Ambidentate H-bonding by heme-bound NO: structural and spectral effects of -O versus -N H-bonding.
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 vFeN/ vNO plots but not in vFeC/vCO 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 vFeN/vNO 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 vFeN/vNO correlation with the same slope as that calculated for H-bonding to N. Such deviations are not observed for CO adducts, because the CO pi* 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.
Xu
Changliang
C
Department of Chemistry, Princeton University, Princeton, NJ 08544, USA.
Thomas
G Spiro
GS
D018360:Crystallography, X-Ray; D006418:Heme / Q000737:chemistry*; D006859:Hydrogen / Q000737:chemistry*; D006860:Hydrogen Bonding; D007536:Isomerism; D008958:Models, Molecular; D008968:Molecular Conformation; D009569:Nitric Oxide / Q000737:chemistry*; D009584:Nitrogen / Q000737:chemistry*; D010100:Oxygen / Q000737:chemistry*
D009569:Nitric Oxide; D006418:Heme; D006859:Hydrogen; D009584:Nitrogen; D010100:Oxygen