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Crystal structures of alkylperoxo and anhydride intermediates in an intradiol ring-cleaving dioxygenase.

Knoot CJ, Purpero VM, Lipscomb JD
Proc Natl Acad Sci U S A 112 388-93 (2015)
Related entries: 4who, 4whp, 4whq, 4whs

Cited: 19 times
EuropePMC logo PMID: 25548185

Abstract

Intradiol aromatic ring-cleaving dioxygenases use an active site, nonheme Fe(3+) to activate O2 and catecholic substrates for reaction. The inability of Fe(3+) to directly bind O2 presents a mechanistic conundrum. The reaction mechanism of protocatechuate 3,4-dioxygenase is investigated here using the alternative substrate 4-fluorocatechol. This substrate is found to slow the reaction at several steps throughout the mechanistic cycle, allowing the intermediates to be detected in solution studies. When the reaction was initiated in an enzyme crystal, it was found to halt at one of two intermediates depending on the pH of the surrounding solution. The X-ray crystal structure of the intermediate at pH 6.5 revealed the key alkylperoxo-Fe(3+) species, and the anhydride-Fe(3+) intermediate was found for a crystal reacted at pH 8.5. Intermediates of these types have not been structurally characterized for intradiol dioxygenases, and they validate four decades of spectroscopic, kinetic, and computational studies. In contrast to our similar in crystallo crystallographic studies of an Fe(2+)-containing extradiol dioxygenase, no evidence for a superoxo or peroxo intermediate preceding the alkylperoxo was found. This observation and the lack of spectroscopic evidence for an Fe(2+) intermediate that could bind O2 are consistent with concerted formation of the alkylperoxo followed by Criegee rearrangement to yield the anhydride and ultimately ring-opened product. Structural comparison of the alkylperoxo intermediates from the intra- and extradiol dioxygenases provides a rationale for site specificity of ring cleavage.

Reviews - 4whr mentioned but not cited (1)

  1. Oxygen activation by mononuclear nonheme iron dioxygenases involved in the degradation of aromatics. Wang Y, Li J, Liu A. J Biol Inorg Chem 22 395-405 (2017)

Articles - 4whr mentioned but not cited (2)

  1. Crystal structures of alkylperoxo and anhydride intermediates in an intradiol ring-cleaving dioxygenase. Knoot CJ, Purpero VM, Lipscomb JD. Proc Natl Acad Sci U S A 112 388-393 (2015)
  2. Structural and functional characterization of an intradiol ring-cleavage dioxygenase from the polyphagous spider mite herbivore Tetranychus urticae Koch. Schlachter CR, Daneshian L, Amaya J, Klapper V, Wybouw N, Borowski T, Van Leeuwen T, Grbic V, Grbic M, Makris TM, Chruszcz M. Insect Biochem Mol Biol 107 19-30 (2019)


Reviews citing this publication (1)

  1. Catalytic strategies of the non-heme iron dependent oxygenases and their roles in plant biology. White MD, Flashman E. Curr Opin Chem Biol 31 126-135 (2016)

Articles citing this publication (15)

  1. Unique coupling of mono- and dioxygenase chemistries in a single active site promotes heme degradation. Matsui T, Nambu S, Goulding CW, Takahashi S, Fujii H, Ikeda-Saito M. Proc Natl Acad Sci U S A 113 3779-3784 (2016)
  2. Crystal structure of CmlI, the arylamine oxygenase from the chloramphenicol biosynthetic pathway. Knoot CJ, Kovaleva EG, Lipscomb JD. J Biol Inorg Chem 21 589-603 (2016)
  3. Observing 3-hydroxyanthranilate-3,4-dioxygenase in action through a crystalline lens. Wang Y, Liu KF, Yang Y, Davis I, Liu A. Proc Natl Acad Sci U S A 117 19720-19730 (2020)
  4. A Long-Lived Fe(III)-(Hydroperoxo) Intermediate in the Active H200C Variant of Homoprotocatechuate 2,3-Dioxygenase: Characterization by Mössbauer, Electron Paramagnetic Resonance, and Density Functional Theory Methods. Meier KK, Rogers MS, Kovaleva EG, Mbughuni MM, Bominaar EL, Lipscomb JD, Münck E. Inorg Chem 54 10269-10280 (2015)
  5. Hydrogen atom abstraction by synthetic heme ferric superoxide and hydroperoxide species. Singha A, Dey A. Chem Commun (Camb) 55 5591-5594 (2019)
  6. Mobile origin-licensing factors confer resistance to conflicts with RNA polymerase. Scherr MJ, Wahab SA, Remus D, Duderstadt KE. Cell Rep 38 110531 (2022)
  7. Substrate-Specific Coupling of O2 Activation to Hydroxylations of Aromatic Compounds by Rieske Non-heme Iron Dioxygenases. Pati SG, Bopp CE, Kohler HE, Hofstetter TB. ACS Catal 12 6444-6456 (2022)
  8. A new regime of heme-dependent aromatic oxygenase superfamily. Shin I, Wang Y, Liu A. Proc Natl Acad Sci U S A 118 e2106561118 (2021)
  9. Catalytic Mechanism of Salicylate Dioxygenase: QM/MM Simulations Reveal the Origin of Unexpected Regioselectivity of the Ring Cleavage. Roy S, Kästner J. Chemistry 23 8949-8962 (2017)
  10. A novel catalytic heme cofactor in SfmD with a single thioether bond and a bis-His ligand set revealed by a de novo crystal structural and spectroscopic study. Shin I, Davis I, Nieves-Merced K, Wang Y, McHardy S, Liu A. Chem Sci 12 3984-3998 (2021)
  11. Pointed-end processive elongation of actin filaments by Vibrio effectors VopF and VopL. Kudryashova E, Ankita, Ulrichs H, Shekhar S, Kudryashov DS. Sci Adv 8 eadc9239 (2022)
  12. The role of spin states in the catalytic mechanism of the intra- and extradiol cleavage of catechols by O2. Stepanović S, Angelone D, Gruden M, Swart M. Org Biomol Chem 15 7860-7868 (2017)
  13. Electronic, Magnetic, and Redox Properties and O2 Reactivity of Iron(II) and Nickel(II) o-Semiquinonate Complexes of a Tris(thioether) Ligand: Uncovering the Intradiol Cleaving Reactivity of an Iron(II) o-Semiquinonate Complex. Wang P, Killian MM, Saber MR, Qiu T, Yap GPA, Popescu CV, Rosenthal J, Dunbar KR, Brunold TC, Riordan CG. Inorg Chem 56 10481-10495 (2017)
  14. Charge Maintenance during Catalysis in Nonheme Iron Oxygenases. Traore ES, Liu A. ACS Catal 12 6191-6208 (2022)
  15. Structure-guided insights into heterocyclic ring-cleavage catalysis of the non-heme Fe (II) dioxygenase NicX. Liu G, Zhao YL, He F, Zhang P, Ouyang X, Tang H, Xu P. Nat Commun 12 1301 (2021)


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