Circular dichroism, magnetic circular dichroism, and variable temperature variable field magnetic circular dichroism studies of biferrous and mixed-valent myo -inositol oxygenase

Insights into substrate activation of O2 reactivity

Rae Ana Snyder, Caleb B. Bell, Yinghui Diao, Carsten Krebs, Joseph M. Bollinger, Jr., Edward I. Solomon

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Abstract

myo-Inositol oxygenase (MIOX) catalyzes the 4e- oxidation of myo-inositol (MI) to d-glucuronate using a substrate activated Fe(II)Fe(III) site. The biferrous and Fe(II)Fe(III) forms of MIOX were studied with circular dichroism (CD), magnetic circular dichroism (MCD), and variable temperature variable field (VTVH) MCD spectroscopies. The MCD spectrum of biferrous MIOX shows two ligand field (LF) transitions near 10000 cm-1, split by ∼2000 cm-1, characteristic of six coordinate (6C) Fe(II) sites, indicating that the modest reactivity of the biferrous form toward O2 can be attributed to the saturated coordination of both irons. Upon oxidation to the Fe(II)Fe(III) state, MIOX shows two LF transitions in the ∼10000 cm-1 region, again implying a coordinatively saturated Fe(II) site. Upon MI binding, these split in energy to 5200 and 11200 cm-1, showing that MI binding causes the Fe(II) to become coordinatively unsaturated. VTVH MCD magnetization curves of unbound and MI-bound Fe(II)Fe(III) forms show that upon substrate binding, the isotherms become more nested, requiring that the exchange coupling and ferrous zero-field splitting (ZFS) both decrease in magnitude. These results imply that MI binds to the ferric site, weakening the Fe(III)-μ-OH bond and strengthening the Fe(II)-μ-OH bond. This perturbation results in the release of a coordinated water from the Fe(II) that enables its O2 activation.

Original languageEnglish (US)
Pages (from-to)15851-15863
Number of pages13
JournalJournal of the American Chemical Society
Volume135
Issue number42
DOIs
StatePublished - Oct 31 2013

Fingerprint

Inositol Oxygenase
Dichroism
Inositol
Magnetic Fields
Circular Dichroism
Chemical activation
Magnetic fields
Temperature
Substrates
Ligands
Circular dichroism spectroscopy
Oxidation
Exchange coupling
Glucuronic Acid
Isotherms
Magnetization
Iron
Spectrum Analysis
Oxygenases
Water

All Science Journal Classification (ASJC) codes

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

Cite this

@article{7a3bdba846704829a3ae1eede25ecf15,
title = "Circular dichroism, magnetic circular dichroism, and variable temperature variable field magnetic circular dichroism studies of biferrous and mixed-valent myo -inositol oxygenase: Insights into substrate activation of O2 reactivity",
abstract = "myo-Inositol oxygenase (MIOX) catalyzes the 4e- oxidation of myo-inositol (MI) to d-glucuronate using a substrate activated Fe(II)Fe(III) site. The biferrous and Fe(II)Fe(III) forms of MIOX were studied with circular dichroism (CD), magnetic circular dichroism (MCD), and variable temperature variable field (VTVH) MCD spectroscopies. The MCD spectrum of biferrous MIOX shows two ligand field (LF) transitions near 10000 cm-1, split by ∼2000 cm-1, characteristic of six coordinate (6C) Fe(II) sites, indicating that the modest reactivity of the biferrous form toward O2 can be attributed to the saturated coordination of both irons. Upon oxidation to the Fe(II)Fe(III) state, MIOX shows two LF transitions in the ∼10000 cm-1 region, again implying a coordinatively saturated Fe(II) site. Upon MI binding, these split in energy to 5200 and 11200 cm-1, showing that MI binding causes the Fe(II) to become coordinatively unsaturated. VTVH MCD magnetization curves of unbound and MI-bound Fe(II)Fe(III) forms show that upon substrate binding, the isotherms become more nested, requiring that the exchange coupling and ferrous zero-field splitting (ZFS) both decrease in magnitude. These results imply that MI binds to the ferric site, weakening the Fe(III)-μ-OH bond and strengthening the Fe(II)-μ-OH bond. This perturbation results in the release of a coordinated water from the Fe(II) that enables its O2 activation.",
author = "Snyder, {Rae Ana} and Bell, {Caleb B.} and Yinghui Diao and Carsten Krebs and {Bollinger, Jr.}, {Joseph M.} and Solomon, {Edward I.}",
year = "2013",
month = "10",
day = "31",
doi = "10.1021/ja406635k",
language = "English (US)",
volume = "135",
pages = "15851--15863",
journal = "Journal of the American Chemical Society",
issn = "0002-7863",
publisher = "American Chemical Society",
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TY - JOUR

T1 - Circular dichroism, magnetic circular dichroism, and variable temperature variable field magnetic circular dichroism studies of biferrous and mixed-valent myo -inositol oxygenase

T2 - Insights into substrate activation of O2 reactivity

AU - Snyder, Rae Ana

AU - Bell, Caleb B.

AU - Diao, Yinghui

AU - Krebs, Carsten

AU - Bollinger, Jr., Joseph M.

AU - Solomon, Edward I.

PY - 2013/10/31

Y1 - 2013/10/31

N2 - myo-Inositol oxygenase (MIOX) catalyzes the 4e- oxidation of myo-inositol (MI) to d-glucuronate using a substrate activated Fe(II)Fe(III) site. The biferrous and Fe(II)Fe(III) forms of MIOX were studied with circular dichroism (CD), magnetic circular dichroism (MCD), and variable temperature variable field (VTVH) MCD spectroscopies. The MCD spectrum of biferrous MIOX shows two ligand field (LF) transitions near 10000 cm-1, split by ∼2000 cm-1, characteristic of six coordinate (6C) Fe(II) sites, indicating that the modest reactivity of the biferrous form toward O2 can be attributed to the saturated coordination of both irons. Upon oxidation to the Fe(II)Fe(III) state, MIOX shows two LF transitions in the ∼10000 cm-1 region, again implying a coordinatively saturated Fe(II) site. Upon MI binding, these split in energy to 5200 and 11200 cm-1, showing that MI binding causes the Fe(II) to become coordinatively unsaturated. VTVH MCD magnetization curves of unbound and MI-bound Fe(II)Fe(III) forms show that upon substrate binding, the isotherms become more nested, requiring that the exchange coupling and ferrous zero-field splitting (ZFS) both decrease in magnitude. These results imply that MI binds to the ferric site, weakening the Fe(III)-μ-OH bond and strengthening the Fe(II)-μ-OH bond. This perturbation results in the release of a coordinated water from the Fe(II) that enables its O2 activation.

AB - myo-Inositol oxygenase (MIOX) catalyzes the 4e- oxidation of myo-inositol (MI) to d-glucuronate using a substrate activated Fe(II)Fe(III) site. The biferrous and Fe(II)Fe(III) forms of MIOX were studied with circular dichroism (CD), magnetic circular dichroism (MCD), and variable temperature variable field (VTVH) MCD spectroscopies. The MCD spectrum of biferrous MIOX shows two ligand field (LF) transitions near 10000 cm-1, split by ∼2000 cm-1, characteristic of six coordinate (6C) Fe(II) sites, indicating that the modest reactivity of the biferrous form toward O2 can be attributed to the saturated coordination of both irons. Upon oxidation to the Fe(II)Fe(III) state, MIOX shows two LF transitions in the ∼10000 cm-1 region, again implying a coordinatively saturated Fe(II) site. Upon MI binding, these split in energy to 5200 and 11200 cm-1, showing that MI binding causes the Fe(II) to become coordinatively unsaturated. VTVH MCD magnetization curves of unbound and MI-bound Fe(II)Fe(III) forms show that upon substrate binding, the isotherms become more nested, requiring that the exchange coupling and ferrous zero-field splitting (ZFS) both decrease in magnitude. These results imply that MI binds to the ferric site, weakening the Fe(III)-μ-OH bond and strengthening the Fe(II)-μ-OH bond. This perturbation results in the release of a coordinated water from the Fe(II) that enables its O2 activation.

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