynamics simulations and QM/MM calculations. J Comput Chem 2009, 30:2443-2454, doi:10.1002/jcc.21251.
18. Mukherjee P, Desai PV, Srivastava A, Tekwani BL, Avery MA. Probing the structures of leishmanial farnesyl pyrophosphate synthases: Homology modeling and docking studies. J Chem Inf Model 2008, 48: 1026-1040, doi:10.1021/ci700355z.
19. Abdel-Halim H, Hanrahan JR, Hibbs DE, Johnston GAR, Chebib M. A molecular basis for agonist and antagonist actions at GABA(C) receptors. Chem Biol Drug Des 2008, 71: 306-327, doi:10.1111/j.1747.0285.2008.00642.x.
20. Guallar V, Olsen B. The role of the heme propionates in heme biochemistry. J Inorg Biochem 2006, 100: 755-760.
21. Maragakis P, Lindorff-Larsen K, Eastwood MP, Dror, RO, Klepeis JL, Arkin IT, Jensen MO, Xu HF, Trbovic N, Friesner RA. et al. Microsecond molecular dynamics simulation shows effect of slow loop dynamics on backbone amide order parameters of proteins. J Phys Chem B 2008, 112, 6155-6158, doi:10.1021/jp077018h.
22. Lee EH, Hsin J, Sotomayor M, Comellas G, Schulten K. Discovery through the computational microscope. Structure 2009, 17: 1295-1306, doi:10.1016/j.str.2009.09.001.
23. Karplus M, Kuriyan J. Molecular dynamics and protein function. Proc Natl Acad Sci U S A 2005, 102: 6679-6685, doi:10.1073/pnas.0408930102.
24. Zhang YK, Kua J, McCammon JA. Influence of structural fluctuation on enzyme reaction energy barriers in combined quantum mechanical/molecular mechancal studies. J Phys Chem B 2003, 107: 4459-4463.
25. Klahn M, Braun-Sand S, Rosta E, Warshel A. On possible pitfalls in ab initio quantum mechanics/molecular mechanics minimization approaches for studies of enzymatic reactions. J Phys Chem B 2005, 109: 15645-15650, doi:10.1021/jp0521757.
26. Lodola A, Mor M, Zurek J, Tarzia G, Piomelli D, Harvey JN, Mulholland AJ. Conformational effects in enzyme catalysis: reaction via a high energy conformation in fatty acid amide hydrolase. Biophys J 2007, 92: 20-22, doi:10.1529/biophysj.106.098434.
27. Puig E, Mixcoha E, Garcia-Viloca M, Gonzalez-Lafont A, Lluch JM. How the substrate D-glutamate drives the catalytic action of bacillus subtilis glutamate racemase. J Am Chem Soc 2009, 131: 3509-3521, doi:10.1021/ja806012h.
28. Hu P, Wang S, Zhang Y. Highly Dissociative and Concerted Mechanism for the Nicotinamide Cleavage Reaction in Sir2Tm Enzyme Suggested by Ab Initio QM/MM Molecular Dynamics Simulations. J Am Chem Soc 2008, 130: 16721-16728.
29. Carnevale V, Raugei S, Micheletti C, Carloni P. Large-scale motions and electrostatic properties of furin and HIV-1 protease. J Phys Chem A 2007, 111: 12327-12332, doi:10.1021/jp0751716.
30. Hong R, Magistrato A, Carloni P. Anthrax lethal factor investigated by molecular simulations. J Chem Theory Comput 2008, 4: 1745-1756, doi:10.1021/ct8001877.
31. Guallar V, Lu C, Borrelli K, Egawa T, Yeh S-R. Ligand migration in the truncated hemoglobin-II from mycobacterium tuberculosis: the role of G8 tryptophan. J Biol Chem 2009, 284: 3106-3116, doi:10.1074/jbc.M806183200.
32. Alcantara RE, Xu C, Spiro TG, Guallar V. A quantum-chemical picture of hemoglobin affinity. Proc Natl Acad Sci 2007, 104: 18451.
33. Alexandrova AN, Rothlisberger D, Baker D, Jorgensen WL. Catalytic mechanism and performance of computationally designed enzymes for kemp elimination. J Am Chem Soc 2008, 130: 15907-15915.
34. Tubert-Brohman I, Acevedo O, Jorgensen WL. Elucidation of hydrolysis mechanisms for fatty acid amide hydrolase and its Lys142Ala variant via QM/MM simulations. J Am Chem Soc 2006, 128: 16904-16913, doi:10.1021/ja065863s.
35. Verbitsky G, Nussinov R, Wolfson H. Flexible structural comparison allowing hinge-bending, swiveling motions. Proteins 1999, 34: 232-254.
36. Rueda M, Bottegoni G, Abagyan R. Consistent improvement of cross-docking results using binding site ensembles generated with elastic network normal modes. J Chem Inf Model 2009, 49: 716-725, doi:doi:10.1021/ci8003732.
37. Friesner RA, Guallar V. Ab initio quantum chemical and mixed quantum mechanics/molecular mechanics (QM/MM) methods for studying enzymatic catalysis. Annu Rev Phys Chem 2005, 56: 389-427.
38. Wanko M, Hoffmann M, Frauenheim T, Elstner M. Computational photochemistry of retinal proteins. J Comput-Aid Mol Des 2006, 20: 511-518.
39. Carnevale V, Raugei S, Neri M, Pantano S, Micheletti C, Carloni P. Multi-scale modeling of HIV-1 proteins. J Mol Struc:THEOCHEM 2009, 898: 97-105.
40. Schoneboom JC, Cohen S, Lin H, Shaik S, Thiel W. Quantum mechanical/molecular mechanical investigation of the mechanism of C-H hydroxylation of camphor by cytochrome P450(cam): Theory supports a two-state rebound mechanism. J Am Chem Soc 2004, 126: 4017-4034.
41. Geethalakshmi KR, Waller MP, Thiel W, Bühl M. 51V NMR chemical shifts calculated from QM/MM models of peroxo forms of vanadium haloperoxidases. J Phys Chem B 2009, 113: 4456-4465.
42. Yang W. Direct calculation of electron density in density-functional theory. Phys Rev Lett 1991, 66: 1438.
43. Kitaura K, Ikeo E, Asada T, Nakano T, Uebayasi M. Fragment molecular orbital method: an approximate computational method for large molecules. Chem Phys Lett 1999, 313: 701-706.
44. Kiyota Y, Hasegawa J-Y, Fujimoto K, Swerts B, Nakatsuji H. A multicore QM/MM approach for the geometry optimization of chromophore aggregate in protein. J Comput Chem 2009, 30: 1351-1359.
45. Sproviero E, Newcomer M, Gascón J, Batista E, Brudvig G, Batista V. The MoD-QM/MM methodology for structural refinement of photosystem II and other biological macromolecules. Photosynth Res 2009, 102: 455-470.
46. He X, Merz KM. Divide and conquer Hartree-Fock calculations on proteins. J Chem Theory Comput 2009, 6: 405-411 doi: 10.1021/ct9006635.
47. Fedorov DG, Ishimura K, Ishida T, Kitaura K, Pulay P, Nagase S. Accuracy of the three-body fragment molecular orbital method applied to Moeller-Plesset perturbation theory. J Comput Chem 2007, 28: 1476-1484.
48. Xie W, Orozco M, Truhlar DG, Gao J. X-pol potential: an electronic structure-based force field for molecular dynamics simulation of a solvated protein in water. J Chem Theory Comput 2009, 5: 459-467, doi:10.1021/ct800239q.
49. Wallrapp F, Masone D, Guallar V. Electron transfer in the P450cam/PDX complex. The QM/MM e-pathway. J Phys Chem A 2008, 112: 12989-12994.
50. Guallar V, Wallrapp F. Mapping protein electron transfer pathways with QM/MM methods. J Roy Soc Interface 2008, 5: 233-239.
51. Ke Z, Wang S, Xie D, Zhang Y. Born-Oppenheimer ab initio QM/MM molecular dynamics simulations of the hydrolysis reaction catalyzed by protein arginine deiminase 4. J Phys Chem B 2009, 113: 16705-16710.
52. Liu J, Zhang Y, Zhan C-G. Reaction pathway and free-energy barrier for reactivation of dimethylphosphoryl-inhibited human acetylcholinesterase. J Phys Chem B 2009, 113: 16226-16236.
53. Crehuet R, Field MJ. A transition path sampling study of the reaction catalyzed by the enzyme chorismate mutase. J Phys Chem B 2007, 111: 5708-5718.
54. Quaytman SL, Schwartz SD. Comparison studies of the human heart and bacillus stearothermophilus lactate dehydrogreanse by transition path sampling. J Phys Chem A 2009, 113: 1892-1897.
55. Masson F, Laino T, Rothlisberger U, Hutter Jr. A QM/MM investigation of thymine dimer radical anion splitting catalyzed by DNA photolyase13. ChemPhysChem 2009, 10: 400-410.
56. Ghosh N, Prat-Resina X, Gunner MR, Cui Q. Microscopic pKa Analysis of Glu286 in cytochrome c oxidase (Rhodobacter sphaeroides): toward a calibrated molecular model. Biochemistry 2009, 48: 2468-2485.
57. Xie L, Liu H, Yang W. Adapting the nudged elastic band method for determining minimum-energy paths of chemical reactions in enzymes. J Chem Phys 2004, 120: 8039-8052.
58. Galvan IF, Field MJ. Improving the efficiency of the NEB reaction path finding algorithm. J Comput Chem 2008, 29: 139-143.
59. Lelimousin M, Adam V, Nienhaus GU, Bourgeois D, Field MJ. Photoconversion of the fluorescent protein EosFP: a hybrid potential simulation study reveals intersystem crossings. J Am Chem Soc 2009, 131: 16814-16823.
60. Riccardi D, Konig P, Guo H, Cui Q. Proton transfer in carbonic anhydrase is controlled by electrostatics rather than the orientation of the acceptor. Biochemistry 2008, 47: 2369-2378.
61. Riccardi D, Schaefer P, Yang Y, Yu H, Ghosh N, Prat-Resina X, Konig P, Li G, Xu D, Guo H. et al. Development of effective quantum mechanical/molecular mechanical (QM/MM) methods for complex biological processes. J Phys Chem B 2006, 110: 6458-6469.
62. Rajamani R, Gao J. Combined QM/MM study of the opsin shift in bacteriorhodopsin. J Comput Chem 2002, 23: 96-105, doi:10.1002/jcc.1159.
63. Wong K-Y, Gao J. The reaction mechanism of paraoxon hydrolysis by phosphotriesterase from combined QM/MM simulations Biochem 2007, 46: 13352-13369, doi:10.1021/bi700460c.
64. Seabra GM, Walker RC, Roitberg AE. Solvation Effects on Molecules and Biomolecules. Vol. 6. Springer Netherlands, Dordrecht; 2008.
65. Car R, Parrinello M. Unified approach for molecular dynamics and density-functional theory. Phys Rev Lett 1985, 55: 2471.
66. Simona F, Magistrato A, Dal Peraro M, Cavalli A, Vila AJ, Carloni P. Common mechanistic features among metallo-β-lactamases. J Biol Chem 2009, 284: 28164-28171.
67. De Vivo M, Cavalli A, Carloni P, Recanatini M. Computational study of the phosphoryl transfer catalyzed by a cyclin-dependent kinase. Chem - Eur J 2007, 13: 8437-8444.
68. Alfonso-Prieto M, Biarnés X, Vidossich P, Rovira C. The molecular mechanism of the catalase reaction. J Am Chem Soc 2009, 131: 11751-11761.
69. Stanton CL, Kuo IFW, Mundy CJ, Laino T, Houk KN. QM/MM metadynamics study of the direct decarboxylation mechanism for orotidine-5′-monophosphate decarboxylase using two different QM regions: acceleration too small to explain rate of enzyme catalysis. J Phys Chem B 2007, 111: 12573-12581.
70. Amara P, Field MJ. Evaluation of an ab initio quantum mechanical/molecular mechanical hybrid-potential link-atom method. Theor Chem Acc 2003, 109: 43-52.
71. Altun A, Guallar V, Friesner RA, Shaik S, Thiel W. The effect of heme environment on the hydrogen abstraction reaction of camphor in P450(cam) catalysis: a QM/MM study. J Am Chem Soc 2006, 128: 3924-3925.
72. Bahar I, Atilgan AR, Erman B. Direct evaluation of thermal fluctuations in proteins using a single-parameter harmonic potential. Folding & Design 1997, 2: 173-181.
73. Gao JL, Truhlar DG. Quantum mechanical methods for enzyme kinetics. Ann Rev Phys Chem 2002, 53: 467-505.
74. Senn HM, Thiel W. QM/MM studies of enzymes. Curr Opin Chem Biol 2007, 11: 182-187.
75. Senn HM, Thiel W. QM/MM methods for biomolecular systems. Angew Chem Int Ed Eng 2009, 48: 1198-1229.