Virtual screening of mandelate racemase mutants with enhanced activity based on binding energy in the transition state

Enzyme and Microbial Technology

Volumn 55, Issue , 2014, Pages 121-127

  Gu, Jiali ^a   Liu, Min ^a   Guo, Fei ^a   Xie, Wenping ^a   Lu, Wenqiang ^a   Ye, Lidan ^a   Chen, Zhirong ^a   Yuan, Shenfeng ^a   Yu, Hongwei ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

Binding energy; Mandelate racemase; Molecular dynamics simulation; Transition state; Virtual screening

Indexed keywords

BINDING ENERGY; ENZYMES; MOLECULAR DYNAMICS; SUBSTRATES;

CATALYTIC EFFICIENCIES; CATALYTIC PROPERTIES; DYNAMIC KINETIC RESOLUTION; EXPERIMENTAL VALIDATIONS; MANDELATE RACEMASE; MOLECULAR DYNAMICS SIMULATIONS; TRANSITION STATE; VIRTUAL SCREENING;

EFFICIENCY;

MANDELATE RACEMASE;

ARTICLE; BINDING AFFINITY; CATALYSIS; ENZYME ASSAY; MOLECULAR DYNAMICS; MUTANT; SCREENING; VIRTUAL SCREENING;

BINDING ENERGY; MANDELATE RACEMASE; MOLECULAR DYNAMICS SIMULATION; TRANSITION STATE; VIRTUAL SCREENING;

AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; BINDING SITES; BIOCATALYSIS; CATALYTIC DOMAIN; ESCHERICHIA COLI; GLYCOLATES; HYDROGEN BONDING; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MANDELIC ACIDS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MUTAGENESIS, SITE-DIRECTED; PEPTIDE LIBRARY; PROTEIN CONFORMATION; PSEUDOMONAS PUTIDA; RACEMASES AND EPIMERASES; RECOMBINANT FUSION PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 84891781608     PISSN: 01410229     EISSN: 18790909     Source Type: Journal    
DOI: 10.1016/j.enzmictec.2013.10.008     Document Type: Article

References (49)

1. Felfer U., Goriup M., Koegl M.E., Wagner U., Larissegger-Schnell B., Faber K., et al. The substrate spectrum of mandelate racemase: minimum structural requirements for substrates and substrate model. Adv Synth Catal 2005, 347:951-961.
2. Neidhart D.J., Powers V.M., Kenyon G.L., Tsou A.Y., Ransom S.C., Gerlt J.A., et al. Preliminary X-ray data on crystals of mandelate racemase. J Biol Chem 1988, 263:9268-9270.
3. Powers V.M., Koo C.W., Kenyon G.L., Gerlt J.A., Kozarich J.W. Mechanism of the reaction catalyzed by mandelate racemase. 1. Chemical and kinetic evidence for a 2-base mechanism. Biochemistry 1991, 30:9255-9263.
4. Frushicheva M.P., Cao J., Chu Z.T., Warshel A. Exploring challenges in rational enzyme design by simulating the catalysis in artificial kemp eliminase. Proc Natl Acad Sci 2010, 107:16869-16874.
5. Toscano M.D., Woycechowsky K.J., Hilvert D. Minimalist active-site redesign: teaching old enzymes new tricks. Angew Chem Int Ed 2007, 46:3212-3236.
6. Zheng F., Yang W.C., Ko M.C., Liu J.J., Cho H., Gao D.Q., et al. Most efficient cocaine hydrolase designed by virtual screening of transition states. J Am Chem Soc 2008, 130:12148-12155.
7. Mader M.M., Bartlett P.A. Binding energy and catalysis: the implications for transition-state analogs and catalytic antibodies. Chem Rev 1997, 97:1281-1301.
8. Fersht A.R., Leatherbarrow R.J., Wells T.N.C. Binding energy and catalysis: a lesson from protein engineering of the tyrosyl-tRNA synthetase. Trends Biochem Sci 1986, 11:321-325.
9. Wolfenden R. Transition state analog inhibitors and enzyme catalysis. Annu Rev Biophys Bioeng 1976, 5:271-306.
10. Deng Y.Q., Roux B. Computations of standard binding free energies with molecular dynamics simulations. J Phys Chem B 2009, 113:2234-2246.
11. Minh D.D.L. Implicit ligand theory: rigorous binding free energies and thermodynamic expectations from molecular docking. J Chem Phys 2012, 137.
12. Brandsdal B.O., Osterberg F., Almlof M., Feierberg I., Luzhkov V.B., Aqvist J. Free energy calculations and ligand binding. Adv Protein Chem 2003, 66:123-158.
13. Campanera J.M., Pouplana R. MMPBSA decomposition of the binding energy throughout a molecular dynamics simulation of amyloid-beta (Aβ10-35) aggregation. Molecules 2010, 15:2730-2748.
14. Obiol-Pardo C., Rubio-Martinez.J. Comparative evaluation of MMPBSA and XSCORE to compute binding free energy in XIAP-peptide complexes. J Chem Inf Model 2007, 47:134-142.
15. Hou T., Wang J., Li Y., Wang W. Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations. J Chem Inf Model 2010, 51:69-82.
16. Lietzan A.D., Nagar M., Pellmann E.A., Bourque J.R., Bearne S.L., St Maurice M. Structure of mandelate racemase with bound intermediate analogues benzohydroxamate and cupferron. Biochemistry 2012, 51:1160-1170.
17. Wang J., Wolf R.M., Caldwell J.W., Kollman P.A., Case D.A. Development and testing of a general amber force field. J Comput Chem 2004, 25:1157-1174.
18. Wang J., Wang W., Kollman P.A., Case D.A. Automatic atom type and bond type perception in molecular mechanical calculations. J Mol Graph Model 2006, 25:247-260.
19. Siddiqi F., Bourque J.R., Jiang H.Y., Gardner M., St Maurice M., Blouin C., et al. Perturbing the hydrophobic pocket of mandelate racemase to probe phenyl motion during catalysis. Biochemistry 2005, 44:9013-9021.
20. Jorgensen W.L., Chandrasekhar J., Madura J.D., Impey R.W., Klein M.L. Comparison of simple potential functions for simulating liquid water. J Chem Phys 1983, 79:10.
21. Gu J.L., Yu H.W. The role of residue S139 of mandelate racemase: synergistic effect of S139 and E317 on transition state stabilization. J Biomol Struct Dyn 2012, 30:585-593.
22. St Maurice M., Bearne S.L. Kinetics and thermodynamics of mandelate racemase catalysis. Biochemistry 2002, 41:4048-4058.
23. Massova I., Kollman P.A. Computational alanine scanning to probe protein-protein interactions: a novel approach to evaluate binding free energies. J Am Chem Soc 1999, 121:8133-8143.
24. Wong S., Amaro R.E., McCammon.J.A. MM-PBSA captures key role of intercalating water molecules at a protein-protein interface. J Chem Theory Comput 2009, 5:422-429.
25. Kar P., Knecht V. Energetic basis for drug resistance of HIV-1 protease mutants against amprenavir. J Comput Aid Mol Des 2012, 26:215-232.
26. Carlsson J., Aqvist J. Calculations of solute and solvent entropies from molecular dynamics simulations. Phys Chem Chem Phys 2006, 8:5385-5395.
27. Huo S., Wang J., Cieplak P., Kollman P.A., Kuntz I.D. Molecular dynamics and free energy analyses of cathepsin D-inhibitor interactions: Insight into structure-based ligand design. J Med Chem 2002, 45:1412-1419.
28. Wang J., Morin P., Wang W., Kollman P.A. Use of MM-PBSA in reproducing the binding free energies to HIV-1 RT of TIBO derivatives and predicting the binding mode to HIV-1 RT of efavirenz by docking and MM-PBSA. J Am Chem Soc 2001, 123:5221-5230.
29. Park S., Morley K.L., Horsman G.P., Holmquist M., Hult K., Kazlauskas R.J. Focusing mutations into the P. fluorescens esterase binding site increases enantioselectivity more effectively than distant mutations. Chem Biol 2005, 12:45-54.
30. Morley K.L., Kazlauskas R.J. Improving enzyme properties: when are closer mutations better. Trends Biotechnol 2005, 23:231-237.
31. Godinho L.F., Reis C.R., Rozeboom H.J., Dekker F.J., Dijkstra B.W., Poelarends G.J., et al. Enhancement of the enantioselectivity of carboxylesterase A by structure-based mutagenesis. J Biotechnol 2012, 158:36-43.
32. Bourque J.R., Bearne S.L.F. Mutational analysis of the active site flap (20s loop) of mandelate racemase. Biochemistry 2008, 47:566-578.
33. Bearne S.L., Wolfenden R. Mandelate racemase in pieces: effective concentrations of enzyme functional groups in the transition state. Biochemistry 1997, 36:1646-1656.
34. Bearne S.L., St Maurice M., Vaughan M.D. An assay for mandelate racemase using high-performance liquid chromatography. Anal Biochem 1999, 269:332-336.
35. Fee J.A., Hegeman G.D., Kenyon G.L. Mandelate racemase from Pseudomonas putida. Subunit composition and absolute divalent metal ion requirement. Biochemistry 1974, 13:2528-2532.
36. Neidhart D.J., Howell P.L., Petsko G.A., Powers V.M., Li R., Kenyon G.L., et al. Mechanism of the reaction catalyzed by mandelate racemase 2. Crystal structure of mandelate racemase at 2.5-ang. resolution: identification of the active site and possible catalytic residues. Biochemistry 1991, 30:9264-9273.
37. Garcia-Viloca M., Gonzalez-Lafont A., Lluch J.M. A QM/MM study of the racemization of vinylglycolate catalyzed by mandelate racemase enzyme. J Am Chem Soc 2001, 123:709-721.
38. Case D.A., Cheatham T.E., Darden T., Gohlke H., Luo R., Merz K.M., et al. The Amber biomolecular simulation programs. J Comput Chem 2005, 26:1668-1688.
39. Ponder J.W., Case D.A. Force fields for protein simulations. Adv Protein Chem 2003, 66:27.
40. Homeyer N., Gohlke H. Free energy calculations by the molecular mechanics Poisson-Boltzmann surface area method. Mol Inform 2012, 31:114-122.
41. Huo S., Wang J., Cieplak P., Kollman P.A., Kuntz Molecular Dynamics I.D. Free energy analyses of cathepsin D-inhibitor interactions: insight into structure-based ligand design. J Med Chem 2002, 45:1412-1419.
42. Lee J., Kim J.-S., Seok Cooperativity C. Specificity of cys2his2 zinc finger protein-DNA interactions: a molecular dynamics simulation study. J Phys Chem B 2010, 114:7662-7671.
43. Frushicheva M.P., Cao J., Warshel Challenges A. Advances in validating enzyme design proposals: the case of kemp eliminase catalysis. Biochemistry 2011, 50:3849-3858.
44. Lafaquiere V., Barbe S., Puech-Guenot S., Guieysse D., Cortes J., Monsan P., et al. Control of lipase enantioselectivity by engineering the substrate binding site and access channel. ChemBioChem 2009, 10:2760-2771.
45. Marton Z., Léonard-Nevers V., Syrén P.O., Bauer C., Lamare S., Hult K., et al. Mutations in the stereospecificity pocket and at the entrance of the active site of Candida antarctica lipase B enhancing enzyme enantioselectivity. J Mol Catal B: Enzym 2010, 65:11-17.
46. Warshel A., Sharma P.K., Kato M., Xiang Y., Liu H., Olsson M.H.M. Electrostatic basis for enzyme catalysis. Chem Rev 2006, 106:3210-3235.
47. Hanoian P., Sigala P.A., Herschlag D., Hammes-Schiffer.S. Hydrogen bonding in the active site of ketosteroid isomerase: electronic inductive effects and hydrogen bond coupling. Biochemistry 2010, 49:10339-10348.
48. Barroso M., Arnaut L.G., Formosinho S.J. The role of reaction energy and hydrogen bonding in the reaction path of enzymatic proton transfers. J Phys Org Chem 2009, 22:254-263.
49. Ma J., Wu L., Guo F., Gu J., Tang X., Jiang L., et al. Enhanced enantioselectivity of a carboxyl esterase from Rhodobacter sphaeroides by directed evolution. Appl Microbiol Biotechnol 2012, 1-10.