To keep or not to keep? the question of crystallographic waters for enzyme simulations in organic solvent

References

• Zaks A, Klibanov AM. Enzymatic catalysis in nonaqueous solvents. J. Biol. Chem. 1988;263:3194–3201.
   PubMed Web of Science ®Google Scholar
• Gupta MN. Enzyme function in organic solvents. Eur. J. Biochem. 1992;203:25–32.10.1111/ejb.1992.203.issue-1-2
   PubMedGoogle Scholar
• Huang YK, Tsai SW. Kinetic and thermodynamic analysis of Candida antarctica lipase B-catalyzed alcoholytic resolution of (R,S)-β-butyrolactone in organic solvents. Appl. Microbiol. Biotechnol. 2014;98:621–628.10.1007/s00253-013-5331-x
   PubMed Web of Science ®Google Scholar
• Lou FW, Liu BK, Wu Q, et al. Candida antarctica lipase B (CAL-B)-catalyzed carbon-sulfur bond addition and controllable selectivity in organic media. Adv. Synth. Catal. 2008;350:1959–1962.10.1002/adsc.v350:13
   Web of Science ®Google Scholar
• Li C, Tan T, Zhang H, et al. Analysis of the conformational stability and activity of Candida antarctica lipase B in organic solvents. J. Biol. Chem. 2010;285:28434–28441.10.1074/jbc.M110.136200
   PubMed Web of Science ®Google Scholar
• Park HJ, Park K, Yoo YJ. Understanding the effect of tert-butanol on Candida antarctica lipase B using molecular dynamics simulations. Mol. Simul. 2013;39:653–659.10.1080/08927022.2012.758850
   Web of Science ®Google Scholar
• Zhu L, Yang W, Meng YY, et al. Effects of organic solvent and crystal water on γ-chymotrypsin in acetonitrile media: observations from molecular dynamics simulation and DFT calculation. J. Phys. Chem. B. 2012;116:3292–3304.10.1021/jp3002405
   PubMed Web of Science ®Google Scholar
• Toba S, Hartsough DS, Merz KM Jr. Solvation and dynamics of chymotrypsin in hexane. J. Am. Chem. Soc. 1996;118:6490–6498.10.1021/ja960153f
   Web of Science ®Google Scholar
• Colombo G, Toba S, Merz KM Jr. Rationalization of the enantioselectivity of subtilisin in DMF. J. Am. Chem. Soc. 1999;121:3486–3493.10.1021/ja9839062
   Web of Science ®Google Scholar
• Lousa D, Cianci M, Helliwell JR, et al. Interaction of counterions with subtilisin in acetonitrile: insights from molecular dynamics simulations. J. Phys. Chem. B. 2012;116:5838–5848.10.1021/jp303008g
   PubMed Web of Science ®Google Scholar
• Zheng YJ, Ornstein RL. A molecular dynamics and quantum mechanics analysis of the effect of DMSO on enzyme structure and dynamics: subtilisin. J. Am. Chem. Soc. 1996;118:4175–4180.10.1021/ja9539195
   Web of Science ®Google Scholar
• Zheng YJ, Ornstein RL. A molecular dynamics study of the effect of carbon tetrachloride on enzyme structure and dynamics: subtilisin. Protein Eng. Des. Sel. 1996;9:485–492.
   Web of Science ®Google Scholar
• Tejo BA, Salleh AB, Pleiss J. Structure and dynamics of Candida rugosa lipase: the role of organic solvent. J. Mol. Model. 2004;10:358–366.10.1007/s00894-004-0203-z
   PubMed Web of Science ®Google Scholar
• Clark DS. Characteristics of nearly dry enzymes in organic solvents: implications for biocatalysis in the absence of water. Philos. Trans. R. Soc. Lond. 2004;359:1299–1307.10.1098/rstb.2004.1506
   PubMed Web of Science ®Google Scholar
• Ke T, Tidor B, Klibanov AM. Molecular-modeling calculations of enzymatic enantioselectivity taking hydration into account. Biotechnol. Bioeng. 1998;57:741–745.10.1002/(ISSN)1097-0290
   PubMed Web of Science ®Google Scholar
• Wedberg R, Abildskov J, Peters GH. Protein dynamics in organic media at varying water activity studied by molecular dynamics simulation. J. Phys. Chem. B. 2012;116:2575–2585.10.1021/jp211054u
   PubMed Web of Science ®Google Scholar
• Berman HM, Westbrook J, Feng Z, et al. The Protein Data Bank. Nucleic Acids Res. 2000;28:235–242.10.1093/nar/28.1.235
   PubMed Web of Science ®Google Scholar
• Ru MT, Hirokane SY, Lo AS, et al. On the salt-induced activation of lyophilized enzymes in organic solvents: effect of salt kosmotropicity on enzyme activity. J. Am. Chem. Soc. 1999;122:1565–1571.
   Web of Science ®Google Scholar
• Halling PJ. What can we learn by studying enzymes in non-aqueous media? Philos. Trans. R. Soc. Lond. B. 2004;359:1287–1297.10.1098/rstb.2004.1505
   PubMed Web of Science ®Google Scholar
• Trodler P, Pleiss J. Modeling structure and flexibility of Candida antarctica lipase B in organic solvents. BMC. Struct. Biol. 2008;8:9.10.1186/1472-6807-8-9
   PubMed Web of Science ®Google Scholar
• Stella L, Melchionna S. Equilibration and sampling in molecular dynamics simulations of biomolecules. J. Chem. Phys. 1998;109:10115–10117.10.1063/1.477703
   Web of Science ®Google Scholar
• Daggett V, Levitt M. Realistic simulations of native-protein dynamics in solution and beyond. Annu. Rev. Biophys. Biomol. Struct. 1993;22:353–380.10.1146/annurev.bb.22.060193.002033
   PubMedGoogle Scholar
• Schopf P, Warshel A. Validating computer simulations of enantioselective catalysis; reproducing the large steric and entropic contributions in Candida antarctica lipase B. Proteins. 2014;82:1387–1399.10.1002/prot.v82.7
   PubMed Web of Science ®Google Scholar
• Walton EB, VanVliet KJ. Equilibration of experimentally determined protein structures for molecular dynamics simulation. Phys. Rev. E. 2006;74:061901–1-8.10.1103/PhysRevE.74.061901
   Web of Science ®Google Scholar
• Baysal C, Atilgan AR. Relaxation kinetics and the glassiness of proteins: the case of bovine pancreatic trypsin inhibitor. Biophys. J. 2002;83:699–705.10.1016/S0006-3495(02)75201-6
   PubMed Web of Science ®Google Scholar
• Anderssen RS, Husain SA, Loy RJ. The Kohlrausch function: properties and applications. ANZIAM. J. 2003;45:C800–C816.
   Google Scholar
• Kohlrausch R. Pogg. Ann. Phys. Chem. 1854;91:56.10.1002/(ISSN)1521-3889
   Google Scholar
• Williams G, Watts D. Non-symmetrical dielectric relaxation behaviour arising from a simple empirical decay function. Trans. Faraday Soc. 1970;66:80–85.10.1039/tf9706600080
   Google Scholar
• Auffinger P, Louise-May S, Westhof E. Multiple molecular dynamics simulations of the anticodon loop of tRNAAsp in aqueous solution with counterions. J. Am. Chem. Soc. 1995;117:6720–6726.10.1021/ja00130a011
   Web of Science ®Google Scholar
• Kirk O, Christensen MW. Lipases from Candida antarctica: unique biocatalysts from a unique origin. Org. Process. Res. Dev. 2002;6:446–451.10.1021/op0200165
   Web of Science ®Google Scholar
• Vazquez-Duhalt R, Semple KM, Westlake DWS, et al. Effect of water-miscible organic solvents on the catalytic activity of cytochrome C. Enzyme. Microb. Tech. 1993;15:936–943.10.1016/0141-0229(93)90169-3
   PubMed Web of Science ®Google Scholar
• Bushnell GW, Louie GV, Brayer GD. High-resolution three-dimensional structure of horse heart cytochrome C. J. Mol. Biol. 1990;214:585–595.10.1016/0022-2836(90)90200-6
   PubMed Web of Science ®Google Scholar
• Duarte DR, Castillo E, Barzana E, et al. Capsaicin hydrolysis by Candida antarctica lipase. Biotechnol. Lett. 2000;22:1811–1814.10.1023/A:1005622704504
   Web of Science ®Google Scholar
• Guyot B, Bosquette B, Pina M, et al. Esterification of phenolic acids from green coffee with an immobilized lipase from Candida antarctica in solvent-free medium. Biotechnol. Lett. 1997;19:529–532.10.1023/A:1018381102466
   Web of Science ®Google Scholar
• Ljunger G, Adlercreutz P, Mattiasson B. Lipase catalyzed acylation of glucose. Biotechnol. Lett. 1994;16:1167–1172.10.1007/BF01020845
   Web of Science ®Google Scholar
• Rahman MBA, Chaibakhsh N, Basri M. Effect of alcohol structure on the optimum condition for Novozym 435-Catalyzed synthesis of adipate esters. Biotechnol. Res. Int. 2011;2011:162987.
   PubMedGoogle Scholar
• Deng L, Xu X, Haraldsson GG, et al. Enzymatic production of alkyl esters through alcoholysis: a critical evaluation of lipases and alcohols. J. Am. Oil. Chem. Soc. 2005;82:341–347.10.1007/s11746-005-1076-3
   Web of Science ®Google Scholar
• Pulawski W, Filipek S, Debinski AZA, et al. Low-temperature molecular dynamics simulation of horse heart cytochrome C and comparison with inelastic neutron scattering data. Eur. Biophys. J. 2013;42:291–300.10.1007/s00249-012-0874-9
   PubMed Web of Science ®Google Scholar
• Zaidi S, Hassan MI, Islam A, et al. The role of key residues in structure, function, and stability of cytochrome-C. Cell. Mol. Life. Sci. 2014;71:229–255.10.1007/s00018-013-1341-1
   PubMed Web of Science ®Google Scholar
• Kamatari YJ, Konno T, Kataoka M, et al. The methanol-induced globular and expanded denatured states of cytochrome C: a study by CD fluorescence, NMR and small-angle X-ray scattering. J. Mol. Biol. 1996;259:512–523.10.1006/jmbi.1996.0336
   PubMed Web of Science ®Google Scholar
• Hess B, Kutzner C, van der Spoel D, et al. GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 2008;4:435–447.10.1021/ct700301q
   PubMed Web of Science ®Google Scholar
• Oostenbrink C, Villa A, Mark AE, et al. A biomolecular force field based on the free enthalpy of hydration and solvation: the GROMOS force-field parameter sets 53A5 and 53A6. J. Comput. Chem. 2004;25:1656–1676.10.1002/(ISSN)1096-987X
   PubMed Web of Science ®Google Scholar
• Jorgensen WL, Maxwell DS, Tirado-Rives J. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 1996;118:11225–11236.10.1021/ja9621760
   Web of Science ®Google Scholar
• Jorgensen WL. Optimized intermolecular potential functions for liquid alcohols. J. Phys. Chem. 1986;90:1276–1284.10.1021/j100398a015
   Web of Science ®Google Scholar
• Price MLP, Ostrovsky D, Jorgensen WL. Gas-phase and liquid-state properties of esters, nitriles, and nitro compounds with the OPLS-AA force field. J. Comp. Chem. 2001;22:1340–1352.10.1002/(ISSN)1096-987X
   Web of Science ®Google Scholar
• Berendsen HJC, Grigera JR, Straatsma TP. The missing term in effective pair potentials. J. Phys. Chem. 1987;91:6269–6271.10.1021/j100308a038
   Web of Science ®Google Scholar
• Hess B, Bekker H, Berendsen HJC, et al. LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 1997;18:1463–1472.10.1002/(ISSN)1096-987X
   Web of Science ®Google Scholar
• Darden T, York D, Pedersen L. Particle mesh Ewald: an N⋅log(N) method for Ewald sums in large systems. J. Chem. Phys. 1993;98:10089–10092.10.1063/1.464397
   Web of Science ®Google Scholar
• Arfken G. Mathematical methods for physicists. 3rd ed. Orlando (FL): Academic Press; 1985.
   Google Scholar
• Bussi G, Donadio D, Parrinello M. Canonical sampling through velocity rescaling. J. Chem. Phys. 2007;126:014101–1-7.10.1063/1.2408420
   PubMed Web of Science ®Google Scholar
• Berendsen HJC, Postma JPM, van Gunsteren WF, et al. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 1984;81:3684–3690.10.1063/1.448118
   Web of Science ®Google Scholar
• Uppenberg J, Hansen MT, Patkar S, et al. The sequence, crystal structure determination and refinement of two crystal forms of lipase B from Candida antarctica. Structure. 1994;2:293–308.10.1016/S0969-2126(00)00031-9
   PubMed Web of Science ®Google Scholar
• Bushnell GW, Louie GV, Brayer DG. High-resolution three-dimensional structure of horse heart cytochrome C. J. Mol. Biol. 1990;214:585–595.10.1016/0022-2836(90)90200-6
   PubMed Web of Science ®Google Scholar
• Qi PX, Urbauer JL, Fuentes EJ, et al. Structural water in oxidized and reduced horse heart cytochrome C. Nat. Struct. Biol. 1994;1:378–382.10.1038/nsb0694-378
   PubMedGoogle Scholar
• Mijovic J, Bian Y, Gross RA, et al. Dynamics of proteins in hydrated state and in solution as studied by dielectric relaxation spectroscopy. Macromolecules. 2005;38:10812–10819.10.1021/ma051854c
   Web of Science ®Google Scholar
• Soares CM, Teixeira VH, Baptista AM. Protein structure and dynamics in nonaqueous solvents: insights from molecular dynamics simulation studies. Biophys. J. 2003;84:1628–1641.10.1016/S0006-3495(03)74972-8
   PubMed Web of Science ®Google Scholar
• Micaelo NM, Soares CM. Modeling hydration mechanisms of enzymes in nonpolar and polar organic solvents. FEBS. J. 2007;274:2424–2436.10.1111/ejb.2007.274.issue-9
   PubMed Web of Science ®Google Scholar
• Klibanov AM. Improving enzymes by using them in organic solvents. Nature. 2001;409:241–246.10.1038/35051719
   PubMed Web of Science ®Google Scholar
• Mattos C, Ringe D. Proteins in organic solvents. Curr. Opin. Struct. Biol. 2001;11:761–764.10.1016/S0959-440X(01)00278-0
   PubMed Web of Science ®Google Scholar
• Berliner LJ, Reuben J. Biological magnetic resonance. Vol. 4. New York (NY): Plenum Press; 1982.10.1007/978-1-4615-6540-6
   Google Scholar
• Zisis T, Freddolino PL, Turunen P, et al. Interfacial activation of Candida antarctica lipase B: combined evidence from experiment and simulation. Biochemistry. 2015;54:5969–5979.10.1021/acs.biochem.5b00586
   PubMed Web of Science ®Google Scholar
• Affleck R, Haynes CA, Clark DS. Solvent dielectric effects on protein dynamics. Proc. Natl. Acad. Sci. USA. 1992;89:5009–5010.
   Google Scholar
• Zaks A, Klibanov AM. The effect of water on enzyme action in organic media. J. Biol. Chem. 1988;263:8017–8021.
   PubMed Web of Science ®Google Scholar
• Yang L, Dordick JS, Garde S. Hydration of enzyme in nonaqueous media is consistent with solvent dependence of its activity. Biophys. J. 2004;87:812–821.10.1529/biophysj.104.041269
   PubMed Web of Science ®Google Scholar
• Micaelo NM, Teixeira VH, Baptista AM, et al. Water dependent properties of cutinase in nonaqueous solvents: a computational study of enantioselectivity. Biophys. J. 2005;89:999–1008.10.1529/biophysj.105.063297
   PubMed Web of Science ®Google Scholar
• Díaz-Vergara N, Piñeiro A. Molecular dynamics study of triosephosphate isomerase from Trypanosoma cruzi in water/decane mixtures. J. Phys. Chem. B. 2008;112:3529–3539.10.1021/jp7102275
   PubMed Web of Science ®Google Scholar
• Cruz A, Ramirez E, Santana A, et al. Molecular dynamic study of subtilisin Carlsberg in aqueous and nonaqueous solvents. Mol. Simul. 2009;35:205–212.10.1080/08927020802415670
   Web of Science ®Google Scholar