Cytochrome P450 monooxygenases: an update on perspectives for synthetic application

Comparison of cytochrome P450 (CYP) genes from the mouse and human genomes, including nomenclature recommendations for genes, pseudogenes and alternative-splice variants

Nelson, D. R., Zeldin, D. C., Hoffman, S. M., Maltais, L. J., Wain, H. M., & Nebert, D. W. (2004) · Pharmacogenetics · doi:10.1097/00008571-200401000-00001 · Cited by 1,027

The Cytochrome P450 Homepage

Nelson, D. R. (2009) · Human Genomics · doi:10.1186/1479-7364-4-1-59 · Cited by 1,014

Cytochromes P450 as versatile biocatalysts

Bernhardt, R. (2006) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2006.01.026 · Cited by 886

Cytochrome P450 systems—biological variations of electron transport chains

Hannemann, F., Bichet, A., Ewen, K. M., & Bernhardt, R. (2007) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2006.07.017 · Cited by 759

Pigments of rat liver microsomes

Klingenberg, M. (1958) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(58)90436-3 · Cited by 664

Characterization of a catalytically self-sufficient 119,000-dalton cytochrome P-450 monooxygenase induced by barbiturates in Bacillus megaterium.

Narhi, L. O., & Fulco, A. J. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)38369-2 · Cited by 627

Comparative Genomics of Rice and Arabidopsis. Analysis of 727 Cytochrome P450 Genes and Pseudogenes from a Monocot and a Dicot

Nelson, D. R., Schuler, M. A., Paquette, S. M., Werck-Reichhart, D., & Bak, S. (2004) · Plant Physiology · doi:10.1104/pp.104.039826 · Cited by 477

Complex reactions catalyzed by cytochrome P450 enzymes

Isin, E. M., & Guengerich, F. P. (2007) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2006.07.003 · Cited by 448

Identification and developmental expression of the full complement of Cytochrome P450 genes in Zebrafish

Goldstone, J. V., McArthur, A. G., Kubota, A., Zanette, J., Parente, T., Jönsson, M. E., Nelson, D. R., & Stegeman, J. J. (2010) · BMC Genomics · doi:10.1186/1471-2164-11-643 · Cited by 425

Pigments of rat liver microsomes

Klingenberg, M. (2003) · Archives of Biochemistry and Biophysics · doi:10.1016/s0003-9861(02)00621-5 · Cited by 411

Cytochrome P450: taming a wild type enzyme

Jung, S. T., Lauchli, R., & Arnold, F. H. (2011) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2011.02.008 · Cited by 293

Cytochromes P450 as useful biocatalysts: addressing the limitations

O'Reilly, E., Köhler, V., Flitsch, S. L., & Turner, N. J. (2011) · Chemical Communications · doi:10.1039/c0cc03165h · Cited by 277

SuperCYP: a comprehensive database on Cytochrome P450 enzymes including a tool for analysis of CYP-drug interactions

Preissner, S., Kroll, K., Dunkel, M., Senger, C., Goldsobel, G., Kuzman, D., Guenther, S., Winnenburg, R., Schroeder, M., & Preissner, R. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkp970 · Cited by 274

Practical issues in the application of oxygenases

van Beilen, J. B., Duetz, W. A., Schmid, A., & Witholt, B. (2003) · Trends in Biotechnology · doi:10.1016/s0167-7799(03)00032-5 · Cited by 251

Engineered Alkane‐Hydroxylating Cytochrome P450BM3 Exhibiting Nativelike Catalytic Properties

Fasan, R., Chen, M. M., Crook, N. C., & Arnold, F. H. (2007) · Angewandte Chemie International Edition · doi:10.1002/anie.200702616 · Cited by 239

Progress in tracing the evolutionary paths of cytochrome P450

Nelson, D. R. (2011) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2010.08.008 · Cited by 219

Cytochrome P450–redox partner fusion enzymes

Munro, A. W., Girvan, H. M., & McLean, K. J. (2007) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2006.08.018 · Cited by 205

Engineered Alkane‐Hydroxylating Cytochrome P450BM3 Exhibiting Nativelike Catalytic Properties

Fasan, R., Chen, M. M., Crook, N. C., & Arnold, F. H. (2007) · Angewandte Chemie · doi:10.1002/ange.200702616 · Cited by 187

A Novel Semi-biosynthetic Route for Artemisinin Production Using Engineered Substrate-Promiscuous P450 BM3

Dietrich, J. A., Yoshikuni, Y., Fisher, K. J., Woolard, F. X., Ockey, D., McPhee, D. J., Renninger, N. S., Chang, M. C. Y., Baker, D., & Keasling, J. D. (2009) · ACS Chemical Biology · doi:10.1021/cb900006h · Cited by 186

Biosynthesis of the Sesquiterpene Antibiotic Albaflavenone in Streptomyces coelicolor A3(2)

Zhao, B., Lin, X., Lei, L., Lamb, D. C., Kelly, S. L., Waterman, M. R., & Cane, D. E. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m710421200 · Cited by 183

Fungal cytochrome P450 database

Park, J., Lee, S., Choi, J., Ahn, K., Park, B., Park, J., Kang, S., & Lee, Y.-H. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-402 · Cited by 175

Engineering cytochrome P450 biocatalysts for biotechnology, medicine and bioremediation

Kumar, S. (2010) · Expert Opinion on Drug Metabolism & Toxicology · doi:10.1517/17425250903431040 · Cited by 162

Enantioselective α-Hydroxylation of 2-Arylacetic Acid Derivatives and Buspirone Catalyzed by Engineered Cytochrome P450 BM-3

Landwehr, M., Hochrein, L. M., Otey, C. R., Kasrayan, A., Bäckvall, J., & Arnold, F. H. (2006) · Journal of the American Chemical Society · doi:10.1021/ja061261x · Cited by 151

Rational Design of a Minimal and Highly Enriched CYP102A1 Mutant Library with Improved Regio‐, Stereo‐ and Chemoselectivity

Seifert, A., Vomund, S., Grohmann, K., Kriening, S., Urlacher, V. B., Laschat, S., & Pleiss, J. (2009) · ChemBioChem · doi:10.1002/cbic.200800799 · Cited by 149

The Mechanism of the Acyl-Carbon Bond Cleavage Reaction Catalyzed by Recombinant Sterol 14α-Demethylase of Candida albicans (Other Names Are: Lanosterol 14α-Demethylase, P-45014DM, and CYP51)

Shyadehi, A. Z., Lamb, D. C., Kelly, S. L., Kelly, D. E., Schunck, W., Wright, J. N., Corina, D. L., & Akhtar, M. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.21.12445 · Cited by 148

Structure-Guided Recombination Creates an Artificial Family of Cytochromes P450

Otey, C. R., Landwehr, M., Endelman, J. B., Hiraga, K., Bloom, J. D., & Arnold, F. H. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040112 · Cited by 147

A Panel of Cytochrome P450 BM3 Variants to Produce Drug Metabolites and Diversify Lead Compounds

Sawayama, A. M., Chen, M. M. Y., Kulanthaivel, P., Kuo, M., Hemmerle, H., & Arnold, F. H. (2009) · Chemistry - A European Journal · doi:10.1002/chem.200900643 · Cited by 146

Preparation of human metabolites of propranolol using laboratory‐evolved bacterial cytochromes P450

Otey, C. R., Bandara, G., Lalonde, J. J., Takahashi, K., & Arnold, F. H. (2005) · Biotechnology and Bioengineering · doi:10.1002/bit.20744 · Cited by 145

The role of cytochrome P450 monooxygenases in microbial fatty acid metabolism

Bogaert, I. V., Groeneboer, S., Saerens, K. M. J., & Soetaert, W. (2010) · FEBS Journal · doi:10.1111/j.1742-4658.2010.07949.x · Cited by 144

An Oxidative Phenol Coupling Reaction Catalyzed by OxyB, a Cytochrome P450 from the Vancomycin‐Producing Microorganism

Zerbe, K., Woithe, K., Li, D. B., Vitali, F., Bigler, L., & Robinson, J. A. (2004) · Angewandte Chemie International Edition · doi:10.1002/anie.200461278 · Cited by 130

The Cytochrome P450 Complement (CYPome) of Streptomyces coelicolor A3(2)

Lamb, D. C., Skaug, T., Song, H., Jackson, C. J., Podust, L. M., Waterman, M. R., Kell, D. B., Kelly, D. E., & Kelly, S. L. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m111109200 · Cited by 124

Cytochromes P450: exploiting diversity and enabling application as biocatalysts

Grogan, G. (2010) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2010.11.014 · Cited by 123

Cytochrome P450 monooxygenase from Clostridium acetobutylicum: A new α-fatty acid hydroxylase

Girhard, M., Schuster, S., Dietrich, M., Dürre, P., & Urlacher, V. B. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.07.155 · Cited by 113

Characterization of the versatile monooxygenase CYP109B1 from Bacillus subtilis

Girhard, M., Klaus, T., Khatri, Y., Bernhardt, R., & Urlacher, V. B. (2010) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-010-2472-z · Cited by 110

Identification of Critical Residues in Novel Drug Metabolizing Mutants of Cytochrome P450 BM3 Using Random Mutagenesis

van Vugt‐Lussenburg, B. M. A., Stjernschantz, E., Lastdrager, J., Oostenbrink, C., Vermeulen, N. P. E., & Commandeur, J. N. M. (2007) · Journal of Medicinal Chemistry · doi:10.1021/jm0609061 · Cited by 108

Regioselective biooxidation of (+)-valencene by recombinant E. coli expressing CYP109B1 from Bacillus subtilis in a two-liquid-phase system

Girhard, M., Machida, K., Itoh, M., Schmid, R. D., Arisawa, A., & Urlacher, V. B. (2009) · Microbial Cell Factories · doi:10.1186/1475-2859-8-36 · Cited by 104

Cytochrome P450 complement (CYPome) of the avermectin-producer Streptomyces avermitilis and comparison to that of Streptomyces coelicolor A3(2)

Lamb, D. C., Ikeda, H., Nelson, D. R., Ishikawa, J., Skaug, T., Jackson, C., Ōmura, S., Waterman, M. R., & Kelly, S. L. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(03)01231-2 · Cited by 97

The CYPome (Cytochrome P450 complement) of Aspergillus nidulans

Kelly, D. E., Kraševec, N., Mullins, J. G. L., & Nelson, D. R. (2008) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2008.08.010 · Cited by 97

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

Weisser, P., Krämer, R., Sahm, H., & Sprenger, G. A. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.11.3351-3354.1995 · Cited by 96

Application of drug metabolising mutants of cytochrome P450 BM3 (CYP102A1) as biocatalysts for the generation of reactive metabolites

Damsten, M. C., van Vugt‐Lussenburg, B. M. A., Zeldenthuis, T., et al. (2007) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2007.09.007 · Cited by 92

Towards Preparative Scale Steroid Hydroxylation with Cytochrome P450 Monooxygenase CYP106A2

Zehentgruber, D., Hannemann, F., Bleif, S., Bernhardt, R., & Lütz, S. (2010) · ChemBioChem · doi:10.1002/cbic.200900706 · Cited by 92

Engineering Cytochrome P450 Enzymes

Gillam, E. M. J. (2007) · Chemical Research in Toxicology · doi:10.1021/tx7002849 · Cited by 91

Crystal Structure of CYP105A1 (P450SU-1) in Complex with 1α,25-Dihydroxyvitamin D3,

Sugimoto, H., Shinkyo, R., Hayashi, K., Yoneda, S., Yamada, M., Kamakura, M., Ikushiro, S., Shiro, Y., & Sakaki, T. (2008) · Biochemistry · doi:10.1021/bi7023767 · Cited by 89

Cytochrome P450 enzymes from the metabolically diverse bacterium Rhodopseudomonas palustris

Bell, S. G., Hoskins, N., Xu, F., Caprotti, D., Rao, Z., & Wong, L. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.01.133 · Cited by 73

Diversification of Catalytic Function in a Synthetic Family of Chimeric Cytochrome P450s

Landwehr, M., Carbone, M. N., Otey, C. R., Li, Y., & Arnold, F. H. (2007) · Chemistry & Biology · doi:10.1016/j.chembiol.2007.01.009 · Cited by 73

Improvement of P450BM-3 whole-cell biocatalysis by integrating heterologous cofactor regeneration combining glucose facilitator and dehydrogenase in E. coli

Schewe, H., Kaup, B., & Schrader, J. (2007) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-007-1277-1 · Cited by 69

Identification of selectivity‐determining residues in cytochrome P450 monooxygenases: A systematic analysis of the substrate recognition site 5

Seifert, A., & Pleiss, J. (2008) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.22242 · Cited by 68

P450BM-3-catalyzed whole-cell biotransformation of α-pinene with recombinant Escherichia coli in an aqueous–organic two-phase system

Schewe, H., Holtmann, D., & Schrader, J. (2009) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-009-1917-8 · Cited by 66

Rearrangement reactions catalyzed by cytochrome P450s

de Montellano, P. R. O., & Nelson, S. D. (2010) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2010.10.016 · Cited by 65

Cytochrome P450s in the development of target-based anticancer drugs

Purnapatre, K. P., Khattar, S. K., & Saini, K. S. (2007) · Cancer Letters · doi:10.1016/j.canlet.2007.10.024 · Cited by 64

Design of an Escherichia coli system for whole cell mediated steroid synthesis and molecular evolution of steroid hydroxylases

Hannemann, F., Virus, C., & Bernhardt, R. (2006) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2006.01.009 · Cited by 62

Regio- and Stereospecificity of Filipin Hydroxylation Sites Revealed by Crystal Structures of Cytochrome P450 105P1 and 105D6 from Streptomyces avermitilis

Xu, L., Fushinobu, S., Takamatsu, S., Wakagi, T., Ikeda, H., & Shoun, H. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.092460 · Cited by 62

The Cytochrome P450 Engineering Database: integration of biochemical properties

Sirim, D., Wagner, F., Lisitsa, A., & Pleiss, J. (2009) · BMC Biochemistry · doi:10.1186/1471-2091-10-27 · Cited by 59

Engineering Bacterial Cytochrome P450 (P450) BM3 into a Prototype with Human P450 Enzyme Activity Using Indigo Formation

Park, S., Kim, D., Kim, D., Kim, D., Jung, H.-C., Pan, J., Ahn, T., Kim, D., & Yun, C. (2010) · Drug Metabolism and Disposition · doi:10.1124/dmd.109.030759 · Cited by 58

Challenges of steroid biotransformation with human cytochrome P450 monooxygenase CYP21 using resting cells of recombinant Schizosaccharomyces pombe

Zehentgruber, D., Drăgan, C.-A., Bureik, M., & Lütz, S. (2010) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2010.01.019 · Cited by 54

Crystal Structures of Cytochrome P450 105P1 fromStreptomyces avermitilis: Conformational Flexibility and Histidine Ligation State

Xu, L., Fushinobu, S., Ikeda, H., Wakagi, T., & Shoun, H. (2008) · Journal of Bacteriology · doi:10.1128/jb.01276-08 · Cited by 53

Improved product‐per‐glucose yields in P450‐dependent propane biotransformations using engineered Escherichia coli

Fasan, R., Crook, N., Peters, M. W., Meinhold, P., Bülter, T., Landwehr, M., Cirino, P. C., & Arnold, F. H. (2010) · Biotechnology and Bioengineering · doi:10.1002/bit.22984 · Cited by 52

The CYPome of Sorangium cellulosum So ce56 and Identification of CYP109D1 as a New Fatty Acid Hydroxylase

Khatri, Y., Hannemann, F., Ewen, K. M., Pistorius, D., Perlova, O., Kagawa, N., Brachmann, A. O., Müller, R., & Bernhardt, R. (2010) · Chemistry & Biology · doi:10.1016/j.chembiol.2010.10.010 · Cited by 51

Thermodynamic and Biophysical Characterization of Cytochrome P450 BioI from Bacillus subtilis

Lawson, R. J., Leys, D., Sutcliffe, M. J., Kemp, C. A., Cheesman, M. R., Smith, S. J., Clarkson, J., Smith, W. E., Haq, I., Perkins, J. B., et al. (2004) · Biochemistry · doi:10.1021/bi049132l · Cited by 50

Engineering and assaying of cytochrome P450 biocatalysts

Rabe, K. S., Gandubert, V. J., Spengler, M., Erkelenz, M., & Niemeyer, C. M. (2008) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-008-2248-9 · Cited by 48

Regioselective hydroxylation of daidzein using P450 (CYP105D7) from Streptomyces avermitilis MA4680

Pandey, B. P., Roh, C., Choi, K., Lee, N., Kim, E. J., Ko, S., Kim, T., Yun, H., & Kim, B. (2009) · Biotechnology and Bioengineering · doi:10.1002/bit.22582 · Cited by 46

How Proteins Adapt: Lessons from Directed EvolutionPreprint

Arnold, F. H. (2009) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2009.74.046 · Cited by 46

ExploitingStreptomyces coelicolorA3(2) P450s as a model for application in drug discovery

Lamb, D. C., Guengerich, F. P., Kelly, S. L., & Waterman, M. R. (2006) · Expert Opinion on Drug Metabolism & Toxicology · doi:10.1517/17425255.2.1.27 · Cited by 43

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

Kudo, F., Motegi, A., Mizoue, K., & Eguchi, T. (2010) · ChemBioChem · doi:10.1002/cbic.201000214 · Cited by 42

Coexpression of redox partners increases the hydrocortisone (cortisol) production efficiency in CYP11B1 expressing fission yeast Schizosaccharomyces pombe

Hakki, T., Zearo, S., Drăgan, C.-A., Bureik, M., & Bernhardt, R. (2007) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2007.06.022 · Cited by 41

Characterizing Proteins of Unknown Function: Orphan Cytochrome P450 Enzymes as a Paradigm

Guengerich, F. P., Tang, Z., Salamanca-Pinzon, S. G., & Cheng, Q. (2010) · Molecular Interventions · doi:10.1124/mi.10.3.6 · Cited by 40

Genome Mining in Sorangium cellulosum So ce56

Ewen, K. M., Hannemann, F., Khatri, Y., Perlova, O., Kappl, R., Krug, D., Hüttermann, J., Müller, R., & Bernhardt, R. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.021717 · Cited by 39

Extending the capabilities of nature’s most versatile catalysts: Directed evolution of mammalian xenobiotic-metabolizing P450s

Gillam, E. M. J. (2007) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2007.04.033 · Cited by 32

Membrane integration of recombinant human P450 forms

Shukla, A., Huang, W., Depaz, I. M. B., & Gillam, E. M. J. (2009) · Xenobiotica · doi:10.1080/00498250902934884 · Cited by 14

Bioconversion of small molecules by cytochrome P450 species expressed in Escherichia coli

Uno, T., Okamoto, S., Masuda, S., Itoh, A., Uno, Y., Nakamura, M., Kanamaru, K., Yamagata, H., & Imaishi, H. (2008) · Biotechnology and Applied Biochemistry · doi:10.1042/ba20070173 · Cited by 12

Catalysis with Cytochrome P 450 Monooxygenases

Urlacher, V. B. (2010) · doi:10.1002/9783527628698.hgc025 · Cited by 5

Diverse Metabolic Capacities of Fungi for Bioremediation

Deshmukh, R., Khardenavis, A. A., & Purohit, H. J. (2016) · Indian Journal of Microbiology · doi:10.1007/s12088-016-0584-6 · Cited by 435

Photobiocatalysis: Activating Redox Enzymes by Direct or Indirect Transfer of Photoinduced Electrons

Lee, S. H., Choi, D. S., Kuk, S. K., & Park, C. B. (2018) · Angewandte Chemie International Edition · doi:10.1002/anie.201710070 · Cited by 422

Expanding the organic toolbox: a guide to integrating biocatalysis in synthesis

Clouthier, C. M., & Pelletier, J. N. (2012) · Chemical Society Reviews · doi:10.1039/c2cs15286j · Cited by 358

Cytochrome P450 Monooxygenases in Biotechnology and Synthetic Biology

Urlacher, V. B., & Girhard, M. (2019) · Trends in Biotechnology · doi:10.1016/j.tibtech.2019.01.001 · Cited by 355

Biotechnology of non-Saccharomyces yeasts—the ascomycetes

Johnson, E. A. (2013) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-012-4497-y · Cited by 193