Modeling the syn disposition of nitrogen donors in non-heme diiron enzymes. Synthesis, characterization, and hydrogen peroxide reactivity of diiron(III) complexes with the syn N-donor ligand H2BPG2DEV

Simone Friedle, Jeremy J. Kodanko, Anna J. Morys, Takahiro Hayashi, Pierre Moenne-Loccoz, Stephen J. Lippard

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

In order to model the syn disposition of histidine residues in carboxylate-bridged non-heme diiron enzymes, we prepared a new dinucleating ligand, H2BPG2DEv, that provides this geometric feature. The ligand incorporates biologically relevant carboxylate functionalities, which have not been explored as extensively as nitrogen-only analogues. Three novel oxo-bridged diiron(III) complexes, [Fe2(μ-O)(H2O) 2(BPG2DEV)](ClO4)2 (6), [Fe 2(μ-O)(μ-O2CAriPrO)(BPG 2DEV)](ClO4) (7), and [Fe2(μ-O)(μ-CO 3)(BPG2DEV)] (8), were prepared. Single-crystal X-ray structural characterization confirms that two pyridyl groups are bound syn with respect to the Fe-Fe vector in these compounds. The carbonato-bridged complex 8 forms quantitatively from 6 in a rapid reaction with gaseous CO2 in organic solvents. A common maroon-colored intermediate (λmax = 490 nm; ε = 1500 M-1 cm-1) forms in reactions of 6, 7, or 8 with H2O2 and NEt3 in CH 3CN/H2O solutions. Mass spectrometric analyses of this species, formed using 18O-labeled H2O2, indicate the presence of a peroxide ligand bound to the oxo-bridged diiron(III) center. The Mössbauer spectrum at 90 K of the EPR-silent intermediate exhibits a quadrupole doublet with δ = 0.58 mm/s and ΔEQ = 0.58 mm/s. The isomer shift is typical for a peroxodiiron(III) species, but the quadrupole splitting parameter is unusually small compared to those of related complexes. These Mössbauer parameters are comparable to those observed for a peroxo intermediate formed in the reaction of reduced toluene/o-xylene monooxygenase hydroxylase with dioxygen. Resonance Raman studies reveal an unusually low-energy O-O stretching mode in the peroxo intermediate that is consistent with a short diiron distance. Although peroxodiiron(III) intermediates generated from 6, 7, and 8 are poor O-atom-transfer catalysts, they display highly efficient catalase activity, with turnover numbers up to 10 000. In contrast to hydrogen peroxide reactions of diiron(III) complexes that lack a dinucleating ligand, the intermediates generated here could be re-formed in significant quantities after a second addition of H2O2, as observed spectroscopically and by mass spectrometry.

Original languageEnglish (US)
Pages (from-to)14508-14520
Number of pages13
JournalJournal of the American Chemical Society
Volume131
Issue number40
DOIs
StatePublished - Oct 14 2009

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Hydrogen peroxide
Hydrogen Peroxide
Nitrogen
Enzymes
Ligands
Peroxides
Carbon Monoxide
Xylene
Histidine
Isomers
Catalase
Organic solvents
Stretching
Mass spectrometry
Toluene
Paramagnetic resonance
Mass Spectrometry
X-Rays
Single crystals
Oxygen

ASJC Scopus subject areas

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

Cite this

Modeling the syn disposition of nitrogen donors in non-heme diiron enzymes. Synthesis, characterization, and hydrogen peroxide reactivity of diiron(III) complexes with the syn N-donor ligand H2BPG2DEV. / Friedle, Simone; Kodanko, Jeremy J.; Morys, Anna J.; Hayashi, Takahiro; Moenne-Loccoz, Pierre; Lippard, Stephen J.

In: Journal of the American Chemical Society, Vol. 131, No. 40, 14.10.2009, p. 14508-14520.

Research output: Contribution to journalArticle

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abstract = "In order to model the syn disposition of histidine residues in carboxylate-bridged non-heme diiron enzymes, we prepared a new dinucleating ligand, H2BPG2DEv, that provides this geometric feature. The ligand incorporates biologically relevant carboxylate functionalities, which have not been explored as extensively as nitrogen-only analogues. Three novel oxo-bridged diiron(III) complexes, [Fe2(μ-O)(H2O) 2(BPG2DEV)](ClO4)2 (6), [Fe 2(μ-O)(μ-O2CAriPrO)(BPG 2DEV)](ClO4) (7), and [Fe2(μ-O)(μ-CO 3)(BPG2DEV)] (8), were prepared. Single-crystal X-ray structural characterization confirms that two pyridyl groups are bound syn with respect to the Fe-Fe vector in these compounds. The carbonato-bridged complex 8 forms quantitatively from 6 in a rapid reaction with gaseous CO2 in organic solvents. A common maroon-colored intermediate (λmax = 490 nm; ε = 1500 M-1 cm-1) forms in reactions of 6, 7, or 8 with H2O2 and NEt3 in CH 3CN/H2O solutions. Mass spectrometric analyses of this species, formed using 18O-labeled H2O2, indicate the presence of a peroxide ligand bound to the oxo-bridged diiron(III) center. The M{\"o}ssbauer spectrum at 90 K of the EPR-silent intermediate exhibits a quadrupole doublet with δ = 0.58 mm/s and ΔEQ = 0.58 mm/s. The isomer shift is typical for a peroxodiiron(III) species, but the quadrupole splitting parameter is unusually small compared to those of related complexes. These M{\"o}ssbauer parameters are comparable to those observed for a peroxo intermediate formed in the reaction of reduced toluene/o-xylene monooxygenase hydroxylase with dioxygen. Resonance Raman studies reveal an unusually low-energy O-O stretching mode in the peroxo intermediate that is consistent with a short diiron distance. Although peroxodiiron(III) intermediates generated from 6, 7, and 8 are poor O-atom-transfer catalysts, they display highly efficient catalase activity, with turnover numbers up to 10 000. In contrast to hydrogen peroxide reactions of diiron(III) complexes that lack a dinucleating ligand, the intermediates generated here could be re-formed in significant quantities after a second addition of H2O2, as observed spectroscopically and by mass spectrometry.",
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AU - Friedle, Simone

AU - Kodanko, Jeremy J.

AU - Morys, Anna J.

AU - Hayashi, Takahiro

AU - Moenne-Loccoz, Pierre

AU - Lippard, Stephen J.

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N2 - In order to model the syn disposition of histidine residues in carboxylate-bridged non-heme diiron enzymes, we prepared a new dinucleating ligand, H2BPG2DEv, that provides this geometric feature. The ligand incorporates biologically relevant carboxylate functionalities, which have not been explored as extensively as nitrogen-only analogues. Three novel oxo-bridged diiron(III) complexes, [Fe2(μ-O)(H2O) 2(BPG2DEV)](ClO4)2 (6), [Fe 2(μ-O)(μ-O2CAriPrO)(BPG 2DEV)](ClO4) (7), and [Fe2(μ-O)(μ-CO 3)(BPG2DEV)] (8), were prepared. Single-crystal X-ray structural characterization confirms that two pyridyl groups are bound syn with respect to the Fe-Fe vector in these compounds. The carbonato-bridged complex 8 forms quantitatively from 6 in a rapid reaction with gaseous CO2 in organic solvents. A common maroon-colored intermediate (λmax = 490 nm; ε = 1500 M-1 cm-1) forms in reactions of 6, 7, or 8 with H2O2 and NEt3 in CH 3CN/H2O solutions. Mass spectrometric analyses of this species, formed using 18O-labeled H2O2, indicate the presence of a peroxide ligand bound to the oxo-bridged diiron(III) center. The Mössbauer spectrum at 90 K of the EPR-silent intermediate exhibits a quadrupole doublet with δ = 0.58 mm/s and ΔEQ = 0.58 mm/s. The isomer shift is typical for a peroxodiiron(III) species, but the quadrupole splitting parameter is unusually small compared to those of related complexes. These Mössbauer parameters are comparable to those observed for a peroxo intermediate formed in the reaction of reduced toluene/o-xylene monooxygenase hydroxylase with dioxygen. Resonance Raman studies reveal an unusually low-energy O-O stretching mode in the peroxo intermediate that is consistent with a short diiron distance. Although peroxodiiron(III) intermediates generated from 6, 7, and 8 are poor O-atom-transfer catalysts, they display highly efficient catalase activity, with turnover numbers up to 10 000. In contrast to hydrogen peroxide reactions of diiron(III) complexes that lack a dinucleating ligand, the intermediates generated here could be re-formed in significant quantities after a second addition of H2O2, as observed spectroscopically and by mass spectrometry.

AB - In order to model the syn disposition of histidine residues in carboxylate-bridged non-heme diiron enzymes, we prepared a new dinucleating ligand, H2BPG2DEv, that provides this geometric feature. The ligand incorporates biologically relevant carboxylate functionalities, which have not been explored as extensively as nitrogen-only analogues. Three novel oxo-bridged diiron(III) complexes, [Fe2(μ-O)(H2O) 2(BPG2DEV)](ClO4)2 (6), [Fe 2(μ-O)(μ-O2CAriPrO)(BPG 2DEV)](ClO4) (7), and [Fe2(μ-O)(μ-CO 3)(BPG2DEV)] (8), were prepared. Single-crystal X-ray structural characterization confirms that two pyridyl groups are bound syn with respect to the Fe-Fe vector in these compounds. The carbonato-bridged complex 8 forms quantitatively from 6 in a rapid reaction with gaseous CO2 in organic solvents. A common maroon-colored intermediate (λmax = 490 nm; ε = 1500 M-1 cm-1) forms in reactions of 6, 7, or 8 with H2O2 and NEt3 in CH 3CN/H2O solutions. Mass spectrometric analyses of this species, formed using 18O-labeled H2O2, indicate the presence of a peroxide ligand bound to the oxo-bridged diiron(III) center. The Mössbauer spectrum at 90 K of the EPR-silent intermediate exhibits a quadrupole doublet with δ = 0.58 mm/s and ΔEQ = 0.58 mm/s. The isomer shift is typical for a peroxodiiron(III) species, but the quadrupole splitting parameter is unusually small compared to those of related complexes. These Mössbauer parameters are comparable to those observed for a peroxo intermediate formed in the reaction of reduced toluene/o-xylene monooxygenase hydroxylase with dioxygen. Resonance Raman studies reveal an unusually low-energy O-O stretching mode in the peroxo intermediate that is consistent with a short diiron distance. Although peroxodiiron(III) intermediates generated from 6, 7, and 8 are poor O-atom-transfer catalysts, they display highly efficient catalase activity, with turnover numbers up to 10 000. In contrast to hydrogen peroxide reactions of diiron(III) complexes that lack a dinucleating ligand, the intermediates generated here could be re-formed in significant quantities after a second addition of H2O2, as observed spectroscopically and by mass spectrometry.

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