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.

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

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

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

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

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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

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