TY - JOUR
T1 - A Six-Coordinate Peroxynitrite Low-Spin Iron(III) Porphyrinate Complex - The Product of the Reaction of Nitrogen Monoxide (·NO(g)) with a Ferric-Superoxide Species
AU - Sharma, Savita K.
AU - Schaefer, Andrew W.
AU - Lim, Hyeongtaek
AU - Matsumura, Hirotoshi
AU - Moënne-Loccoz, Pierre
AU - Hedman, Britt
AU - Hodgson, Keith O.
AU - Solomon, Edward I.
AU - Karlin, Kenneth D.
N1 - Funding Information:
For K.D.K., this research was supported by the USA National Institutes of Health (GM60353). H.L. was supported by an Abbott Laboratories Stanford Graduate Fellowship. For E.I.S., this research is supported by the USA National Institutes of Health (GM040392). Use of the Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, is supported by the U.S. Department of Energy, Office of Science, Office of Basic Sciences under Contract No. DEAC02- 76SF00515. The SSRL Structural Molecular Biology Program is supported by the DOE Office of Biological and Environmental Research, and by the National Institutes of Health, National Institute of General Medical Sciences (P41GM103393). For P.M-L., this research was supported by the USA National Institutes of Health (GM074785). The contents of this publication are solely the responsibility of the authors and do not necessarily represent the official views of NIGMS or NIH.
Funding Information:
For K.D.K., this research was supported by the USA National Institutes of Health (GM60353). H.L. was supported by an Abbott Laboratories Stanford Graduate Fellowship. For E.I.S., this research is supported by the USA National Institutes of Health (GM040392). Use of the Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, is supported by the U.S. Department of Energy, Office of Science, Office of Basic Sciences under Contract No. DE-AC02-76SF00515. The SSRL Structural Molecular Biology Program is supported by the DOE Office of Biological and Environmental Research, and by the National Institutes of Health, National Institute of General Medical Sciences (P41GM103393). For P.M-L., this research was supported by the USA National Institutes of Health (GM074785). The contents of this publication are solely the responsibility of the authors and do not necessarily represent the official views of NIGMS or NIH.
Publisher Copyright:
© 2017 American Chemical Society.
PY - 2017/12/6
Y1 - 2017/12/6
N2 - Peroxynitrite (-OON=O, PN) is a reactive nitrogen species (RNS) which can effect deleterious nitrative or oxidative (bio)chemistry. It may derive from reaction of superoxide anion (O2•-) with nitric oxide (·NO) and has been suggested to form an as-yet unobserved bound heme-iron-PN intermediate in the catalytic cycle of nitric oxide dioxygenase (NOD) enzymes, which facilitate a ·NO homeostatic process, i.e., its oxidation to the nitrate anion. Here, a discrete six-coordinate low-spin porphyrinate-FeIII complex [(PIm)FeIII(-OON=O)] (3) (PIm a porphyrin moiety with a covalently tethered imidazole axial "base" donor ligand) has been identified and characterized by various spectroscopies (UV-vis, NMR, EPR, XAS, resonance Raman) and DFT calculations, following its formation at -80 °C by addition of ·NO(g) to the heme-superoxo species, [(PIm)FeIII(O2•-)] (2). DFT calculations confirm that 3 is a six-coordinate low-spin species with the PN ligand coordinated to iron via its terminal peroxidic anionic O atom with the overall geometry being in a cis-configuration. Complex 3 thermally transforms to its isomeric low-spin nitrato form [(PIm)FeIII(NO3-)] (4a). While previous (bio)chemical studies show that phenolic substrates undergo nitration in the presence of PN or PN-metal complexes, in the present system, addition of 2,4-di-tert-butylphenol (2,4DTBP) to complex 3 does not lead to nitrated phenol; the nitrate complex 4a still forms. DFT calculations reveal that the phenolic H atom approaches the terminal PN O atom (farthest from the metal center and ring core), effecting O-O cleavage, giving nitrogen dioxide (·NO2) plus a ferryl compound [(PIm)FeIV=O] (7); this rebounds to give [(PIm)FeIII(NO3-)] (4a).The generation and characterization of the long sought after ferriheme peroxynitrite complex has been accomplished.
AB - Peroxynitrite (-OON=O, PN) is a reactive nitrogen species (RNS) which can effect deleterious nitrative or oxidative (bio)chemistry. It may derive from reaction of superoxide anion (O2•-) with nitric oxide (·NO) and has been suggested to form an as-yet unobserved bound heme-iron-PN intermediate in the catalytic cycle of nitric oxide dioxygenase (NOD) enzymes, which facilitate a ·NO homeostatic process, i.e., its oxidation to the nitrate anion. Here, a discrete six-coordinate low-spin porphyrinate-FeIII complex [(PIm)FeIII(-OON=O)] (3) (PIm a porphyrin moiety with a covalently tethered imidazole axial "base" donor ligand) has been identified and characterized by various spectroscopies (UV-vis, NMR, EPR, XAS, resonance Raman) and DFT calculations, following its formation at -80 °C by addition of ·NO(g) to the heme-superoxo species, [(PIm)FeIII(O2•-)] (2). DFT calculations confirm that 3 is a six-coordinate low-spin species with the PN ligand coordinated to iron via its terminal peroxidic anionic O atom with the overall geometry being in a cis-configuration. Complex 3 thermally transforms to its isomeric low-spin nitrato form [(PIm)FeIII(NO3-)] (4a). While previous (bio)chemical studies show that phenolic substrates undergo nitration in the presence of PN or PN-metal complexes, in the present system, addition of 2,4-di-tert-butylphenol (2,4DTBP) to complex 3 does not lead to nitrated phenol; the nitrate complex 4a still forms. DFT calculations reveal that the phenolic H atom approaches the terminal PN O atom (farthest from the metal center and ring core), effecting O-O cleavage, giving nitrogen dioxide (·NO2) plus a ferryl compound [(PIm)FeIV=O] (7); this rebounds to give [(PIm)FeIII(NO3-)] (4a).The generation and characterization of the long sought after ferriheme peroxynitrite complex has been accomplished.
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U2 - 10.1021/jacs.7b08468
DO - 10.1021/jacs.7b08468
M3 - Article
C2 - 29091732
AN - SCOPUS:85037531563
VL - 139
SP - 17421
EP - 17430
JO - Journal of the American Chemical Society
JF - Journal of the American Chemical Society
SN - 0002-7863
IS - 48
ER -