QM/MM study of the stereospecific proton exchange of glutathiohydroxyacetone by glyoxalase I

Rosner, 1995, Purification and characterization of acetylene hydratase of Pelobacter acetylenicus, a tungsten iron-sulfur protein, J. Bacteriol., 177, 5767, 10.1128/jb.177.20.5767-5772.1995 Frykman, 1993, S-ethyl thiooctanoate as acyl donor in lipase catalysed resolution of secondary alcohols, Tetrahedron Lett., 34, 1367, 10.1016/S0040-4039(00)91797-0 Landro, 1992, Isomerization of (R)- and (S)-glutathiolactaldehydes by glyoxalase I: the case for dichotomous stereochemical behavior in a single active site, Biochemistry, 31, 6069, 10.1021/bi00141a016 Monterde, 2004, Enzymatic transformations. Part 58: enantioconvergent biohydrolysis of styrene oxide derivatives catalysed by the Solanum tuberosum epoxide hydrolase, Tetrahedron Asymmetry, 15, 2801, 10.1016/j.tetasy.2004.06.032 Kazemi, 2018, Computational study of mycobacterium smegmatis acyl transferase reaction mechanism and specificity, ACS Catal., 8, 10698, 10.1021/acscatal.8b03360 Qian, 2018, QM/MM study of tungsten-dependent benzoyl-coenzyme a reductase: rationalization of regioselectivity and predication of W vs Mo selectivity, Inorg. Chem., 57, 10667, 10.1021/acs.inorgchem.8b01328 Jafari, 2018, Higher flexibility of Glu-172 explains the unusual stereospecificity of glyoxalase I, Inorg. Chem., 57, 4944, 10.1021/acs.inorgchem.7b03215 Escorcia, 2017, Quantum mechanics/molecular mechanics insights into the enantioselectivity of the O-acetylation of (R,S)-propranolol catalyzed by candida antarctica lipase B, ACS Catal., 7, 115, 10.1021/acscatal.6b02310 Dubey, 2017, MD simulations and QM/MM calculations show that single-site mutations of cytochrome P450BM3alter the active site’s complexity and the chemoselectivity of oxidation without changing the active species, Chem. Sci., 8, 5335, 10.1039/C7SC01932G Jafari, 2016, Catalytic mechanism of human glyoxalase I studied by quantum-mechanical cluster calculations, J. Mol. Catal. B Enzym., 131, 18, 10.1016/j.molcatb.2016.05.010 Maršavelski, 2015, The origin of specificity and insight into recognition between an aminoacyl carrier protein and its partner ligase, Phys. Chem. Chem. Phys., 17, 19030, 10.1039/C5CP03066H Wijma, 2014, Computationally efficient and accurate enantioselectivity modeling by clusters of molecular dynamics simulations, J. Chem. Inf. Model., 54, 2079, 10.1021/ci500126x Liao, 2011, Theoretical study of the chemoselectivity of tungsten-dependent acetylene hydratase, ACS Catal., 1, 937, 10.1021/cs200242m Liao, 2010, Mechanism of tungsten-dependent acetylene hydratase from quantum chemical calculations, Proc. Natl. Acad. Sci., 107, 22523, 10.1073/pnas.1014060108 Kuhn, 2000, QM-FE and molecular dynamics calculations on catechol O- methyltransferase: free energy of activation in the enzyme and in aqueous solution and regioselectivity of the enzyme-catalyzed reaction, J. Am. Chem. Soc., 122, 2586, 10.1021/ja992218v M. Kazemi, X. Sheng, F. Himo, Origins of Enantiopreference of Mycobacterium smegmatis Acyl Transferase: A Computational Analysis, Chem. – A Eur. J. 0 (2019). doi:https://doi.org/10.1002/chem.201902351. S.S. Hall, A.M. Doweyko, F. Jordan, Glyoxalase I enzyme studies. 2. Nuclear magnetic resonance evidence for an enediol-proton transfer mechanism, J. Am. Chem. Soc. 98 (1976) 7460–7461. doi:https://doi.org/10.1021/ja00439a077. Chari, 1981, Deuterium isotope effects on the product partitioning of fluoromethylglyoxal by glyoxalase I. Proof of a proton transfer mechanism, J. Biol. Chem., 256, 9785, 10.1016/S0021-9258(19)68690-4 Kozarich, 1982, (Glutathiomethyl) glyoxal: mirror-image catalysis by glyoxalase I, J. Am. Chem. Soc., 104, 2655, 10.1021/ja00373a062 Chari, 1983, Glutathiohydroxyacetone: proton NMR determination of the stereochemistry of proton exchange by glyoxalase I. Evidence for a cis-enediol intermediate based on mirror-image catalysis, J. Am. Chem. Soc., 105, 7169, 10.1021/ja00362a024 Cameron, 1997, Crystal structure of human glyoxalase I_evidence for gene duplication and 3D domain swapping, EMBO J., 16, 3386, 10.1093/emboj/16.12.3386 Cameron, 1999, Reaction mechanism of glyoxalase I explored by an X-ray crystallographic analysis of the human enzyme in complex with a transition state analogue, Biochemistry., 38, 13480, 10.1021/bi990696c Feierberg, 1999, Energetics of the proposed rate-determining step of the glyoxalase I reaction, FEBS Lett., 453, 90, 10.1016/S0014-5793(99)00703-6 Ridderström, 1998, Involvement of an active-site Zn2+ ligand in the catalytic mechanism of human glyoxalase I, J. Biol. Chem., 273, 21623, 10.1074/jbc.273.34.21623 Richter, 2001, Active site structure and mechanism of human glyoxalase I-an ab initio theoretical study, J. Am. Chem. Soc., 123, 6973, 10.1021/ja0105966 Himo, 2001, Catalytic mechanism of Glyoxalase I: a theoretical study, J. Am. Chem. Soc., 123, 10280, 10.1021/ja010715h Creighton, 2001, Brief history of glyoxalase I and what we have learned about metal ion-dependent, enzyme-catalyzed isomerizations, Arch. Biochem. Biophys., 387, 1, 10.1006/abbi.2000.2253 Sousa Silva, 2012, The glyoxalase pathway in protozoan parasites, Int. J. Med. Microbiol., 302, 225, 10.1016/j.ijmm.2012.07.005 Siegbahn, 2011, The quantum chemical cluster approach for modeling enzyme reactions, Wiley Interdiscip. Rev. Comput. Mol. Sci., 1, 323, 10.1002/wcms.13 Baes, 1976 Aronsson, 1978, Glyoxalase I, a zinc metalloenzyme of mammals and yeast, Biochem. Biophys. Res. Commun., 81, 1235, 10.1016/0006-291X(78)91268-8 Srnec, 2009, Reaction mechanism of manganese superoxide dismutase studied by combined quantum and molecular mechanical calculations and multiconfigurational methods, J. Phys. Chem. B, 113, 6074, 10.1021/jp810247u Heimdal, 2011, Reduction potentials and acidity constants of Mn superoxide dismutase calculated by QM/MM free-energy methods, ChemPhysChem., 12, 3337, 10.1002/cphc.201100339 Olsson, 2011, PROPKA3: consistent treatment of internal and surface residues in empirical pKa predictions, J. Chem. Theory Comput., 7, 525, 10.1021/ct100578z Le Grand, 2013, SPFP: speed without compromise - a mixed precision model for GPU accelerated molecular dynamics simulations, Comput. Phys. Commun., 184, 374, 10.1016/j.cpc.2012.09.022 Salomon-Ferrer, 2013, Routine microsecond molecular dynamics simulations with AMBER on GPUs. 2. Explicit solvent particle mesh ewald, J. Chem. Theory Comput., 9, 3878, 10.1021/ct400314y Götz, 2012, Routine microsecond molecular dynamics simulations with AMBER on GPUs. 1. Generalized born, J. Chem. Theory Comput., 8, 1542, 10.1021/ct200909j D.A. Case, R.M. Betz, D.S. Cerutti, T.E. Cheatham, T.A. Darden, R.E. Duke, T.J. Giese, H. Gohlke, A.W. Goetz, N. Homeyer, S. Izadi, P. Janowski, J. Kaus, A. Kovalenko, T.S. Lee, S. LeGrand, P. Li, C. Lin, T. Luchko, R. Luo, B. Madej, D. Mermelstein, K.M. Merz, G. Monard, H. Nguyen, H.T. Nguyen, I. Omelyan, D.R. Onufriev, D.R. Roe, A. Roitberg, C. Sagui, C.L. Simmerling, W.M. Botello-Smith, J. Swails, R.C. Walker, J. Wang, R.M. Wolf, X. Wu, L. Xiao, P.A. Kollman, AMBER 2016, University of California:, (2016). citeulike-article-id:14028955. Maier, 2015, ff14SB: improving the accuracy of protein side chain and backbone parameters from ff99SB, J. Chem. Theory Comput., 11, 3696, 10.1021/acs.jctc.5b00255 Wang, 2004, Development and testing of a general Amber force field, J. Comput. Chem., 25, 1157, 10.1002/jcc.20035 Jorgensen, 1983, Comparison of simple potential functions for simulating liquid water, J. Chem. Phys., 79, 926, 10.1063/1.445869 Hu, 2011, Comparison of methods to obtain force-field parameters for metal sites, J. Chem. Theory Comput., 7, 2452, 10.1021/ct100725a Bayly, 1993, A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: the RESP model, J. Phys. Chem., 97, 10269, 10.1021/j100142a004 Besler, 1990, Atomic charges derived from semiempirical methods, J. Comput. Chem., 11, 431, 10.1002/jcc.540110404 Lee, 1988, Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density, Phys. Rev. B, 37, 785, 10.1103/PhysRevB.37.785 Becke, 1988, Density-functional exchange-energy approximation with correct asymptotic behavior, Phys. Rev. A, 38, 3098, 10.1103/PhysRevA.38.3098 Becke, 1993, Density-functional thermochemistry. III. The role of exact exchange, J. Chem. Phys., 98, 5648, 10.1063/1.464913 Grimme, 2010, A consistent and accurate ab initio parametrization of density functional dispersion correction (DFT-D) for the 94 elements H-Pu, J. Chem. Phys., 132, 154104, 10.1063/1.3382344 Grimme, 2011, Effect of the damping function in dispersion corrected density functional theory, J. Comput. Chem., 32, 1456, 10.1002/jcc.21759 Schäfer, 1992, Fully optimized contracted Gaussian-basis sets for atoms Li to Kr, J. Chem. Phys., 97, 2571, 10.1063/1.463096 Furche, 2014, Turbomole, Wiley Interdiscip. Rev. Comput. Mol. Sci., 4, 91, 10.1002/wcms.1162 Seminario, 1996, Calculation of intramolecular force fields from second-derivative tensors, Int. J. Quantum Chem., 60, 1271, 10.1002/(SICI)1097-461X(1996)60:7<1271::AID-QUA8>3.0.CO;2-W Nilsson, 2003, An automatic method to generate force-field parameters for hetero-compounds, Acta Crystallogr. - Sect. D Biol. Crystallogr., 59, 274, 10.1107/S0907444902021431 Sigfridsson, 1998, Comparison of methods for deriving atomic charges from the electrostatic potential and moments, J. Comput. Chem., 19, 377, 10.1002/(SICI)1096-987X(199803)19:4<377::AID-JCC1>3.0.CO;2-P Cao, 2017, Protonation states of homocitrate and nearby residues in nitrogenase studied by computational methods and quantum refinement, J. Phys. Chem. B, 121, 8242, 10.1021/acs.jpcb.7b02714 Wu, 2003, Self-guided Langevin dynamics simulation method, Chem. Phys. Lett., 381, 512, 10.1016/j.cplett.2003.10.013 Berendsen, 1984, Molecular dynamics with coupling to an external bath, J. Chem. Phys., 81, 3684, 10.1063/1.448118 Darden, 1993, Particle mesh Ewald: an N·log(N) method for Ewald sums in large systems, J. Chem. Phys., 98, 10089, 10.1063/1.464397 Ryckaert, 1977, H.J. Berendsen, numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes, J. Comput. Phys., 23, 327, 10.1016/0021-9991(77)90098-5 Roe, 2013, PTRAJ and CPPTRAJ: software for processing and analysis of molecular dynamics trajectory data, J. Chem. Theory Comput., 9, 3084, 10.1021/ct400341p Ryde, 1996, The coordination of the catalytic zinc in alcohol dehydrogenase studied by combined quantum-chemical and molecular mechanics calculations, J. Comput. Aided Mol. Des., 10, 153, 10.1007/BF00402823 Ryde, 2001, Structure, strain, and reorganization energy of blue copper models in the protein, Int. J. Quantum Chem., 81, 335, 10.1002/1097-461X(2001)81:5<335::AID-QUA1003>3.0.CO;2-Q Ryde, 2016, QM/MM calculations on proteins, Methods Enzymol., 577, 119, 10.1016/bs.mie.2016.05.014 Senn, 2009, QM/MM methods for biomolecular systems, Angew. Chemie - Int. Ed., 48, 1198, 10.1002/anie.200802019 Reuter, 2000, Frontier bonds in QM/MM methods: a comparison of different approaches, J. Phys. Chem. A, 104, 1720, 10.1021/jp9924124 Hu, 2011, On the convergence of QM/MM energies, J. Chem. Theory Comput., 7, 761, 10.1021/ct100530r D.A. Case, V. Babin, J.T. Berryman, R.M. Betz, Q. Cai, D.S. Cerutti, T.E. Cheatham, T.A. Darden, R.E. Duke, H. Gohlke, A.W. Goetz, S. Gusarov, N. Homeyer, P. Janowski, J. Kaus, I. Kolossváry, A. Kovalenko, T.S. Lee, S. LeGrand, T. Luchko, R. Luo, B. Madej, K.M. Merz, F. Paesani, D.R. Roe, A. Roitberg, C. Sagui, R. Salomon-Ferrer, G. Seabra, C.L. Simmerling, W. Smith, J. Swails, Walker, J. Wang, R.M. Wolf, X. Wu, P.A. Kollman, Amber 14 - University of California:, (2014). citeulike-article-id:14028955. Svensson, 2002, 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., 100, 19357, 10.1021/jp962071j Cao, 2018, On the difference between additive and subtractive QM/MM calculations, Front. Chem., 6, 89, 10.3389/fchem.2018.00089 Tao, 2003, Climbing the density functional ladder: nonempirical meta–generalized gradient approximation designed for molecules and solids, Phys. Rev. Lett., 91, 146401, 10.1103/PhysRevLett.91.146401 Eichkorn, 1995, Auxiliary basis sets to approximate coulomb potentials, Chem. Phys. Lett., 240, 283, 10.1016/0009-2614(95)00621-A K. Eichkorn, F. Weigend, O. Treutler, R. Ahlrichs, Auxiliary basis sets for main row atoms and transition metals and their use to approximate Coulomb potentials, Theor. Chem. Accounts Theory, Comput. Model. (Theoretica Chim. Acta). 97 (1997) 119–124. doi:https://doi.org/10.1007/s002140050244. Hu, 2009, Do quantum mechanical energies calculated for small models of protein-active sites converge?, J. Phys. Chem. A, 113, 11793, 10.1021/jp9029024 S. Sumner, P. Söderhjelm, U. Ryde, Studies of Reaction Energies in Proteins, J. Chem. Theory Comput. 9 (2013) 4205–4214. doi:https://doi.org/10.1021/ct400339c. Hu, 2013, Accurate reaction energies in proteins obtained by combining QM/MM and large QM calculations, J. Chem. Theory Comput., 9, 640, 10.1021/ct3005003 Sierka, 2003, Fast evaluation of the coulomb potential for electron densities using multipole accelerated resolution of identity approximation, J. Chem. Phys., 118, 9136, 10.1063/1.1567253 Von Arnim, 1998, Performance of parallel TURBOMOLE for density functional calculations, J. Comput. Chem., 19, 1746, 10.1002/(SICI)1096-987X(19981130)19:15<1746::AID-JCC7>3.0.CO;2-N Kaukonen, 2008, QM/MM-PBSA method to estimate free energies for reactions in proteins, J. Phys. Chem. B, 112, 12537, 10.1021/jp802648k Hu, 2011, Reorganization energy for internal electron transfer in multicopper oxidases, J. Phys. Chem. B, 115, 13111, 10.1021/jp205897z Srinivasan, 1998, Continuum solvent studies of the stability of rna hairpin loops and helices, J. Biomol. Struct. Dyn., 16, 671, 10.1080/07391102.1998.10508279 Genheden, 2015, The MM/PBSA and MM/GBSA methods to estimate ligand-binding affinities, Expert Opin. Drug Discov., 10, 449, 10.1517/17460441.2015.1032936 Kaukonen, 2008, Proton transfer at metal sites in proteins studied by quantum mechanical free-energy perturbations, J. Chem. Theory Comput., 4, 985, 10.1021/ct700347h Luzhkov, 1992, Microscopic models for quantum mechanical calculations of chemical processes in solutions: LD/AMPAC and SCAAS/AMPAC calculations of solvation energies, J. Comput. Chem., 13, 199, 10.1002/jcc.540130212 Rod, 2005, Quantum mechanical free energy barrier for an enzymatic reaction, Phys. Rev. Lett., 94, 138302, 10.1103/PhysRevLett.94.138302 Rod, 2005, MM free energy calculations of enzyme reactions: methylation by catechol O-methyltransferase, J. Chem. Theory Comput., 1, 1240, 10.1021/ct0501102 Uranga, 2012, Can the protonation state of histidine residues be determined from molecular dynamics simulations?, Comput. Theor. Chem., 1000, 75, 10.1016/j.comptc.2012.09.025