Computational analysis of the effect of Gly100Ala mutation on the thermostability of SazCA

References

• Adcock, S., & McCammon, J. (2006). Molecular dynamics: Survey of methods for simulating the activity of proteins. Chemical Reviews, 106(5), 1589–1615. https://doi.org/10.1021/cr040426m
   PubMed Web of Science ®Google Scholar
• Alterio, V., Monti, S., & De Simone, G. (2014). Thermal-stable carbonic anhydrases: A structural overview, Carbonic anhydrase: Mechanism, regulation, links to disease, and industrial applications 387–404.
   Google Scholar
• Alvizo, O., Nguyen, L. J., Savile, C. K., Bresson, J. A., Lakhapatri, S. L., Solis, E. O. P., Fox, R. J., Broering, J. M., Benoit, M. R., Zimmerman, S. A., Novick, S. J., Liang, J., & Lalonde, J. J. (2014). Directed evolution of an ultrastable carbonic anhydrase for highly efficient carbon capture from flue gas. Proceedings of the National Academy of Sciences of the United States of America, 111(46), 16436–16441. https://doi.org/10.1073/pnas.1411461111
   PubMed Web of Science ®Google Scholar
• Ban, X., Lahiri, P., Dhoble, A., Li, D., Gu, Z., Li, C., Cheng, L., Hong, Y., Li, Z., & Kaustubh, B. (2019). Evolutionary stability of salt bridges hints its contribution to stability of proteins. Computational and Structural Biotechnology Journal, 17, 895–903. https://doi.org/10.1016/j.csbj.2019.06.022
   PubMed Web of Science ®Google Scholar
• Barbero, R., Carnelli, L., Simon, A., Kao, A., Monforte, A., Ricco, M., Bianchi, D., & Belcher, A. (2013). Engineered yeast for enhanced CO2 mineralization. Energy & Environmental Science, 6(2), 660–674. https://doi.org/10.1039/C2EE24060B
   PubMed Web of Science ®Google Scholar
• Berendsen, H., Postma, J., van Gunsteren, W., DiNola, A., & Haak, J. (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
• Best, R., & Hummer, G. (2009). Optimized molecular dynamics force fields applied to the helix- coil transition of polypeptides. The Journal of Physical Chemistry. B, 113(26), 9004–9015. https://doi.org/10.1021/jp901540t
   PubMed Web of Science ®Google Scholar
• Bharatiy, S., Hazra, M., Paul, M., Mohapatra, S., Samantaray, D., Dubey, R., Sanyal, S., Datta, S., & Hazra, S. (2016). In silico designing of an industrially sustainable carbonic anhydrase using molecular dynamics simulation. ACS Omega,.1(6), 1081–1103. https://doi.org/10.1021/acsomega.6b00041
   PubMed Web of Science ®Google Scholar
• Boone, C., Habibzadegan, A., Gill, S., & McKenna, R. (2013). Carbonic anhydrases and their biotechnological applications. Biomolecules, 3(3), 553–562. https://doi.org/10.3390/biom3030553
   PubMedGoogle Scholar
• Bosshard, H., Marti, D., & Jelesarov, I. (2004). Protein stabilization by salt bridges: Concepts, experimental approaches and clarification of some misunderstandings. Journal of Molecular Recognition: JMR, 17(1), 1–16. https://doi.org/10.1002/jmr.657
   PubMed Web of Science ®Google Scholar
• Camilloni, C., Sutto, L., Provasi, D., Tiana, G., & Broglia, R. (2008). Early events in protein folding: Is there something more than hydrophobic burst? Protein Science: A Publication of the Protein Society, 17(8), 1424–1433. https://doi.org/10.1110/ps.035105.108
   PubMed Web of Science ®Google Scholar
• Capasso, C., De Luca, V., Carginale, V., Cannio, R., & Rossi, M. (2012). Biochemical properties of a novel and highly thermostable bacterial α-carbonic anhydrase from Sulfurihydrogenibium yellowstonense YO3AOP1. Journal of Enzyme Inhibition and Medicinal Chemistry, 27(6), 892–897. https://doi.org/10.3109/14756366.2012.703185
   PubMed Web of Science ®Google Scholar
• Chan, C., Yu, T., & Wong, K. (2011). Stabilizing salt-bridge enhances protein thermostability by reducing the heat capacity change of unfolding. PLOS One, 6(6), e21624. https://doi.org/10.1371/journal.pone.0021624
   PubMed Web of Science ®Google Scholar
• Cheatham, T. I., Miller, J., Fox, T., Darden, T., & Kollman, P. (1995). Molecular dynamics simulations on solvated biomolecular systems: The particle mesh ewald method leads to stable trajectories of DNA, RNA, and proteins. Journal of the American Chemical Society, 117(14), 4193–4194. https://doi.org/10.1021/ja00119a045
   Web of Science ®Google Scholar
• Chen, X., Weber, I., & Harrison, R. (2008). Hydration water and bulk water in proteins have distinct properties in radial distributions calculated from 105 atomic resolution crystal structures. The Journal of Physical Chemistry. B, 112(38), 12073–12080. https://doi.org/10.1021/jp802795a
   PubMed Web of Science ®Google Scholar
• De Simone, G., Monti, S., Alterio, V., Buonanno, M., De Luca, V., Rossi, M., Carginale, V., Supuran, C., Capasso, C., & Di Fiore, A. (2015). Crystal structure of the most catalytically effective carbonic anhydrase enzyme known, SazCA from the thermophilic bacterium Sulfurihydrogenibium azorense. Bioorganic & Medicinal Chemistry Letters, 25(9), 2002–2006. https://doi.org/10.1016/j.bmcl.2015.02.068
   PubMed Web of Science ®Google Scholar
• Di Fiore, A., Alterio, V., Monti, S. M., De Simone, G., & D'Ambrosio, K. (2015). Thermostable carbonic anhydrases in biotechnological applications. International Journal of Molecular Sciences, 16(7), 15456–15480. https://doi.org/10.3390/ijms160715456
   PubMed Web of Science ®Google Scholar
• Effendi, S., & Ng, I. (2019). The prospective and potential of carbonic anhydrase for carbon dioxide sequestration: A critical review. Process Biochemistry, 87, 55–65. https://doi.org/10.1016/j.procbio.2019.08.018
   Web of Science ®Google Scholar
• Elleby, B., Sjoblom, B., & Lindskog, S. (1999). Changing the efficiency and specificity of the esterase activity of human carbonic anhydrase ii by site-specific mutagenesis. European Journal of Biochemistry, 262(2), 516–521. https://doi.org/10.1046/j.1432-1327.1999.00400.x
   PubMedGoogle Scholar
• Feller, S., Zhang, Y., Pastor, R., & Brooks, B. (1995). Constant pressure molecular dynamics simulation: The langevin piston method. The Journal of Chemical Physics, 103(11), 4613–4621. https://doi.org/10.1063/1.470648
   Web of Science ®Google Scholar
• Fierke, C., Calderone, T., & Krebs, J. (1991). Functional consequences of engineering the hydrophobic pocket of carbonic anhydrase ii. Biochemistry, 30(46), 11054–11063. https://doi.org/10.1021/bi00110a007
   PubMed Web of Science ®Google Scholar
• Fisher, Z., Boone, C., Biswas, S., Venkatakrishnan, B., Aggarwal, M., Tu, C., Agbandje-McKenna, M., Silverman, D., & McKenna, R. (2012). Kinetic and structural characterization of thermostabilized mutants of human carbonic anhydrase II. Protein Engineering, Design & Selection: PEDS, 25(7), 347–355. https://doi.org/10.1093/protein/gzs027
   PubMed Web of Science ®Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38. https://doi.org/10.1016/0263-7855(96)00018-5
   PubMedGoogle Scholar
• Jo, B., Kim, I., Seo, J., Kang, D., & Cha, H. (2013). Engineered Escherichia coli with periplasmic carbonic anhydrase as a biocatalyst for CO2 sequestration. Applied and Environmental Microbiology, 79(21), 6697–6705. https://doi.org/10.1128/AEM.02400-13
   PubMed 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
• Kockar, F., Maresca, A., Aydin, M., Işik, S., Turkoglu, S., Sinan, S., Arslan, O., Güler, O. O., Turan, Y., & Supuran, C. T. (2010). Mutation of Phe91 to asn in human carbonic anhydrase I unexpectedly enhanced both catalytic activity and affinity for sulfonamide inhibitors. Bioorganic & Medicinal Chemistry, 18(15), 5498–5503. https://doi.org/10.1016/j.bmc.2010.06.056
   PubMed Web of Science ®Google Scholar
• Kosa, J., & Karlsen, P. (1993). Conformational behavior and flexibility of terminally blocked alanine di- and tripeptides. Journal of Molecular Structure, 291, 271–286.
   Web of Science ®Google Scholar
• Krebs, J. F., & Fierke, C. (1993). Determinants of catalytic activity and stability of carbonic anhydrase ii as revealed by random mutagenesis. The Journal of Biological Chemistry, 268(2), 948–954. https://doi.org/10.1016/S0021-9258(18)54025-4
   PubMed Web of Science ®Google Scholar
• Kumar, S., & Deshpande, P. (2021). Structural and thermodynamic analysis of factors governing the stability and thermal folding/unfolding of SazCA. PLOS One,.16(4), e0249866. https://doi.org/10.1371/journal.pone.0249866
   PubMed Web of Science ®Google Scholar
• Kumar, S., & Nussinov, R. (2002). Close-range electrostatic interactions in proteins. ChemBioChem, 3(7), 604–617. https://doi.org/10.1002/1439-7633(20020703)3:7<604::AID-CBIC604>3.0.CO;2-X
   PubMed Web of Science ®Google Scholar
• Kumar, S., Seth, D., & Deshpande, P. (2021). Molecular dynamics simulations identify the regions of compromised thermostability in SazCA. Proteins: Structure, FUnction, and Bioinformatics. 89(4), 375–388. https://doi.org/10.1002/prot.26022
   PubMed Web of Science ®Google Scholar
• Kumar, S., Tsai, C., & Nussinov, R. (2000). Factors enhancing protein thermostability. Protein Engineering, 13(3), 179–191. https://doi.org/10.1093/protein/13.3.179
   PubMedGoogle Scholar
• Lee, J., Kwak, N., Lee, I., Jang, K., Lee, D., Jang, S., Kim, B., & Shim, J. (2015). Performance and economic analysis of commercial-scale coal-fired power plant with post-combustion CO2 capture. Korean Journal of Chemical Engineering, 32(5), 800–807. https://doi.org/10.1007/s11814-014-0267-0
   Web of Science ®Google Scholar
• Lee, K. (2012). Molecular dynamics simulations of a hyperthermophilic and a mesophilic protein l30e. Journal of Chemical Information and Modeling, 52(1), 7–15. https://doi.org/10.1021/ci200184y
   PubMed Web of Science ®Google Scholar
• Levy, Y., & Onuchic, J. (2004). Water and proteins: A love–hate relationship. Proceedings of the National Academy of Sciences of the United States of America, 101(10), 3325–3326. https://doi.org/10.1073/pnas.0400157101
   PubMed Web of Science ®Google Scholar
• Lippow, S., & Tidor, B. (2007). Progress in computational protein design. Current Opinion in Biotechnology, 18(4), 305–311. https://doi.org/10.1016/j.copbio.2007.04.009
   PubMed Web of Science ®Google Scholar
• Lopez-Llano, J., Campos, L., & Sancho, J. (2006). α-helix stabilization by alanine relative to glycine: Roles of polar and apolar solvent exposures and of backbone entropy. Proteins: Structure, Function, and Bioinformatics, 64(3), 769–778. https://doi.org/10.1002/prot.21041
   PubMed Web of Science ®Google Scholar
• Mallamace, F., Corsaro, C., Mallamace, D., Vasi, S., Vasi, C., & Dugo, G. (2015). The role of water in protein’s behavior: The two dynamical crossovers studied by nmr and ftir techniques. Computational and Structural Biotechnology Journal, 13, 33–37. https://doi.org/10.1016/j.csbj.2014.11.007
   PubMed Web of Science ®Google Scholar
• Mårtensson, L.-G., Karlsson, M., & Carlsson, U. (2002). Dramatic stabilization of the native state of human carbonic anhydrase II by an engineered disulfide bond. Biochemistry, 41(52), 15867–15875. https://doi.org/10.1021/bi020433+
   PubMed Web of Science ®Google Scholar
• Matthews, B., Nicholson, H., & Becktel, W. (1987). Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding. Proceedings of the National Academy of Sciences of the United States of America, 84(19), 6663–6667. https://doi.org/10.1073/pnas.84.19.6663
   PubMed Web of Science ®Google Scholar
• Paquet, E., & Viktor, H. (2015). Molecular dynamics, monte carlo simulations, and langevin dynamics: A computational review. BioMed Research International, 2015, 1–18. https://doi.org/10.1155/2015/183918
   Web of Science ®Google Scholar
• Parra-Cruz, R., Jager, C., Lau, P., Gomes, R., & Pordea, A. (2018). Rational design of thermostable carbonic anhydrase mutants using molecular dynamics simulations. The Journal of Physical Chemistry. B, 122(36), 8526–8536. https://doi.org/10.1021/acs.jpcb.8b05926
   PubMed Web of Science ®Google Scholar
• Phillips, J., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R., Kale, L., & Schulten, K. (2005). Scalable molecular dynamics with NAMD. Journal of Computational Chemistry, 26(16), 1781–1802. https://doi.org/10.1002/jcc.20289
   PubMed Web of Science ®Google Scholar
• Rani, P., & Biswas, P. (2014). Shape dependence of the radial distribution function of hydration water around proteins. Journal of Physics. Condensed Matter: An Institute of Physics Journal, 26(33), 335102. https://doi.org/10.1088/0953-8984/26/33/335102
   PubMed Web of Science ®Google Scholar
• Sahoo, P., Kumar, M., Puri, S., & Ramakumar, S. (2018). Enzyme inspired complexes for industrial CO2 capture: Opportunities and challenges. Journal of CO2 Utilization, 24, 419–429. https://doi.org/10.1016/j.jcou.2018.02.003
   Web of Science ®Google Scholar
• Savile, C., & Lalonde, J. (2011). Biotechnology for the acceleration of carbon dioxide capture and sequestration. Current Opinion in Biotechnology, 22(6), 818–823. https://doi.org/10.1016/j.copbio.2011.06.006
   PubMed Web of Science ®Google Scholar
• Sayre, T., Lee, T., King, N., & Yeates, T. (2011). Protein stabilization in a highly knotted protein polymer. Protein Engineering, Design & Selection: PEDS, 24(8), 627–630. https://doi.org/10.1093/protein/gzr024
   PubMed Web of Science ®Google Scholar
• Scott, K., Alonso, D., Sato, S., Fersht, A., & Daggett, V. (2007). Conformational entropy of alanine versus glycine in protein denatured states. Proceedings of the National Academy of Sciences of the United States of America, 104(8), 2661–2666. https://doi.org/10.1073/pnas.0611182104
   PubMed Web of Science ®Google Scholar
• Sheu, S., Yang, D., Selzle, H., & Schlag, E. (2003). Energetics of hydrogen bonds in peptides. Proceedings of the National Academy of Sciences of the United States of America, 100(22), 12683–12687. https://doi.org/10.1073/pnas.2133366100
   PubMed Web of Science ®Google Scholar
• Supuran, C. (2016). Structure and function of carbonic anhydrases. The Biochemical Journal, 473(14), 2023–2032. https://doi.org/10.1042/BCJ20160115
   PubMedGoogle Scholar
• Szilagyi, A., & Zavodszky, P. (2000). Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: Results of a comprehensive survey. Structure, 8(5), 493–504. https://doi.org/10.1016/S0969-2126(00)00133-7
   PubMed Web of Science ®Google Scholar
• Yakimov, A., Afanaseva, A., Khodorkovskiy, M., & Petukhov, M. (2016). Design of stable α-helical peptides and thermostable proteins in biotechnology and biomedicine. Acta Naturae, 8(4), 70–81. https://doi.org/10.32607/20758251-2016-8-4-70-81
   PubMed Web of Science ®Google Scholar
• Yan, B., & Sun, Y. (1997). Glycine residues provide flexibility for enzyme active sites. The Journal of Biological Chemistry, 272(6), 3190–3194. https://doi.org/10.1074/jbc.272.6.3190
   PubMed Web of Science ®Google Scholar