Limits...
Spectral and electronic properties of nitrosylcobalamin.

Pallares IG, Brunold TC - Inorg Chem (2014)

Bottom Line: Previous studies revealed that among the known biologically relevant cobalamin species, NOCbl possesses the longest bond between the Co ion and the axially bound 5,6-dimethylbenzimidazole base, which was postulated to result from a strong trans influence exerted by the NO ligand.Collectively, our results indicate that the formally unoccupied Co 3dz(2) orbital engages in a highly covalent bonding interaction with the filled NO π* orbital and that the Co-NO bond is strengthened further by sizable π-backbonding interactions that are not present in any other Co(III)Cbl characterized to date.The implications of our results with respect to the unusual structural features and thermochromism of NOCbl and the proposed inhibition mechanisms of B12-dependent enzymes by NOCbl are discussed.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemistry, University of Wisconsin-Madison , Madison, Wisconsin 53706, United States.

ABSTRACT
Nitrosylcobalamin (NOCbl) is readily formed when Co(II)balamin reacts with nitric oxide (NO) gas. NOCbl has been implicated in the inhibition of various B12-dependent enzymes, as well as in the modulation of blood pressure and of the immunological response. Previous studies revealed that among the known biologically relevant cobalamin species, NOCbl possesses the longest bond between the Co ion and the axially bound 5,6-dimethylbenzimidazole base, which was postulated to result from a strong trans influence exerted by the NO ligand. In this study, various spectroscopic (electronic absorption, circular dichroism, magnetic circular dichroism, and resonance Raman) and computational (density functional theory (DFT) and time-dependent DFT) techniques were used to generate experimentally validated electronic structure descriptions for the "base-on" and "base-off" forms of NOCbl. Further insights into the principal Co-ligand bonding interactions were obtained by carrying out natural bond orbital analyses. Collectively, our results indicate that the formally unoccupied Co 3dz(2) orbital engages in a highly covalent bonding interaction with the filled NO π* orbital and that the Co-NO bond is strengthened further by sizable π-backbonding interactions that are not present in any other Co(III)Cbl characterized to date. Because of the substantial NO(-) to Co(III) charge donation, NOCbl is best described as a hybrid of Co(III)-NO(-) and Co(II)-NO(•) resonance structures. In contrast, our analogous computational characterization of a related species, superoxocobalamin, reveals that in this case a Co(III)-O2(-) description is adequate due to the larger oxidizing power of O2 versus NO. The implications of our results with respect to the unusual structural features and thermochromism of NOCbl and the proposed inhibition mechanisms of B12-dependent enzymes by NOCbl are discussed.

Show MeSH
High-energy region of rR spectra of NOCbl and its 15NO-enrichedisotopomer in the base-on and base-off conformations, obtained at77 K with 488 nm (20 491 cm–1) laser excitation.A difference spectrum for each conformation is included below thetwo data sets to highlight the isotope-sensitive vibrational features.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4334241&req=5

fig5: High-energy region of rR spectra of NOCbl and its 15NO-enrichedisotopomer in the base-on and base-off conformations, obtained at77 K with 488 nm (20 491 cm–1) laser excitation.A difference spectrum for each conformation is included below thetwo data sets to highlight the isotope-sensitive vibrational features.

Mentions: A comparison of the low-energy regions of the rR spectraof NOCbl and its 15NOCbl isotopomer reveals an isotope-sensitivefeature at 532 cm–1 (Figure 4, top), a region where the Co–NO stretching and Co–N–Obending modes are expected to occur.10 Subtractionof the 15NOCbl from the NOCbl trace yields a differencespectrum that shows an apparent shift of the 532 cm–1 feature to 496 cm–1 upon 14NO → 15NO substitution. An analogous isotope-sensitive feature ispresent in the rR spectrum of base-off NOCbl (our model of NOCbi+, Figure 4, bottom traces), thoughin this case a much better-resolved difference spectrum is obtained.Closer examination of this difference spectrum clearly discloses thepresence of a shoulder on the low-energy side of the positive feature,suggesting that two isotope-sensitive modes actually occur in thisregion. Indeed, a Gaussian deconvolution of the rR spectra in Figure 4 reveals that the vibrational modes of base-on andbase-off NOCbl at 515 and 532 cm–1 shift to 500and 521 cm–1, respectively, upon 14NO→ 15NO substitution (see SupportingInformation, Figure S9). In a previous rR study of NOCbl, asingle isotope-sensitive peak was observed at 514 cm–1 that shifted to 496 cm–1 upon 14NO→15NO substitution. However, the spectral resolutionof these published data appears to be relatively low, as only twohigh-energy (>1,500 cm–1) features associatedwith corrin-based modes could be identified,10 compared to the four features that are readily apparent in our spectra(Figure 5). Additionally, considering thatmode coupling typically leads to lower isotope shifts than expected,the reported isotope shift of 18 cm–1, which largelyexceeds the 14 cm–1 decrease in vibrational frequencycalculated using a harmonic oscillator model for a localized Co–Nstretching mode, seems unreasonably large.


Spectral and electronic properties of nitrosylcobalamin.

Pallares IG, Brunold TC - Inorg Chem (2014)

High-energy region of rR spectra of NOCbl and its 15NO-enrichedisotopomer in the base-on and base-off conformations, obtained at77 K with 488 nm (20 491 cm–1) laser excitation.A difference spectrum for each conformation is included below thetwo data sets to highlight the isotope-sensitive vibrational features.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4334241&req=5

fig5: High-energy region of rR spectra of NOCbl and its 15NO-enrichedisotopomer in the base-on and base-off conformations, obtained at77 K with 488 nm (20 491 cm–1) laser excitation.A difference spectrum for each conformation is included below thetwo data sets to highlight the isotope-sensitive vibrational features.
Mentions: A comparison of the low-energy regions of the rR spectraof NOCbl and its 15NOCbl isotopomer reveals an isotope-sensitivefeature at 532 cm–1 (Figure 4, top), a region where the Co–NO stretching and Co–N–Obending modes are expected to occur.10 Subtractionof the 15NOCbl from the NOCbl trace yields a differencespectrum that shows an apparent shift of the 532 cm–1 feature to 496 cm–1 upon 14NO → 15NO substitution. An analogous isotope-sensitive feature ispresent in the rR spectrum of base-off NOCbl (our model of NOCbi+, Figure 4, bottom traces), thoughin this case a much better-resolved difference spectrum is obtained.Closer examination of this difference spectrum clearly discloses thepresence of a shoulder on the low-energy side of the positive feature,suggesting that two isotope-sensitive modes actually occur in thisregion. Indeed, a Gaussian deconvolution of the rR spectra in Figure 4 reveals that the vibrational modes of base-on andbase-off NOCbl at 515 and 532 cm–1 shift to 500and 521 cm–1, respectively, upon 14NO→ 15NO substitution (see SupportingInformation, Figure S9). In a previous rR study of NOCbl, asingle isotope-sensitive peak was observed at 514 cm–1 that shifted to 496 cm–1 upon 14NO→15NO substitution. However, the spectral resolutionof these published data appears to be relatively low, as only twohigh-energy (>1,500 cm–1) features associatedwith corrin-based modes could be identified,10 compared to the four features that are readily apparent in our spectra(Figure 5). Additionally, considering thatmode coupling typically leads to lower isotope shifts than expected,the reported isotope shift of 18 cm–1, which largelyexceeds the 14 cm–1 decrease in vibrational frequencycalculated using a harmonic oscillator model for a localized Co–Nstretching mode, seems unreasonably large.

Bottom Line: Previous studies revealed that among the known biologically relevant cobalamin species, NOCbl possesses the longest bond between the Co ion and the axially bound 5,6-dimethylbenzimidazole base, which was postulated to result from a strong trans influence exerted by the NO ligand.Collectively, our results indicate that the formally unoccupied Co 3dz(2) orbital engages in a highly covalent bonding interaction with the filled NO π* orbital and that the Co-NO bond is strengthened further by sizable π-backbonding interactions that are not present in any other Co(III)Cbl characterized to date.The implications of our results with respect to the unusual structural features and thermochromism of NOCbl and the proposed inhibition mechanisms of B12-dependent enzymes by NOCbl are discussed.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemistry, University of Wisconsin-Madison , Madison, Wisconsin 53706, United States.

ABSTRACT
Nitrosylcobalamin (NOCbl) is readily formed when Co(II)balamin reacts with nitric oxide (NO) gas. NOCbl has been implicated in the inhibition of various B12-dependent enzymes, as well as in the modulation of blood pressure and of the immunological response. Previous studies revealed that among the known biologically relevant cobalamin species, NOCbl possesses the longest bond between the Co ion and the axially bound 5,6-dimethylbenzimidazole base, which was postulated to result from a strong trans influence exerted by the NO ligand. In this study, various spectroscopic (electronic absorption, circular dichroism, magnetic circular dichroism, and resonance Raman) and computational (density functional theory (DFT) and time-dependent DFT) techniques were used to generate experimentally validated electronic structure descriptions for the "base-on" and "base-off" forms of NOCbl. Further insights into the principal Co-ligand bonding interactions were obtained by carrying out natural bond orbital analyses. Collectively, our results indicate that the formally unoccupied Co 3dz(2) orbital engages in a highly covalent bonding interaction with the filled NO π* orbital and that the Co-NO bond is strengthened further by sizable π-backbonding interactions that are not present in any other Co(III)Cbl characterized to date. Because of the substantial NO(-) to Co(III) charge donation, NOCbl is best described as a hybrid of Co(III)-NO(-) and Co(II)-NO(•) resonance structures. In contrast, our analogous computational characterization of a related species, superoxocobalamin, reveals that in this case a Co(III)-O2(-) description is adequate due to the larger oxidizing power of O2 versus NO. The implications of our results with respect to the unusual structural features and thermochromism of NOCbl and the proposed inhibition mechanisms of B12-dependent enzymes by NOCbl are discussed.

Show MeSH