Stabilization of cyclohexanone monooxygenase by a computationally designed disulfide bond spanning only one residue

FEBS Open Bio

Volumn 4, Issue , 2014, Pages 168-174

  van Beek, Hugo L ^a   Wijma, Hein J ^a   Fromont, Lucie ^a   Janssen, Dick B ^a   Fraaije, Marco W ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Baeyer Villiger monooxygenase; Computational design; Disulfide bonds; Enzyme engineering; Flavoprotein; Thermostability

Indexed keywords

CYCLOHEXANONE DERIVATIVE; CYCLOHEXANONE MONOOXYGENASE; CYSTEINE; DISULFIDE; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE;

ACINETOBACTER; ARTICLE; BIOCATALYSIS; DISULFIDE BOND; ENANTIOSELECTIVITY; ENZYME ACTIVITY; ENZYME STABILITY; MELTING POINT; MOLECULAR LIBRARY; MUTANT; PRIORITY JOURNAL; SCREENING; THERMOSTABILITY;

EID: 84894354808     PISSN: 22115463     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fob.2014.01.009     Document Type: Article

References (54)

1. Bornscheuer U., Huisman G., Kazlauskas R., Lutz S., Moore J., Robins K. Engineering the third wave of biocatalysis. Nature 2012, 485:185-194.
2. Bommarius A.S., Broering J.M., Chaparro-Riggers J.F., Polizzi K.M. High-throughput screening for enhanced protein stability. Curr. Opin. Biotechnol. 2006, 17:606.
3. Eijsink V.G.H., Bjørk A., Gåseidnes S., Sirevåg R., Synstad B., Burg B., Vriend G. Rational engineering of enzyme stability. J. Biotechnol. 2004, 113:105-120.
4. Van den Burg B., Vriend G., Veltman O.R., Venema G., Eijsink V.G. Engineering an enzyme to resist boiling. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:2056-2060.
5. Eijsink V.G., Vriend G., van der Vinne B., Hazes B., van den Burg B., Venema G. Effects of changing the interaction between subdomains on the thermostability of Bacillus neutral proteases. Proteins 1992, 14:224-236.
6. Wijma H.J., Floor R.J., Janssen D.B. Structure-and sequence-analysis inspired engineering of proteins for enhanced thermostability. Curr. Opin. Struct. Biol. 2013, 23:588-594.
7. Reetz M.T., Carballeira J.D. Iterative saturation mutagenesis (ISM) for rapid directed evolution of functional enzymes. Nat. Protoc. 2007, 2:891-903.
8. Jochens H., Aerts D., Bornscheuer U.T. Thermostabilization of an esterase by alignment-guided focussed directed evolution. Protein Eng. Des. Sel. 2010, 23:903-909.
9. Wijma H.J., Floor R., Janssen D.B. Computationally designed libraries for rapid enzyme stabilization. Protein Eng. Des. Sel. 2014, 27:49-58.
10. Krieger E., Joo K., Lee J., Lee J., Raman S., Thompson J., Tyka M., Baker D., Karplus K. Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: four approaches that performed well in CASP8. Proteins 2009, 77:114-122.
11. Petersen M.T.N., Jonson P.H., Petersen S.B. Amino acid neighbours and detailed conformational analysis of cysteines in proteins. Protein Eng. 1999, 12:535-548.
12. Dombkowski A.A., Sultana K.Z., Craig D.B. Protein disulfide engineering. FEBS Lett. 2013, 588:206-212.
13. Betz S.F. Disulfide bonds and the stability of globular proteins. Protein Sci. 2008, 2:1551-1558.
14. Chen Y., Peoples O., Walsh C. Acinetobacter cyclohexanone monooxygenase: gene cloning and sequence determination. J. Bacteriol. 1988, 170:781-789.
15. Ryerson C.C., Ballou D.P., Walsh C. Mechanistic studies on cyclohexanone oxygenase. Biochemistry 1982, 21:2644-2655.
16. Donoghue N.A., Norris D.B., Trudgill P.W. The purification and properties of cyclohexanone oxygenase from Nocardia globerula CL1 and Acinetobacter NCIB 9871. Eur. J. Biochem. 1976, 63:175-192.
17. de Gonzalo G., Mihovilovic M.D., Fraaije M.W. Recent developments in the application of Baeyer-Villiger monooxygenases as biocatalysts. Chembiochem 2010, 11:2208-2231.
18. Torres Pazmiño D.E., Dudek H.M., Fraaije M.W. Baeyer-Villiger monooxygenases: recent advances and future challenges. Curr. Opin. Chem. Biol. 2010, 14:138-144.
19. Leisch H., Morley K., Lau P.C.K. Baeyer-Villiger monooxygenases: more than just green chemistry. Chem. Rev. 2011, 111:4165-4222.
20. Kadow M., Loschinski K., Mallin H., Saß S., Bornscheuer U. Discovery, application and protein engineering of Baeyer-Villiger monooxygenases for organic synthesis. Org. Biomol. Chem. 2012, 10:6249-6265.
21. Fink M.J., Rial D.V., Kapitanova P., Lengar A., Rehdorf J., Cheng Q., Rudroff F., Mihovilovic M.D. Quantitative comparison of chiral catalysts selectivity and performance. A generic concept illustrated with cyclododecanone monooxygenase as Baeyer-Villiger biocatalyst. Adv. Synth. Catal. 2012, 354:3491-3500.
22. Mihovilovic M.D., Rudroff F., Winninger A., Schneider T., Schulz F., Reetz M.T. Microbial Baeyer-Villiger oxidation: stereopreference and substrate acceptance of cyclohexanone monooxygenase mutants prepared by directed evolution. Org. Lett. 2006, 8:1221-1224.
23. Opperman D.J., Reetz M.T. Towards practical Baeyer-Villiger monooxygenases: design of cyclohexanone monooxygenase mutants with enhanced oxidative stability. Chembiochem 2010, 11:2589-2596.
24. Reetz M.T., Brunner B., Schneider T., Schulz F., Clouthier C.M., Kayser M.M. Directed evolution as a method to create enantioselective cyclohexanone monooxygenases for catalysis in Baeyer-Villiger reactions. Angew. Chem. Int. Ed. 2004, 43:4075-4078.
25. Reetz M.T., Daligault F., Brunner B., Hinrichs H., Deege A. Directed evolution of cyclohexanone monooxygenases: enantioselective biocatalysts for the oxidation of prochiral thioethers. Angew. Chem. Int. Ed. 2004, 43:4078-4081.
26. Y.K.,Bong, M.D., Clay, S.J., Collier, B., Mijts, M., Vogel, X., Zhang, J., Zhu, J., Nazor, D., Smith, S., Song. Synthesis of prazole compounds, European Patent Application No. EP2010836590, 2013.
27. Secundo F., Zambianchi F., Crippa G., Carrea G., Tedeschi G. Comparative study of the properties of wild type and recombinant cyclohexanone monooxygenase, an enzyme of synthetic interest. J. Mol. Catal. B 2005, 34:1-6.
28. Zambianchi F., Pasta P., Carrea G., Colonna S., Gaggero N., Woodley J.M. Use of isolated cyclohexanone monooxygenase from recombinant Escherichia coli as a biocatalyst for Baeyer-Villiger and sulfide oxidations. Biotechnol. Bioeng. 2002, 78:489-496.
29. Staudt S., Bornscheuer U.T., Menyes U., Hummel W., Gröger H. Direct biocatalytic one-pot-transformation of cyclohexanol with molecular oxygen into e-caprolactone. Enzyme Microb. Technol. 2013, 53:288-292.
30. Malito E., Alfieri A., Fraaije M.W., Mattevi A. Crystal structure of a Baeyer-Villiger monooxygenase. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:13157-13162.
31. Orru R., Dudek H.M., Martinoli C., Torres Pazmiño D.E., Royant A., Weik M., Fraaije M.W., Mattevi A. Snapshots of enzymatic Baeyer-Villiger catalysis: oxygen activation and intermediate stabilization. J. Biol. Chem. 2011, 286:29284-29291.
32. Mirza I.A., Yachnin B.J., Wang S., Grosse S., Bergeron H., Imura A., Iwaki H., Hasegawa Y., Lau P.C., Berghuis A.M. Crystal structures of cyclohexanone monooxygenase reveal complex domain movements and a sliding cofactor. J. Am. Chem. Soc. 2009, 131:8848-8854.
33. Yachnin B.J., Sprules T., McEvoy M.B., Lau P.C., Berghuis A.M. The substrate-bound crystal structure of a Baeyer-Villiger monooxygenase exhibits a Criegee-like conformation. J. Am. Chem. Soc. 2012, 134:7788.
34. Fraaije M.W., Wu J., Heuts D.P., van Hellemond E.W., Spelberg J.H., Janssen D.B. Discovery of a thermostable Baeyer-Villiger monooxygenase by genome mining. Appl. Microbiol. Biotechnol. 2005, 66:393-400.
35. van Beek H.L., de Gonzalo G., Fraaije M.W. Blending Baeyer-Villiger monooxygenases: using a robust BVMO as a scaffold for creating chimeric enzymes with novel catalytic properties. Chem. Commun. 2012, 48:3288-3290.
36. Rogers T.A., Bommarius A.S. Utilizing simple biochemical measurements to predict lifetime output of biocatalysts in continuous isothermal processes. Chem. Eng. Sci. 2010, 65:2118-2124.
37. Sheng D., Ballou D.P., Massey V. Mechanistic studies of cyclohexanone monooxygenase: chemical properties of intermediates involved in catalysis. Biochemistry 2001, 40:11156-11167.
38. Korkegian A., Black M.E., Baker D., Stoddard B.L. Computational thermostabilization of an enzyme. Science 2005, 308:857-860.
39. 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.
40. Joo J.C., Pack S.P., Kim Y.H., Yoo Y.J. Thermostabilization of Bacillus circulans xylanase: computational optimization of unstable residues based on thermal fluctuation analysis. J. Biotechnol. 2011, 151:56-65.
41. Forneris F., Orru R., Bonivento D., Chiarelli L.R., Mattevi A. ThermoFAD, a Thermofluor®-adapted flavin ad hoc detection system for protein folding and ligand binding. FEBS J. 2009, 276:2833-2840.
42. Kamerbeek N.M., Fraaije M.W., Janssen D.B. Identifying determinants of NADPH specificity in Baeyer-Villiger monooxygenases. Eur. J. Biochem. 2004, 271:2107-2116.
43. Dudek H.M., Torres Pazmiño D.E., Rodríguez C., de Gonzalo G., Gotor V., Fraaije M.W. Investigating the coenzyme specificity of phenylacetone monooxygenase from Thermobifida fusca. Appl. Microbiol. Biotechnol. 2010, 88:1135-1143.
44. Torres Pazmiño D.E., Baas B.J., Janssen D.B., Fraaije M.W. Kinetic mechanism of phenylacetone monooxygenase from Thermobifida fusca. Biochemistry 2008, 47:4082-4093.
45. Fersht A. Structure and Mechanism in Protein Science 1999, WH Freeman & Co, New York. 2nd edition.
46. Matsumura M., Becktel W.J., Levitt M., Matthews B.W. Stabilization of phage T4 lysozyme by engineered disulfide bonds. Proc. Natl. Acad. Sci. U.S.A. 1989, 86:6562-6566.
47. Doig A.J., Williams D.H. Is the hydrophobic effect stabilizing or destabilizing in proteins? The contribution of disulphide bonds to protein stability. J. Mol. Biol. 1991, 217:389.
48. Thornton J. Disulphide bridges in globular proteins. J. Mol. Biol. 1981, 151:261-287.
49. Mückstein U., Hofacker I.L., Stadler P.F. Stochastic pairwise alignments. Bioinformatics 2002, 18:S153-S160.
50. Canutescu A.A., Dunbrack R.L. Cyclic coordinate descent: a robotics algorithm for protein loop closure. Protein Sci. 2009, 12:963-972.
51. Westerbeek A., Szymański W., Wijma H.J., Marrink S.J., Feringa B.L., Janssen D.B. Kinetic resolution of α-bromoamides: experimental and theoretical investigation of highly enantioselective reactions catalyzed by haloalkane dehalogenases. Adv. Synth. Catal. 2011, 353:931-944.
52. Caves L.S.D., Evanseck J.D., Karplus M. Locally accessible conformations of proteins: multiple molecular dynamics simulations of crambin. Protein Sci. 1998, 7:649-666.
53. Vihinen M. Relationship of protein flexibility to thermostability. Protein Eng. 1987, 1:477-480.
54. Torres Pazmiño D.E., Riebel A., de Lange J., Rudroff F., Mihovilovic M.D., Fraaije M.W. Efficient biooxidations catalyzed by a new generation of self-sufficient Baeyer-Villiger monooxygenases. Chembiochem 2009, 10:2595-2598.