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Kinetic analysis of product inhibition in human manganese superoxide dismutase.

Hearn AS, Stroupe ME, Cabelli DE, Lepock JR, Tainer JA, Nick HS, Silverman DN
Biochemistry 40 12051-8 (2001)
Cited: 29 times
EuropePMC logo PMID: 11580280

Abstract

Manganese superoxide dismutase (MnSOD) cycles between the Mn(II) and Mn(III) states during the catalyzed disproportionation of O(2)(*-), a catalysis that is limited at micromolar levels of superoxide by a peroxide-inhibited complex with the metal. We have investigated the role in catalysis and inhibition of the conserved residue Trp161 which forms a hydrophobic side of the active site cavity of MnSOD. Crystal structures of mutants of human MnSOD in which Trp161 was replaced with Ala or Phe showed significant conformational changes on adjacent residues near the active site, particularly Gln143 and Tyr34 which in wild-type MnSOD participate in a hydrogen bond network believed to support proton transfer during catalysis. Using pulse radiolysis and observing the UV absorbance of superoxide, we have determined rate constants for the catalytic dismutation of superoxide. In addition, the rates of formation and dissociation of the product-inhibited complex of these mutants were determined by direct observation of the characteristic visible absorption of the oxidized and inhibited states. Catalysis by W161A and W161F MnSOD was associated with a decrease of at least 100-fold in the catalytic rate of reduction of superoxide, which then promotes a competing pathway leading to product inhibition. The structural changes caused by the mutations at position 161 led to small changes, at most a 6-fold decrease, in the rate constant for formation of the inhibited complex. Solvent hydrogen isotope effects support a mechanism in which formation of this complex, presumably the peroxide dianion bound to the manganese, involves no rate-contributing proton transfer; however, the dissociation of the complex requires proton transfer to generate HO(2)(-) or H2O2.

Reviews - 1ja8 mentioned but not cited (1)

  1. The structure-function relationships and physiological roles of MnSOD mutants. Bonetta Valentino R. Biosci Rep 42 BSR20220202 (2022)

Articles - 1ja8 mentioned but not cited (1)

  1. Substrate-analog binding and electrostatic surfaces of human manganese superoxide dismutase. Azadmanesh J, Trickel SR, Borgstahl GEO. J Struct Biol 199 68-75 (2017)


Reviews citing this publication (5)

  1. Superoxide dismutases and superoxide reductases. Sheng Y, Abreu IA, Cabelli DE, Maroney MJ, Miller AF, Teixeira M, Valentine JS. Chem Rev 114 3854-3918 (2014)
  2. The Ca2+/Mn2+ pumps in the Golgi apparatus. Van Baelen K, Dode L, Vanoevelen J, Callewaert G, De Smedt H, Missiaen L, Parys JB, Raeymaekers L, Wuytack F. Biochim Biophys Acta 1742 103-112 (2004)
  3. SPCA1 pumps and Hailey-Hailey disease. Missiaen L, Raeymaekers L, Dode L, Vanoevelen J, Van Baelen K, Parys JB, Callewaert G, De Smedt H, Segaert S, Wuytack F. Biochem Biophys Res Commun 322 1204-1213 (2004)
  4. A Review of the Catalytic Mechanism of Human Manganese Superoxide Dismutase. Azadmanesh J, Borgstahl GEO. Antioxidants (Basel) 7 E25 (2018)
  5. The role of the Golgi-resident SPCA Ca²⁺/Mn²⁺ pump in ionic homeostasis and neural function. He W, Hu Z. Neurochem Res 37 455-468 (2012)

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  1. Selective Persulfide Detection Reveals Evolutionarily Conserved Antiaging Effects of S-Sulfhydration. Zivanovic J, Kouroussis E, Kohl JB, Adhikari B, Bursac B, Schott-Roux S, Petrovic D, Miljkovic JL, Thomas-Lopez D, Jung Y, Miler M, Mitchell S, Milosevic V, Gomes JE, Benhar M, Gonzalez-Zorn B, Ivanovic-Burmazovic I, Torregrossa R, Mitchell JR, Whiteman M, Schwarz G, Snyder SH, Paul BD, Carroll KS, Filipovic MR. Cell Metab 30 1152-1170.e13 (2019)
  2. Crystal structure of nitrated human manganese superoxide dismutase: mechanism of inactivation. Quint P, Reutzel R, Mikulski R, McKenna R, Silverman DN. Free Radic Biol Med 40 453-458 (2006)
  3. Contribution of human manganese superoxide dismutase tyrosine 34 to structure and catalysis. Perry JJ, Hearn AS, Cabelli DE, Nick HS, Tainer JA, Silverman DN. Biochemistry 48 3417-3424 (2009)
  4. Potent anti-tumor effects of an active site mutant of human manganese-superoxide dismutase. Evolutionary conservation of product inhibition. Davis CA, Hearn AS, Fletcher B, Bickford J, Garcia JE, Leveque V, Melendez JA, Silverman DN, Zucali J, Agarwal A, Nick HS. J Biol Chem 279 12769-12776 (2004)
  5. Correlation between structural, spectroscopic, and reactivity properties within a series of structurally analogous metastable manganese(III)-alkylperoxo complexes. Coggins MK, Martin-Diaconescu V, DeBeer S, Kovacs JA. J Am Chem Soc 135 4260-4272 (2013)
  6. Spectroscopic and computational investigation of second-sphere contributions to redox tuning in Escherichia coli iron superoxide dismutase. Grove LE, Xie J, Yikilmaz E, Miller AF, Brunold TC. Inorg Chem 47 3978-3992 (2008)
  7. Amino acid substitution at the dimeric interface of human manganese superoxide dismutase. Hearn AS, Fan L, Lepock JR, Luba JP, Greenleaf WB, Cabelli DE, Tainer JA, Nick HS, Silverman DN. J Biol Chem 279 5861-5866 (2004)
  8. Structural analysis of peroxide-soaked MnSOD crystals reveals side-on binding of peroxide to active-site manganese. Porta J, Vahedi-Faridi A, Borgstahl GE. J Mol Biol 399 377-384 (2010)
  9. Can Melatonin Act as an Antioxidant in Hydrogen Peroxide-Induced Oxidative Stress Model in Human Peripheral Blood Mononuclear Cells? Emamgholipour S, Hossein-Nezhad A, Ansari M. Biochem Res Int 2016 5857940 (2016)
  10. Comparison of two yeast MnSODs: mitochondrial Saccharomyces cerevisiae versus cytosolic Candida albicans. Sheng Y, Stich TA, Barnese K, Gralla EB, Cascio D, Britt RD, Cabelli DE, Valentine JS. J Am Chem Soc 133 20878-20889 (2011)
  11. Geometric and electronic structures of peroxomanganese(III) complexes supported by pentadentate amino-pyridine and -imidazole ligands. Geiger RA, Leto DF, Chattopadhyay S, Dorlet P, Anxolabéhère-Mallart E, Jackson TA. Inorg Chem 50 10190-10203 (2011)
  12. Investigation of the highly active manganese superoxide dismutase from Saccharomyces cerevisiae. Barnese K, Sheng Y, Stich TA, Gralla EB, Britt RD, Cabelli DE, Valentine JS. J Am Chem Soc 132 12525-12527 (2010)
  13. Mn/Fe superoxide dismutase interaction fingerprints and prediction of oligomerization and metal cofactor from sequence. Wintjens R, Gilis D, Rooman M. Proteins 70 1564-1577 (2008)
  14. Autoregulation of free radicals via uncoupling protein control in pancreatic beta-cell mitochondria. Heuett WJ, Periwal V. Biophys J 98 207-217 (2010)
  15. Geometric and electronic structure of a peroxomanganese(III) complex supported by a scorpionate ligand. Colmer HE, Geiger RA, Leto DF, Wijeratne GB, Day VW, Jackson TA. Dalton Trans 43 17949-17963 (2014)
  16. Facile and scalable synthesis of a novel rigid artificial superoxide dismutase based on modified hollow mesoporous silica microspheres. Yu J, Ge L, Liu S, Dai P, Ge S, Zheng W. Biosens Bioelectron 26 1936-1941 (2011)
  17. Tissue-specific expression and molecular modeling of cytosolic manganese superoxide dismutases from the white shrimp Litopenaeus vannamei. Gómez-Anduro GA, Sotelo-Mundo RR, Muhlia-Almazán A, Yepiz-Plascencia G. Dev Comp Immunol 31 783-789 (2007)
  18. Efficacy of aldose reductase inhibitors is affected by oxidative stress induced under X-ray irradiation. Castellví A, Crespo I, Crosas E, Cámara-Artigas A, Gavira JA, Aranda MAG, Parés X, Farrés J, Juanhuix J. Sci Rep 9 3177 (2019)
  19. Engineering and characterization of human manganese superoxide dismutase mutants with high activity and low product inhibition. Chockalingam K, Luba J, Nick HS, Silverman DN, Zhao H. FEBS J 273 4853-4861 (2006)
  20. Direct detection of coupled proton and electron transfers in human manganese superoxide dismutase. Azadmanesh J, Lutz WE, Coates L, Weiss KL, Borgstahl GEO. Nat Commun 12 2079 (2021)
  21. Cryotrapping peroxide in the active site of human mitochondrial manganese superoxide dismutase crystals for neutron diffraction. Azadmanesh J, Lutz WE, Coates L, Weiss KL, Borgstahl GEO. Acta Crystallogr F Struct Biol Commun 78 8-16 (2022)
  22. Perfect Crystals: microgravity capillary counterdiffusion crystallization of human manganese superoxide dismutase for neutron crystallography. Lutz WE, Azadmanesh J, Lovelace JJ, Kolar C, Coates L, Weiss KL, Borgstahl GEO. NPJ Microgravity 9 39 (2023)


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