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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 3417-24 (2009)
Related entries: 1zsp, 1zte, 1zuq

Cited: 35 times
EuropePMC logo PMID: 19265433

Abstract

Superoxide dismutase (SOD) enzymes are critical in controlling levels of reactive oxygen species (ROS) that are linked to aging, cancer, and neurodegenerative disease. Superoxide (O(2)(*-)) produced during respiration is removed by the product of the SOD2 gene, the homotetrameric manganese superoxide dismutase (MnSOD). Here, we examine the structural and catalytic roles of the highly conserved active-site residue Tyr34, based upon structure-function studies of MnSOD enzymes with mutations at this site. Substitution of Tyr34 with five different amino acids retained the active-site protein structure and assembly but caused a substantial decrease in the catalytic rate constant for the reduction of superoxide. The rate constant for formation of the product inhibition complex also decreases but to a much lesser extent, resulting in a net increase in the level of product inhibited form of the mutant enzymes. Comparisons of crystal structures and catalytic rates also suggest that one mutation, Y34V, interrupts the hydrogen-bonded network, which is associated with a rapid dissociation of the product-inhibited complex. Notably, with three of the Tyr34 mutants, we also observe an intermediate in catalysis, which has not been reported previously. Thus, these mutants establish a means of trapping a catalytic intermediate that promises to help elucidate the mechanism of catalysis.

Reviews - 2p4k 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 - 2p4k mentioned but not cited (4)

  1. 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)
  2. Differential protein acetylation assists import of excess SOD2 into mitochondria and mediates SOD2 aggregation associated with cardiac hypertrophy in the murine SOD2-tg heart. Zhang L, Chen CL, Kang PT, Jin Z, Chen YR. Free Radic Biol Med 108 595-609 (2017)
  3. The structure of the Caenorhabditis elegans manganese superoxide dismutase MnSOD-3-azide complex. Hunter GJ, Trinh CH, Bonetta R, Stewart EE, Cabelli DE, Hunter T. Protein Sci 24 1777-1788 (2015)
  4. The dipeptidyl peptidase IV inhibitors vildagliptin and K-579 inhibit a phospholipase C: a case of promiscuous scaffolds in proteins. Chakraborty S, Rendón-Ramírez A, Ásgeirsson B, Dutta M, Ghosh AS, Oda M, Venkatramani R, Rao BJ, Dandekar AM, Goñi FM. F1000Res 2 286 (2013)


Reviews citing this publication (6)

  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 structural biochemistry of the superoxide dismutases. Perry JJ, Shin DS, Getzoff ED, Tainer JA. Biochim Biophys Acta 1804 245-262 (2010)
  3. Insights into the Dichotomous Regulation of SOD2 in Cancer. Kim YS, Gupta Vallur P, Phaëton R, Mythreye K, Hempel N. Antioxidants (Basel) 6 E86 (2017)
  4. A Review of the Catalytic Mechanism of Human Manganese Superoxide Dismutase. Azadmanesh J, Borgstahl GEO. Antioxidants (Basel) 7 E25 (2018)
  5. Human Mn-superoxide dismutase inactivation by peroxynitrite: a paradigm of metal-catalyzed tyrosine nitration in vitro and in vivo. Demicheli V, Moreno DM, Radi R. Metallomics 10 679-695 (2018)
  6. Metalloprotein catalysis: structural and mechanistic insights into oxidoreductases from neutron protein crystallography. Schröder GC, Meilleur F. Acta Crystallogr D Struct Biol 77 1251-1269 (2021)

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  2. Amyotrophic lateral sclerosis: update and new developments. Pratt AJ, Getzoff ED, Perry JJ. Degener Neurol Neuromuscul Dis 2012 1-14 (2012)
  3. A manganese-rich environment supports superoxide dismutase activity in a Lyme disease pathogen, Borrelia burgdorferi. Aguirre JD, Clark HM, McIlvin M, Vazquez C, Palmere SL, Grab DJ, Seshu J, Hart PJ, Saito M, Culotta VC. J Biol Chem 288 8468-8478 (2013)
  4. Robust protein nitration contributes to acetaminophen-induced mitochondrial dysfunction and acute liver injury. Abdelmegeed MA, Jang S, Banerjee A, Hardwick JP, Song BJ. Free Radic Biol Med 60 211-222 (2013)
  5. Exploring the molecular basis of human manganese superoxide dismutase inactivation mediated by tyrosine 34 nitration. Moreno DM, Martí MA, De Biase PM, Estrin DA, Demicheli V, Radi R, Boechi L. Arch Biochem Biophys 507 304-309 (2011)
  6. Label-free quantitative proteomic analysis reveals potential biomarkers and pathways in renal cell carcinoma. Zhao Z, Wu F, Ding S, Sun L, Liu Z, Ding K, Lu J. Tumour Biol 36 939-951 (2015)
  7. 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)
  8. Investigation of the mechanism of formation of a thiolate-ligated Fe(III)-OOH. Nam E, Alokolaro PE, Swartz RD, Gleaves MC, Pikul J, Kovacs JA. Inorg Chem 50 1592-1602 (2011)
  9. Autophagy protein Ulk1 promotes mitochondrial apoptosis through reactive oxygen species. Mukhopadhyay S, Das DN, Panda PK, Sinha N, Naik PP, Bissoyi A, Pramanik K, Bhutia SK. Free Radic Biol Med 89 311-321 (2015)
  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. Crystal structure of the cambialistic superoxide dismutase from Aeropyrum pernix K1--insights into the enzyme mechanism and stability. Nakamura T, Torikai K, Uegaki K, Morita J, Machida K, Suzuki A, Kawata Y. FEBS J 278 598-609 (2011)
  12. Regulation of SOD2 and β-arrestin1 by interleukin-6 contributes to the increase of IGF-1R expression in docetaxel resistant prostate cancer cells. Zhang D, Cui Y, Niu L, Xu X, Tian K, Young CY, Lou H, Yuan H. Eur J Cell Biol 93 289-298 (2014)
  13. Six-coordinate manganese(3+) in catalysis by yeast manganese superoxide dismutase. Sheng Y, Butler Gralla E, Schumacher M, Cascio D, Cabelli DE, Valentine JS. Proc Natl Acad Sci U S A 109 14314-14319 (2012)
  14. LC-MS/MS Analysis Unravels Deep Oxidation of Manganese Superoxide Dismutase in Kidney Cancer. Zhao Z, Azadzoi KM, Choi HP, Jing R, Lu X, Li C, Wang F, Lu J, Yang JH. Int J Mol Sci 18 E319 (2017)
  15. Substrate-analog binding and electrostatic surfaces of human manganese superoxide dismutase. Azadmanesh J, Trickel SR, Borgstahl GEO. J Struct Biol 199 68-75 (2017)
  16. Effects of dietary plant polyphenols and seaweed extract mixture on male-rabbit semen: Quality traits and antioxidant markers. Vizzari F, Massányi M, Knížatová N, Corino C, Rossi R, Ondruška Ľ, Tirpák F, Halo M, Massányi P. Saudi J Biol Sci 28 1017-1025 (2021)
  17. 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)
  18. Effects of acetaminophen on mitochondrial complex I activity in the rat liver and kidney: a PET study with 18F-BCPP-BF. Ohba H, Kanazawa M, Kakiuchi T, Tsukada H. EJNMMI Res 6 82 (2016)
  19. Pulse radiolysis studies on the reaction of the reduced vitamin B₁₂ complex Cob(II)alamin with superoxide. Dassanayake RS, Cabelli DE, Brasch NE. Chembiochem 14 1081-1083 (2013)
  20. Probing the metal specificity mechanism of superoxide dismutase from human pathogen Clostridium difficile. Li W, Wang H, Chen Z, Ye Q, Tian Y, Xu X, Huang Z, Li P, Tan X. Chem Commun (Camb) 50 584-586 (2014)
  21. Combined QM/MM and Monte Carlo study for redox leveling in Mn and Fe superoxide dismutase. Amin M, Mohamed Z, El-Sayed M, Samy A, Sultan A, Bassuoni M, Alkordi MH, Alkordi MH. J Biol Inorg Chem 23 285-293 (2018)
  22. Cobinamide is a strong and versatile antioxidant that overcomes oxidative stress in cells, flies, and diabetic mice. Chang S, Tat J, China SP, Kalyanaraman H, Zhuang S, Chan A, Lai C, Radic Z, Abdel-Rahman EA, Casteel DE, Pilz RB, Ali SS, Boss GR. PNAS Nexus 1 pgac191 (2022)
  23. Determination of Manganese in Serum Using GFAAS: Serum Reference Values for Manganese in the Adolescent Girls of the DERVAN Cohort. Chavan S, Bhat R, Nandoskar A, Bhat P, Rokade SR, Mohire RR, Patil SN. Indian J Clin Biochem 37 487-493 (2022)
  24. 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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