XAS structural comparisons of reversibly interconvertible oxo- and hydroxo-bridged heme-copper oxidase model compounds

Stephen Fox, Alaganandan Nanthakumar, Mårten Wikström, Kenneth D. Karlin, Ninian Blackburn

Research output: Contribution to journalArticle

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Abstract

In this study on model compounds for the iron-copper dinuclear center in heme-copper oxidases, we (i) detail the synthesis and reversible acid-base interconversion of μ-oxo and μ-hydroxo complexes [(F8-TPP)FeIII-(O2-)-CuII(TMPA) - (1) and [(F8-TPP)FeIII-(OH-)-Cu II(TMPA)]2+ (2) [F8-TPP = tetrakis(2,6-difluorophenyl)-porhyrinate(2-), TMPA = tris[(2-pyridylmethyl)amine]; (ii) compare their physical properties; (iii) establish the structure of 2 using XAS (X-ray absorption spectroscopy), a novel application of a three-body two-edge multiple-scattering (MS) analysis of ligand connectivity; and (iv) compare the XAS of 2 with those of 1 and an enzyme preparation. Complex 1 was prepared by reaction of [(TMPA)CuII(CH3CN)]2+ (3) and [(F8-TPP)FeIII-OH] (4) with triethylamine in acetonitrile (>70% yield). Salts 2-(ClO4)2 and 2-(CF3SO3)2 were synthesized (>60% yield) by addition of 3 with 4 in dichloroethane or by protonation of 1 with triflic acid. In a 1H-NMR spectroscopic titration (298 K) with triflic acid, the pyrrole 65 ppm resonance for 1 progressively converts to one near 70 ppm (71.5 for triflate, 68.5 for perchlorate), diagnostic of 2. The protonation-deprotonation rate is slow on the NMR time scale, the 1H-NMR spectral properties are consistent with antiferromagnetically coupled high-spin iron(III) and Cu(II) ions (S = 2 ground state), and the interaction is weaker in 2 (2, 5.5 ± 0.1 μB; 1, 5.1 ± 0.1 μB, Evans method). UV-vis spectroscopy was also used to monitor the conversion of 2 (Soret, 410 nm) to 1 (434 nm) using Et3N. The aqueous pXa for deprotonation of 2 is estimated as 8 ± 2.5. Both Fe and Cu K-edge XAS was performed on 1, 2, and μ-peroxo complex [{(TMPA)Cu}2(O2)]2+ (5). The strong MS interaction observed in the EXAFS of 1 is due to the nearly linear Fe-O-Cu moiety. Least-squares refinement of the Cu K-EXAFS of 1 gives Cu⋯Fe = 3.56 ± 0.03 Å, 〈Cu-O-Fe = 176 ± 5°, Cu-O = 1.83 ± 0.02 Å; the Fe K-EXAFS analysis gives Fe-O = 1.72 ± 0.02 Å, Fe⋯Cu = 3.54 ± 0.05 Å, 〈Fe-O-Cu = 172 ± 10°. The intense Fe-Cu (or Cu-Fe) feature is lacking in 2, but the iron-edge spectra do reveal a weaker MS ascribed to the Fe-Cu interaction. The Cu-O(H) and Fe-O(H) bonds are elongated in 2 (1.89 ± 0.02 Å and 1.87 ± 0.02 Å, respectively), with Fe⋯Cu = 3.66 ± 0.03 Å. This protonated complex is bent; 〈Fe-O(H)-Cu = 157 ± 5°. An EXAFS comparison with an enzyme preparation of the quinol oxidase aa3-600 from Bacillus subtilis supports the notion that μ-OH- complex 2 may be a good heme-Cu enzyme model for the resting state and/or turnover intermediate.

Original languageEnglish (US)
Pages (from-to)24-34
Number of pages11
JournalJournal of the American Chemical Society
Volume118
Issue number1
StatePublished - Jan 10 1996

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X-Ray Absorption Spectroscopy
X ray absorption spectroscopy
Multiple scattering
Heme
Deprotonation
Enzymes
Protonation
Nuclear magnetic resonance
Iron
Copper
Acids
Iron Compounds
Ethylene Dichlorides
Pyrroles
Bacilli
Bacillus subtilis
Least-Squares Analysis
Ultraviolet spectroscopy
Acetonitrile
Titration

ASJC Scopus subject areas

  • Chemistry(all)

Cite this

XAS structural comparisons of reversibly interconvertible oxo- and hydroxo-bridged heme-copper oxidase model compounds. / Fox, Stephen; Nanthakumar, Alaganandan; Wikström, Mårten; Karlin, Kenneth D.; Blackburn, Ninian.

In: Journal of the American Chemical Society, Vol. 118, No. 1, 10.01.1996, p. 24-34.

Research output: Contribution to journalArticle

Fox, Stephen ; Nanthakumar, Alaganandan ; Wikström, Mårten ; Karlin, Kenneth D. ; Blackburn, Ninian. / XAS structural comparisons of reversibly interconvertible oxo- and hydroxo-bridged heme-copper oxidase model compounds. In: Journal of the American Chemical Society. 1996 ; Vol. 118, No. 1. pp. 24-34.
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title = "XAS structural comparisons of reversibly interconvertible oxo- and hydroxo-bridged heme-copper oxidase model compounds",
abstract = "In this study on model compounds for the iron-copper dinuclear center in heme-copper oxidases, we (i) detail the synthesis and reversible acid-base interconversion of μ-oxo and μ-hydroxo complexes [(F8-TPP)FeIII-(O2-)-CuII(TMPA) - (1) and [(F8-TPP)FeIII-(OH-)-Cu II(TMPA)]2+ (2) [F8-TPP = tetrakis(2,6-difluorophenyl)-porhyrinate(2-), TMPA = tris[(2-pyridylmethyl)amine]; (ii) compare their physical properties; (iii) establish the structure of 2 using XAS (X-ray absorption spectroscopy), a novel application of a three-body two-edge multiple-scattering (MS) analysis of ligand connectivity; and (iv) compare the XAS of 2 with those of 1 and an enzyme preparation. Complex 1 was prepared by reaction of [(TMPA)CuII(CH3CN)]2+ (3) and [(F8-TPP)FeIII-OH] (4) with triethylamine in acetonitrile (>70{\%} yield). Salts 2-(ClO4)2 and 2-(CF3SO3)2 were synthesized (>60{\%} yield) by addition of 3 with 4 in dichloroethane or by protonation of 1 with triflic acid. In a 1H-NMR spectroscopic titration (298 K) with triflic acid, the pyrrole 65 ppm resonance for 1 progressively converts to one near 70 ppm (71.5 for triflate, 68.5 for perchlorate), diagnostic of 2. The protonation-deprotonation rate is slow on the NMR time scale, the 1H-NMR spectral properties are consistent with antiferromagnetically coupled high-spin iron(III) and Cu(II) ions (S = 2 ground state), and the interaction is weaker in 2 (2, 5.5 ± 0.1 μB; 1, 5.1 ± 0.1 μB, Evans method). UV-vis spectroscopy was also used to monitor the conversion of 2 (Soret, 410 nm) to 1 (434 nm) using Et3N. The aqueous pXa for deprotonation of 2 is estimated as 8 ± 2.5. Both Fe and Cu K-edge XAS was performed on 1, 2, and μ-peroxo complex [{(TMPA)Cu}2(O2)]2+ (5). The strong MS interaction observed in the EXAFS of 1 is due to the nearly linear Fe-O-Cu moiety. Least-squares refinement of the Cu K-EXAFS of 1 gives Cu⋯Fe = 3.56 ± 0.03 {\AA}, 〈Cu-O-Fe = 176 ± 5°, Cu-O = 1.83 ± 0.02 {\AA}; the Fe K-EXAFS analysis gives Fe-O = 1.72 ± 0.02 {\AA}, Fe⋯Cu = 3.54 ± 0.05 {\AA}, 〈Fe-O-Cu = 172 ± 10°. The intense Fe-Cu (or Cu-Fe) feature is lacking in 2, but the iron-edge spectra do reveal a weaker MS ascribed to the Fe-Cu interaction. The Cu-O(H) and Fe-O(H) bonds are elongated in 2 (1.89 ± 0.02 {\AA} and 1.87 ± 0.02 {\AA}, respectively), with Fe⋯Cu = 3.66 ± 0.03 {\AA}. This protonated complex is bent; 〈Fe-O(H)-Cu = 157 ± 5°. An EXAFS comparison with an enzyme preparation of the quinol oxidase aa3-600 from Bacillus subtilis supports the notion that μ-OH- complex 2 may be a good heme-Cu enzyme model for the resting state and/or turnover intermediate.",
author = "Stephen Fox and Alaganandan Nanthakumar and M{\aa}rten Wikstr{\"o}m and Karlin, {Kenneth D.} and Ninian Blackburn",
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TY - JOUR

T1 - XAS structural comparisons of reversibly interconvertible oxo- and hydroxo-bridged heme-copper oxidase model compounds

AU - Fox, Stephen

AU - Nanthakumar, Alaganandan

AU - Wikström, Mårten

AU - Karlin, Kenneth D.

AU - Blackburn, Ninian

PY - 1996/1/10

Y1 - 1996/1/10

N2 - In this study on model compounds for the iron-copper dinuclear center in heme-copper oxidases, we (i) detail the synthesis and reversible acid-base interconversion of μ-oxo and μ-hydroxo complexes [(F8-TPP)FeIII-(O2-)-CuII(TMPA) - (1) and [(F8-TPP)FeIII-(OH-)-Cu II(TMPA)]2+ (2) [F8-TPP = tetrakis(2,6-difluorophenyl)-porhyrinate(2-), TMPA = tris[(2-pyridylmethyl)amine]; (ii) compare their physical properties; (iii) establish the structure of 2 using XAS (X-ray absorption spectroscopy), a novel application of a three-body two-edge multiple-scattering (MS) analysis of ligand connectivity; and (iv) compare the XAS of 2 with those of 1 and an enzyme preparation. Complex 1 was prepared by reaction of [(TMPA)CuII(CH3CN)]2+ (3) and [(F8-TPP)FeIII-OH] (4) with triethylamine in acetonitrile (>70% yield). Salts 2-(ClO4)2 and 2-(CF3SO3)2 were synthesized (>60% yield) by addition of 3 with 4 in dichloroethane or by protonation of 1 with triflic acid. In a 1H-NMR spectroscopic titration (298 K) with triflic acid, the pyrrole 65 ppm resonance for 1 progressively converts to one near 70 ppm (71.5 for triflate, 68.5 for perchlorate), diagnostic of 2. The protonation-deprotonation rate is slow on the NMR time scale, the 1H-NMR spectral properties are consistent with antiferromagnetically coupled high-spin iron(III) and Cu(II) ions (S = 2 ground state), and the interaction is weaker in 2 (2, 5.5 ± 0.1 μB; 1, 5.1 ± 0.1 μB, Evans method). UV-vis spectroscopy was also used to monitor the conversion of 2 (Soret, 410 nm) to 1 (434 nm) using Et3N. The aqueous pXa for deprotonation of 2 is estimated as 8 ± 2.5. Both Fe and Cu K-edge XAS was performed on 1, 2, and μ-peroxo complex [{(TMPA)Cu}2(O2)]2+ (5). The strong MS interaction observed in the EXAFS of 1 is due to the nearly linear Fe-O-Cu moiety. Least-squares refinement of the Cu K-EXAFS of 1 gives Cu⋯Fe = 3.56 ± 0.03 Å, 〈Cu-O-Fe = 176 ± 5°, Cu-O = 1.83 ± 0.02 Å; the Fe K-EXAFS analysis gives Fe-O = 1.72 ± 0.02 Å, Fe⋯Cu = 3.54 ± 0.05 Å, 〈Fe-O-Cu = 172 ± 10°. The intense Fe-Cu (or Cu-Fe) feature is lacking in 2, but the iron-edge spectra do reveal a weaker MS ascribed to the Fe-Cu interaction. The Cu-O(H) and Fe-O(H) bonds are elongated in 2 (1.89 ± 0.02 Å and 1.87 ± 0.02 Å, respectively), with Fe⋯Cu = 3.66 ± 0.03 Å. This protonated complex is bent; 〈Fe-O(H)-Cu = 157 ± 5°. An EXAFS comparison with an enzyme preparation of the quinol oxidase aa3-600 from Bacillus subtilis supports the notion that μ-OH- complex 2 may be a good heme-Cu enzyme model for the resting state and/or turnover intermediate.

AB - In this study on model compounds for the iron-copper dinuclear center in heme-copper oxidases, we (i) detail the synthesis and reversible acid-base interconversion of μ-oxo and μ-hydroxo complexes [(F8-TPP)FeIII-(O2-)-CuII(TMPA) - (1) and [(F8-TPP)FeIII-(OH-)-Cu II(TMPA)]2+ (2) [F8-TPP = tetrakis(2,6-difluorophenyl)-porhyrinate(2-), TMPA = tris[(2-pyridylmethyl)amine]; (ii) compare their physical properties; (iii) establish the structure of 2 using XAS (X-ray absorption spectroscopy), a novel application of a three-body two-edge multiple-scattering (MS) analysis of ligand connectivity; and (iv) compare the XAS of 2 with those of 1 and an enzyme preparation. Complex 1 was prepared by reaction of [(TMPA)CuII(CH3CN)]2+ (3) and [(F8-TPP)FeIII-OH] (4) with triethylamine in acetonitrile (>70% yield). Salts 2-(ClO4)2 and 2-(CF3SO3)2 were synthesized (>60% yield) by addition of 3 with 4 in dichloroethane or by protonation of 1 with triflic acid. In a 1H-NMR spectroscopic titration (298 K) with triflic acid, the pyrrole 65 ppm resonance for 1 progressively converts to one near 70 ppm (71.5 for triflate, 68.5 for perchlorate), diagnostic of 2. The protonation-deprotonation rate is slow on the NMR time scale, the 1H-NMR spectral properties are consistent with antiferromagnetically coupled high-spin iron(III) and Cu(II) ions (S = 2 ground state), and the interaction is weaker in 2 (2, 5.5 ± 0.1 μB; 1, 5.1 ± 0.1 μB, Evans method). UV-vis spectroscopy was also used to monitor the conversion of 2 (Soret, 410 nm) to 1 (434 nm) using Et3N. The aqueous pXa for deprotonation of 2 is estimated as 8 ± 2.5. Both Fe and Cu K-edge XAS was performed on 1, 2, and μ-peroxo complex [{(TMPA)Cu}2(O2)]2+ (5). The strong MS interaction observed in the EXAFS of 1 is due to the nearly linear Fe-O-Cu moiety. Least-squares refinement of the Cu K-EXAFS of 1 gives Cu⋯Fe = 3.56 ± 0.03 Å, 〈Cu-O-Fe = 176 ± 5°, Cu-O = 1.83 ± 0.02 Å; the Fe K-EXAFS analysis gives Fe-O = 1.72 ± 0.02 Å, Fe⋯Cu = 3.54 ± 0.05 Å, 〈Fe-O-Cu = 172 ± 10°. The intense Fe-Cu (or Cu-Fe) feature is lacking in 2, but the iron-edge spectra do reveal a weaker MS ascribed to the Fe-Cu interaction. The Cu-O(H) and Fe-O(H) bonds are elongated in 2 (1.89 ± 0.02 Å and 1.87 ± 0.02 Å, respectively), with Fe⋯Cu = 3.66 ± 0.03 Å. This protonated complex is bent; 〈Fe-O(H)-Cu = 157 ± 5°. An EXAFS comparison with an enzyme preparation of the quinol oxidase aa3-600 from Bacillus subtilis supports the notion that μ-OH- complex 2 may be a good heme-Cu enzyme model for the resting state and/or turnover intermediate.

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