Abstract
Resonance Raman studies have uncovered puzzling complexities in the structures of NO adducts of heme proteins. Although CO adducts of heme proteins obey well-behaved anti-correlations between Fe–C and C–O stretching frequencies, which reflect changes in backbonding induced by distal H-bonding residues, the corresponding NO data are scattered. This scatter can be traced to distal influences, since protein-free NO–hemes do show well-behaved anti-correlations. Why do distal effects produce irregularities in νFeN/νNO plots but not in νFeC/νCO plots? We show via density functional theory (DFT) computations on model systems that the response to distal H-bonding differs markedly when the NO acceptor atom is N versus O. Backbonding is augmented by H-bonding to O, but the effect of H-bonding to N is to weaken both N–O and N–Fe bonds. The resulting downward deviation from the νFeN/νNO backbonding line increases with increasing H-bond strength. This effect explains the deviations observed for a series of myoglobin variants, in which the strength of distal H-bonding is modulated by distal pocket residue substitutions. Most of the data follow a positive νFeN/νNO correlation with the same slope as that calculated for H-bonding to N. Such deviations are not observed for CO adducts, because the CO π* orbital is unoccupied, and serves as a delocalized acceptor of H-bonds. H-bonding to N primes NO–heme for reduction to the HNO adduct, a putative intermediate in NO-reducing enzymes.
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Abbreviations
- DFT:
-
Density functional theory
- EPR:
-
Electron paramagnetic spectroscopy
- ImH:
-
Imidazole
- Mb:
-
Myoglobin
- NMeIm:
-
N-Methylimidazole
- NRVS:
-
Nuclear resonance vibrational spectroscopy
- P:
-
Porphine
- RR:
-
Resonance Raman
- TPP:
-
Tetraphenylporphine
- XAFS:
-
X-ray absorption fine-structure
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Acknowledgments
This work was supported by NIH grant GM 33576 from the National Institute of General Medical Sciences. We thank Dr. Mohammed Ibrahim for helpful discussions and for assistance in preparing the manuscript.
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Xu, C., Spiro, T.G. Ambidentate H-bonding by heme-bound NO: structural and spectral effects of –O versus –N H-bonding. J Biol Inorg Chem 13, 613–621 (2008). https://doi.org/10.1007/s00775-008-0349-8
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DOI: https://doi.org/10.1007/s00775-008-0349-8