The role of arginine 143 in the electrostatics and mechanism of Cu, Zn superoxide dismutase: Computational and experimental evaluation by mutational analysis
Abstract
Cu, Zn superoxide dismutase protects cells from oxidative damage by removing superoxide radicals in one of the fastest enzyme reactions known. The redox reaction at the active‐site Cu ion is rate‐limited by diffusion and enhanced by electrostatic guidance. To quantitatively define the electrostatic and mechanistic contributions of sequence‐invariant Arg‐143 in human Cu, Zn superoxide dismutase, single‐site mutants at this position were investigated experimentally and computationally. Rate constants for several Arg‐143 mutants were determined at different pH and ionic strength conditions using pulse radiolytic methods and compared to results from Brownian dynamics simulations. At physiological pH, substitution of Arg‐143 by Lys caused a 2‐fold drop in rate, neutral substitutions (Ile, Ala) reduced the rate about 10‐fold, while charge‐reversing substitutions (Asp, Glu) caused a 100‐fold decrease. Position 143 mutants showed pH dependencies not seen in other mutants. At low pH, the acidic residue mutations exhibited pro‐tonation/deprotonation effects. At high pH, all enzymes showed typical decreases in rate except the Lys mutant in which the rate dropped off at an unusually low pH. Increasing ionic strength at acidic pH decreased the rates of the wild‐type enzyme and Lys mutant, while the rate of the Glu mutant was unaffected. Increasing ionic strength at higher pH (>10) increased the rates of the Lys and Glu mutants while the rate of the wild‐type enzyme was unaffected. Reaction simulations with Brownian dynamics incorporating electrostatic effects tested computational predictability of ionic strength dependencies of the wild‐type enzyme and the Lys, Ile, and Glu mutants. The calculated and experimental ionic strength profiles gave similar slopes in all but the Glu mutant, indicating that the electrostatic attraction of the substrate is accurately modeled. Differences between the calculated and experimental rates for the Glu and Lys mutants reflect the mechanistic contribution of Arg‐143. Results from this joint analysis establish that, aside from the Cu ligands, Arg‐143 is the single most important residue in Cu, Zn superoxide dismutase both electrostatically and mechanistically, and provide an explanation for the evolutionary selection of arginine at position 143. © 1994 Wiley‐Liss, Inc.
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Several studies have been carried out using pulsed radiolysis to generate HO2•/O2•− and to understand the Cu,Zn-SOD-catalysed reaction of superoxide dismutation.
“Several studies have been carried out using pulsed radiolysis to generate HO2•/O2•− and to understand the Cu,Zn-SOD-catalysed reaction of superoxide dismutation [74,75,76,77], Figure 32.”
From Superoxide Anion Chemistry—Its Role at the Core of the Innate Immunity (2023) · cites this paper as [75]
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- Authors
- Fisher, C. L., Cabelli, D. E., Tainer, J. A., Hallewell, R. A., & Getzoff, E. D.
- Affiliations
- Scripps Research Institute (US)
- Brookhaven National Laboratory (US)
- Imperial College London (GB)
- Corresponding author
- Getzoff, Elizabeth D.
- ORCID
- Tainer, John A.
- Venue
- Proteins: Structure, Function, and Bioinformatics
- Publisher
- Wiley
- Published
- 1994-05
- Volume
- 19
- Issue
- 1
- Pages
- 24-34
- ISSN
- 0887-3585 (ISSN-L)
- 1097-0134
- OpenAlex
- W2021594222
- Cited by
- 125
- References
- 40
- Citations by year
- 2026: 3 · 2025: 5 · 2023: 8 · 2022: 3 · 2021: 5 · 2020: 9 · 2019: 7 · 2018: 1 · 2017: 5 · 2016: 3 · 2015: 1 · 2014: 5 · 2013: 2 · 2012: 1
- FWCI
- 4.58
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Proteins Structure Function and Bioinformatics (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Houston
- Wellcome Trust
- National Institutes of Health (7f32gm011612-02)
- National Institute of General Medical Sciences (GM-37684, GM11612, GM-39345, R01GM039345, R01GM037684)
- Topics
- Physical Sciences › Chemistry › Inorganic Chemistry › Metal-Catalyzed Oxygenation Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Glutathione Transferases and Polymorphisms
- Keywords
- Cu/Zn superoxide dismutase, electrostatics, reaction mechanism, single-site mutants, pH dependence, ionic strength dependence, Brownian dynamics, pulse radiolysis, superoxide, protonation effects
- MeSH terms
- Arginine, Binding Sites, Chemistry, Physical, Computer Simulation, Copper, Diffusion, Humans, Hydrogen-Ion Concentration, Kinetics, Models, Molecular, Osmolar Concentration, Oxidation-Reduction, Recombinant Fusion Proteins, Superoxide Dismutase, Zinc, Mutagenesis, Site-Directed, Chemical Phenomena
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