Enzyme engineering of choline oxidase for improving stability

References

• Arduini, F., Scognamiglio, V., Covaia, C., Amine, A., Moscone, D., & Palleschi, G. (2015). A choline oxidase amperometric bioassay for the detection of mustard agents based on screen-printed electrodes modified with Prussian Blue nanoparticles. Sensors, 15(2), 4353–4367. https://doi.org/10.3390/s150204353
   PubMed Web of Science ®Google Scholar
• Bayly, C. I., Cieplak, P., Cornell, W., & Kollman, P. A. (1993). A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: The RESP model. The Journal of Physical Chemistry, 97(40), 10269–10280. https://doi.org/10.1021/j100142a004
   Web of Science ®Google Scholar
• Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., & Haak, J. R. (1984). Molecular dynamics with coupling to an external bath. The Journal of Chemical Physics, 81(8), 3684–3690. https://doi.org/10.1063/1.448118
   Web of Science ®Google Scholar
• Bremer, E., & Krämer, R. (2019). Responses of microorganisms to osmotic stress. Annual Review of Microbiology, 73(1), 313–334. https://doi.org/10.1146/annurev-micro-020518-115504
   PubMedGoogle Scholar
• Cavener, D. R. (1992). GMC oxidoreductases: A newly defined family of homologous proteins with diverse catalytic activities. Journal of Molecular Biology, 223(3), 811–814. https://doi.org/10.1016/0022-2836(92)90992-s
   PubMed Web of Science ®Google Scholar
• Cornell, W. D., Cieplak, P., Bayly, C. I., & Kollman, P. A. (1993). Application of RESP charges to calculate conformational energies, hydrogen bond energies, and free energies of solvation. Journal of the American Chemical Society, 115(21), 9620–9631. https://doi.org/10.1021/ja00074a030
   Web of Science ®Google Scholar
• Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N⋅log(N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98(12), 10089–10092. https://doi.org/10.1063/1.464397
   Web of Science ®Google Scholar
• Eadie, G., & Bernheim, F. (1950). Studies on the stability of the choline oxidase. The Journal of Biological Chemistry, 185(2), 731–739. https://doi.org/10.1016/S0021-9258(18)56362-6
   PubMed Web of Science ®Google Scholar
• Eberhardt, J., Santos-Martins, D., Tillack, A. F., & Forli, S. (2021). AutoDock Vina 1.2. 0: New docking methods, expanded force field, and python bindings. Journal of Chemical Information and Modeling, 61(8), 3891–3898. https://doi.org/10.1021/acs.jcim.1c00203
   PubMed Web of Science ®Google Scholar
• Fan, F., & Gadda, G. (2005). On the catalytic mechanism of choline oxidase. Journal of the American Chemical Society, 127(7), 2067–2074. https://doi.org/10.1021/ja044541q
   PubMed Web of Science ®Google Scholar
• Finnegan, S., Agniswamy, J., Weber, I. T., & Gadda, G. (2010). Role of valine 464 in the flavin oxidation reaction catalyzed by choline oxidase. Biochemistry, 49(13), 2952–2961. https://doi.org/10.1021/bi902048c
   PubMed Web of Science ®Google Scholar
• Furuoya, I., Suzuki, T., & Takahashi, T. (1992). Novel choline oxidase and method for producing the same. U.S. Patent 5,079,157.
   Google Scholar
• Gadda, G. (2008). Hydride transfer made easy in the reaction of alcohol oxidation catalyzed by flavin-dependent oxidases. Biochemistry, 47(52), 13745–13753. https://doi.org/10.1021/bi801994c
   PubMed Web of Science ®Google Scholar
• Gadda, G. (2012). Oxygen activation in flavoprotein oxidases: The importance of being positive. Biochemistry, 51(13), 2662–2669. https://doi.org/10.1021/bi300227d
   PubMed Web of Science ®Google Scholar
• Gadda, G., & Yuan, H. (2017). Substitutions of S101 decrease proton and hydride transfers in the oxidation of betaine aldehyde by choline oxidase. Archives of Biochemistry and Biophysics, 634, 76–82. https://doi.org/10.1016/j.abb.2017.10.004
   PubMed Web of Science ®Google Scholar
• Ghanem, M., & Gadda, G. (2005). On the catalytic role of the conserved active site residue His466 of choline oxidase. Biochemistry, 44(3), 893–904. https://doi.org/10.1021/bi048056j
   PubMed Web of Science ®Google Scholar
• Gholizadeh, M., Shareghi, B., & Farhadian, S. (2023). Elucidating binding mechanisms of naringenin by alpha-chymotrypsin: Insights into non-binding interactions and complex formation. International Journal of Biological Macromolecules, 253(Pt 1), 126605. https://doi.org/10.1016/j.ijbiomac.2023.126605
   PubMedGoogle Scholar
• Gordon, J. C., Myers, J. B., Folta, T., Shoja, V., Heath, L. S., & Onufriev, A. (2005). H++: A server for estimating pKas and adding missing hydrogens to macromolecules. Nucleic Acids Research, 33(Web Server issue), W368–W371. https://doi.org/10.1093/nar/gki464
   PubMed Web of Science ®Google Scholar
• Habibian-Dehkordi, S., Farhadian, S., Ghasemi, M., & Evini, M. (2022). Insight into the binding behavior, structure, and thermal stability properties of β-lactoglobulin/Amoxicillin complex in a neutral environment. Food Hydrocolloids. 133, 107830. https://doi.org/10.1016/j.foodhyd.2022.107830
   Web of Science ®Google Scholar
• Hekmat, A., Saboury, A., Divsalar, A., & Khanmohammadi, M. (2008). Conformational and structural changes of choline oxidase from alcaligenes species by changing pH values. Bulletin of the Korean Chemical Society, 29(8), 1510–1518. https://doi.org/10.5012/bkcs.2008.29.8.1510
   Web of Science ®Google Scholar
• Izaguirre, J. A., Catarello, D. P., Wozniak, J. M., & Skeel, R. D. (2001). Langevin stabilization of molecular dynamics. The Journal of Chemical Physics, 114(5), 2090–2098. https://doi.org/10.1063/1.1332996
   Web of Science ®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(2), 926–935. https://doi.org/10.1063/1.445869
   Web of Science ®Google Scholar
• Kabsch, W., & Sander, C. (1983). Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22(12), 2577–2637. https://doi.org/10.1002/bip.360221211
   PubMed Web of Science ®Google Scholar
• Laskowski, R. A., & Swindells, M. B. (2011). LigPlot+: Multiple ligand-protein interaction diagrams for drug discovery. Journal of Chemical Information and Modeling, 51(10), 2778–2786. https://doi.org/10.1021/ci200227u
   PubMed Web of Science ®Google Scholar
• Liu, J., Wei, B., Che, C., Gong, Z., Jiang, Y., Si, M., Zhang, J., & Yang, G. (2019). Enhanced stability of manganese superoxide dismutase by amino acid replacement designed via molecular dynamics simulation. International Journal of Biological Macromolecules, 128, 297–303. https://doi.org/10.1016/j.ijbiomac.2019.01.126
   PubMed Web of Science ®Google Scholar
• Lokesha, S., Ravi Kumar, Y., Sujan Ganapathy, P., Gaur, P., & Arjun, H. (2021). Production of recombinant choline oxidase and its application in betaine production. 3 Biotech, 11(9), 410. https://doi.org/10.1007/s13205-021-02960-z
   PubMedGoogle Scholar
• Miller, B. R. I., McGee, T. D., Jr., Swails, J. M., Homeyer, N., Gohlke, H., & Roitberg, A. E. (2012). MMPBSA.py: An efficient program for end-state free energy calculations. Journal of Chemical Theory and Computation, 8(9), 3314–3321. https://doi.org/10.1021/ct300418h
   PubMed Web of Science ®Google Scholar
• Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF chimera—a visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. https://doi.org/10.1002/jcc.20084
   PubMed Web of Science ®Google Scholar
• Quaye, O., Lountos, G. T., Fan, F., Orville, A. M., & Gadda, G. (2008). Role of Glu312 in binding and positioning of the substrate for the hydride transfer reaction in choline oxidase. Biochemistry, 47(1), 243–256. https://doi.org/10.1021/bi7017943
   PubMed Web of Science ®Google Scholar
• Rahimi, P., & Joseph, Y. (2019). Enzyme-based biosensors for choline analysis: A review. Trends in Analytical Chemistry, 110, 367–374. https://doi.org/10.1016/j.trac.2018.11.035
   Web of Science ®Google Scholar
• Ribitsch, D., Winkler, S., Gruber, K., Karl, W., Wehrschütz-Sigl, E., Eiteljörg, I., Schratl, P., Remler, P., Stehr, R., Bessler, C., Mussmann, N., Sauter, K., Maurer, K. H., & Schwab, H. (2010). Engineering of choline oxidase from Arthrobacter nicotianae for potential use as biological bleach in detergents. Applied Microbiology and Biotechnology, 87(5), 1743–1752. https://doi.org/10.1007/s00253-010-2637-9
   PubMed Web of Science ®Google Scholar
• Roe, D. R., & Cheatham, T. E. I. (2013). PTRAJ and CPPTRAJ: Software for processing and analysis of molecular dynamics trajectory data. Journal of Chemical Theory and Computation, 9(7), 3084–3095. https://doi.org/10.1021/ct400341p
   PubMed Web of Science ®Google Scholar
• Rungsrisuriyachai, K., & Gadda, G. (2008). On the role of histidine 351 in the reaction of alcohol oxidation catalyzed by choline oxidase. Biochemistry, 47(26), 6762–6769. https://doi.org/10.1021/bi800650w
   PubMed Web of Science ®Google Scholar
• Rungsrisuriyachai, K., & Gadda, G. (2010). Role of asparagine 510 in the relative timing of substrate bond cleavages in the reaction catalyzed by choline oxidase. Biochemistry, 49(11), 2483–2490. https://doi.org/10.1021/bi901796a
   PubMed Web of Science ®Google Scholar
• Ryckaert, J.-P., Ciccotti, G., & Berendsen, H. J. C. (1977). Numerical integration of the Cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. Journal of Computational Physics, 23(3), 327–341. https://doi.org/10.1016/0021-9991(77)90098-5
   Web of Science ®Google Scholar
• Sakamoto, A., & Murata, N. (2000). Genetic engineering of glycinebetaine synthesis in plants: Current status and implications for enhancement of stress tolerance. Journal of Experimental Botany, 51(342), 81–88. https://doi.org/10.1093/jexbot/51.342.81
   PubMed Web of Science ®Google Scholar
• Sakamoto, A., & Murata, N. (2001). The use of bacterial choline oxidase, a glycinebetaine-synthesizing enzyme, to create stress-resistant transgenic plants. Plant Physiology, 125(1), 180–188. https://doi.org/10.1104/pp.125.1.180
   PubMed Web of Science ®Google Scholar
• Salomon-Ferrer, R., Götz, A. W., Poole, D., Le Grand, S., & Walker, R. C. (2013). Routine microsecond molecular dynamics simulations with AMBER on GPUs. 2. Explicit solvent particle Mesh Ewald. Journal of Chemical Theory and Computation, 9(9), 3878–3888. https://doi.org/10.1021/ct400314y
   PubMed Web of Science ®Google Scholar
• Salvi, F., & Gadda, G. (2013). Human choline dehydrogenase: Medical promises and biochemical challenges. Archives of Biochemistry and Biophysics, 537(2), 243–252. https://doi.org/10.1016/j.abb.2013.07.018
   PubMed Web of Science ®Google Scholar
• Salvi, F., Wang, Y.-F., Weber, I. T., & Gadda, G. (2014). Structure of choline oxidase in complex with the reaction product glycine betaine. Acta Crystallographica-Section D, Biological Crystallography, 70(Pt 2), 405–413. https://doi.org/10.1107/S1399004713029283
   PubMedGoogle Scholar
• Siloto, R. M., & Weselake, R. J. (2012). Site saturation mutagenesis: Methods and applications in protein engineering. Biocatalysis and Agricultural Biotechnology, 1(3), 181–189. https://doi.org/10.1016/j.bcab.2012.03.010
   Google Scholar
• Singh, U. C., & Kollman, P. A. (1984). An approach to computing electrostatic charges for molecules. Journal of Computational Chemistry, 5(2), 129–145. https://doi.org/10.1002/jcc.540050204
   Web of Science ®Google Scholar
• Tian, C., Kasavajhala, K., Belfon, K. A. A., Raguette, L., Huang, H., Migues, A. N., Bickel, J., Wang, Y., Pincay, J., Wu, Q., & Simmerling, C. (2020). ff19SB: Amino-acid-specific protein backbone parameters trained against quantum mechanics energy surfaces in solution. Journal of Chemical Theory and Computation, 16(1), 528–552. https://doi.org/10.1021/acs.jctc.9b00591
   PubMed Web of Science ®Google Scholar
• Touw, W. G., Baakman, C., Black, J., Te Beek, T. A. H., Krieger, E., Joosten, R. P., & Vriend, G. (2015). A series of PDB-related databanks for everyday needs. Nucleic Acids Research, 43(Database issue), D364–368. https://doi.org/10.1093/nar/gku1028
   PubMedGoogle Scholar
• Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., & Case, D. A. (2004). Development and testing of a general amber force field. Journal of Computational Chemistry, 25(9), 1157–1174. https://doi.org/10.1002/jcc.20035
   PubMed Web of Science ®Google Scholar
• Wu, X., Tian, Z., Jiang, X., Zhang, Q., & Wang, L. (2018). Enhancement in catalytic activity of Aspergillus niger XynB by selective site-directed mutagenesis of active site amino acids. Applied Microbiology and Biotechnology, 102(1), 249–260. https://doi.org/10.1007/s00253-017-8607-8
   PubMed Web of Science ®Google Scholar
• Xin, Y., Gadda, G., & Hamelberg, D. (2009). The cluster of hydrophobic residues controls the entrance to the active site of choline oxidase. Biochemistry, 48(40), 9599–9605. https://doi.org/10.1021/bi901295a
   PubMed Web of Science ®Google Scholar
• Yadollahi, E., Shareghi, B., & Farhadian, S. (2022a). Insight of the interaction of Naphthol yellow S with trypsin: Experimental and computational techniques. Journal of the Iranian Chemical Society, 19(7), 2871–2882. https://doi.org/10.1007/s13738-022-02497-9
   Web of Science ®Google Scholar
• Yadollahi, E., Shareghi, B., & Farhadian, S. (2022b). Noncovalent interactions between quinoline yellow and trypsin: In vitro and in silico methods. Journal of Molecular Liquids, 353, 118826. https://doi.org/10.1016/j.molliq.2022.118826
   Web of Science ®Google Scholar
• Yadollahi, E., Shareghi, B., Farhadian, S., & Hashemi Shahraki, F. (2023). Conformational dynamics of trypsin in the presence of caffeic acid: A spectroscopic and computational investigation. Journal of Biomolecular Structure & Dynamics, 0(0), 1–10. https://doi.org/10.1080/07391102.2023.2212077
   Google Scholar