Photoenzymatic Reductions Enabled by Direct Excitation of Flavin-Dependent “Ene”-Reductases

Sandoval, Braddock A.; Clayman, Phillip D.; Oblinsky, Daniel G.; Oh, Seokjoon; Nakano, Yuji; Bird, Matthew; Scholes, Gregory D.; Hyster, Todd K.

doi:10.1021/jacs.0c11494

Photoenzymatic Reductions Enabled by Direct Excitation of Flavin-Dependent “Ene”-Reductases

Journal Article · Wed Dec 30 23:00:00 EST 2020 · Journal of the American Chemical Society

DOI:https://doi.org/10.1021/jacs.0c11494· OSTI ID:1756851

Sandoval, Braddock A. ^[1]; Clayman, Phillip D. ^[2]; ^[2]; ^[3]; Nakano, Yuji ^[2]; ^[3]; ^[2]; ^[2]

Princeton Univ., NJ (United States); Princeton University
Princeton Univ., NJ (United States)
Brookhaven National Lab. (BNL), Upton, NY (United States)

Non-natural photoenzymatic reactions reported to date have depended on the excitation of electron donor–acceptor complexes formed between substrates and cofactors within protein active sites to facilitate electron transfer. While this mechanism has unlocked new reactivity, it limits the types of substrates that can be involved in this area of catalysis. Here we demonstrate that direct excitation of flavin hydroquinone within “ene”-reductase active sites enables new substrates to participate in photoenzymatic reactions. Here, we found that by using photoexcitation these enzymes gain the ability to reduce acrylamides through a single electron transfer mechanism

View Accepted Manuscript (DOE)

Research Organization:: Princeton Univ., NJ (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0019370

OSTI ID:: 1756851

Alternate ID(s):: OSTI ID: 1756853

Journal Information:: Journal of the American Chemical Society, Journal Name: Journal of the American Chemical Society Journal Issue: 4 Vol. 143; ISSN 0002-7863

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (37)

Photoenzymatic Catalysis Enables Radical‐Mediated Ketone Reduction in Ene‐Reductases Sandoval, Braddock A.; Kurtoic, Sarah I.; Chung, Megan M. Angewandte Chemie International Edition, Vol. 58, Issue 26 https://doi.org/10.1002/anie.201902005	journal	June 2019
Photoenzymatic Hydrogenation of Heteroaromatic Olefins Using ‘Ene’‐Reductases with Photoredox Catalysts Nakano, Yuji; Black, Michael J.; Meichan, Andrew J. Angewandte Chemie International Edition, Vol. 59, Issue 26 https://doi.org/10.1002/anie.202003125	journal	April 2020
Biocatalytic Reductions and Chemical Versatility of the Old Yellow Enzyme Family of Flavoprotein Oxidoreductases Toogood, Helen S.; Gardiner, John M.; Scrutton, Nigel S. ChemCatChem, Vol. 2, Issue 8 https://doi.org/10.1002/cctc.201000094	journal	June 2010
The Organic-Synthetic Potential of Recombinant Ene Reductases: Substrate-Scope Evaluation and Process Optimization Reß, Tina; Hummel, Werner; Hanlon, Steven P. ChemCatChem, Vol. 7, Issue 8 https://doi.org/10.1002/cctc.201402903	journal	March 2015
Asymmetric reduction of activated alkenes using an enoate reductase from Gluconobacter oxydans Richter, Nina; Gröger, Harald; Hummel, Werner Applied Microbiology and Biotechnology, Vol. 89, Issue 1 https://doi.org/10.1007/s00253-010-2793-y	journal	August 2010
Water oxidation in photosystem II Lubitz, Wolfgang; Chrysina, Maria; Cox, Nicholas Photosynthesis Research, Vol. 142, Issue 1 https://doi.org/10.1007/s11120-019-00648-3	journal	June 2019
Potentiometric studies of native and flavin-substituted Old Yellow Enzyme. Stewart, R. C.; Massey, V. Journal of Biological Chemistry, Vol. 260, Issue 25 https://doi.org/10.1016/S0021-9258(17)38773-2	journal	November 1985
Applications of protein engineering to members of the old yellow enzyme family Amato, Erica D.; Stewart, Jon D. Biotechnology Advances, Vol. 33, Issue 5 https://doi.org/10.1016/j.biotechadv.2015.04.011	journal	September 2015
Emerging strategies for expanding the toolbox of enzymes in biocatalysis Sandoval, Braddock A.; Hyster, Todd K. Current Opinion in Chemical Biology, Vol. 55 https://doi.org/10.1016/j.cbpa.2019.12.006	journal	April 2020
Electron hopping through proteins Warren, Jeffrey J.; Ener, Maraia E.; Vlček, Antonín Coordination Chemistry Reviews, Vol. 256, Issue 21-22 https://doi.org/10.1016/j.ccr.2012.03.032	journal	November 2012
Asymmetric bioreduction of activated alkenes to industrially relevant optically active compounds Winkler, Christoph K.; Tasnádi, Gábor; Clay, Dorina Journal of Biotechnology, Vol. 162, Issue 4 https://doi.org/10.1016/j.jbiotec.2012.03.023	journal	December 2012
Recent advances in photoinduced catalysis for water splitting and environmental applications Agbe, Henry; Nyankson, Emmanuel; Raza, Nadeem Journal of Industrial and Engineering Chemistry, Vol. 72 https://doi.org/10.1016/j.jiec.2019.01.004	journal	April 2019
Organic Photoredox Catalysis Romero, Nathan A.; Nicewicz, David A. Chemical Reviews, Vol. 116, Issue 17 https://doi.org/10.1021/acs.chemrev.6b00057	journal	June 2016
Fluorescence and optical characteristics of reduced flavines and flavoproteins Ghisla, Sandro; Massey, Vincent; Lhoste, Jean-Marc Biochemistry, Vol. 13, Issue 3 https://doi.org/10.1021/bi00700a029	journal	January 1974
Kinetics and Pathways of Charge Recombination in Photosystem II ^† Rappaport, Fabrice; Guergova-Kuras, Mariana; Nixon, Peter J. Biochemistry, Vol. 41, Issue 26 https://doi.org/10.1021/bi025725p	journal	July 2002
Synthetic Methods Driven by the Photoactivity of Electron Donor–Acceptor Complexes Crisenza, Giacomo E. M.; Mazzarella, Daniele; Melchiorre, Paolo Journal of the American Chemical Society, Vol. 142, Issue 12 https://doi.org/10.1021/jacs.0c01416	journal	March 2020
Photoenzymatic Generation of Unstabilized Alkyl Radicals: An Asymmetric Reductive Cyclization Clayman, Phillip D.; Hyster, Todd K. Journal of the American Chemical Society, Vol. 142, Issue 37 https://doi.org/10.1021/jacs.0c07918	journal	August 2020
Quantification and Theoretical Analysis of the Electrophilicities of Michael Acceptors Allgäuer, Dominik S.; Jangra, Harish; Asahara, Haruyasu Journal of the American Chemical Society, Vol. 139, Issue 38 https://doi.org/10.1021/jacs.7b05106	journal	September 2017
Enantioselective Hydrogen Atom Transfer: Discovery of Catalytic Promiscuity in Flavin-Dependent ‘Ene’-Reductases Sandoval, Braddock A.; Meichan, Andrew J.; Hyster, Todd K. Journal of the American Chemical Society, Vol. 139, Issue 33 https://doi.org/10.1021/jacs.7b05468	journal	August 2017
Selective Single C(sp ³ )–F Bond Cleavage in Trifluoromethylarenes: Merging Visible-Light Catalysis with Lewis Acid Activation Chen, Kang; Berg, Nele; Gschwind, Ruth Journal of the American Chemical Society, Vol. 139, Issue 51 https://doi.org/10.1021/jacs.7b10755	journal	December 2017
Catalytic Defluoroalkylation of Trifluoromethylaromatics with Unactivated Alkenes Wang, Hengbin; Jui, Nathan T. Journal of the American Chemical Society, Vol. 140, Issue 1 https://doi.org/10.1021/jacs.7b12590	journal	December 2017
Selective C–F Functionalization of Unactivated Trifluoromethylarenes Vogt, David B.; Seath, Ciaran P.; Wang, Hengbin Journal of the American Chemical Society, Vol. 141, Issue 33 https://doi.org/10.1021/jacs.9b06004	journal	August 2019
Enantioselective Intermolecular Excited-State Photoreactions Using a Chiral Ir Triplet Sensitizer: Separating Association from Energy Transfer in Asymmetric Photocatalysis Zheng, Jian; Swords, Wesley B.; Jung, Hoimin Journal of the American Chemical Society, Vol. 141, Issue 34 https://doi.org/10.1021/jacs.9b06244	journal	July 2019
Lewis Acid Catalyzed Enantioselective Photochemical Rearrangements on the Singlet Potential Energy Surface Leverenz, Malte; Merten, Christian; Dreuw, Andreas Journal of the American Chemical Society, Vol. 141, Issue 51 https://doi.org/10.1021/jacs.9b12068	journal	December 2019
Redox-photosensitized reactions. 11. Ru(bpy)32+-photosensitized reactions of 1-benzyl-1,4-dihydronicotinamide with aryl-substituted enones, derivatives of methyl cinnamate, and substituted cinnamonitriles: electron-transfer mechanism and structure-reactivity relationships Pac, Chyongjin; Miyauchi, Yoji; Ishitani, Osamu The Journal of Organic Chemistry, Vol. 49, Issue 1 https://doi.org/10.1021/jo00175a006	journal	January 1984
Accessing non-natural reactivity by irradiating nicotinamide-dependent enzymes with light Emmanuel, Megan A.; Greenberg, Norman R.; Oblinsky, Daniel G. Nature, Vol. 540, Issue 7633 https://doi.org/10.1038/nature20569	journal	December 2016
The molecular origin of high DNA-repair efficiency by photolyase Tan, Chuang; Liu, Zheyun; Li, Jiang Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms8302	journal	June 2015
Photovoltaic solar cell technologies: analysing the state of the art Nayak, Pabitra K.; Mahesh, Suhas; Snaith, Henry J. Nature Reviews Materials, Vol. 4, Issue 4 https://doi.org/10.1038/s41578-019-0097-0	journal	March 2019
Dynamics and mechanisms of DNA repair by photolyase Liu, Zheyun; Wang, Lijuan; Zhong, Dongping Physical Chemistry Chemical Physics, Vol. 17, Issue 18 https://doi.org/10.1039/C4CP05286B	journal	January 2015
The Oxidative Half-reaction of Old Yellow Enzyme Kohli, Rahul M.; Massey, Vincent Journal of Biological Chemistry, Vol. 273, Issue 49 https://doi.org/10.1074/jbc.273.49.32763	journal	December 1998
Photoenzymes and Related Topics: An Update Björn, Lars Olof Photochemistry and Photobiology, Vol. 94, Issue 3 https://doi.org/10.1111/php.12892	journal	March 2018
Enantioselective Lewis Acid Catalysis of Intramolecular Enone [2+2] Photocycloaddition Reactions Brimioulle, R.; Bach, T. Science, Vol. 342, Issue 6160 https://doi.org/10.1126/science.1244809	journal	November 2013
A Dual-Catalysis Approach to Enantioselective [2 + 2] Photocycloadditions Using Visible Light Du, J.; Skubi, K. L.; Schultz, D. M. Science, Vol. 344, Issue 6182 https://doi.org/10.1126/science.1251511	journal	April 2014
Enantioselective photochemistry through Lewis acid–catalyzed triplet energy transfer Blum, Travis R.; Miller, Zachary D.; Bates, Desiree M. Science, Vol. 354, Issue 6318 https://doi.org/10.1126/science.aai8228	journal	December 2016
An algal photoenzyme converts fatty acids to hydrocarbons Sorigué, Damien; Légeret, Bertrand; Cuiné, Stéphan Science, Vol. 357, Issue 6354 https://doi.org/10.1126/science.aan6349	journal	August 2017
Photoexcitation of flavoenzymes enables a stereoselective radical cyclization Biegasiewicz, Kyle F.; Cooper, Simon J.; Gao, Xin Science, Vol. 364, Issue 6446 https://doi.org/10.1126/science.aaw1143	journal	June 2019
Old Yellow Enzyme-Catalysed Asymmetric Hydrogenation: Linking Family Roots with Improved Catalysis Scholtissek, Anika; Tischler, Dirk; Westphal, Adrie Catalysts, Vol. 7, Issue 12 https://doi.org/10.3390/catal7050130	journal	April 2017

Similar Records

Quaternary Charge-Transfer Complex Enables Photoenzymatic Intermolecular Hydroalkylation of Olefins

Journal Article · Sun Dec 27 23:00:00 EST 2020 · Journal of the American Chemical Society · OSTI ID:1756844

Photoexcitation of flavoenzymes enables a stereoselective radical cyclization

Journal Article · Thu Jun 20 00:00:00 EDT 2019 · Science · OSTI ID:1528674

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Amides
Charge transfer
Flavins
Peptides and proteins
Transfer reactions

Photoenzymatic Reductions Enabled by Direct Excitation of Flavin-Dependent “Ene”-Reductases

Citation Formats

References (37)

Similar Records

Related Subjects