A Continuing Career in Biocatalysis: Frances H. Arnold

Fasan, Rudi; Jennifer Kan, S. B.; Zhao, Huimin

doi:10.1021/acscatal.9b02737

A Continuing Career in Biocatalysis: Frances H. Arnold

Journal Article · Tue Sep 17 00:00:00 EDT 2019 · ACS Catalysis

DOI:https://doi.org/10.1021/acscatal.9b02737· OSTI ID:1803334

^[1]; ^[2]; ^[3]

Univ. of Rochester, NY (United States); OSTI
California Institute of Technology (CalTech), Pasadena, CA (United States)
Univ. of Illinois at Urbana-Champaign, IL (United States)

On the occasion of Professor Frances H. Arnold’s recent acceptance of the 2018 Nobel Prize in Chemistry, we honor her numerous contributions to the fields of directed evolution and biocatalysis. Arnold pioneered the development of directed evolution methods for engineering enzymes as biocatalysts. Her highly interdisciplinary research has provided grounds not only for understanding the mechanisms of enzyme evolution but also for developing commercially viable enzyme biocatalysts and biocatalytic processes. In this Account, we highlight some of her notable contributions in the past three decades in the development of foundational directed evolution methods and their applications in the design and engineering of enzymes with desired functions for biocatalysis. Her work has created a paradigm shift in the broad catalysis field.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Illinois at Urbana-Champaign, IL (United States)

Sponsoring Organization:: National Institutes of Health (NIH); National Science Foundation (NSF); USDOE

Grant/Contract Number:: SC0018260; SC0018420

OSTI ID:: 1803334

Journal Information:: ACS Catalysis, Journal Name: ACS Catalysis Journal Issue: 11 Vol. 9; ISSN 2155-5435

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (146)

Directed evolution of an esterase for the stereoselective resolution of a key intermediate in the synthesis of epothilones Bornscheuer, Uwe T.; Altenbuchner, Josef; Meyer, Hartmut H. Biotechnology and Bioengineering, Vol. 58, Issue 5 https://doi.org/10.1002/(SICI)1097-0290(19980605)58:5<554::AID-BIT12>3.0.CO;2-B	journal	June 1998
Enantioselective Enzymes for Organic Synthesis Created by Directed Evolution Reetz, Manfred T.; Jaeger, Karl-Erich Chemistry - A European Journal, Vol. 6, Issue 3 https://doi.org/10.1002/(SICI)1521-3765(20000204)6:3<407::AID-CHEM407>3.0.CO;2-Y	journal	February 2000
Directed Evolution of a Cytochrome P450 Monooxygenase for Alkane Oxidation Farinas, Edgardo T.; Schwaneberg, Ulrich; Glieder, Anton Advanced Synthesis & Catalysis, Vol. 343, Issue 6-7 https://doi.org/10.1002/1615-4169(200108)343:6/7<601::AID-ADSC601>3.0.CO;2-9	journal	August 2001
Creation of Enantioselective Biocatalysts for Organic Chemistry by In Vitro Evolution Reetz, Manfred T.; Zonta, Albin; Schimossek, Klaus Angewandte Chemie International Edition in English, Vol. 36, Issue 24 https://doi.org/10.1002/anie.199728301	journal	January 1997
A Self-Sufficient Peroxide-Driven Hydroxylation Biocatalyst Cirino, Patrick C.; Arnold, Frances H. Angewandte Chemie International Edition, Vol. 42, Issue 28, p. 3299-3301 https://doi.org/10.1002/anie.200351434	journal	July 2003
Engineered Alkane-Hydroxylating Cytochrome P450_BM3 Exhibiting Nativelike Catalytic Properties Fasan, Rudi; Chen, Mike M.; Crook, Nathan C. Angewandte Chemie International Edition, Vol. 46, Issue 44, p. 8414-8418 https://doi.org/10.1002/anie.200702616	journal	November 2007
Enantiocomplementary Enzymes: Classification, Molecular Basis for Their Enantiopreference, and Prospects for Mirror-Image Biotransformations Mugford, Paul F.; Wagner, Ulrike G.; Jiang, Yun Angewandte Chemie International Edition, Vol. 47, Issue 46 https://doi.org/10.1002/anie.200705159	journal	November 2008
Laboratory Evolution of Stereoselective Enzymes: A Prolific Source of Catalysts for Asymmetric Reactions Reetz, Manfred T. Angewandte Chemie International Edition, Vol. 50, Issue 1 https://doi.org/10.1002/anie.201000826	journal	August 2010
If CH Bonds Could Talk: Selective CH Bond Oxidation Newhouse, Timothy; Baran, Phil S. Angewandte Chemie International Edition, Vol. 50, Issue 15 https://doi.org/10.1002/anie.201006368	journal	March 2011
Enantioselective Intramolecular CH Amination Catalyzed by Engineered Cytochrome P450 Enzymes In Vitro and In Vivo McIntosh, John A.; Coelho, Pedro S.; Farwell, Christopher C. Angewandte Chemie International Edition, Vol. 52, Issue 35 https://doi.org/10.1002/anie.201304401	journal	July 2013
Iron Porphyrin Carbenes as Catalytic Intermediates: Structures, Mössbauer and NMR Spectroscopic Properties, and Bonding Khade, Rahul L.; Fan, Wenchao; Ling, Yan Angewandte Chemie International Edition, Vol. 53, Issue 29 https://doi.org/10.1002/anie.201402472	journal	June 2014
Improved Cyclopropanation Activity of Histidine-Ligated Cytochrome P450 Enables the Enantioselective Formal Synthesis of Levomilnacipran Wang, Z. Jane; Renata, Hans; Peck, Nicole E. Angewandte Chemie International Edition, Vol. 53, Issue 26 https://doi.org/10.1002/anie.201402809	journal	May 2014
Highly Diastereoselective and Enantioselective Olefin Cyclopropanation Using Engineered Myoglobin-Based Catalysts Bordeaux, Melanie; Tyagi, Vikas; Fasan, Rudi Angewandte Chemie International Edition, Vol. 54, Issue 6 https://doi.org/10.1002/anie.201409928	journal	December 2014
Directed Evolution of RebH for Site-Selective Halogenation of Large Biologically Active Molecules Payne, James T.; Poor, Catherine B.; Lewis, Jared C. Angewandte Chemie International Edition, Vol. 54, Issue 14 https://doi.org/10.1002/anie.201411901	journal	February 2015
Myoglobin‐Catalyzed Olefination of Aldehydes Tyagi, Vikas; Fasan, Rudi Angewandte Chemie International Edition, Vol. 55, Issue 7 https://doi.org/10.1002/anie.201508817	journal	January 2016
Asymmetric Enzymatic Synthesis of Allylic Amines: A Sigmatropic Rearrangement Strategy Prier, Christopher K.; Hyster, Todd K.; Farwell, Christopher C. Angewandte Chemie International Edition, Vol. 55, Issue 15 https://doi.org/10.1002/anie.201601056	journal	March 2016
Gram-Scale Synthesis of Chiral Cyclopropane-Containing Drugs and Drug Precursors with Engineered Myoglobin Catalysts Featuring Complementary Stereoselectivity Bajaj, Priyanka; Sreenilayam, Gopeekrishnan; Tyagi, Vikas Angewandte Chemie International Edition, Vol. 55, Issue 52 https://doi.org/10.1002/anie.201608680	journal	November 2016
Biocatalytic Routes to Enantiomerically Enriched Dibenz[ c , e ]azepines France, Scott P.; Aleku, Godwin A.; Sharma, Mahima Angewandte Chemie International Edition, Vol. 56, Issue 49 https://doi.org/10.1002/anie.201708453	journal	November 2017
Directed Evolution Empowered Redesign of Natural Proteins for the Sustainable Production of Chemicals and Pharmaceuticals Bornscheuer, Uwe T.; Hauer, Bernhard; Jaeger, Karl Erich Angewandte Chemie International Edition, Vol. 58, Issue 1 https://doi.org/10.1002/anie.201812717	journal	December 2018
Laboratory evolution of cytochrome P450 BM-3 monooxygenase for organic cosolvents Seng Wong, Tuck; Arnold, Frances H.; Schwaneberg, Ulrich Biotechnology and Bioengineering, Vol. 85, Issue 3 https://doi.org/10.1002/bit.10896	journal	January 2004
Preparation of human metabolites of propranolol using laboratory-evolved bacterial cytochromes P450 Otey, Christopher R.; Bandara, Geethani; Lalonde, James Biotechnology and Bioengineering, Vol. 93, Issue 3 https://doi.org/10.1002/bit.20744	journal	January 2006
Recombinant human cytochrome P450 monooxygenases for drug metabolite synthesis Schroer, Kirsten; Kittelmann, Matthias; Lütz, Stephan Biotechnology and Bioengineering, Vol. 106, Issue 5 https://doi.org/10.1002/bit.22775	journal	April 2010
Improved product-per-glucose yields in P450-dependent propane biotransformations using engineered Escherichia coli Fasan, Rudi; Crook, Nathan C.; Peters, Matthew W. Biotechnology and Bioengineering, Vol. 108, Issue 3 https://doi.org/10.1002/bit.22984	journal	November 2010
Thermostabilization of a Cytochrome P450 Peroxygenase Salazar, Oriana; Cirino, Patrick C.; Arnold, Frances H. ChemBioChem, Vol. 4, Issue 9 https://doi.org/10.1002/cbic.200300660	journal	September 2003
Direct Conversion of Ethane to Ethanol by Engineered Cytochrome P450 BM3 Meinhold, Peter; Peters, Matthew W.; Chen, Michael M. Y. ChemBioChem, Vol. 6, Issue 10 https://doi.org/10.1002/cbic.200500261	journal	September 2005
Evolution in Reverse: Engineering a D-Xylose-Specific Xylose Reductase Nair, Nikhil U.; Zhao, Huimin ChemBioChem, Vol. 9, Issue 8 https://doi.org/10.1002/cbic.200700765	journal	May 2008
Non-natural Olefin Cyclopropanation Catalyzed by Diverse Cytochrome P450s and Other Hemoproteins Heel, Thomas; McIntosh, John A.; Dodani, Sheel C. ChemBioChem, Vol. 15, Issue 17 https://doi.org/10.1002/cbic.201402286	journal	October 2014
Mutating a Highly Conserved Residue in Diverse Cytochrome P450s Facilitates Diastereoselective Olefin Cyclopropanation Gober, Joshua G.; Rydeen, Amy E.; Gibson-O'Grady, Evan J. ChemBioChem, Vol. 17, Issue 5 https://doi.org/10.1002/cbic.201500624	journal	February 2016
Engineered Bacterial Mimics of Human Drug Metabolizing Enzyme CYP2C9 Rentmeister, Andrea; Brown, Tristan R.; Snow, Christopher D. ChemCatChem, Vol. 3, Issue 6 https://doi.org/10.1002/cctc.201000452	journal	April 2011
Enantioselective Epoxidation of Terminal Alkenes to (R)- and (S)-Epoxides by Engineered Cytochromes P450 BM-3 Kubo, Takafumi; Peters, Matthew W.; Meinhold, Peter Chemistry - A European Journal, Vol. 12, Issue 4 https://doi.org/10.1002/chem.200500584	journal	January 2006
A Panel of Cytochrome P450 BM3 Variants to Produce Drug Metabolites and Diversify Lead Compounds Sawayama, Andrew M.; Chen, Michael M. Y.; Kulanthaivel, Palaniappan Chemistry - A European Journal, Vol. 15, Issue 43 https://doi.org/10.1002/chem.200900643	journal	September 2009
Enzymatic Racemization of Amines Catalyzed by Enantiocomplementary ω-Transaminases Koszelewski, Dominik; Grischek, Barbara; Glueck, Silvia M. Chemistry - A European Journal, Vol. 17, Issue 1 https://doi.org/10.1002/chem.201001602	journal	November 2010
C−H Insertions by Iron Porphyrin Carbene: Basic Mechanism and Origin of Substrate Selectivity Khade, Rahul L.; Zhang, Yong Chemistry – A European Journal, Vol. 23, Issue 70 https://doi.org/10.1002/chem.201704631	journal	November 2017
Cytochromes P450 as promising catalysts for biotechnological application: chances and limitations Bernhardt, Rita; Urlacher, Vlada B. Applied Microbiology and Biotechnology, Vol. 98, Issue 14 https://doi.org/10.1007/s00253-014-5767-7	journal	May 2014
(ω–2) Hydroxylation of Fatty Acids by a Soluble System from Bacillus megaterium Miura, Yoshiro; Fulco, Armand J. Journal of Biological Chemistry, Vol. 249, Issue 6 https://doi.org/10.1016/S0021-9258(19)42868-8	journal	March 1974
Rational evolution of a medium chain-specific cytochrome P -450 BM-3 variant Li, Qing-Shan; Schwaneberg, Ulrich; Fischer, Markus Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 1545, Issue 1-2 https://doi.org/10.1016/S0167-4838(00)00268-5	journal	February 2001
Rational approach to improving reductive catalysis by cytochrome P450cam Manchester, J. I.; Ornstein, R. L. Biochimie, Vol. 78, Issue 8-9 https://doi.org/10.1016/S0300-9084(97)82529-1	journal	January 1996
A high-throughput digital imaging screen for the discovery and directed evolution of oxygenases Joo, Hyun; Arisawa, Akira; Lin, Zhanglin Chemistry & Biology, Vol. 6, Issue 10 https://doi.org/10.1016/S1074-5521(00)80017-4	journal	October 1999
Cytochrome P450 systems—biological variations of electron transport chains Hannemann, Frank; Bichet, Andreas; Ewen, Kerstin M. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1770, Issue 3 https://doi.org/10.1016/j.bbagen.2006.07.017	journal	March 2007
Cytochrome P450 diversity in the tree of life Nelson, David R. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1866, Issue 1 https://doi.org/10.1016/j.bbapap.2017.05.003	journal	January 2018
Heterotropic and homotropic cooperativity by a drug-metabolising mutant of cytochrome P450 BM3 van Vugt-Lussenburg, Barbara M. A.; Damsten, Micaela C.; Maasdijk, Dianne M. Biochemical and Biophysical Research Communications, Vol. 346, Issue 3 https://doi.org/10.1016/j.bbrc.2006.05.179	journal	August 2006
Intramolecular C(sp3)H amination of arylsulfonyl azides with engineered and artificial myoglobin-based catalysts Bordeaux, Melanie; Singh, Ritesh; Fasan, Rudi Bioorganic & Medicinal Chemistry, Vol. 22, Issue 20 https://doi.org/10.1016/j.bmc.2014.05.015	journal	October 2014
Biocatalysts for the pharmaceutical industry created by structure-guided directed evolution of stereoselective enzymes Li, Guangyue; Wang, Jian-bo; Reetz, Manfred T. Bioorganic & Medicinal Chemistry, Vol. 26, Issue 7 https://doi.org/10.1016/j.bmc.2017.05.021	journal	April 2018
Directed enzyme evolution: climbing fitness peaks one amino acid at a time Tracewell, Cara A.; Arnold, Frances H. Current Opinion in Chemical Biology, Vol. 13, Issue 1 https://doi.org/10.1016/j.cbpa.2009.01.017	journal	February 2009
Deracemisation methods Turner, Nicholas J. Current Opinion in Chemical Biology, Vol. 14, Issue 2 https://doi.org/10.1016/j.cbpa.2009.11.027	journal	April 2010
Engineering and application of P450 monooxygenases in pharmaceutical and metabolite synthesis Caswell, Jill M.; O’Neill, Maeve; Taylor, Steve JC Current Opinion in Chemical Biology, Vol. 17, Issue 2 https://doi.org/10.1016/j.cbpa.2013.01.028	journal	April 2013
Selective C H bond functionalization with engineered heme proteins: new tools to generate complexity Zhang, Ruijie K.; Huang, Xiongyi; Arnold, Frances H. Current Opinion in Chemical Biology, Vol. 49 https://doi.org/10.1016/j.cbpa.2018.10.004	journal	April 2019
Diversification of Catalytic Function in a Synthetic Family of Chimeric Cytochrome P450s Landwehr, Marco; Carbone, Martina; Otey, Christopher R. Chemistry & Biology, Vol. 14, Issue 3 https://doi.org/10.1016/j.chembiol.2007.01.009	journal	March 2007
Exploiting and engineering hemoproteins for abiological carbene and nitrene transfer reactions Brandenberg, Oliver F.; Fasan, Rudi; Arnold, Frances H. Current Opinion in Biotechnology, Vol. 47 https://doi.org/10.1016/j.copbio.2017.06.005	journal	October 2017
Rapid Creation of a Novel Protein Function by in Vitro Coevolution Chen, Zhilei; Zhao, Huimin Journal of Molecular Biology, Vol. 348, Issue 5 https://doi.org/10.1016/j.jmb.2005.02.070	journal	May 2005
Evolutionary History of a Specialized P450 Propane Monooxygenase Fasan, Rudi; Meharenna, Yergalem T.; Snow, Christopher D. Journal of Molecular Biology, Vol. 383, Issue 5 https://doi.org/10.1016/j.jmb.2008.06.060	journal	November 2008
Formation and Cleavage of C–C Bonds by Enzymatic Oxidation–Reduction Reactions Guengerich, F. Peter; Yoshimoto, Francis K. Chemical Reviews, Vol. 118, Issue 14 https://doi.org/10.1021/acs.chemrev.8b00031	journal	June 2018
Chemoselective Cyclopropanation over Carbene Y–H Insertion Catalyzed by an Engineered Carbene Transferase Moore, Eric J.; Steck, Viktoria; Bajaj, Priyanka The Journal of Organic Chemistry, Vol. 83, Issue 14 https://doi.org/10.1021/acs.joc.8b00946	journal	June 2018
Stereoselective Olefin Cyclopropanation under Aerobic Conditions with an Artificial Enzyme Incorporating an Iron-Chlorin e6 Cofactor Sreenilayam, Gopeekrishnan; Moore, Eric J.; Steck, Viktoria ACS Catalysis, Vol. 7, Issue 11 https://doi.org/10.1021/acscatal.7b02583	journal	October 2017
Beyond Iron: Iridium-Containing P450 Enzymes for Selective Cyclopropanations of Structurally Diverse Alkenes Key, Hanna M.; Dydio, Paweł; Liu, Zhennan ACS Central Science, Vol. 3, Issue 4 https://doi.org/10.1021/acscentsci.6b00391	journal	April 2017
Diverse Engineered Heme Proteins Enable Stereodivergent Cyclopropanation of Unactivated Alkenes Knight, Anders M.; Kan, S. B. Jennifer; Lewis, Russell D. ACS Central Science, Vol. 4, Issue 3 https://doi.org/10.1021/acscentsci.7b00548	journal	February 2018
A Biocatalytic Platform for Synthesis of Chiral α- Trifluoromethylated Organoborons Huang, Xiongyi; Garcia-Borràs, Marc; Miao, Kun ACS Central Science, Vol. 5, Issue 2 https://doi.org/10.1021/acscentsci.8b00679	journal	January 2019
Detection of a Peptide Biomarker by Engineered Yeast Receptors Adeniran, Adebola; Stainbrook, Sarah; Bostick, John W. ACS Synthetic Biology, Vol. 7, Issue 2 https://doi.org/10.1021/acssynbio.7b00410	journal	January 2018
Ring-Strain-Enabled Reaction Discovery: New Heterocycles from Bicyclo[1.1.0]butanes Walczak, Maciej A. A.; Krainz, Tanja; Wipf, Peter Accounts of Chemical Research, Vol. 48, Issue 4 https://doi.org/10.1021/ar500437h	journal	March 2015
Discovery of Potent Parthenolide-Based Antileukemic Agents Enabled by Late-Stage P450-Mediated C—H Functionalization Kolev, Joshua N.; O’Dwyer, Kristen M.; Jordan, Craig T. ACS Chemical Biology, Vol. 9, Issue 1 https://doi.org/10.1021/cb400626w	journal	October 2013
Stereoselective Cyclopropanation Reactions Lebel, Hélène; Marcoux, Jean-François; Molinaro, Carmela Chemical Reviews, Vol. 103, Issue 4 https://doi.org/10.1021/cr010007e	journal	April 2003
Structure and Chemistry of Cytochrome P450 Denisov, Ilia G.; Makris, Thomas M.; Sligar, Stephen G. Chemical Reviews, Vol. 105, Issue 6 https://doi.org/10.1021/cr0307143	journal	June 2005
Enzymatic Fluorination and Biotechnological Developments of the Fluorinase O’Hagan, David; Deng, Hai Chemical Reviews, Vol. 115, Issue 2 https://doi.org/10.1021/cr500209t	journal	August 2014
Hydrocarbon Hydroxylation by Cytochrome P450 Enzymes Ortiz de Montellano, Paul R. Chemical Reviews, Vol. 110, Issue 2 https://doi.org/10.1021/cr9002193	journal	February 2010
Tuning P450 Enzymes as Oxidation Catalysts Fasan, Rudi ACS Catalysis, Vol. 2, Issue 4 https://doi.org/10.1021/cs300001x	journal	March 2012
P450-Catalyzed Intramolecular sp ³ C–H Amination with Arylsulfonyl Azide Substrates Singh, Ritesh; Bordeaux, Melanie; Fasan, Rudi ACS Catalysis, Vol. 4, Issue 2 https://doi.org/10.1021/cs400893n	journal	December 2013
Enzymatic C(sp ³ )-H Amination: P450-Catalyzed Conversion of Carbonazidates into Oxazolidinones Singh, Ritesh; Kolev, Joshua N.; Sutera, Philip A. ACS Catalysis, Vol. 5, Issue 3 https://doi.org/10.1021/cs5018612	journal	February 2015
Functionalized nitrogen atom transfer catalyzed by cytochrome P-450 Svastits, Edmund W.; Dawson, John H.; Breslow, Ronald Journal of the American Chemical Society, Vol. 107, Issue 22 https://doi.org/10.1021/ja00308a064	journal	October 1985
Regio- and Enantioselective Alkane Hydroxylation with Engineered Cytochromes P450 BM-3 Peters, Matthew W.; Meinhold, Peter; Glieder, Anton Journal of the American Chemical Society, Vol. 125, Issue 44, p. 13442-13450 https://doi.org/10.1021/ja0303790	journal	November 2003
Enantioselective α-Hydroxylation of 2-Arylacetic Acid Derivatives and Buspirone Catalyzed by Engineered Cytochrome P450 BM-3 Landwehr, Marco; Hochrein, Lisa; Otey, Christopher R. Journal of the American Chemical Society, Vol. 128, Issue 18 https://doi.org/10.1021/ja061261x	journal	May 2006
Controlled Oxidation of Remote sp ³ C–H Bonds in Artemisinin via P450 Catalysts with Fine-Tuned Regio- and Stereoselectivity Zhang, Kaidong; Shafer, Brian M.; Demars, Matthew D. Journal of the American Chemical Society, Vol. 134, Issue 45 https://doi.org/10.1021/ja3073462	journal	November 2012
Laboratory Evolution of Enantiocomplementary Candida antarctica Lipase B Mutants with Broad Substrate Scope Wu, Qi; Soni, Pankaj; Reetz, Manfred T. Journal of the American Chemical Society, Vol. 135, Issue 5 https://doi.org/10.1021/ja310455t	journal	January 2013
Biocatalysis in Organic Chemistry and Biotechnology: Past, Present, and Future Reetz, Manfred T. Journal of the American Chemical Society, Vol. 135, Issue 34 https://doi.org/10.1021/ja405051f	journal	August 2013
Enzyme-Controlled Nitrogen-Atom Transfer Enables Regiodivergent C–H Amination Hyster, Todd K.; Farwell, Christopher C.; Buller, Andrew R. Journal of the American Chemical Society, Vol. 136, Issue 44 https://doi.org/10.1021/ja509308v	journal	October 2014
Catalytic and Biocatalytic Iron Porphyrin Carbene Formation: Effects of Binding Mode, Carbene Substituent, Porphyrin Substituent, and Protein Axial Ligand Khade, Rahul L.; Zhang, Yong Journal of the American Chemical Society, Vol. 137, Issue 24 https://doi.org/10.1021/jacs.5b03437	journal	June 2015
Computation Sheds Insight into Iron Porphyrin Carbenes’ Electronic Structure, Formation, and N–H Insertion Reactivity Sharon, Dina A.; Mallick, Dibyendu; Wang, Binju Journal of the American Chemical Society, Vol. 138, Issue 30 https://doi.org/10.1021/jacs.6b04636	journal	July 2016
Identification of Mechanism-Based Inactivation in P450-Catalyzed Cyclopropanation Facilitates Engineering of Improved Enzymes Renata, Hans; Lewis, Russell D.; Sweredoski, Michael J. Journal of the American Chemical Society, Vol. 138, Issue 38 https://doi.org/10.1021/jacs.6b06823	journal	September 2016
Highly Diastereo- and Enantioselective Synthesis of Trifluoromethyl-Substituted Cyclopropanes via Myoglobin-Catalyzed Transfer of Trifluoromethylcarbene Tinoco, Antonio; Steck, Viktoria; Tyagi, Vikas Journal of the American Chemical Society, Vol. 139, Issue 15 https://doi.org/10.1021/jacs.7b00768	journal	April 2017
Chemoenzymatic Total Synthesis and Structural Diversification of Tylactone-Based Macrolide Antibiotics through Late-Stage Polyketide Assembly, Tailoring, and C—H Functionalization Lowell, Andrew N.; DeMars, Matthew D.; Slocum, Samuel T. Journal of the American Chemical Society, Vol. 139, Issue 23 https://doi.org/10.1021/jacs.7b02875	journal	June 2017
Enantioselective Total Synthesis of Nigelladine A via Late-Stage C–H Oxidation Enabled by an Engineered P450 Enzyme Loskot, Steven A.; Romney, David K.; Arnold, Frances H. Journal of the American Chemical Society, Vol. 139, Issue 30 https://doi.org/10.1021/jacs.7b05196	journal	July 2017
Cyclopropanations via Heme Carbenes: Basic Mechanism and Effects of Carbene Substituent, Protein Axial Ligand, and Porphyrin Substitution Wei, Yang; Tinoco, Antonio; Steck, Viktoria Journal of the American Chemical Society, Vol. 140, Issue 5 https://doi.org/10.1021/jacs.7b09171	journal	December 2017
Unprecedented Cyclization Catalyzed by a Cytochrome P450 in Benzastatin Biosynthesis Tsutsumi, Hayama; Katsuyama, Yohei; Izumikawa, Miho Journal of the American Chemical Society, Vol. 140, Issue 21 https://doi.org/10.1021/jacs.8b02769	journal	May 2018
Identification of Critical Residues in Novel Drug Metabolizing Mutants of Cytochrome P450 BM3 Using Random Mutagenesis van Vugt-Lussenburg, Barbara M. A.; Stjernschantz, Eva; Lastdrager, Jeroen Journal of Medicinal Chemistry, Vol. 50, Issue 3 https://doi.org/10.1021/jm0609061	journal	January 2007
Enantiodivergent, Biocatalytic Routes to Both Taxol Side Chain Antipodes Feske, Brent D.; Kaluzna, Iwona A.; Stewart, Jon D. The Journal of Organic Chemistry, Vol. 70, Issue 23 https://doi.org/10.1021/jo0516077	journal	November 2005
Development of an NADPH-Dependent Homophenylalanine Dehydrogenase by Protein Engineering Li, Han; Liao, James C. ACS Synthetic Biology, Vol. 3, Issue 1 https://doi.org/10.1021/sb400093x	journal	September 2013
Laboratory evolution of peroxide-mediated cytochrome P450 hydroxylation Joo, Hyun; Lin, Zhanglin; Arnold, Frances H. Nature, Vol. 399, Issue 6737 https://doi.org/10.1038/21395	journal	June 1999
Natural Selection and the Concept of a Protein Space Maynard Smith, John Nature, Vol. 225, Issue 5232 https://doi.org/10.1038/225563a0	journal	February 1970
Rapid evolution of a protein in vitro by DNA shuffling Stemmer, Willem P. C. Nature, Vol. 370, Issue 6488 https://doi.org/10.1038/370389a0	journal	August 1994
Industrial research: Drug companies must adopt green chemistry Tucker, John L.; Faul, Margaret M. Nature, Vol. 534, Issue 7605 https://doi.org/10.1038/534027a	journal	May 2016
Engineering the third wave of biocatalysis Bornscheuer, U. T.; Huisman, G. W.; Kazlauskas, R. J. Nature, Vol. 485, Issue 7397 https://doi.org/10.1038/nature11117	journal	May 2012
Abiological catalysis by artificial haem proteins containing noble metals in place of iron Key, Hanna M.; Dydio, Paweł; Clark, Douglas S. Nature, Vol. 534, Issue 7608 https://doi.org/10.1038/nature17968	journal	June 2016
Genetically programmed chiral organoborane synthesis Kan, S. B. Jennifer; Huang, Xiongyi; Gumulya, Yosephine Nature, Vol. 552, Issue 7683 https://doi.org/10.1038/nature24996	journal	November 2017
Molecular evolution by staggered extension process (StEP) in vitro recombination Zhao, Huimin; Giver, Lori; Shao, Zhixin Nature Biotechnology, Vol. 16, Issue 3 https://doi.org/10.1038/nbt0398-258	journal	March 1998
Directed evolution of a para-nitrobenzyl esterase for aqueous-organic solvents Moore, Jeffrey C.; Arnold, Frances H. Nature Biotechnology, Vol. 14, Issue 4 https://doi.org/10.1038/nbt0496-458	journal	April 1996
A diverse family of thermostable cytochrome P450s created by recombination of stabilizing fragments Li, Yougen; Drummond, D. Allan; Sawayama, Andrew M. Nature Biotechnology, Vol. 25, Issue 9 https://doi.org/10.1038/nbt1333	journal	August 2007
Laboratory evolution of a soluble, self-sufficient, highly active alkane hydroxylase Glieder, Anton; Farinas, Edgardo T.; Arnold, Frances H. Nature Biotechnology, Vol. 20, Issue 11 https://doi.org/10.1038/nbt744	journal	October 2002
Enantioselective, intermolecular benzylic C–H amination catalysed by an engineered iron-haem enzyme Prier, Christopher K.; Zhang, Ruijie K.; Buller, Andrew R. Nature Chemistry, Vol. 9, Issue 7 https://doi.org/10.1038/nchem.2783	journal	May 2017
A serine-substituted P450 catalyzes highly efficient carbene transfer to olefins in vivo Coelho, Pedro S.; Wang, Z. Jane; Ener, Maraia E. Nature Chemical Biology, Vol. 9, Issue 8 https://doi.org/10.1038/nchembio.1278	journal	June 2013
Chemo-enzymatic fluorination of unactivated organic compounds Rentmeister, Andrea; Arnold, Frances H.; Fasan, Rudi Nature Chemical Biology, Vol. 5, Issue 1 https://doi.org/10.1038/nchembio.128	journal	November 2008
Highly active and selective endopeptidases with programmed substrate specificities Varadarajan, Navin; Rodriguez, Sarah; Hwang, Bum-Yeol Nature Chemical Biology, Vol. 4, Issue 5 https://doi.org/10.1038/nchembio.80	journal	March 2008
Cytochrome p450 enzymes in the generation of commercial products Guengerich, F. Peter Nature Reviews Drug Discovery, Vol. 1, Issue 5 https://doi.org/10.1038/nrd792	journal	May 2002
Protein building blocks preserved by recombination Voigt, Christopher A.; Martinez, Carlos; Wang, Zhen-Gang Nature Structural Biology https://doi.org/10.1038/nsb805	journal	June 2002
Enzymatic assembly of carbon–carbon bonds via iron-catalysed sp3 C–H functionalization Zhang, Ruijie K.; Chen, Kai; Huang, Xiongyi Nature, Vol. 565, Issue 7737 https://doi.org/10.1038/s41586-018-0808-5	journal	December 2018
Capture and characterization of a reactive haem–carbenoid complex in an artificial metalloenzyme Hayashi, Takahiro; Tinzl, Matthias; Mori, Takahiro Nature Catalysis, Vol. 1, Issue 8 https://doi.org/10.1038/s41929-018-0105-6	journal	July 2018
Structural Analysis of an Evolved Transketolase Reveals Divergent Binding Modes Affaticati, Pierre E.; Dai, Shao-Bo; Payongsri, Panwajee Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep35716	journal	October 2016
Variations on a (t)heme—novel mechanisms, redox partners and catalytic functions in the cytochrome P450 superfamily Munro, Andrew W.; Girvan, Hazel M.; McLean, Kirsty J. Nat. Prod. Rep., Vol. 24, Issue 3 https://doi.org/10.1039/B604190F	journal	January 2007
P450 _BM3 (CYP102A1): connecting the dots Whitehouse, Christopher J. C.; Bell, Stephen G.; Wong, Luet-Lok Chem. Soc. Rev., Vol. 41, Issue 3 https://doi.org/10.1039/C1CS15192D	journal	January 2012
Natural and engineered biosynthesis of fluorinated natural products Walker, Mark C.; Chang, Michelle C. Y. Chem. Soc. Rev., Vol. 43, Issue 18 https://doi.org/10.1039/C4CS00027G	journal	January 2014
P450-catalyzed asymmetric cyclopropanation of electron-deficient olefins under aerobic conditions Renata, Hans; Wang, Z. Jane; Kitto, Rebekah Z. Catal. Sci. Technol., Vol. 4, Issue 10 https://doi.org/10.1039/C4CY00633J	journal	January 2014
Intermolecular carbene S–H insertion catalysed by engineered myoglobin-based catalysts Tyagi, Vikas; Bonn, Rachel B.; Fasan, Rudi Chemical Science, Vol. 6, Issue 4 https://doi.org/10.1039/C5SC00080G	journal	January 2015
Recent advances in the synthesis of cyclopropanes Wu, Wanqing; Lin, Zhiming; Jiang, Huanfeng Organic & Biomolecular Chemistry, Vol. 16, Issue 40 https://doi.org/10.1039/C8OB01187G	journal	January 2018
Engineering the substrate specificity of Bacillus megaterium cytochrome P-450 BM3: hydroxylation of alkyl trimethylammonium compounds Oliver, F. Catherine; Modi, Sandeep; Primrose, U. William Biochemical Journal, Vol. 327, Issue 2 https://doi.org/10.1042/bj3270537	journal	October 1997
Roles of key active-site residues in flavocytochrome P450 BM3 Noble, Michael A.; Miles, Caroline S.; Chapman, Stephen K. Biochemical Journal, Vol. 339, Issue 2 https://doi.org/10.1042/bj3390371	journal	April 1999
Engineered Cytochrome c-Catalyzed Lactone-Carbene B–H Insertion Chen, Kai; Huang, Xiongyi; Zhang, Shuo-Qing Synlett, Vol. 30, Issue 04 https://doi.org/10.1055/s-0037-1611662	journal	January 2019
On the conservative nature of intragenic recombination Drummond, D. A.; Silberg, J. J.; Meyer, M. M. Proceedings of the National Academy of Sciences, Vol. 102, Issue 15 https://doi.org/10.1073/pnas.0500729102	journal	April 2005
Protein stability promotes evolvability Bloom, J. D.; Labthavikul, S. T.; Otey, C. R. Proceedings of the National Academy of Sciences, Vol. 103, Issue 15, p. 5869-5874 https://doi.org/10.1073/pnas.0510098103	journal	March 2006
A family of thermostable fungal cellulases created by structure-guided recombination Heinzelman, P.; Snow, C. D.; Wu, I. Proceedings of the National Academy of Sciences, Vol. 106, Issue 14, p. 5610-5615 https://doi.org/10.1073/pnas.0901417106	journal	March 2009
In the light of directed evolution: Pathways of adaptive protein evolution Bloom, J. D.; Arnold, F. H. Proceedings of the National Academy of Sciences, Vol. 106, Issue Supplement_1 https://doi.org/10.1073/pnas.0901522106	journal	June 2009
Chemoenzymatic elaboration of monosaccharides using engineered cytochrome P450_BM3 demethylases Lewis, J. C.; Bastian, S.; Bennett, C. S. Proceedings of the National Academy of Sciences, Vol. 106, Issue 39, p. 16550-16555 https://doi.org/10.1073/pnas.0908954106	journal	September 2009
Catalytic iron-carbene intermediate revealed in a cytochrome c carbene transferase Lewis, Russell D.; Garcia-Borràs, Marc; Chalkley, Matthew J. Proceedings of the National Academy of Sciences, Vol. 115, Issue 28 https://doi.org/10.1073/pnas.1807027115	journal	June 2018
Tuning the activity of an enzyme for unusual environments: sequential random mutagenesis of subtilisin E for catalysis in dimethylformamide. Chen, K.; Arnold, F. H. Proceedings of the National Academy of Sciences, Vol. 90, Issue 12 https://doi.org/10.1073/pnas.90.12.5618	journal	June 1993
DNA shuffling by random fragmentation and reassembly: in vitro recombination for molecular evolution. Stemmer, W. P. Proceedings of the National Academy of Sciences, Vol. 91, Issue 22 https://doi.org/10.1073/pnas.91.22.10747	journal	October 1994
Exploring the active site of chorismate mutase by combinatorial mutagenesis and selection: the importance of electrostatic catalysis. Kast, P.; Asif-Ullah, M.; Jiang, N. Proceedings of the National Academy of Sciences, Vol. 93, Issue 10 https://doi.org/10.1073/pnas.93.10.5043	journal	May 1996
Directed evolution of a thermostable esterase Giver, L.; Gershenson, A.; Freskgard, P.-O. Proceedings of the National Academy of Sciences, Vol. 95, Issue 22, p. 12809-12813 https://doi.org/10.1073/pnas.95.22.12809	journal	October 1998
Engineering a Mineralocorticoid- to a Glucocorticoid-synthesizing Cytochrome P450 Böttner, Benjamin; Schrauber, Hannelore; Bernhardt, Rita Journal of Biological Chemistry, Vol. 271, Issue 14 https://doi.org/10.1074/jbc.271.14.8028	journal	April 1996
Diversification and Specialization of HIV Protease Function During In Vitro Evolution O'Loughlin, T. L. Molecular Biology and Evolution, Vol. 23, Issue 4 https://doi.org/10.1093/molbev/msj098	journal	February 2006
Optimization of DNA shuffling for high fidelity recombination Zhao, H. Nucleic Acids Research, Vol. 25, Issue 6 https://doi.org/10.1093/nar/25.6.1307	journal	March 1997
Random-priming in vitro recombination: An effective tool for directed evolution Shao, Z.; Zhao, H.; Giver, L. Nucleic Acids Research, Vol. 26, Issue 2 https://doi.org/10.1093/nar/26.2.681	journal	January 1998
Directed evolution converts subtilisin E into a functional equivalent of thermitase Zhao, Huimin; Arnold, Frances H. Protein Engineering, Design and Selection, Vol. 12, Issue 1 https://doi.org/10.1093/protein/12.1.47	journal	January 1999
Protein engineering of cytochrome P450cam (CYP101) for the oxidation of polycyclic aromatic hydrocarbons Harford-Cross, Charles F.; Carmichael, Angus B.; Allan, Fiona K. Protein Engineering, Design and Selection, Vol. 13, Issue 2 https://doi.org/10.1093/protein/13.2.121	journal	February 2000
Characterization of His-X ₃ -His sites in α-helices of synthetic metal-binding bovine somatotropin Suh, Sung-Sup; Haymore, Barry L.; Arnold, Frances H. "Protein Engineering, Design and Selection", Vol. 4, Issue 3 https://doi.org/10.1093/protein/4.3.301	journal	January 1991
How Proteins Adapt: Lessons from Directed Evolution Arnold, F. H. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 74, Issue 0 https://doi.org/10.1101/sqb.2009.74.046	journal	January 2009
Biocatalytic Asymmetric Synthesis of Chiral Amines from Ketones Applied to Sitagliptin Manufacture Savile, C. K.; Janey, J. M.; Mundorff, E. C. Science, Vol. 329, Issue 5989 https://doi.org/10.1126/science.1188934	journal	June 2010
Cytochrome P450 Compound I: Capture, Characterization, and C-H Bond Activation Kinetics Rittle, J.; Green, M. T. Science, Vol. 330, Issue 6006 https://doi.org/10.1126/science.1193478	journal	November 2010
Olefin Cyclopropanation via Carbene Transfer Catalyzed by Engineered Cytochrome P450 Enzymes Coelho, P. S.; Brustad, E. M.; Kannan, A. Science, Vol. 339, Issue 6117 https://doi.org/10.1126/science.1231434	journal	December 2012
Engineered metal-binding proteins: purification to protein folding Arnold, F.; Haymore, B. Science, Vol. 252, Issue 5014 https://doi.org/10.1126/science.1648261	journal	June 1991
Directed evolution of cytochrome c for carbon–silicon bond formation: Bringing silicon to life Kan, S. B. Jennifer; Lewis, Russell D.; Chen, Kai Science, Vol. 354, Issue 6315 https://doi.org/10.1126/science.aah6219	journal	November 2016
Mechanochemical unzipping of insulating polyladderene to semiconducting polyacetylene Chen, Zhixing; Mercer, Jaron A. M.; Zhu, Xiaolei Science, Vol. 357, Issue 6350 https://doi.org/10.1126/science.aan2797	journal	August 2017
Enzymatic construction of highly strained carbocycles Chen, Kai; Huang, Xiongyi; Kan, S. B. Jennifer Science, Vol. 360, Issue 6384 https://doi.org/10.1126/science.aar4239	journal	April 2018
Site-selective enzymatic C‒H amidation for synthesis of diverse lactams Cho, Inha; Jia, Zhi-Jun; Arnold, Frances H. Science, Vol. 364, Issue 6440 https://doi.org/10.1126/science.aaw9068	journal	May 2019
Structural Aspects of Ligand Binding to and Electron Transfer in Bacterial and Fungal P450s Pylypenko, Olena; Schlichting, Ilme Annual Review of Biochemistry, Vol. 73, Issue 1 https://doi.org/10.1146/annurev.biochem.73.011303.073711	journal	June 2004
A Versatile High Throughput Screen for Dioxygenase Activity Using Solid-Phase Digital Imaging Joern, John M.; Sakamoto, Takeshi; Arisawa, Akira Journal of Biomolecular Screening, Vol. 6, Issue 4 https://doi.org/10.1177/108705710100600403	journal	August 2001
Neutral genetic drift can alter promiscuous protein functions, potentially aiding functional evolution Bloom, Jesse D.; Romero, Philip A.; Lu, Zhongyi Biology Direct, Vol. 2, Issue 1 https://doi.org/10.1186/1745-6150-2-17	journal	January 2007
Evolutionary molecular engineering based on RNA replication Eigen, M.; Gardiner, William Pure and Applied Chemistry, Vol. 56, Issue 8 https://doi.org/10.1351/pac198456080967	journal	January 1984
Structure-Guided Recombination Creates an Artificial Family of Cytochromes P450 Otey, Christopher R.; Landwehr, Marco; Endelman, Jeffrey B. PLoS Biology, Vol. 4, Issue 5 https://doi.org/10.1371/journal.pbio.0040112	journal	April 2006
Conventional and Novel Approaches in Generating and Characterization of Reactive Intermediates from Drugs/Drug Candidates Orhan, Hilmi; P. E. Vermeulen, Nico Current Drug Metabolism, Vol. 12, Issue 4 https://doi.org/10.2174/138920011795202974	journal	May 2011

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Advances in ultrahigh-throughput screening for directed enzyme evolution Markel, Ulrich; Essani, Khalil D.; Besirlioglu, Volkan Chemical Society Reviews, Vol. 49, Issue 1 https://doi.org/10.1039/c8cs00981c	journal	January 2020

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37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
C-H functionalization
P450s
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enzyme engineering
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A Continuing Career in Biocatalysis: Frances H. Arnold

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