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Insights into the role of the unusual disulfide bond in copper-zinc superoxide dismutase.

Sea K, Sohn SH, Durazo A, Sheng Y, Shaw BF, Cao X, Taylor AB, Whitson LJ, Holloway SP, Hart PJ, Cabelli DE, Gralla EB, Valentine JS
J Biol Chem 290 2405-18 (2015)
Cited: 35 times
EuropePMC logo PMID: 25433341

Abstract

The functional and structural significance of the intrasubunit disulfide bond in copper-zinc superoxide dismutase (SOD1) was studied by characterizing mutant forms of human SOD1 (hSOD) and yeast SOD1 lacking the disulfide bond. We determined x-ray crystal structures of metal-bound and metal-deficient hC57S SOD1. C57S hSOD1 isolated from yeast contained four zinc ions per protein dimer and was structurally very similar to wild type. The addition of copper to this four-zinc protein gave properly reconstituted 2Cu,2Zn C57S hSOD, and its spectroscopic properties indicated that the coordination geometry of the copper was remarkably similar to that of holo wild type hSOD1. In contrast, the addition of copper and zinc ions to apo C57S human SOD1 failed to give proper reconstitution. Using pulse radiolysis, we determined SOD activities of yeast and human SOD1s lacking disulfide bonds and found that they were enzymatically active at ∼10% of the wild type rate. These results are contrary to earlier reports that the intrasubunit disulfide bonds in SOD1 are essential for SOD activity. Kinetic studies revealed further that the yeast mutant SOD1 had less ionic attraction for superoxide, possibly explaining the lower rates. Saccharomyces cerevisiae cells lacking the sod1 gene do not grow aerobically in the absence of lysine, but expression of C57S SOD1 increased growth to 30-50% of the growth of cells expressing wild type SOD1, supporting that C57S SOD1 retained a significant amount of activity.

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  1. Insights into the role of the unusual disulfide bond in copper-zinc superoxide dismutase. Sea K, Sohn SH, Durazo A, Sheng Y, Shaw BF, Cao X, Taylor AB, Whitson LJ, Holloway SP, Hart PJ, Cabelli DE, Gralla EB, Valentine JS. J Biol Chem 290 2405-2418 (2015)
  2. Molecular recognition and maturation of SOD1 by its evolutionarily destabilised cognate chaperone hCCS. Sala FA, Wright GSA, Antonyuk SV, Garratt RC, Hasnain SS. PLoS Biol 17 e3000141 (2019)
  3. Novel Antioxidant Peptides from Pearl Shell Meat Hydrolysate and Their Antioxidant Activity Mechanism. Huang P, Miao J, Li J, Li Y, Wang X, Yu Y, Cao Y. Molecules 28 864 (2023)
  4. Molecular dynamics analysis of superoxide dismutase 1 mutations suggests decoupling between mechanisms underlying ALS onset and progression. Kalia M, Miotto M, Ness D, Opie-Martin S, Spargo TP, Di Rienzo L, Biagini T, Petrizzelli F, Al Khleifat A, Kabiljo R, Project MinE ALS Sequencing Consortium, SOD1-ALS clinical and genetic data collection group, Mazza T, Ruocco G, Milanetti E, Dobson RJ, Al-Chalabi A, Iacoangeli A. Comput Struct Biotechnol J 21 5296-5308 (2023)


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  1. Proteomics Approaches for Biomarker and Drug Target Discovery in ALS and FTD. Hedl TJ, San Gil R, Cheng F, Rayner SL, Davidson JM, De Luca A, Villalva MD, Ecroyd H, Walker AK, Lee A. Front Neurosci 13 548 (2019)
  2. Autophagy and ALS: mechanistic insights and therapeutic implications. Chua JP, De Calbiac H, Kabashi E, Barmada SJ. Autophagy 18 254-282 (2022)
  3. Oxygen-dependent activation of Cu,Zn-superoxide dismutase-1. M Fetherolf M, Boyd SD, Winkler DD, Winge DR. Metallomics 9 1047-1059 (2017)
  4. SOD1 in ALS: Taking Stock in Pathogenic Mechanisms and the Role of Glial and Muscle Cells. Peggion C, Scalcon V, Massimino ML, Nies K, Lopreiato R, Rigobello MP, Bertoli A. Antioxidants (Basel) 11 614 (2022)
  5. Phenotypic diversity in ALS and the role of poly-conformational protein misfolding. Ayers JI, Borchelt DR. Acta Neuropathol 142 41-55 (2021)
  6. Vorapaxar and Amyotrophic Lateral Sclerosis: Coincidence or Adverse Association? Serebruany VL, Fortmann SD, Hanley DF, Kim MH. Am J Ther 24 e139-e143 (2017)
  7. Multiple ways to a dead end: diverse mechanisms by which ALS mutant genes induce cell death. Tsai YL, Manley JL. Cell Cycle 20 631-646 (2021)

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  4. α-Lipoic acid prevents against cisplatin cytotoxicity via activation of the NRF2/HO-1 antioxidant pathway. Lee J, Jung SY, Yang KJ, Kim Y, Lee D, Lee MH, Kim DK. PLoS One 14 e0226769 (2019)
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  8. Relationship between mutant Cu/Zn superoxide dismutase 1 maturation and inclusion formation in cell models. Ayers JI, McMahon B, Gill S, Lelie HL, Fromholt S, Brown H, Valentine JS, Whitelegge JP, Borchelt DR. J Neurochem 140 140-150 (2017)
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  10. Tripartite Separation of Glomerular Cell Types and Proteomes from Reporter-Free Mice. Hatje FA, Wedekind U, Sachs W, Loreth D, Loreth D, Reichelt J, Demir F, Kosub C, Heintz L, Tomas NM, Huber TB, Skuza S, Sachs M, Zielinski S, Rinschen MM, Meyer-Schwesinger C. J Am Soc Nephrol 32 2175-2193 (2021)
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  18. Biochemical Analysis of CaurSOD4, a Potential Therapeutic Target for the Emerging Fungal Pathogen Candida auris. Chandler CE, Hernandez FG, Totten M, Robinett NG, Schatzman SS, Zhang SX, Culotta VC. ACS Infect Dis 8 584-595 (2022)
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  20. Characterization of a novel cysteine-less Cu/Zn-superoxide dismutase in Paenibacillus lautus missing a conserved disulfide bond. Furukawa Y, Shintani A, Narikiyo S, Sue K, Akutsu M, Muraki N. J Biol Chem 299 105040 (2023)
  21. First Principles Calculation of Protein-Protein Dimer Affinities of ALS-Associated SOD1 Mutants. Hsueh SCC, Nijland M, Peng X, Hilton B, Plotkin SS. Front Mol Biosci 9 845013 (2022)
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