Electronic structure of iron–dioxygen bond in oxy-Hb-A and its isolated oxy-α and oxy-β chains

Tsai, T. E.; Groves, J.L.; Wu, Cheng-Wen

doi:10.1063/1.441662

Cited by 21 publications

(13 citation statements)

References 19 publications

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“…Thus, our spin densities could be interpreted as a mixture of 75-80% Fe III -O 2 Ϫ and 20 -25% Fe II -O 2 . This is in accordance with the experimental observation that a quantum mixture of approximately twothirds ferric and one-third ferrous states gives the best agreement with Mössbauer spectra (43). Thus, oxyheme is inherently multiconfigurational, with an electronic structure that is somewhat analogous to that found in ozone (44).…”

Section: Resultssupporting

confidence: 78%

How O2 Binds to Heme

Jensen

Ryde

2004

Journal of Biological Chemistry

185

189

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We have used density functional methods to calculate fully relaxed potential energy curves of the seven lowest electronic states during the binding of O 2 to a realistic model of ferrous deoxyheme. Beyond a Fe-O distance of ϳ2.5 Å, we find a broad crossing region with five electronic states within 15 kJ/mol. The almost parallel surfaces strongly facilitate spin inversion, which is necessary in the reaction of O 2 with heme (deoxyheme is a quintet and O 2 a triplet, whereas oxyheme is a singlet). Thus, despite a small spin-orbit coupling in heme, the transition probability approaches unity. Using reasonable parameters, we estimate a transition probability of 0.06 -1, which is at least 15 times larger than for the nonbiological Fe-O ؉ system. Spin crossing is anticipated between the singlet ground state of bound oxyheme, the triplet and septet dissociation states, and a quintet intermediate state. The fact that the quintet state is close in energy to the dissociation couple is of biological importance, because it explains how both spin states of O 2 may bind to heme, thereby increasing the overall efficiency of oxygen binding. The activation barrier is estimated to be <15 kJ/mol based on our results and Mö ssbauer experiments. Our results indicate that both the activation energy and the spin-transition probability are tuned by the porphyrin as well as by the choice of the proximal heme ligand, which is a histidine in the globins. Together, they may accelerate O 2 binding to iron by ϳ10 11 compared with the Fe-O ؉ system. A similar near degeneracy between spin states is observed in a ferric deoxyheme model with the histidine ligand hydrogen bonded to a carboxylate group, i.e. a model of heme peroxidases, which bind H 2 O 2 in this oxidation state.All electrons have a spin, which is an intrinsic quantum chemical property that can take only two possible values, normally called ␣ and ␤ (or spin up and down). Almost all normal organic molecules contain an even number of electrons and also an equal number of ␣ and ␤ electrons. They are then said to have paired spin or to be singlets. Molecular oxygen (O 2 ) is a famous exception to this rule. In its ground state, it has two more electrons of one spin state than the other. Thus, it is said to have two unpaired electrons or to be a triplet. The singlet state of O 2 , with all electron spins paired, is ϳ90 kJ/mol higher in energy than the triplet ground state (1).A chemical reaction can normally not change the spin state of an electron. Therefore, reactions between singlet and triplet states are formally spin-forbidden, which means that they are slow. This is the reason why organic matter may exist in an atmosphere containing much O 2 . There is a strong thermodynamic drive of O 2 to oxidize organic matter to H 2 O and CO, but because these products (as well as the organic molecules) are singlets (whereas O 2 is a triplet), this reaction is spin-forbidden and therefore very slow at ambient temperatures. On the other hand, this is a problem when living organisms want to emp...

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Section: Resultssupporting

confidence: 78%

How O2 Binds to Heme

Jensen

Ryde

2004

Journal of Biological Chemistry

185

189

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“…Specifically, at 4.2 K the line width of the HbO2 spectrum is 0.27 ± 0.01 mms-'. This agrees with the results reported by Tsai et al (19) for HbO2 and the isolated a subunit sample. At higher temperatures the line widths generally increase probably due to relaxation effects.…”

Section: Figuresupporting

confidence: 93%

“…On the other hand, the quadrupole splittings found in the : subunit sample are smaller. This trend also has been recently observed by others (19), but as yet is unexplained.…”

Section: Discussionsupporting

confidence: 81%

“…There has been considerable progress made in understanding the Mossbauer results in oxyhemoglobin (6), including a number of theoretical investigations (7)(8)(9)(10)(11)(12)(13) (14)(15)(16)(17)(18) have also supported the observation that oxyand carbonmonoxyhemoglobin are both low spin. Recently, Tsai et al (19) have proposed an interesting model for the iron dioxygen bond in HbO2.…”

Section: Introductionmentioning

confidence: 99%

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Mössbauer spectroscopic studies of hemoglobin and its isolated subunits

Hoy¹,

Cook²,

Berger³

et al. 1986

Biophysical Journal

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Samples of 90% enriched 57Fe hemoglobin and its isolated subunits have been prepared. Mössbauer spectroscopic measurements have been made on three such samples. Sample one contained contributions of oxyhemoglobin, deoxyhemoglobin, and carbonmonoxyhemoglobin. This sample was studied from a temperature of 90 K down to 230 mK. Measurements were also made at 4.2 K using a small applied magnetic field of 1.0 T. In general, the measured quadrupole splittings and isomer shifts for each component agreed with previous measurements on single component samples in the literature, and thus demonstrated that chemically enriched hemoglobin has not been altered. The second and third samples were isolated alpha and beta subunits, respectively. We have found measurable Mössbauer spectral differences between the HbO2 sites in the alpha subunit sample and the beta subunit sample. The measured Mössbauer spectral areas indicate that the iron ion has the largest mean-square displacement at the deoxy Hb sites as compared to that at the oxy- and carbonmonoxy Hb sites. The mean-square displacement at the HbO2 sites is the smallest.

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“…That study determined that the pfpO 2 model compound had an electronic structure more similar to the Pauling model. The pfpO 2 compound has been seen as a good model for HbO 2 , with similar vibrational (24)(25)(26)(27) and Mössbauer spectra (28)(29)(30)(31)(32)(33). One major difference between the model complex and the protein is that the protein has a conserved histidine in the active site that can hydrogen-bond to the O 2 .…”

mentioning

confidence: 99%

Resonant inelastic X-ray scattering determination of the electronic structure of oxyhemoglobin and its model complex

Yan

Kröll

Baker

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Hemoglobin and myoglobin are oxygen-binding proteins with S = 0 heme {FeO2}8 active sites. The electronic structure of these sites has been the subject of much debate. This study utilizes Fe K-edge X-ray absorption spectroscopy (XAS) and 1s2p resonant inelastic X-ray scattering (RIXS) to study oxyhemoglobin and a related heme {FeO2}8 model compound, [(pfp)Fe(1-MeIm)(O2)] (pfp = meso-tetra(α,α,α,α-o-pivalamido-phenyl)porphyrin, or TpivPP, 1-MeIm = 1-methylimidazole) (pfpO2), which was previously analyzed using L-edge XAS. The K-edge XAS and RIXS data of pfpO2 and oxyhemoglobin are compared with the data for low-spin FeII and FeIII [Fe(tpp)(Im)2]0/+ (tpp = tetra-phenyl porphyrin) compounds, which serve as heme references. The X-ray data show that pfpO2 is similar to FeII, while oxyhemoglobin is qualitatively similar to FeIII, but with significant quantitative differences. Density-functional theory (DFT) calculations show that the difference between pfpO2 and oxyhemoglobin is due to a distal histidine H bond to O2 and the less hydrophobic environment in the protein, which lead to more backbonding into the O2. A valence bond configuration interaction multiplet model is used to analyze the RIXS data and show that pfpO2 is dominantly FeII with 6–8% FeIII character, while oxyhemoglobin has a very mixed wave function that has 50–77% FeIII character and a partially polarized Fe–O2 π-bond.

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Electronic structure of iron–dioxygen bond in oxy-Hb-A and its isolated oxy-α and oxy-β chains

Cited by 21 publications

References 19 publications

How O2 Binds to Heme

How O2 Binds to Heme

Mössbauer spectroscopic studies of hemoglobin and its isolated subunits

Resonant inelastic X-ray scattering determination of the electronic structure of oxyhemoglobin and its model complex

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