Directed evolution reveals requisite sequence elements in the functional expression of P450 2F1 in Escherichia coli

Chemical Research in Toxicology

Volumn 25, Issue 9, 2012, Pages 1964-1974

  Behrendorff, James B Y H ^a   Moore, Chad D ^b   Kim, Keon Hee ^c   Kim, Dae Hwan ^c   Smith, Christopher A ^a   Johnston, Wayne A ^a   Yun, Chul Ho ^c   Yost, Garold S ^b   Gillam, Elizabeth M J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF UTAH   (United States)

^c Chonnam National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME P450; GLUTATHIONE; HEMOPROTEIN; NUCLEOTIDE;

AEROBIC CELL CULTURE; AMINO ACID SEQUENCE; ARTICLE; CATALYSIS; CONTROLLED STUDY; DEHYDROGENATION; DIRECTED MOLECULAR EVOLUTION; DNA SCREENING; DNA SHUFFLING; ESCHERICHIA COLI; HUMAN; INCUBATION TEMPERATURE; MUTANT; NONHUMAN; PROTEIN EXPRESSION; STRUCTURE ACTIVITY RELATION;

CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYTOCHROME P-450 ENZYME SYSTEM; DIRECTED MOLECULAR EVOLUTION; ESCHERICHIA COLI; GLUTATHIONE; HUMANS; INDOLES; MASS SPECTROMETRY; MODELS, MOLECULAR; RECOMBINANT PROTEINS; SKATOLE; THERMODYNAMICS;

CAPRA; ESCHERICHIA COLI;

EID: 84866379763     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx300281g     Document Type: Article

References (47)

1. Bieche, I., Narjoz, C., Asselah, T., Vacher, S., Marcellin, P., Lidereau, R., Beaune, P., and de Waziers, I. (2007) Reverse transcriptase-PCR quantification of mRNA levels from cytochrome (CYP)1, CYP2 and CYP3 families in 22 different human tissues Pharmacogenet. Genomics 17, 731-742 (Pubitemid 47263068)
2. Nhamburo, P. T., Kimura, S., McBride, O. W., Kozak, C. A., Gelboin, H. V., and Gonzalez, F. J. (1990) The human CYP2F gene subfamily: Identification of a cDNA encoding a new cytochrome P450, cDNA-directed expression, and chromosome mapping Biochemistry 29, 5491-5499 (Pubitemid 20202273)
3. Zhang, X., Zhang, Q. Y., Liu, D., Su, T., Weng, Y., Ling, G., Chen, Y., Gu, J., Schilling, B., and Ding, X. (2005) Expression of cytochrome P450 and other biotransformation genes in fetal and adult human nasal mucosa Drug Metab. Dispos. 33, 1423-1428
4. Lanza, D. L., Code, E., Crespi, C. L., Gonzalez, F. J., and Yost, G. S. (1999) Specific dehydrogenation of 3-methylindole and epoxidation of naphthalene by recombinant human CYP2F1 expressed in lymphoblastoid cells Drug Metab. Dispos. 27, 798-803 (Pubitemid 29297777)
5. Nakajima, T., Elovaara, E., Gonzalez, F. J., Gelboin, H. V., Raunio, H., Pelkonen, O., Vainio, H., and Aoyama, T. (1994) Styrene metabolism by cDNA-expressed human hepatic and pulmonary cytochromes P450 Chem. Res. Toxicol. 7, 891-896 (Pubitemid 24370251)
6. Thornton-Manning, J. R., Ruangyuttikarn, W., Gonzalez, F. J., and Yost, G. S. (1991) Metabolic activation of the pneumotoxin, 3-methylindole, by vaccinia-expressed cytochrome P450s Biochem. Biophys. Res. Commun. 181, 100-107
7. Lanza, D. L. and Yost, G. S. (2001) Selective dehydrogenation/oxygenation of 3-methylindole by cytochrome P450 enzymes Drug Metab. Dispos. 29, 950-953 (Pubitemid 32605908)
8. Kartha, J. S. and Yost, G. S. (2008) Mechanism-based inactivation of lung-selective cytochrome P450 CYP2F enzymes Drug Metab. Dispos. 36, 155-162
9. Ruangyuttikarn, W., Skiles, G. L., and Yost, G. S. (1992) Identification of a cysteinyl adduct of oxidized 3-methylindole from goat lung and human liver microsomal proteins Chem. Res. Toxicol. 5, 713-719
10. Regal, K. A., Laws, G. M., Yuan, C., Yost, G. S., and Skiles, G. L. (2001) Detection and characterization of DNA adducts of 3-methylindole Chem. Res. Toxicol. 14, 1014-1024 (Pubitemid 32800157)
11. Yan, Z., Easterwood, L. M., Maher, N., Torres, R., Huebert, N., and Yost, G. S. (2007) Metabolism and bioactivation of 3-methylindole by human liver microsomes Chem. Res. Toxicol. 20, 140-148 (Pubitemid 46220164)
12. D'Agostino, J., Zhuo, X., Shadid, M., Morgan, D. G., Zhang, X., Humphreys, W. G., Shu, Y. Z., Yost, G. S., and Ding, X. (2009) The pneumotoxin 3-methylindole is a substrate and a mechanism-based inactivator of CYP2A13, a human cytochrome P450 enzyme preferentially expressed in the respiratory tract Drug Metab. Dispos. 37, 2018-2027
13. Weems, J. M., Cutler, N. S., Moore, C., Nichols, W. K., Martin, D., Makin, E., Lamb, J. G., and Yost, G. S. (2009) 3-Methylindole is mutagenic and a possible pulmonary carcinogen Toxicol. Sci. 112, 59-67
14. Thornton-Manning, J., Appleton, M. L., Gonzalez, F. J., and Yost, G. S. (1996) Metabolism of 3-methylindole by vaccinia-expressed P450 enzymes: correlation of 3-methyleneindolenine formation and protein-binding J. Pharmacol. Exp. Ther. 276, 21-29 (Pubitemid 26150948)
15. Weems, J. M., Lamb, J. G., D'Agostino, J., Ding, X., and Yost, G. S. (2010) Potent mutagenicity of 3-methylindole requires pulmonary cytochrome P450-mediated bioactivation: A comparison to the prototype cigarette smoke mutagens B(a)P and NNK Chem. Res. Toxicol. 23, 1682-1690
16. Barnes, H. J., Arlotto, M. P., and Waterman, M. R. (1991) Expression and enzymatic activity of recombinant cytochrome P450 17 alpha-hydroxylase in Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 88, 5597-5601 (Pubitemid 21914792)
17. Wang, H., Lanza, D. L., and Yost, G. S. (1998) Cloning and expression of CYP2F3, a cytochrome P450 that bioactivates the selective pneumotoxins 3-methylindole and naphthalene Arch. Biochem. Biophys. 349, 329-340 (Pubitemid 28368678)
18. Crameri, A., Raillard, S. A., Bermudez, E., and Stemmer, W. P. (1998) DNA shuffling of a family of genes from diverse species accelerates directed evolution Nature 391, 288-291 (Pubitemid 28099016)
19. Skiles, G. L. and Yost, G. S. (1996) Mechanistic studies on the cytochrome P450-catalyzed dehydrogenation of 3-methylindole Chem. Res. Toxicol. 9, 291-297
20. Cuttle, L., Munns, A. J., Hogg, N. A., Scott, J. R., Hooper, W. D., Dickinson, R. G., and Gillam, E. M. J. (2000) Phenytoin metabolism by human cytochrome P450: involvement of P450 3A and 2C forms in secondary metabolism and drug-protein adduct formation Drug Metab. Dispos. 28, 945-950 (Pubitemid 30612614)
21. Parikh, A., Gillam, E. M. J., and Guengerich, F. P. (1997) Drug metabolism by Escherichia coli expressing human cytochromes P450 Nat. Biotechnol. 15, 784-788 (Pubitemid 27329483)
22. Nishihara, K., Kanemori, M., Kitagawa, M., Yanagi, H., and Yura, T. (1998) Chaperone coexpression plasmids: differential and synergistic roles of DnaK-DnaJ-GrpE and GroEL-GroES in assisting folding of an allergen of Japanese cedar pollen, Cryj2, in Escherichia coli Appl. Environ. Microbiol. 64, 1694-1699 (Pubitemid 28234771)
23. Prodromou, C. and Pearl, L. H. (1992) Recursive PCR: A novel technique for total gene synthesis Protein Eng. 5, 827-829 (Pubitemid 23036555)
24. Kikuchi, M., Ohnishi, K., and Harayama, S. (1999) Novel family shuffling methods for the in vitro evolution of enzymes Gene 236, 159-167 (Pubitemid 29350717)
25. Huang, W., Johnston, W. A., Hayes, M. A., De Voss, J. J., and Gillam, E. M. J. (2007) A shuffled CYP2C library with a high degree of structural integrity and functional versatility Arch. Biochem. Biophys. 467, 193-205 (Pubitemid 350050891)
26. Behrendorff, J. B. Y. H., Johnston, W. A., and Gillam, E. M. J. DNA shuffling of cytochrome P450 enzymes. Methods Mol. Biol. 2012, in press.
27. Kadokami, Y. and Lewis, R. V. (1995) Reverse electrophoresis to concentrate DNA fractions Anal. Biochem. 226, 193-195
28. Abecassis, V., Pompon, D., and Truan, G. (2000) High efficiency family shuffling based on multi-step PCR and in vivo DNA recombination in yeast: Statistical and functional analysis of a combinatorial library between human cytochrome P450 1A1 and 1A2 Nucleic Acids Res. 28, E88
29. Johnston, W. A., Huang, W., De Voss, J. J., Hayes, M. A., and Gillam, E. M. J. (2007) A shuffled CYP1A library shows both structural integrity and functional diversity Drug Metab. Dispos. 35, 2177-2185 (Pubitemid 350146203)
30. Johnston, W. A., Huang, W., De Voss, J. J., Hayes, M. A., and Gillam, E. M. J. (2008) Quantitative whole-cell cytochrome P450 measurement suitable for high-throughput application J. Biomol. Screening 13, 135-141 (Pubitemid 351248692)
31. Gillam, E. M. J., Aguinaldo, A. M., Notley, L. M., Kim, D., Mundkowski, R. G., Volkov, A. A., Arnold, F. H., Soucek, P., DeVoss, J. J., and Guengerich, F. P. (1999) Formation of indigo by recombinant mammalian cytochrome P450 Biochem. Biophys. Res. Commun. 265, 469-472
32. Gillam, E. M. J., Baba, T., Kim, B.-R., Ohmori, S., and Guengerich, F. P. (1993) Expression of modified human cytochrome P450 3A4 in Escherichia coli and purification and reconstitution of the enzyme Arch. Biochem. Biophys. 305, 123-131 (Pubitemid 23242002)
33. Laemmli, U. K., Beguin, F., and Gujer-Kellenberger, G. (1970) A factor preventing the major head protein of bacteriophage T4 from random aggregation J. Mol. Biol. 47, 69-85
34. Wray, W., Boulikas, T., Wray, V. P., and Hancock, R. (1981) Silver staining of proteins in polyacrylamide gels Anal. Biochem. 118, 197-203
35. Kim, D. E., Chivian, D., and Baker, D. (2004) Protein structure prediction and analysis using the Robetta server Nucleic Acids Res. 32, W526-531
36. Yin, S., Ding, F., and Dokholyan, N. V. (2007) Eris: An automated estimator of protein stability Nat. Methods 4, 466-467 (Pubitemid 46852064)
37. Looman, A. C., Bodlaender, J., Comstock, L. J., Eaton, D., Jhurani, P., de Boer, H. A., and van Knippenberg, P. H. (1987) Influence of the codon following the AUG initiation codon on the expression of a modified lacZ gene in Escherichia coli EMBO J. 6, 2489-2492
38. Yun, C. H., Yim, S. K., Kim, D. H., and Ahn, T. (2006) Functional expression of human cytochrome P450 enzymes in Escherichia coli Curr. Drug Metab. 7, 411-429
39. Wulff, B. B., Thomas, C. M., Smoker, M., Grant, M., and Jones, J. D. (2001) Domain swapping and gene shuffling identify sequences required for induction of an Avr-dependent hypersensitive response by the tomato Cf-4 and Cf-9 proteins Plant Cell 13, 255-272 (Pubitemid 32207682)
40. Williams, P. A., Cosme, J., Sridhar, V., Johnson, E. F., and McRee, D. E. (2000) Mammalian microsomal cytochrome P450 monooxygenase: Structural adaptations for membrane binding and functional diversity Mol. Cell 5, 121-131 (Pubitemid 30105441)
41. Wang, A., Savas, U., Stout, C. D., and Johnson, E. F. (2011) Structural characterization of the complex between alpha-naphthoflavone and human cytochrome P450 1B1 J. Biol. Chem. 286, 5736-5743
42. Sansen, S., Hsu, M. H., Stout, C. D., and Johnson, E. F. (2007) Structural insight into the altered substrate specificity of human cytochrome P450 2A6 mutants Arch. Biochem. Biophys. 464, 197-206 (Pubitemid 47210930)
43. Sansen, S., Yano, J. K., Reynald, R. L., Schoch, G. A., Griffin, K. J., Stout, C. D., and Johnson, E. F. (2007) Adaptations for the oxidation of polycyclic aromatic hydrocarbons exhibited by the structure of human P450 1A2 J. Biol. Chem. 282, 14348-14355 (Pubitemid 47100434)
44. Kim, D. H., Kim, K. H., Isin, E. M., Guengerich, F. P., Chae, H. Z., Ahn, T., and Yun, C. H. (2008) Heterologous expression and characterization of wild-type human cytochrome P450 1A2 without conventional N-terminal modification in Escherichia coli Protein Expression Purif. 57, 188-200 (Pubitemid 350296980)
45. Shumyantseva, V. V., Bulko, T. V., Alexandrova, S. A., Sokolov, N. N., Schmid, R. D., Bachmann, T., and Archakov, A. I. (1999) N-terminal truncated cytochrome P450 2B4: Catalytic activities and reduction with alternative electron sources Biochem. Biophys. Res. Commun. 263, 678-680 (Pubitemid 29490685)
46. Kartha, J. S., Skordos, K. W., Sun, H., Hall, C., Easterwood, L. M., Reilly, C. A., Johnson, E. F., and Yost, G. S. (2008) Single mutations change CYP2F3 from a dehydrogenase of 3-methylindole to an oxygenase Biochemistry 47, 9756-9770
47. Gotoh, O. (1992) Substrate recognition sites in cytochrome P450 family 2 (CYP2) proteins inferred from comparative analyses of amino acid and coding nucleotide sequences J. Biol. Chem. 267, 83-90