Peroxide Activation for Electrophilic Reactivity by the Binuclear Non-heme Iron Enzyme AurF

Kiyoung Park, Ning Li, Yeonju Kwak, Martin Srnec, Caleb B. Bell, Lei V. Liu, Shaun D. Wong, Yoshitaka Yoda, Shinji Kitao, Makoto Seto, Michael Hu, Jiyong Zhao, Carsten Krebs, Joseph M. Bollinger, Jr., Edward I. Solomon

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

Binuclear non-heme iron enzymes activate O2 for diverse chemistries that include oxygenation of organic substrates and hydrogen atom abstraction. This process often involves the formation of peroxo-bridged biferric intermediates, only some of which can perform electrophilic reactions. To elucidate the geometric and electronic structural requirements to activate peroxo reactivity, the active peroxo intermediate in 4-aminobenzoate N-oxygenase (AurF) has been characterized spectroscopically and computationally. A magnetic circular dichroism study of reduced AurF shows that its electronic and geometric structures are poised to react rapidly with O2. Nuclear resonance vibrational spectroscopic definition of the peroxo intermediate formed in this reaction shows that the active intermediate has a protonated peroxo bridge. Density functional theory computations on the structure established here show that the protonation activates peroxide for electrophilic/single-electron-transfer reactivity. This activation of peroxide by protonation is likely also relevant to the reactive peroxo intermediates in other binuclear non-heme iron enzymes.

Original languageEnglish (US)
Pages (from-to)7062-7070
Number of pages9
JournalJournal of the American Chemical Society
Volume139
Issue number20
DOIs
StatePublished - May 24 2017

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Protonation
Peroxides
para-Aminobenzoates
Iron
Enzymes
Chemical activation
Oxygenases
Oxygenation
Dichroism
Circular Dichroism
Density functional theory
Hydrogen
Electrons
Atoms
Substrates

All Science Journal Classification (ASJC) codes

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

Cite this

Park, K., Li, N., Kwak, Y., Srnec, M., Bell, C. B., Liu, L. V., ... Solomon, E. I. (2017). Peroxide Activation for Electrophilic Reactivity by the Binuclear Non-heme Iron Enzyme AurF. Journal of the American Chemical Society, 139(20), 7062-7070. https://doi.org/10.1021/jacs.7b02997
Park, Kiyoung ; Li, Ning ; Kwak, Yeonju ; Srnec, Martin ; Bell, Caleb B. ; Liu, Lei V. ; Wong, Shaun D. ; Yoda, Yoshitaka ; Kitao, Shinji ; Seto, Makoto ; Hu, Michael ; Zhao, Jiyong ; Krebs, Carsten ; Bollinger, Jr., Joseph M. ; Solomon, Edward I. / Peroxide Activation for Electrophilic Reactivity by the Binuclear Non-heme Iron Enzyme AurF. In: Journal of the American Chemical Society. 2017 ; Vol. 139, No. 20. pp. 7062-7070.
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abstract = "Binuclear non-heme iron enzymes activate O2 for diverse chemistries that include oxygenation of organic substrates and hydrogen atom abstraction. This process often involves the formation of peroxo-bridged biferric intermediates, only some of which can perform electrophilic reactions. To elucidate the geometric and electronic structural requirements to activate peroxo reactivity, the active peroxo intermediate in 4-aminobenzoate N-oxygenase (AurF) has been characterized spectroscopically and computationally. A magnetic circular dichroism study of reduced AurF shows that its electronic and geometric structures are poised to react rapidly with O2. Nuclear resonance vibrational spectroscopic definition of the peroxo intermediate formed in this reaction shows that the active intermediate has a protonated peroxo bridge. Density functional theory computations on the structure established here show that the protonation activates peroxide for electrophilic/single-electron-transfer reactivity. This activation of peroxide by protonation is likely also relevant to the reactive peroxo intermediates in other binuclear non-heme iron enzymes.",
author = "Kiyoung Park and Ning Li and Yeonju Kwak and Martin Srnec and Bell, {Caleb B.} and Liu, {Lei V.} and Wong, {Shaun D.} and Yoshitaka Yoda and Shinji Kitao and Makoto Seto and Michael Hu and Jiyong Zhao and Carsten Krebs and {Bollinger, Jr.}, {Joseph M.} and Solomon, {Edward I.}",
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Park, K, Li, N, Kwak, Y, Srnec, M, Bell, CB, Liu, LV, Wong, SD, Yoda, Y, Kitao, S, Seto, M, Hu, M, Zhao, J, Krebs, C, Bollinger, Jr., JM & Solomon, EI 2017, 'Peroxide Activation for Electrophilic Reactivity by the Binuclear Non-heme Iron Enzyme AurF', Journal of the American Chemical Society, vol. 139, no. 20, pp. 7062-7070. https://doi.org/10.1021/jacs.7b02997

Peroxide Activation for Electrophilic Reactivity by the Binuclear Non-heme Iron Enzyme AurF. / Park, Kiyoung; Li, Ning; Kwak, Yeonju; Srnec, Martin; Bell, Caleb B.; Liu, Lei V.; Wong, Shaun D.; Yoda, Yoshitaka; Kitao, Shinji; Seto, Makoto; Hu, Michael; Zhao, Jiyong; Krebs, Carsten; Bollinger, Jr., Joseph M.; Solomon, Edward I.

In: Journal of the American Chemical Society, Vol. 139, No. 20, 24.05.2017, p. 7062-7070.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Peroxide Activation for Electrophilic Reactivity by the Binuclear Non-heme Iron Enzyme AurF

AU - Park, Kiyoung

AU - Li, Ning

AU - Kwak, Yeonju

AU - Srnec, Martin

AU - Bell, Caleb B.

AU - Liu, Lei V.

AU - Wong, Shaun D.

AU - Yoda, Yoshitaka

AU - Kitao, Shinji

AU - Seto, Makoto

AU - Hu, Michael

AU - Zhao, Jiyong

AU - Krebs, Carsten

AU - Bollinger, Jr., Joseph M.

AU - Solomon, Edward I.

PY - 2017/5/24

Y1 - 2017/5/24

N2 - Binuclear non-heme iron enzymes activate O2 for diverse chemistries that include oxygenation of organic substrates and hydrogen atom abstraction. This process often involves the formation of peroxo-bridged biferric intermediates, only some of which can perform electrophilic reactions. To elucidate the geometric and electronic structural requirements to activate peroxo reactivity, the active peroxo intermediate in 4-aminobenzoate N-oxygenase (AurF) has been characterized spectroscopically and computationally. A magnetic circular dichroism study of reduced AurF shows that its electronic and geometric structures are poised to react rapidly with O2. Nuclear resonance vibrational spectroscopic definition of the peroxo intermediate formed in this reaction shows that the active intermediate has a protonated peroxo bridge. Density functional theory computations on the structure established here show that the protonation activates peroxide for electrophilic/single-electron-transfer reactivity. This activation of peroxide by protonation is likely also relevant to the reactive peroxo intermediates in other binuclear non-heme iron enzymes.

AB - Binuclear non-heme iron enzymes activate O2 for diverse chemistries that include oxygenation of organic substrates and hydrogen atom abstraction. This process often involves the formation of peroxo-bridged biferric intermediates, only some of which can perform electrophilic reactions. To elucidate the geometric and electronic structural requirements to activate peroxo reactivity, the active peroxo intermediate in 4-aminobenzoate N-oxygenase (AurF) has been characterized spectroscopically and computationally. A magnetic circular dichroism study of reduced AurF shows that its electronic and geometric structures are poised to react rapidly with O2. Nuclear resonance vibrational spectroscopic definition of the peroxo intermediate formed in this reaction shows that the active intermediate has a protonated peroxo bridge. Density functional theory computations on the structure established here show that the protonation activates peroxide for electrophilic/single-electron-transfer reactivity. This activation of peroxide by protonation is likely also relevant to the reactive peroxo intermediates in other binuclear non-heme iron enzymes.

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