Structural and functional models of the dimanganese catalase enzymes. 3. Kinetics and mechanism of hydrogen peroxide dismutation

P. J. Pessiki, G Charles Dismukes

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Abstract

The mechanism of peroxide dismutation by synthetic mimics of the dimanganese catalase enzymes has been investigated by steady-state kinetic methods. These compounds, [LMn2 II,II(μ-X)](ClO4)2, X- = CH3CO2 - and ClCH2CO2 -, were found to share structural, redox, and spectroscopic properties analogous to the catalase enzymes (Pessiki et al. J. Am. Chem. Soc. preceding paper in this issue). The dismutation mechanism proceeds by two consecutive two-electron steps: H2O2 + 2e- + 2H+ → 2H2O and H2O2 → O2 + 2e- + 2H+ which are coupled to redox transformation of the catalyst: Mn2 III,III ↔ Mn2 II,II. The μ-carboxylate derivatives are inactive, but in the presence of water they autocatalytically dismutate H2O2 after an initial hydration reaction in which the μ-carboxylate ligand appears to dissociate, as judged by inhibition with acetate. The observed steady-state rate expression, v(O2) = kobs[H2O2]1-[(LMn 2(CH3CO2)(ClO4)2], 1 kobs = 0.23 M-1 s-1, exhibits the same molecularities with respect to peroxide and catalyst as observed for the enzyme from T. thermophilus, for which kobs is 107 faster. In contrast, the rate law for the μ-Cl- derivative, LMn2Cl3, is second order in [H2O2] (Mathur et al. J. Am. Chem. Soc. 1987, 109, 5227). EPR and optical studies support a mechanism involving oxidation to a Mn2 III,III intermediate and against formation of the mixed valence states, Mn2 II,III and Mn2 III,IV. The rate-limiting step for the model complexes is ascribed to either the inner-sphere two-electron intramolecular oxidation of the peroxide complex, [LMn2 II,II(H2O2)]3+ → [LMn2 III,III(OH)2]3+, or a proton dissociation reaction coupled to this oxidation. Subsequent two-electron reduction to the Mn2 II,II oxidation state via a second H2O2 molecule occurs 7-9-fold faster and completes the catalytic cycle. The 107 faster rate for the enzyme is proposed to reflect either a substantially lower reduction potential for the MnCatIII,III oxidation state, the availability of active site residues which function as proton donors and acceptors, or both.

Original languageEnglish
Pages (from-to)898-903
Number of pages6
JournalJournal of the American Chemical Society
Volume116
Issue number3
Publication statusPublished - Feb 9 1994

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Enzyme kinetics
Structural Models
Hydrogen peroxide
Catalase
Hydrogen Peroxide
Peroxides
Enzymes
Oxidation
Kinetics
Electrons
Oxidation-Reduction
Protons
Derivatives
Catalysts
Catalytic Domain
Acetates
Hydration
Paramagnetic resonance
Ligands
Water

Keywords

  • Catalase
  • Enzyme mechanism
  • Hydrogen peroxide
  • Kinetics
  • Manganese

ASJC Scopus subject areas

  • Chemistry(all)

Cite this

@article{b3c607290ae44e97acf5980c4c484ecf,
title = "Structural and functional models of the dimanganese catalase enzymes. 3. Kinetics and mechanism of hydrogen peroxide dismutation",
abstract = "The mechanism of peroxide dismutation by synthetic mimics of the dimanganese catalase enzymes has been investigated by steady-state kinetic methods. These compounds, [LMn2 II,II(μ-X)](ClO4)2, X- = CH3CO2 - and ClCH2CO2 -, were found to share structural, redox, and spectroscopic properties analogous to the catalase enzymes (Pessiki et al. J. Am. Chem. Soc. preceding paper in this issue). The dismutation mechanism proceeds by two consecutive two-electron steps: H2O2 + 2e- + 2H+ → 2H2O and H2O2 → O2 + 2e- + 2H+ which are coupled to redox transformation of the catalyst: Mn2 III,III ↔ Mn2 II,II. The μ-carboxylate derivatives are inactive, but in the presence of water they autocatalytically dismutate H2O2 after an initial hydration reaction in which the μ-carboxylate ligand appears to dissociate, as judged by inhibition with acetate. The observed steady-state rate expression, v(O2) = kobs[H2O2]1-[(LMn 2(CH3CO2)(ClO4)2], 1 kobs = 0.23 M-1 s-1, exhibits the same molecularities with respect to peroxide and catalyst as observed for the enzyme from T. thermophilus, for which kobs is 107 faster. In contrast, the rate law for the μ-Cl- derivative, LMn2Cl3, is second order in [H2O2] (Mathur et al. J. Am. Chem. Soc. 1987, 109, 5227). EPR and optical studies support a mechanism involving oxidation to a Mn2 III,III intermediate and against formation of the mixed valence states, Mn2 II,III and Mn2 III,IV. The rate-limiting step for the model complexes is ascribed to either the inner-sphere two-electron intramolecular oxidation of the peroxide complex, [LMn2 II,II(H2O2)]3+ → [LMn2 III,III(OH)2]3+, or a proton dissociation reaction coupled to this oxidation. Subsequent two-electron reduction to the Mn2 II,II oxidation state via a second H2O2 molecule occurs 7-9-fold faster and completes the catalytic cycle. The 107 faster rate for the enzyme is proposed to reflect either a substantially lower reduction potential for the MnCatIII,III oxidation state, the availability of active site residues which function as proton donors and acceptors, or both.",
keywords = "Catalase, Enzyme mechanism, Hydrogen peroxide, Kinetics, Manganese",
author = "Pessiki, {P. J.} and Dismukes, {G Charles}",
year = "1994",
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TY - JOUR

T1 - Structural and functional models of the dimanganese catalase enzymes. 3. Kinetics and mechanism of hydrogen peroxide dismutation

AU - Pessiki, P. J.

AU - Dismukes, G Charles

PY - 1994/2/9

Y1 - 1994/2/9

N2 - The mechanism of peroxide dismutation by synthetic mimics of the dimanganese catalase enzymes has been investigated by steady-state kinetic methods. These compounds, [LMn2 II,II(μ-X)](ClO4)2, X- = CH3CO2 - and ClCH2CO2 -, were found to share structural, redox, and spectroscopic properties analogous to the catalase enzymes (Pessiki et al. J. Am. Chem. Soc. preceding paper in this issue). The dismutation mechanism proceeds by two consecutive two-electron steps: H2O2 + 2e- + 2H+ → 2H2O and H2O2 → O2 + 2e- + 2H+ which are coupled to redox transformation of the catalyst: Mn2 III,III ↔ Mn2 II,II. The μ-carboxylate derivatives are inactive, but in the presence of water they autocatalytically dismutate H2O2 after an initial hydration reaction in which the μ-carboxylate ligand appears to dissociate, as judged by inhibition with acetate. The observed steady-state rate expression, v(O2) = kobs[H2O2]1-[(LMn 2(CH3CO2)(ClO4)2], 1 kobs = 0.23 M-1 s-1, exhibits the same molecularities with respect to peroxide and catalyst as observed for the enzyme from T. thermophilus, for which kobs is 107 faster. In contrast, the rate law for the μ-Cl- derivative, LMn2Cl3, is second order in [H2O2] (Mathur et al. J. Am. Chem. Soc. 1987, 109, 5227). EPR and optical studies support a mechanism involving oxidation to a Mn2 III,III intermediate and against formation of the mixed valence states, Mn2 II,III and Mn2 III,IV. The rate-limiting step for the model complexes is ascribed to either the inner-sphere two-electron intramolecular oxidation of the peroxide complex, [LMn2 II,II(H2O2)]3+ → [LMn2 III,III(OH)2]3+, or a proton dissociation reaction coupled to this oxidation. Subsequent two-electron reduction to the Mn2 II,II oxidation state via a second H2O2 molecule occurs 7-9-fold faster and completes the catalytic cycle. The 107 faster rate for the enzyme is proposed to reflect either a substantially lower reduction potential for the MnCatIII,III oxidation state, the availability of active site residues which function as proton donors and acceptors, or both.

AB - The mechanism of peroxide dismutation by synthetic mimics of the dimanganese catalase enzymes has been investigated by steady-state kinetic methods. These compounds, [LMn2 II,II(μ-X)](ClO4)2, X- = CH3CO2 - and ClCH2CO2 -, were found to share structural, redox, and spectroscopic properties analogous to the catalase enzymes (Pessiki et al. J. Am. Chem. Soc. preceding paper in this issue). The dismutation mechanism proceeds by two consecutive two-electron steps: H2O2 + 2e- + 2H+ → 2H2O and H2O2 → O2 + 2e- + 2H+ which are coupled to redox transformation of the catalyst: Mn2 III,III ↔ Mn2 II,II. The μ-carboxylate derivatives are inactive, but in the presence of water they autocatalytically dismutate H2O2 after an initial hydration reaction in which the μ-carboxylate ligand appears to dissociate, as judged by inhibition with acetate. The observed steady-state rate expression, v(O2) = kobs[H2O2]1-[(LMn 2(CH3CO2)(ClO4)2], 1 kobs = 0.23 M-1 s-1, exhibits the same molecularities with respect to peroxide and catalyst as observed for the enzyme from T. thermophilus, for which kobs is 107 faster. In contrast, the rate law for the μ-Cl- derivative, LMn2Cl3, is second order in [H2O2] (Mathur et al. J. Am. Chem. Soc. 1987, 109, 5227). EPR and optical studies support a mechanism involving oxidation to a Mn2 III,III intermediate and against formation of the mixed valence states, Mn2 II,III and Mn2 III,IV. The rate-limiting step for the model complexes is ascribed to either the inner-sphere two-electron intramolecular oxidation of the peroxide complex, [LMn2 II,II(H2O2)]3+ → [LMn2 III,III(OH)2]3+, or a proton dissociation reaction coupled to this oxidation. Subsequent two-electron reduction to the Mn2 II,II oxidation state via a second H2O2 molecule occurs 7-9-fold faster and completes the catalytic cycle. The 107 faster rate for the enzyme is proposed to reflect either a substantially lower reduction potential for the MnCatIII,III oxidation state, the availability of active site residues which function as proton donors and acceptors, or both.

KW - Catalase

KW - Enzyme mechanism

KW - Hydrogen peroxide

KW - Kinetics

KW - Manganese

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VL - 116

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EP - 903

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