Mechanism of Oxygen Activation in a Flavin-Dependent Monooxygenase: A Nearly Barrierless Formation of C4a-Hydroperoxyflavin via Proton-Coupled Electron Transfer.

Understanding how flavin-dependent enzymes activate oxygen for their oxidation and oxygenation reactions is one of the most challenging issues in flavoenzymology. Density functional calculations and transient kinetics were performed to investigate the mechanism of oxygen activation in the oxygenase...

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Publicado en:Journal of the American Chemical Society Vol. 137; no. 29; pp. 9363 - 9375
Autores principales: Visitsatthawong, Surawit, Chenprakhon, Pirom, Chaiyen, Pimchai, Surawatanawong, Panida
Formato: Artículo
Publicado: American Chemical Society 7/29/2015
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Acceso en línea:Ver este registro en EBSCOhost
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      dt: 7/29/2015
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      pub: American Chemical Society
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        108955530
        10.1021/jacs.5b04328
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        atl: Mechanism of Oxygen Activation in a Flavin-Dependent Monooxygenase: A Nearly Barrierless Formation of C4a-Hydroperoxyflavin via Proton-Coupled Electron Transfer.
      aug:
        au:
          Visitsatthawong, Surawit
          Chenprakhon, Pirom
          Chaiyen, Pimchai
          Surawatanawong, Panida
        affil:
          Department of Chemistry and Center of Excellence for Innovation in Chemistry, Faculty of Science, Mahidol University, Bangkok 10400, Thailand
          Institute for Innovative Learning, Mahidol University, Bangkok 10400, Thailand
          Department of Biochemistry and Center of Excellence in Protein Structure and Function, Faculty of Science, Mahidol University, Bangkok 10400, Thailand
      su:
        Activation (Chemistry)
        Flavins
        Monooxygenases
        Hydroperoxides
        Charge exchange
        Proton-proton interactions
      sug:
        subj:
          Activation (Chemistry)
          Flavins
          Monooxygenases
          Hydroperoxides
          Charge exchange
          Proton-proton interactions
      ab: Understanding how flavin-dependent enzymes activate oxygen for their oxidation and oxygenation reactions is one of the most challenging issues in flavoenzymology. Density functional calculations and transient kinetics were performed to investigate the mechanism of oxygen activation in the oxygenase component (C) of p-hydroxyphenylacetate 3-hydroxylase (HPAH). We found that the protonation of dioxygen by His396 via a proton-coupled electron transfer mechanism is the key step in the formation of the triplet diradical complex of flavin semiquinone and ·OOH. This complex undergoes intersystem crossing to form the open-shell singlet diradical complex before it forms the closed-shell singlet C4a-hydroperoxyflavin intermediate (C4aOOH). Notably, density functional calculations indicated that the formation of C4aOOH is nearly barrierless, possibly facilitated by the active site arrangement in which His396 positions the proximal oxygen of the ·OOH in an optimum position to directly attack the C4a atom of the isoalloxazine ring. The nearly barrierless formation of C4aOOH agrees well with the experimental results; based on transient kinetics and Eyring plot analyses, the enthalpy of activation for the formation of C4aOOH is only 1.4 kcal/mol and the formation of C4aOOH by C is fast (~10 M s at 4 °C). The calculations identified Ser171 as the key residue that stabilizes C4aOOH by accepting a hydrogen bond from the H(N5) of the isoalloxazine ring. Both Ser171 and Trp112 facilitate HO elimination by donating hydrogen bonds to the proximal oxygen of the OOH moiety during the proton transfer. According to our combined theoretical and experimental studies, the existence of a positively charged general acid at the position optimized for facilitating the proton-coupled electron transfer has emerged as an important catalytic feature for the oxygen activation process in flavin-dependent enzymes.
      pubtype: Academic Journal
      doctype: Article
      src: R
    language: English
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