Theoretical study on electronic structures of FeOO, FeOOH, FeO(H2O), and FeO in hemes: As intermediate models of dioxygen reduction in cytochrome c oxidase

Yoshioka, Yasunori; Satoh, Hiroyuki; Mitani, Masaki

doi:10.1016/j.jinorgbio.2007.05.018

Cited by 22 publications

(35 citation statements)

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“…As such, a number of heme–peroxo–copper complexes have been synthesized to model this species and understand its reactivity, 8,20–26 and many computational studies addressing O–O cleavage in C c O have invoked a bridging peroxo as an energetic local minimum. 19,27,28 …”

Section: Introductionmentioning

confidence: 99%

Phenol-Induced O–O Bond Cleavage in a Low-Spin Heme–Peroxo–Copper Complex: Implications for O₂ Reduction in Heme–Copper Oxidases

et al. 2017

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This study evaluates the reaction of a biomimetic heme–peroxo–copper complex, {[(DCHIm)(F8)-FeIII]–(O22−)–[CuII(AN)]}+ (1), with a phenolic substrate, involving a net H-atom abstraction to cleave the bridging peroxo O–O bond that produces FeIV=O, CuII—OH, and phenoxyl radical moieties, analogous to the chemistry carried out in heme–copper oxidases (HCOs). A 3D potential energy surface generated for this reaction reveals two possible reaction pathways: one involves nearly complete proton transfer (PT) from the phenol to the peroxo ligand before the barrier; the other involves O–O homolysis, where the phenol remains H-bonding to the peroxo OCu in the transition state (TS) and transfers the H+ after the barrier. In both mechanisms, electron transfer (ET) from phenol occurs after the PT (and after the barrier); therefore, only the interaction with the H+ is involved in lowering the O–O cleavage barrier. The relative barriers depend on covalency (which governs ET from Fe), and therefore vary with DFT functional. However, as these mechanisms differ by the amount of PT at the TS, kinetic isotope experiments were conducted to determine which mechanism is active. It is found that the phenolic proton exhibits a secondary kinetic isotope effect, consistent with the calculations for the H-bonded O–O homolysis mechanism. The consequences of these findings are discussed in relation to O–O cleavage in HCOs, supporting a model in which a peroxo intermediate serves as the active H+ acceptor, and both the H+ and e− required for O–O cleavage derive from the cross-linked Tyr residue present at the active site.

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Section: Introductionmentioning

confidence: 99%

Phenol-Induced O–O Bond Cleavage in a Low-Spin Heme–Peroxo–Copper Complex: Implications for O₂ Reduction in Heme–Copper Oxidases

et al. 2017

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“…Also discussed and calculated is an electron-transfer from Cu B I in A which is accompanied by H + uptake to give a μ-hydroperoxo transient, Fe a3 III -O-O(H)-Cu B II ; the protonation event in this scenario would trigger electron transfer (from the heme a 3 and the Tyr244) yielding a cleaved O—O product ferryl moiety (state P M , Scheme 1). 10,13-15…”

Section: Introductionmentioning

confidence: 99%

Heme−Copper−Dioxygen Complexes: Toward Understanding Ligand-Environmental Effects on the Coordination Geometry, Electronic Structure, and Reactivity

et al. 2010

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The nature of the ligand is an important aspect of controlling structure and reactivity in coordination chemistry. In connection with our study of heme/copper/oxygen reactivity relevant to cytochrome c oxidase O 2 -reduction chemistry, we compare the molecular and electronic structure of two highspin heme-peroxo-copper [Fe III -O 2 2--Cu II ] + complexes containing N 4 -tetradentate (1) or N 3 -tridentate (2) copper ligands. Combining previously reported and new resonance Raman and EXAFS data coupled to DFT calculations we report a geometric structure and more complete electronic description of the high-spin heme-peroxo-copper complexes 1 and 2, which establish μ-(O 2 2-) sideon to the Fe III and end-on to Cu II (μ-η 2 :η 1 ) binding for the complex 1 but side-on/side-on (μ-η 2 :η 2 ) μ-peroxo coordination for the complex 2. We also compare and summarize the differences and similarities of these two complexes in their reactivity toward CO, PPh 3 , acid and phenols. The comparison of a new X-ray structure of μ-oxo complex 2a with the previously reported 1a X-ray structure, two thermal decomposition products respectively of 2 and 1, reveals a considerable difference in the Fe-O-Cu angle between the two μ-oxo complexes (∠Fe-O-Cu = 178.2° in 1a, ∠Fe-O-Cu = 149.5° in 2a). The reaction of 2 with one equivalent of exogenous N-donor axial base leads to the formation of a distinctive low-temperature stable, low-spin heme-O 2 -Cu complex (2b), but under the same conditions the addition of an axial base to 1 leads to the dissociation of the hemeperoxo-Cu assembly and the release of O 2 . 2b reacts with phenols performing hydrogen-atom (e -+ H + ) abstraction resulting in O-O bond cleavage and the formation of high-valent ferryl [Fe IV =O] complex (2c). The nature of 2c was confirmed by comparison of its spectroscopic features and reactivity with those of an independently prepared ferryl complex. The phenoxyl radical generated by the hydrogen-atom abstraction was either 1) directly detected by EPR spectroscopy using phenols that produce stable radicals or 2) indirectly by detection of the coupling product of two phenoxyl radicals.karlin@jhu.edu, edward.solomon@stanford.edu. Supporting Information Available. UV-visible spectra of the reaction of (2b) with 1 equiv. of 2,4-di-tertbutylphenol ( Figure S1), UVvis spectra of the reaction of [(F 8 )Fe III -(O 2 2-)-Cu II (TMPA)] + (1) with DMAP ( Figure S2), EPR spectra of (2b) reaction with 1 equiv.of 2,4-di-tert-butylphenol ( Figure S3), GC-MS trace of the oxidative coupling of 2,4-di-tert-butylphenol in presence of (2b) ( Figure S4), ORTEP diagram ( Figure S5) and crystal data and structure refinement for [(F 8 )Fe III -(O 2-)-Cu II (AN)] + (2a) X-ray structure (Table S1), XAS spectra and computational data.NIH Public Access

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“…Compared to other density functional methods, B3LYP has shown good performance for the study of intramolecular addition of Cys-S ● to Phe and Tyr residues (35). The different steps of the catalytic cycle of cytochrome oxidase, which include electron and proton or hydrogen transfer reactions have also been successfully studied using this level of theory (34, 36-38), while the experience using Density Functional Theory methods for PCET in metallo-enzymes was recently reviewed (39). The implicit solvation methods correspond to the Polarizable Continuum Model (PCM) as developed in (40).…”

Section: Methodsmentioning

confidence: 99%

Molecular basis of intramolecular electron transfer in proteins during radical-mediated oxidations: Computer simulation studies in model tyrosine–cysteine peptides in solution

Petruk

Bartesaghi

Trujillo

et al. 2012

Archives of Biochemistry and Biophysics

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Experimental studies in hemeproteins and model Tyr/Cys-containing peptides exposed to oxidizing and nitrating species suggest that intramolecular electron transfer (IET) between tyrosyl radicals (Tyr-O●) and Cys residues controls oxidative modification yields. The molecular basis of this IET process is not sufficiently understood with structural atomic detail. Herein, we analyzed using molecular dynamics and quantum mechanics-based computational calculations, mechanistic possibilities for the radical transfer reaction in Tyr/Cys-containing peptides in solution and correlated them with existing experimental data. Our results support that Tyr-O● to Cys radical transfer is mediated by an acid/base equilibrium that involves deprotonation of Cys to form the thiolate, followed by a likely rate-limiting transfer process to yield cysteinyl radical and a Tyr phenolate; proton uptake by Tyr completes the reaction. Both, the pKa values of the Tyr phenol and Cys thiol groups and the energetic and kinetics of the reversible IET are revealed as key physico-chemical factors. The proposed mechanism constitutes a case of sequential, acid/base equilibrium-dependent and solvent-mediated, proton-coupled electron transfer and explains the dependency of oxidative yields in Tyr/Cys peptides as a function of the number of alanine spacers. These findings contribute to explain oxidative modifications in proteins that contain sequence and/or spatially close Tyr-Cys residues.

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Theoretical study on electronic structures of FeOO, FeOOH, FeO(H2O), and FeO in hemes: As intermediate models of dioxygen reduction in cytochrome c oxidase

Cited by 22 publications

References 50 publications

Phenol-Induced O–O Bond Cleavage in a Low-Spin Heme–Peroxo–Copper Complex: Implications for O₂ Reduction in Heme–Copper Oxidases

Phenol-Induced O–O Bond Cleavage in a Low-Spin Heme–Peroxo–Copper Complex: Implications for O₂ Reduction in Heme–Copper Oxidases

Heme−Copper−Dioxygen Complexes: Toward Understanding Ligand-Environmental Effects on the Coordination Geometry, Electronic Structure, and Reactivity

Molecular basis of intramolecular electron transfer in proteins during radical-mediated oxidations: Computer simulation studies in model tyrosine–cysteine peptides in solution

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Theoretical study on electronic structures of FeOO, FeOOH, FeO(H2O), and FeO in hemes: As intermediate models of dioxygen reduction in cytochrome c oxidase

Cited by 22 publications

References 50 publications

Phenol-Induced O–O Bond Cleavage in a Low-Spin Heme–Peroxo–Copper Complex: Implications for O2 Reduction in Heme–Copper Oxidases

Phenol-Induced O–O Bond Cleavage in a Low-Spin Heme–Peroxo–Copper Complex: Implications for O2 Reduction in Heme–Copper Oxidases

Heme−Copper−Dioxygen Complexes: Toward Understanding Ligand-Environmental Effects on the Coordination Geometry, Electronic Structure, and Reactivity

Molecular basis of intramolecular electron transfer in proteins during radical-mediated oxidations: Computer simulation studies in model tyrosine–cysteine peptides in solution

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Phenol-Induced O–O Bond Cleavage in a Low-Spin Heme–Peroxo–Copper Complex: Implications for O₂ Reduction in Heme–Copper Oxidases

Phenol-Induced O–O Bond Cleavage in a Low-Spin Heme–Peroxo–Copper Complex: Implications for O₂ Reduction in Heme–Copper Oxidases