Versatile biocatalysis of fungal cytochrome P450 monooxygenases

Microbial Cell Factories

Volumn 15, Issue 1, 2016, Pages

  Durairaj, Pradeepraj ^a   Hur, Jae Seoun ^a   Yun, Hyungdon ^b  

^a Sunchon National University   (South Korea)

^b Konkuk University   (South Korea)

Author keywords

Biocatalysis; Cytochrome P450; Cytochrome P450 reductase; Fungi; Monooxygenase reaction

Indexed keywords

CYTOCHROME P450; CYTOCHROME P450 MONOOXYGENASE; FUNGAL ENZYME; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE; FUNGAL PROTEIN;

ASPERGILLUS FUMIGATUS; ASPERGILLUS NIDULANS; ASPERGILLUS NIGER; ASPERGILLUS ORYZAE; BACTERIUM; BATRACHOCHYTRIUM DENDROBATIDIS; BIOCATALYSIS; CANDIDA ALBICANS; CANDIDA TROPICALIS; CURVULARIA LUNATA; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; FUNGAL GENOME; FUSARIUM GRAMINEARUM; FUSARIUM OXYSPORUM; FUSARIUM VERTICILLIOIDES; HETEROLOGOUS EXPRESSION; HOST PATHOGEN INTERACTION; MAGNAPORTHE ORYZAE; MICROBIAL DIVERSITY; MOLECULAR EVOLUTION; NEUROSPORA CRASSA; NONHUMAN; PENICILLIUM CHRYSOGENUM; PHANEROCHAETE; PHYCOMYCES BLAKESLEEANUS; POSTIA PLACENTA; PROTEIN EXPRESSION; REVIEW; RHIZOPUS ORYZAE; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; USTILAGO MAYDIS; YARROWIA LIPOLYTICA; CHEMISTRY; ENZYMOLOGY; FUNGUS; GENETICS; METABOLISM;

BIOCATALYSIS; CYTOCHROME P-450 ENZYME SYSTEM; FUNGAL PROTEINS; FUNGI;

EID: 84978910887     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/s12934-016-0523-6     Document Type: Review

References (109)

1. Bernhardt R, Urlacher VB. Cytochromes P450 as promising catalysts for biotechnological application: chances and limitations. Appl Microbiol Biotechnol. 2014;98:6185-203.
2. Urlacher VB, Girhard M. Cytochrome P450 monooxygenases: an update on perspectives for synthetic application. Trends Biotechnol. 2012;30:26-36.
3. Kumar S. Engineering cytochrome P450 biocatalysts for biotechnology, medicine and bioremediation. Expert Opin Drug Metabol Toxicol. 2010;6:115-31.
4. Coon MJ. Cytochrome P450: nature's most versatile biological catalyst. Annu Rev Pharmacol Toxicol. 2005;45:1-25.
5. Munro AW, Girvan HM, Mason AE, Dunford AJ, McLean KJ. What makes a P450 tick? Trends Biochem Sci. 2013;38:140-50.
6. Renault H, Bassard J-E, Hamberger B, Werck-Reichhart D. Cytochrome P450-mediated metabolic engineering: current progress and future challenges. Curr Opin Plant Biol. 2014;19:27-34.
7. Julsing MK, Cornelissen S, Bühler B, Schmid A. Heme-iron oxygenases: powerful industrial biocatalysts? Curr Opin Chem Biol. 2008;12:177-86.
8. Isin EM, Guengerich FP. Complex reactions catalyzed by cytochrome P450 enzymes. Biochimica et Biophysica Acta (BBA) Gen Subj. 2007;1770:314-29.
9. Urlacher VB, Eiben S. Cytochrome P450 monooxygenases: perspectives for synthetic application. Trends Biotechnol. 2006;24:324-30.
10. McIntosh JA, Farwell CC, Arnold FH. Expanding P450 catalytic reaction space through evolution and engineering. Curr Opin Chem Biol. 2014;19:126-34.
11. Grogan G. Cytochromes P450: exploiting diversity and enabling application as biocatalysts. Curr Opin Chem Biol. 2011;15:241-8.
12. Caswell JM, O'Neill M, Taylor SJ, Moody TS. Engineering and application of P450 monooxygenases in pharmaceutical and metabolite synthesis. Curr Opin Chem Biol. 2013;17:271-5.
13. Hannemann F, Bichet A, Ewen KM, Bernhardt R. Cytochrome P450 systems-biological variations of electron transport chains. Biochimica et Biophysica Acta (BBA) Gen Subj. 2007;1770:330-44.
14. Moktali V, Park J, Fedorova-Abrams ND, Park B, Choi J, Lee Y-H, Kang S. Systematic and searchable classification of cytochrome P450 proteins encoded by fungal and oomycete genomes. BMC Genom. 2012;13:525.
15. van Gorcom RF, van den Hondel CA, Punt PJ. Cytochrome P450 enzyme systems in fungi. Fungal Genet Biol. 1998;23:1-17.
16. Crešnar B, Petrič Š. Cytochrome P450 enzymes in the fungal kingdom. Biochimica et Biophysica Acta (BBA) Proteins Proteom. 2011;1814:29-35.
17. Blackwell M. The fungi: 1, 2, 3. 5.1 million species? Am J Bot. 2011;98:426-38.
18. Ichinose H. Molecular and functional diversity of fungal cytochrome P450s. Biol Pharm Bull. 2012;35:833-7.
19. Mohanta TK, Bae H. The diversity of fungal genome. Biol Proced Online. 2015;17:8.
20. Nelson. Progress in tracing the evolutionary paths of cytochrome P450. Biochimica et Biophysica Acta (BBA) Proteins Proteom. 2011;1814:14-8.
21. Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking R. A higher-level phylogenetic classification of the Fungi. Mycol Res. 2007;111:509-47.
22. Chen W, Lee M-K, Jefcoate C, Kim S-C, Chen F, Yu J-H. Fungal cytochrome p450 monooxygenases: their distribution, structure, functions, family expansion, and evolutionary origin. Genome Biol Evol. 2014;6:1620-34.
23. Nelson D, Werck-Reichhart D. A P450-centric view of plant evolution. Plant J. 2011;66:194-211.
24. Nelson DR. The cytochrome p450 homepage. Human Genom. 2009;4:59.
25. Deng J, Carbone I, Dean RA. The evolutionary history of cytochrome P450 genes in four filamentous Ascomycetes. BMC Evol Biol. 2007;7:30.
26. Kelly DE, Kraševec N, Mullins J, Nelson DR. The CYPome (cytochrome P450 complement) of Aspergillus nidulans. Fungal Genet Biol. 2009;46:S53-61.
27. Sezutsu H, Le Goff G, Feyereisen R. Origins of P450 diversity. Philos Trans R Soc Lond B Biol Sci. 2013;368:20120428.
28. Scazzocchio C. Fungal biology in the post-genomic era. Fungal Biol Biotechnol. 2014;1:1.
29. McLean K, Sabri M, Marshall K, Lawson R, Lewis D, Clift D, Balding P, Dunford A, Warman A, McVey J. Biodiversity of cytochrome P450 redox systems. Biochem Soc Trans. 2005;33:796-801.
30. Podust LM, Sherman DH. Diversity of P450 enzymes in the biosynthesis of natural products. Nat Prod Rep. 2012;29:1251-66.
31. Ichinose H, Wariishi H. Heterologous expression and mechanistic investigation of a fungal cytochrome P450 (CYP5150A2): involvement of alternative redox partners. Arch Biochem Biophys. 2012;518:8-15.
32. Shoun H, Takaya N. Cytochromes P450nor and P450foxy of the fungus Fusarium oxysporum. In: International Congress Series. Amsterdam: Elsevier; 2002. p. 89-97.
33. Price CL, Warrilow AG, Parker JE, Mullins JG, Nes WD, Kelly DE, Kelly SL. Novel substrate specificity and temperature-sensitive activity of Mycosphaerella graminicola CYP51 supported by the native NADPH cytochrome P450 reductase. Appl Environ Microbiol. 2015;81:3379-86.
34. Hargrove TY, Wawrzak Z, Liu J, Waterman MR, Nes WD, Lepesheva GI. Structural complex of sterol 14α-demethylase (CYP51) with 14α-methylenecyclopropyl-7-24, 25-dihydrolanosterol. J Lipid Res. 2012;53:311-20.
35. Hoobler EK, Rai G, Warrilow AG, Perry SC, Smyrniotis CJ, Jadhav A, Simeonov A, Parker JE, Kelly DE, Maloney DJ. Discovery of a novel dual fungal CYP51/human 5-lipoxygenase inhibitor: implications for anti-fungal therapy. PloS one. 2013;8:e65928.
36. Jawallapersand P, Mashele SS, Kovačič L, Stojan J, Komel R, Pakala SB, Kraševec N, Syed K. Cytochrome P450 monooxygenase CYP53 family in fungi: comparative structural and evolutionary analysis and its role as a common alternative anti-fungal drug target. PloS one. 2014;9(9):e107209.
37. Podobnik B, Stojan J, Lah L, Krasevec N, Seliskar M, Rizner TL, Rozman D, Komel R. CYP53A15 of Cochliobolus lunatus, a target for natural antifungal compounds. J Med Chem. 2008;51:3480-6.
38. Durairaj P, Jung E, Park HH, Kim B-G, Yun H. Comparative functional characterization of a novel benzoate hydroxylase cytochrome P450 of Fusarium oxysporum. Enzyme Microbial Technol. 2015;70:58-65.
39. Matsuzaki F, Wariishi H. Molecular characterization of cytochrome P450 catalyzing hydroxylation of benzoates from the white-rot fungus Phanerochaete chrysosporium. Biochem Biophys Res Commun. 2005;334:1184-90.
40. Ide M, Ichinose H, Wariishi H. Molecular identification and functional characterization of cytochrome P450 monooxygenases from the brown-rot basidiomycete Postia placenta. Arch Microbiol. 2012;194:243-53.
41. Durairaj P, Malla S, Nadarajan SP, Lee P-G, Jung E, Park HH, Kim B-G, Yun H. Fungal cytochrome P450 monooxygenases of Fusarium oxysporum for the synthesis of ω-hydroxy fatty acids in engineered Saccharomyces cerevisiae. Microb Cell Fact. 2015;14:45.
42. Johnston JB, Ouellet H, Podust LM, de Montellano PRO. Structural control of cytochrome P450-catalyzed ω-hydroxylation. Arch Biochem Biophys. 2011;507:86-94.
43. Lu W, Ness JE, Xie W, Zhang X, Minshull J, Gross RA. Biosynthesis of monomers for plastics from renewable oils. J Am Chem Soc. 2010;132:15451-5.
44. Huang F-C, Peter A, Schwab W. Expression and characterization of CYP52 genes involved in the biosynthesis of sophorolipid and alkane metabolism from Starmerella bombicola. Appl Environ Microbiol. 2014;80:766-76.
45. Lin L, Fang W, Liao X, Wang F, Wei D, Leger RJS. The MrCYP52 cytochrome P450 monoxygenase gene of Metarhizium robertsii is important for utilizing insect epicuticular hydrocarbons. PloS one. 2011;6:e28984.
46. Zhang S, Widemann E, Bernard G, Lesot A, Pinot F, Pedrini N, Keyhani NO. CYP52X1, representing new cytochrome P450 subfamily, displays fatty acid hydroxylase activity and contributes to virulence and growth on insect cuticular substrates in entomopathogenic fungus Beauveria bassiana. J Biol Chem. 2012;287:13477-86.
47. Novak M, Lah L, Šala M, Stojan J, Bohlmann J, Komel R. Oleic acid metabolism via a conserved cytochrome P450 System-mediated ω-hydroxylation in the bark beetle-associated fungus Grosmannia clavigera. PLoS One. 2015;10:e0120119.
48. Kasai N, Ikushiro S-i, Hirosue S, Arisawa A, Ichinose H, Wariishi H, Ohta M, Sakaki T. Enzymatic properties of cytochrome P450 catalyzing 3'-hydroxylation of naringenin from the white-rot fungus Phanerochaete chrysosporium. Biochem Biophys Res Commun. 2009;387:103-8.
49. Kasai N, Ikushiro S, Hirosue S, Arisawa A, Ichinose H, Uchida Y, Wariishi H, Ohta M, Sakaki T. Atypical kinetics of cytochromes P450 catalysing 3'-hydroxylation of flavone from the white-rot fungus Phanerochaete chrysosporium. J Biochem. 2010;147:117-25.
50. Nazir KNH, Ichinose H, Wariishi H. Construction and application of a functional library of cytochrome P450 monooxygenases from the filamentous fungus Aspergillus oryzae. Appl Environ Microbiol. 2011;77:3147-50.
51. Syed K, Doddapaneni H, Subramanian V, Lam YW, Yadav JS. Genome-to-function characterization of novel fungal P450 monooxygenases oxidizing polycyclic aromatic hydrocarbons (PAHs). Biochem Biophys Res Commun. 2010;399:492-7.
52. Syed K, Porollo A, Lam YW, Grimmett PE, Yadav JS. CYP63A2, a catalytically versatile fungal P450 monooxygenase capable of oxidizing higher-molecular-weight polycyclic aromatic hydrocarbons, alkylphenols, and alkanes. Appl Environ Microbiol. 2013;79:2692-702.
53. Syed K, Porollo A, Lam YW, Yadav JS. A fungal P450 (CYP5136A3) capable of oxidizing polycyclic aromatic hydrocarbons and endocrine disrupting alkylphenols: role of Trp129 and Leu324. PLoS One. 2011;6:e28286.
54. Donova MV, Egorova OV. Microbial steroid transformations: current state and prospects. Appl Microbiol Biotechnol. 2012;94:1423-47.
55. Petrič Š, Hakki T, Bernhardt R, Žigon D, Črešnar B. Discovery of a steroid 11α-hydroxylase from Rhizopus oryzae and its biotechnological application. J Biotechnol. 2010;150:428-37.
56. Mazzaferro LS, Hüttel W, Fries A, Müller M. Cytochrome P450-catalyzed regio-and stereoselective phenol coupling of fungal natural products. J Am Chem Soc. 2015;137:12289-95.
57. Tudzynski B, Rojas MaC, Gaskin P, Hedden P. The gibberellin 20-oxidase of Gibberella fujikuroi is a multifunctional monooxygenase. J Biol Chem. 2002;277:21246-53.
58. Proctor RH, Plattner RD, Desjardins AE, Busman M, Butchko RA. Fumonisin production in the maize pathogen Fusarium verticillioides: genetic basis of naturally occurring chemical variation. J Agric Food Chem. 2006;54:2424-30.
59. Tokai T, Koshino H, Takahashi-Ando N, Sato M, Fujimura M, Kimura M. Fusarium Tri4 encodes a key multifunctional cytochrome P450 monooxygenase for four consecutive oxygenation steps in trichothecene biosynthesis. Biochem Biophys Res Commun. 2007;353:412-7.
60. Matsuda Y, Iwabuchi T, Wakimoto T, Awakawa T, Abe I. Uncovering the unusual D-Ring construction in terretonin biosynthesis by collaboration of a multifunctional cytochrome P450 and a unique isomerase. J Am Chem Soc. 2015;137:3393-401.
61. Barriuso J, Nguyen DT, Li JW-H, Roberts JN, MacNevin DT, Chaytor JL, Marcus SL, Vederas JC, Ro D-K. Double oxidation of the cyclic nonaketide dihydromonacolin L to monacolin J by a single cytochrome P450 monooxygenase, LovA. J Am Chem Soc. 2011;133:8078-81.
62. Cochrane RV, Vederas JC. Highly selective but multifunctional oxygenases in secondary metabolism. Acc Chem Res. 2014;47:3148-61.
63. Lin H-C, Tsunematsu Y, Dhingra S, Xu W, Fukutomi M, Chooi Y-H, Cane DE, Calvo AM, Watanabe K, Tang Y. Generation of complexity in fungal terpene biosynthesis: discovery of a multifunctional cytochrome P450 in the fumagillin pathway. J Am Chem Soc. 2014;136:4426-36.
64. Hofrichter M, Kellner H, Pecyna MJ, Ullrich R. Fungal unspecific peroxygenases: heme-thiolate proteins that combine peroxidase and cytochrome P450 properties. In: Monooxygenase, peroxidase and peroxygenase properties and mechanisms of cytochrome P450. Berlin: Springer; 2015. p. 341-68.
65. Hoffmann I, Jernerén F, Oliw EH. Epoxy alcohol synthase of the rice blast fungus represents a novel subfamily of dioxygenase-cytochrome P450 fusion enzymes. J Lipid Res. 2014;55:2113-23.
66. Illanes A, Cauerhff A, Wilson L, Castro GR. Recent trends in biocatalysis engineering. Bioresour Technol. 2012;115:48-57.
67. Lah L, Podobnik B, Novak M, Korošec B, Berne S, Vogelsang M, Kraševec N, Zupanec N, Stojan J, Bohlmann J. The versatility of the fungal cytochrome P450 monooxygenase system is instrumental in xenobiotic detoxification. Mol Microbiol. 2011;81:1374-89.
68. Ning D, Wang H. Involvement of cytochrome P450 in pentachlorophenol transformation in a white rot fungus Phanerochaete chrysosporium. PloS one. 2012;7(9):e45887.
69. Matsuzaki F, Wariishi H. Functional diversity of cytochrome P450s of the white-rot fungus Phanerochaete chrysosporium. Biochem Biophys Res Commun. 2004;324:387-93.
70. Nazir KNH, Ichinose H, Wariishi H. Molecular characterization and isolation of cytochrome P450 genes from the filamentous fungus Aspergillus oryzae. Arch Microbiol. 2010;192:395-408.
71. Waegeman H, Soetaert W. Increasing recombinant protein production in Escherichia coli through metabolic and genetic engineering. J Ind Microbiol Biotechnol. 2011;38:1891-910.
72. Chang MC, Keasling JD. Production of isoprenoid pharmaceuticals by engineered microbes. Nat Chem Biol. 2006;2:674-81.
73. Zelasko S, Palaria A, Das A. Optimizations to achieve high-level expression of cytochrome P450 proteins using Escherichia coli expression systems. Protein Expr Purif. 2013;92:77-87.
74. Kim D, Cryle MJ, De Voss JJ, de Montellano PRO. Functional expression and characterization of cytochrome P450 52A21 from Candida albicans. Arch Biochem Biophys. 2007;464:213-20.
75. Ichinose H, Wariishi H. High-level heterologous expression of fungal cytochrome P450s in Escherichia coli. Biochem Biophys Res Commun. 2013;438:289-94.
76. Ichinose H, Hatakeyama M, Yamauchi Y. Sequence modifications and heterologous expression of eukaryotic cytochromes P450 in Escherichia coli. J Biosci Bioeng. 2015;120(3):268-74.
77. Braun A, Geier M, Bühler B, Schmid A, Mauersberger S, Glieder A. Steroid biotransformations in biphasic systems with Yarrowia lipolytica expressing human liver cytochrome P450 genes. Microb Cell Fact. 2012;11:106.
78. Lah L, Kraševec N, Trontelj P, Komel R. High diversity and complex evolution of fungal cytochrome P450 reductase: cytochrome P450 systems. Fungal Genet Biol. 2008;45:446-58.
79. Kavšček M, Stražar M, Curk T, Natter K, Petrovič U. Yeast as a cell factory: current state and perspectives. Microb Cell Fact. 2015;14:94.
80. Pscheidt B, Glieder A. Yeast cell factories for fine chemical and API production. Microb Cell Fact. 2008;7:25.
81. Zöllner A, Buchheit D, Meyer MR, Maurer HH, Peters FT, Bureik M. Production of human phase 1 and 2 metabolites by whole-cell biotransformation with recombinant microbes. Bioanalysis. 2010;2:1277-90.
82. Yamazaki H. Fifty years of cytochrome P450 research. Berlin: Springer; 2014.
83. Hirosue S, Tazaki M, Hiratsuka N, Yanai S, Kabumoto H, Shinkyo R, Arisawa A, Sakaki T, Tsunekawa H, Johdo O. Insight into functional diversity of cytochrome P450 in the white-rot basidiomycete Phanerochaete chrysosporium: involvement of versatile monooxygenase. Biochem Biophys Res Commun. 2011;407:118-23.
84. Gudiminchi RK, Geier M, Glieder A, Camattari A. Screening for cytochrome P450 expression in Pichia pastoris whole cells by P450-carbon monoxide complex determination. Biotechnol J. 2013;8:146-52.
85. Palabiyik B, Karaer S, Arda N, Erturk Toker S, Temizkan G, Kelly S, Topal Sarikaya A. Expression of human cytochrome p450 3A4 gene in Schizosaccharomyces pombe. Biologia. 2008;63:450-4.
86. Mauersberger S, Novikova LA, Shkumatov VM. Cytochrome P450 expression in Yarrowia lipolytica and its use in steroid biotransformation. In: Yarrowia lipolytica. Berlin: Springer; 2013. p. 171-226.
87. Theron CW, Labuschagné M, Gudiminchi R, Albertyn J, Smit MS. A broad-range yeast expression system reveals Arxula adeninivorans expressing a fungal self-sufficient cytochrome P450 monooxygenase as an excellent whole-cell biocatalyst. FEMS Yeast Res. 2014;14:556-66.
88. Engler KH, Kelly SL, Coker RD, Evans IH. Toxin-binding properties of cytochrome P450 in Saccharomyces cerevisiae and Kluyveromyces marxianus. Biotechnol Lett. 2000;22:3-8.
89. Syed K, Kattamuri C, Thompson TB, Yadav JS. Cytochrome b 5 reductase-cytochrome b 5 as an active P450 redox enzyme system in Phanerochaete chrysosporium: atypical properties and in vivo evidence of electron transfer capability to CYP63A2. Arch Biochem Biophys. 2011;509:26-32.
90. Polak J, Jarosz-Wilkołazka A. Research whole-cell fungal transformation of precursors into dyes. Microbial Cell Fact. 2010;9(1):1.
91. Nevalainen H, Peterson R. Making recombinant proteins in filamentous fungi-are we expecting too much? Front Microbiol. 2014;5:86.
92. Tanaka M, Tokuoka M, Gomi K. Effects of codon optimization on the mRNA levels of heterologous genes in filamentous fungi. Appl Microbiol Biotechnol. 2014;98:3859-67.
93. Nevalainen KH, Te'o VS, Bergquist PL. Heterologous protein expression in filamentous fungi. Trends Biotechnol. 2005;23:468-74.
94. Faber BW, van Gorcom RF, Duine JA. Purification and characterization of benzoate-para-hydroxylase, a cytochrome P450 (CYP53A1), from Aspergillus niger. Arch Biochem Biophys. 2001;394:245-54.
95. Fujii R, Minami A, Tsukagoshi T, Sato N, Sahara T, Ohgiya S, Gomi K, Oikawa H. Total biosynthesis of diterpene aphidicolin, a specific inhibitor of DNA polymerase α: heterologous expression of four biosynthetic genes in Aspergillus oryzae. Biosci Biotechnol Biochem. 2011;75:1813-7.
96. Heneghan MN, Yakasai AA, Halo LM, Song Z, Bailey AM, Simpson TJ, Cox RJ, Lazarus CM. First heterologous reconstruction of a complete functional fungal biosynthetic multigene cluster. ChemBioChem. 2010;11:1508-12.
97. Fisch KM, Bakeer W, Yakasai AA, Song Z, Pedrick J, Wasil Z, Bailey AM, Lazarus CM, Simpson TJ, Cox RJ. Rational domain swaps decipher programming in fungal highly reducing polyketide synthases and resurrect an extinct metabolite. J Am Chem Soc. 2011;133:16635-41.
98. Sono M, Roach MP, Coulter ED, Dawson JH. Heme-containing oxygenases. Chem Rev. 1996;96:2841-88.
99. Jennewein S, Park H, DeJong JM, Long RM, Bollon AP, Croteau RB. Coexpression in yeast of Taxus cytochrome P450 reductase with cytochrome P450 oxygenases involved in Taxol biosynthesis. Biotechnol Bioeng. 2005;89:588-98.
100. O'Reilly E, Köhler V, Flitsch SL, Turner NJ. Cytochromes P450 as useful biocatalysts: addressing the limitations. Chem Commun. 2011;47:2490-501.
101. Syed K, Porollo A, Miller D, Yadav JS. Rational engineering of the fungal P450 monooxygenase CYP5136A3 to improve its oxidizing activity toward polycyclic aromatic hydrocarbons. Protein Eng Design Select. 2013; gzt036.
102. Syed K, Shale K, Nazir KNH, Krasevec N, Mashele SS, Pagadala NS. Genome-wide identification, annotation and characterization of novel thermostable cytochrome P450 monooxygenases from the thermophilic biomass-degrading fungi Thielavia terrestris and Myceliophthora thermophila. Genes Genom. 2014;36:321-33.
103. Sadeghi SJ, Fantuzzi A, Gilardi G. Breakthrough in P450 bioelectrochemistry and future perspectives. Biochimica et Biophysica Acta (BBA) Proteins Proteom. 2011;1814:237-48.
104. Sadeghi SJ, Gilardi G. Chimeric P450 enzymes: activity of artificial redox fusions driven by different reductases for biotechnological applications. Biotechnol Appl Biochem. 2013;60:102-10.
105. Lu Y, Mei L. Co-expression of P450 BM3 and glucose dehydrogenase by recombinant Escherichia coli and its application in an NADPH-dependent indigo production system. J Ind Microbiol Biotechnol. 2007;34:247-53.
106. Park JH, Lee SH, Cha GS, Choi DS, Nam DH, Lee JH, Lee JK, Yun CH, Jeong KJ, Park CB. Cofactor-free light-driven whole-cell cytochrome P450 catalysis. Angew Chem. 2015;127:983-7.
107. Verma R, Schwaneberg U, Roccatano D. Insight into the redox partner interaction mechanism in cytochrome P450BM-3 using molecular dynamics simulations. Biopolymers. 2014;101:197-209.
108. Denisov IG, Sligar SG. Cytochromes P450 in nanodiscs. Biochimica et Biophysica Acta (BBA) Proteins Proteom. 2011;1814:223-9.
109. Paddon CJ, Westfall P, Pitera D, Benjamin K, Fisher K, McPhee D, Leavell M, Tai A, Main A, Eng D. High-level semi-synthetic production of the potent antimalarial artemisinin. Nature. 2013;496:528-32.