Lysine-based site-directed mutagenesis increased rigid β-sheet structure and thermostability of mesophilic 1,3-1,4-β-glucanase

Journal of Agricultural and Food Chemistry

Volumn 63, Issue 21, 2015, Pages 5249-5256

  Niu, Chengtuo ^a,b   Zhu, Linjiang ^a,b   Zhu, Pei ^a,b   Li, Qi ^a,b  

^a BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^b JIANGNAN UNIVERSITY   (China)

Author keywords

1,3 1,4 glucanase; lysine residues; molecular dynamics simulation; site directed mutagenesis; thermostability

Indexed keywords

AMINO ACIDS; BACTERIOLOGY; CHEMICAL MODIFICATION; MOLECULAR DYNAMICS; MUTAGENESIS; STABILITY;

GLUCANASE; LYSINE RESIDUES; MOLECULAR DYNAMICS SIMULATIONS; SITE DIRECTED MUTAGENESIS; THERMOSTABILITY;

ENZYME ACTIVITY;

BACTERIAL PROTEIN; GLYCOSIDASE; LYSINE;

AMINO ACID SEQUENCE; BACILLUS; CHEMISTRY; ENZYME STABILITY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN SECONDARY STRUCTURE; SITE DIRECTED MUTAGENESIS; TEMPERATURE;

AMINO ACID SEQUENCE; BACILLUS; BACTERIAL PROTEINS; ENZYME STABILITY; GLYCOSIDE HYDROLASES; LYSINE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, SECONDARY; TEMPERATURE;

EID: 84930625027     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.5b00480     Document Type: Article

References (40)

1. Wang, J.; Niu, C.; Liu, X.; Chen, X.; Li, Q. Characterization of a new 1,3-1,4-beta-glucanase gene from Bacillus tequilensis CGX5-1 Appl. Biochem. Biotechnol. 2014, 173, 826-837
2. Planas, N. Bacterial 1,3-1,4-beta-glucanases: Structure, function and protein engineering Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol. 2000, 1543, 361-382
3. Chaari, F.; Belghith-Fendri, L.; Blibech, M.; Driss, D.; Ellouzi, S. Z.; sameh, M.; Ellouz-Chaabouni, S. Biochemical characterization of a lichenase from Penicillium occitanis Pol6 and its potential application in the brewing industry Process Biochem. (Amsterdam, Neth.) 2014, 49, 1040-1046
4. Luo, Z.; Gao, Q.; Li, X.; Bao, J. Cloning of LicB from Clostridium thermocellum and its efficient secretive expression of thermostable β-1,3-1,4-glucanase Appl. Biochem. Biotechnol. 2014, 173, 562-570
5. Michael, J.; Lewis, T. W. Y. Brewing, 2 nd ed.; Springer: New York, 2013.
6. Spring, P.; Newman, K. E.; Wenk, C.; Messkommer, R.; Vranjes, M. V. Effect of pelleting temperature on the activity of different enzymes Poult. Sci. 1996, 75, 357-361
7. Olsen, O.; Borriss, R.; Simon, O.; Thomsen, K. K. Hybrid bacillus (1-3,1-4)-beta-glucanases-engineering thermostable enzymes by construction of hybrid genes Mol. Gen. Genet. 1991, 225, 177-185
8. Schimming, S.; Schwarz, W. H.; Staudenbauer, W. L. Properties of a thermoactive beta-1,3-1,4-glucanase (lichenase) from Clostridium thermocellum expressed in Escherichia coli Biochem. Biophys. Res. Commun. 1991, 177, 447-452
9. Cheng, Y.-S.; Huang, C.-H.; Chen, C.-C.; Huang, T.-Y.; Ko, T.-P.; Huang, J.-W.; Wu, T.-H.; Liu, J.-R.; Guo, R.-T. Structural and mutagenetic analyses of a 1,3-1,4-β-glucanase from Paecilomyces thermophila BBA-Proteins Proteom. 2014, 1844, 366-373
10. Fields, P. A. Review: Protein function at thermal extremes: Balancing stability and flexibility Comp. Biochem. Physiol., Part A 2001, 129, 417-431
11. Eijsink, V. G. H.; Bjork, A.; Gaseidnes, S.; Sirevag, R.; Synstad, B.; van den Burg, B.; Vriend, G. Rational engineering of enzyme stability J. Biotechnol. 2004, 113, 105-120
12. Dombkowski, A. A.; Sultana, K. Z.; Craig, D. B. Protein disulfide engineering FEBS Lett. 2014, 588, 206-212
13. Niu, C. T.; Zhu, L. J.; Wang, J. J.; Li, Q. Simultaneous enhanced catalytic activity and thermostability of a 1,3-1,4-beta-glucanase from Bacillus amyloliqueformi s by chemical modification of lysine residues Biotechnol. Lett. 2014, 36, 2453-2460
14. Khajeh, K.; Naderi-Manesh, H.; Ranjbar, B.; Moosavi-Movahedi, A. A.; Nemat-Gorgani, M. Chemical modification of lysine residues in Bacillus alpha-amylases: Effect on activity and stability Enzyme Microb. Technol. 2001, 28, 543-549
15. Pack, S. P.; Yoo, Y. J. Protein thermostability: Structure-based difference of amino acid between thermophilic and mesophilic proteins J. Biotechnol. 2004, 111, 269-277
16. Huang, X.; Gao, D.; Zhan, C. G. Computational design of a thermostable mutant of cocaine esterase via molecular dynamics simulations Org. Biomol. Chem. 2011, 9, 4138-4143
17. Joo, J. C.; Pohkrel, S.; Pack, S. P.; Yoo, Y. J. Thermostabilization of Bacillus circulans xylanase via computational design of a flexible surface cavity J. Biotechnol. 2010, 146, 31-39
18. Purmonen, M.; Valjakka, J.; Takkinen, K.; Laitinen, T.; Rouvinen, J. Molecular dynamics studies on the thermostability of family 11 xylanases Protein Eng., Des. Sel. 2007, 20, 551-559
19. Badieyan, S.; Bevan, D. R.; Zhang, C. Study and design of stability in GH5 cellulases Biotechnol. Bioeng. 2012, 109, 31-44
20. Di Marino, D.; Achsel, T.; Lacoux, C.; Falconi, M.; Bagni, C. Molecular dynamics simulations show how the FMRP Ile304Asn mutation destabilizes the KH2 domain structure and affects its function J. Biomol. Struct. Dyn. 2014, 32, 337-350
21. Biasini, M.; Bienert, S.; Waterhouse, A.; Arnold, K.; Studer, G.; Schmidt, T.; Kiefer, F.; Cassarino, T. G.; Bertoni, M.; Bordoli, L.; Schwede, T. SWISS-MODEL: Modelling protein tertiary and quaternary structure using evolutionary information Nucleic Acids Res. 2014, 42, W252-258
22. Hahn, M.; Pons, J.; Planas, A.; Querol, E.; Heinemann, U. Crystal structure of Bacillus licheniformis 1,3-1,4-beta-D-glucan 4-glucanohydrolase at 1.8 A resolution FEBS Lett. 1995, 374, 221-224
23. Pronk, S.; Pall, S.; Schulz, R.; Larsson, P.; Bjelkmar, P.; Apostolov, R.; Shirts, M. R.; Smith, J. C.; Kasson, P. M.; van der Spoel, D.; Hess, B.; Lindahl, E. GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit Bioinformatics 2013, 29, 845-854
24. Oostenbrink, C.; Villa, A.; Mark, A. E.; Van Gunsteren, W. F. A biomolecular force field based on the free enthalpy of hydration and solvation: The GROMOS force-field parameter sets 53A5 and 53A6 J. Comput. Chem. 2004, 25, 1656-1676
25. Berendsen, H. J.; Postma, J. P. M.; van Gunsteren, W. F.; DiNola, A.; Haak, J. Molecular dynamics with coupling to an external bath J. Chem. Phys. 1984, 81, 3684-3690
26. Parrinello, M.; Rahman, A. Polymorphic transitions in single crystals: A new molecular dynamics method J. Appl. Phys. 1981, 52, 7182-7190
27. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 1976, 72, 248-254
28. Chen, Y. C.; Chiang, Y. C.; Hsu, F. Y.; Tsai, L. C.; Cheng, H. L. Structural modeling and further improvement in pH stability and activity of a highly-active xylanase from an uncultured rumen fungus Bioresour. Technol. 2012, 123, 125-134
29. Lineweaver, H.; Burk, D. The determination of enzyme dissociation constants J. Am. Chem. Soc. 1934, 56, 658-666
30. Whitmore, L.; Wallace, B. A. Protein secondary structure analyses from circular dichroism spectroscopy: Methods and reference databases Biopolymers 2008, 89, 392-400
31. Quang, A. T. L.; Joo, J. C.; Yoo, Y. J.; Kim, Y. H. Development of thermostable Candida antarctica lipase B through novel in silico design of disulfide bridge Biotechnol. Bioeng. 2012, 109, 867-876
32. Zhang, W.; Mullaney, E. J.; Lei, X. G. Adopting selected hydrogen bonding and ionic interactions from Aspergillus fumigatus phytase structure improves the thermostability of Aspergillus niger PhyA phytase Appl. Environ. Microbiol. 2007, 73, 3069-3076
33. Zhang, Z. G.; Yi, Z. L.; Pei, X. Q.; Wu, Z. L. Improving the thermostability of Geobacillus stearothermophilus xylanase XT6 by directed evolution and site-directed mutagenesis Bioresour. Technol. 2010, 101, 9272-9278
34. Paul, M.; Hazra, M.; Barman, A.; Hazra, S. Comparative molecular dynamics simulation studies for determining factors contributing to the thermostability of chemotaxis protein "CheY" J. Biomol. Struct. Dyn. 2014, 32, 928-949
35. Batista, P. R.; Costa, M. G. D.; Pascutti, P. G.; Bisch, P. M.; de Souza, W. High temperatures enhance cooperative motions between CBM and catalytic domains of a thermostable cellulase: Mechanism insights from essential dynamics Phys. Chem. Chem. Phys. 2011, 13, 13709-13720
36. Politz, O.; Simon, O.; Olsen, O.; Borriss, R. Determinants for the enhanced thermostability of hybrid (1-3,1-4)-beta-glucanases Eur. J. Biochem. 1993, 216, 829-834
37. Li, Y. Q.; Middaugh, C. R.; Fang, J. W. A novel scoring function for discriminating hyperthermophilic and mesophilic proteins with application to predicting relative thermostability of protein mutants. BMC Bioinform. 2010, 11.
38. Papaleo, E.; Parravicini, F.; Grandori, R.; De Gioia, L.; Brocca, S. Structural investigation of the cold-adapted acylaminoacyl peptidase from Sporosarcina psychrophila by atomistic simulations and biophysical methods Biochim. Biophy. Acta, Proteins Proteom. 2014, 1844, 2203-2213
39. Yu, H. R.; Huang, H. Engineering proteins for thermostability through rigidifying flexible sites Biotechnol. Adv. 2014, 32, 308-315
40. Finke, J. M.; Roy, M.; Zimm, B. H.; Jennings, P. A. Aggregation events occur prior to stable intermediate formation during refolding of interleukin 1beta Biochemistry 2000, 39, 575-583