Heme-copper/dioxygen adduct formation relevant to cytochrome c oxidase

Spectroscopic characterization of [(6L)FeIII-(O 2 2-)-CuII]+

Reza A. Ghiladi, Hong Wei Huang, Pierre Moenne-Loccoz, Jay Stasser, Ninian Blackburn, Amina S. Woods, Robert J. Cotter, Christopher D. Incarvito, Arnold L. Rheingold, Kenneth D. Karlin

Research output: Contribution to journalArticle

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Abstract

In the further development and understanding of heme-copper dioxygen reactivity relevant to cytochrome c oxidase O2-reduction chemistry, we describe a high-spin, five-coordinate dioxygen (peroxo) adduct of an iron(II)-copper(I) complex, [(6L)FeIICu I](BArF20) (1), where 6L is a tetraarylporphyrinate with a tethered tris(2-pyridylmethyl)amine chelate for copper. Reaction of 1 with O2 in MeCN affords a remarkably stable [t1/2 (rt; MeCN)≈60 min] adduct, [(6L)Fe III-(O2 2-)-CuII]+ (2) [EPR silent; λmax = 418 (Soret), 561 nm], formulated as a peroxo complex based on manometry (1:O2 = 1:1; spectrophotometric titration, -40°C, MeCN), mass spectrometry {MALDI-TOF-MS: 16O2, m/z 1191 ([(6L)FeIII-( 16O2 2-)-CuII]+); 18O2, m/z 1195}, and resonance Raman spectroscopy (νv(O-O) = 788 cm-1; Δ16O 2/18O2 = 44 cm-1; Δ16O2/16/18O2 = 22 cm -1). 1H and 2H NMR spectroscopy (-40°C, MeCN) reveals that 2 is the first heme-copper peroxo complex which is high-spin, with downfield-shifted pyrrole resonances (δpyrrole = 75 ppm, s, br) and upfield shifted peaks at δ = -22, -35, and -40 ppm, similar to the pattern observed for the μ-oxo complex [(6L)Fe III-O-CuII](BArF) (3) (known S = 2 system, antiferromagnetically coupled high-spin FeIII and CuII). The corresponding magnetic moment measurement (Evans method, CD3CN, -40°C) also confirms the S = 2 spin state, with μB = 4.9. Structural insights were obtained from X-ray absorption spectroscopy, showing Fe-O (1.83 Å) and Cu-O (1.882 Å) bonds, and an Fe...Cu distance of 3.35(2) Å, suggestive of a μ-1,2-peroxo ligand present in 2. The reaction of 2 with cobaltocene gives 3, differing from the observed full reduction seen with other heme-Cu peroxo complexes. Finally, thermal decomposition of 2 yields 3, with concomitant release of 0.5 mol O2 per mol 2, as confirmed quantitatively by an alkaline pyrogallol dioxygen scavenging solution.

Original languageEnglish (US)
Pages (from-to)63-77
Number of pages15
JournalJournal of Biological Inorganic Chemistry
Volume10
Issue number1
DOIs
StatePublished - Jan 2005

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Electron Transport Complex IV
Heme
Copper
Oxygen
Pyrroles
X-Ray Absorption Spectroscopy
Pyrogallol
X ray absorption spectroscopy
Raman Spectrum Analysis
Matrix-Assisted Laser Desorption-Ionization Mass Spectrometry
Scavenging
Manometry
Magnetic moments
Titration
Nuclear magnetic resonance spectroscopy
Mass spectrometry
Paramagnetic resonance
Raman spectroscopy
Mass Spectrometry
Pyrolysis

Keywords

  • Dioxygen adduct
  • Heme-copper
  • Iron(II)-copper(I) complex
  • Mass spectrometry
  • Model compound
  • Peroxo complex
  • Resonance Raman spectroscopy

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Biochemistry

Cite this

Heme-copper/dioxygen adduct formation relevant to cytochrome c oxidase : Spectroscopic characterization of [(6L)FeIII-(O 2 2-)-CuII]+. / Ghiladi, Reza A.; Huang, Hong Wei; Moenne-Loccoz, Pierre; Stasser, Jay; Blackburn, Ninian; Woods, Amina S.; Cotter, Robert J.; Incarvito, Christopher D.; Rheingold, Arnold L.; Karlin, Kenneth D.

In: Journal of Biological Inorganic Chemistry, Vol. 10, No. 1, 01.2005, p. 63-77.

Research output: Contribution to journalArticle

Ghiladi, Reza A. ; Huang, Hong Wei ; Moenne-Loccoz, Pierre ; Stasser, Jay ; Blackburn, Ninian ; Woods, Amina S. ; Cotter, Robert J. ; Incarvito, Christopher D. ; Rheingold, Arnold L. ; Karlin, Kenneth D. / Heme-copper/dioxygen adduct formation relevant to cytochrome c oxidase : Spectroscopic characterization of [(6L)FeIII-(O 2 2-)-CuII]+. In: Journal of Biological Inorganic Chemistry. 2005 ; Vol. 10, No. 1. pp. 63-77.
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abstract = "In the further development and understanding of heme-copper dioxygen reactivity relevant to cytochrome c oxidase O2-reduction chemistry, we describe a high-spin, five-coordinate dioxygen (peroxo) adduct of an iron(II)-copper(I) complex, [(6L)FeIICu I](BArF20) (1), where 6L is a tetraarylporphyrinate with a tethered tris(2-pyridylmethyl)amine chelate for copper. Reaction of 1 with O2 in MeCN affords a remarkably stable [t1/2 (rt; MeCN)≈60 min] adduct, [(6L)Fe III-(O2 2-)-CuII]+ (2) [EPR silent; λmax = 418 (Soret), 561 nm], formulated as a peroxo complex based on manometry (1:O2 = 1:1; spectrophotometric titration, -40°C, MeCN), mass spectrometry {MALDI-TOF-MS: 16O2, m/z 1191 ([(6L)FeIII-( 16O2 2-)-CuII]+); 18O2, m/z 1195}, and resonance Raman spectroscopy (νv(O-O) = 788 cm-1; Δ16O 2/18O2 = 44 cm-1; Δ16O2/16/18O2 = 22 cm -1). 1H and 2H NMR spectroscopy (-40°C, MeCN) reveals that 2 is the first heme-copper peroxo complex which is high-spin, with downfield-shifted pyrrole resonances (δpyrrole = 75 ppm, s, br) and upfield shifted peaks at δ = -22, -35, and -40 ppm, similar to the pattern observed for the μ-oxo complex [(6L)Fe III-O-CuII](BArF) (3) (known S = 2 system, antiferromagnetically coupled high-spin FeIII and CuII). The corresponding magnetic moment measurement (Evans method, CD3CN, -40°C) also confirms the S = 2 spin state, with μB = 4.9. Structural insights were obtained from X-ray absorption spectroscopy, showing Fe-O (1.83 {\AA}) and Cu-O (1.882 {\AA}) bonds, and an Fe...Cu distance of 3.35(2) {\AA}, suggestive of a μ-1,2-peroxo ligand present in 2. The reaction of 2 with cobaltocene gives 3, differing from the observed full reduction seen with other heme-Cu peroxo complexes. Finally, thermal decomposition of 2 yields 3, with concomitant release of 0.5 mol O2 per mol 2, as confirmed quantitatively by an alkaline pyrogallol dioxygen scavenging solution.",
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T1 - Heme-copper/dioxygen adduct formation relevant to cytochrome c oxidase

T2 - Spectroscopic characterization of [(6L)FeIII-(O 2 2-)-CuII]+

AU - Ghiladi, Reza A.

AU - Huang, Hong Wei

AU - Moenne-Loccoz, Pierre

AU - Stasser, Jay

AU - Blackburn, Ninian

AU - Woods, Amina S.

AU - Cotter, Robert J.

AU - Incarvito, Christopher D.

AU - Rheingold, Arnold L.

AU - Karlin, Kenneth D.

PY - 2005/1

Y1 - 2005/1

N2 - In the further development and understanding of heme-copper dioxygen reactivity relevant to cytochrome c oxidase O2-reduction chemistry, we describe a high-spin, five-coordinate dioxygen (peroxo) adduct of an iron(II)-copper(I) complex, [(6L)FeIICu I](BArF20) (1), where 6L is a tetraarylporphyrinate with a tethered tris(2-pyridylmethyl)amine chelate for copper. Reaction of 1 with O2 in MeCN affords a remarkably stable [t1/2 (rt; MeCN)≈60 min] adduct, [(6L)Fe III-(O2 2-)-CuII]+ (2) [EPR silent; λmax = 418 (Soret), 561 nm], formulated as a peroxo complex based on manometry (1:O2 = 1:1; spectrophotometric titration, -40°C, MeCN), mass spectrometry {MALDI-TOF-MS: 16O2, m/z 1191 ([(6L)FeIII-( 16O2 2-)-CuII]+); 18O2, m/z 1195}, and resonance Raman spectroscopy (νv(O-O) = 788 cm-1; Δ16O 2/18O2 = 44 cm-1; Δ16O2/16/18O2 = 22 cm -1). 1H and 2H NMR spectroscopy (-40°C, MeCN) reveals that 2 is the first heme-copper peroxo complex which is high-spin, with downfield-shifted pyrrole resonances (δpyrrole = 75 ppm, s, br) and upfield shifted peaks at δ = -22, -35, and -40 ppm, similar to the pattern observed for the μ-oxo complex [(6L)Fe III-O-CuII](BArF) (3) (known S = 2 system, antiferromagnetically coupled high-spin FeIII and CuII). The corresponding magnetic moment measurement (Evans method, CD3CN, -40°C) also confirms the S = 2 spin state, with μB = 4.9. Structural insights were obtained from X-ray absorption spectroscopy, showing Fe-O (1.83 Å) and Cu-O (1.882 Å) bonds, and an Fe...Cu distance of 3.35(2) Å, suggestive of a μ-1,2-peroxo ligand present in 2. The reaction of 2 with cobaltocene gives 3, differing from the observed full reduction seen with other heme-Cu peroxo complexes. Finally, thermal decomposition of 2 yields 3, with concomitant release of 0.5 mol O2 per mol 2, as confirmed quantitatively by an alkaline pyrogallol dioxygen scavenging solution.

AB - In the further development and understanding of heme-copper dioxygen reactivity relevant to cytochrome c oxidase O2-reduction chemistry, we describe a high-spin, five-coordinate dioxygen (peroxo) adduct of an iron(II)-copper(I) complex, [(6L)FeIICu I](BArF20) (1), where 6L is a tetraarylporphyrinate with a tethered tris(2-pyridylmethyl)amine chelate for copper. Reaction of 1 with O2 in MeCN affords a remarkably stable [t1/2 (rt; MeCN)≈60 min] adduct, [(6L)Fe III-(O2 2-)-CuII]+ (2) [EPR silent; λmax = 418 (Soret), 561 nm], formulated as a peroxo complex based on manometry (1:O2 = 1:1; spectrophotometric titration, -40°C, MeCN), mass spectrometry {MALDI-TOF-MS: 16O2, m/z 1191 ([(6L)FeIII-( 16O2 2-)-CuII]+); 18O2, m/z 1195}, and resonance Raman spectroscopy (νv(O-O) = 788 cm-1; Δ16O 2/18O2 = 44 cm-1; Δ16O2/16/18O2 = 22 cm -1). 1H and 2H NMR spectroscopy (-40°C, MeCN) reveals that 2 is the first heme-copper peroxo complex which is high-spin, with downfield-shifted pyrrole resonances (δpyrrole = 75 ppm, s, br) and upfield shifted peaks at δ = -22, -35, and -40 ppm, similar to the pattern observed for the μ-oxo complex [(6L)Fe III-O-CuII](BArF) (3) (known S = 2 system, antiferromagnetically coupled high-spin FeIII and CuII). The corresponding magnetic moment measurement (Evans method, CD3CN, -40°C) also confirms the S = 2 spin state, with μB = 4.9. Structural insights were obtained from X-ray absorption spectroscopy, showing Fe-O (1.83 Å) and Cu-O (1.882 Å) bonds, and an Fe...Cu distance of 3.35(2) Å, suggestive of a μ-1,2-peroxo ligand present in 2. The reaction of 2 with cobaltocene gives 3, differing from the observed full reduction seen with other heme-Cu peroxo complexes. Finally, thermal decomposition of 2 yields 3, with concomitant release of 0.5 mol O2 per mol 2, as confirmed quantitatively by an alkaline pyrogallol dioxygen scavenging solution.

KW - Dioxygen adduct

KW - Heme-copper

KW - Iron(II)-copper(I) complex

KW - Mass spectrometry

KW - Model compound

KW - Peroxo complex

KW - Resonance Raman spectroscopy

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