Design of mutants of GH11 xylanase from Bacillus pumilus for enhanced stability by amino acid substitutions in the N-terminal region: an in silico analysis

References

• Abraham, M. J., Murtola, T., Schulz, R., Páll, S., Smith, J. C., Hess, B., & Lindah, E. (2015). Gromacs: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, 1–2, 19–25. https://doi.org/10.1016/j.softx.2015.06.001
   Google Scholar
• Adamcsek, B., Palla, G., Farkas, I. J., Derényi, I., & Vicsek, T. (2006). CFinder: Locating cliques and overlapping modules in biological networks. Bioinformatics (Oxford, England), 22(8), 1021–1023. https://doi.org/10.1093/bioinformatics/btl039
   PubMed Web of Science ®Google Scholar
• Bateman, A. (2019). UniProt: A worldwide hub of protein knowledge. Nucleic Acids Research, 47(D1), D506–D515. https://doi.org/10.1093/nar/gky1049
   PubMed Web of Science ®Google Scholar
• Berman, H. M., Battistuz, T., Bhat, T. N., Bluhm, W. F., Bourne, P. E., Burkhardt, K., Feng, Z., Gilliland, G. L., Iype, L., Jain, S., Fagan, P., Marvin, J., Padilla, D., Ravichandran, V., Schneider, B., Thanki, N., Weissig, H., Westbrook, J. D., & Zardecki, C. (2002). The protein data bank. Acta Crystallographica: Section D Biological Crystallography, 58(Part 6 No 1), 899–907. https://doi.org/10.1107/s0907444902003451
   PubMedGoogle Scholar
• Chen, C., Ko, T., Huang, J., & Guo, R. (2015). Heat- and alkaline-stable xylanases : Application, protein structure and engineering. ChemBioEng Reviews, 2(2), 95–106. https://doi.org/10.1002/cben.201400035
   Google Scholar
• Cheng, Y.-S., Chen, C.-C., Huang, C.-H., Ko, T.-P., Luo, W., Huang, J.-W., Liu, J.-R., & Guo, R.-T. (2014). Structural analysis of a glycoside hydrolase family 11 xylanase from Neocallimastix patriciarum: Insights into the molecular basis of a thermophilic enzyme. Journal of Biological Chemistry, 289(16), 11020–11028. https://doi.org/10.1074/jbc.M114.550905
   PubMed Web of Science ®Google Scholar
• Collins, T., Gerday, C., & Feller, G. (2005). Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiology Reviews, 29(1), 3–23. https://doi.org/10.1016/j.femsre.2004.06.005
   PubMed Web of Science ®Google Scholar
• Dumon, C., Varvak, A., Wall, M. A., Flint, J. E., Lewis, R. J., Lakey, J. H., Morland, C., Luginbühl, P., Healey, S., Todaro, T., DeSantis, G., Sun, M., Parra-Gessert, L., Tan, X., Weiner, D. P., & Gilbert, H. J. (2008). Engineering hyperthermostability into a GH11 xylanase is mediated by subtle changes to protein structure. The Journal of Biological Chemistry, 283(33), 22557–22564. https://doi.org/10.1074/jbc.M800936200
   PubMed Web of Science ®Google Scholar
• Hakulinen, N., Turunen, O., Jänis, J., Leisola, M., & Rouvinen, J. (2003). Three-dimensional structures of thermophilic beta-1,4-xylanases from Chaetomium thermophilum and Nonomuraea flexuosa. Comparison of twelve xylanases in relation to their thermal stability. European Journal of Biochemistry, 270(7), 1399–1412. https://doi.org/10.1046/j.1432-1033.2003.03496.x
   PubMedGoogle Scholar
• Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N., & Sternberg, M. J. (2015). Trabajo práctico No 13. Varianzas en función de variable independiente categórica. Nature Protocols, 10(6), 845–858. https://doi.org/10.1038/nprot.2015-053
   PubMed Web of Science ®Google Scholar
• Kim, T., Chan, J., & Je, Y. (2012). Hydrophobic interaction network analysis for thermostabilization of a mesophilic xylanase. Journal of Biotechnology, 161(1), 49–59. https://doi.org/10.1016/j.jbiotec.2012.04.015
   PubMed Web of Science ®Google Scholar
• Li, H., Murtomäki, L., Leisola, M., & Turunen, O. (2012). The effect of thermostabilising mutations on the pressure stability of Trichoderma reesei GH11 xylanase. Protein Engineering, Design and Selection, 25(12), 821–826. https://doi.org/10.1093/protein/gzs052
   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(6–7), 414–419. https://doi.org/10.1016/j.enzmictec.2013.09.004
   PubMed Web of Science ®Google Scholar
• Meng, D.-D., Ying, Y., Chen, X.-H., Lu, M., Ning, K., Wang, L.-S., & Li, F.-L. (2015). Distinct roles for carbohydrate-binding modules of glycoside hydrolase 10 (GH10) and GH11 xylanases from Caldicellulosiruptor sp. strain F32 in thermostability and catalytic efficiency. Applied and Environmental Microbiology, 81(6), 2006–2014. https://doi.org/10.1128/AEM.03677-14
   PubMed Web of Science ®Google Scholar
• Paës, G., Berrin, J.-G., & Beaugrand, J. (2011). GH11 xylanases: Structure/function/properties relationships and applications. Biotechnology Advances, 30(3), 564–592. https://doi.org/10.1016/j.biotechadv.2011.10.003
   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
• Purmonen, M., Valjakka, J., Takkinen, K., Laitinen, T., & Rouvinen, J. (2007). Molecular dynamics studies on the thermostability of family 11 xylanases. Protein Engineering, Design & Selection, 20(11), 551–559. https://doi.org/10.1093/protein/gzm056
   PubMed Web of Science ®Google Scholar
• Ruller, R., Alponti, J., Deliberto, L. A., Zanphorlin, L. M., Machado, C. B., & Ward, R. J. (2014). Concommitant adaptation of a GH11 xylanase by directed evolution to create an alkali-tolerant/thermophilic enzyme. Protein Engineering, Design and Selection, 27(8), 255–262. https://doi.org/10.1093/protein/gzu027
   PubMed Web of Science ®Google Scholar
• Santos, C. R., Meza, A. N., Hoffmam, Z. B., Silva, J. C., Alvarez, T. M., Ruller, R., Giesel, G. M., Verli, H., Squina, F. M., Prade, R. A., & Murakami, M. T. (2010). Thermal-induced conformational changes in the product release area drive the enzymatic activity of xylanases 10B: Crystal structure, conformational stability and functional characterization of the xylanase 10B from Thermotoga petrophila RKU-1. Biochemical and Biophysical Research Communications, 403(2), 214–219. https://doi.org/10.1016/j.bbrc.2010.11.010
   PubMed Web of Science ®Google Scholar
• Singh, S., Madlala, A. M., & Prior, B. A. (2003). Thermomyces lanuginosus: Properties of strains and their hemicellulases. FEMS Microbiology Reviews, 27(1), 3–16. https://doi.org/10.1016/S0168-6445(03)00018-4
   PubMed Web of Science ®Google Scholar
• Stephens, D. E., Rumbold, K., Permaul, K., Prior, B. A., & Singh, S. (2007). Directed evolution of the thermostable xylanase from Thermomyces lanuginosus. Journal of Biotechnology, 127(3), 348–354. https://doi.org/10.1016/j.jbiotec.2006.06.015
   PubMed Web of Science ®Google Scholar
• Tina, K. G., Bhadra, R., & Srinivasan, N. (2007). PIC : Protein interactions calculator. Nucleic Acid Research, 35(Web Server Issue), W473–W476. https://doi.org/10.1093/nar/gkm423.
   PubMed Web of Science ®Google Scholar
• Trevizano, L. M., Ventorim, R. Z., De Rezende, S. T., Silva, F. P., & Guimarães, V. M. (2012). Thermostability improvement of Orpinomyces sp. xylanase by directed evolution. Journal of Molecular Catalysis B: Enzymatic, 81, 12–18. https://doi.org/10.1016/j.molcatb.2012.04.021
   Google Scholar
• Turunen, O., Etuaho, K., Fenel, F., Vehmaanperä, J., Wu, X., Rouvinen, J., & Leisola, M. (2001). A combination of weakly stabilizing mutations with a disulfide bridge in the α-helix region of Trichoderma reesei endo-1,4-β-xylanase II increases the thermal stability through synergism. Journal of Biotechnology, 88(1), 37–46. https://doi.org/10.1016/S0168-1656(01)00253-X
   PubMed Web of Science ®Google Scholar
• Ventorim, R. Z., de Oliveira Mendes, T. A., Trevizano, L. M., dos Santos Camargos, A. M., & Guimarães, V. M. (2018). Impact of the removal of N-terminal non-structured amino acids on activity and stability of xylanases from Orpinomyces sp. PC-2. International Journal of Biological Macromolecules, 106, 312–319. https://doi.org/10.1016/j.ijbiomac.2017.08.015
   PubMed Web of Science ®Google Scholar
• Verma, D., Kawarabayasi, Y., Miyazaki, K., & Satyanarayana, T. (2013). Cloning, expression and characteristics of a novel alkalistable and thermostable xylanase encoding gene (Mxyl) retrieved from compost-soil metagenome. PLoS One, 8(1), e52459. https://doi.org/10.1371/journal.pone.0052459
   PubMed Web of Science ®Google Scholar
• Wang, K., Luo, H., Tian, J., Turunen, O., Huang, H., Shi, P., Hua, H., Wang, C., Wang, S., & Yao, B. (2014). Thermostability improvement of a streptomyces xylanase by introducing proline and glutamic acid residues. Applied and Environmental Microbiology, 80(7), 2158–2165. https://doi.org/10.1128/AEM.03458-13
   PubMed Web of Science ®Google Scholar
• Wang, Y., Fu, Z., Huang, H., Zhang, H., Yao, B., Xiong, H., & Turunen, O. (2012). Improved thermal performance of Thermomyces lanuginosus GH11 xylanase by engineering of an N-terminal disulfide bridge. Bioresource Technology, 112, 275–279. https://doi.org/10.1016/j.biortech.2012.02.092
   PubMed Web of Science ®Google Scholar
• Yu, H., & Huang, H. (2014). Engineering proteins for thermostability through rigidifying flexible sites. Biotechnology Advances, 32(2), 308–315. https://doi.org/10.1016/j.biotechadv.2013.10.012
   PubMed Web of Science ®Google Scholar
• Zhang, S., He, Y., Yu, H., & Dong, Z. (2014). Seven N-terminal residues of a thermophilic xylanase are sufficient to confer hyperthermostability on its mesophilic counterpart. PLoS One, 9(1), e87632. https://doi.org/10.1371/journal.pone.0087632.
   PubMed Web of Science ®Google Scholar