Thermal stability & kinetic constants for 129 variants of a family 1 glycoside hydrolase reveal that enzyme activity & stability can be separately designed

PLoS ONE

Volumn 12, Issue 5, 2017, Pages

  Carlin, Dylan Alexander ^a   Hapig Ward, Siena ^a   Chan, Bill Wayne ^a   Damrau, Natalie ^a   Riley, Mary ^a   Caster, Ryan W ^a   Bethards, Bowen ^a   Siegel, Justin B ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOSIDASE;

ALGORITHM; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME STABILITY; ENZYME STRUCTURE; ESCHERICHIA COLI; MICHAELIS MENTEN KINETICS; MOLECULAR CLONING; MOLECULAR MODEL; MUTAGENESIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN STABILITY; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; SEQUENCE ANALYSIS; THERMOSTABILITY; CHEMISTRY; ENZYME ACTIVE SITE; ENZYMOLOGY; GENETIC VARIATION; GENETICS; KINETICS; PROTEIN TERTIARY STRUCTURE; TEMPERATURE; X RAY CRYSTALLOGRAPHY;

ALGORITHMS; CATALYTIC DOMAIN; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; ENZYME STABILITY; ESCHERICHIA COLI; GENETIC VARIATION; GLYCOSIDE HYDROLASES; KINETICS; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY; TEMPERATURE;

EID: 85019957005     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0176255     Document Type: Article

References (32)

1. Fersht A. Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding. Macmillan; 1999.
2. Beadle BM, Shoichet BK. Structural Bases of Stability-function Tradeoffs in Enzymes. J Mol Biol. 2002; 321: 285-296. PMID: 12144785.
3. Tokuriki N, Stricher F, Serrano L, Tawfik DS. How protein stability and new functions trade off. PLoS Comput Biol. 2008; 4: e1000002. https://doi.org/10.1371/journal.pcbi.1000002 PMID: 18463696.
4. Sunden F, Peck A, Salzman J, Ressl S, Herschlag D, Kuriyan J. Extensive site-directed mutagenesis reveals interconnected functional units in the alkaline phosphatase active site. eLife Sciences. eLife Sciences Publications Limited; 2015; 4: e06181.
5. van der Meer, J-Y, Poddar H, Baas B-J, Miao Y, Rahimi M, Kunzendorf A, et al. Using mutability landscapes of a promiscuous tautomerase to guide the engineering of enantioselective Michaelases. Nat Commun. 2016; 7: 10911. https://doi.org/10.1038/ncomms10911 PMID: 26952338.
6. Romero PA, Tran TM, Abate AR. Dissecting enzyme function with microfluidic-based deep mutational scanning. Proc Natl Acad Sci U S A. 2015; 112: 7159-7164. https://doi.org/10.1073/pnas.1422285112 PMID: 26040002.
7. Kumar MDS, Bava KA, Gromiha MM, Prabakaran P, Kitajima K, Uedaira H, et al. ProTherm and Pro- NIT: Thermodynamic databases for proteins and protein-nucleic acid interactions. Nucleic Acids Res. 2006; 34: 204-6. https://doi.org/10.1093/nar/gkj103 PMID: 16381846.
8. Guerois R, Nielsen JE, Serrano L. Predicting changes in the stability of proteins and protein complexes: A study of more than 1000 mutations. J Mol Biol. 2002; 320: 369-387. https://doi.org/10.1016/S0022-2836(02)00442-4 PMID: 12079393.
9. Schymkowitz J, Borg J, Stricher F, Nys R, Rousseau F, Serrano L. The FoldX web server: An online force field. Nucleic Acids Res. 2005; 33: 382-8. https://doi.org/10.1093/nar/gki387 PMID: 15980494.
10. Carlin DA, Caster RW, Wang X, Betzenderfer SA, Chen CX, Duong VM, et al. Kinetic Characterization of 100 Glycoside Hydrolase Mutants Enables the Discovery of Structural Features Correlated with Kinetic Constants. PLoS One. 2016; 11: e0147596. https://doi.org/10.1371/journal.pone.0147596 PMID: 26815142.
11. Richter F, Leaver-Fay A, Khare SD, Bjelic S, Baker D. De Novo Enzyme Design Using Rosetta3. PLoS One. Public Library of Science; 2011; 6: e19230.
12. Kellogg EH, Leaver-Fay A, Baker D. Role of conformational sampling in computing mutation-induced changes in protein structure and stability. Proteins. 2011; 79: 830-838. https://doi.org/10.1002/prot.22921PMID: 21287615.
13. Koshland DE. Stereochemistry And The Mechanism Of Enzymatic Reactions. Biol Rev Camb Philos Soc. 1953; 28: 416-436.
14. Isorna P, Polaina J, Latorre-Garcõa L, Cañada FJ, Gonzalez B, Sanz-Aparicio J. Crystal structures of Paenibacillus polymyxa beta-glucosidase B complexes reveal the molecular basis of substrate specificity and give new insights into the catalytic machinery of family I glycosidases. J Mol Biol. 2007; 371: 1204-1218. https://doi.org/10.1016/j.jmb.2007.05.082 PMID: 17585934.
15. McIntosh LP, Hand G, Johnson PE, Joshi MD, Korner M, Plesniak LA, et al. The pKa of the general acid/base carboxyl group of a glycosidase cycles during catalysis: A 13C-NMR study of bacillus circulans xylanase. Biochemistry. 1996; 35: 9958-9966. https://doi.org/10.1021/bi9613234 PMID: 8756457.
16. Harris TK, Turner GJ. Structural basis of perturbed pKa values of catalytic groups in enzyme active sites. IUBMB Life. 2002; 53: 85-98. https://doi.org/10.1080/15216540211468 PMID: 12049200.
17. Siegel JB, Zanghellini A, Lovick HM, Kiss G, Lambert AR, St Clair JL, et al. Computational design of an enzyme catalyst for a stereoselective bimolecular Diels-Alder reaction. Science. 2010; 329: 309-313. https://doi.org/10.1126/science.1190239 PMID: 20647463.
18. RoÈthlisberger D, Khersonsky O, Wollacott AM, Jiang L, DeChancie J, Betker J, et al. Kemp elimination catalysts by computational enzyme design. Nature. 2008; 453: 190-195. https://doi.org/10.1038/nature06879 PMID: 18354394.
19. Wolf C, Siegel JB, Tinberg C, Camarca A, Gianfrani C, Paski S, et al. Engineering of Kuma030: A Gliadin Peptidase That Rapidly Degrades Immunogenic Gliadin Peptides in Gastric Conditions. J Am Chem Soc. 2015; 137: 13106-13113. https://doi.org/10.1021/jacs.5b08325 PMID: 26374198.
20. Leaver-Fay A, O'Meara MJ, Tyka M, Jacak R, Song Y, Kellogg EH, et al. Scientific Benchmarks for Guiding Macromolecular Energy Function Improvement. Methods Enzymol. NIH Public Access; 2013; 523: 109.
21. Meiering EM, Serrano L, Fersht AR. Effect of active site residues in barnase on activity and stability. J Mol Biol. 1992; 225: 585-589. PMID: 1602471.
22. Shoichet BK, Baase WA, Kuroki R, Matthews BW. A relationship between protein stability and protein function. Proc Natl Acad Sci U S A. 1995; 92: 452-456. PMID: 7831309.
23. Thomas VL, McReynolds AC, Shoichet BK. Structural Bases for Stability-Function Tradeoffs in Antibiotic Resistance. J Mol Biol. 2010; 396: 47-59. https://doi.org/10.1016/j.jmb.2009.11.005 PMID: 19913034.
24. Currin A, Swainston N, Day PJ, Kell DB. Synthetic biology for the directed evolution of protein biocatalysts: navigating sequence space intelligently. Chem Soc Rev. 2015; 44: 1172-1239. https://doi.org/10.1039/c4cs00351a PMID: 25503938.
25. Romero PA, Arnold FH. Exploring protein fitness landscapes by directed evolution. Nat Rev Mol Cell Biol. 2009; 10: 866-876. https://doi.org/10.1038/nrm2805 PMID: 19935669.
26. Bloom JD, Labthavikul ST, Otey CR, Arnold FH. Protein stability promotes evolvability. Proc Natl Acad Sci U S A. 2006; 103: 5869-5874. https://doi.org/10.1073/pnas.0510098103 PMID: 16581913.
27. Bloom JD, Arnold FH. In the light of directed evolution: Pathways of adaptive protein evolution. Proceedings of the National Academy of Sciences. 2009; 106: 9995-10000.
28. Soskine M, Tawfik DS. Mutational effects and the evolution of new protein functions. Nat Rev Genet. 2010; 11: 572-582. https://doi.org/10.1038/nrg2808 PMID: 20634811.
29. Goldenzweig A, Goldsmith M, Hill SE, Gertman O, Laurino P, Ashani Y, et al. Automated Structure-And Sequence-Based Design of Proteins for High Bacterial Expression and Stability. Mol Cell. 2016; 63: 337-346. https://doi.org/10.1016/j.molcel.2016.06.012 PMID: 27425410.
30. Wrenbeck EE, Faber MS, Whitehead TA. Deep sequencing methods for protein engineering and design. Curr Opin Struct Biol. 2016; 45: 36-44. https://doi.org/10.1016/j.sbi.2016.11.001 PMID: 27886568.
31. Whitehead TA, Chevalier A, Song Y, Dreyfus C, Fleishman SJ, De Mattos, C, et al. Optimization of affinity, specificity and function of designed influenza inhibitors using deep sequencing. Nat Biotechnol. 2012; 30: 543-548. https://doi.org/10.1038/nbt.2214 PMID: 22634563.
32. Schrodinger L. The PyMOL Molecular Graphics System [Internet]. Available: https://www.pymol.org.