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

doi:10.1021/jacs.7b08468

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 (O ₂ ^•–) 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-Fe ^III complex [(P ^Im)Fe ^III( ^–OON=O)] (P ^Im; 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, [(P ^Im)Fe ^III(O ₂ ^•–)]. 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 [(P ^Im)Fe ^III(NO ₃ ^–)]. 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 ofmore »« less

Authors:

Sharma, Savita K. ^[1]; Schaefer, Andrew W. ^[2]; Lim, Hyeongtaek ^[2]; Matsumura, Hirotoshi ^[3];

^[3]; Hedman, Britt ^[4]; Hodgson, Keith O. ^[5];

^[5];

^[1]

Johns Hopkins Univ., Baltimore, MD (United States)
Stanford Univ., Stanford, CA (United States)
Oregon Health & Science Univ., Portland, OR (United States)
SLAC National Accelerator Lab., Menlo Park, CA (United States)
Stanford Univ., Stanford, CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)

Publication Date:: 2017-11-01

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.  doi: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.  doi: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.  doi: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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DOI: 10.1021/jacs.7b08468

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Direct Resonance Raman Characterization of a Peroxynitrito Copper Complex Generated from O ₂ and NO and Mechanistic Insights into Metal‐Mediated Peroxynitrite Decomposition
journal, July 2019

Liu, Jeffrey J.; Siegler, Maxime A.; Karlin, Kenneth D.
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DOI: 10.1002/ange.201904672

Direct Resonance Raman Characterization of a Peroxynitrito Copper Complex Generated from O ₂ and NO and Mechanistic Insights into Metal-Mediated Peroxynitrite Decomposition
journal, July 2019

Liu, Jeffrey J.; Siegler, Maxime A.; Karlin, Kenneth D.
Angewandte Chemie International Edition, Vol. 58, Issue 32
DOI: 10.1002/anie.201904672

Towards the understanding of the enzymatic cleavage of polyisoprene by the dihaem-dioxygenase RoxA
journal, October 2019

Schmitt, Georg; Birke, Jakob; Jendrossek, Dieter
AMB Express, Vol. 9, Issue 1
DOI: 10.1186/s13568-019-0888-0

Direct Resonance Raman Characterization of a Peroxynitrito Copper Complex Generated from O ₂ and NO and Mechanistic Insights into Metal-Mediated Peroxynitrite Decomposition
journal, July 2019

Liu, Jeffrey J.; Siegler, Maxime A.; Karlin, Kenneth D.
Angewandte Chemie International Edition, Vol. 58, Issue 32
DOI: 10.1002/anie.201904672

Towards the understanding of the enzymatic cleavage of polyisoprene by the dihaem-dioxygenase RoxA
journal, October 2019

Schmitt, Georg; Birke, Jakob; Jendrossek, Dieter
AMB Express, Vol. 9, Issue 1
DOI: 10.1186/s13568-019-0888-0

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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

Citation Formats

Direct Resonance Raman Characterization of a Peroxynitrito Copper Complex Generated from O 2 and NO and Mechanistic Insights into Metal‐Mediated Peroxynitrite Decomposition journal, July 2019

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