Structural and biochemical characterisation of Archaeoglobus fulgidus esterase reveals a bound CoA molecule in the vicinity of the active site

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Sayer, Christopher ^a   Finnigan, William ^a   Isupov, Michail N ^a   Levisson, Mark ^b   Kengen, Servé W M ^b   Van Der Oost, John ^b   Harmer, Nicholas J ^a   Littlechild, Jennifer A ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

COENZYME A; ENZYME INHIBITOR; ESTERASE; LIGAND; PROTEIN BINDING; SOLVENT;

ANTAGONISTS AND INHIBITORS; ARCHAEOGLOBUS FULGIDUS; CHEMICAL PHENOMENA; CHEMISTRY; CONFORMATION; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYME STABILITY; ENZYMOLOGY; METABOLISM; MOLECULAR MODEL; PH; STRUCTURE ACTIVITY RELATION; THERMODYNAMICS;

ARCHAEOGLOBUS FULGIDUS; CATALYTIC DOMAIN; COENZYME A; ENZYME ACTIVATION; ENZYME INHIBITORS; ENZYME STABILITY; ESTERASES; HYDROGEN-ION CONCENTRATION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIGANDS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; PROTEIN BINDING; SOLVENTS; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

EID: 84969132700     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep25542     Document Type: Article

References (60)

1. Klenk, H. P. et al. The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature 390, 364-370 (1997).
2. Littlechild, J. A. et al. Natural methods of protein stabilization: thermostable biocatalysts. Biochem Soc Trans 35, 1558-1563 (2007).
3. Littlechild, J. A. Enzymes from extreme environments and their industrial applications. Front Bioeng Biotechnol 3, 161 (2015).
4. Levisson, M., van der Oost, J. and Kengen, S. W. M. Carboxylic ester hydrolases from hyperthermophiles. Extremophiles 13, 567-581 (2009).
5. Romano, D. et al. Esterases as stereoselective biocatalysts. Biotechnol Adv 33, 547-565 (2015).
6. Panda, T. and Gowrishankar, B. S. Production and application of esterases. Appl Microbiol Biotechnol 67, 160-169 (2005).
7. Wei, R., Oeser, T. and Zimmermann, W. Synthetic polyester-hydrolyzing enzymes from thermophilic actinomycetes. Adv Appl Microbiol 89, 267-305 (2014).
8. Klibanov, M. A. Improving enzymes by using them in organic solvents. Nature 409, 241-246 (2001).
9. Yang, S., Qin, Z., Duan, X., Yan, Q. and Jiang, Z. Structural insights into the substrate specificity of two esterases from the thermophilic Rhizomucor miehei. J Lipid Res 56, 1616-1624 (2015).
10. Somers, N. A. and Kazlauskas, R. J. Mapping the substrate selectivity and enantioselectivity of esterases from thermophiles. Tetrahedron Asymmetry 15, 2991-3004 (2004).
11. Lomolino, G., Rizzi, C., Spettoli, P., Curioni, A. and Lante, A. Cell vitality and esterase activity of Saccharomyces cerevisiae is affected by increasing calcium concentration. Agro food ind hi-tech, 14, 32-35 (2003).
12. Quax, W. J. and Broekhuizen, C. P. Development of a new Bacillus carboxyl esterase for use in the resolution of chiral drugs. Appl Microbiol Biotechnol 41, 425-431 (1994).
13. Schrag, J. and Cygler, M. Lipases and alpha/beta hydrolase fold. Methods Enzymol 284, 85-107 (1997).
14. Wagner, U. G., Petersen, E. I., Schwab, H. and Kratky, C. EstB from Burkholderia gladioli: A novel esterase with a β-lactamase fold reveals steric factors to discriminate between esterolytic and β-lactam cleaving activity. Protein Sci 11, 467-478 (2002).
15. Upton, C. and Buckley, J. T. A new family of lipolytic enzymes? Trends Biochem Sci 20, 178-179 (1995).
16. Höst, G., Martensson, L. G. and Jonsson, B. H. Redesign of human carbonic anhydrase II for increased esterase activity and specificity towards esters with long acyl chains. Biochim Biophys Acta 1764, 1601-1606 (2006).
17. Lenfant, N. et al. ESTHER, the database of the α/β hydrolase fold superfamily of proteins: tools to explore diversity of functions. Nucleic Acids Res 41, D423-D429 (2013).
18. Blow, D. M., Birktoft, J. J. and Hartley, B. S. Role of a buried acid group in the mechanism of action of chymotrypsin. Nature, 221, 337-340 (1969).
19. Bourne, P. C., Isupov, M. N. and Littlechild, J. A. The atomic-resolution structure of a novel bacterial esterase. Structure, 8, 143-151 (2000).
20. Levisson, M., van der Oost, J. and Kengen, S. W. M. Characterization and structural modeling of a new type of thermostable esterase from Thermotoga maritima. FEBS J 274, 2832-2842 (2007).
21. Levisson, M. et al. Functional and structural characterization of a thermostable acetyl esterase from Thermotoga maritima. Proteins 80, 1545-1559 (2012).
22. Liu, P. et al. Covalent reaction intermediate revealed in crystal structure of the Geobacillus stearothermophilus carboxylesterase Est30. J Mol Biol 342, 551-561 (2004).
23. Liu, P., Ewis, H. E., Tai, P. C., Lu, C. D. and Weber, I. T. Crystal structure of the Geobacillus stearothermophilus carboxylesterase Est55 and its activation of prodrug CPT-11. J Mol Biol 367, 212-223 (2007).
24. Mandrich, L. et al. Functional and structural features of the oxyanion hole in a thermophilic esterase from Alicyclobacillus acidocaldarius. Proteins 71, 1721-1731 (2008).
25. Billig, S., Oeser, T., Birkemeyer, C. and Zimmermann, W. Hydrolysis of cyclic poly(ethylene terephthalate) trimers by a carboxylesterase from Thermobifida fusca KW3. Appl Microbiol Biotechnol 87, 1753-1764 (2010).
26. Angkawidjaja, C., Koga, Y., Takano, K. and Kanaya, S. Structure and stability of a thermostable carboxylesterase from the thermoacidophilic archaeon Sulfolobus tokodaii. FEBS J 279, 3071-3084 (2012).
27. Manco, G. et al. Cloning, overexpression, and properties of a new thermophilic and thermostable esterase with sequence similarity to hormone-sensitive lipase subfamily from the archaeon Archaeoglobus fulgidus. Arch Biochem. Biophys 373, 182-192 (2000).
28. De Simone, G. et al. The crystal structure of a hyper-thermophilic carboxylesterase from the archaeon Archaeoglobus fulgidus. J Mol Biol 314, 507-518 (2001).
29. Kim, S. B., Lee, W. and Ryu, Y. W. Cloning and characterization of thermostable esterase from Archaeoglobus fulgidus. J Microbiol 46, 100-107 (2008).
30. Kim, J., Kim, S., Yoon, S., Hong, E. and Ryu, Y. Improved enantioselectivity of thermostable esterase from Archaeoglobus fulgidus toward (S)-ketoprofen ethyl ester by directed evolution and characterization of mutant esterases. Appl Microbiol Biotechnol 99, 6293-6301 (2015).
31. Cao, H. et al. Biocatalytic Synthesis of Poly(γ-Valerolactone) Using a thermophilic esterase from Archaeoglobus fulgidus as catalyst. Int J Mol Sci 13, 12232-12241 (2012).
32. Chen, C. K. et al. Structure of the alkalohyperthermophilic Archaeoglobus fulgidus lipase contains a unique C-terminal domain essential for long-chain substrate binding. J Mol Biol 390, 672-685 (2009).
33. Copeland, R. A. Evaluation of enzyme inhibitors in drug discovery. (Wiley, 2005). IBSN:0471686964
34. Ollis, D. L. et al. The α/β hydrolase fold. Protein Eng 5, 197-211 (1992).
35. Finn, R. D. et al. Pfam: the protein families database. Nucleic Acids Res 42, D222-230 (2014).
36. Yin, D. L. et al. Switching catalysis from hydrolysis to perhydrolysis in P. fluorescens esterase. Biochemistry, 49, 1931-1942 (2010).
37. Hofmann, B. et al. Structural investigation of the cofactor-free chloroperoxidases. J Mol Biol 279, 889-900 (1998).
38. Bains, J., Kaufman, L., Farnell, B. and Boulanger, M. J. A product analog bound form of 3-oxoadipate-enol-lactonase (PcaD) reveals a multifunctional role for the divergent cap domain. J Mol Biol 406, 649-658 (2011).
39. Line, K., Isupov, M. N. and Littlechild, J. A. The crystal structure of a (-) gamma-lactamase from an Aureobacterium species reveals a tetrahedral intermediate in the active site. J Mol Biol 338, 519-532 (2004).
40. Dunn, G. et al. The structure of the C-C bond hydrolase MhpC provides insights into its catalytic mechanism. J Mol Biol 346, 253-265 (2005).
41. Lack, N. et al. Structure of HsaD, a steroid-degrading hydrolase, from Mycobacterium tuberculosis. Acta Crystallogr F Biol Cryst Commun 64, 2-7 (2008).
42. Lack, N. A. et al. Characterization of a Carbon-Carbon hydrolase from Mycobacterium tuberculosis involved in cholesterol metabolism. J Biol Chem 285, 434-443 (2010).
43. Sanishvili, R. et al. Integrating structure, bioinformatics, and enzymology to discover function: BioH, a new carboxylesterase from Escherichia coli. J Biol Chem 278, 26039-26045 (2003).
44. Holm, L. and Rosenström, P. Dali server: conservation mapping in 3D. Nucleic Acids Res 38, W545-549 (2010).
45. Sayer, C., Isupov, M. N., Bonch-Osmolovskaya, E. and Littlechild, J. A. Structural studies of a thermophilic esterase from a new Planctomycetes species, Thermogutta terrifontis. FEBS J 282, 2846-2857 (2015).
46. Bencharit, S. et al. Multisite promiscuity in the processing of endogenous substrates by human carboxylesterase 1. J Mol Biol 363, 201-214 (2006).
47. Armstrong, J. M., Myers, D. V., Verpoorte, J. A. and Edsall, J. T. Purification and properties of human erythrocyte carbonic anhydrases. J Biol Chem 241, 5137-5149 (1966).
48. Riddles, P. W., Blakeley, R. L. and Zerner, B. Reassessment of Ellmans reagent. Methods Enzymol 91, 49-60 (1983).
49. Kabsch, W. XDS. Acta Crystallogr D Biol Crystallogr 66, 125-132 (2010).
50. Evans, P. R. and Murshudov, G. N. How good are my data and what is the resolution? Acta Crystallogr D Biol Crystallogr 69, 1204-1214 (2013).
51. Winter, G., Lobley, C. M. C. and Prince, S. M. Decision making in xia2. Acta Crystallogr D Biol Crystallogr 69, 1260-1273 (2013).
52. Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67, 235-242 (2011).
53. Cowtan, K. Recent developments in classical density modification. Acta Crystallogr D Biol Crystallogr 66, 470-478 (2010).
54. Murshudov, G. N. et al. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D Biol Crystallogr 67, 355-367 (2011).
55. Emsley, P., Lohkamp, B., Scott, W. G. and Cowtan, K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66, 486-501 (2010).
56. Joosten, R. P., Long, F., Murshudov, G. N. and Perrakis, A. The PDB-REDO server for macromolecular structure model optimization. IUCrJ, 1, 213-220 (2014).
57. Lebedev, A. A. et al. JLigand: a graphical tool for the CCP4 template-restraint library. Acta Crystallogr D Biol Crystallogr 68, 431-440 (2012).
58. McNicholas, S., Potterton, E., Wilson, K. S. and Noble, M. E. Presenting your structures: the CCP4mg molecular-graphics software. Acta Crystallogr D Biol Crystallogr 67, 386-94 (2011).
59. Vaguine, A. A., Richelle, J. and Wodak, S. J. SFCHECK: a unified set of procedures for evaluating the quality of macromolecular structure-factor data and their agreement with the atomic model. Acta Crystallogr D Biol Crystallogr 55, 191-205 (1999).
60. Laskowski, R. A., MacArthur, M. W., Moss, D. S. and Thornton, J. M. PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Cryst 26, 283-291 (1993).