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Title: 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

Abstract

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)] (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•–)]. DFT calculations confirm that 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 thermally transforms to its isomeric low-spin nitrato form [(PIm)FeIII(NO3–)]. 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 does not lead to nitrated phenol; the nitrate complex still forms. Furthermore, DFTmore » 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–)].The generation and characterization of the long sought after ferriheme peroxynitrite complex has been accomplished.« less

Authors:
 [1];  [2];  [2];  [3]; ORCiD logo [3];  [4];  [5]; ORCiD logo [5]; ORCiD logo [1]
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  1. Johns Hopkins Univ., Baltimore, MD (United States)
  2. Stanford Univ., Stanford, CA (United States)
  3. Oregon Health & Science Univ., Portland, OR (United States)
  4. SLAC National Accelerator Lab., Menlo Park, CA (United States)
  5. Stanford Univ., Stanford, CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)
Publication Date:
Research Org.:
SLAC National Accelerator Lab., Menlo Park, CA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1457149
Grant/Contract Number:  
24221005; GM118030; GM40392; AC02-76SF00515
Resource Type:
Accepted Manuscript
Journal Name:
Journal of the American Chemical Society
Additional Journal Information:
Journal Volume: 139; Journal Issue: 48; Journal ID: ISSN 0002-7863
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Sharma, Savita K., Schaefer, Andrew W., Lim, Hyeongtaek, Matsumura, Hirotoshi, Moenne-Loccoz, Pierre, Hedman, Britt, Hodgson, Keith O., Solomon, Edward I., and Karlin, Kenneth D.. 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. United States: N. p., 2017. Web. https://doi.org/10.1021/jacs.7b08468.
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Sharma, Savita K., Schaefer, Andrew W., Lim, Hyeongtaek, Matsumura, Hirotoshi, Moenne-Loccoz, Pierre, Hedman, Britt, Hodgson, Keith O., Solomon, Edward I., & Karlin, Kenneth D.. 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. United States. https://doi.org/10.1021/jacs.7b08468
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Sharma, Savita K., Schaefer, Andrew W., Lim, Hyeongtaek, Matsumura, Hirotoshi, Moenne-Loccoz, Pierre, Hedman, Britt, Hodgson, Keith O., Solomon, Edward I., and Karlin, Kenneth D.. Wed . "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". United States. https://doi.org/10.1021/jacs.7b08468. https://www.osti.gov/servlets/purl/1457149.
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@article{osti_1457149,
title = {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},
author = {Sharma, Savita K. and Schaefer, Andrew W. and Lim, Hyeongtaek and Matsumura, Hirotoshi and Moenne-Loccoz, Pierre and Hedman, Britt and Hodgson, Keith O. and Solomon, Edward I. and Karlin, Kenneth D.},
abstractNote = {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)] (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•–)]. DFT calculations confirm that 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 thermally transforms to its isomeric low-spin nitrato form [(PIm)FeIII(NO3–)]. 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 does not lead to nitrated phenol; the nitrate complex still forms. Furthermore, 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–)].The generation and characterization of the long sought after ferriheme peroxynitrite complex has been accomplished.},
doi = {10.1021/jacs.7b08468},
journal = {Journal of the American Chemical Society},
number = 48,
volume = 139,
place = {United States},
year = {2017},
month = {11}
}
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