Synthesis and characterization of alkanethiolate-coordinated iron porphyrins and their dioxygen adducts as models for the active center of cytochrome p450

Direct evidence for hydrogen bonding to bound dioxygen

Fumito Tani, M. Matsu-Ura, S. Nakayama, M. Ichimura, N. Nakamura, Y. Naruta

Research output: Contribution to journalArticle

61 Citations (Scopus)

Abstract

Two kind of novel cytochrome P450 models, which have alkanethiolate axial ligands and hydroxyl groups inside molecular cavities, were designed and synthesized as functional O2 binding systems. A superstructured porphyrin, designated as "twin-coronet" porphyrin, was used as the common framework of the model complexes. This porphyrin bears four binaphthalene bridges on the both sides and forms two pockets surrounded by the bulky aromatic rings. Thiobenzyloxy and thioglycolate moieties, which contain an alkanethiolate group exhibiting various electron-donating abilities and degrees of bulkiness, were covalently linked to twin-coronet porphyrin to yield thiolate-coordinated hemes, TCP-TB and TCP-TG (twin-coronet porphyrin with thiobenzyloxy and thioglycolate groups), respectively. Both ferric complexes exhibited high stability during usual experimental manipulation under air and were characterized by MS, UV/vis, ESR spectroscopies, and CV. The ESR spectra exhibited low-spin signals (TCP-TB: g = 2.334, 2.210, 1.959; TCP-TG: g = 2.313, 2.209, 1.966). The cyclic voltammogram of TCP-TB in CH3CN gave a quasi-reversible wave which corresponds to the FeIII/FeII redox couple: Ep/2 = -1.35 V (vs Fc/Fc+). On the other hand, TCP-TG showed a fine reversible wave: E1/2 (FeIII/FeII) = -1.12 V. The stable dioxygen adducts were formed in the reaction of the ferric complexes with KO2 under an oxygen atmosphere and characterized by UV/vis and resonance Raman (RR) spectroscopies. In the RR spectra, the v(O-O) bands of the dioxygen adducts were observed at 1138 cm-1 (TCP-TB) and 1137 cm-1 (TCP-TG). The hypothesis that hydrogen bonding between the bound oxygen and the hydroxyl groups of the binaphthyl moieties could increase their stability was verified by RR spectroscopy. When all hydroxyl groups were deuterated, only the frequencies of the v(O-O) bands were upshifted by 2 cm-1 without any perturbation in the porphyrin skeleton. This work shows the first direct evidence for a hydrogen bond to dioxygen in an oxy form of a thiolate-coordinated heme model system. These results are discussed in context of the process of dioxygen binding and activation in cytochrome P450.

Original languageEnglish
Pages (from-to)1133-1142
Number of pages10
JournalJournal of the American Chemical Society
Volume123
Issue number6
DOIs
Publication statusPublished - Feb 14 2001

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Porphyrins
Hydrogen Bonding
Cytochrome P-450 Enzyme System
Hydrogen bonds
Iron
Thioglycolates
Oxygen
Hydroxyl Radical
Raman Spectrum Analysis
Heme
Paramagnetic resonance
Raman spectroscopy
Atmosphere
Skeleton
Oxidation-Reduction
Raman scattering
Hydrogen
Spectrum Analysis
Chemical activation
Ligands

All Science Journal Classification (ASJC) codes

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

Cite this

@article{c3dc41c5ed7f47aea74017cc07a56afd,
title = "Synthesis and characterization of alkanethiolate-coordinated iron porphyrins and their dioxygen adducts as models for the active center of cytochrome p450: Direct evidence for hydrogen bonding to bound dioxygen",
abstract = "Two kind of novel cytochrome P450 models, which have alkanethiolate axial ligands and hydroxyl groups inside molecular cavities, were designed and synthesized as functional O2 binding systems. A superstructured porphyrin, designated as {"}twin-coronet{"} porphyrin, was used as the common framework of the model complexes. This porphyrin bears four binaphthalene bridges on the both sides and forms two pockets surrounded by the bulky aromatic rings. Thiobenzyloxy and thioglycolate moieties, which contain an alkanethiolate group exhibiting various electron-donating abilities and degrees of bulkiness, were covalently linked to twin-coronet porphyrin to yield thiolate-coordinated hemes, TCP-TB and TCP-TG (twin-coronet porphyrin with thiobenzyloxy and thioglycolate groups), respectively. Both ferric complexes exhibited high stability during usual experimental manipulation under air and were characterized by MS, UV/vis, ESR spectroscopies, and CV. The ESR spectra exhibited low-spin signals (TCP-TB: g = 2.334, 2.210, 1.959; TCP-TG: g = 2.313, 2.209, 1.966). The cyclic voltammogram of TCP-TB in CH3CN gave a quasi-reversible wave which corresponds to the FeIII/FeII redox couple: Ep/2 = -1.35 V (vs Fc/Fc+). On the other hand, TCP-TG showed a fine reversible wave: E1/2 (FeIII/FeII) = -1.12 V. The stable dioxygen adducts were formed in the reaction of the ferric complexes with KO2 under an oxygen atmosphere and characterized by UV/vis and resonance Raman (RR) spectroscopies. In the RR spectra, the v(O-O) bands of the dioxygen adducts were observed at 1138 cm-1 (TCP-TB) and 1137 cm-1 (TCP-TG). The hypothesis that hydrogen bonding between the bound oxygen and the hydroxyl groups of the binaphthyl moieties could increase their stability was verified by RR spectroscopy. When all hydroxyl groups were deuterated, only the frequencies of the v(O-O) bands were upshifted by 2 cm-1 without any perturbation in the porphyrin skeleton. This work shows the first direct evidence for a hydrogen bond to dioxygen in an oxy form of a thiolate-coordinated heme model system. These results are discussed in context of the process of dioxygen binding and activation in cytochrome P450.",
author = "Fumito Tani and M. Matsu-Ura and S. Nakayama and M. Ichimura and N. Nakamura and Y. Naruta",
year = "2001",
month = "2",
day = "14",
doi = "10.1021/ja003430y",
language = "English",
volume = "123",
pages = "1133--1142",
journal = "Journal of the American Chemical Society",
issn = "0002-7863",
publisher = "American Chemical Society",
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TY - JOUR

T1 - Synthesis and characterization of alkanethiolate-coordinated iron porphyrins and their dioxygen adducts as models for the active center of cytochrome p450

T2 - Direct evidence for hydrogen bonding to bound dioxygen

AU - Tani, Fumito

AU - Matsu-Ura, M.

AU - Nakayama, S.

AU - Ichimura, M.

AU - Nakamura, N.

AU - Naruta, Y.

PY - 2001/2/14

Y1 - 2001/2/14

N2 - Two kind of novel cytochrome P450 models, which have alkanethiolate axial ligands and hydroxyl groups inside molecular cavities, were designed and synthesized as functional O2 binding systems. A superstructured porphyrin, designated as "twin-coronet" porphyrin, was used as the common framework of the model complexes. This porphyrin bears four binaphthalene bridges on the both sides and forms two pockets surrounded by the bulky aromatic rings. Thiobenzyloxy and thioglycolate moieties, which contain an alkanethiolate group exhibiting various electron-donating abilities and degrees of bulkiness, were covalently linked to twin-coronet porphyrin to yield thiolate-coordinated hemes, TCP-TB and TCP-TG (twin-coronet porphyrin with thiobenzyloxy and thioglycolate groups), respectively. Both ferric complexes exhibited high stability during usual experimental manipulation under air and were characterized by MS, UV/vis, ESR spectroscopies, and CV. The ESR spectra exhibited low-spin signals (TCP-TB: g = 2.334, 2.210, 1.959; TCP-TG: g = 2.313, 2.209, 1.966). The cyclic voltammogram of TCP-TB in CH3CN gave a quasi-reversible wave which corresponds to the FeIII/FeII redox couple: Ep/2 = -1.35 V (vs Fc/Fc+). On the other hand, TCP-TG showed a fine reversible wave: E1/2 (FeIII/FeII) = -1.12 V. The stable dioxygen adducts were formed in the reaction of the ferric complexes with KO2 under an oxygen atmosphere and characterized by UV/vis and resonance Raman (RR) spectroscopies. In the RR spectra, the v(O-O) bands of the dioxygen adducts were observed at 1138 cm-1 (TCP-TB) and 1137 cm-1 (TCP-TG). The hypothesis that hydrogen bonding between the bound oxygen and the hydroxyl groups of the binaphthyl moieties could increase their stability was verified by RR spectroscopy. When all hydroxyl groups were deuterated, only the frequencies of the v(O-O) bands were upshifted by 2 cm-1 without any perturbation in the porphyrin skeleton. This work shows the first direct evidence for a hydrogen bond to dioxygen in an oxy form of a thiolate-coordinated heme model system. These results are discussed in context of the process of dioxygen binding and activation in cytochrome P450.

AB - Two kind of novel cytochrome P450 models, which have alkanethiolate axial ligands and hydroxyl groups inside molecular cavities, were designed and synthesized as functional O2 binding systems. A superstructured porphyrin, designated as "twin-coronet" porphyrin, was used as the common framework of the model complexes. This porphyrin bears four binaphthalene bridges on the both sides and forms two pockets surrounded by the bulky aromatic rings. Thiobenzyloxy and thioglycolate moieties, which contain an alkanethiolate group exhibiting various electron-donating abilities and degrees of bulkiness, were covalently linked to twin-coronet porphyrin to yield thiolate-coordinated hemes, TCP-TB and TCP-TG (twin-coronet porphyrin with thiobenzyloxy and thioglycolate groups), respectively. Both ferric complexes exhibited high stability during usual experimental manipulation under air and were characterized by MS, UV/vis, ESR spectroscopies, and CV. The ESR spectra exhibited low-spin signals (TCP-TB: g = 2.334, 2.210, 1.959; TCP-TG: g = 2.313, 2.209, 1.966). The cyclic voltammogram of TCP-TB in CH3CN gave a quasi-reversible wave which corresponds to the FeIII/FeII redox couple: Ep/2 = -1.35 V (vs Fc/Fc+). On the other hand, TCP-TG showed a fine reversible wave: E1/2 (FeIII/FeII) = -1.12 V. The stable dioxygen adducts were formed in the reaction of the ferric complexes with KO2 under an oxygen atmosphere and characterized by UV/vis and resonance Raman (RR) spectroscopies. In the RR spectra, the v(O-O) bands of the dioxygen adducts were observed at 1138 cm-1 (TCP-TB) and 1137 cm-1 (TCP-TG). The hypothesis that hydrogen bonding between the bound oxygen and the hydroxyl groups of the binaphthyl moieties could increase their stability was verified by RR spectroscopy. When all hydroxyl groups were deuterated, only the frequencies of the v(O-O) bands were upshifted by 2 cm-1 without any perturbation in the porphyrin skeleton. This work shows the first direct evidence for a hydrogen bond to dioxygen in an oxy form of a thiolate-coordinated heme model system. These results are discussed in context of the process of dioxygen binding and activation in cytochrome P450.

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U2 - 10.1021/ja003430y

DO - 10.1021/ja003430y

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EP - 1142

JO - Journal of the American Chemical Society

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SN - 0002-7863

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