Myeloperoxidase-derived oxidants rapidly oxidize and disrupt zinc-cysteine/histidine clusters in proteins

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2012

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Cook, N.L.
Pattison, D.I.
Davies, M.J.

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Free Radical Biology and Medicine, 2012; 53(11):2072-2080

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Naomi L. Cook, David I. Pattison, Michael J. Davies

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Abstract

Zinc is an abundant cellular transition metal ion, which binds avidly to protein cysteine (Cys) and histidine (His) residues to form zinc-Cys/His clusters; these play a key role in the function of many proteins (e.g., DNA binding and repair enzymes, transcription factors, nitric oxide synthase). Leukocyte-derived myeloperoxidase generates powerful oxidants including hypochlorous (HOCl), hypobromous (HOBr), and hypothiocyanous (HOSCN) acids from H₂O₂ and (pseudo)halide ions. Excessive or misplaced formation of these species is associated with cellular dysfunction, apoptosis and necrosis, and multiple inflammatory diseases. HOCl and HOBr react rapidly with sulfur-containing compounds, and HOSCN reacts specifically with thiols. Consequently, we hypothesized that zinc-Cys/His clusters would be targets for these oxidants, and the activity of such enzymes would be perturbed. This hypothesis has been tested using yeast alcohol dehydrogenase (YADH), which contains a well-characterized Zn₁Cys₂His₁ cluster. Incubation of YADH with pathologically relevant concentrations of HOSCN, HOCl, and HOBr resulted in rapid oxidation of the protein (rate constants, determined by competition kinetics, for reaction of HOCl and HOSCN with YADH being (3.3±0.9)×10⁸ and (2.9±0.4)×10⁴ M⁻¹ s⁻¹ per YADH monomer, respectively), loss of enzyme activity, Zn²⁺ release, changes in protein structure (particularly formation of disulfide cross-links), and oxidation of Cys residues. The loss of enzyme activity correlated with Zn²⁺ release, loss of thiols, and changes in protein structure. We conclude that exposure of zinc-Cys/His clusters to inflammatory oxidants can result in impaired protein activity, thiol oxidation, and Zn²⁺ release. These reactions may contribute to inflammation-induced tissue damage.

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© 2012 Elsevier Inc. All rights reserved.

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