Cytochrome P450 monooxygenases: An update on perspectives for synthetic application

Trends in Biotechnology

Volumn 30, Issue 1, 2012, Pages 26-36

  Urlacher, Vlada B ^a   Girhard, Marco ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL CATALYST; CYTOCHROME P450; MONOOXYGENASES; PROTEIN ENGINEERING; RECOMBINANT ENZYMES; SYNTHETIC APPLICATION; TECHNICAL APPLICATIONS; WHOLE-CELL BIOCATALYSIS;

BIOCATALYSTS; BIODEGRADATION; ENZYMES; GENETIC ENGINEERING; HYDROCARBONS;

BIOCHEMICAL ENGINEERING;

ARTEMISININ; BUSPIRONE; CHLORZOXAZONE; CYTOCHROME P450; CYTOCHROME P450 BM3; DRUG METABOLITE; ETHOXYRESORUFIN; MUTANT PROTEIN; PHENACETIN; PROPRANOLOL;

BIOCATALYSIS; BIOSYNTHESIS; BIOTECHNOLOGY; BIOTRANSFORMATION; COMPUTER MODEL; CRYSTAL STRUCTURE; DIRECTED EVOLUTION; DNA RECOMBINATION; DRUG OXIDATION; ENZYME ACTIVITY; ENZYME ENGINEERING; ENZYME SPECIFICITY; ENZYME STRUCTURE; ESCHERICHIA COLI; HYDROXYLATION; MOLECULAR MODEL; MUTAGENESIS; MUTATION; PEPTIDE LIBRARY; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW; SITE DIRECTED MUTAGENESIS; STEROIDOGENESIS; STREPTOMYCES; WILD TYPE;

ANIMALS; BIOCATALYSIS; BIOTECHNOLOGY; CYTOCHROME P-450 ENZYME SYSTEM; HUMANS; OXIDATION-REDUCTION; PROTEIN ENGINEERING; PROTEIN STABILITY; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY;

EID: 84355163053     PISSN: 01677799     EISSN: 18793096     Source Type: Journal    
DOI: 10.1016/j.tibtech.2011.06.012     Document Type: Review

References (89)

1. Klingenberg M. Pigments of rat liver microsomes. Arch. Biochem. Biophys. 1958, 75:376-386.
2. Van Bogaert I.N., et al. The role of cytochrome P450 monooxygenases in microbial fatty acid metabolism. FEBS J. 2011, 278:206-221.
3. Hannemann F., et al. Cytochrome P450 systems - biological variations of electron transport chains. Biochim. Biophys. Acta 2007, 1770:330-344.
4. Zerbe K., et al. An oxidative phenol coupling reaction catalyzed by oxyB, a cytochrome P450 from the vancomycin-producing microorganism. Angew. Chem. Int. Ed. 2004, 43:6709-6713.
5. Shyadehi A.Z., et al. The mechanism of the acyl-carbon bond cleavage reaction catalyzed by recombinant sterol 14 alpha-demethylase of Candida albicans (other names are: lanosterol 14 alpha-demethylase, P-45014DM, and CYP51). J. Biol. Chem. 1996, 271:12445-12450.
6. Isin E.M., Guengerich F.P. Complex reactions catalyzed by cytochrome P450 enzymes. Biochim. Biophys. Acta 2007, 1770:314-329.
7. Ortiz de Montellano P.R., Nelson S.D. Rearrangement reactions catalyzed by cytochrome P450s. Arch. Biochem. Biophys. 2011, 507:95-110.
8. Bernhardt R. Cytochromes P450 as versatile biocatalysts. J. Biotechnol. 2006, 124:128-145.
9. Urlacher V.B. Catalysis with cytochrome P450 monooxygenases. Green Catalysis: Biocatalysis 2009, Vol. 3:1-25. Wiley-VCH. 1st edn.
10. Urlacher V.B., Eiben S. Cytochrome P450 monooxygenases: perspectives for synthetic application. Trends Biotechnol. 2006, 24:324-330.
11. Arnold F.H. How proteins adapt: lessons from directed evolution. Cold Spring Harb. Symp. Quant. Biol. 2009, 74:41-46.
12. Gillam E.M. Engineering cytochrome P450 enzymes. Chem. Res. Toxicol. 2008, 21:220-231.
13. Grogan G. Cytochromes P450: exploiting diversity and enabling application as biocatalysts. Curr. Opin. Chem. Biol. 2011, 15:241-248.
14. Jung S.T., et al. Cytochrome P450: taming a wild type enzyme. Curr. Opin. Biotechnol. 2011, 22:809-817.
15. Kumar S. Engineering cytochrome P450 biocatalysts for biotechnology, medicine and bioremediation. Expert Opin. Drug Metab. Toxicol. 2010, 6:115-131.
16. O'Reilly E., et al. Cytochromes P450 as useful biocatalysts: addressing the limitations. Chem. Commun. (Camb.) 2011, 47:2490-2501.
17. Rabe K.S., et al. Engineering and assaying of cytochrome P450 biocatalysts. Anal. Bioanal. Chem. 2008, 392:1059-1073.
18. Gillam E.M. Extending the capabilities of nature's most versatile catalysts: directed evolution of mammalian xenobiotic-metabolizing P450s. Arch. Biochem. Biophys. 2007, 464:176-186.
19. Narhi L.O., Fulco A.J. Characterization of a catalytically self-sufficient 119,000-dalton cytochrome P450 monooxygenase induced by barbiturates in Bacillus megaterium. J. Biol. Chem. 1986, 261:7160-7169.
20. Warman A.J., et al. Flavocytochrome P450 BM3: an update on structure and mechanism of a biotechnologically important enzyme. Biochem. Soc. Trans. 2005, 33:747-753.
21. Fasan R., et al. Engineered alkane-hydroxylating cytochrome P450(BM3) exhibiting nativelike catalytic properties. Angew. Chem. Int. Ed. Engl. 2007, 46:8414-8418.
22. Otey C.R., et al. Preparation of human metabolites of propranolol using laboratory-evolved bacterial cytochromes P450. Biotechnol. Bioeng. 2006, 93:494-499.
23. Landwehr M., et al. Enantioselective alpha-hydroxylation of 2-arylacetic acid derivatives and buspirone catalyzed by engineered cytochrome P450 BM-3. J. Am. Chem. Soc. 2006, 128:6058-6059.
24. Otey C.R., et al. Structure-guided recombination creates an artificial family of cytochromes P450. PLoS Biol. 2006, 4:e112.
25. Landwehr M., et al. Diversification of catalytic function in a synthetic family of chimeric cytochrome P450s. Chem. Biol. 2007, 14:269-278.
26. Sawayama A.M., et al. A panel of cytochrome P450 BM3 variants to produce drug metabolites and diversify lead compounds. Chemistry 2009, 15:11723-11729.
27. Park S.H., et al. Engineering bacterial cytochrome P450 (P450) BM3 into a prototype with human P450 enzyme activity using indigo formation. Drug Metab. Dispos. 2010, 38:732-739.
28. van Vugt-Lussenburg B.M., et al. Identification of critical residues in novel drug metabolizing mutants of cytochrome P450 BM3 using random mutagenesis. J. Med. Chem. 2007, 50:455-461.
29. Damsten M.C., et al. Application of drug metabolising mutants of cytochrome P450 BM3 (CYP102A1) as biocatalysts for the generation of reactive metabolites. Chem. Biol. Interact. 2008, 171:96-107.
30. Seifert A., Pleiss J. Identification of selectivity-determining residues in cytochrome P450 monooxygenases: a systematic analysis of the substrate recognition site 5. Proteins 2009, 74:1028-1035.
31. Seifert A., et al. Rational design of a minimal and highly enriched CYP102A1 mutant library with improved regio-, stereo- and chemoselectivity. Chembiochem 2009, 10:853-861.
32. Weber E., et al. Screening of a minimal enriched P450 BM3 mutant library for hydroxylation of cyclic and acyclic alkanes. Chem. Commun. (Camb.) 2011, 47:944-946.
33. Dietrich J.A., et al. A novel semi-biosynthetic route for artemisinin production using engineered substrate-promiscuous P450(BM3). ACS Chem. Biol. 2009, 4:261-267.
34. Nelson D.R. Progress in tracing the evolutionary paths of cytochrome P450. Biochim. Biophys. Acta 2011, 1814:14-18.
35. Khatri Y., et al. The CYPome of Sorangium cellulosum So ce56 and identification of CYP109D1 as a new fatty acid hydroxylase. Chem. Biol. 2010, 17:1295-1305.
36. Goldstone J.V., et al. Identification and developmental expression of the full complement of cytochrome P450 genes in Zebrafish. BMC Genomics 2010, 11:643.
37. Kelly D.E., et al. The CYPome (cytochrome P450 complement) of Aspergillus nidulans. Fungal Genet. Biol. 2009, 46:53-61.
38. Bell S.G., et al. Cytochrome P450 enzymes from the metabolically diverse bacterium Rhodopseudomonas palustris. Biochem. Biophys. Res. Commun. 2006, 342:191-196.
39. Ewen K.M., et al. Genome mining in Sorangium cellulosum So ce56: identification and characterization of the homologous electron transfer proteins of a myxobacterial cytochrome P450. J. Biol. Chem. 2009, 284:28590-28598.
40. Girhard M., et al. Characterization of the versatile monooxygenase CYP109B1 from Bacillus subtilis. Appl. Microbiol. Biotechnol. 2010, 87:595-607.
41. Furuya T., Kino K. Genome mining approach for the discovery of novel cytochrome P450 biocatalysts. Appl. Microbiol. Biotechnol. 2010, 86:991-1002.
42. Guengerich F.P., et al. Characterizing proteins of unknown function: orphan cytochrome P450 enzymes as a paradigm. Mol. Interv. 2010, 10:153-163.
43. Lamb D.C., et al. Exploiting Streptomyces coelicolor A3(2) P450s as a model for application in drug discovery. Expert Opin. Drug. Metab. Toxicol. 2006, 2:27-40.
44. Gaisser S., et al. Parallel pathways for oxidation of 14-membered polyketide macrolactones in Saccharopolyspora erythraea. Mol. Microbiol. 2002, 44:771-781.
45. Machida K., et al. Organization of the biosynthetic gene cluster for the polyketide antitumor macrolide, pladienolide, in Streptomyces platensis Mer-11107. Biosci. Biotechnol. Biochem. 2008, 72:2946-2952.
46. Machida K., et al. One-pot fermentation of pladienolide D by Streptomyces platensis expressing a heterologous cytochrome P450 gene. J. Biosci. Bioeng. 2009, 107:596-598.
47. Shrestha P., et al. Cytochrome P450 (CYP105F2) from Streptomyces peucetius and its activity with oleandomycin. Appl. Microbiol. Biotechnol. 2008, 79:555-562.
48. Kudo F., et al. Cloning and characterization of the biosynthetic gene cluster of 16-membered macrolide antibiotic FD-891: involvement of a dual functional cytochrome P450 monooxygenase catalyzing epoxidation and hydroxylation. Chembiochem 2010, 11:1574-1582.
49. Xu L.H., et al. Regio- and stereospecificity of filipin hydroxylation sites revealed by crystal structures of cytochrome P450 105P1 and 105D6 from Streptomyces avermitilis. J. Biol. Chem. 2010, 285:16844-16853.
50. Zhao B., et al. Biosynthesis of the sesquiterpene antibiotic albaflavenone in Streptomyces coelicolor A3(2). J. Biol. Chem. 2008, 283:8183-8189.
51. Pandey B.P., et al. Regioselective hydroxylation of daidzein using P450 (CYP105D7) from Streptomyces avermitilis MA4680. Biotechnol. Bioeng. 2010, 105:697-704.
52. Makino M., et al. Crystal structures and catalytic mechanism of cytochrome P450 StaP that produces the indolocarbazole skeleton. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:11591-11596.
53. Sugimoto H., et al. Crystal structure of CYP105A1 (P450SU-1) in complex with 1alpha, 25-dihydroxyvitamin D3. Biochemistry 2008, 47:4017-4027.
54. Xu L.H., et al. Crystal structures of cytochrome P450 105P1 from Streptomyces avermitilis: conformational flexibility and histidine ligation state. J. Bacteriol. 2009, 191:1211-1219.
55. Kells P.M., et al. Structure of cytochrome P450 PimD suggests epoxidation of the polyene macrolide pimaricin occurs via a hydroperoxoferric intermediate. Chem. Biol. 2010, 17:841-851.
56. Chefson A., Auclair K. Progress towards the easier use of P450 enzymes. Mol. Biosyst. 2006, 2:462-469.
57. van Beilen J.B., et al. Practical issues in the application of oxygenases. Trends Biotechnol. 2003, 21:170-177.
58. Schewe H., et al. Improvement of P450(BM-3) whole-cell biocatalysis by integrating heterologous cofactor regeneration combining glucose facilitator and dehydrogenase in E. coli. Appl. Microbiol. Biotechnol. 2008, 78:55-65.
59. Weisser P., et al. Functional expression of the glucose transporter of Zymomonas mobilis leads to restoration of glucose and fructose uptake in Escherichia coli mutants and provides evidence for its facilitator action. J. Bacteriol. 1995, 177:3351-3354.
60. Schewe H., et al. P450(BM-3)-catalyzed whole-cell biotransformation of alpha-pinene with recombinant Escherichia coli in an aqueous-organic two-phase system. Appl. Microbiol. Biotechnol. 2009, 83:849-857.
61. Kim D., Ortiz de Montellano P.R. Tricistronic overexpression of cytochrome P450(cam), putidaredoxin, and putidaredoxin reductase provides a useful cell-based catalytic system. Biotechnol. Lett. 2009, 31:1427-1431.
62. Girhard M., et al. Regioselective biooxidation of (+)-valencene by recombinant E. coli expressing CYP109B1 from Bacillus subtilis in a two-liquid-phase system. Microb. Cell Fact. 2009, 8:36.
63. Zhang J.D., et al. Synthesis of optically pure S-sulfoxide by Escherichia coli transformant cells coexpressing the P450 monooxygenase and glucose dehydrogenase genes. J. Ind. Microbiol. Biotechnol. 2011, 38:633-641.
64. Fasan R., et al. Improved product-per-glucose yields in P450-dependent propane biotransformations using engineered Escherichia coli. Biotechnol. Bioeng. 2011, 108:500-510.
65. Purnapatre K., et al. Cytochrome P450s in the development of target-based anticancer drugs. Cancer Lett. 2008, 259:1-15.
66. Shukla A., et al. Membrane integration of recombinant human P450 forms. Xenobiotica 2009, 39:495-507.
67. Tang Z., et al. Human cytochrome P450 4F11: heterologous expression in bacteria, purification, and characterization of catalytic function. Arch. Biochem. Biophys. 2010, 494:86-93.
68. Rupasinghe S.G., et al. High-yield expression and purification of isotopically labeled cytochrome P450 monooxygenases for solid-state NMR spectroscopy. Biochim. Biophys. Acta 2007, 1768:3061-3070.
69. Yun C.H., et al. Functional expression of human cytochrome P450 enzymes in Escherichia coli. Curr. Drug Metab. 2006, 7:411-429.
70. Pritchard M.P., et al. Establishment of functional human cytochrome P450 monooxygenase systems in Escherichia coli. Methods Mol. Biol. 2006, 320:19-29.
71. Munro A.W., et al. Cytochrome P450-redox partner fusion enzymes. Biochim. Biophys. Acta 2007, 1770:345-359.
72. Hanlon S.P., et al. Recombinant yeast and bacteria that express human P450s: bioreactors for drug discovery, -development and -biotechnology. Modern Biooxidation 2007, 233-252. Wiley-VCH. R.D. Schmid, V.B. Urlacher (Eds.).
73. Uno T., et al. Bioconversion of small molecules by cytochrome P450 species expressed in Escherichia coli. Biotechnol. Appl. Biochem. 2008, 50:165-171.
74. Hakki T., et al. Coexpression of redox partners increases the hydrocortisone (cortisol) production efficiency in CYP11B1 expressing fission yeast Schizosaccharomyces pombe. J. Biotechnol. 2008, 133:351-359.
75. Zehentgruber D., et al. Challenges of steroid biotransformation with human cytochrome P450 monooxygenase CYP21 using resting cells of recombinant Schizosaccharomyces pombe. J. Biotechnol. 2010, 146:179-185.
76. Arisawa A., Agematu H. A modular approach to biotransformation using microbial cytochrome P450 monooxygenases. Modern Biooxidation 2007, 177-192. Wiley-VCH. R.D. Schmid, V.B. Urlacher (Eds.).
77. Agematu H., et al. Hydroxylation of testosterone by bacterial cytochromes P450 using the Escherichia coli expression system. Biosci. Biotechnol. Biochem. 2006, 70:307-311.
78. Hannemann F., et al. Design of an Escherichia coli system for whole cell mediated steroid synthesis and molecular evolution of steroid hydroxylases. J. Biotechnol. 2006, 124:172-181.
79. Zehentgruber D., et al. Towards preparative scale steroid hydroxylation with cytochrome P450 monooxygenase CYP106A2. Chembiochem 2010, 11:713-721.
80. Nelson D.R., et al. Comparative genomics of rice and Arabidopsis. Analysis of 727 cytochrome P450 genes and pseudogenes from a monocot and a dicot. Plant Physiol. 2004, 135:756-772.
81. Nelson D.R. The cytochrome P450 homepage. Hum. Genomics 2009, 4:59-65.
82. Sirim D., et al. The cytochrome P450 engineering database: integration of biochemical properties. BMC Biochem. 2009, 10:27.
83. Park J., et al. Fungal cytochrome P450 database. BMC Genomics 2008, 9:402.
84. Preissner S., et al. SuperCYP: a comprehensive database on Cytochrome P450 enzymes including a tool for analysis of CYP-drug interactions. Nucleic Acids Res. 2010, 38:237-243.
85. Nelson D.R., et al. Comparison of cytochrome P450 (CYP) genes from the mouse and human genomes, including nomenclature recommendations for genes, pseudogenes and alternative-splice variants. Pharmacogenetics 2004, 14:1-18.
86. Lamb D.C., et al. Cytochrome P450 complement (CYPome) of the avermectin-producer Streptomyces avermitilis and comparison to that of Streptomyces coelicolor A3(2). Biochem. Biophys. Res. Commun. 2003, 307:610-619.
87. Lamb D.C., et al. The cytochrome P450 complement (CYPome) of Streptomyces coelicolor A3(2). J. Biol. Chem. 2002, 277:24000-24005.
88. Lawson R.J., et al. Thermodynamic and biophysical characterization of cytochrome P450 BioI from Bacillus subtilis. Biochemistry 2004, 43:12410-12426.
89. Girhard M., et al. Cytochrome P450 monooxygenase from Clostridium acetobutylicum: a new alpha-fatty acid hydroxylase. Biochem. Biophys. Res. Commun. 2007, 362:114-119.