New insights into the molecular mechanism of methanol-induced inactivation of Thermomyces lanuginosus lipase: a molecular dynamics simulation study

References

• Lotti M, Pleiss J, Valero F, Ferrer P. Effects of methanol on lipases: molecular, kinetic and process issues in the production of biodiesel. Biotechnol J. 2015;10(1):22–30. 10.1002/biot.201400158.
   PubMed Web of Science ®Google Scholar
• Ma F, Hanna MA. Biodiesel production: a review. Bioresour Technol. 1999;70(1):1–15. doi:10.1016/S0960-8524(99)00025-5.
   Web of Science ®Google Scholar
• Nielsen PM, Brask J, Fjerbaek L. Enzymatic biodiesel production: technical and economical considerations. Eur J Lipid Sci Technol. 2008;110(8):692–700. doi:10.1002/ejlt.200800064.
   Web of Science ®Google Scholar
• Fukuda H, Hama S, Tamalampudi S, Noda H. Whole-cell biocatalysts for biodiesel fuel production. Trends Biotechnol. 2008;26(12):668–673. doi:10.1016/j.tibtech.2008.08.001.
   PubMed Web of Science ®Google Scholar
• Cesarini S, Diaz P, Nielsen PM. Exploring a new, soluble lipase for FAMEs production in water-containing systems using crude soybean oil as a feedstock. Process Biochem. 2013;48(3):484–487. doi:10.1016/j.procbio.2013.02.001.
   Web of Science ®Google Scholar
• Price JA, Nordblad M, Woodley J, Huusom JK. Fed-batch feeding strategies for enzymatic biodiesel production. Paper presented at: 19th World Congress of the International Federation of Automatic Control; 2014 August 24–29; Cape Town, South Africa.
   Google Scholar
• Cesarini S, Haller RF, Diaz P, Nielsen PM. Combining phospholipases and a liquid lipase for one-step biodiesel production using crude oils. Biotechnol Biofuels. 2014;7(1):29–40. doi:10.1186/1754-6834-7-29.
   PubMed Web of Science ®Google Scholar
• Price J, Hofmann B, Silva VT, Nordblad M, Woodley JM, Huusom JK. Mechanistic modeling of biodiesel production using a liquid lipase formulation. Biotechnol Prog. 2014;30(6):1277–1290. doi:10.1002/btpr.1985.
   PubMed Web of Science ®Google Scholar
• Derewenda U, Swenson L, Wei Y, Green R, Kobos PM, Joerger R, Haas MJ, Derewenda ZS. Conformational lability of lipases observed in the absence of an oil-water interface: crystallographic studies of enzymes from the fungi Humicola lanuginosa and Rhizopus delemar. J Lipid Res. 1994;35:524–534.
   PubMed Web of Science ®Google Scholar
• Brzozowski AM, Savage H, Verma CS, Turkenburg JP, Lawson DM, Svendsen A, Patkar S. Structural origins of the interfacial activation in Thermomyces (Humicola) lanuginosa lipase. Biochemistry. 2000;39(49):15071–15082. doi:10.1021/bi0013905.
   PubMed Web of Science ®Google Scholar
• Svendsen A. Lipase protein engineering. Biochim Biophys Acta. 2000;1543(2):223–238. doi:10.1016/S0167-4838(00)00239-9.
   PubMed Web of Science ®Google Scholar
• Brady L, Brzozowski AM, Derewenda ZS, Dodson E, Dodson G, Tolley S, Turkenburg JP, Christiansen L, Huge-Jensen B, Norskov L, Thim L, Menge U. A serine protease triad forms the catalytic centre of a triacylglycerol lipase. Nature. 1990;343(6260):767–770. doi:10.1038/343767a0.
   PubMed Web of Science ®Google Scholar
• Kamal M, Yedavalli P, Deshmukh MV, Rao NM. Lipase in aqueous-polar organic solvents: activity, structure, and stability. Protein Sci. 2013;22(7):904–915. doi:10.1002/pro.2271.
   PubMed Web of Science ®Google Scholar
• Mattos C, Bellamacina CR, Peisach E, Pereira A, Vitkup D, Petsko GA, Ringe D. Multiple solvent crystal structures: probing binding sites, plasticity and hydration. J Mol Biol. 2006;357(5):1471–1482. doi:10.1016/j.jmb.2006.01.039.
   PubMed Web of Science ®Google Scholar
• Tanaka A. Differential scanning calorimetric studies on the thermal unfolding of Pseudomonas cepacia lipase in the absence and presence of alcohols. J Biochem. 1998;123(2):289–293. doi:10.1093/oxfordjournals.jbchem.a021935.
   PubMed Web of Science ®Google Scholar
• 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/simulations. J Biol Chem. 2010;285(37):28434–28441. doi:10.1074/jbc.M110.136200.
   PubMed Web of Science ®Google Scholar
• Park HJ, Joo JC, Park K, Kim YH, Yoo YJ. Prediction of the solvent affecting site and the computational design of stable Candida antarctica lipase B in a hydrophilic organic solvent. J Biotechnol. 2013;163(3):346–352. doi:10.1016/j.jbiotec.2012.11.006.
   PubMed Web of Science ®Google Scholar
• Li L, Jiang Y, Zhang H, Feng W, Chen B, Tan T. Theoretical and experimental studies on activity of Yarrowia lipolytica lipase in methanol/water mixtures. J Phys Chem B. 2014;118:1976–1983.
   PubMed Web of Science ®Google Scholar
• Kellogg EH, Leaver-Fay A, Baker D. Role of conformational sampling in computing mutation-induced changes in protein structure and stability. Proteins. 2011;79(3):830–838. doi:10.1002/prot.22921.
   PubMed Web of Science ®Google Scholar
• Liu Y, Kuhlman B. RosettaDesign server for protein design. Nucleic Acids Res. 2006;34:W235–W238. doi:10.1093/nar/gkl163.
   PubMed Web of Science ®Google Scholar
• Dennington R, Keith T, Millam J. GaussView, version 5. Shawnee Mission (KS): Semichem, Inc.; 2009.
   Google Scholar
• Anandakrishnan R, Aguilar B, Onufriev AV. H++ 3.0: automating pK prediction and the preparation of biomolecular structures for atomistic molecular modeling and simulations. Nucleic Acids Res. 2012;40(W1):W537–W541. doi:10.1093/nar/gks375.
   PubMed Web of Science ®Google Scholar
• Case D, Darden T, Cheatham T III, Simmerling C, Wang J, Duke R, Luo R, Walker R, Zhang W, Merz K. AMBER 12. San Francisco (CA): University of California; 2012.
   Google Scholar
• Wang J, Wang W, Kollman PA, Case DA. Automatic atom type and bond type perception in molecular mechanical calculations. J Mol Graph Model. 2006;25(2):247–260. doi:10.1016/j.jmgm.2005.12.005.
   PubMed Web of Science ®Google Scholar
• Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. Comparison of simple potential functions for simulating liquid water. J Chem Phys. 1983;79(2):926–935. doi:10.1063/1.445869.
   Web of Science ®Google Scholar
• Cieplak P, Caldwell J, Kollman P. Molecular mechanical models for organic and biological systems going beyond the atom centered two body additive approximation: aqueous solution free energies of methanol and N-methyl acetamide, nucleic acid base, and amide hydrogen bonding and chloroform/water partition coefficients of the nucleic acid bases. J Comput Chem. 2001;22(10):1048–1057. doi:10.1002/jcc.1065.
   Web of Science ®Google Scholar
• Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, Simmerling C. Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins. 2006;65(3):712–725. doi:10.1002/prot.21123.
   PubMed Web of Science ®Google Scholar
• Wang J, Wolf RM, Caldwell JW, Kollman PA, Case DA. Development and testing of a general amber force field. J Comput Chem. 2004;25(9):1157–1174. doi:10.1002/jcc.20035.
   PubMed Web of Science ®Google Scholar
• Torda AE, Scheek RM, Van Gunsteren WF. Time-dependent distance restraints in molecular dynamics simulations. Chem Phys Lett. 1989;157(4):289–294. doi:10.1016/0009-2614(89)87249-5.
   Web of Science ®Google Scholar
• Miyamoto S, Kollman PA. SETTLE: an analytical version of the SHAKE and RATTLE algorithm for rigid water models. J Comput Chem. 1992;13(8):952–962. doi:10.1002/jcc.540130805.
   Web of Science ®Google Scholar
• Roe DR, Cheatham TE III. PTRAJ and CPPTRAJ: software for processing and analysis of molecular dynamics trajectory data. J Chem Theory Comput. 2013;9(7):3084–3095. doi:10.1021/ct400341p.
   PubMed Web of Science ®Google Scholar
• Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics. J Mol Graph. 1996;14(1):33–38. doi:10.1016/0263-7855(96)00018-5.
   PubMedGoogle Scholar
• Lobanov MI, Bogatyreva NS, Galzitskaya OV. Radius of gyration as an indicator of protein structure compactness. Mol Biol (Mosk). 2008;42(4):623–628. doi:10.1134/S0026893308040195.
   Web of Science ®Google Scholar
• Zhu K, Jutila A, Tuominen EK, Kinnunen PK. Effects of i-propanol on the structural dynamics of Thermomyces lanuginosa lipase revealed by tryptophan fluorescence. Protein Sci. 2001;10(2):339–351. doi:10.1110/ps.21201.
   PubMed Web of Science ®Google Scholar
• Fitzpatrick PA, Steinmetz AC, Ringe D, Klibanov AM. Enzyme crystal structure in a neat organic solvent. Proc Natl Acad Sci USA. 1993;90(18):8653–8657. doi:10.1073/pnas.90.18.8653.
   PubMed Web of Science ®Google Scholar
• Weiser J, Shenkin PS, Still WC. Approximate atomic surfaces from linear combinations of pairwise overlaps (LCPO). J Comput Chem. 1999;20(2):217–230. 10.1002/(SICI)1096-987X(19990130)20:2 < 217:AID-JCC4>3.0.CO;2-A.
   Web of Science ®Google Scholar
• Gekko K, Ohmae E, Kameyama K, Takagi T. Acetonitrile–protein interactions: amino acid solubility and preferential solvation. Biochim Biophys Acta. 1998;1387(1-2):195–205. doi:10.1016/S0167-4838(98)00121-6.
   PubMed Web of Science ®Google Scholar
• Sashi P, Yasin UM, Bhuyan AK. Unfolding action of alcohols on a highly negatively charged state of cytochrome c. Biochemistry. 2012;51(15):3273–3283. doi:10.1021/bi201716r.
   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(8):653–659. doi:10.1080/08927022.2012.758850.
   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(2):812–821. doi:10.1529/biophysj.104.041269.
   PubMed Web of Science ®Google Scholar
• Hünenberger P, Mark A, Van Gunsteren W. Fluctuation and cross-correlation analysis of protein motions observed in nanosecond molecular dynamics simulations. J Mol Biol. 1995;252:492–503.
   PubMed Web of Science ®Google Scholar
• Dror A, Shemesh E, Dayan N, Fishman A. Protein engineering by random mutagenesis and structure-guided consensus of Geobacillus stearothermophilus Lipase T6 for enhanced stability in methanol. Appl Environ Microbiol. 2014;80(4):1515–1527. doi:10.1128/AEM.03371-13.
   PubMed Web of Science ®Google Scholar
• Reetz MT, Soni P, Fernández L, Gumulya Y, Carballeira JD. Increasing the stability of an enzyme toward hostile organic solvents by directed evolution based on iterative saturation mutagenesis using the B-FIT method. Chem Commun (Camb). 2010;46(45):8657–8658. doi:10.1039/c0cc02657c.
   PubMed Web of Science ®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
• Liu W, Bratko D, Prausnitz JM, Blanch HW. Effect of alcohols on aqueous lysozyme-lysozyme interactions from static light-scattering measurements. Biophys Chem. 2004;107(3):289–298. doi:10.1016/j.bpc.2003.09.012.
   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(8):2575–2585. doi:10.1021/jp211054u.
   PubMed Web of Science ®Google Scholar
• Cruz A, Ramirez E, Santana A, Barletta G, López GE. Molecular dynamic study of subtilisin Carlsberg in aqueous and nonaqueous solvents. Mol Simul. 2009;35(3):205–212. doi:10.1080/08927020802415670.
   Web of Science ®Google Scholar
• Wangikar PP, Michels PC, Clark DS, Dordick JS. Structure and function of subtilisin BPN’ solubilized in organic solvents. J Am Chem Soc. 1997;119(1):70–76. doi:10.1021/ja962620z.
   Web of Science ®Google Scholar
• Micaêlo NM, Soares CM. Modeling hydration mechanisms of enzymes in nonpolar and polar organic solvents. FEBS J. 2007;274:2424–2436.
   PubMed Web of Science ®Google Scholar
• Badoei-Dalfard A, Khajeh K, Asghari SM, Ranjbar B, Karbalaei-Heidari HR. Enhanced activity and stability in the presence of organic solvents by increased active site polarity and stabilization of a surface loop in a metalloprotease. J Biochem. 2010;148(2):231–238. doi:10.1093/jb/mvq057.
   PubMed Web of Science ®Google Scholar