Active-Site Controlled, Jahn–Teller Enabled Regioselectivity in Reductive S–C Bond Cleavage of S -Adenosylmethionine in Radical SAM Enzymes

Impano, Stella; Yang, Hao; Jodts, Richard J.; Pagnier, Adrien; Swimley, Ryan; McDaniel, Elizabeth C.; Shepard, Eric M.; Broderick, William E.; Broderick, Joan B.; Hoffman, Brian M.

doi:10.1021/jacs.0c10925

Title: Active-Site Controlled, Jahn–Teller Enabled Regioselectivity in Reductive S–C Bond Cleavage of S -Adenosylmethionine in Radical SAM Enzymes

Journal Article · Tue Dec 29 00:00:00 EST 2020 · Journal of the American Chemical Society

DOI:https://doi.org/10.1021/jacs.0c10925· OSTI ID:1850937

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Department of Chemistry & Biochemistry, Montana State University, Bozeman, Montana 59717, United States
Department of Chemistry, Northwestern University, Evanston, Illinois 60208, United States

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Research Organization:: Montana State Univ., Bozeman, MT (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

DOE Contract Number:: SC0005404

OSTI ID:: 1850937

Journal Information:: Journal of the American Chemical Society, Vol. 143, Issue 1; ISSN 0002-7863

Publisher:: American Chemical Society (ACS)

Country of Publication:: United States

Language:: English

References (52)

The Radical SAM Superfamily Frey, Perry A.; Hegeman, Adrian D.; Ruzicka, Frank J. Critical Reviews in Biochemistry and Molecular Biology, Vol. 43, Issue 1 https://doi.org/10.1080/10409230701829169	journal	January 2008
Radical S -Adenosylmethionine Enzymes Broderick, Joan B.; Duffus, Benjamin R.; Duschene, Kaitlin S. Chemical Reviews, Vol. 114, Issue 8 https://doi.org/10.1021/cr4004709	journal	January 2014
Structure–function relationships of radical SAM enzymes Nicolet, Yvain Nature Catalysis, Vol. 3, Issue 4 https://doi.org/10.1038/s41929-020-0448-7	journal	April 2020
Radical S -Adenosylmethionine Enzymes in Human Health and Disease Landgraf, Bradley J.; McCarthy, Erin L.; Booker, Squire J. Annual Review of Biochemistry, Vol. 85, Issue 1 https://doi.org/10.1146/annurev-biochem-060713-035504	journal	June 2016
The [4Fe-4S] ¹⁺ Cluster of Pyruvate Formate-Lyase Activating Enzyme Generates the Glycyl Radical on Pyruvate Formate-Lyase: EPR-Detected Single Turnover Henshaw, Timothy F.; Cheek, Jennifer; Broderick, Joan B. Journal of the American Chemical Society, Vol. 122, Issue 34 https://doi.org/10.1021/ja002012q	journal	August 2000
S K-edge XAS and DFT Calculations on SAM Dependent Pyruvate Formate-Lyase Activating Enzyme: Nature of Interaction between the Fe ₄ S ₄ Cluster and SAM and its Role in Reactivity Dey, Abhishek; Peng, Yi; Broderick, William E. Journal of the American Chemical Society, Vol. 133, Issue 46 https://doi.org/10.1021/ja203780t	journal	November 2011
Coordination of Adenosylmethionine to a Unique Iron Site of the [4Fe-4S] of Pyruvate Formate-Lyase Activating Enzyme: A Mössbauer Spectroscopic Study Krebs, Carsten; Broderick, William E.; Henshaw, Timothy F. Journal of the American Chemical Society, Vol. 124, Issue 6, p. 912-913 https://doi.org/10.1021/ja017562i	journal	February 2002
Electron-Nuclear Double Resonance Spectroscopic Evidence That S -Adenosylmethionine Binds in Contact with the Catalytically Active [4Fe−4S] ⁺ Cluster of Pyruvate Formate-Lyase Activating Enzyme Walsby, Charles J.; Hong, Wei; Broderick, William E. Journal of the American Chemical Society, Vol. 124, Issue 12 https://doi.org/10.1021/ja012034s	journal	March 2002
An Anchoring Role for FeS Clusters: Chelation of the Amino Acid Moiety of S-Adenosylmethionine to the Unique Iron Site of the [4Fe−4S] Cluster of Pyruvate Formate-Lyase Activating Enzyme Walsby, Charles J.; Ortillo, Danilo; Broderick, William E. Journal of the American Chemical Society, Vol. 124, Issue 38 https://doi.org/10.1021/ja027078v	journal	September 2002
Radical SAM catalysis via an organometallic intermediate with an Fe-[5'-C]-deoxyadenosyl bond Horitani, M.; Shisler, K.; Broderick, W. E. Science, Vol. 352, Issue 6287 https://doi.org/10.1126/science.aaf5327	journal	May 2016
Paradigm Shift for Radical S -Adenosyl- l -methionine Reactions: The Organometallic Intermediate Ω Is Central to Catalysis Byer, Amanda S.; Yang, Hao; McDaniel, Elizabeth C. Journal of the American Chemical Society, Vol. 140, Issue 28 https://doi.org/10.1021/jacs.8b04061	journal	June 2018
An [Fe ₄ S ₄ ] ³⁺ –Alkyl Cluster Stabilized by an Expanded Scorpionate Ligand McSkimming, Alex; Sridharan, Arun; Thompson, Niklas B. Journal of the American Chemical Society, Vol. 142, Issue 33 https://doi.org/10.1021/jacs.0c06334	journal	July 2020
The role of S-adenosylmethionine in the lysine 2,3-aminomutase reaction. Moss, M.; Frey, P. A. Journal of Biological Chemistry, Vol. 262, Issue 31 https://doi.org/10.1016/S0021-9258(18)48103-3	journal	November 1987
Travels with Carbon-Centered Radicals. 5′-Deoxyadenosine and 5′-Deoxyadenosine-5′-yl in Radical Enzymology Frey, Perry A. Accounts of Chemical Research, Vol. 47, Issue 2 https://doi.org/10.1021/ar400194k	journal	December 2013
A Rich Man, Poor Man Story of S -Adenosylmethionine and Cobalamin Revisited Bridwell-Rabb, Jennifer; Grell, Tsehai A. J.; Drennan, Catherine L. Annual Review of Biochemistry, Vol. 87, Issue 1 https://doi.org/10.1146/annurev-biochem-062917-012500	journal	June 2018
Mechanism of Radical Initiation in the Radical S -Adenosyl- l -methionine Superfamily Broderick, William E.; Hoffman, Brian M.; Broderick, Joan B. Accounts of Chemical Research, Vol. 51, Issue 11 https://doi.org/10.1021/acs.accounts.8b00356	journal	October 2018
The Elusive 5′-Deoxyadenosyl Radical: Captured and Characterized by Electron Paramagnetic Resonance and Electron Nuclear Double Resonance Spectroscopies Yang, Hao; McDaniel, Elizabeth C.; Impano, Stella Journal of the American Chemical Society, Vol. 141, Issue 30 https://doi.org/10.1021/jacs.9b05926	journal	July 2019
Photoinduced Electron Transfer in a Radical SAM Enzyme Generates an S -Adenosylmethionine Derived Methyl Radical Yang, Hao; Impano, Stella; Shepard, Eric M. Journal of the American Chemical Society, Vol. 141, Issue 40 https://doi.org/10.1021/jacs.9b08541	journal	September 2019
Diphthamide biosynthesis requires an organic radical generated by an iron–sulphur enzyme Zhang, Yang; Zhu, Xuling; Torelli, Andrew T. Nature, Vol. 465, Issue 7300 https://doi.org/10.1038/nature09138	journal	June 2010
Direct FeS Cluster Involvement in Generation of a Radical in Lysine 2,3-Aminomutase ^† Cosper, Nathaniel J.; Booker, Squire J.; Ruzicka, Frank Biochemistry, Vol. 39, Issue 51 https://doi.org/10.1021/bi0022184	journal	December 2000
Coordination and Mechanism of Reversible Cleavage of S -Adenosylmethionine by the [4Fe-4S] Center in Lysine 2,3-Aminomutase Chen, Dawei; Walsby, Charles; Hoffman, Brian M. Journal of the American Chemical Society, Vol. 125, Issue 39 https://doi.org/10.1021/ja036120z	journal	October 2003
Binding Energy in the One-Electron Reductive Cleavage of S -Adenosylmethionine in Lysine 2,3-Aminomutase, a Radical SAM Enzyme ^† Wang, Susan C.; Frey, Perry A. Biochemistry, Vol. 46, Issue 45 https://doi.org/10.1021/bi701745h	journal	November 2007
S ‐Adenosyl‐ l ‐ethionine is a Catalytically Competent Analog of S ‐Adenosyl‐ l ‐methionine (SAM) in the Radical SAM Enzyme HydG Impano, Stella; Yang, Hao; Shepard, Eric M. Angewandte Chemie International Edition, Vol. 60, Issue 9 https://doi.org/10.1002/anie.202014337	journal	January 2021
[FeFe]-Hydrogenase Maturation: Insights into the Role HydE Plays in Dithiomethylamine Biosynthesis Betz, Jeremiah N.; Boswell, Nicholas W.; Fugate, Corey J. Biochemistry, Vol. 54, Issue 9 https://doi.org/10.1021/bi501205e	journal	March 2015
Pseudo-Jahn–Teller Effect—A Two-State Paradigm in Formation, Deformation, and Transformation of Molecular Systems and Solids Bersuker, Isaac B. Chemical Reviews, Vol. 113, Issue 3 https://doi.org/10.1021/cr300279n	journal	January 2013
EPR/ENDOR and Theoretical Study of the Jahn–Teller-Active [HIPTN ₃ N]Mo ^V L Complexes (L = N ^– , NH) Sharma, Ajay; Roemelt, Michael; Reithofer, Michael Inorganic Chemistry, Vol. 56, Issue 12 https://doi.org/10.1021/acs.inorgchem.7b00364	journal	May 2017
Experimental and Theoretical EPR Study of Jahn−Teller-Active [HIPTN ₃ N]MoL Complexes (L = N ₂ , CO, NH ₃ ) McNaughton, Rebecca L.; Roemelt, Michael; Chin, Jia Min Journal of the American Chemical Society, Vol. 132, Issue 25 https://doi.org/10.1021/ja1004619	journal	April 2010
The ORCA program system: The ORCA program system Neese, Frank Wiley Interdisciplinary Reviews: Computational Molecular Science, Vol. 2, Issue 1 https://doi.org/10.1002/wcms.81	journal	June 2011
Avogadro: an advanced semantic chemical editor, visualization, and analysis platform Hanwell, Marcus D.; Curtis, Donald E.; Lonie, David C. Journal of Cheminformatics, Vol. 4, Issue 1 https://doi.org/10.1186/1758-2946-4-17	journal	August 2012
Density-functional exchange-energy approximation with correct asymptotic behavior Becke, A. D. Physical Review A, Vol. 38, Issue 6 https://doi.org/10.1103/PhysRevA.38.3098	journal	September 1988
Density-functional approximation for the correlation energy of the inhomogeneous electron gas Perdew, John P. Physical Review B, Vol. 33, Issue 12 https://doi.org/10.1103/PhysRevB.33.8822	journal	June 1986
Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density Lee, Chengteh; Yang, Weitao; Parr, Robert G. Physical Review B, Vol. 37, Issue 2 https://doi.org/10.1103/PhysRevB.37.785	journal	January 1988
Fully optimized contracted Gaussian basis sets for atoms Li to Kr Schäfer, Ansgar; Horn, Hans; Ahlrichs, Reinhart The Journal of Chemical Physics, Vol. 97, Issue 4 https://doi.org/10.1063/1.463096	journal	August 1992
Structural insights into recognition and repair of UV-DNA damage by Spore Photoproduct Lyase, a radical SAM enzyme Benjdia, Alhosna; Heil, Korbinian; Barends, Thomas R. M. Nucleic Acids Research, Vol. 40, Issue 18 https://doi.org/10.1093/nar/gks603	journal	July 2012
Unexpected electron transfer mechanism upon AdoMet cleavage in radical SAM proteins Nicolet, Y.; Amara, P.; Mouesca, J. -M. Proceedings of the National Academy of Sciences, Vol. 106, Issue 35 https://doi.org/10.1073/pnas.0904385106	journal	August 2009
Structural Insights into Radical Generation by the Radical SAM Superfamily Vey, Jessica L.; Drennan, Catherine L. Chemical Reviews, Vol. 111, Issue 4 https://doi.org/10.1021/cr9002616	journal	March 2011
Structural basis for glycyl radical formation by pyruvate formate-lyase activating enzyme Vey, J. L.; Yang, J.; Li, M. Proceedings of the National Academy of Sciences, Vol. 105, Issue 42 https://doi.org/10.1073/pnas.0806640105	journal	October 2008
X-ray crystallographic and EPR spectroscopic analysis of HydG, a maturase in [FeFe]-hydrogenase H-cluster assembly Dinis, Pedro; Suess, Daniel L. M.; Fox, Stephen J. Proceedings of the National Academy of Sciences, Vol. 112, Issue 5 https://doi.org/10.1073/pnas.1417252112	journal	January 2015
The A and B conformations of DNA and RNA subunits. Potential energy calculations for dGpdC Broyde, Suse B.; Stellman, Steven D.; Wartell, Roger M. Biopolymers, Vol. 14, Issue 12 https://doi.org/10.1002/bip.1975.360141217	journal	December 1975
The x-ray crystal structure of lysine-2,3-aminomutase from Clostridium subterminale Lepore, B. W.; Ruzicka, F. J.; Frey, P. A. Proceedings of the National Academy of Sciences, Vol. 102, Issue 39 https://doi.org/10.1073/pnas.0505726102	journal	September 2005
Regioselectivity in the Homolytic Cleavage of S-Adenosylmethionine Kampmeier, Jack A. Biochemistry, Vol. 49, Issue 51 https://doi.org/10.1021/bi101509u	journal	December 2010
Analysis of Electrochemical Properties of S -Adenosyl- l -methionine and Implications for Its Role in Radical SAM Enzymes Miller, Sven A.; Bandarian, Vahe Journal of the American Chemical Society, Vol. 141, Issue 28 https://doi.org/10.1021/jacs.9b00933	journal	June 2019
Mechanism of one-electron electrochemical reductive cleavage reactions of sulfonium salts Saeva, Franklin D.; Morgan, Bradley P. Journal of the American Chemical Society, Vol. 106, Issue 15 https://doi.org/10.1021/ja00327a010	journal	July 1984
Photosensitized Reduction of Sulfonium Salts: Evidence for Nondissociative Electron Transfer Wang, Xiuzhi; Saeva, Franklin D.; Kampmeier, J. A. Journal of the American Chemical Society, Vol. 121, Issue 18 https://doi.org/10.1021/ja982932x	journal	April 1999
Visible-Light Photocatalytic Reduction of Sulfonium Salts as a Source of Aryl Radicals Donck, Simon; Baroudi, Abdulkader; Fensterbank, Louis Advanced Synthesis & Catalysis, Vol. 355, Issue 8 https://doi.org/10.1002/adsc.201300040	journal	May 2013
Second order Jahn–Teller interactions at unusually high molecular orbital energy separations Wedler, Henry B.; Wendelboe, Paul; Tantillo, Dean J. Dalton Transactions, Vol. 49, Issue 16 https://doi.org/10.1039/D0DT00137F	journal	January 2020
Vibronic origin of the H3O metastability Ogurtsov, Ivan; Gorinchoy, Natalia; Balan, Iolanta Journal of Molecular Structure, Vol. 838, Issue 1-3 https://doi.org/10.1016/j.molstruc.2007.01.065	journal	July 2007
Regioselectivity in the Reductive Bond Cleavage of Diarylalkylsulfonium Salts: Variation with Driving Force and Structure of Sulfuranyl Radical Intermediates Kampmeier, Jack A.; Hoque, AKM Mansurul; Saeva, Franklin D. Journal of the American Chemical Society, Vol. 131, Issue 29 https://doi.org/10.1021/ja809918k	journal	July 2009
EPR Study of the Low-Spin [d ³ ; S = ¹ / ₂ ], Jahn−Teller-Active, Dinitrogen Complex of a Molybdenum Trisamidoamine McNaughton, Rebecca L.; Chin, Jia Min; Weare, Walter W. Journal of the American Chemical Society, Vol. 129, Issue 12 https://doi.org/10.1021/ja068546u	journal	March 2007
Free H ₂ Rotation vs Jahn–Teller Constraints in the Nonclassical Trigonal (TPB)Co–H ₂ Complex Gunderson, William A.; Suess, Daniel L. M.; Fong, Henry Journal of the American Chemical Society, Vol. 136, Issue 42 https://doi.org/10.1021/ja508117h	journal	October 2014
X-ray Structure of the [FeFe]-Hydrogenase Maturase HydE from Thermotoga maritima Nicolet, Yvain; Rubach, Jon K.; Posewitz, Matthew C. Journal of Biological Chemistry, Vol. 283, Issue 27 https://doi.org/10.1074/jbc.M801161200	journal	April 2008
Carbon–sulfur bond-forming reaction catalysed by the radical SAM enzyme HydE Rohac, Roman; Amara, Patricia; Benjdia, Alhosna Nature Chemistry, Vol. 8, Issue 5 https://doi.org/10.1038/nchem.2490	journal	April 2016

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