Molecular dynamics simulations of cellulase homologs in aqueous 1-ethyl-3-methylimidazolium chloride

References

• Badieyan, S., Bevan, D. R., & Zhang, C. (2012). Study and design of stability in GH5 cellulases. Biotechnology and Bioengineering, 109, 31–44.10.1002/bit.v109.1
   PubMed Web of Science ®Google Scholar
• Baker, J. O., Adney, W. S., Nleves, R. A., Thomas, S. R., Wilson, D. B., & Himmel, M. E. (1994). A new thermostable endoglucanase, Acidothermus cellulolyticus E1. Applied Biochemistry and Biotechnology, 45–46, 245–256.10.1007/BF02941803
   Web of Science ®Google Scholar
• Baker, J. O., McCarley, J. R., Lovett, R., Yu, C. H., Adney, W. S., Rignall, T. R., … Himmel, M. E. (2005). Catalytically enhanced endocellulase CeI5A from Acidothermus cellulolyticus. Applied Biochemistry and Biotechnology, 121–124, 129–148.10.1007/978-1-59259-991-2
   Google Scholar
• Bornscheuer, U. T., Huisman, G. W., Kazlauskas, R. J., Lutz, S., Moore, J. C., & Robins, K. (2012). Engineering the third wave of biocatalysis. Nature, 485, 185–194.10.1038/nature11117
   PubMed Web of Science ®Google Scholar
• Bose, S., Barnes, C. A., & Petrich, J. W. (2012). Enhanced stability and activity of cellulase in an ionic liquid and the effect of pretreatment on cellulose hydrolysis. Biotechnology and Bioengineering, 109, 434–443.10.1002/bit.23352
   PubMed Web of Science ®Google Scholar
• Brandt, A., Gräsvik, J., Hallett, J. P., & Welton, T. (2013). Deconstruction of lignocellulosic biomass with ionic liquids. Green Chemistry, 15, 550–583.10.1039/c2gc36364j
   Web of Science ®Google Scholar
• Burney, P. R., Nordwald, E. M., Hickman, K., Kaar, J. L., & Pfaendtner, J. (2015). Molecular dynamics investigation of the ionic liquid/enzyme interface: Application to engineering enzyme surface charge. Proteins: Structure, Function, and Bioinformatics, 83, 670–680.10.1002/prot.v83.4
   PubMed Web of Science ®Google Scholar
• Burney, P. R., & Pfaendtner, J. (2013). Structural and dynamic features of Candida rugosa lipase 1 in water, octane, toluene, and ionic liquids BMIM-PF6 and BMIM-NO3. The Journal of Physical Chemistry B, 117, 2662–2670.10.1021/jp312299d
   PubMed Web of Science ®Google Scholar
• Bussi, G., Donadio, D., & Parrinello, M. (2007). Canonical sampling through velocity rescaling. The Journal of Chemical Physics, 126, 014101.10.1063/1.2408420
   PubMed Web of Science ®Google Scholar
• Canongia Lopes, J. N., Deschamps, J., & Pádua, A. A. (2004). Modeling ionic liquids using a systematic all-atom force field. The Journal of Physical Chemistry B, 108, 2038–2047.10.1021/jp0362133
   Web of Science ®Google Scholar
• Datta, S., Holmes, B., Park, J. I., Chen, Z., Dibble, D. C., Hadi, M., … Sapra, R. (2010). Ionic liquid tolerant hyperthermophilic cellulases for biomass pretreatment and hydrolysis. Green Chemistry, 12, 338–345.10.1039/b916564a
   Web of Science ®Google Scholar
• Day, R., Bennion, B. J., Ham, S., & Daggett, V. (2002). Increasing temperature accelerates protein unfolding without changing the pathway of unfolding. Journal of Molecular Biology, 322, 189–203.10.1016/S0022-2836(02)00672-1
   PubMed Web of Science ®Google Scholar
• Gao, W.-W., Zhang, F.-X., Zhang, G.-X., & Zhou, C.-H. (2015). Key factors affecting the activity and stability of enzymes in ionic liquids and novel applications in biocatalysis. Biochemical Engineering Journal, 99, 67–84.10.1016/j.bej.2015.03.005
   Web of Science ®Google Scholar
• Ghaedizadeh, S., Emamzadeh, R., Nazari, M., Rasa, S. M. M., Zarkesh-Esfahani, S. H., & Yousefi, M. (2016). Understanding the molecular behaviour of Renilla luciferase in imidazolium-based ionic liquids, a new model for the α/β fold collapse. Biochemical Engineering Journal, 105, 505–513.10.1016/j.bej.2015.10.024
   Web of Science ®Google Scholar
• Ghosh, S., Parui, S., Jana, B., & Bhattacharyya, K. (2015). Ionic liquid induced dehydration and domain closure in lysozyme: FCS and MD simulation. The Journal of Chemical Physics, 143, 125103.10.1063/1.4931974
   PubMed Web of Science ®Google Scholar
• Haberler, M., Schröder, C., & Steinhauser, O. (2011). Solvation studies of a zinc finger protein in hydrated ionic liquids. Physical Chemistry Chemical Physics, 13, 6955–6969.10.1039/c0cp02487b
   PubMed Web of Science ®Google Scholar
• Haberler, M., & Steinhauser, O. (2011). On the influence of hydrated ionic liquids on the dynamical structure of model proteins: A computational study. Physical Chemistry Chemical Physics, 13, 17994–18004.10.1039/c1cp22266j
   PubMed Web of Science ®Google Scholar
• Henrissat, B., Callebaut, I., Fabrega, S., Lehn, P., Mornon, J. P., & Davies, G. (1995). Conserved catalytic machinery and the prediction of a common fold for several families of glycosyl hydrolases. Proceedings of the National Academy of Sciences, 92, 7090–7094.10.1073/pnas.92.15.7090
   PubMed Web of Science ®Google Scholar
• Himmel, M. E., Adney, W. S., Tucker, M. P., & Grohmann, K. (1994). Thermostable purified endoglucanas from Acidothermus cellulolyticus ATCC 43068. US Patent 5366884 A.
   Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14, 33–38.10.1016/0263-7855(96)00018-5
   PubMed Web of Science ®Google Scholar
• Jaeger, V., Burney, P., & Pfaendtner, J. (2015). Comparison of three ionic liquid-tolerant cellulases by molecular dynamics. Biophysical Journal, 108, 880–892.10.1016/j.bpj.2014.12.043
   PubMed Web of Science ®Google Scholar
• Jaeger, V., & Pfaendtner, J. (2013). Structure, dynamics, and activity of xylanase solvated in binary mixtures of ionic liquid and water. ACS Chemical Biology, 8, 1179–1186.10.1021/cb3006837
   PubMed Web of Science ®Google Scholar
• Jenkins, J., Lo Leggio, L., Harris, G., & Pickersgill, R. (1995). β-Glucosidase, β-galactosidase, family A cellulases, family F xylanases and two barley glycanases form a superfamily of enzymes wit 8-fold β/α architecture and with two conserved glutamates near the carboxy-terminal ends of β-strands four and seven. FEBS Letters, 362, 281–285.10.1016/0014-5793(95)00252-5
   PubMed Web of Science ®Google Scholar
• Johnson, L. B., Gintner, L. P., Park, S., & Snow, C. D. (2015). Discriminating between stabilizing and destabilizing protein design mutations via recombination and simulation. Protein Engineering Design and Selection, 28, 259–267.10.1093/protein/gzv030
   PubMed Web of Science ®Google Scholar
• Johnson, L. B., Park, S., Gintner, L. P., & Snow, C. D. (in press). Characterization of supercharged cellulase activity and stability in ionic liquids. Journal of Molecular Catalysis B: Enzymatic.
   Google Scholar
• Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. The Journal of Chemical Physics, 79, 926–935.10.1063/1.445869
   Web of Science ®Google Scholar
• Jorgensen, W. L., & Tirado-Rives, J. (2005). Potential energy functions for atomic-level simulations of water and organic and biomolecular systems. Proceedings of the National academy of Sciences of the United States of America, 102, 6665–6670.10.1073/pnas.0408037102
   PubMed Web of Science ®Google Scholar
• Kaminski, G. A., Friesner, R. A., Tirado-Rives, J., & Jorgensen, W. L. (2001). Evaluation and reparametrization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides. The Journal of Physical Chemistry B, 105, 6474–6487.10.1021/jp003919d
   Web of Science ®Google Scholar
• Kim, H. S., Ha, S. H., Sethaphong, L., Koo, Y.-M., & Yingling, Y. G. (2014). The relationship between enhanced enzyme activity and structural dynamics in ionic liquids: A combined computational and experimental study. Physical Chemistry Chemical Physics, 16, 2944–2953.10.1039/c3cp52516c
   PubMed Web of Science ®Google Scholar
• Klähn, M., Lim, G. S., Seduraman, A., & Wu, P. (2011). On the different roles of anions and cations in the solvation of enzymes in ionic liquids. Physical Chemistry Chemical Physics, 13, 1649–1662.10.1039/C0CP01509A
   PubMed Web of Science ®Google Scholar
• Klähn, M., Lim, G. S., & Wu, P. (2011). How ion properties determine the stability of a lipase enzyme in ionic liquids: A molecular dynamics study. Physical Chemistry Chemical Physics, 13, 18647–18660.10.1039/c1cp22056j
   PubMed Web of Science ®Google Scholar
• Köddermann, T., Paschek, D., & Ludwig, R. (2007). Molecular dynamic simulations of ionic liquids: A reliable description of structure, thermodynamics and dynamics. ChemPhysChem, 8, 2464–2470.10.1002/(ISSN)1439-7641
   PubMed Web of Science ®Google Scholar
• Kowsari, M. H., Alavi, S., Ashrafizaadeh, M., & Najafi, B. (2008). Molecular dynamics simulation of imidazolium-based ionic liquids. I. Dynamics and diffusion coefficient. The Journal of Chemical Physics, 129, 224508.10.1063/1.3035978
   PubMed Web of Science ®Google Scholar
• Kowsari, M. H., Alavi, S., Ashrafizaadeh, M., & Najafi, B. (2009). Molecular dynamics simulation of imidazolium-based ionic liquids. II. Transport coefficients. The Journal of Chemical Physics, 130, 014703.10.1063/1.3042279
   PubMed Web of Science ®Google Scholar
• Kragl, U., Eckstein, M., & Kaftzik, N. (2002). Enzyme catalysis in ionic liquids. Current Opinion in Biotechnology, 13, 565–571.10.1016/S0958-1669(02)00353-1
   PubMed Web of Science ®Google Scholar
• Lai, J.-Q., Li, Z., Lü, Y.-H., & Yang, Z. (2011). Specific ion effects of ionic liquids on enzyme activity and stability. Green Chemistry, 13, 1860–1868.10.1039/c1gc15140a
   Web of Science ®Google Scholar
• Latif, M. A. M., Micaêlo, N. M., & Rahman, M. B. A. (2014a). Influence of anion–water interactions on the behaviour of lipases in room temperature ionic liquids. RSC Advances, 4, 48202–48211.10.1039/C4RA07460B
   Web of Science ®Google Scholar
• Latif, M. A. M., Micaêlo, N., & Rahman, M. B. A. (2014b). Solvation free energies in [bmim]-based ionic liquids: Anion effect toward solvation of amino acid side chain analogues. Chemical Physics Letters, 615, 69–74.10.1016/j.cplett.2014.08.073
   Web of Science ®Google Scholar
• Latif, M. A. M., Tejo, B. A., Abedikargiban, R., Abdul Rahman, M. B., & Micaêlo, N. M. (2013). Modeling stability and flexibility of α-Chymotrypsin in room temperature ionic liquids. Journal of Biomolecular Structure and Dynamics, 32, 1263–1273.
   PubMed Web of Science ®Google Scholar
• Lehmann, C., Bocola, M., Streit, W. R., Martinez, R., & Schwaneberg, U. (2014). Ionic liquid and deep eutectic solvent-activated CelA2 variants generated by directed evolution. Applied Microbiology and Biotechnology, 98, 5775–5785.10.1007/s00253-014-5771-y
   PubMed Web of Science ®Google Scholar
• Li, G., Camaioni, D. M., Amonette, J. E., Zhang, Z. C., Johnson, T. J., & Fulton, J. L. (2010). [CuCl n ] 2− n ion-pair species in 1-ethyl-3-methylimidazolium chloride ionic liquid−water mixtures: Ultraviolet−visible, x-ray absorption fine structure, and density functional theory characterization. The Journal of Physical Chemistry B, 114, 12614–12622.10.1021/jp106762b
   PubMed Web of Science ®Google Scholar
• Li, H., Kankaanpää, A., Xiong, H., Hummel, M., Sixta, H., Ojamo, H., & Turunen, O. (2013). Thermostabilization of extremophilic dictyoglomus thermophilum GH11 xylanase by an N-terminal disulfide bridge and the effect of ionic liquid [emim] OAc on the enzymatic performance. Enzyme and Microbial Technology, 53, 414–419.10.1016/j.enzmictec.2013.09.004
   PubMed Web of Science ®Google Scholar
• Li, L., Li, C., Sarkar, S., Zhang, J., Witham, S., Zhang, Z., … Alexov, E. (2012). DelPhi: A comprehensive suite for DelPhi software and associated resources. BMC Biophysics, 5, 9.10.1186/2046-1682-5-9
   PubMed Web of Science ®Google Scholar
• Li, W., Wang, L., Zhou, R., & Mu, Y. (2015). Ionic liquid induced inactivation of cellobiohydrolase I from Trichoderma reesei. Green Chemistry, 17, 1618–1625.
   Web of Science ®Google Scholar
• Lindorff-Larsen, K., Maragakis, P., Piana, S., Eastwood, M. P., Dror, R. O., & Shaw, D. E. (2012). Systematic validation of protein force fields against experimental data. PLoS One, 7, e32131.10.1371/journal.pone.0032131
   PubMed Web of Science ®Google Scholar
• Loksha, I. V., Maiolo III, J. R., Hong, C. W., Ng, A., & Snow, C. D. (2009). SHARPEN-systematic hierarchical algorithms for rotamers and proteins on an extended network. Journal of Computational Chemistry, 30, 999–1005.10.1002/jcc.v30:6
   PubMed Web of Science ®Google Scholar
• Martínez, L., Andrade, R., Birgin, E. G., & Martínez, J. M. (2009). PACKMOL: A package for building initial configurations for molecular dynamics simulations. Journal of Computational Chemistry, 30, 2157–2164.10.1002/jcc.v30:13
   PubMed Web of Science ®Google Scholar
• McCarter, S. L., Adney, W. S., Vinzant, T. B., Jennings, E., Eddy, F. P., Decker, S. R., … Himmel, M. E. (2002). Exploration of cellulose surface-binding properties of Acidothermus cellulolyticus Cel5A by site-specific mutagenesis. Applied Biochemistry and Biotechnology, 98–100, 273–288.10.1385/ABAB:98-100:1-9
   PubMed Web of Science ®Google Scholar
• Micaêlo, N. M., & Soares, C. M. (2008). Protein structure and dynamics in ionic liquids. insights from molecular dynamics simulation studies. The Journal of Physical Chemistry B, 112, 2566–2572.10.1021/jp0766050
   PubMed Web of Science ®Google Scholar
• Moniruzzaman, M., Kamiya, N., & Goto, M. (2010). Activation and stabilization of enzymes in ionic liquids. Organic & Biomolecular Chemistry, 8, 2887–2899.
   PubMed Web of Science ®Google Scholar
• Monk, J., Singh, R., & Hung, F. R. (2011). Effects of pore size and pore loading on the properties of ionic liquids confined inside nanoporous CMK-3 carbon materials. The Journal of Physical Chemistry C, 115, 3034–3042.10.1021/jp1089189
   Web of Science ®Google Scholar
• Mora-Pale, M., Meli, L., Doherty, T. V., Linhardt, R. J., & Dordick, J. S. (2011). Room temperature ionic liquids as emerging solvents for the pretreatment of lignocellulosic biomass. Biotechnology and Bioengineering, 108, 1229–1245.10.1002/bit.23108
   PubMed Web of Science ®Google Scholar
• Nordwald, E. M., Armstrong, G. S., & Kaar, J. L. (2014). NMR-guided rational engineering of an ionic-liquid-tolerant lipase. ACS Catalysis, 4, 4057–4064.10.1021/cs500978x
   Web of Science ®Google Scholar
• Nordwald, E. M., Brunecky, R., Himmel, M. E., Beckham, G. T., & Kaar, J. L. (2014). Charge engineering of cellulases improves ionic liquid tolerance and reduces lignin inhibition. Biotechnology and Bioengineering, 111, 1541–1549.10.1002/bit.25216
   PubMed Web of Science ®Google Scholar
• Nordwald, E. M., & Kaar, J. L. (2013a). Mediating electrostatic binding of 1-butyl-3-methylimidazolium chloride to enzyme surfaces improves conformational stability. The Journal of Physical Chemistry B, 117, 8977–8986.10.1021/jp404760w
   PubMed Web of Science ®Google Scholar
• Nordwald, E. M., & Kaar, J. L. (2013b). Stabilization of enzymes in ionic liquids via modification of enzyme charge. Biotechnology and Bioengineering, 110, 2352–2360.10.1002/bit.v110.9
   PubMed Web of Science ®Google Scholar
• Nosé, S., & Klein, M. L. (1983). Constant pressure molecular dynamics for molecular systems. Molecular Physics, 50, 1055–1076.10.1080/00268978300102851
   Web of Science ®Google Scholar
• Porter, A. R., Liem, S. Y., & Popelier, P. L. (2008). Room temperature ionic liquids containing low water concentrations – a molecular dynamics study. Physical Chemistry Chemical Physics, 10, 4240–4248.10.1039/b718011j
   PubMed Web of Science ®Google Scholar
• Portillo, M. D. C., & Saadeddin, A. (2015). Recent trends in ionic liquid (IL) tolerant enzymes and microorganisms for biomass conversion. Critical Reviews in Biotechnology, 35, 294–301.10.3109/07388551.2013.843069
   PubMed Web of Science ®Google Scholar
• Pronk, S., Pall, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., … Lindahl, E. (2013). GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics, 29, 845–854.10.1093/bioinformatics/btt055
   PubMed Web of Science ®Google Scholar
• Qiao, B., Krekeler, C., Berger, R., Delle Site, L., & Holm, C. (2008). Effect of anions on static orientational correlations, hydrogen bonds, and dynamics in ionic liquids: A simulational study. The Journal of Physical Chemistry B, 112, 1743–1751.10.1021/jp0759067
   PubMed Web of Science ®Google Scholar
• Rignall, T. R., Baker, J. O., McCarter, S. L., Adney, W. S., Vinzant, T. B., Decker, S. R., & Himmel, M. E. (2002). Effect of single active-site cleft mutation on product specificity in a thermostable bacterial cellulase. Applied Biochemistry and Biotechnology, 98–100, 383–394.10.1385/ABAB:98-100:1-9
   PubMed Web of Science ®Google Scholar
• Rohl, C. A., Strauss, C. E. M., Misura, K. M. S., & Baker, D. (2004). Protein structure prediction using Rosetta. Methods in Enzymology, 383, 66–93.10.1016/S0076-6879(04)83004-0
   PubMed Web of Science ®Google Scholar
• Sakon, J., Adney, W. S., Himmel, M. E., Thomas, S. R., & Karplus, P. A. (1996). Crystal structure of thermostable family 5 endocellulase E1 from Acidothermus cellulolyticus in complex with cellotetraose. Biochemistry, 35, 10648–10660.10.1021/bi9604439
   PubMed Web of Science ®Google Scholar
• Shu, Y., Liu, M., Chen, S., Chen, X., & Wang, J. (2011). New insight into molecular interactions of imidazolium ionic liquids with bovine serum albumin. The Journal of Physical Chemistry B, 115, 12306–12314.10.1021/jp2071925
   PubMed Web of Science ®Google Scholar
• Sitkoff, D., Lockhart, D. J., Sharp, K. A., & Honig, B. (1994). Calculation of electrostatic effects at the amino terminus of an alpha helix. Biophysical Journal, 67, 2251–2260.10.1016/S0006-3495(94)80709-X
   PubMed Web of Science ®Google Scholar
• Sprenger, K. G., Choudhury, A., Kaar, J. L., & Pfaendtner, J. (2016). The lytic polysaccharide monooxygenases ScLPMO10B and ScLPMO10C are stable in ionic liquids as determined by molecular simulations. The Journal of Physical Chemistry B, 120, 3863–3872.
   PubMed Web of Science ®Google Scholar
• Tee, K. L., Roccatano, D., Stolte, S., Arning, J., Jastorff, B., & Schwaneberg, U. (2008). Ionic liquid effects on the activity of monooxygenase P450 BM-3. Green Chemistry, 10, 117–123.10.1039/B714674D
   Web of Science ®Google Scholar
• Tucker, M. P., Mohagheghi, A., Grohmann, K., & Himmel, M. E. (1989). Ultra-thermostable cellulases from Acidothermus cellulolyticus: Comparison of temperature optima with previously reported cellulases. Nature Biotechnology, 7, 817–820.10.1038/nbt0889-817
   Web of Science ®Google Scholar
• Vancov, T., Alston, A.-S., Brown, T., & McIntosh, S. (2012). Use of ionic liquids in converting lignocellulosic material to biofuels. Renewable Energy, 45, 1–6.10.1016/j.renene.2012.02.033
   Web of Science ®Google Scholar
• van Rantwijk, F., & Sheldon, R. A. (2007). Biocatalysis in ionic liquids. Chemical Reviews, 107, 2757–2785.10.1021/cr050946x
   PubMed Web of Science ®Google Scholar
• Vrbka, L., Jungwirth, P., Bauduin, P., Touraud, D., & Kunz, W. (2006). Specific ion effects at protein surfaces: A molecular dynamics study of bovine pancreatic trypsin inhibitor and horseradish peroxidase in selected salt solutions. The Journal of Physical Chemistry B, 110, 7036–7043.10.1021/jp0567624
   PubMed Web of Science ®Google Scholar
• Wahlström, R., King, A., Parviainen, A., Kruus, K., & Suurnäkki, A. (2013). Cellulose hydrolysis with thermo-and alkali-tolerant cellulases in cellulose-dissolving superbase ionic liquids. RSC Advances, 3, 20001–20009.10.1039/c3ra42987c
   Web of Science ®Google Scholar
• Wahlström, R. M., & Suurnäkki, A. (2015). Enzymatic hydrolysis of lignocellulosic polysaccharides in the presence of ionic liquids. Green Chemistry, 17, 694–714.10.1039/C4GC01649A
   Web of Science ®Google Scholar
• Xia, S., Baker, G. A., Li, H., Ravula, S., & Zhao, H. (2014). Aqueous ionic liquids and deep eutectic solvents for cellulosic biomass pretreatment and saccharification. RSC Advances, 4, 10586–10596.10.1039/c3ra46149a
   PubMed Web of Science ®Google Scholar
• Xu, J., Xiong, P., & He, B. (2016). Advances in improving the performance of cellulase in ionic liquids for lignocellulose biorefinery. Bioresource Technology, 200, 961–970.10.1016/j.biortech.2015.10.031
   PubMed Web of Science ®Google Scholar
• Zhao, H. (2005). Effect of ions and other compatible solutes on enzyme activity, and its implication for biocatalysis using ionic liquids. Journal of Molecular Catalysis B: Enzymatic, 37, 16–25.10.1016/j.molcatb.2005.08.007
   Web of Science ®Google Scholar