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

Abstract

Binuclear non-heme iron enzymes activate O-2 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 O-2. 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.

Authors:
 [1];  [2];  [3]; ORCiD logo [3];  [3];  [3];  [3];  [4];  [5];  [5];  [6];  [6]; ORCiD logo [2];  [2]; ORCiD logo [7]
+ Show Author Affiliations
  1. Stanford Univ., Stanford, CA (United States); KAIST, Daejeon (Republic of Korea)
  2. Pennsylvania State Univ., University Park, PA (United States)
  3. Stanford Univ., Stanford, CA (United States)
  4. SPring-8/JASRO, Hyogo (Japan)
  5. Kyoto Univ., Osaka (Japan)
  6. Argonne National Lab. (ANL), Lemont, IL (United States)
  7. Stanford Univ., Stanford, CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)
Publication Date:
Research Org.:
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States); Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); National Science Foundation (NSF); Japan Society for the Promotion of Science (JSPS) - KAKENHI
OSTI Identifier:
1369431
Alternate Identifier(s):
OSTI ID: 1377396
Grant/Contract Number:  
AC02-76SF00515; CHE-1058931; MCB1404866; 24221005; GM40392; AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Journal of the American Chemical Society
Additional Journal Information:
Journal Volume: 139; Journal Issue: 20; 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; O2 activation; diiron site; peroxo intermediate; nuclear resonance vibrational spectroscopy; O2; activation

Citation Formats

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., J. Martin, and Solomon, Edward I. Peroxide Activation for Electrophilic Reactivity by the Binuclear Non-heme Iron Enzyme AurF. United States: N. p., 2017. Web. doi:10.1021/jacs.7b02997.
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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., J. Martin, & Solomon, Edward I. Peroxide Activation for Electrophilic Reactivity by the Binuclear Non-heme Iron Enzyme AurF. United States. https://doi.org/10.1021/jacs.7b02997
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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., J. Martin, and Solomon, Edward I. Mon . "Peroxide Activation for Electrophilic Reactivity by the Binuclear Non-heme Iron Enzyme AurF". United States. https://doi.org/10.1021/jacs.7b02997. https://www.osti.gov/servlets/purl/1369431.
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@article{osti_1369431,
title = {Peroxide Activation for Electrophilic Reactivity by the Binuclear Non-heme Iron Enzyme AurF},
author = {Park, Kiyoung and Li, Ning and Kwak, Yeonju and Srnec, Martin and Bell, Caleb B. and Liu, Lei V. and Wong, Shaun D. and Yoda, Yoshitaka and Kitao, Shinji and Seto, Makoto and Hu, Michael and Zhao, Jiyong and Krebs, Carsten and Bollinger, Jr., J. Martin and Solomon, Edward I.},
abstractNote = {Binuclear non-heme iron enzymes activate O-2 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 O-2. 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.},
doi = {10.1021/jacs.7b02997},
journal = {Journal of the American Chemical Society},
number = 20,
volume = 139,
place = {United States},
year = {Mon May 01 00:00:00 EDT 2017},
month = {Mon May 01 00:00:00 EDT 2017}
}
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https://doi.org/10.1021/jacs.7b02997
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