Validating computer simulations of enantioselective catalysis; reproducing the large steric and entropic contributions in Candida Antarctica lipase B

Proteins: Structure, Function and Bioinformatics

Volumn 82, Issue 7, 2014, Pages 1387-1399

  Schopf, Patrick ^a   Warshel, Arieh ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Enzyme design; EVB; Free energy calculations; Mutation; Serine hydrolase; Stereoselective enzyme; Transesterification

Indexed keywords

LIPASE B; ALCOHOL DERIVATIVE; FUNGAL PROTEIN; LIPASE B, CANDIDA ANTARCTICA; PROTEIN BINDING; TRIACYLGLYCEROL LIPASE;

ARTICLE; CANDIDA ANTARCTICA; CATALYSIS; CHEMICAL REACTION; COMPUTER AIDED DESIGN; COMPUTER SIMULATION; DEACYLATION; EMPIRICAL VALENCE BOND; ENANTIOMER; ENANTIOSELECTIVITY; ENTROPY; HYDROGEN BOND; HYDROLYSIS; MOLECULAR MECHANICS; NONHUMAN; NUCLEOPHILICITY; PRIORITY JOURNAL; PROTON TRANSPORT; QUANTUM MECHANICS; STATIC ELECTRICITY; STEREOCHEMISTRY; STEREOISOMERISM; TRANSESTERIFICATION; WILD TYPE; CHEMICAL STRUCTURE; CHEMISTRY; ESTERIFICATION; METABOLISM; REPRODUCIBILITY; THERMODYNAMICS;

CANDIDA ANTARCTICA;

ALCOHOLS; CATALYSIS; COMPUTER SIMULATION; ESTERIFICATION; FUNGAL PROTEINS; LIPASE; MODELS, MOLECULAR; PROTEIN BINDING; REPRODUCIBILITY OF RESULTS; STEREOISOMERISM; THERMODYNAMICS;

EID: 84902175912     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24506     Document Type: Article

References (81)

1. Beck G. Synthesis of chiral drug substances. Synlett 2002;6:837-850.
2. Breuer M, Ditrich K, Habicher T, Hauer B, Keßeler M, Stürmer R, Zelinski T. Industrial methods for the production of optically active intermediates. Angew Chem Int Ed 2004;43:788-824.
3. Engström K, Nyhlén J, Sandström AG, Bäckvall J-E. Directed evolution of an enantioselective lipase with broad substrate scope for hydrolysis of α-substituted esters. J Am Chem Soc 2010;132:7038-7042.
4. Prasad S, Bocola M, Reetz MT. Revisiting the lipase from Pseudomonas aeruginosa: Directed evolution of substrate acceptance and enantioselectivity using iterative saturation mutagenesis. ChemPhysChem 2011;12:1550-1557.
5. Reetz MT, Prasad S, Carballeira JD, Gumulya Y, Bocola M. Iterative saturation mutagenesis accelerates laboratory evolution of enzyme stereoselectivity: Rigorous comparison with traditional methods. J Am Chem Soc 2010;132:9144-9152.
6. Magnusson AO, Rotticci-Mulder JC, Santagostino A, Hult K. Creating space for large secondary alcohols by rational redesign of Candida antarctica lipase B. ChemBioChem 2005;6:1051-1056.
7. Magnusson AO, Takwa M, Hamberg A, Hult K. An S-selective lipase was created by rational redesign and the enantioselectivity increased with temperature. Angew Chem Int Ed 2005;44:4582-4585.
8. Martinelle M, Hult K. Kinetics of acyl transfer reactions in organic media catalysed by Candida antarctica lipase B. Biochim Biophys Acta 1995;1251:191-197.
9. Ottosson J, Fransson L, Hult K. Substrate entropy in enzyme enantioselectivity: An experimental and molecular modeling study of a lipase. Protein Sci 2002;11:1462-1471.
10. Rotticci D, Hæffner F, Orrenius C, Norin T, Hult K. Molecular recognition of sec-alcohol enantiomers by Candida antarctica lipase B. J Mol Catal B Enzym 1998;5:267-272.
11. Sandström AG, Engström K, Nyhlén J, Kasrayan A, Bäckvall J-E. Directed evolution of Candida antarctica lipase A using an episomaly replicating yeast plasmid. Protein Eng Design Sel 2009;22:413-420.
12. Sandström AG, Wikmark Y, Engström K, Nyhlén J, Bäckvall J-E. Combinatorial reshaping of the Candida antarctica lipase A substrate pocket for enantioselectivity using an extremely condensed library. Proc Natl Acad Sci USA 2012;109:78-83.
13. Nyhlén J, Martín-Matute B, Sandström AG, Bocola M, Bäckvall J-E. Influence of δ-functional groups on the enantiorecognition of secondary alcohols by Candida antarctica lipase B. ChemBioChem 2008;9:1968-1974.
14. Orrenius C, Haeffner F, Rotticci D, Ohrner N, Norin T, Hult K. Chiral recognition of alcohol enantiomers in acyl transfer reactions catalysed by Candida antarctica lipase B. Biocatal Biotransform 1998;16:1-15.
15. Léonard V, Fransson L, Lamare S, Hult K, Graber M. A water molecule in the stereospecificity pocket of Candida antarctica lipase B enhances enantioselectivity towards pentan-2-ol. ChemBioChem 2007;8:662-667.
16. Raza S, Fransson L, Hult K. Enantioselectivity in Candida antarctica lipase B: A molecular dynamics study. Protein Sci 2001;10:329-338.
17. Svedendahl M, Carlqvist P, Branneby C, Allnér O, Frise A, Hult K, Berglund P, Brinck T. Direct epoxidation in Candida antarctica lipase B studied by experiment and theory. ChemBioChem 2008;9:2443-2451.
18. Hopmann KH, Hallberg BM, Himo F. Catalytic mechanism of limonene epoxide hydrolase: A theoretical study. J Am Chem Soc 2005;127:14339-14347.
19. Siegbahn PEM, Himo F. The quantum chemical cluster approach for modeling enzyme reactions. Wiley Interdiscip Rev Comput Mol Sci 2011;1:323-336.
20. Aqvist J, Warshel A. Simulation of enzyme-reactions using valence-bond force-fields and other hybrid quantum-classical approaches. Chem Rev 1993;93:2523-2544.
21. Warshel A. Computer modeling of chemical reactions in enzymes and solutions. Wiley-Interscience, New York; 1991.
22. Frushicheva MP, Warshel A. Towards quantitative computer-aided studies of enzymatic enantioselectivity: The case of candida antarctica lipase A. ChemBioChem 2012;13:215-223.
23. Uppenberg J, Hansen M, Patkar S, Jones T. The sequence, crystal structure determination and refinement of two crystal forms of lipase B from Candida antarctica. Structure 1994;2:293-308.
24. Uppenberg J, Oehrner N, Norin M, Hult K, Kleywegt GJ, Patkar S, Waagen V, Anthonsen T, Jones TA. Crystallographic and molecular-modeling studies of lipase B from Candida antarctica reveal a stereospecificity pocket for secondary alcohols. Biochemistry 1995;34:16838-16851.
25. Egmond MR, van Bemmel CJ. Impact of structural information on understanding lipolytic function. In: Byron Rubin EAD, editor. Methods in enzymology, Vol. 284. Academic Press, Netherlands; 1997. pp 119-129.
26. Schrag JD, Cygler M. Lipases and α-β hydrolase fold. In: Byron Rubin EAD, editor. Methods in enzymology, Vol. 284: Academic Press, Netherlands; 1997. pp 85-107.
27. Chaput L, Sanejouand YH, Balloumi A, Tran V, Graber M. Contribution of both catalytic constant and Michaelis constant to CALB enantioselectivity: Use of FEP calculations for prediction studies. J Mol Catal B Enzym 2012;76:29-36.
28. Xu T, Zhang L, Su E, Cui D, Wang X, Wei D. Disparity in productive binding mode of the slow-reacting enantiomer determines the novel catalytic behavior of Candida antarctica lipase B. J Mol Catal B Enzym 2010;62:288-296.
29. Bocola M, Otte N, Jaeger K-E, Reetz MT, Thiel W. Learning from directed evolution: Theoretical investigations into cooperative mutations in lipase enantioselectivity. ChemBioChem 2004;5:214-223.
30. de los Ríos AP, Hernández-Fernández FJ, Tomás-Alonso F, Gómez D, Víllora G. Biocatalytic kinetic resolution of rac-1-phenylethanol and rac-2-pentanol in hexane medium: Acyl donor and water content effects. Can J Chem Eng 2010;88:442-446.
31. Hæffner F, Norin T, Hult K. Molecular modeling of the enantioselectivity in lipase-catalyzed transesterification reactions. Biophys J 1998;74:1251-1262.
32. Kwon HC, Shin DY, Lee JH, Kim SW, Kang JW. Molecular modeling and its experimental verification for the catalytic mechanism of Candida antarctica lipase B. J Microbiol Biotechnol 2007;17:1098-1105.
33. Léonard-Nevers V, Marton Z, Lamare S, Hult K, Graber M. Understanding water effect on Candida antarctica lipase B activity and enantioselectivity towards secondary alcohols. J Mol Catal B Enzym 2009;59:90-95.
34. Li C, Tan T, Zhang H, Feng W. Analysis of the conformational stability and activity of candida antarctica lipase B in organic solvents insight from molecular dynamics and quantum mechanics/molecular mechanics simulations. J Biol Chem 2010;285:28434-28441.
35. Marton Z, Léonard-Nevers V, Syrén PO, Bauer C, Lamare S, Hult K, Tranc V, Graber M. 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.
36. Ottosson J, Fransson L, King JW, Hult K. Size as a parameter for solvent effects on Candida antarctica lipase B enantioselectivity. Biochim Biophys Acta 2002;1594:325-334.
37. Parida S, Dordick JS. Tailoring lipase specificity by solvent and substrate chemistries. J Org Chem 1993;58:3238-3244.
38. Vallin M, Syrén P-O, Hult K. Mutant lipase-catalyzed kinetic resolution of bulky phenyl alkyl sec-alcohols: A thermodynamic analysis of enantioselectivity. ChemBioChem 2010;11:411-416.
39. Wittrup Larsen M, Zielinska DF, Martinelle M, Hidalgo A, Jensen LJ, Bornscheuer UT, Hult K. Suppression of water as a nucleophile in Candida antarctica lipase B catalysis. ChemBioChem 2010;11:796-801.
40. Warshel A, Russell S. Theoretical correlation of structure and energetics in the catalytic reaction of trypsin. J Am Chem Soc 1986;108:6569-6579.
41. Warshel A, Naray-Szabo G, Sussman F, Hwang JK. How do serine proteases really work. Biochemistry 1989;28:3629-3637.
42. Creighton S, Hwang JK, Warshel A, Parson WW, Norris J. Simulating the dynamics of the primary charge separation process in bacterial photosynthesis. Biochemistry 1988;27:774-781.
43. Strajbl M, Florián J, Warshel A. Ab initio evaluation of the potential surface for general base-catalyzed methanolysis of formamide: A reference solution reaction for studies of serine proteases. J Am Chem Soc 2000;122:5354-5366.
44. Ishikita H, Warshel A. Predicting drug-resistant mutations of HIV protease. Angew Chem Int Ed 2008;47:697-700.
45. Warshel A, Sussman F, King G. Free energy of charges in solvated proteins: Microscopic calculations using a reversible charging process. Biochemistry 1986;25:8368-8372.
46. Strajbl M, Hong G, Warshel A. Ab initio QM/MM simulation with proper sampling: "First Principle" calculations of the free energy of the autodissociation of water in aqueous solution. J Phys Chem B 2002;106:13333-13343.
47. Shurki A, Warshel A. Structure/function correlations of proteins using MM, QM/MM, and related approaches: Methods, #concepts, {box drawings light vertical}pitfalls, and current progress. Protein Simul 2003;66:249-313.
48. Ranaghan KE, Mulholland AJ. Investigations of enzyme-catalysed reactions with combined quantum mechanics/molecular mechanics (QM/MM) methods. Int Rev Phys Chem 2010;29:65-133.
49. Senn HM, Thiel W. QM/MM Methods for Biomolecular Systems. Angew Chem Int Ed 2009;48:1198-1229.
50. Chu ZT, Villa J, Strajbl M, Schutz CN, Shurki A, Warshel A. MOLARIS, Revision 9.06, University of Southern California, Los Angeles, CA, USA 2006.
51. Lee FS, Chu ZT, Warshel A. Microscopic and semimicroscopic calculations of electrostatic energies in proteins by the Polaris and Enzymix programs. J Comput Chem 1993;14:161-185.
52. Warshel A, Sharma PK, Kato M, Xiang Y, Liu H, Olsson MHM. Electrostatic basis for enzyme catalysis. Chem Rev 2006;106:3210-3235.
53. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. The protein data bank. Nucleic Acids Res 2000;28:235-242.
54. Singh UC, Kollman PA. An approach to computing electrostatic charges for molecules. J Comput Chem 1984;5:129-145.
55. Becke AD. Density-functional thermochemistry. III. The role of exact exchange. J Chem Phys 1993;98:5648-5652.
56. Lee C, Yang W, Parr RG. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys Rev B 1988;37:785-789.
57. Stephens PJ, Devlin FJ, Chabalowski CF, Frisch MJ. Ab initio calculation of vibrational absorption and circular dichroism spectra using density functional force fields. J Phys Chem 1994;98:11623-11627.
58. Vosko SH, Wilk L, Nusair M. Accurate spin-dependent electron liquid correlation energies for local spin density calculations: A critical analysis. Can J Phys 1980;58:1200-1211.
59. Hay PJ. Gaussian basis sets for molecular calculations. The representation of 3d orbitals in transition-metal atoms. J Chem Phys 1977;66:4377-4384.
60. McGrath MP, Radom L. Extension of Gaussian-1 (G1) theory to bromine-containing molecules. J Chem Phys 1991;94:511-516.
61. McLean AD, Chandler GS. Contracted Gaussian basis sets for molecular calculations. I. Second row atoms, Z=11--18. J Chem Phys 1980;72:5639-5648.
62. Wachters AJH. Gaussian basis set for molecular wavefunctions containing third-row atoms. J Chem Phys 1970;52:1033-1036.
63. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Scalmani G, Barone V, Mennucci B, Petersson GA, Nakatsuji H, Caricato M, Li X, Hratchian HP, Izmaylov AF, Bloino J, Zheng G, Sonnenberg JL, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Vreven T, Montgomery JA, Peralta JE, Ogliaro F, Bearpark M, Heyd JJ, Brothers E, Kudin KN, Staroverov VN, Kobayashi R, Normand J, Raghavachari K, Rendell A, Burant JC, Iyengar SS, Tomasi J, Cossi M, Rega N, Millam JM, Klene M, Knox JE, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Martin RL, Morokuma K, Zakrzewski VG, Voth GA, Salvador P, Dannenberg JJ, Dapprich S, Daniels AD, Farkas Foresman JB, Ortiz JV, Cioslowski J, Fox DJ. Gaussian 09, Revision B.01. Wallingford, CT; 2009.
64. Singh N, Warshel A. Towards accurate microscopic calculation of solvation entropies: Extending the restraint release approach to studies of solvation effects. J Phys Chem B 2009;113:7372-7382.
65. Singh N, Warshel A. Absolute binding free energy calculations: On the accuracy of computational scoring of protein-ligand interactions. Proteins 2010;78:1705-1723.
66. Strajbl M, Sham YY, Villa J, Chu ZT, Warshel A. Calculations of activation entropies of chemical reactions in solution. J Phys Chem B 2000;104:4578-4584.
67. Karplus M, Kushick JN. Method for estimating the configurational entropy of macromolecules. Macromolecules 1981;14:325-332.
68. WL DeLano, The PyMOL Molecular Graphics, Revision 1.2r3pre, DeLano Scientific, San Carlos, CA, USA, 2002.
69. Guthrie JP. Hydration of carbonyl compounds, an analysis in terms of multidimensional marcus theory. J Am Chem Soc 2000;122:5529-5538.
70. Wang H. An accurate theoretical study of energy barriers of alkaline hydrolysis of carboxylic esters. Res Chem Intermed 2012;38:2175-2190.
71. Kazlauskas R. Engineering enantioselectivity in enzyme-catalyzed reactions. Protein engineering handbook. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany; 2008. pp 15-46.
72. Cahn RS, Ingold C, Prelog V. Specification of molecular chirality. Angew Chem Int Ed Engl 1966;5:385-415.
73. Prelog V, Helmchen G. Basic principles of the CIP-system and proposals for a revision. Angew Chem Int Ed Engl 1982;21:567-583.
74. Hwang JK, Warshel A. Semiquantitative calculations of catalytic free energies in genetically modified enzymes. Biochemistry 1987;26:2669-2673.
75. Singh N, Warshel A. A comprehensive examination of the contributions to the binding entropy of protein-ligand complexes. Proteins 2010;78:1724-1735.
76. Reetz MT, Krebs GPL. Challenges in the directed evolution of stereoselective enzymes for use in organic chemistry. Comptes Rendus Chim 2011;14:811-818.
77. Lee S-C, Kim J-H, Kim H-S. Design and evolution of biocatalysts. Curr Org Chem 2010;14:1894-1901.
78. Reetz MT. Directed evolution of enantioselective enzymes: An unconventional approach to asymmetric catalysis in organic chemistry. J Org Chem 2009;74:5767-5778.
79. Morley KL, Kazlauskas RJ. Improving enzyme properties: when are closer mutations better? Trends Biotechnol 2005;23:231-237.
80. Pan J, Yu H-L, Xu J-H, Lin G-Q. Advances in biocatalysis: Enzymatic reactions and their applications. In: Ma S, editor. Asymmetric catalysis from a Chinese perspective, Vol. 36. Topics in organometallic chemistry. Heidelberg, Berlin: Springer; 2011. pp 67-103.
81. Gröger H. Enzyme-catalyzed asymmetric synthesis. Catalytic asymmetric synthesis. John Wiley & Sons, Inc., New York; 2010. pp 269-341.