Organic co-solvents affect activity, stability and enantioselectivity of haloalkane dehalogenases

Biotechnology Journal

Volumn 8, Issue 6, 2013, Pages 719-729

  Stepankova, Veronika ^a,b   Damborsky, Jiri ^a,b,c   Chaloupkova, Radka ^a,c  

^a MASARYK UNIVERSITY   (Czech Republic)

^b ST ANNE S UNIVERSITY HOSPITAL   (Czech Republic)

^c Enantis Ltd   (Czech Republic)

Author keywords

Biocatalysis; Enzyme activity; Haloalkane dehalogenases; Medium engineering; Protein stability

Indexed keywords

BIOCATALYSIS; BIOCATALYTIC APPLICATIONS; BIOCATALYTIC PERFORMANCE; BIOTECHNOLOGICAL APPLICATIONS; CONFORMATIONAL CHANGE; HALOALKANE DEHALOGENASES; HYDROPHOBIC SUBSTRATE; PROTEIN STABILITY;

DIMETHYL SULFOXIDE; ENANTIOSELECTIVITY; ENZYME ACTIVITY; ENZYMES; ETHYLENE GLYCOL; POLYOLS; SOLVENTS;

ORGANIC SOLVENTS;

DIMETHYL SULFOXIDE; DIOXANE; ENZYME; ETHYLENE GLYCOL; HALOALKANE DEHALOGENASE; MICROBIAL ENZYME; ORGANIC SOLVENT; TETRAHYDROFURAN; UNCLASSIFIED DRUG;

ARTICLE; BIOCATALYSIS; CHEMICAL STRUCTURE; CIRCULAR DICHROISM; CONCENTRATION LOSS; CONFORMATIONAL TRANSITION; DENATURATION; DIELECTRIC CONSTANT; DIPOLE; ENANTIOSELECTIVITY; ENZYME ACTIVITY; FLUORESCENCE; FLUORESCENCE SPECTROSCOPY; HUMAN; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STABILITY; STEADY STATE; THERMOSTABILITY;

BACTERIAL PROTEINS; CIRCULAR DICHROISM; ENZYME STABILITY; FURANS; HOT TEMPERATURE; HYDROLASES; ORGANIC CHEMICALS; RECOMBINANT FUSION PROTEINS; SOLVENTS;

EID: 84878971756     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201200378     Document Type: Article

References (83)

1. Clouthier, C. M., Pelletier, J. N., Expanding the organic toolbox: A guide to integrating biocatalysis in synthesis. Chem. Soc. Rev. 2012, 41, 1585.
2. Koeller, K. M., Wong, C. H., Enzymes for chemical synthesis. Nature 2001, 409, 232-240.
3. Soetaert, W., Vandamme, E., The impact of industrial biotechnology. Biotechnol. J. 2006, 1, 756-769.
4. Carrea, G., Riva, S., Properties and synthetic applications of enzymes in organic solvents. Angew. Chem. Int. Ed. 2000, 39, 2226-2254.
5. Klibanov, A. M., Improving enzymes by using them in organic solvents. Nature 2001, 409, 241-246.
6. Schmid, A., Dordick, J. S., Hauer, B., Kiener, A. et al., Industrial biocatalysis today and tomorrow. Nature 2001, 409, 258-268.
7. Andrade, L. H., Piovan, L., Pasquini, M. D., Improving the enantioselective bioreduction of aromatic ketones mediated by Aspergillus terreus and Rhizopus oryzae: The role of glycerol as a co-solvent. Tetrahedron: Asymm. 2009, 20, 1521-1525.
8. Kansal, H., Banerjee, U. C., Enhancing the biocatalytic potential of carbonyl reductase of Candida viswanathii using aqueous-organic solvent system. Bioresour. Technol. 2009, 100, 1041-1047.
9. Klibanov, A. M., Asymmetric enzymatic oxidoreductions in organic solvents. Curr. Opin. Biotechnol. 2003, 14, 427-431.
10. Lavandera, I., Kern, A., Schaffenberger, M., Gross, J. et al., An exceptionally DMSO-tolerant alcohol dehydrogenase for the stereoselective reduction of ketones. ChemSusChem 2008, 1, 431-436.
11. Watanabe, K., Ueji, S., Dimethyl sulfoxide as a co-solvent dramatically enhances the enantioselectivity in lipase-catalysed resolutions of 2-phenoxypropionic acyl derivatives. J. Chem. Soc., Perkin Trans. 2001, 1, 1386-1390.
12. Clark, D. S., Characteristics of nearly dry enzymes in organic solvents: Implications for biocatalysis in the absence of water. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 2004, 359, 1299-1307.
13. Fasoli, E., Ferrer, A., Barletta, G. L., Hydrogen/deuterium exchange study of subtilisin Carlsberg during prolonged exposure to organic solvents. Biotechnol. Bioeng. 2009, 102, 1025-1032.
14. Graber, M., Irague, R., Rosenfeld, E., Lamare, S. et al., Solvent as a competitive inhibitor for Candida antarctica lipase B. Biochim. Biophys. Acta, Proteins Proteomics 2007, 1774, 1052-1057.
15. Mattos, C., Ringe, D., Proteins in organic solvents. Curr. Opin. Struct. Biol. 2001, 11, 761-764.
16. Serdakowski, A. L., Dordick, J. S., Enzyme activation for organic solvents made easy. Trends Biotechnol. 2008, 26, 48-54.
17. Copley, S. D., Microbial dehalogenases: Enzymes recruited to convert xenobiotic substrates. Curr. Opin. Chem. Biol. 1998, 2, 613-617.
18. Koudelakova, T., Bidmanova, S, Dvorak, P., Pavelka, A. et al., Haloalkane dehalogenases: Biotechnological applications. Biotechnol. J. 2012, 8, 32-45.
19. Stucki, G., Thueer, M., Experiences of a large-scale application of 1, 2-dichloroethane degrading microorganisms for groundwater treatment. Environ. Sci. Technol. 1995, 29, 2339-2345.
20. Prokop, Z., Oplustil, F., DeFrank, J., Damborsky, J., Enzymes fight chemical weapons. Biotechnol. J. 2006, 1, 1370-1380.
21. Lal, R., Pandey, G., Sharma, P., Kumari, K. et al., Biochemistry of microbial degradation of hexachlorocyclohexane and prospects for bioremediation. Microbiol. Mol. Biol. Rev. 2010, 74, 58-80.
22. Mozga, T., Prokop, Z., Chaloupkova, R., Damborsky, J., Chiral aliphatic hydroxy compounds in nature: A review of biological functions and practical applications. Coll. Czech. Chem. Commun. 2009, 74, 1195-1278.
23. Patel, R. N., Biocatalytic synthesis of intermediates for the synthesis of chiral drug substances. Curr. Opin. Biotechnol. 2001, 12, 587-604.
24. Prokop, Z., Sato, Y., Brezovsky, J., Mozga, T. et al., Enantioselectivity of haloalkane dehalogenases and its modulation by surface loop engineering. Angew. Chem. Int. Ed. 2010, 49, 6111-6115.
25. Westerbeek, A., Szymanski, W., Feringa, B. L., Janssen, D. B., Dynamic kinetic resolution process employing haloalkane dehalogenase. ACS Catal. 2011, 1, 1654-1660.
26. Sato, Y., Monincová, M., Chaloupková, R., Prokop, Z. et al., Two rhizobial strains, Mesorhizobium loti MAFF303099 and Bradyrhizobium japonicum USDA110, encode haloalkane dehalogenases with novel structures and substrate specificities. Appl. Environ. Microbiol. 2005, 71, 4372-4379.
27. Newman, J., Peat, T. S., Richard, R., Kan, L. et al., Haloalkane dehalogenases: Structure of a Rhodococcus enzyme. Biochemistry 1999, 38, 16105-16114.
28. Marek, J., Vevodova, J., Smatanova, I. K., Nagata, Y. et al., Crystal structure of the haloalkane dehalogenase from Sphingomonas paucimobilis UT26. Biochemistry 2000, 39, 14082-14086.
29. Nagata, Y., Hynkova, K., Damborsky, J., Takagi, M., Construction and characterization of histidine-tagged haloalkane dehalogenase (LinB) of a new substrate class from a gamma-hexachlorocyclohexane-degrading bacterium, Sphingomonas paucimobilis UT26. Protein Expr. Purif. 1999, 17, 299-304.
30. Pavlova, M., Klvana, M., Prokop, Z., Chaloupkova, R. et al., Redesigning dehalogenase access tunnels as a strategy for degrading an anthropogenic substrate. Nat. Chem. Biol. 2009, 5, 727-733.
31. Iwasaki, I., Utsumi, S., Ozawa, T., New colorimetric determination of chloride using mercuric thiocyanate and ferric ion. Bull. Chem. Soc. Jpn. 1952, 25, 226-226.
32. Ladbrooke, B. D., Williams, R. M., Chapman, D., Studies on lecithin-cholesterol-water interactions by differential scanning calorimetry and X-ray diffraction. Biochim. Biophys. Acta, Biomembranes 1968, 150, 333-340.
33. Chen, C. S., Fujimoto, Y., Girdaukas, G., Sih, C. J., Quantitative analyses of biochemical kinetic resolutions of enantiomers. J. Am. Chem. Soc. 1982, 104, 7294-7299.
34. Kumar, A., Venkatesu, P., Overview of the stability of (-chymotrypsin in different solvent media. Chem. Rev. 2012, 112, 4283-4307.
35. Abbas, S. A., Sharma, V. K., Patapoff, T. W., Kalonia, D. S., Opposite effects of polyols on antibody aggregation thermal versus mechanical stresses. Pharm. Res. 2012, 29, 683-694.
36. Mozhaev, V. V., Khmelnitsky, Y. L., Sergeeva, M. V., Belova, A. B. et al., Catalytic activity and denaturation of enzymes in water/organic cosolvent mixtures. Eur. J. Biochem. 1989, 184, 597-602.
37. Kim, J., Clark, D. S., Dordick, J. S., Intrinsic effects of solvent polarity on enzymic activation energies. Biotechnol. Bioeng. 2000, 67, 112-116.
38. Klibanov, A., Why are enzymes less active in organic solvents than in water? Trends Biotechnol. 1997, 15, 97-101.
39. Toth, K., Sedlak, E., Musatov, A., Zoldak, G., Activity of NADH oxidase from Thermus thermophilus in water/alcohol binary mixtures is limited by the stability of quaternary structure. J. Mol. Catal. B Enzym. 2010, 64, 60-67.
40. Khmelnitsky, Y. L., Mozhaev, V. V., Belova, A. B., Sergeeva, M. V., Martinek, K., Denaturation capacity: A new quantitative criterion for selection of organic solvents as reaction media in biocatalysis. Eur. J. Biochem. 1991, 198, 31-41.
41. Park, H., Lee, K.-S., Chi, Y.-M., Jeong, S.-W., Effects of methanol on the catalytic properties of porcine pancreatic lipase. J. Microb. Biotechnol. 2005, 15, 296-301.
42. Tsuzuki, W., Ue, A., Nagao, A., Polar organic solvent added to an aqueous solution changes hydrolytic property of lipase. Biosci. Biotechnol. Biochem. 2003, 67, 1660-1666.
43. Kudryashova, E. V., Gladilin, A. K., Vakurov, A. V., Heitz, F. et al., Enzyme-polyelectrolyte complexes in water-ethanol mixtures: Negatively charged groups artificially introduced into (-chymotrypsin provide additional activation and stabilization effects. Biotechnol. Bioeng. 1997, 55, 267-277.
44. Lozano, P., Diego, T., Iborra, J. L., Effect of water-miscible aprotic solvents on kyotorphin synthesis catalyzed by immobilized α-chymotrypsin. Biotechnol. Lett. 1995, 17, 603-608.
45. Wiggers, H. J., Cheleski, J., Zottis, A., Oliva, G. et al., Effects of organic solvents on the enzyme activity of Trypanosoma cruzi glyceraldehyde-3-phosphate dehydrogenase in calorimetric assays. Anal. Biochem. 2007, 370, 107-114.
46. Inouye, K., Izawa, S., Saito, A., Tonomura, B., Effects of alcohols on the hydrolysis of colominic acid catalyzed by Streptococcus neuraminidase. J. Biochem. 1995, 117, 629-634.
47. Serebryakova, L. T., Zorin, N. A., Karyakin, A. A., Improvement of hydrogenase enzyme activity by water-miscible organic solvents. Enzyme Microb. Technol. 2009, 44, 329-333.
48. Secundo, F., Fialà, S., Fraaije, M. W., De Gonzalo, G. et al., Effects of water miscible organic solvents on the activity and conformation of the Baeyer-Villiger monooxygenases from Thermobifida fusca and Acinetobacter calcoaceticus: A comparative study. Biotechnol. Bioeng. 2011, 108, 491-499.
49. Mandrich, L., De Santi, C., De Pascale, D., Manco, G., Effect of low organic solvents concentration on the stability and catalytic activity of HSL-like carboxylesterases: Analysis from psychrophiles to (hyper)thermophiles. J. Mol. Catal. B Enzym. 2012, 82, 46-52.
50. Faulds, C. B., Pérez-Boada, M., Martínez, A. T., Influence of organic co-solvents on the activity and substrate specificity of feruloyl esterases. Bioresour. Technol. 2011, 102, 4962-4967.
51. Shan, S. O., Herschlag, D., The change in hydrogen bond strength accompanying charge rearrangement: Implications for enzymatic catalysis. Proc. Natl. Acad. Sci. USA 1996, 93, 14474-14479.
52. Venyaminov, S. Y., Yang, Y. T., Determination of protein secondary structure, in: Fasman, G. D., (Ed.), Circular Dichroism and the Conformational Analysis of Biomolecules. Plenum Press, New York 1996, pp. 69-107.
53. Kelly, S. M., Jess, T. J., Price, N. C., How to study proteins by circular dichroism. Biochim. Biophys. Acta Proteins Proteomics 2005, 1751, 119-139.
54. Lakowicz, J. R. (Ed.), Principles of Fluorescence Spectroscopy. Kluwer Academic/Plenum Publishers, New York 2006, 446-485.
55. Vinogradov, A. A., Kudryashova, E. V., Grinberg, V. Y., Grinberg, N. V. et al., The chemical modification of (-chymotrypsin with both hydrophobic and hydrophilic compounds stabilizes the enzyme against denaturation in water-organic media. Protein Eng. 2001, 14, 683-689.
56. Bhattacharjya, S., Balaram, P., Effects of organic solvents on protein structures: Observation of a structured helical core in hen egg-white lysozyme in aqueous dimethylsulfoxide. Proteins 1997, 29, 492-507.
57. Pazhang, M., Khajeh, K., Ranjbar, B., Hosseinkhani, S., Effects of water-miscible solvents and polyhydroxy compounds on the structure and enzymatic activity of thermolysin. J. Biotechnol. 2006, 127, 45-53.
58. Kijima, T., Yamamoto, S., Kise, H., Study on tryptophan fluorescence and catalytic activity of α-chymotrypsin in aqueous-organic media. Enzyme Microb. Technol. 1996, 18, 2-6.
59. Miroliaei, M., Nemat-Gorgani, M., Effect of organic solvents on stability and activity of two related alcohol dehydrogenases: A comparative study. Int. J. Biochem. Cell Biol. 2002, 34, 169-175.
60. Simon, L. M., Kotormán, M., Szabó, A., Nemcsók, J., Laczkó, I., The effects of organic solvent/water mixtures on the structure and catalytic activity of porcine pepsin. Process Biochem. 2007, 42, 909-912.
61. Xu, K., Griebenow, K., Klibanov, A. M., Correlation between catalytic activity and secondary structure of subtilisin dissolved in organic solvents. Biotechnol. Bioeng. 1997, 56, 485-491.
62. Polizzi, K. M., Bommarius, A. S., Broering, J. M., Chaparro-Riggers, J. F., Stability of biocatalysts. Curr. Opin. Chem. Biol. 2007, 11, 220-225.
63. Invernizzi, G., Casiraghi, L., Grandori, R., Lotti, M., Deactivation and unfolding are uncoupled in a bacterial lipase exposed to heat, low pH and organic solvents. J. Biotechnol. 2009, 141, 42-46.
64. Tsou, C. L., Inactivation precedes overall molecular conformation changes during enzyme denaturation. Biochim. Biophys. Acta 1995, 1253, 151-162.
65. Aldercreutz, P., Mattiasson, B., Aspects of biocatalyst stability in organic solvents. Biocatal. Biotrans. 1987, 1, 99-108.
66. Griebenow, K., Klibanov, A. M., On protein denaturation in aqueous-organic mixtures but not in pure organic solvents. J. Am. Chem. Soc. 1996, 118, 11695-11700.
67. Ogino, H., Ishikawa, H., Enzymes which are stable in the presence of organic solvents. J. Biosci. Bioeng. 2001, 91, 109-116.
68. Micaêlo, N. M., Soares, C. M., Modeling hydration mechanisms of enzymes in nonpolar and polar organic solvents. FEBS J. 2007, 274, 2424-2436.
69. Yang, P.-H., Rupley, J. A., Protein-water interactions. Heat capacity of the lysozyme-water system. Biochemistry 1979, 18, 2654-2661.
70. Bovara, R., Carrea, G., Ferrara, L., Riva, S., Resolution of (±)-trans-sobrerol by lipase PS-catalyzed transesterification and effects of organic solvents on enantioselectivity. Tetrahedron: Asymm. 1991, 2, 931-938.
71. Chua, L. S., Sarmidi, M. R., Effect of solvent and initial water content on (R, S)-1-phenylethanol resolution. Enzyme Microb. Technol. 2006, 38, 551-556.
72. Wang, Y., Li, Q., Zhang, Z., Ma, J., Feng, Y., Solvent effects on the enantioselectivity of the thermophilic lipase QLM in the resolution of (R, S)-2-octanol and (R, S)-2-pentanol. J. Catal. B Enzym. 2009, 56, 146-150.
73. Ammazzalorso, A., Amoroso, R., Bettoni, G., De Filippis, B. et al., Candida rugosa lipase-catalysed kinetic resolution of 2-substituted-aryloxyacetic esters with dimethylsulfoxide and isopropanol as additives. Chirality 2008, 20, 115-118.
74. Heinsman, N. W., Valente, A. M., Smienk, H. G., Van der Padt, A. et al., The effect of ethanol on the kinetics of lipase-mediated enantioselective esterification of 4-methyloctanoic acid and the hydrolysis of its ethyl ester. Biotechnol. Bioeng. 2001, 76, 193-199.
75. Jin, X., Liu, B., Ni, Z., Wu, Q., Lin, X., A novel control of enzymatic enantioselectivity through the racemic temperature influenced by reaction media. Enzyme Microb. Technol. 2011, 48, 454-457.
76. Ottosson, J., Fransson, L., King, J. W., Hult, K., Size as a parameter for solvent effects on Candida antarctica lipase B enantioselectivity. Biochim. Biophys. Acta Protein Struct. Mol. Enzymol. 2002, 1594, 325-334.
77. De Gonzalo, G., Ottolina, G., Zambianchi, F., Fraaije, M. W., Carrea, G., Biocatalytic properties of Baeyer-Villiger monooxygenases in aqueous-organic media. J. Mol. Catal. B Enzym. 2006, 39, 91-97.
78. Schumacher, J., Eckstein, M., Kragl, U., Influence of water-miscible organic solvents on kinetics and enantioselectivity of the (R)-specific alcohol dehydrogenase from Lactobacillus brevis. Biotechnol. J. 2006, 1, 574-581.
79. Fitzpatrick, P. A., Klibanov, A. M., How can the solvent affect enzyme enantioselectivity? J. Am. Chem. Soc. 1991, 113, 3166-3171.
80. Kawashiro, K., Sugahara, H., Sugiyama, S., Hayashi, H., Effect of organic solvents on enantioselectivity of protease catalysis. Biotechnol. Bioeng. 1997, 53, 26-31.
81. Carrea, G., Ottolina, G., Riva, S., Role of solvents in the control of enzyme selectivity in organic media. Trends Biotechnol. 1995, 13, 63-70.
82. De Gonzalo, G., Rodríguez, C., Rioz-Martínez, A., Gotor, V., Improvement of the biocatalytic properties of one phenylacetone monooxygenase mutant in hydrophilic organic solvents. Enzyme Microb. Technol. 2012, 50, 43-49.
83. Colombo, G., Toba, S., Merz, K. M., Rationalization of the enantioselectivity of subtilisin in DMF. J. Am. Chem. Soc. 1999, 121, 3486-3493.