Class Ib Ribonucleotide Reductases: Activation of a Peroxido-Mn II Mn III to Generate a Reactive Oxo-Mn III Mn IV Oxidant
Abstract
In the postulated catalytic cycle of class Ib Mn2 ribonucleotide reductases (RNRs), a MnII2 core is suggested to react with superoxide (O2·–) to generate peroxido-MnIIMnIII and oxo-MnIIIMnIV entities prior to proton-coupled electron transfer (PCET) oxidation of tyrosine. There is limited experimental support for this mechanism. We demonstrate that [MnII2(BPMP)(OAc)2](ClO4) (1, HBPMP = 2,6-bis[(bis(2 pyridylmethyl)amino)methyl]-4-methylphenol) was converted to peroxido-MnIIMnIII (2) in the presence of superoxide anion that converted to (μ-O)(μ-OH)MnIIIMnIV (3) via the addition of an H+-donor (p-TsOH) or (μ-O)2MnIIIMnIV (4) upon warming to room temperature. The physical properties of 3 and 4 were probed using UV–vis, EPR, X-ray absorption, and IR spectroscopies and mass spectrometry. Compounds 3 and 4 were capable of phenol oxidation to yield a phenoxyl radical via a concerted PCET oxidation, supporting the proposed mechanism of tyrosyl radical cofactor generation in RNRs. The synthetic models demonstrate that the postulated O2/Mn2/tyrosine activation mechanism in class Ib Mn2 RNRs is plausible and provides spectral insights into intermediates currently elusive in the native enzyme.
- Authors:
-
[2];
[3];
[4];
[2];
[1]
- School of Chemistry, Trinity College Dublin, The University of Dublin, College Green, Dublin 2, Ireland
- Department of Chemistry and Centre for Metals in Biocatalysis, University of Minnesota, 207 Pleasant Street SE, Minneapolis, Minnesota 55455, United States
- Case Western Reserve University Center for Synchrotron Biosciences, National Synchrotron Light Source II, Brookhaven National Laboratory Upton, New York 11973, United States
- CNRS UMR 5250, DCM, Univ. Grenoble Alpes, Grenoble F-38000, France
- Publication Date:
- Research Org.:
- University of Dublin (Ireland)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 2281632
- Alternate Identifier(s):
- OSTI ID: 2283147
- Grant/Contract Number:
- AC02-76SF00515
- Resource Type:
- Published Article
- Journal Name:
- Inorganic Chemistry
- Additional Journal Information:
- Journal Name: Inorganic Chemistry Journal Volume: 63 Journal Issue: 4; Journal ID: ISSN 0020-1669
- Publisher:
- American Chemical Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Aromatic compounds; Electron paramagnetic resonance spectroscopy; Electronic absorption; Proton coupled electron transfer; Transition metals
Citation Formats
Doyle, Lorna, Magherusan, Adriana, Xu, Shuangning, Murphy, Kayleigh, Farquhar, Erik R., Molton, Florian, Duboc, Carole, Que, Jr., Lawrence, and McDonald, Aidan R. Class Ib Ribonucleotide Reductases: Activation of a Peroxido-Mn II Mn III to Generate a Reactive Oxo-Mn III Mn IV Oxidant. United States: N. p., 2024.
Web. doi:10.1021/acs.inorgchem.3c04163.
Doyle, Lorna, Magherusan, Adriana, Xu, Shuangning, Murphy, Kayleigh, Farquhar, Erik R., Molton, Florian, Duboc, Carole, Que, Jr., Lawrence, & McDonald, Aidan R. Class Ib Ribonucleotide Reductases: Activation of a Peroxido-Mn II Mn III to Generate a Reactive Oxo-Mn III Mn IV Oxidant. United States. https://doi.org/10.1021/acs.inorgchem.3c04163
Doyle, Lorna, Magherusan, Adriana, Xu, Shuangning, Murphy, Kayleigh, Farquhar, Erik R., Molton, Florian, Duboc, Carole, Que, Jr., Lawrence, and McDonald, Aidan R. Wed .
"Class Ib Ribonucleotide Reductases: Activation of a Peroxido-Mn II Mn III to Generate a Reactive Oxo-Mn III Mn IV Oxidant". United States. https://doi.org/10.1021/acs.inorgchem.3c04163.
@article{osti_2281632,
title = {Class Ib Ribonucleotide Reductases: Activation of a Peroxido-Mn II Mn III to Generate a Reactive Oxo-Mn III Mn IV Oxidant},
author = {Doyle, Lorna and Magherusan, Adriana and Xu, Shuangning and Murphy, Kayleigh and Farquhar, Erik R. and Molton, Florian and Duboc, Carole and Que, Jr., Lawrence and McDonald, Aidan R.},
abstractNote = {In the postulated catalytic cycle of class Ib Mn2 ribonucleotide reductases (RNRs), a MnII2 core is suggested to react with superoxide (O2·–) to generate peroxido-MnIIMnIII and oxo-MnIIIMnIV entities prior to proton-coupled electron transfer (PCET) oxidation of tyrosine. There is limited experimental support for this mechanism. We demonstrate that [MnII2(BPMP)(OAc)2](ClO4) (1, HBPMP = 2,6-bis[(bis(2 pyridylmethyl)amino)methyl]-4-methylphenol) was converted to peroxido-MnIIMnIII (2) in the presence of superoxide anion that converted to (μ-O)(μ-OH)MnIIIMnIV (3) via the addition of an H+-donor (p-TsOH) or (μ-O)2MnIIIMnIV (4) upon warming to room temperature. The physical properties of 3 and 4 were probed using UV–vis, EPR, X-ray absorption, and IR spectroscopies and mass spectrometry. Compounds 3 and 4 were capable of phenol oxidation to yield a phenoxyl radical via a concerted PCET oxidation, supporting the proposed mechanism of tyrosyl radical cofactor generation in RNRs. The synthetic models demonstrate that the postulated O2/Mn2/tyrosine activation mechanism in class Ib Mn2 RNRs is plausible and provides spectral insights into intermediates currently elusive in the native enzyme.},
doi = {10.1021/acs.inorgchem.3c04163},
journal = {Inorganic Chemistry},
number = 4,
volume = 63,
place = {United States},
year = {Wed Jan 17 00:00:00 EST 2024},
month = {Wed Jan 17 00:00:00 EST 2024}
}
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