Structural Basis for Superoxide Activation of Flavobacterium johnsoniae Class I Ribonucleotide Reductase and for Radical Initiation by Its Dimanganese Cofactor

Rose, Hannah R.; Ghosh, Manas K.; Maggiolo, Ailiena O.; Pollock, Christopher J.; Blaesi, Elizabeth J.; Hajj, Viviane; Wei, Yifeng; Rajakovich, Lauren J.; Chang, Wei-chen; Han, Yilin; Hajj, Mariana; Krebs, Carsten; Silakov, Alexey; Pandelia, Maria-Eirini; Bollinger, J. Martin; Boal, Amie K.

doi:10.1021/acs.biochem.8b00247

Structural Basis for Superoxide Activation of Flavobacterium johnsoniae Class I Ribonucleotide Reductase and for Radical Initiation by Its Dimanganese Cofactor

Journal Article · Mon Apr 02 00:00:00 EDT 2018 · Biochemistry

DOI:https://doi.org/10.1021/acs.biochem.8b00247· OSTI ID:1499749

Rose, Hannah R. ^[1]; Ghosh, Manas K. ^[1]; Maggiolo, Ailiena O. ^[1]; ^[1]; Blaesi, Elizabeth J. ^[1]; Hajj, Viviane ^[1]; Wei, Yifeng ^[2]; Rajakovich, Lauren J. ^[1]; ^[1]; Han, Yilin ^[1]; Hajj, Mariana ^[1]; ^[1]; ^[1]; Pandelia, Maria-Eirini ^[3]; ^[1]; ^[1]

Pennsylvania State Univ., University Park, PA (United States)
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Brandeis Univ., Waltham, MA (United States)

A ribonucleotide reductase (RNR) from Flavobacterium johnsoniae (Fj) differs fundamentally from known (subclass a–c) class I RNRs, warranting its assignment to a new subclass, Id. Its β subunit shares with Ib counterparts the requirements for manganese(II) and superoxide (O₂^–) for activation, but it does not require the O₂^–-supplying flavoprotein (NrdI) needed in Ib systems, instead scavenging the oxidant from solution. Although Fj β has tyrosine at the appropriate sequence position (Tyr 104), this residue is not oxidized to a radical upon activation, as occurs in the Ia/b proteins. Rather, Fj β directly deploys an oxidized dimanganese cofactor for radical initiation. In treatment with one-electron reductants, we note the cofactor can undergo cooperative three-electron reduction to the II/II state, in contrast to the quantitative univalent reduction to inactive “met” (III/III) forms seen with I(a–c) βs. This tendency makes Fj β unusually robust, as the II/II form can readily be reactivated. The structure of the protein rationalizes its distinctive traits. A distortion in a core helix of the ferritin-like architecture renders the active site unusually open, introduces a cavity near the cofactor, and positions a subclass-d-specific Lys residue to shepherd O₂^– to the Mn₂^II/II cluster. Relative to the positions of the radical tyrosines in the Ia/b proteins, the unreactive Tyr 104 of Fj β is held away from the cofactor by a hydrogen bond with a subclass-d-specific Thr residue. Structural comparisons, considered with its uniquely simple mode of activation, suggest that the Id protein might most closely resemble the primordial RNR-β.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS); SLAC National Accelerator Laboratory, Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS)

Sponsoring Organization:: Searle Scholars Program; National Institutes of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); National Institute of General Medical Sciences (NIGMS); Howard Hughes Medical Institute; National Cancer Institute (NCI); Michigan Economic Development Corporation and the Michigan Technology Tri-Corridor

Grant/Contract Number:: AC02-76SF00515; AC02-05CH11231; AC02-06CH11357

OSTI ID:: 1499749

Journal Information:: Biochemistry, Journal Name: Biochemistry Journal Issue: 18 Vol. 57; ISSN 0006-2960

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (81)

High-field EPR investigations of MnIIIMnIV and MnIIMnIII states of dimanganese catalase and related model systems Teutloff, Christian; Schäfer, Kai-Oliver; Sinnecker, Sebastian Magnetic Resonance in Chemistry, Vol. 43, Issue S1 https://doi.org/10.1002/mrc.1685	journal	January 2005
Structure and Function of the Escherichia coli Ribonucleotide Reductase Protein R2 Nordlund, Pär; Eklund, Hans Journal of Molecular Biology, Vol. 232, Issue 1 https://doi.org/10.1006/jmbi.1993.1374	journal	July 1993
EPR of Mn(II) Complexes with Enzymes and Other Proteins Reed, George H.; Markham, George D. Biological Magnetic Resonance https://doi.org/10.1007/978-1-4615-6546-8_3	book	January 1984
Automated Structure Solution with the PHENIX Suite Zwart, Peter H.; Afonine, Pavel V.; Grosse-Kunstleve, Ralf W. Methods in Molecular Biology https://doi.org/10.1007/978-1-60327-058-8_28	book	January 2008
Mixed Valence Manganese Carboxylates of Various Nuclearities Christou, G. Mixed Valency Systems: Applications in Chemistry, Physics and Biology https://doi.org/10.1007/978-94-011-3606-8_26	book	January 1991
Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria Cadenas, Enrique; Boveris, Alberto; Ragan, C. Ian Archives of Biochemistry and Biophysics, Vol. 180, Issue 2 https://doi.org/10.1016/0003-9861(77)90035-2	journal	April 1977
Molecular mechanisms of quinone cytotoxicity O'Brien, P. J. Chemico-Biological Interactions, Vol. 80, Issue 1 https://doi.org/10.1016/0009-2797(91)90029-7	journal	January 1991
Activation of molecular oxygen by flavins and flavoproteins. Massey, V. Journal of Biological Chemistry, Vol. 269, Issue 36 https://doi.org/10.1016/S0021-9258(17)31664-2	journal	September 1994
Iron and Free Radical in Ribonucleotide Reductase Atkin, Curtis L.; Thelander, Lars; Reichard, Peter Journal of Biological Chemistry, Vol. 248, Issue 21 https://doi.org/10.1016/S0021-9258(19)43313-9	journal	November 1973
On the mechanism of ribonucleoside diphosphate reductase from Escherichia coli. Evidence for 3'-C–H bond cleavage. Stubbe, J.; Ackles, D. Journal of Biological Chemistry, Vol. 255, Issue 17 https://doi.org/10.1016/S0021-9258(19)70598-5	journal	September 1980
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Ribonucleotide reductases: the link between an RNA and a DNA world? Stubbe, JoAnne Current Opinion in Structural Biology, Vol. 10, Issue 6 https://doi.org/10.1016/S0959-440X(00)00153-6	journal	December 2000
The Ferritin-like superfamily: Evolution of the biological iron storeman from a rubrerythrin-like ancestor Andrews, Simon C. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1800, Issue 8 https://doi.org/10.1016/j.bbagen.2010.05.010	journal	August 2010
Cyanobacterial alkane biosynthesis further expands the catalytic repertoire of the ferritin-like ‘di-iron-carboxylate’ proteins Krebs, Carsten; Bollinger, J. Martin; Booker, Squire J. Current Opinion in Chemical Biology, Vol. 15, Issue 2 https://doi.org/10.1016/j.cbpa.2011.02.019	journal	April 2011
Evolutionary Origin of a Secondary Structure: π-Helices as Cryptic but Widespread Insertional Variations of α-Helices That Enhance Protein Functionality Cooley, Richard B.; Arp, Daniel J.; Karplus, P. Andrew Journal of Molecular Biology, Vol. 404, Issue 2 https://doi.org/10.1016/j.jmb.2010.09.034	journal	November 2010
The manganese(IV)/iron(III) cofactor of Chlamydia trachomatis ribonucleotide reductase: structure, assembly, radical initiation, and evolution Bollinger, J. Martin; Jiang, Wei; Green, Michael T. Current Opinion in Structural Biology, Vol. 18, Issue 6 https://doi.org/10.1016/j.sbi.2008.11.007	journal	December 2008
Direct Measurement of the Radical Translocation Distance in the Class I Ribonucleotide Reductase from Chlamydia trachomatis Livada, Jovan; Martinie, Ryan J.; Dassama, Laura M. K. The Journal of Physical Chemistry B, Vol. 119, Issue 43 https://doi.org/10.1021/acs.jpcb.5b04067	journal	April 2015
Reversible, Long-Range Radical Transfer in E. coli Class Ia Ribonucleotide Reductase Minnihan, Ellen C.; Nocera, Daniel G.; Stubbe, JoAnne Accounts of Chemical Research, Vol. 46, Issue 11 https://doi.org/10.1021/ar4000407	journal	June 2013
The dimanganese(III,IV) oxidation state of catalase from Thermus thermophilus: electron nuclear double resonance analysis of water and protein ligands in the active site Khangulov, S.; Sivaraja, M.; Barynin, V. V. Biochemistry, Vol. 32, Issue 18 https://doi.org/10.1021/bi00069a028	journal	May 1993
Characterization of C439SR1, a mutant of Escherichia coli ribonucleotide diphosphate reductase: evidence that C439 is a residue essential for nucleotide reduction and C439SR1 is a protein possessing novel thioredoxin-like activity Mao, S. S.; Yu, G. X.; Chalfoun, D. Biochemistry, Vol. 31, Issue 40 https://doi.org/10.1021/bi00155a031	journal	October 1992
Chloroperoxidase compound I: electron paramagnetic resonance and Moessbauer studies Rutter, Rick; Hager, Lowell P.; Dhonau, Howard Biochemistry, Vol. 23, Issue 26 https://doi.org/10.1021/bi00321a082	journal	December 1984
Escherichia coli Class Ib Ribonucleotide Reductase Contains a Dimanganese(III)-Tyrosyl Radical Cofactor in Vivo Cotruvo, Joseph A.; Stubbe, JoAnne Biochemistry, Vol. 50, Issue 10 https://doi.org/10.1021/bi101881d	journal	March 2011
Structural Basis for Assembly of the Mn ^IV /Fe ^III Cofactor in the Class Ic Ribonucleotide Reductase from Chlamydia trachomatis Dassama, Laura M. K.; Krebs, Carsten; Bollinger, J. Martin Biochemistry, Vol. 52, Issue 37 https://doi.org/10.1021/bi400819x	journal	September 2013
A Manganese(IV)/Iron(IV) Intermediate in Assembly of the Manganese(IV)/Iron(III) Cofactor of Chlamydia trachomatis Ribonucleotide Reductase ^† Jiang, Wei; Hoffart, Lee M.; Krebs, Carsten Biochemistry, Vol. 46, Issue 30 https://doi.org/10.1021/bi700906g	journal	July 2007
Rapid and Quantitative Activation of Chlamydia trachomatis Ribonucleotide Reductase by Hydrogen Peroxide Jiang, Wei; Xie, Jiajia; Nørgaard, Hanne Biochemistry, Vol. 47, Issue 15 https://doi.org/10.1021/bi702085z	journal	March 2008
Branched Activation- and Catalysis-Specific Pathways for Electron Relay to the Manganese/Iron Cofactor in Ribonucleotide Reductase from Chlamydia trachomatis Jiang, Wei; Saleh, Lana; Barr, Eric W. Biochemistry, Vol. 47, Issue 33 https://doi.org/10.1021/bi800881m	journal	July 2008
Formation and Function of the Manganese(IV)/Iron(III) Cofactor in Chlamydia trachomatis Ribonucleotide Reductase Jiang, Wei; Yun, Danny; Saleh, Lana Biochemistry, Vol. 47, Issue 52 https://doi.org/10.1021/bi8017625	journal	December 2008
An Active Dimanganese(III)−Tyrosyl Radical Cofactor in Escherichia coli Class Ib Ribonucleotide Reductase Cotruvo, Joseph A.; Stubbe, JoAnne Biochemistry, Vol. 49, Issue 6 https://doi.org/10.1021/bi902106n	journal	February 2010
Structure of Salmonella typhimurium nrdF Ribonucleotide Reductase in Its Oxidized and Reduced Forms ^† ^, ^‡ Eriksson, Mathias; Jordan, Albert; Eklund, Hans Biochemistry, Vol. 37, Issue 38 https://doi.org/10.1021/bi981380s	journal	September 1998
Radical Initiation in the Class I Ribonucleotide Reductase: Long-Range Proton-Coupled Electron Transfer? Stubbe, JoAnne; Nocera, Daniel G.; Yee, Cyril S. Chemical Reviews, Vol. 103, Issue 6 https://doi.org/10.1021/cr020421u	journal	June 2003
Magnetic and Spectroscopic Properties of Mixed Valence Manganese(III,IV) Dimers: A Systematic Study Using Broken Symmetry Density Functional Theory Orio, Maylis; Pantazis, Dimitrios A.; Petrenko, Taras Inorganic Chemistry, Vol. 48, Issue 15 https://doi.org/10.1021/ic9005899	journal	July 2009
Mechanism of Assembly of the Tyrosyl Radical-Diiron(III) Cofactor of E. coli Ribonucleotide Reductase. 2. Kinetics of The Excess Fe2+ Reaction by Optical, EPR, and Moessbauer Spectroscopies Bollinger, J. Martin; Tong, Wing Hang; Ravi, Natarajan Journal of the American Chemical Society, Vol. 116, Issue 18 https://doi.org/10.1021/ja00097a008	journal	September 1994
Structural and Magnetic Effects of Successive Protonations of Oxo Bridges in High-Valent Manganese Dimers Baldwin, Michael J.; Stemmler, Timothy L.; Riggs-Gelasco, Pamela J. Journal of the American Chemical Society, Vol. 116, Issue 25 https://doi.org/10.1021/ja00104a014	journal	December 1994
Mechanism of Rapid Electron Transfer during Oxygen Activation in the R2 Subunit of Escherichia c oli Ribonucleotide Reductase. 1. Evidence for a Transient Tryptophan Radical Baldwin, Jeffrey; Krebs, Carsten; Ley, Brenda A. Journal of the American Chemical Society, Vol. 122, Issue 49 https://doi.org/10.1021/ja001278u	journal	December 2000
Reduction of the binuclear iron site in octameric methemerythrins. Characterizations of intermediates and a unifying reaction scheme Pearce, Linda L.; Kurtz, Donald M.; Xia, Yao Min Journal of the American Chemical Society, Vol. 109, Issue 24 https://doi.org/10.1021/ja00258a007	journal	November 1987
Mechanistic Implications for the Formation of the Diiron Cluster in Ribonucleotide Reductase Provided by Quantitative EPR Spectroscopy Pierce, Brad S.; Elgren, Timothy E.; Hendrich, Michael P. Journal of the American Chemical Society, Vol. 125, Issue 29 https://doi.org/10.1021/ja021290h	journal	July 2003
Pulsed ELDOR Spectroscopy Measures the Distance between the Two Tyrosyl Radicals in the R2 Subunit of the E. coli Ribonucleotide Reductase Bennati, Marina; Weber, Axel; Antonic, Jelena Journal of the American Chemical Society, Vol. 125, Issue 49 https://doi.org/10.1021/ja0362095	journal	December 2003
Variable Coordination Geometries at the Diiron(II) Active Site of Ribonucleotide Reductase R2 Voegtli, Walter C.; Sommerhalter, Monika; Saleh, Lana Journal of the American Chemical Society, Vol. 125, Issue 51 https://doi.org/10.1021/ja0370387	journal	December 2003
Structure of the Nitrogen-Centered Radical Formed during Inactivation of E. coli Ribonucleotide Reductase by 2‘-Azido-2‘-deoxyuridine-5‘-diphosphate: Trapping of the 3‘-Ketonucleotide Fritscher, Jörg; Artin, Erin; Wnuk, Stanislaw Journal of the American Chemical Society, Vol. 127, Issue 21 https://doi.org/10.1021/ja043111x	journal	June 2005
The Active Form of Chlamydia trachomatis Ribonucleotide Reductase R2 Protein Contains a Heterodinuclear Mn(IV)/Fe(III) Cluster with S = 1 Ground State Jiang, Wei; Bollinger,, J. Martin; Krebs, Carsten Journal of the American Chemical Society, Vol. 129, Issue 24 https://doi.org/10.1021/ja072528a	journal	May 2007
A Tyrosyl−Dimanganese Coupled Spin System is the Native Metalloradical Cofactor of the R2F Subunit of the Ribonucleotide Reductase of Corynebacterium ammoniagenes Cox, Nicholas; Ogata, Hideaki; Stolle, Patrick Journal of the American Chemical Society, Vol. 132, Issue 32 https://doi.org/10.1021/ja1036995	journal	August 2010
The Manganese Ion of the Heterodinuclear Mn/Fe Cofactor in Chlamydia trachomatis Ribonucleotide Reductase R2c Is Located at Metal Position 1 Andersson, Charlotta S.; Öhrström, Maria; Popović-Bijelić, Ana Journal of the American Chemical Society, Vol. 134, Issue 1 https://doi.org/10.1021/ja209678x	journal	December 2011
Evidence That the β Subunit of Chlamydia trachomatis Ribonucleotide Reductase Is Active with the Manganese Ion of Its Manganese(IV)/Iron(III) Cofactor in Site 1 Dassama, Laura M. K.; Boal, Amie K.; Krebs, Carsten Journal of the American Chemical Society, Vol. 134, Issue 5 https://doi.org/10.1021/ja211314p	journal	January 2012
Radical-Translocation Intermediates and Hurdling of Pathway Defects in “Super-oxidized” (Mn ^IV /Fe ^IV ) Chlamydia trachomatis Ribonucleotide Reductase Dassama, Laura M. K.; Jiang, Wei; Varano, Paul T. Journal of the American Chemical Society, Vol. 134, Issue 50 https://doi.org/10.1021/ja309468s	journal	December 2012
Mechanism of Assembly of the Dimanganese-Tyrosyl Radical Cofactor of Class Ib Ribonucleotide Reductase: Enzymatic Generation of Superoxide Is Required for Tyrosine Oxidation via a Mn(III)Mn(IV) Intermediate Cotruvo, Joseph A.; Stich, Troy A.; Britt, R. David Journal of the American Chemical Society, Vol. 135, Issue 10 https://doi.org/10.1021/ja312457t	journal	February 2013
Function of the Diiron Cluster of Escherichia coli Class Ia Ribonucleotide Reductase in Proton-Coupled Electron Transfer Wörsdörfer, Bigna; Conner, Denise A.; Yokoyama, Kenichi Journal of the American Chemical Society, Vol. 135, Issue 23 https://doi.org/10.1021/ja401342s	journal	May 2013
Rapid Freeze−Quench ENDOR of the Radical X Intermediate of Escherichia coli Ribonucleotide Reductase Using ¹⁷ O ₂ , H ₂ ¹⁷ O, and ² H ₂ O Burdi, Doug; Sturgeon, Bradley E.; Tong, Wing H. Journal of the American Chemical Society, Vol. 118, Issue 1 https://doi.org/10.1021/ja952651e	journal	January 1996
Mechanism of Assembly of the Diferric Cluster−Tyrosyl Radical Cofactor of Escherichia coli Ribonucleotide Reductase from the Diferrous Form of the R2 Subunit Tong, W. H.; Chen, S.; Lloyd, S. G. Journal of the American Chemical Society, Vol. 118, Issue 8 https://doi.org/10.1021/ja952764y	journal	January 1996
A Multiplet Analysis of Fe K-Edge 1s → 3d Pre-Edge Features of Iron Complexes Westre, Tami E.; Kennepohl, Pierre; DeWitt, Jane G. Journal of the American Chemical Society, Vol. 119, Issue 27 https://doi.org/10.1021/ja964352a	journal	July 1997
Composition and Structure of the Inorganic Core of Relaxed Intermediate X (Y122F) of Escherichia coli Ribonucleotide Reductase Doan, Peter E.; Shanmugam, Muralidharan; Stubbe, JoAnne Journal of the American Chemical Society, Vol. 137, Issue 49 https://doi.org/10.1021/jacs.5b10763	journal	December 2015
Evidence for a Di-μ-oxo Diamond Core in the Mn(IV)/Fe(IV) Activation Intermediate of Ribonucleotide Reductase from Chlamydia trachomatis Martinie, Ryan J.; Blaesi, Elizabeth J.; Krebs, Carsten Journal of the American Chemical Society, Vol. 139, Issue 5 https://doi.org/10.1021/jacs.6b11563	journal	January 2017
Three-dimensional structure of the free radical protein of ribonucleotide reductase Nordlund, Pär; Sjöberg, Britt-Marie; Eklund, Hans Nature, Vol. 345, Issue 6276 https://doi.org/10.1038/345593a0	journal	June 1990
Structure of ribonucleotide reductase protein R1 Uhlin, Ulla; Eklund, Hans Nature, Vol. 370, Issue 6490 https://doi.org/10.1038/370533a0	journal	August 1994
Theoretical magnetochemistry of dinuclear manganese complexes: broken symmetry density functional theory investigation on the influence of bridging motifs on structure and magnetism Pantazis, Dimitrios A.; Krewald, Vera; Orio, Maylis Dalton Transactions, Vol. 39, Issue 20 https://doi.org/10.1039/c001286f	journal	January 2010
Molecular dynamics using atomic-resolution structure reveal structural fluctuations that may lead to polymerization of human Cu Zn superoxide dismutase Strange, R. W.; Yong, C. W.; Smith, W. Proceedings of the National Academy of Sciences, Vol. 104, Issue 24 https://doi.org/10.1073/pnas.0703857104	journal	June 2007
A possible glycine radical in anaerobic ribonucleotide reductase from Escherichia coli: nucleotide sequence of the cloned nrdD gene. Sun, X.; Harder, J.; Krook, M. Proceedings of the National Academy of Sciences, Vol. 90, Issue 2 https://doi.org/10.1073/pnas.90.2.577	journal	January 1993
The Active Form of the R2F Protein of Class Ib Ribonucleotide Reductase from Corynebacterium ammoniagenes Is a Diferric Protein Huque, Yasmin; Fieschi, Franck; Torrents, Eduard Journal of Biological Chemistry, Vol. 275, Issue 33 https://doi.org/10.1074/jbc.M002751200	journal	May 2000
Cloning and Characterization of Ribonucleotide Reductase fromChlamydia trachomatis Roshick, Christine; Iliffe-Lee, Emma R.; McClarty, Grant Journal of Biological Chemistry, Vol. 275, Issue 48 https://doi.org/10.1074/jbc.M006367200	journal	December 2000
Use of Structural Phylogenetic Networks for Classification of the Ferritin-like Superfamily Lundin, Daniel; Poole, Anthony M.; Sjöberg, Britt-Marie Journal of Biological Chemistry, Vol. 287, Issue 24 https://doi.org/10.1074/jbc.M112.367458	journal	June 2012
ProtTest: selection of best-fit models of protein evolution Abascal, F.; Zardoya, R.; Posada, D. Bioinformatics, Vol. 21, Issue 9 https://doi.org/10.1093/bioinformatics/bti263	journal	January 2005
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods Sofia, H. J. Nucleic Acids Research, Vol. 29, Issue 5 https://doi.org/10.1093/nar/29.5.1097	journal	March 2001
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
Likelihood-enhanced fast translation functions McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Storoni, Laurent C. Acta Crystallographica Section D Biological Crystallography, Vol. 61, Issue 4 https://doi.org/10.1107/S0907444905001617	journal	March 2005
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Refinement of Macromolecular Structures by the Maximum-Likelihood Method Murshudov, G. N.; Vagin, A. A.; Dodson, E. J. Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3 https://doi.org/10.1107/S0907444996012255	journal	May 1997
Blueprint XAS : a Matlab -based toolbox for the fitting and analysis of XAS spectra Delgado-Jaime, Mario Ulises; Mewis, Craig Philip; Kennepohl, Pierre Journal of Synchrotron Radiation, Vol. 17, Issue 1 https://doi.org/10.1107/S0909049509046561	journal	December 2009
2'-Deoxy-2'-azidocytidine, a New Inhibitor of DNA Replication in Mammalian Cells Skoog, Lambert; Bjursell, Gunnar; Thelander, Lars European Journal of Biochemistry, Vol. 72, Issue 2 https://doi.org/10.1111/j.1432-1033.1977.tb11261.x	journal	January 1977
The Radical Site in Chlamydial Ribonucleotide Reductase Defines a New R2 Subclass Hogbom, M. Science, Vol. 305, Issue 5681 https://doi.org/10.1126/science.1098419	journal	July 2004
A Manganese(IV)/Iron(III) Cofactor in Chlamydia trachomatis Ribonucleotide Reductase Jiang, W.; Yun, D.; Saleh, L. Science, Vol. 316, Issue 5828 https://doi.org/10.1126/science.1141179	journal	May 2007
Structural Basis for Activation of Class Ib Ribonucleotide Reductase Boal, A. K.; Cotruvo, J. A.; Stubbe, J. Science, Vol. 329, Issue 5998 https://doi.org/10.1126/science.1190187	journal	August 2010
Mechanism of assembly of the tyrosyl radical-dinuclear iron cluster cofactor of ribonucleotide reductase Bollinger, J.; Edmondson, D.; Huynh, B. Science, Vol. 253, Issue 5017 https://doi.org/10.1126/science.1650033	journal	July 1991
Thiyl Radicals in Ribonucleotide Reductases Licht, S.; Gerfen, G. J.; Stubbe, J. Science, Vol. 271, Issue 5248 https://doi.org/10.1126/science.271.5248.477	journal	January 1996
From RNA to DNA, why so many ribonucleotide reductases? Reichard, P. Science, Vol. 260, Issue 5115 https://doi.org/10.1126/science.8511586	journal	June 1993
Novel Features of the Polysaccharide-Digesting Gliding Bacterium Flavobacterium johnsoniae as Revealed by Genome Sequence Analysis McBride, M. J.; Xie, G.; Martens, E. C. Applied and Environmental Microbiology, Vol. 75, Issue 21 https://doi.org/10.1128/AEM.01495-09	journal	August 2009
Cloning, overproduction, and purification of the B2 subunit of ribonucleoside-diphosphate reductase. Salowe, S. P.; Stubbe, J. Journal of Bacteriology, Vol. 165, Issue 2 https://doi.org/10.1128/jb.165.2.363-366.1986	journal	February 1986
Class I Ribonucleotide Reductases: Metallocofactor Assembly and Repair In Vitro and In Vivo Cotruvo, Joseph A.; Stubbe, JoAnne Annual Review of Biochemistry, Vol. 80, Issue 1 https://doi.org/10.1146/annurev-biochem-061408-095817	journal	July 2011
Ribonucleotide Reductases Nordlund, Pär; Reichard, Peter Annual Review of Biochemistry, Vol. 75, Issue 1 https://doi.org/10.1146/annurev.biochem.75.103004.142443	journal	June 2006
The Origin and Evolution of Ribonucleotide Reduction Lundin, Daniel; Berggren, Gustav; Logan, Derek Life, Vol. 5, Issue 1 https://doi.org/10.3390/life5010604	journal	February 2015
Novel ATP-cone-driven allosteric regulation of ribonucleotide reductase via the radical-generating subunit Rozman Grinberg, Inna; Lundin, Daniel; Hasan, Mahmudul eLife, Vol. 7 https://doi.org/10.7554/eLife.31529	journal	February 2018

Cited By (10)

Class Id ribonucleotide reductase utilizes a Mn2(IV,III) cofactor and undergoes large conformational changes on metal loading Rozman Grinberg, Inna; Berglund, Sigrid; Hasan, Mahmudul JBIC Journal of Biological Inorganic Chemistry, Vol. 24, Issue 6 https://doi.org/10.1007/s00775-019-01697-8	journal	August 2019
Metal-free class Ie ribonucleotide reductase from pathogens initiates catalysis with a tyrosine-derived dihydroxyphenylalanine radical Blaesi, Elizabeth J.; Palowitch, Gavin M.; Hu, Kai Proceedings of the National Academy of Sciences, Vol. 115, Issue 40 https://doi.org/10.1073/pnas.1811993115	journal	September 2018
Involvement of high-valent manganese-oxo intermediates in oxidation reactions: realisation in nature, nano and molecular systems Balamurugan, Mani; Saravanan, Natarajan; Ha, Heonjin Nano Convergence, Vol. 5, Issue 1 https://doi.org/10.1186/s40580-018-0150-5	journal	July 2018
Assembly of a heterodinuclear Mn/Fe cofactor is coupled to tyrosine–valine ether cross-link formation in the R2-like ligand-binding oxidase Griese, Julia J.; Kositzki, Ramona; Haumann, Michael JBIC Journal of Biological Inorganic Chemistry, Vol. 24, Issue 2 https://doi.org/10.1007/s00775-019-01639-4	journal	January 2019
Redox-induced structural changes in the di-iron and di-manganese forms of Bacillus anthracis ribonucleotide reductase subunit NrdF suggest a mechanism for gating of radical access Grāve, Kristīne; Lambert, Wietske; Berggren, Gustav JBIC Journal of Biological Inorganic Chemistry, Vol. 24, Issue 6 https://doi.org/10.1007/s00775-019-01703-z	journal	August 2019
A glutaredoxin domain fused to the radical-generating subunit of ribonucleotide reductase (RNR) functions as an efficient RNR reductant Rozman Grinberg, Inna; Lundin, Daniel; Sahlin, Margareta Journal of Biological Chemistry, Vol. 293, Issue 41 https://doi.org/10.1074/jbc.ra118.004991	journal	August 2018
Chemical flexibility of heterobimetallic Mn/Fe cofactors: R2lox and R2c proteins Kutin, Yury; Kositzki, Ramona; Branca, Rui M. M. Journal of Biological Chemistry, Vol. 294, Issue 48 https://doi.org/10.1074/jbc.ra119.010570	journal	October 2019
Assembly of a heterodinuclear Mn/Fe cofactor is coupled to tyrosine–valine ether cross-link formation in the R2-like ligand-binding oxidase Griese, Julia J.; Kositzki, Ramona; Haumann, Michael Freie Universität Berlin https://doi.org/10.17169/refubium-1663	text	January 2019
Class Id ribonucleotide reductase utilizes a Mn2(IV,III) cofactor and undergoes large conformational changes on metal loading Rozman Grinberg, Inna; Berglund, Sigrid; Hasan, Mahmudul Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2019-03523	text	January 2019
Reannotation of the Ribonucleotide Reductase in a Cyanophage Reveals Life History Strategies Within the Virioplankton Harrison, Amelia O.; Moore, Ryan M.; Polson, Shawn W. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00134	journal	February 2019

Similar Records

Structures of Class Id Ribonucleotide Reductase Catalytic Subunits Reveal a Minimal Architecture for Deoxynucleotide Biosynthesis

Journal Article · Mon Mar 11 00:00:00 EDT 2019 · Biochemistry · OSTI ID:1544859

Metal-free class Ie ribonucleotide reductase from pathogens initiates catalysis with a tyrosine-derived dihydroxyphenylalanine radical

Journal Article · Mon Sep 17 00:00:00 EDT 2018 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1499708

The Dimanganese(II) Site of Bacillus subtilis Class Ib Ribonucleotide Reductase

Journal Article · Thu Oct 02 00:00:00 EDT 2014 · Biochemistry-US · OSTI ID:1047906

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
Cluster chemistry
Electron paramagnetic resonance spectroscopy
Monomers
Peptides and proteins
Transition metals

Structural Basis for Superoxide Activation of Flavobacterium johnsoniae Class I Ribonucleotide Reductase and for Radical Initiation by Its Dimanganese Cofactor

Citation Formats

References (81)

Cited By (10)

Similar Records

Related Subjects