Solid-state oxygen-17 nuclear magnetic resonance spectroscopic studies of [17O2] picket fence porphyrin, myoglobin, and hemoglobin

Abstract

We have studied a model compound for oxyhemoglobin and oxymyoglobin, the iron-dioxygen complex of "picket fence porphyrin" (5,10,15,a,a,porphyrinato)iron (II) ((1-Melm)02), as well as oxymyoglobin and oxyhemoglobin themselves, by using 170 solid-state nuclear magnetic resonance spectroscopy. For the model picket fence porphyrin, the principal components of the chemical shift tensors for both bridging and terminal oxygens in the Fe-02 unit have been determined, and the isotropic chemical shifts occur at 1200-1600 and 2000 ppm, respectively, somewhat deshielded from the -1750 and ~2500 ppm values found by Gerothanassis et al. in solution {J. Am. Chem. Soc. 1989, III, 7006-7012).The anisotropies of the shift tensors are very large for both oxygens ( = ~2200 ppm for the bridging oxygen and = 3350 ppm for the terminal oxygen, at 77 K). From partial averaging of the shift tensors at room temperature, due to fast axial rotation of the dioxygen ligand, an Fe-O-O bond angle of ~140°has been derived for the model system. Temperature dependence studies indicate essentially no change in the isotropic chemical shift of the terminal oxygen down to 4.2 K, while there is an apparent low-frequency shift of the bridging oxygen on cooling to 77 K, possibly due to the freezing in of one conformational substate. Spectra of oxymyoglobin and oxyhemoglobin, at 77 K, are very similar to those of the model compound at low temperature. Our results indicate that the 170 nuclear quadrupole coupling constants must be relatively small for both oxygens (55 MHz) in all systems, much smaller than the 8.5and 20-MHz values found for ozone, suggesting extensive ir-delocalization in the Fe-O-O fragment. Our results are also consistent with an overwhelmingly spin paired configuration, both in the model system, and in oxyhemoglobin and oxymyoglobin themselves.

Density-functional molecular dynamics studies of biologically relevant iron and cobalt complexes with macrocyclic ligands

“…This behavior provides a direct evidence for the fast rotational motion of O 2 around the Fe-O bond, as invoked to explain the fourfold disorder found in the crystal structure of synthetic heme models [15]. It also confirms that the O-O/Fe-N overlapping configuration is the transition state for the dynamic motion of O 2 between the porphyrin quadrants [79][80][81].…”

“…For instance, several studies have shown that structural differences among heme models are able to vary the equilibrium constant (K eq ) of the O 2 and CO binding reaction. These changes have been attributed mainly to hydrogen bonding and polar interactions [78][79][80][81][82][83], but steric interactions, porphyrin distortions and the interplay of various factors have also been proposed [84,85].…”

“…X-ray structures of picket-fence-oxygen complexes commonly show a fourfold disorder of the bound O 2 [15,16,77,86], something that has been interpreted as a dynamic O 2 motion [79][80][81]. The structure of the iron-picket-fence-oxygen complex was previously studied [63].…”

Oxygen-17 NMR spectroscopy: Basic principles and applications (part II)

“…It was suggested that the inequivalence is due to unequal charge-transfer interactions between the oxygen atoms and a nearby phenyl ring [507]. These v values are only slightly different from those obtained for hydrogen peroxide (v = 16.31 MHz; g = 0.687) [718] but significantly different from those obtained for the picket-fence porphyrin model [719].…”

17O NMR study of oxo metalloporphyrin complexes: Correlation with electronic structure of M O moiety

“…Furthermore, 17 O NMR spectroscopy has been applied for polyoxometallates for studying their structure, electronic states, and reactivities [65][66][67][68][69][70][71][72][73][74][75][76][77][78][79]. Recently, 17 O NMR spectroscopy is becoming of frequent use in solid-state NMR for the analysis of minerals and synthetic materials [80][81][82][83][84][85].…”