New Light on NO Bonding in Fe(III) Heme Proteins from Resonance Raman Spectroscopy and DFT Modeling

Soldatova, Alexandra; Ibrahim, Mohammed; Olson, John S.; Czernuszewicz, Roman S.; Spiro, Thomas G.

doi:10.1021/ja906233m

Cited by 97 publications

(110 citation statements)

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“…Also encountered, however, are Fe III (NO) complexes, which are isoelectronic with Fe II (CO), but have altered polarity, and quite different secondary interactions. 15–18 The important Fe II (OO) adducts are less-well studied, primarily due to experimental difficulties, 19–21 but useful data are accumulating. 22–36 O 2 has two π* electrons, and the complex FeOO electronic structure has been much investigated recently.…”

Section: Introductionmentioning

confidence: 99%

Electronic Structure and Ligand Vibrations in FeNO, CoNO, and FeOO Porphyrin Adducts

2013

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The gaseous ligands, CO, NO and O2 interact with the Fe ion in heme proteins largely via backbonding of Fe electrons to the π* orbitals of the XO (X = C, N, O) ligands. In these FeXO adducts, the Fe–X stretching frequency varies inversely with the X–O stretching frequency, since increased backbonding strengthens the Fe–X bond while weakening the X–O bond. Inverse frequency correlations have been observed for all three ligands, despite differing electronic and geometric structures, and despite variable composition of the `FeX' vibrational mode, in which Fe–X stretching and Fe–X–O coordinates are mixed for bent FeXO adducts. We report experimental data for 5-coordinate CoII(NO) porphyrin adducts (isoelectronic with FeII(OO) adducts), and the results of DFT modeling for 5-coordinate FeII(NO), CoII(NO) and FeII(OO) adducts. Inverse ν(MX)/ν(XO) correlations are obtained computationally, using model porphyrins with graded electron-donating and -withdrawing substituents to modulate the backbonding. Computed slopes agree satisfactorily with experiment, provided non-hybrid functionals are used, which avoid overemphasizing high-spin states. The BP86 functional gives correct ground states, a closed-shell singlet for CoII(NO) and an open-shell singlet for the isoelectronic FeII(OO), as corroborated by structural data for CoII(NO), and the ν(MX)/ν(XO) slope agreement with experiment for both adducts. However, for FeII(OO) adducts, the computed inverse ν(MX)/ν(XO) correlation applies only to porphyrins with electron-donating and withdrawing substituents of moderate strength. For substituents more donating than –CH3, a direct correlation is obtained, the Fe–O and O–O bonds weakening in concert. This effect is ascribed to the dominance of σ bonding via the in-plane dxz(+dz2)-π* orbital, when electron-donating substituents raise the d orbital energies sufficiently to render backbonding (dyz-π*) unimportant.

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Section: Introductionmentioning

confidence: 99%

Electronic Structure and Ligand Vibrations in FeNO, CoNO, and FeOO Porphyrin Adducts

2013

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“…23, 38 This effect has been attributed to the fact that, when 40 bound to ferric haems, the electronic ground state of the Fe(III)-NO moiety is somewhat better-described by the Fe(II)-NO+ formalism. 39 This engenders interactions between the NO and the distal histidine in myoglobin that occur through a lone pair donation mechanism rather than a hydrogen bond leading to an upshift of the frequency.…”

Section: Ftir Spectroscopymentioning

confidence: 99%

The effect on structural and solvent water molecules of substrate binding to ferric horseradish peroxidase

et al. 2015

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“…A similar wavenumber for ν 4 is observed for the weakly-bound complex formed between the ferric state of myoglobin, Mb III , and NO. 24,27 In this example, EPR studies indicate that charge transfer, in the linear Fe-N-O geometry, gives a high spin complex possessing ferrous character, i.e. Mb III -NO ↔ Mb II -NO + , 28 however the higher electron density on the metal ion in Mb II -NO + must not lead to increased π-backbonding to the porphyrin as the anticipated shift in ν 4 to lower frequencies is not observed (see figure 3).…”

Section: Raman Spectroscopic Measurement Of Nitrosyl Myoglobin In Carmentioning

confidence: 99%

Monitoring Changes in the Redox State of Myoglobin in Cardiomyocytes by Raman Spectroscopy Enables the Protective Effect of NO Donors to Be Evaluated

Almohammedi¹,

Kapetanaki²,

Hudson³

et al. 2015

Anal. Chem.

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Raman microspectroscopy has been used to monitor changes in the redox and ligandcoordination states of the heme complex in myoglobin during the pre-conditioning of ex vivo cardiomyocytes with pharmacological drugs that release nitric oxide (NO). These chemical agents are known to confer protection on heart tissue against ischemia-reperfusion injury.Subsequent changes in the redox and ligand-coordination states during experimental simulations of ischemia and reperfusion have also been monitored. We found that these measurements, in real time, could be used to evaluate the pre-conditioning treatment of cardiomyocytes, and predict the likelihood of cell survival following a potentially-lethal period of ischemia.Evaluation of the pre-conditioning treatment was done at the single-cell level. The binding of NO to myoglobin, giving a 6-coordinate ferrous-heme complex, was inferred from the measured Raman bands of a cardiomyocyte by comparison to pure solution of the protein in the presence of NO. A key change in the Raman spectrum was observed after perfusion of the NO-donor was completed, where if the pre-conditioning treatment was successful then the bands corresponding to the nitrosyl complex were replaced by bands corresponding to metmyoglobin, Mb III . An observation of Mb III bands in the Raman spectrum was made for all the cardiomyocytes that recovered contractile function, whilst the absence of Mb III bands always indicated that the cardiomyocyte would be unable to recover contractile function, following the simulated conditions of ischemia and reperfusion in these experiments.3

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New Light on NO Bonding in Fe(III) Heme Proteins from Resonance Raman Spectroscopy and DFT Modeling

Cited by 97 publications

References 84 publications

Electronic Structure and Ligand Vibrations in FeNO, CoNO, and FeOO Porphyrin Adducts

Electronic Structure and Ligand Vibrations in FeNO, CoNO, and FeOO Porphyrin Adducts

The effect on structural and solvent water molecules of substrate binding to ferric horseradish peroxidase

Monitoring Changes in the Redox State of Myoglobin in Cardiomyocytes by Raman Spectroscopy Enables the Protective Effect of NO Donors to Be Evaluated

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