Balancing the stability-activity trade-off by fine-tuning dehalogenase access tunnels

ChemCatChem

Volumn 7, Issue 4, 2015, Pages 648-659

  Liskova, Veronika ^a,b   Bednar, David ^a,b   Prudnikova, Tatyana ^c,d   Rezacova, Pavlina ^e,f   Koudelakova, Tana ^a   Sebestova, Eva ^a   Smatanova, Ivana Kuta ^c,d   Brezovsky, Jan ^a   Chaloupkova, Radka ^a   Damborsky, Jiri ^a,b  

^a MASARYK UNIVERSITY   (Czech Republic)

^b ST ANNE S UNIVERSITY HOSPITAL   (Czech Republic)

^c UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^d INSTITUTE OF MATHEMATICS   (Czech Republic)

^e INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

^f INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

Author keywords

alkanes; enzyme catalysis; halogenation; molecular dynamics; protein engineering

Indexed keywords

BIOCHEMICAL ENGINEERING; ECONOMIC AND SOCIAL EFFECTS; ENZYME ACTIVITY; ENZYMES; HALOGENATION; MOLECULAR DYNAMICS; PARAFFINS; STABILITY;

1 ,2-DIBROMOETHANE; ACTIVE SITE; BULK SOLVENTS; DEHALOGENASE; ENHANCED STABILITY; ENZYME CATALYSIS; FINE TUNING; PROTEIN ENGINEERING;

CATALYST ACTIVITY;

EID: 85027929577     PISSN: 18673880     EISSN: 18673899     Source Type: Journal    
DOI: 10.1002/cctc.201402792     Document Type: Article

References (103)

1. Y. Xie, J. An, G. Yang, G. Wu, Y. Zhang, L. Cui, Y. Feng, J. Biol. Chem. 2014, 289, 7994-8006.
2. B. M. Beadle, B. K. Shoichet, J. Mol. Biol. 2002, 321, 285-296.
3. E. M. Meiering, L. Serrano, A. R. Fersht, J. Mol. Biol. 1992, 225, 585-589.
4. C. Schreiber, A. M. Buckle, A. R. Fersht, Structure 1994, 2, 945-951.
5. V. L. Thomas, A. C. McReynolds, B. K. Shoichet, J. Mol. Biol. 2010, 396, 47-59.
6. X. Wang, G. Minasov, B. K. Shoichet, J. Mol. Biol. 2002, 320, 85-95.
7. T. Davids, M. Schmidt, D. Böttcher, U. T. Bornscheuer, Curr. Opin. Chem. Biol. 2013, 17, 215-220.
8. R. Chaloupková, J. Sýkorová, Z. Prokop, A. Jesenská, M. Monincová, M. Pavlová, M. Tsuda, Y. Nagata, J. Damborský, J. Biol. Chem. 2003, 278, 52622-52628.
9. V. G. H. Eijsink, A. Bjørk, S. Gåseidnes, R. Sirevåg, B. Synstad, B. vandenBurg, G. Vriend, J. Biotechnol. 2004, 113, 105-120.
10. J. T. Holland, J. C. Harper, P. L. Dolan, M. M. Manginell, D. C. Arango, J. A. Rawlings, C. A. Apblett, S. M. Brozik, PLoS One 2012, 7, e 37924.
11. H. Zhao, K. Chockalingam, Z. Chen, Curr. Opin. Biotechnol. 2002, 13, 104-110.
12. P. Dalby, Curr. Opin. Struct. Biol. 2011, 21, 473-480.
13. M. Lehmann, M. Wyss, Curr. Opin. Biotechnol. 2001, 12, 371-375.
14. R. A. Chica, N. Doucet, J. N. Pelletier, Curr. Opin. Biotechnol. 2005, 16, 378-384.
15. H. B. Brundiek, A. S. Evitt, R. Kourist, U. T. Bornscheuer, Angew. Chem. Int. Ed. 2012, 51, 412-414
16. Angew. Chem. 2012, 124, 425-428.
17. H. J. Wijma, R. J. Floor, D. B. Janssen, Curr. Opin. Struct. Biol. 2013, 23, 588-594.
18. J. Damborský, E. Rorije, A. Jesenská, Y. Nagata, G. Klopman, W. J. Peijnenburg, Environ. Toxicol. Chem. 2001, 20, 2681-2689.
19. M. Stucki, G. Thuer, Environ. Sci. Technol. 1995, 29, 2339-2345.
20. K. Skopelitou, N. Georgakis, R. Efrose, E. Flemetakis, N. E. Labrou, J. Mol. Catal. B 2013, 97, 5-11.
21. Z. Prokop, F. Oplustil, J. DeFrank, J. Damborský, Biotechnol. J. 2006, 1, 1370-1380.
22. A. Westerbeek, W. Szymański, H. J. Wijma, S. J. Marrink, B. L. Feringa, D. B. Janssen, Adv. Synth. Catal. 2011, 353, 931-944.
23. Z. Prokop, Y. Sato, J. Brezovsky, T. Mozga, R. Chaloupkova, T. Koudelakova, P. Jerabek, V. Stepankova, R. Natsume, J. G. E. vanLeeuwen, D. B. Janssen, J. Florian, Y. Nagata, T. Senda, J. Damborsky, Angew. Chem. Int. Ed. 2010, 49, 6111-6115
24. Angew. Chem. 2010, 122, 6247-6251.
25. S. Bidmanova, R. Chaloupkova, J. Damborsky, Z. Prokop, Anal. Bioanal. Chem. 2010, 398, 1891-1898.
26. S. Bidmanova, A. Hlavacek, J. Damborsky, Z. Prokop, Sens. Actuators B 2012, 161, 93-99.
27. S. Bidmanova, J. Damborsky, Z. Prokop, J. Biocatal. Biotransformation 2013, 2, 1-7.
28. S. Mazzucchelli, M. Colombo, P. Verderio, E. Rozek, F. Andreata, E. Galbiati, P. Tortora, F. Corsi, D. Prosperi, Angew. Chem. Int. Ed. 2013, 52, 3121-3125
29. Angew. Chem. 2013, 125, 3203-3207.
30. G. Los, R. Learish, N. Karassina, C. Zimprich, M. G. Mcdougall, L. P. Encell, R. Freidman-Ohana, M. Wood, G. Vidugiris, K. Zimmerman, P. Otto, S. Berhstock, D. H. Klaubert, K. Wood, Cell Notes 2006, 10-14.
31. G.V. Los, K. Wood in Methods in Molecular Biology: High Content Screening: A Powerful Approach to Systems Cell Biology and Drug Discovery, Vol.356 (Eds.: D.L. Taylor, J.R. Haskins, K. Giuliano) Humana Press, Inc, Totowa, 2006, pp.195-208.
32. G. V. Los, L. P. Encell, M. G. Mcdougall, D. D. Hartzell, N. Karassina, C. Zimprich, M. G. Wood, R. Learish, R. F. Ohana, M. Urh, D. Simpson, J. Mendez, K. Zimmerman, P. Otto, G. Vidugiris, J. Zhu, A. Darzins, D. H. Klaubert, R. F. Bulleit, K. V. Wood, ACS Chem. Biol. 2008, 3, 373-382.
33. G. V. Los, A. Drazins, N. Karassina, C. Zimprich, R. Learish, M. G. Mcdougall, L. P. Encell, R. Friedman-Ohana, M. Wood, G. Vidugiris, K. Zimmerman, P. Otto, D. H. Klaubert, K. V. Wood, Cell Notes 2005, 2-6.
34. R. Chaloupkova, Z. Prokop, Y. Sato, Y. Nagata, J. Damborsky, FEBS J. 2011, 278, 2728-2738.
35. V. Stepankova, J. Damborsky, R. Chaloupkova, Biotechnol. J. 2013, 8, 719-729.
36. T. Koudelakova, R. Chaloupkova, J. Brezovsky, Z. Prokop, E. Sebestova, M. Hesseler, M. Khabiri, M. Plevaka, D. Kulik, I. K. Smatanova, P. Rezacova, R. Ettrich, U. T. Bornscheuer, J. Damborsky, Angew. Chem. Int. Ed. 2013, 52, 1959-1963
37. Angew. Chem. 2013, 125, 2013-2017.
38. A. N. Kulakova, M. J. Larkin, L. A. Kulakov, Microbiology 1997, 143, 109-115.
39. K. A. Gray, T. H. Richardson, K. Kretz, J. M. Short, F. Bartnek, R. Knowles, L. Kan, P. E. Swanson, D. E. Robertson, Adv. Synth. Catal. 2001, 343, 607-617.
40. R. Guerois, J. E. Nielsen, L. Serrano, J. Mol. Biol. 2002, 320, 369-387.
41. M. T. Reetz, J. D. Carballeira, Nat. Protoc. 2007, 2, 891-903.
42. P. Holloway, J. T. Trevors, H. Lee, J. Microbiol. Methods 1998, 32, 31-36.
43. S. Y. Venyaminov, J. T. Yang, in Circular Dichroism and the Conformational Analysis of Biomolecules, (Ed.:, G.D. Fasman,), Plenum Press, New York and London, 1996, pp. 69-108.
44. T. Koudelakova, E. Chovancova, J. Brezovsky, M. Monincova, A. Fortova, J. Jarkovsky, J. Damborsky, Biochem. J. 2011, 435, 345-354.
45. A. Stsiapanava, J. Dohnalek, J. Gavira, M. Kuty, T. Koudelakova, J. Damborsky, I. K. Smatanova, Acta Crystallogr. Sect. D 2010, 66, 962-969.
46. J. Newman, T. S. Peat, R. Richard, L. Kan, P. E. Swanson, J. A. Affholter, I. H. Holmes, J. F. Schindler, C. J. Unkefer, T. C. Terwilliger, Biochemistry 1999, 38, 16105-16114.
47. E. Chovancova, A. Pavelka, P. Benes, O. Strnad, J. Brezovsky, B. Kozlikova, A. Gora, V. Sustr, M. Klvana, P. Medek, L. Biedermannova, J. Sochor, J. Damborsky, PLoS Comput. Biol. 2012, 8, e 1002708.
48. J. Damborsky, J. Brezovsky, Curr. Opin. Chem. Biol. 2014, 19, 8-16.
49. B. X. Yan, Y. Q. Sun, J. Biol. Chem. 1997, 272, 3190-3194.
50. H. Neurath, J. Am. Chem. Soc. 1943, 65, 2039-2041.
51. M. T. Reetz, J. D. Carballeira, A. Vogel, Angew. Chem. Int. Ed. 2006, 45, 7745-7751
52. Angew. Chem. 2006, 118, 7909-7915.
53. G. Feller, J. Phys. Condens. Matter 2010, 22, 323101.
54. H. Jochens, D. Aerts, U. T. Bornscheuer, Protein Eng. Des. Sel. 2010, 23, 903-909.
55. M. T. Reetz, P. Soni, L. Fernández, Y. Gumulya, J. D. Carballeira, Chem. Commun. 2010, 46, 8657-8658.
56. P. Fields, Comp. Biochem. Physiol. Part A 2001, 129, 417-431.
57. S. Cesarini, C. Bofill, F. I. J. Pastor, M. T. Reetz, P. Diaz, Process Biochem. 2012, 47, 2064-2071.
58. C. L. Tsou, Science 1993, 262, 380-381.
59. P. Banás, M. Otyepka, P. Jerábek, M. Petrek, J. Damborský, J. Comput.-Aided. Mol. Des. 2006, 20, 375-383.
60. M. Pavlova, M. Klvana, Z. Prokop, R. Chaloupkova, P. Banas, M. Otyepka, R. C. Wade, M. Tsuda, Y. Nagata, J. Damborsky, Nat. Chem. Biol. 2009, 5, 727-733.
61. J. Damborsky, Z. Prokop, T. Koudelakova, V. Stepankova, R. Chaloupkova, A. Gora, E. Chovancova, J. Brezovsky, Method of Thermostabilisation of a Protein and/or Stabilisation Towards Organic Solvents, 2013, US 8,580,932.
62. Z. Prokop, A. Gora, J. Brezovsky, R. Chaloupkova, V. Stepankova, J. Damborsky, in Protein Engineering Handbook (Eds.:, S. Lutz, U.T. Bornscheuer,), Wiley-VCH, Weinheim, 2012, pp. 421-464.
63. G. Smith, S. Modi, I. Pillai, L. Lian, M. J. Sutcliffe, M. P. Pritchard, T. Friedberg, G. C. K. Roberts, C. R. Wolf, Biochem. J. 1998, 331, 783-792.
64. T. Nguyen, M. Tychopoulos, F. Bichat, C. Zimmermann, J. Flinois, M. Diry, E. Ahlberg, M. Delaforge, L. Corcos, P. Beaune, P. Dansette, F. Andre, I. deWaziers, Mol. Pharmacol. 2008, 73, 1122-1133.
65. D. Fishelovitch, S. Shaik, H. J. Wolfson, R. Nussinov, J. Phys. Chem. B 2009, 113, 13018-13025.
66. K. K. Khan, Y. Q. He, T. L. Domanski, J. R. Halpert, Mol. Pharmacol. 2002, 61, 495-506.
67. Z. Wen, J. Baudry, M. R. Berenbaum, M. A. Schuler, Protein Eng. Des. Sel. 2005, 18, 191-199.
68. A. B. Carmichael, L. L. Wong, Eur. J. Biochem. 2001, 268, 3117-3125.
69. H.-L. Lee, C.-K. Chang, W.-Y. Jeng, A. H.-J. Wang, P.-H. Liang, Protein Eng. Des. Sel. 2012, 25, 733-740.
70. J. Schmitt, S. Brocca, R. D. Schmid, J. Pleiss, Protein Eng. 2002, 15, 595-601.
71. Z. Qian, J. R. Horton, X. Cheng, S. Lutz, J. Mol. Biol. 2009, 393, 191-201.
72. Z. Marton, V. Léonard-Nevers, P.-O. Syrén, C. Bauer, S. Lamare, K. Hult, V. Tranc, M. Graber, J. Mol. Catal. B 2010, 65, 11-17.
73. M. Z. Kamal, T. A. S. Mohammad, G. Krishnamoorthy, N. M. Rao, PLoS One 2012, 7, e 35188.
74. H. Brundiek, S. K. Padhi, R. Kourist, A. Evitt, U. T. Bornscheuer, Eur. J. Lipid Sci. Technol. 2012, 114, 1148-1153.
75. A. Schließmann, A. Hidalgo, J. Berenguer, U. T. Bornscheuer, ChemBioChem 2009, 10, 2920-2923.
76. M. Kotik, V. Stepánek, P. Kyslík, H. Maresová, J. Biotechnol. 2007, 132, 8-15.
77. B. VanLoo, J. H. L. Spelberg, J. Kingma, T. Sonke, M. G. Wubbolts, D. B. Janssen, Chem. Biol. 2004, 11, 981-990.
78. L. Biedermannová, Z. Prokop, A. Gora, E. Chovancová, M. Kovács, J. Damborsky, R. C. Wade, J. Biol. Chem. 2012, 287, 29062-29074.
79. T. Bosma, G. Stucki, D. B. Janssen, Appl. Environ. Microbiol. 2002, 68, 3582-3587.
80. M. Klvana, M. Pavlova, T. Koudelakova, R. Chaloupkova, P. Dvorak, Z. Prokop, A. Stsiapanava, M. Kuty, I. Kuta-Smatanova, J. Dohnalek, P. Kulhanek, R. C. Wade, J. Damborsky, J. Mol. Biol. 2009, 392, 1339-1356.
81. A. Gora, J. Brezovsky, J. Damborsky, Chem. Rev. 2013, 113, 5871-5923.
82. H. M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T. N. Bhat, H. Weissig, I. N. Shindyalov, P. E. Bourne, Nucleic Acids Res. 2000, 28, 235-242.
83. J. Sambrook, D. W. Russel, Molecular Cloning, A Laboratory Manual, 3rded., Cold Spring Harbor Laboratory Press, New York, 2001.
84. I. Iwasaki, S. Utsumi, T. Ozawa, Bull. Chem. Soc. Jpn. 1952, 25, 226-226.
85. S. Wold, K. Esbensen, P. Geladi, Chemom. Intell. Lab. Syst. 1987, 2, 37-52.
86. I. H. Segel, Enzyme Kinetics, Wiley, New York, 1993.
87. V. Stepankova, M. Khabiri, J. Brezovsky, A. Pavelka, J. Sykora, M. Amaro, B. Minofar, Z. Prokop, M. Hof, R. Ettrich, R. Chaloupkova, J. Damborsky, ChemBioChem 2013, 14, 890-897.
88. W. Kabsch, J. Appl. Crystallogr. 1993, 26, 795-800.
89. A. Vagin, A. Teplyakov, J. Appl. Crystallogr. 1997, 30, 1022-1025.
90. A. Stsiapanava, R. Chaloupkova, A. Fortova, J. Brynda, M. S. Weiss, J. Damborsky, I. K. Smatanova, Acta Crystallogr. Sect. F 2011, 67, 253-257.
91. G. N. Murshudov, A. A. Vagin, Acta Crystallogr. Sect. D 1997, 53, 240-255.
92. P. Emsley, B. Lohkamp, W. G. Scott, K. Cowtan, Acta Crystallogr. Sect. D 2010, 66, 486-501.
93. A. A. Vaguine, J. Richelle, S. J. Wodak, Acta Crystallogr. Sect. D 1999, 55, 191-205.
94. V. B. Chen, W. B. Arendall, J. J. Headd, D. A. Keedy, R. M. Immormino, G. J. Kapral, L. W. Murray, J. S. Richardson, D. C. Richardson, Acta Crystallogr. Sect. D 2010, 66, 12-21.
95. E. H. Kellogg, A. Leaver-Fay, D. Baker, Proteins 2011, 79, 830-838.
96. J. C. Gordon, J. B. Myers, T. Folta, V. Shoja, L. S. Heath, A. Onufriev, Nucleic Acids Res. 2005, 33, W 368 -W 371.
97. D.A. Case, T.A. Darden, T.E. Cheatham, III, C.L. Simmerling, J. Wang, R.E. Duke, R. Luo, R.C. Walker, W. Zhang, K.M. Merz, B. Roberts, S. Hayik, A. Roitberg, G. Seabra, J. Swails, A.W. Götz, I. Kolossváry, K.F. Wong, F. Paesani, J. Vanicek, R.M. Wolf, J. Liu, X. Wu, S.R. Brozell, T. Steinbrecher, H. Gohlke, Q. Cai, X. Ye, J. Wang, M.-J. Hsieh, G. Cui, D.R. Roe, D.H. Mathews, M.G. Seetin, R. Salomon-Ferrer, C. Sagui, V. Babin, T. Luchko, S. Gusarov, A. Kovalenko, P.A. Kollman, AMBER 12, 2012, University of California, San Francisco.
98. W. L. Jorgensen, J. Chandrasekhar, J. D. Madura, R. W. Impey, M. L. Klein, J. Chem. Phys. 1983, 79, 926-935.
99. V. Hornak, R. Abel, A. Okur, B. Strockbine, A. Roitberg, C. Simmerling, Proteins 2006, 65, 712-725.
100. T. Darden, D. York, L. Pedersen, J. Chem. Phys. 1993, 98, 10089-10092.
101. U. Essmann, L. Perera, M. L. Berkowitz, T. Darden, H. Lee, L. G. Pedersen, J. Chem. Phys. 1995, 103, 8577-8593.
102. J. P. Ryckaert, G. Ciccotti, H. J. Berendsen, J. Comput. Phys. 1977, 23, 327-341.
103. W. Humphrey, A. Dalke, K. Schulten, J. Mol. Graphics 1996, 14, 33-38.