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., J. Martin; Solomon, Edward I.

doi:10.1021/jacs.7b02997

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:

Park, Kiyoung ^[1]; Li, Ning ^[2]; Kwak, Yeonju ^[3];

^[3]; Bell, Caleb B. ^[3]; Liu, Lei V. ^[3]; Wong, Shaun D. ^[3]; Yoda, Yoshitaka ^[4]; Kitao, Shinji ^[5]; Seto, Makoto ^[5]; Hu, Michael ^[6]; Zhao, Jiyong ^[6];

^[2]; Bollinger, Jr., J. Martin ^[2];

^[7]

Stanford Univ., Stanford, CA (United States); KAIST, Daejeon (Republic of Korea)
Pennsylvania State Univ., University Park, PA (United States)
Stanford Univ., Stanford, CA (United States)
SPring-8/JASRO, Hyogo (Japan)
Kyoto Univ., Osaka (Japan)
Argonne National Lab. (ANL), Lemont, IL (United States)
Stanford Univ., Stanford, CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)

Publication Date:: 2017-05-01

Research Org.:: SLAC National Accelerator Lab., Menlo Park, CA (United States); Argonne National Lab. (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.  doi: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.  doi: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         = {2017},

  month        = {5}

}

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DOI: https://doi.org/10.1021/jacs.7b02997

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Works referencing / citing this record:

Origin of Nitric Oxide Reduction Activity in Flavo–Diiron NO Reductase: Key Roles of the Second Coordination Sphere
journal, February 2019

Lu, Jiarui; Bi, Bo; Lai, Wenzhen
Angewandte Chemie, Vol. 131, Issue 12
DOI: 10.1002/ange.201812343

Mechanism of the Dinuclear Iron Enzyme p ‐Aminobenzoate N‐oxygenase from Density Functional Calculations
journal, October 2018

Wei, Wen‐Jie; Siegbahn, Per E. M.; Liao, Rong‐Zhen
ChemCatChem, Vol. 11, Issue 1
DOI: 10.1002/cctc.201801072

Diiron monooxygenases in natural product biosynthesis
journal, January 2018

Komor, Anna J.; Jasniewski, Andrew J.; Que, Lawrence
Natural Product Reports, Vol. 35, Issue 7
DOI: 10.1039/c7np00061h

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

Abstract

Citation Formats

Origin of Nitric Oxide Reduction Activity in Flavo–Diiron NO Reductase: Key Roles of the Second Coordination Sphere journal, February 2019

Mechanism of the Dinuclear Iron Enzyme p ‐Aminobenzoate N‐oxygenase from Density Functional Calculations journal, October 2018

Diiron monooxygenases in natural product biosynthesis journal, January 2018

Origin of Nitric Oxide Reduction Activity in Flavo–Diiron NO Reductase: Key Roles of the Second Coordination Sphere
journal, February 2019

Mechanism of the Dinuclear Iron Enzyme p ‐Aminobenzoate N‐oxygenase from Density Functional Calculations
journal, October 2018

Diiron monooxygenases in natural product biosynthesis
journal, January 2018