Density functional theory calculations on entire proteins for free energies of binding: Application to a model polar binding site

Proteins: Structure, Function and Bioinformatics

Volumn 82, Issue 12, 2014, Pages 3335-3346

  Fox, Stephen J ^a   Dziedzic, Jacek ^a,b   Fox, Thomas ^c   Tautermann, Christofer S ^c   Skylaris, Chris Kriton ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b GDANSK UNIVERSITY OF TECHNOLOGY   (Poland)

^c BOEHRINGER INGELHEIM PHARMA GMBH AND CO KG   (Germany)

Author keywords

DFT; Free energies of binding; Large scale DFT; ONETEP; Protein ligand interactions; QM PBSA; T4 lysozyme L99A M102Q

Indexed keywords

LYSOZYME; SOLVENT; LIGAND; N ACETYLMURAMOYLALANINE AMIDASE; VIRUS PROTEIN;

ACCURACY; ANALYTIC METHOD; ARTICLE; BINDING SITE; CALCULATION; COMPLEX FORMATION; DENSITY FUNCTIONAL THEORY; ENERGY; ENTEROBACTERIA PHAGE T4; LIGAND BINDING; MOLECULAR MECHANICS POISSON BOLTZMANN SURFACE AREA; MUTANT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; QUANTUM MECHANICS POISSON BOLTZMANN SURFACE AREA; SIMULATION; SOLVATION; ALGORITHM; AMINO ACID SUBSTITUTION; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; ENERGY TRANSFER; ENZYMOLOGY; GENETICS; KINETICS; MATHEMATICAL PHENOMENA; METABOLISM; MOLECULAR DYNAMICS; MUTATION; PROTEIN CONFORMATION; PROTEIN DATABASE; SURFACE PROPERTY;

ALGORITHMS; AMINO ACID SUBSTITUTION; BACTERIOPHAGE T4; BINDING SITES; DATABASES, PROTEIN; ENERGY TRANSFER; KINETICS; LIGANDS; MATHEMATICAL CONCEPTS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MUTATION; N-ACETYLMURAMOYL-L-ALANINE AMIDASE; PROTEIN CONFORMATION; SOLVENTS; SURFACE PROPERTIES; VIRAL PROTEINS;

EID: 84928337487     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24686     Document Type: Article

References (55)

1. Gilson MK, Zhou H-X. Calculation of protein-ligand binding affinities. Annu Rev Biophys Biomol Struct 2007;36:21-42.
2. Brandsdal BO, Österberg F, Almlöf M, Feierberg I, Luzhkov VB, Åqvist J. Free energy calculations and ligand binding. Adv Protein Chem 2003;66:123-158.
3. Zwanzig R. High-temperature equation of state by a perturbation method. I. nonpolar gases. J Chem Phys 1954;22:1420-1426.
4. Christ CD, Mark AE, van Gunsteren WF. Basic ingredients of free energy calculations: A review. J Comp Chem 2010;31:1569-1582.
5. Kirkwood JG. Statistical mechanics of fluid mixtures. J Chem Phys 1935;3:300-313.
6. Halperin I, Ma BY, Wolfson H, Nussinov R. Principles of docking: An overview of search algorithms and a guide to scoring functions. Proteins 2002;47:409-443.
7. Srinivasan J, Cheatham TE, Cieplak P, Kollman PA, Case DA. Continuum solvent studies of the stability of DNA, RNA, and phosphoramidate-DNA helices. J Am Chem Soc 1998;120:9401-9409.
8. Skylaris C-K, Haynes PD, Mostofi AA, Payne MC. Introducing {ONETEP}: Linear-scaling density functional simulations on parallel computers. J Chem Phys 2005;122:084119.
9. Dziedzic J, Fox SJ, Fox T, Tautermann C, Skylaris C-K, Large-scale {DFT} calculations in implicit solvent - {A} case study on the {T}4 lysozyme {L}99{A}/{M}102{Q} protein. Int J Quantum Chem 2012;113:771-785.
10. Dziedzic J, Helal HH, Skylaris C-K, Mostofi AA, Payne MC, Minimal parameter implicit solvent model for ab initio electronic structure calculations. Europhys Lett 2011;95:43001.
11. Wei BQ, Baase WA, Weaver LH, Matthews BW, Shoichet BK. A model binding site for testing scoring functions in molecular docking. J Mol Biol 2002;322:339-355.
12. Baase WA, Zhang XJ, Heinz DW, Blaber M, Baldwin EP, Matthews BW, Eriksson AE. Responce of a protein-structure to cavity-creating mutations and its relation to the hydrophobic effect. Science 1992;255:178-183.
13. Eriksson AE, Baase WA, Matthews BW. Similar hydrophobic replacement of Leu99 and Phe153 within the core of T4-lysozyme have different structural and thermodynamic consequences. J Mol Biol 1993;229:747-769.
14. Deng Y, Roux B. Calculation of standard binding free energies: Aromatic molecules in the {T}4 lysozyme {L99A} mutant. J Chem Theory Comput 2006;2:1255-1273.
15. Morton A, Baase W, Matthews BW. Energetic origins of specificity of ligand binding in an interior nonpolar cavity of {T}4 {L}ysozyme. Biochemistry 1995;34:8564-8575.
16. Morton A. Specificity of ligand binding in a buried nonpolar cavity of {T}4 lysozyme: Linkage of dynamics and structural plasticity. Biochemistry 1995;34:8576-8588.
17. Gallicchio E, Lapelosa M, Levy RM. Binding energy distribution analysis method ({BEDAM}) for estimation of protein-Ligand binding affinities. J Chem Theory Comput 2010;6:2961-2977.
18. Leitgeb M, Karplus M, Boresch S, Tettinger F. Absolute binding free energies: A quantitative approach for their calculation. J Phys Chem B 2003;107:9535-9551.
19. Mobley DL, Graves AP, Chodera JD, McReynolds AC, Shoichet BK, Dill KA. Predicting absolute ligand binding free energies to a simple model site. J Mol Biol 2007;371:1118-1134.
20. Deng Y, Roux B. Computations of standard binding free energies with molecular dynamics simulations. J Phys Chem B 2009;113:2234-2246.
21. Graves AP, Brenk R, Shoichet BK. Decoys for docking. J Med Chem 2005;48:3714-3728.
22. Boyce SE, Mobley DL, Rocklin GJ, Graves AP, Dill KA, Shoichet BK. Predicting lingand binding affinity with alchemical free energy methods in a polar model binding site. J Mol Biol 2009;394:747-763.
23. Graves AP, Shivakumar DM, Boyce SE, Jacobson MP, Case DA, Shoichet BK. Rescoring docking hit lists for model cavity sites: Predictions and experimental testing. J Mol Biol 2008;377:914-934.
24. Massova I, Kollman PA. Computational alanine scanning to probe protein-protein interactions: A novel approach to evaluate binding free energies. J Am Chem Soc 1999;121:8133-8143.
25. Kaukonen M, Söderhjelm P, Heimdal J, Ryde U. {QM/MM-PBSA} method to estimate free energies for reactions in proteins. J Phys Chem B 2008;112:12537-12548.
26. Rod TH, Ryde U. A method for calculating high-level {QM/MM} free energies for enzymatic reactions: methyl transfer catalyzed by catechol {O}-methyltransferase. Phys Rev Lett 2005;94:198302.
27. Wang M, Wong CF. Rank-ordering protein-ligand binding affinity by a quantum mechanics/molecular mechanics/Poisson-Boltzmann-surface area model. J Chem Phys 2007;126:026101.
28. Soler JM, Artacho E, Gale JD, Garcia A, Junquera J, Ordejon P, Sanchez D. The {S}iesta method for ab initio order-N materials simulation. J Phys Cond Mater 2002;14:2745-2779.
29. Davis ME, Madura JD, Luty BA, McCammon JA. Electrostatic and diffusion of molecules in solution: {S}imulations with the University of Houston Brownian Dynamics Program. Comp Phys Commun 1991;62:187-197.
30. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Montgomery JJA, Vreven T, Kudin KN, Burant JC, Millam JM, Iyengar SS, Tomasi J, Barone V, Mennucci B, Cossi M, Scalmani G, Rega N, Petersson GA, Nakatsuji H, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Klene M, Li X, Knox JE, Hratchian HP, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Ayala PY, Morokuma K, Voth GA, Salvador P, Dannenberg JJ, Zakrzewski VG, Dapprich S, Daniels AD, Strain MC, Farkas O, Malick DK, Rabuck AD, Raghavachari K, Foresman JB, Ortiz JV, Cui Q, Baboul AG, Clifford S, Cioslowski J, Stefanov BB, Liu G, Liashenko A, Piskorz P, Komaromi I, Martin RL, Fox DJ, Keith T, Al-Laham MA, Peng CY, Nanayakkara A, Challacombe M, Gill PMW, Johnson B, Chen W, Wong MW, Gonzalez C, Pople JA. Gaussian 03, revision C.02. Wallingford, CT: Gaussian, Inc.; 2004.
31. Diaz N, Suárez D, Merz KM, Sordo TL. Molecular dynamics simulations of the TEM-1 {β}-lactamase complexed with cephalothi. J Med Chem 2005;48:780-791.
32. Dixon SL, van der Vaart A, Wang B, Gogonea V, Vincent JJ, Brothers EN, Suarez D, Westerhoff LM, Merz JKM, Divcon. University Park, PA: The Pennsylvania State University; 2004.
33. Cole DJ, Skylaris C-K, Rajendra E, Venkitaraman AR, Payne MC. Protein-protein interaction from linear-scaling first-principles quantum-mechanical calculations. Europhys Lett 2010;91:37004.
34. Hill Q, Skylaris C-K. Including dispersion interactions in the {ONETEP} program for linear-scaling density functional theory calculations. Proc R Soc A 2009;465:669-683.
35. Fox S, Wallnoefer HG, Fox T, Tautermann CS, Skylaris C-K. First principles-based calculations of free energy of binding: Application to ligand binding in a self-assembling superstructure. J Chem Theory Comput 2011;7:1102-1108.
36. Skylaris C-K, Haynes PD, Mostofi AA, Payne MC. Implementation of linear scaling plane wave density functional theory on parallel computers. Phys Stat Sol 2006;243:973-988.
37. Hine NDM, Haynes PD, Mostofi AA, Skylaris C-K, Payne MC, Linear-scaling density-functional theory with tens of thousands of atoms: Expanding the scope and scale of calculations with ONETEP. Comp Phys Commun 2009;180:1041-1053.
38. Skylaris C-K, Mostofi AA, Haynes PD, Diéguez O, Payne MC, Nonorthogonal generalized Wannier function pseudopotential plane-wave method. Phys Rev B 2002;66:035119.
39. Mostofi AA, Haynes PD, Skylaris C-K, Payne MC. Preconditioned iterative minimization for linear-scaling electronic structure calculations. J Chem Phys 2003;119:8842-8848.
40. Haynes PD, Skylaris C-K, Mostofi AA, Payne MC. Elimination of the basis set superposition error in linear-scaling density-functional calculations with local orbitals optimized in situ. Chem Phys Lett 2006;422:345-349.
41. Anton L, Dziedzic J, Skylaris C-K, Probert M. Multigrid solver module for onetep, castep and other codes. http://www.hector.ac.uk/cse/distributedcse/reports/onetep/; 2013.
42. Fattebert J-L, Gygi F. Density functional theory for efficient ab initio molecular dynamics simulations in solution. J Comp Chem 2002;23:662-666.
43. Tomasi J, Persico M. Molecular interactions in solution: An overview of methods based on continuous distributions of the solvent. Chem Rev 1994;94:2027-2094.
44. Marenich AV, Cramer CJ, Truhlar DG. Universal solvation model based on solute electron density and on a continuum model of the solvent defined by the bulk dielectric constant and atomic surface tensions. J Phys Chem B 2009;113:6378-6396.
45. Molecular operating environment (MOE), 2013.08. Montreal, QC, Canada: Chemical Computing Group Inc.; 2013.
46. Case DA, Darden T, Cheatham T, Simmerling C, Wang J, Duke R, Luo R, Crowley M, Roitberg SHA, Seabra G, Kolossváry I, Wong KF, Paesani F, Vanicek J, Wu X, Brozell SR, Steinbrecher T, Gohlke H, Yang H, Tan C, Mongan J, Hornak V, Cui G, Mathews D, Seetin M, Sagui C, Babin V, Kollman PA. Amber10; 2008.
47. Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, Simmerling C. Comparison of multiple amber force fields and development of improved protein backbone parameters. Proteins 2006;65:712-725.
48. Wang J, Wolf RM, Caldwell JW, Kollman PA, Case DA, Development and testing of a general amber force field. J Comp Chem 2004;25:1157-1174.
49. Jorgensen WL, Chandrasekhar J, Madura JD. Comparison of simple potential functions for simulating liquid water. J Chem Phys 1983;79:926-935.
50. Alderman SA, Doll JD. Generalized Langevin equation approach for atom-solid-surface scattering - general formulation for classical scattering off harmonic solids. J Chem Phys 1976;64:2375-2388.
51. Ryckaert J-P, Ciccotti G, Berendsen HJC. Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 1977;23:327-341.
52. Perdew JP, Burke K, Ernzerhof M. Generalized gradient approximation made simple. Phys Rev Lett 1996;77:3865-3868.
53. Fox S, Pittock C, Fox T, Tautermann C, Malcolm N, Skylaris C-K. Electrostatic embedding in large-scale first principles quantum mechanical calculations on biomolecules. J Chem Phys 2011;135:224107.
54. Mordasini TZ, McCammon JA. Calculations of relative hydration free energies: A comparative study using thermodynamic integration and an extrapolation method based on a single reference state J Phys Chem B 2000;104:360-397.
55. Marenich AV, Kelly CP, Thompson JD, Hawkins GD, Chambers CC, Giesen DJ, Winget P, Cramer CJ, Truhlar DG. Minnesota solvation database-version 2012. Minneapolis: University of Minnesota; 2012.