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

Savita K. Sharma, Andrew W. Schaefer, Hyeongtaek Lim, Hirotoshi Matsumura, Pierre Moenne-Loccoz, Britt Hedman, Keith O. Hodgson, Edward I. Solomon, Kenneth D. Karlin

Research output: Contribution to journalArticle

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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)] (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.

Original languageEnglish (US)
Pages (from-to)17421-17430
Number of pages10
JournalJournal of the American Chemical Society
Volume139
Issue number48
DOIs
StatePublished - Dec 6 2017

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Peroxynitrous Acid
Nitric oxide
Discrete Fourier transforms
Superoxides
Nitric Oxide
2,4-di-tert-butylphenol
Iron
Nitrogen
Heme
Nitrates
Atoms
Negative ions
Ligands
Nitration
Reactive Nitrogen Species
Nitrogen Dioxide
Coordination Complexes
Porphyrins
Metal complexes
Phenol

ASJC Scopus subject areas

  • Catalysis
  • Chemistry(all)
  • Biochemistry
  • Colloid and Surface Chemistry

Cite this

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. / Sharma, Savita K.; Schaefer, Andrew W.; Lim, Hyeongtaek; Matsumura, Hirotoshi; Moenne-Loccoz, Pierre; Hedman, Britt; Hodgson, Keith O.; Solomon, Edward I.; Karlin, Kenneth D.

In: Journal of the American Chemical Society, Vol. 139, No. 48, 06.12.2017, p. 17421-17430.

Research output: Contribution to journalArticle

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. In: Journal of the American Chemical Society. 2017 ; Vol. 139, No. 48. pp. 17421-17430.
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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)] (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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AU - Lim, Hyeongtaek

AU - Matsumura, Hirotoshi

AU - Moenne-Loccoz, Pierre

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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.

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