Use of directed evolution of mammalian cytochromes P450 for investigating the molecular basis of enzyme function and generating novel biocatalysts

Biochemical and Biophysical Research Communications

Volumn 338, Issue 1, 2005, Pages 456-464

  Kumar, Santosh ^a   Halpert, James R ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Biocatalysts; Cytochrome P450; Directed evolution; P450; Random mutagenesis

Indexed keywords

CYTOCHROME P450; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; CYTOCHROME P450 2A6; CYTOCHROME P450 2B1; CYTOCHROME P450 2B6; CYTOCHROME P450 2C8; CYTOCHROME P450 2C9; CYTOCHROME P450 2D6; CYTOCHROME P450 2E1; CYTOCHROME P450 3A4; CYTOCHROME P450 3A5; DNA FRAGMENT; DNA POLYMERASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; XENOBIOTIC AGENT;

AMINO ACID SEQUENCE; BIOCATALYST; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME MECHANISM; ENZYME STRUCTURE; ENZYME SUBSTRATE; FLUORESCENCE ANALYSIS; HUMAN; IN VITRO STUDY; MOLECULAR BIOLOGY; MOLECULAR EVOLUTION; MUTAGENESIS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REVIEW; SCREENING; STRUCTURE ANALYSIS; XENOBIOTIC METABOLISM;

ANIMALS; BACTERIAL PROTEINS; CYTOCHROME P-450 ENZYME SYSTEM; DIRECTED MOLECULAR EVOLUTION; HUMANS;

MAMMALIA;

EID: 27544466682     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2005.08.080     Document Type: Review

References (73)

1. Z. Shao, and F.H. Arnold Engineering new functions and altering existing functions Curr. Opin. Struct. Biol. 6 1996 513 518
2. F.H. Arnold, P.L. Wintrode, K. Miyazaki, and A. Gershenson How enzymes adapt: lessons from directed evolution Trends Biochem. Sci. 26 2001 100 1066
3. N.J. Turner Directed evolution of enzymes for applied biocatalysis Trends Biotechnol. 21 2003 474 478
4. E.G. Hibbert, F. Baganz, H.C. Hailes, J.M. Ward, G.J. Lye, J.M. Woodley, and P.A. Dalby Directed evolution of biocatalytic processes Biomol. Engin. 22 2005 11 19
5. H.E. Schoemaker Dispelling the myths-biocatalysis in industrial synthesis Science 299 2003 1694 1697
6. E.M. Gillam Exploring the potential of xenobiotic-metabolising enzymes as biocatalysts: Evolving designer catalysts from polyfunctional cytochrome P450 enzymes Clin. Exp. Pharm. Phys. 32 2005 147 152
7. P.T. Anastas, and M.M. Kirchhoff Origins, current status, and future challenges of green chemistry Acc. Chem. Res. 35 2002 686 694
8. E.C. Watkins Role of cytochrome P450 phenotyping in cancer treatment J. Clin. Oncol. 23 2005 1053 1055
9. M.W. Peters, P. Meinhold, A. Glieder, and F.H. Arnold Regio- and enantioselective alkane hydroxylation with engineered cytochromes P450 BM3 J. Am. Chem. Soc. 125 2003 13442 13450
10. A. Glieder, E.T. Farinas, and F.H. Arnold Laboratory evolution of a soluble, self-sufficient, highly active alkane hydroxylase Nat. Biotechnol. 20 2002 1135 1139
11. P.C. Cirino, and F.H. Arnold A self-sufficient peroxide-driven hydroxylation biocatalyst Angew. Chem. Int. Ed. 42 2003 3299 3301
12. H. Joo, Z. Lin, and F.H. Arnold Laboratory evolution of peroxide-mediated cytochrome P450 hydroxylation Nature 399 1999 670 672
13. M.J. Coon Cytochrome P450: nature's most versatile biological catalyst Annu. Rev. Pharmacol. Toxicol. 45 2005 1 25
14. P. Anzenbacher, and F. Anzenbacherova Cytochromes P450 and metabolism of xenobiotics Cell. Mol. Life Sci. 58 2001 737 747
15. F.P. Guengerich Cytochromes P450, drugs, and diseases Mol. Interv. 3 2003 194 204
16. A.W. Munro, D.G. Leys, K.J. McLean, K.R. Marshall, T.W. Ost, S. Daff, C.S. Miles, S.K. Chapman, D.A. Lysek, C.C. Moser, C.C. Page, and P.L. Dutton P450 BM3: the very model of a modern flavocytochrome Trends Biochem. Sci. 27 2002 250 257
17. Y.M. Meharenna, T.L. Poulos, The structure of the alkane mutant of the P450 BM3, in: 14th International Conference on Cytochrome P450 P.ST40, 2005, p. 8.
18. P. Meinhold, M.W. Peters, M.M. Chen, K. Takahashi, and F.H. Arnold Direct conversion of ethane to ethanol by engineered cytochrome P450 BM3 ChemBioChem 6 2005 1 4
19. O. Salazar, P.C. Cirino, and F.H. Arnold Thermostabilization of a cytochrome P450 peroxygenase ChemBioChem 4 2003 891 893
20. T.S. Wong, F.H. Arnold, and U. Schwaneberg Laboratory evolution of cytochrome P450 BM3 monooxygenase for organic cosolvents Biotechnol. Bioeng. 85 2004 351 358
21. K.L. Tee, J. Grujic, T.S. Wong, U. Schwaneberg, Laboratory evolution of monooxygenase P450 BM3 for industrial applications, in: 14th International Conference on Cytochrome P450 P.S120, 2005, p. 166.
22. F.P. Guengerich Cytochrome P450 3A4: regulation and role in drug metabolism Annu. Rev. Pharmacol. Toxicol. 39 1999 1 17
23. T.S. Tracy Atypical enzyme kinetics: their effect on in vitro-in vivo pharmacokinetic predictions and drug interactions Curr. Drug Metab. 4 2003 341 346
24. L. Chen, and D.J. Waxman Cytochrome P450 gene-directed enzyme prodrug therapy (GDEPT) for cancer Curr. Pharm. Des. 8 2002 1405 1416
25. C.S. Chen, J.T. Lin, K.A. Goss, Y.A. He, J.R. Halpert, and D.J. Waxman Activation of the anticancer prodrugs cyclophosphamide and ifosfamide: identification of cytochrome P450 2B enzymes and site-specific mutants with improved enzyme kinetics Mol. Pharmacol. 65 2004 1278 1285
26. S.C. Waller, Y.A. He, G.R. Harlow, Y.Q. He, E.A. Mash, and J.R. Halpert 2,2′,3,3′,6,6′-hexachlorobiphenyl hydroxylation by active site mutants of cytochrome P450 2B1 and 2B11 Chem. Res. Toxicol. 12 1999 690 699
27. D. Kim, and F.P. Guengerich Cytochrome P450 activation of arylamines and heterocyclic amines Annu. Rev. Pharmacol. Toxicol. 45 2005 27 49
28. E.M. Gillam, L.M. Notley, H. Cai, J.J. De Voss, and F.P. Guengerich Oxidation of indole by cytochrome P450 enzymes Biochemistry 39 2000 13817 13824
29. J.A. Goldstein Clinical relevance of genetic polymorphisms in the human CYP2C subfamily Br. J. Clin. Pharmacol. 52 2001 349 355
30. T.L. Domanski, and J.R. Halpert Analysis of mammalian cytochrome P450 structure and function by site-directed mutagenesis Curr. Drug Metab. 2 2001 117 137
31. S. Kumar, E.E. Scott, H. Liu, and J.R. Halpert A rational approach to re-engineer cytochrome P450 2B1 regioselectivity based on the crystal structure of P450 2C5 J. Biol. Chem. 278 2003 17178 17184
32. E.E. Scott, Y.A. He, M.R. Wester, M.A. White, C.C. Chin, J.R. Halpert, E.F. Johnson, and C.D. Stout An open conformation of mammalian cytochrome P450 2B4 at 1.6-A resolution Proc. Nat. Acad. Sci. USA 100 2003 13196 13201
33. E.E. Scott, M.A. White, Y.A. He, E.F. Johnson, C.D. Stout, and J.R. Halpert Structure of mammalian cytochrome P450 2B4 complexed with 4-(4-chlorophenyl)imidazole at 1.9-Å resolution: insight into the range of P450 conformations and the coordination of redox partner binding J. Biol. Chem. 279 2004 27294 272301
34. G.D. Szklarz, and J.R. Halpert Use of homology modeling in conjunction with site-directed mutagenesis for analysis of structure-function relationships of mammalian cytochromes P450 Life Sci. 61 1997 2507 2520
35. E.E. Scott, and J.R. Halpert Structures of cytochrome P450 3A4 Trends Biochem. Sci. 30 2005 5 7
36. G.D. Szklarz, and J.R. Halpert Molecular modeling of cytochrome P450 3A4 J. Comput. Aided Mol. Des. 11 1997 265 272
37. P.A. Williams, J. Cosme, D.M. Vinkovic, A. Ward, H.C. Angove, P.J. Day, C. Vonrhein, I.J. Tickle, and H. Jhoti Crystal structures of human cytochrome P450 3A4 bound to metyrapone and progesterone Science 305 2004 683 686
38. J.K. Yano, M.R. Wester, G.A. Schoch, K.J. Griffin, C.D. Stout, and E.F. Johnson The structure of human microsomal cytochrome P450 3A4 determined by X-ray crystallography to 2.05 Å resolution J. Biol. Chem. 279 2004 38091 38094
39. E.E. Scott, Y.Q. He, and J.R. Halpert Substrate routes to the buried active site may vary among cytochromes P450: mutagenesis of the F-G region in P450 2B1 Chem. Res. Toxicol. 15 2002 1407 1413
40. W.H. Li, H. Liu, E.E. Scott, F. Grater, and J.R. Halpert Possible pathway(s) of testosterone egress from the active site of cytochrome P450 2B1: a steered molecular dynamics simulation Drug Metab. Dispos. 33 2005 910 919
41. W. Honma, W. Li, H. Liu, E.E. Scott, and J.R. Halpert Functional role of residues in the helix B' region of cytochrome P450 2B1 Arch. Biochem. Biophys. 435 2005 157 165
42. E.E. Scott, H. Liu, Y.Q. He, W. Li, and J.R. Halpert Mutagenesis and molecular dynamics suggest structural and functional roles for residues in the N-terminal portion of the cytochrome P450 2B1 I helix Arch. Biochem. Biophys. 423 2004 266 276
43. S. Kumar, C.S. Cheng, D.J. Waxman, and J.R. Halpert Directed evolution of mammalian cytochrome P450 2B1: mutations outside of the active site enhance the metabolism of several substrates including the anticancer prodrugs cyclophosphamide and ifosfamide J. Biol. Chem. 280 2005 19569 19575
44. F.P. Guengerich, A. Parikh, E.F. Johnson, T.H. Richardson, C. von Wachenfeldt, J. Cosme, F. Jung, C.P. Strassburg, M.P. Manns, R.H. Tukey, M. Pritchard, S. Fournel-Gigleux, and B. Burchell Heterologous expression of human drug-metabolizing enzymes Drug Metab. Dispos. 25 1997 1234 1241
45. M. Alcalde, E.T. Farinas, and F.H. Arnold Colorimetric high-throughput assay for alkene epoxidation catalyzed by cytochrome P450 BM3 variant 139-3 J. Biomol. Screen. 9 2004 141 146
46. D. Kim, and F.P. Guengerich Enhancement of 7-methoxyresorufin O-demethylation activity of human cytochrome P450 1A2 by molecular breeding Arch. Biochem. Biophys. 432 2004 102 108
47. K. Nakamura, M.V. Martin, and F.P. Guengerich Random mutagenesis of human cytochrome P450 2A6 and screening with indole oxidation products Arch. Biochem. Biophys. 395 2001 25 31
48. D. Kim, F.P. Guengerich, Analysis of coumarin 7-hydroxylation activity of cytochrome P450 2A6 using random mutagenesis, in: 14th International Conference on Cytochrome P450 P.SI12, 2005, p. 164.
49. Z. Wu, F.P. Guengerich, Expansion of substrate specificity of cytochrome P450 2A6 by mutagenesis, in: 14th International Conference on Cytochrome P450 P.SI24, 2005, p. 168.
50. A. Parikh, P.D. Josephy, and F.P. Guengerich Selection and characterization of human cytochrome P450 1A2 mutants with altered catalytic properties Biochemistry 38 1999 5283 5289
51. C.H. Yun, M.P. Miller, and F.H. Guengerich Rate-determining steps in phenacetin oxidations by human cytochrome P450 1A2 and selected mutants Biochemistry 39 2000 11319 11329
52. D. Kim, and F.P. Guengerich Selection of human cytochrome P450 1A2 mutants with enhanced catalytic activity for heterocyclic amine N-hydroxylation Biochemistry 43 2004 981 988
53. P.C. Cirino, K.M. Mayer, and D. Umero Generating mutant libraries using error-prone PCR F.H. Arnold G. Georgiou Directed Evolution Library Creation 2003 Humana Press Totowa 3 10
54. A. Parikh, and F.P. Guengerich Random mutagenesis by whole-plasmid PCR amplification Biotechniques 24 1999 428 431
55. H. Zhao, L. Giver, Z. Shao, J.A. Affholter, and F.H. Arnold Molecular evolution by staggered extension process (StEP) in vitro recombination Nat. Biotechnol. 16 1998 258 261
56. Z. Shao, H. Zhao, L. Giver, and F.H. Arnold Random-priming in vitro recombination: an effective tool for directed evolution Nucleic Acids Res. 26 1998 681 683
57. T.S. Wong, K.L. Tee, B. Hauer, and U. Schwaneberg Sequence saturation mutagenesis (SeSaM): a novel method for directed evolution Nucleic Acids Res. 32 2004 e26
58. C.A. Voigt, S.L. Mayo, F.H. Arnold, and Z.G. Wang Computationally focusing the directed evolution of proteins J. Cell. Biochem. Suppl. 37 2001 58 63
59. R. Fox, A. Roy, S. Govindarajan, J. Minshull, C. Gustafsson, J.T. Jones, and R. Emig Optimizing the search algorithm for protein engineering by directed evolution Protein Engin. 16 2003 589 597
60. K. Hiraga, and F.H. Arnold General method for sequence-independent site-directed chimeragenesis J. Mol. Biol. 330 2003 287 296
61. L. Giver, and F.H. Arnold Combinatorial protein design by in vitro recombination Curr. Opin. Chem. Biol. 2 1998 335 338
62. A.V. Tobias Preparing libraries in E. coli. F.H. Arnold G. Georgiou Directed Evolution Library Creation 2003 Humana Press Totowa, NJ 11 16
63. O. Salzar, and L. Sun Evaluation of a screen and analysis of mutant libraries F.H. Arnold G. Georgiou Directed Evolution Library Creation 2003 Humana Press Totowa, NJ 85 89
64. E.M. Gillam, A.M. Aguinaldo, L.M. Notley, D. Kim, R.G. Mundkowski, A.A. Volkov, F.H. Arnold, P. Soucek, J.J. DeVoss, and F.P. Guengerich Formation of indigo by recombinant mammalian cytochrome P450 Biochem. Biophys. Res. Commun. 265 1999 469 472
65. E.E. Scott, M. Spatzenegger, and J.R. Halpert A truncation of 2B subfamily cytochromes P450 yields increased expression levels, increased solubility, and decreased aggregation while retaining function Arch. Biochem. Biophys. 395 2001 57 68
66. J. Cosme, and E.F. Johnson Engineering microsomal cytochrome P450 2C5 to be a soluble, monomeric enzyme. Mutations that alter aggregation, phospholipid dependence of catalysis, and membrane binding J. Biol. Chem. 275 2000 2545 2553
67. 5 in modulating peroxide-supported CYP3A4 activity: evidence for a conformational transition and P450 heterogeneity Drug Metab. Dispos. 33 2005 1131 1136
68. J.J. Cali, D. Ma, M. Sobol, D. Liu, Using luminescence to screen for xenobiotic effects in cytochrome P450 enzyme activities, in: 14th International Conference on Cytochrome P450 P.S14, 2005, p. 7.
69. V.G.H. Eijsink, S. Gaseidnes, T.V. Borchert, and B. van den Burg Directed evolution of enzyme stability Biomol. Engin. 22 2005 21 30
70. J.P. Aucamp, A.M. Cosme, G.J. Lye, and P.A. Dalby High-throughput measurement of protein stability in microtiter plates Biotechnol. Bioeng. 89 2005 599 607
71. P. Cirino, and R. Georgescu Screening for thermostability F.H. Arnold G. Georgiou Directed Enzyme Evolution 2003 Humana Press Totowa 117 126
72. C. Roodveldt, A. Aharoni, and D.S. Tawfik Directed evolution of proteins for heterologous expression and stability Curr. Opin. Struct. Biol. 15 2005 50 56
73. C.R. Otey High throughput carbon monoxide binding assay for cytochromes P450 F.H. Arnold G. Georgiou Directed Enzyme Evolution 2003 Humana Press Totowa 137 140