Computationally efficient and accurate enantioselectivity modeling by clusters of molecular dynamics simulations

Journal of Chemical Information and Modeling

Volumn 54, Issue 7, 2014, Pages 2079-2092

  Wijma, Hein J ^a   Marrink, Siewert J ^a,b   Janssen, Dick B ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

COMPUTATIONAL CHEMISTRY; ENANTIOMERS; ENANTIOSELECTIVITY; ENZYMES; SUBSTRATES;

CARBON-HALOGEN BOND; COMPUTATIONAL APPROACH; COMPUTATIONALLY EFFICIENT; CONFORMATIONAL SAMPLINGS; DIFFERENT SUBSTRATES; ENZYME-SUBSTRATE COMPLEXES; MOLECULAR DYNAMICS SIMULATIONS; NUCLEOPHILIC ATTACK;

MOLECULAR DYNAMICS;

HALOALKANE DEHALOGENASE; HYDROLASE;

CHEMISTRY; ENZYME SPECIFICITY; METABOLISM; MOLECULAR DYNAMICS; PROTEIN CONFORMATION; STEREOISOMERISM; TIME;

HYDROLASES; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION; STEREOISOMERISM; SUBSTRATE SPECIFICITY; TIME FACTORS;

EID: 84904977463     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci500126x     Document Type: Article

References (90)

1. Schmid, A.; Dordick, J.; Hauer, B.; Kiener, A.; Wubbolts, M.; Witholt, B. Industrial biocatalysis today and tomorrow Nature 2001, 6817, 258-268
2. Bornscheuer, U. T.; Huisman, G. W.; Kazlauskas, R. J.; Lutz, S.; Moore, J. C.; Robins, K. Engineering the third wave of biocatalysis Nature 2012, 7397, 185-194
3. Eijsink, V.; Gaseidnes, S.; Borchert, T.; Van den Burg, B. Directed evolution of enzyme stability Biomol. Eng. 2005, 1-3, 21-30
4. Polizzi, K. M.; Bommarius, A. S.; Broering, J. M.; Chaparro-Riggers, J. F. Stability of biocatalysts Curr. Opin. Chem. Biol. 2007, 2, 220-225
5. Magliery, T. J.; Lavinder, J. J.; Sullivan, B. J. Protein stability by number: High-throughput and statistical approaches to one of protein sciences most difficult problems Curr. Opin. Chem. Biol. 2011, 3, 443-451
6. Wijma, H. J.; Floor, R. J.; Janssen, D. B. Structure- and sequence-analysis inspired engineering of proteins for enhanced thermostability Curr. Opin. Struct. Biol. 2013, 23, 588-594
7. Munoz Solano, D.; Hoyos, P.; Hernaiz, M. J.; Alcantara, A. R.; Sanchez-Montero, J. M. Industrial biotransformations in the synthesis of building blocks leading to enantiopure drugs Bioresour. Technol. 2012, 151, 196-207
8. Sukumaran, J.; Hanefeld, U. Enantioselective C-C bond synthesis catalysed by enzymes Chem. Soc. Rev. 2005, 6, 530-542
9. Reetz, M. T. Laboratory evolution of stereoselective enzymes: A prolific source of catalysts for asymmetric reactions Angew. Chem., Int. Ed. 2011, 1, 138-174
10. Koudelakova, T.; Bidmanova, S.; Dvorak, P.; Pavelka, A.; Chaloupkova, R.; Prokop, Z.; Damborsky, J. Haloalkane dehalogenases: Biotechnological applications Biotechnol. J. 2013, 1, 32-45
11. Pikkemaat, M. G.; Janssen, D. B. Generating segmental mutations in haloalkane dehalogenase: A novel part in the directed evolution toolbox Nucleic Acids Res. 2002, 8, E35-5
12. Chang, C. H.; Schindler, J. F.; Unkefer, C. J.; Vanderberg, L. A.; Brainard, J. R.; Terwilliger, T. C. In vivo screening of haloalkane dehalogenase mutants Bioorg. Med. Chem. 1999, 10, 2175-2181
13. Bosma, T.; Damborsky, J.; Stucki, G.; Janssen, D. B. Biodegradation of 1,2,3-trichloropropane through directed evolution and heterologous expression of a haloalkane dehalogenase gene Appl. Environ. Microbiol. 2002, 7, 3582-3587
14. Chaloupkova, R.; Sykorova, J.; Prokop, Z.; Jesenska, A.; Monincova, M.; Pavlova, M.; Tsuda, M.; Nagata, Y.; Damborsky, J. Modification of activity and specificity of haloalkane dehalogenase from Sphingomonas paucimobilis UT26 by engineering of its entrance tunnel J. Biol. Chem. 2003, 52, 52622-52628
15. Van Leeuwen, J. G. E.; Wijma, H. J.; Floor, R. J.; Van der Laan, J.; Janssen, D. B. Directed evolution strategies for enantiocomplementary haloalkane dehalogenases: From chemical waste to enantiopure building blocks ChemBioChem. 2012, 1, 137-148
16. Koudelakova, T.; Chaloupkova, R.; Brezovsky, J.; Prokop, Z.; Sebestova, E.; Hesseler, M.; Khabiri, M.; Plevaka, M.; Kulik, D.; Kuta Smatanova, I.; Rezacova, P.; Ettrich, R.; Bornscheuer, U. T.; Damborsky, J. Engineering enzyme stability and resistance to an organic cosolvent by modification of residues in the access tunnel Angew. Chem., Int. Ed. 2013, 7, 1959-1963
17. Arnold, F. H. Combinatorial and computational challenges for biocatalyst design Nature 2001, 6817, 253-257
18. Fox, R. J.; Davis, S. C.; Mundorff, E. C.; Newman, L. M.; Gavrilovic, V.; Ma, S. K.; Chung, L. M.; Ching, C.; Tam, S.; Muley, S.; Grate, J.; Gruber, J.; Whitman, J. C.; Sheldon, R. A.; Huisman, G. W. Improving catalytic function by ProSAR-driven enzyme evolution Nat. Biotechnol. 2007, 3, 338-344
19. Jackel, C.; Hilvert, D. Biocatalysts by evolution Curr. Opin. Biotechnol. 2010, 6, 753-759
20. Juhl, P. B.; Doderer, K.; Hollmann, F.; Thum, O.; Pleiss, J. Engineering of Candida antarctica lipase B for hydrolysis of bulky carboxylic acid esters J. Biotechnol. 2010, 4, 474-480
21. Pace, V.; Cortes Cabrera, A.; Ferrario, V.; Sinisterra, J. V.; Ebert, C.; Gardossi, L.; Braiuca, P.; Alcantara, A. R. Structural bases for understanding the stereoselectivity in ketone reductions with ADH from Thermus thermophilus: A quantitative model J. Mol. Catal. B 2011, 1-2, 23-31
22. Braiuca, P.; Lorena, K.; Ferrario, V.; Ebert, C.; Gardossi, L. A three-dimensional quanititative structure-activity relationship (3D-QSAR) model for predicting the enantioselectivity of Candida antarctica lipase B Adv. Synth. Catal. 2009, 9, 1293-1302
23. Seifert, A.; Antonovici, M.; Hauer, B.; Pleiss, J. An efficient route to selective bio-oxidation catalysts: an iterative approach comprising modeling, diversification, and screening, based on CYP102A1 ChemBioChem. 2011, 9, 1346-1351
24. Hediger, M. R.; De Vico, L.; Svendsen, A.; Besenmatter, W.; Jensen, J. H. A computational methodology to screen activities of enzyme variants PloS one 2012, 12, e49849-e49849
25. Zheng, H.; Reetz, M. T. Manipulating the stereoselectivity of limonene epoxide hydrolase by directed evolution based on iterative saturation mutagenesis J. Am. Chem. Soc. 2010, 44, 15744-15751
26. Stjernschantz, E.; van Vugt-Lussenburg, B. M.; Bonifacio, A.; de Beer, S. B.; van der Zwan, G.; Gooijer, C.; Commandeur, J. N.; Vermeulen, N. P.; Oostenbrink, C. Structural rationalization of novel drug metabolizing mutants of cytochrome P450 BM3 Proteins 2008, 1, 336-352
27. Kiss, G.; Rothlisberger, D.; Baker, D.; Houk, K. N. Evaluation and ranking of enzyme designs Protein Sci. 2010, 9, 1760-1773
28. Syren, P. O.; Hendil-Forssell, P.; Aumailley, L.; Besenmatter, W.; Gounine, F.; Svendsen, A.; Martinelle, M.; Hult, K. Esterases with an introduced amidase-like hydrogen bond in the transition state have increased amidase specificity ChemBioChem. 2012, 5, 645-648
29. Zheng, F.; Yang, W.; Ko, M. C.; Liu, J.; Cho, H.; Gao, D.; Tong, M.; Tai, H. H.; Woods, J. H.; Zhan, C. G. Most efficient cocaine hydrolase designed by virtual screening of transition states J. Am. Chem. Soc. 2008, 36, 12148-12155
30. Pan, Y.; Gao, D.; Yang, W.; Cho, H.; Yang, G.; Tai, H. H.; Zhan, C. G. Computational redesign of human butyrylcholinesterase for anticocaine medication Proc. Natl. Acad. Sci. U. S. A. 2005, 46, 16656-16661
31. Privett, H. K.; Kiss, G.; Lee, T. M.; Blomberg, R.; Chica, R. A.; Thomas, L. M.; Hilvert, D.; Houk, K. N.; Mayo, S. L. Iterative approach to computational enzyme design Proc. Natl. Acad. Sci. U.S.A. 2012, 10, 3790-3795
32. Bruice, T. C. Computational approaches: Reaction trajectories, structures, and atomic motions. Enzyme reactions and proficiency Chem. Rev. 2006, 8, 3119-3139
33. Negri, A.; Marco, E.; Damborsky, J.; Gago, F. Stepwise dissection and visualization of the catalytic mechanism of haloalkane dehalogenase LinB using molecular dynamics simulations and computer graphics J. Mol. Graph. Model 2007, 3, 643-651
34. 2- in a haloalkane dehalogenase Proc. Natl. Acad. Sci. U.S.A. 2003, 5, 2215-2219
35. Lau, E. Y.; Kahn, K.; Bash, P. A.; Bruice, T. C. The importance of reactant positioning in enzyme catalysis: A hybrid quantum mechanics/molecular mechanics study of a haloalkane dehalogenase Proc. Natl. Acad. Sci. U.S.A. 2000, 18, 9937-9942
36. Lightstone, F. C.; Zheng, Y. J.; Maulitz, A. H.; Bruice, T. C. Non-enzymatic and enzymatic hydrolysis of alkyl halides: a haloalkane dehalogenation enzyme evolved to stabilize the gas-phase transition state of an SN2 displacement reaction Proc. Natl. Acad. Sci. U.S.A. 1997, 16, 8417-8420
37. Bruice, T. C. A view at the millennium: the efficiency of enzymatic catalysis Acc. Chem. Res. 2002, 3, 139-148
38. Bruice, T.; Benkovic, S. Chemical basis for enzyme catalysis Biochemistry 2000, 21, 6267-6274
39. Warshel, A.; Sharma, P. K.; Kato, M.; Xiang, Y.; Liu, H.; Olsson, M. H. M. Electrostatic basis for enzyme catalysis Chem. Rev. 2006, 8, 3210-3235
40. Ranaghan, K. E.; Mulholland, A. J. Conformational effects in enzyme catalysis: QM/MM free energy calculation of the NAC contribution in chorismate mutase Chem. Commun. (Camb) 2004, 10, 1238-1239
41. Klepeis, J. L.; Lindorff-Larsen, K.; Dror, R. O.; Shaw, D. E. Long-timescale molecular dynamics simulations of protein structure and function Curr. Opin. Struct. Biol. 2009, 2, 120-127
42. Caves, L. S. D.; Evanseck, J. D.; Karplus, M. Locally accessible conformations of proteins: Multiple molecular dynamics simulations of crambin Protein Sci. 1998, 3, 649-666
43. Daggett, V. Long timescale simulations Curr. Opin. Struct. Biol. 2000, 2, 160-164
44. Monticelli, L.; Sorin, E. J.; Tieleman, D. P.; Pande, V. S.; Colombo, G. Molecular simulation of multistate peptide dynamics: A comparison between microsecond timescale sampling and multiple shorter trajectories J. Comput. Chem. 2008, 11, 1740-1752
45. Genheden, S.; Ryde, U. A comparison of different initialization protocols to obtain statistically independent molecular dynamics simulations J. Comput. Chem. 2011, 2, 187-195
46. Kiss, G.; Pande, V. S.; Houk, K. N. Molecular dynamics simulations for the ranking, evaluation, and refinement of computationally designed proteins Methods in Protein Design 2013, 523, 145-170
47. Keizers, P. H.; de Graaf, C.; de Kanter, F. J.; Oostenbrink, C.; Feenstra, K. A.; Commandeur, J. N.; Vermeulen, N. P. Metabolic regio- and stereoselectivity of cytochrome P450 2D6 towards 3,4-methylenedioxy-N- alkylamphetamines: In silico predictions and experimental validation J. Med. Chem. 2005, 19, 6117-6127
48. Westerbeek, A.; Szymanski, W.; Wijma, H. J.; Marrink, S. J.; Feringa, B. L.; Janssen, D. B. Kinetic resolution of alpha-bromoamides: Experimental and theoretical investigation of highly enantioselective reactions catalyzed by haloalkane dehalogenases Adv. Synth. Catalys. 2011, 6, 931-944
49. Pieters, R.; Spelberg, J.; Kellogg, R.; Janssen, D. The enantioselectivity of haloalkane dehalogenases Tetrahedron Lett. 2001, 3, 469-471
50. Prokop, Z.; Sato, Y.; Brezovsky, J.; Mozga, T.; Chaloupkova, R.; Koudelakova, T.; Jerabek, P.; Stepankova, V.; Natsume, R.; van Leeuwen, J. G.; Janssen, D. B.; Florian, J.; Nagata, Y.; Senda, T.; Damborsky, J. Enantioselectivity of haloalkane dehalogenases and its modulation by surface loop engineering Angew. Chem., Int. Ed. 2010, 35, 6111-6115
51. Szymanski, W.; Westerbeek, A.; Janssen, D. B.; Feringa, B. L. A simple enantioconvergent and chemoenzymatic synthesis of optically active alpha-substituted amides Angew. Chem., Int. Ed. 2011, 45, 10712-10715
52. Keuning, S.; Janssen, D. B.; Witholt, B. Purification and characterization of hydrolytic haloalkane dehalogenase from Xanthobacter autotrophicus GJ10 J. Bacteriol. 1985, 2, 635-639
53. Kulakova, A. N.; Larkin, M. J.; Kulakov, L. A. The plasmid-located haloalkane dehalogenase gene from Rhodococcus rhodochrous NCIMB 13064 Microbiology 1997, Pt 1, 109-115
54. Sato, Y.; Monincova, M.; Chaloupkova, R.; Prokop, Z.; Ohtsubo, Y.; Minamisawa, K.; Tsuda, M.; Damborsky, J.; Nagata, Y. Two rhizobial strains, Mesorhizobium loti MAFF303099 and Bradyrhizobium japonicum USDA110, encode haloalkane dehalogenases with novel structures and substrate specificities Appl. Environ. Microbiol. 2005, 8, 4372-4379
55. Nagata, Y.; Miyauchi, K.; Damborsky, J.; Manova, K.; Ansorgova, A.; Takagi, M. Purification and characterization of a haloalkane dehalogenase of a new substrate class from a gamma-hexachlorocyclohexane-degrading bacterium, Sphingomonas paucimobilis UT26 Appl. Environ. Microbiol. 1997, 9, 3707-3710
56. Verschueren, K. H.; Seljee, F.; Rozeboom, H. J.; Kalk, K. H.; Dijkstra, B. W. Crystallographic analysis of the catalytic mechanism of haloalkane dehalogenase Nature 1993, 6431, 693-698
57. Prokop, Z.; Monincova, M.; Chaloupkova, R.; Klvana, M.; Nagata, Y.; Janssen, D. B.; Damborsky, J. Catalytic mechanism of the haloalkane dehalogenase LinB from Sphingomonas paucimobilis UT26 J. Biol. Chem. 2003, 46, 45094-45100
58. Oakley, A. J.; Klvana, M.; Otyepka, M.; Nagata, Y.; Wilce, M. C.; Damborsky, J. Crystal structure of haloalkane dehalogenase LinB from Sphingomonas paucimobilis UT26 at 0.95 A resolution: dynamics of catalytic residues Biochemistry 2004, 4, 870-878
59. Newman, J.; Peat, T.; Richard, R.; Kan, L.; Swanson, P.; Affholter, J.; Holmes, I.; Schindler, J.; Unkefer, C.; Terwilliger, T. Haloalkane dehalogenases: Structure of a Rhodococcus enzyme Biochemistry 1999, 49, 16105-16114
60. Ridder, I. S.; Rozeboom, H. J.; Dijkstra, B. W. Haloalkane dehalogenase from Xanthobacter autotrophicus GJ10 refined at 1.15 A resolution Acta Crystallogr., Sect. D: Biol. Crystallogr. 1999, Pt 7, 1273-1290
61. Chaloupkova, R.; Prokop, Z.; Sato, Y.; Nagata, Y.; Damborsky, J. Stereoselectivity and conformational stability of haloalkane dehalogenase DbjA from Bradyrhizobium japonicum USDA110: The effect of pH and temperature FEBS J. 2011, 15, 2728-2738
62. a prediction by Ewald summation J. Mol. Graph. Model 2006, 4, 481-486
63. Ito, M.; Prokop, Z.; Klvana, M.; Otsubo, Y.; Tsuda, M.; Damborsky, J.; Nagata, Y. Degradation of beta-hexachlorocyclohexane by haloalkane dehalogenase LinB from gamma-hexachlorocyclohexane-utilizing bacterium Sphingobium sp. MI1205 Arch. Microbiol. 2007, 4, 313-325
64. Richter, F.; Leaver-Fay, A.; Khare, S. D.; Bjelic, S.; Baker, D. De novo enzyme design using Rosetta3 PLoS One 2011, 5, e19230
65. Stewart, J. Special issue-MOPAC: A semiempirical molecular-orbital program J. Comput. Aided Mol. Des. 1990, 1, 1-45
66. Jakalian, A.; Jack, D. B.; Bayly, C. I. Fast, efficient generation of high-quality atomic charges. AM1-BCC model: II. Parameterization and validation J. Comput. Chem. 2002, 16, 1623-1641
67. Morris, G. M.; Huey, R.; Lindstrom, W.; Sanner, M. F.; Belew, R. K.; Goodsell, D. S.; Olson, A. J. AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility J. Comput. Chem. 2009, 16, 2785-2791
68. Krieger, E.; Darden, T.; Nabuurs, S.; Finkelstein, A.; Vriend, G. Making optimal use of empirical energy functions: Force-field parameterization in crystal space Prot. Struct. Funct. Bioinform. 2004, 4, 678-683
69. Berendsen, H. J. C.; Postma, J. P. M.; Van Gunsteren, W. F.; Dinola, A.; Haak, J. R. Molecular-dynamics with coupling to an external bath J. Chem. Phys. 1984, 8, 3684-3690
70. Hess, B.; Bekker, H.; Berendsen, H.; Fraaije, J. LINCS: A linear constraint solver for molecular simulations J. Comput. Chem. 1997, 12, 1463-1472
71. Miyamoto, S.; Kollman, P. A. SETTLE-An analytical version of the Shake and Rattle algorithm for rigid water models J. Comput. Chem. 1992, 8, 952-962
72. Essmann, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G. A smooth particle Mesh Ewald method J. Chem. Phys. 1995, 19, 8577-8593
73. Duan, Y.; Wu, C.; Chowdhury, S.; Lee, M. C.; Xiong, G.; Zhang, W.; Yang, R.; Cieplak, P.; Luo, R.; Lee, T.; Caldwell, J.; Wang, J.; Kollman, P. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations J. Comput. Chem. 2003, 16, 1999-2012
74. Cook, P.; Cleland, W. W. Enzyme kinetics and mechanism; Garland Science: London, 2007.
75. Huey, R.; Morris, G. M.; Olson, A. J.; Goodsell, D. S. A semiempirical free energy force field with charge-based desolvation J. Comput. Chem. 2007, 6, 1145-1152
76. Wang, J.; Cieplak, P.; Kollman, P. How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem. 2000, 12, 1049-1074
77. Lange, O. F.; van der Spoel, D.; de Groot, B. L. Scrutinizing molecular mechanics force fields on the submicrosecond timescale with NMR data Biophys. J. 2010, 2, 647-655
78. Lindorff-Larsen, K.; Piana, S.; Palmo, K.; Maragakis, P.; Klepeis, J. L.; Dror, R. O.; Shaw, D. E. Improved side-chain torsion potentials for the Amber ff99SB protein force field Proteins 2010, 8, 1950-1958
79. Kmunicek, J.; Bohac, M.; Luengo, S.; Gago, F.; Wade, R. C.; Damborsky, J. Comparative binding energy analysis of haloalkane dehalogenase substrates: modelling of enzyme-substrate complexes by molecular docking and quantum mechanical calculations J. Comput.-Aided Mol. Des. 2003, 5-6, 299-311
80. Stjernschantz, E.; Vermeulen, N. P.; Oostenbrink, C. Computational prediction of drug binding and rationalisation of selectivity towards cytochromes P450 Expert Opin. Drug Metab. Toxicol. 2008, 5, 513-527
81. Pries, F.; van den Wijngaard, A. J.; Bos, R.; Pentenga, M.; Janssen, D. B. The role of spontaneous cap domain mutations in haloalkane dehalogenase specificity and evolution J. Biol. Chem. 1994, 26, 17490-17494
82. Banas, P.; Otyepka, M.; Jerabek, P.; Petrek, M.; Damborsky, J. Mechanism of enhanced conversion of 1,2,3-trichloropropane by mutant haloalkane dehalogenase revealed by molecular modeling J. Comput.-Aided Mol. Des. 2006, 6, 375-383
83. Schanstra, J. P.; Kingma, J.; Janssen, D. B. Specificity and kinetics of haloalkane dehalogenase J. Biol. Chem. 1996, 25, 14747-14753
84. Shaw, D. E.; Maragakis, P.; Lindorff-Larsen, K.; Piana, S.; Dror, R. O.; Eastwood, M. P.; Bank, J. A.; Jumper, J. M.; Salmon, J. K.; Shan, Y.; Wriggers, W. Atomic-level characterization of the structural dynamics of proteins Science 2010, 6002, 341-346
85. Genheden, S.; Ryde, U. Will molecular dynamics simulations of proteins ever reach equilibrium? Phys. Chem. Chem. Phys. 2012, 24, 8662-8677
86. Genheden, S.; Ryde, U. How to obtain statistically converged MM/GBSA results J. Comput. Chem. 2010, 4, 837-846
87. Genheden, S.; Diehl, C.; Akke, M.; Ryde, U. Starting-condition dependence of order parameters derived from molecular dynamics simulations J. Chem. Theory Comput. 2010, 7, 2176-2190
88. Zagrovic, B.; van Gunsteren, W. F. Computational analysis of the mechanism and thermodynamics of inhibition of phosphodiesterase 5A by synthetic ligands J. Chem. Theory Comput. 2007, 1, 301-311
89. Lind, M. E. S.; Himo, F. Quantum chemistry as a tool in asymmetric biocatalysis: Limonene epoxide hydrolase test case Angew. Chem., Int. Ed. 2013, 17, 4563-4567
90. Lonsdale, R.; Harvey, J. N.; Mulholland, A. J. A practical guide to modelling enzyme-catalysed reactions Chem. Soc. Rev. 2012, 8, 3025-3038