Tuning the Geometric and Electronic Structure of Synthetic High-Valent Heme Iron(IV)-Oxo Models in the Presence of a Lewis Acid and Various Axial Ligands

Ehudin, Melanie A.; Gee, Leland B.; Sabuncu, Sinan; Braun, Augustin; Moënne-Loccoz, Pierre; Hedman, Britt; Hodgson, Keith O.; Solomon, Edward I.; Karlin, Kenneth D.

doi:10.1021/jacs.9b00795

Title: Tuning the Geometric and Electronic Structure of Synthetic High-Valent Heme Iron(IV)-Oxo Models in the Presence of a Lewis Acid and Various Axial Ligands

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Abstract

High-valent ferryl species (e.g., (Por)FeIV═O, Cmpd-II) are observed or proposed key oxidizing intermediates in the catalytic cycles of heme-containing enzymes (P-450s, peroxidases, catalases, and cytochrome c oxidase) involved in biological respiration and oxidative metabolism. Herein, various axially ligated iron(IV)-oxo complexes were prepared to examine the influence of the identity of the base. These were generated by addition of various axial ligands (1,5-dicyclohexylimidazole (DCHIm), a tethered-imidazole system, and sodium derivatives of 3,5-dimethoxyphenolate and imidazolate). Characterization was carried out via UV–vis, electron paramagnetic resonance (EPR), ⁵⁷Fe Mössbauer, Fe X-ray absorption (XAS), and ^54/57Fe resonance Raman (rR) spectroscopies to confirm their formation and compare the axial ligand perturbation on the electronic and geometric structures of these heme iron(IV)-oxo species. Mössbauer studies confirmed that the axially ligated derivatives were iron(IV) and six-coordinate complexes. XAS and ^54/57Fe rR data correlated with slight elongation of the iron-oxo bond with increasing donation from the axial ligands. The first reported synthetic H-bonded iron(IV)-oxo heme systems were made in the presence of the protic Lewis acid, 2,6-lutidinium triflate (LutH⁺), with (or without) DCHIm. Mössbauer, rR, and XAS spectroscopic data indicated the formation of molecular Lewis acid ferryl adducts (rather than full protonation). The reduction potentials of these novel Lewismore »« less

Authors:

^[1];

^[2];

^[3];

^[2];

^[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)
Stanford Univ., Menlo Park, CA (United States)
Stanford Univ., Stanford, CA (United States); Stanford Univ., Menlo Park, CA (United States)

Publication Date:: 2019-03-12

Research Org.:: SLAC National Accelerator Lab., Menlo Park, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:: 1529246

Alternate Identifier(s):: OSTI ID: 1542892

Grant/Contract Number:: AC02-76SF00515; R01GM074785; F32GM122194; GM60353; P41GM103393; R01GM040392; AC02-05CH11231

Resource Type:: Accepted Manuscript

Journal Name:: Journal of the American Chemical Society

Additional Journal Information:: Journal Volume: 141; Journal Issue: 14; 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


                    Ehudin, Melanie A., Gee, Leland B., Sabuncu, Sinan, Braun, Augustin, Moënne-Loccoz, Pierre, Hedman, Britt, Hodgson, Keith O., Solomon, Edward I., and Karlin, Kenneth D. Tuning the Geometric and Electronic Structure of Synthetic High-Valent Heme Iron(IV)-Oxo Models in the Presence of a Lewis Acid and Various Axial Ligands.  United States: N. p., 2019. 
Web.  doi:10.1021/jacs.9b00795.

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                    Ehudin, Melanie A., Gee, Leland B., Sabuncu, Sinan, Braun, Augustin, Moënne-Loccoz, Pierre, Hedman, Britt, Hodgson, Keith O., Solomon, Edward I., & Karlin, Kenneth D. Tuning the Geometric and Electronic Structure of Synthetic High-Valent Heme Iron(IV)-Oxo Models in the Presence of a Lewis Acid and Various Axial Ligands.  United States.  https://doi.org/10.1021/jacs.9b00795

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                    Ehudin, Melanie A., Gee, Leland B., Sabuncu, Sinan, Braun, Augustin, Moënne-Loccoz, Pierre, Hedman, Britt, Hodgson, Keith O., Solomon, Edward I., and Karlin, Kenneth D. Tue .  
"Tuning the Geometric and Electronic Structure of Synthetic High-Valent Heme Iron(IV)-Oxo Models in the Presence of a Lewis Acid and Various Axial Ligands".  United States.  https://doi.org/10.1021/jacs.9b00795.  https://www.osti.gov/servlets/purl/1529246.

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@article{osti_1529246,

  title        = {Tuning the Geometric and Electronic Structure of Synthetic High-Valent Heme Iron(IV)-Oxo Models in the Presence of a Lewis Acid and Various Axial Ligands},

  author       = {Ehudin, Melanie A. and Gee, Leland B. and Sabuncu, Sinan and Braun, Augustin and Moënne-Loccoz, Pierre and Hedman, Britt and Hodgson, Keith O. and Solomon, Edward I. and Karlin, Kenneth D.},

  abstractNote = {High-valent ferryl species (e.g., (Por)FeIV═O, Cmpd-II) are observed or proposed key oxidizing intermediates in the catalytic cycles of heme-containing enzymes (P-450s, peroxidases, catalases, and cytochrome c oxidase) involved in biological respiration and oxidative metabolism. Herein, various axially ligated iron(IV)-oxo complexes were prepared to examine the influence of the identity of the base. These were generated by addition of various axial ligands (1,5-dicyclohexylimidazole (DCHIm), a tethered-imidazole system, and sodium derivatives of 3,5-dimethoxyphenolate and imidazolate). Characterization was carried out via UV–vis, electron paramagnetic resonance (EPR), 57Fe Mössbauer, Fe X-ray absorption (XAS), and 54/57Fe resonance Raman (rR) spectroscopies to confirm their formation and compare the axial ligand perturbation on the electronic and geometric structures of these heme iron(IV)-oxo species. Mössbauer studies confirmed that the axially ligated derivatives were iron(IV) and six-coordinate complexes. XAS and 54/57Fe rR data correlated with slight elongation of the iron-oxo bond with increasing donation from the axial ligands. The first reported synthetic H-bonded iron(IV)-oxo heme systems were made in the presence of the protic Lewis acid, 2,6-lutidinium triflate (LutH+), with (or without) DCHIm. Mössbauer, rR, and XAS spectroscopic data indicated the formation of molecular Lewis acid ferryl adducts (rather than full protonation). The reduction potentials of these novel Lewis acid adducts were bracketed through addition of outer-sphere reductants. The oxidizing capabilities of the ferryl species with or without Lewis acid vary drastically; addition of LutH+ to F8Cmpd-II (F8 = tetrakis(2,6-difluorophenyl)porphyrinate) increased its reduction potential by more than 890 mV, experimentally confirming that H-bonding interactions can increase the reactivity of ferryl species.},

  doi          = {10.1021/jacs.9b00795},

  journal      = {Journal of the American Chemical Society},

  number       = 14,

  volume       = 141,

  place        = {United States},

  year         = {2019},

  month        = {3}

}

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