The structure of the Caenorhabditis elegans manganese superoxide dismutase MnSOD-3-azide complex

Hunter, Gary J.; Trinh, Chi H.; Bonetta, Rosalin; Stewart, Emma E.; Cabelli, Diane E.; Hunter, Therese

doi:10.1002/pro.2768

Title: The structure of the Caenorhabditis elegans manganese superoxide dismutase MnSOD-3-azide complex

Journal Article · Thu Aug 27 00:00:00 EDT 2015 · Protein Science

DOI:https://doi.org/10.1002/pro.2768· OSTI ID:1221758

Hunter, Gary J. ^[1]; Trinh, Chi H. ^[2]; Bonetta, Rosalin ^[1]; Stewart, Emma E. ^[2]; Cabelli, Diane E. ^[3]; Hunter, Therese ^[1]

Univ. of Malta (Malta)
Univ. of Leeds, Leeds (United Kingdom)
Brookhaven National Lab. (BNL), Upton, NY (United States)

C. elegans MnSOD-3 has been implicated in the longevity pathway and its mechanism of catalysis is relevant to the aging process and carcinogenesis. The structures of MnSOD-3 provide unique crystallographic evidence of a dynamic region of the tetrameric interface (residues 41–54). We have determined the structure of the MnSOD-3-azide complex to 1.77-Å resolution. The analysis of this complex shows that the substrate analog, azide, binds end-on to the manganese center as a sixth ligand and that it ligates directly to a third and new solvent molecule also positioned within interacting distance to the His30 and Tyr34 residues of the substrate access funnel. This is the first structure of a eukaryotic MnSOD-azide complex that demonstrates the extended, uninterrupted hydrogen-bonded network that forms a proton relay incorporating three outer sphere solvent molecules, the substrate analog, the gateway residues, Gln142, and the solvent ligand. This configuration supports the formation and release of the hydrogen peroxide product in agreement with the 5-6-5 catalytic mechanism for MnSOD. The high product dissociation constant k₄ of MnSOD-3 reflects low product inhibition making this enzyme efficient even at high levels of superoxide.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States). Laser Electron Accelerator Facility (LEAF).

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC00112704

OSTI ID:: 1221758

Report Number(s):: BNL-108388-2015-JA; R&D Project: CO-004; KC0304030

Journal Information:: Protein Science, Journal Name: Protein Science; ISSN 0961-8368

Publisher:: The Protein SocietyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 17 works

Citation information provided by
Web of Science

References (84)

Construction of an Escherichia coli K-12 strain deleted for manganese and iron superoxide dismutase genes and its use in cloning the iron superoxide dismutase gene of Legionella pneumophila Steinman, HowardM. MGG Molecular & General Genetics, Vol. 232, Issue 3 https://doi.org/10.1007/BF00266247	journal	April 1992
Water Oxidation by Single-Site Ruthenium Complexes: Using Ligands as Redox and Proton Transfer Mediators Kärkäs, Markus D.; Åkermark, Torbjörn; Johnston, Eric V. Angewandte Chemie, Vol. 124, Issue 46 https://doi.org/10.1002/ange.201205018	journal	September 2012
A pulse-radiolysis study of the manganese-containing superoxide dismutase from Bacillus stearothermophilus. A kinetic model for the enzyme action McAdam, M. E.; Fox, R. A.; Lavelle, F. Biochemical Journal, Vol. 165, Issue 1 https://doi.org/10.1042/bj1650071	journal	July 1977
Cloning, Expression, and Characterization of Two Manganese Superoxide Dismutases from Caenorhabditis elegans Hunter, Thérèse; Bannister, William H.; Hunter, Gary J. Journal of Biological Chemistry, Vol. 272, Issue 45 https://doi.org/10.1074/jbc.272.45.28652	journal	November 1997
Genetic pathways that regulate ageing in model organisms Guarente, Leonard; Kenyon, Cynthia Nature, Vol. 408, Issue 6809 https://doi.org/10.1038/35041700	journal	November 2000
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Aging: A Theory Based on Free Radical and Radiation Chemistry Harman, D. Journal of Gerontology, Vol. 11, Issue 3 https://doi.org/10.1093/geronj/11.3.298	journal	July 1956
Adaptive responses to oxidative damage in three mutants of Caenorhabditis elegans (age-1, mev-1 and daf-16) that affect life span Yanase, Sumino; Yasuda, Kayo; Ishii, Naoaki Mechanisms of Ageing and Development, Vol. 123, Issue 12 https://doi.org/10.1016/S0047-6374(02)00093-3	journal	November 2002
The Conserved Residue Tyrosine 34 Is Essential for Maximal Activity of Iron−Superoxide Dismutase from Escherichia coli ^† Hunter, Therese; Ikebukuro, Kazunori; Bannister, William H. Biochemistry, Vol. 36, Issue 16 https://doi.org/10.1021/bi9629541	journal	April 1997
Anion Binding Properties of Reduced and Oxidized Iron-Containing Superoxide Dismutase Reveal No Requirement for Tyrosine 34 ^† Miller, Anne-Frances; Sorkin, David L.; Padmakumar, K. Biochemistry, Vol. 44, Issue 16 https://doi.org/10.1021/bi0476331	journal	April 2005
GroESL protects superoxide dismutase (SOD)— Deficient cells against oxidative stress and is a chaperone for SOD Hunter, Gary J.; Hunter, Thérèse Health, Vol. 05, Issue 10 https://doi.org/10.4236/health.2013.510232	journal	January 2013
Six-coordinate manganese(3+) in catalysis by yeast manganese superoxide dismutase Sheng, Y.; Butler Gralla, E.; Schumacher, M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 36 https://doi.org/10.1073/pnas.1212367109	journal	August 2012
Outer Sphere Mutations Perturb Metal Reactivity in Manganese Superoxide Dismutase ^† ^, ^{^‡} Edwards, Ross A.; Whittaker, Mei M.; Whittaker, James W. Biochemistry, Vol. 40, Issue 1 https://doi.org/10.1021/bi0018943	journal	January 2001
REFMAC 5 dictionary: organization of prior chemical knowledge and guidelines for its use Vagin, Alexei A.; Steiner, Roberto A.; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12 https://doi.org/10.1107/S0907444904023510	journal	November 2004
Exploring the gas access routes in a [NiFeSe] hydrogenase using crystals pressurized with krypton and oxygen Zacarias, Sónia; Temporão, Adriana; Carpentier, Philippe JBIC Journal of Biological Inorganic Chemistry, Vol. 25, Issue 6 https://doi.org/10.1007/s00775-020-01814-y	journal	August 2020
A C. elegans mutant that lives twice as long as wild type Kenyon, Cynthia; Chang, Jean; Gensch, Erin Nature, Vol. 366, Issue 6454 https://doi.org/10.1038/366461a0	journal	December 1993
Structure and flexibility in cold-adapted iron superoxide dismutases: The case of the enzyme isolated from Pseudoalteromonas haloplanktis Merlino, Antonello; Krauss, Irene Russo; Castellano, Immacolata Journal of Structural Biology, Vol. 172, Issue 3 https://doi.org/10.1016/j.jsb.2010.08.008	journal	December 2010
X-ray structure of the cambialistic superoxide dismutase from Propionibacterium shermanii active with Fe or Mn Schmidt, Marius; Meier, Beate; Parak, F. JBIC Journal of Biological Inorganic Chemistry, Vol. 1, Issue 6 https://doi.org/10.1007/s007750050089	journal	December 1996
Aging and resistance to oxidative damage in Caenorhabditis elegans. Larsen, P. L. Proceedings of the National Academy of Sciences, Vol. 90, Issue 19 https://doi.org/10.1073/pnas.90.19.8905	journal	October 1993
ROS in Aging Caenorhabditis elegans : Damage or Signaling? Back, Patricia; Braeckman, Bart P.; Matthijssens, Filip Oxidative Medicine and Cellular Longevity, Vol. 2012 https://doi.org/10.1155/2012/608478	journal	January 2012
Curbing cancer's sweet tooth: Is there a role for MnSOD in regulation of the Warburg effect? Holley, Aaron K.; Dhar, Sanjit Kumar; St. Clair, Daret K. Mitochondrion, Vol. 13, Issue 3 https://doi.org/10.1016/j.mito.2012.07.104	journal	May 2013
Crystal structure of Escherichia coli manganese superoxide dismutase at 2.1-Å resolution Edwards, Ross A.; Baker, Heather M.; Whittaker, M. M. JBIC Journal of Biological Inorganic Chemistry, Vol. 3, Issue 2 https://doi.org/10.1007/s007750050217	journal	April 1998
Role of Tryptophan 161 in Catalysis by Human Manganese Superoxide Dismutase ^† Cabelli, Diane E.; Guan, Yue; Leveque, Vincent Biochemistry, Vol. 38, Issue 36 https://doi.org/10.1021/bi9909142	journal	September 1999
Changes in Gene Expression Associated with Developmental Arrest and Longevity in Caenorhabditis elegans Jones, S. J. M. Genome Research, Vol. 11, Issue 8 https://doi.org/10.1101/gr.184401	journal	July 2001
Water Oxidation by Single-Site Ruthenium Complexes: Using Ligands as Redox and Proton Transfer Mediators Kärkäs, Markus D.; Åkermark, Torbjörn; Johnston, Eric V. Angewandte Chemie International Edition, Vol. 51, Issue 46 https://doi.org/10.1002/anie.201205018	journal	September 2012
Comparison of Two Yeast MnSODs: Mitochondrial Saccharomyces cerevisiae versus Cytosolic Candida albicans Sheng, Yuewei; Stich, Troy A.; Barnese, Kevin Journal of the American Chemical Society, Vol. 133, Issue 51 https://doi.org/10.1021/ja2077476	journal	December 2011
The redox stress hypothesis of aging Sohal, Rajindar S.; Orr, William C. Free Radical Biology and Medicine, Vol. 52, Issue 3 https://doi.org/10.1016/j.freeradbiomed.2011.10.445	journal	February 2012
daf-2, an Insulin Receptor-Like Gene That Regulates Longevity and Diapause in Caenorhabditis elegans Kimura, K. D. Science, Vol. 277, Issue 5328 https://doi.org/10.1126/science.277.5328.942	journal	August 1997
Evolutionary conservation of regulated longevity assurance mechanisms McElwee, Joshua J.; Schuster, Eugene; Blanc, Eric Genome Biology, Vol. 8, Issue 7 https://doi.org/10.1186/gb-2007-8-7-r132	journal	January 2007
Combined NMR and computational study for azide binding to human manganese superoxide dismutase Emmler, Th.; Ayala, I.; Silverman, D. Solid State Nuclear Magnetic Resonance, Vol. 34, Issue 1-2 https://doi.org/10.1016/j.ssnmr.2008.03.005	journal	July 2008
A Mitochondrial Superoxide Signal Triggers Increased Longevity in Caenorhabditis elegans Yang, Wen; Hekimi, Siegfried PLoS Biology, Vol. 8, Issue 12 https://doi.org/10.1371/journal.pbio.1000556	journal	December 2010
Scaling and assessment of data quality Evans, Philip Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1, p. 72-82 https://doi.org/10.1107/S0907444905036693	journal	December 2005
Crystal structure of the cambialistic superoxide dismutase from Aeropyrum pernix K1 - insights into the enzyme mechanism and stability: Crystal structure of SOD from A. pernix K1 Nakamura, Tsutomu; Torikai, Kasumi; Uegaki, Koichi FEBS Journal, Vol. 278, Issue 4 https://doi.org/10.1111/j.1742-4658.2010.07977.x	journal	December 2010
Superoxide Dismutase McCord, Joe M.; Fridovich, Irwin Journal of Biological Chemistry, Vol. 244, Issue 22 https://doi.org/10.1016/S0021-9258(18)63504-5	journal	November 1969
Quantitative resolution of Cu,Zn- and Mn-superoxide dismutase activities Ysebaert-Vanneste, Maria; Vanneste, Walter H. Analytical Biochemistry, Vol. 107, Issue 1 https://doi.org/10.1016/0003-2697(80)90496-0	journal	September 1980
Structural Analysis of Peroxide-Soaked MnSOD Crystals Reveals Side-On Binding of Peroxide to Active-Site Manganese Porta, Jason; Vahedi-Faridi, Ardeschir; Borgstahl, Gloria E. O. Journal of Molecular Biology, Vol. 399, Issue 3 https://doi.org/10.1016/j.jmb.2010.04.031	journal	June 2010
Manganese superoxide dismutase from Thermus thermophilus Ludwig, Martha L.; Metzger, Anita L.; Pattridge, Katherine A. Journal of Molecular Biology, Vol. 219, Issue 2 https://doi.org/10.1016/0022-2836(91)90569-R	journal	May 1991
The importance of free radicals and catalytic metal ions in human diseases Halliwell, Barry; Gutteridge, John M. C. Molecular Aspects of Medicine, Vol. 8, Issue 2 https://doi.org/10.1016/0098-2997(85)90001-9	journal	January 1985
Crystal Structure of Y34F Mutant Human Mitochondrial Manganese Superoxide Dismutase and the Functional Role of Tyrosine 34 ^† ^, ^‡ Guan, Yue; Hickey, Michael J.; Borgstahl, Gloria E. O. Biochemistry, Vol. 37, Issue 14 https://doi.org/10.1021/bi972394l	journal	April 1998
A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans Morris, Jason Z.; Tissenbaum, Heidi A.; Ruvkun, Gary Nature, Vol. 382, Issue 6591 https://doi.org/10.1038/382536a0	journal	August 1996
DAF-16 Target Genes That Control C. elegans Life-Span and Metabolism Lee, S. S. Science, Vol. 300, Issue 5619 https://doi.org/10.1126/science.1083614	journal	April 2003
Protein structure alignment by incremental combinatorial extension (CE) of the optimal path Shindyalov, I. N.; Bourne, P. E. Protein Engineering Design and Selection, Vol. 11, Issue 9 https://doi.org/10.1093/protein/11.9.739	journal	September 1998
Accurate bond and angle parameters for X-ray protein structure refinement Engh, R. A.; Huber, R. Acta Crystallographica Section A Foundations of Crystallography, Vol. 47, Issue 4 https://doi.org/10.1107/S0108767391001071	journal	July 1991
Superoxide Radical and Superoxide Dismutases Fridovich, Irwin Annual Review of Biochemistry, Vol. 64, Issue 1 https://doi.org/10.1146/annurev.bi.64.070195.000525	journal	June 1995
Potent Anti-tumor Effects of an Active Site Mutant of Human Manganese-Superoxide Dismutase: EVOLUTIONARY CONSERVATION OF PRODUCT INHIBITION Davis, Christopher A.; Hearn, Amy S.; Fletcher, Bradley Journal of Biological Chemistry, Vol. 279, Issue 13 https://doi.org/10.1074/jbc.M310623200	journal	December 2003
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13641-0	journal	December 2019
Iron superoxide dismutase from the archaeon Sulfolobus solfataricus: analysis of structure and thermostability Ursby, Thomas; Adinolfi, Bianca Stella; Al-Karadaghi, Salam Journal of Molecular Biology, Vol. 286, Issue 1 https://doi.org/10.1006/jmbi.1998.2471	journal	February 1999
Cloning, Sequencing and Mapping of a Manganese Superoxide Dismutase Gene of the Nematode Caenorhabditis elegans Suzuki, N.; Inokuma, K.; Yasuda, K. DNA Research, Vol. 3, Issue 3 https://doi.org/10.1093/dnares/3.3.171	journal	January 1996
Redox regulation, gene expression and longevity: Redox regulation and lifespan Honda, Yoko; Tanaka, Masashi; Honda, Shuji Geriatrics & Gerontology International, Vol. 10 https://doi.org/10.1111/j.1447-0594.2010.00591.x	journal	June 2010
Characterization of the Product-inhibited Complex in Catalysis by Human Manganese Superoxide Dismutase Hearn, Amy S.; Tu, Chingkuang; Nick, Harry S. Journal of Biological Chemistry, Vol. 274, Issue 35 https://doi.org/10.1074/jbc.274.35.24457	journal	August 1999
X-ray Structure Analysis of the Iron-dependent Superoxide Dismutase fromMycobacterium tuberculosisat 2.0 Ångstroms Resolution Reveals Novel Dimer–Dimer Interactions Cooper, J. B.; McIntyre, K.; Badasso, M. O. Journal of Molecular Biology, Vol. 246, Issue 4 https://doi.org/10.1006/jmbi.1994.0105	journal	March 1995
Contribution of Human Manganese Superoxide Dismutase Tyrosine 34 to Structure and Catalysis ^† Perry, J. Jefferson P.; Hearn, Amy S.; Cabelli, Diane E. Biochemistry, Vol. 48, Issue 15 https://doi.org/10.1021/bi8023288	journal	April 2009
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
A Mild Impairment of Mitochondrial Electron Transport Has Sex-Specific Effects on Lifespan and Aging in Mice Hughes, Bryan G.; Hekimi, Siegfried PLoS ONE, Vol. 6, Issue 10 https://doi.org/10.1371/journal.pone.0026116	journal	October 2011
A novel nickel-containing superoxide dismutase from Streptomyces spp Youn, Hong-Duk; Kim, Eun-Ja; Roe, Jung-Hye Biochemical Journal, Vol. 318, Issue 3 https://doi.org/10.1042/bj3180889	journal	September 1996
Kinetic studies of superoxide dismutases: properties of the manganese-containing protein from Thermus thermophilus Bull, Christopher; Niederhoffer, Eric C.; Yoshida, Tatsuro Journal of the American Chemical Society, Vol. 113, Issue 11 https://doi.org/10.1021/ja00011a003	journal	May 1991
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Purification, crystallization and X-ray structures of the two manganese superoxide dismutases from Caenorhabditis elegans Trinh, Chi H.; Hunter, Thérèse; Stewart, Emma E. Acta Crystallographica Section F Structural Biology and Crystallization Communications, Vol. 64, Issue 12 https://doi.org/10.1107/S1744309108037056	journal	November 2008
Role of Tyrosine-34 in the Anion Binding Equilibria in Manganese(II) Superoxide Dismutases ^† Tabares, Leandro C.; Cortez, Néstor; Un, Sun Biochemistry, Vol. 46, Issue 32 https://doi.org/10.1021/bi700438j	journal	August 2007
The structure of human mitochondrial manganese superoxide dismutase reveals a novel tetrameric interface of two 4-helix bundles Borgstahl, Gloria E. O.; Parge, Hans E.; Hickey, Michael J. Cell, Vol. 71, Issue 1 https://doi.org/10.1016/0092-8674(92)90270-M	journal	October 1992
Structure-function in Escherichia coli iron superoxide dismutase: Comparisons with the manganese enzyme from Thermus thermophilus Lah, Myoung S.; Dixon, Melinda M.; Pattridge, Katherine A. Biochemistry, Vol. 34, Issue 5 https://doi.org/10.1021/bi00005a021	journal	February 1995
Active site spectral studies on manganese superoxide dismutase Whittaker, James W.; Whittaker, Mei M. Journal of the American Chemical Society, Vol. 113, Issue 15 https://doi.org/10.1021/ja00015a003	journal	July 1991
Structures of the Superoxide Reductase from Pyrococcus furiosus in the Oxidized and Reduced States ^, Yeh, Andrew P.; Hu, Yonglin; Jenney, Francis E. Biochemistry, Vol. 39, Issue 10 https://doi.org/10.1021/bi992428k	journal	February 2000
Comparison of the Crystal Structures of the Human Manganese Superoxide Dismutase and the Homologous Aspergillus fumigatus Allergen at 2-Å Resolution Flückiger, Sabine; Mittl, Peer R. E.; Scapozza, Leonardo The Journal of Immunology, Vol. 168, Issue 3 https://doi.org/10.4049/jimmunol.168.3.1267	journal	February 2002
Overview of the CCP4 suite and current developments. Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.52322	text	January 2011
Role of Metabolic H ₂ O ₂ Generation : REDOX SIGNALING AND OXIDATIVE STRESS Sies, Helmut Journal of Biological Chemistry, Vol. 289, Issue 13 https://doi.org/10.1074/jbc.R113.544635	journal	February 2014
Substitution of histidine 30 by asparagine in manganese superoxide dismutase alters biophysical properties and supports proliferation in a K562 leukemia cell line Bonetta, Rosalin; Hunter, Gary J.; Trinh, Chi H. European Biophysics Journal, Vol. 50, Issue 3-4 https://doi.org/10.1007/s00249-021-01544-2	journal	May 2021
The Hsp60 folding machinery is crucial for manganese superoxide dismutase folding and function Magnoni, R.; Palmfeldt, J.; Hansen, J. Free Radical Research, Vol. 48, Issue 2 https://doi.org/10.3109/10715762.2013.858147	journal	October 2013
Crystal Structure of the Metal-bound Superoxide Dismutase from Pyrobaculum aerophilum and Comparison with the Metal-free Form Lee, Sangho Bulletin of the Korean Chemical Society, Vol. 29, Issue 12, p. 2399-2402 https://doi.org/10.5012/bkcs.2008.29.12.2399	journal	December 2008
The daf‐2 gene network for longevity regulates oxidative stress resistance and Mn‐superoxide dismutase gene expression in Caenorhabditis elegans Honda, Yoko; Honda, Shuji The FASEB Journal, Vol. 13, Issue 11 https://doi.org/10.1096/fasebj.13.11.1385	journal	August 1999
Catalytic and Structural Effects of Amino Acid Substitution at Histidine 30 in Human Manganese Superoxide Dismutase: Insertion of Valine Cγ into the Substrate Access Channel ^† Hearn, Amy S.; Stroupe, M. Elizabeth; Cabelli, Diane E. Biochemistry, Vol. 42, Issue 10 https://doi.org/10.1021/bi0266481	journal	March 2003
Taking a “good” look at free radicals in the aging process Hekimi, Siegfried; Lapointe, Jérôme; Wen, Yang Trends in Cell Biology, Vol. 21, Issue 10 https://doi.org/10.1016/j.tcb.2011.06.008	journal	October 2011
Structural Mobility in Human Manganese Superoxide Dismutase ^† Quint, Patrick; Ayala, Idelisa; Busby, Scott A. Biochemistry, Vol. 45, Issue 27 https://doi.org/10.1021/bi0606288	journal	July 2006
A Novel Superoxide Dismutase Gene Encoding Membrane-bound and Extracellular Isoforms by Alternative Splicing in Caenorhabditis elegans Fujii, M. DNA Research, Vol. 5, Issue 1 https://doi.org/10.1093/dnares/5.1.25	journal	January 1998
Probing the Geometric and Electronic Structures of the Low-Temperature Azide Adduct and the Product-Inhibited Form of Oxidized Manganese Superoxide Dismutase ^† Jackson, Timothy A.; Karapetian, Anush; Miller, Anne-Frances Biochemistry, Vol. 44, Issue 5 https://doi.org/10.1021/bi048639t	journal	February 2005
The Redox System in C. elegans , a Phylogenetic Approach Johnston, Andrew D.; Ebert, Paul R. Journal of Toxicology, Vol. 2012 https://doi.org/10.1155/2012/546915	journal	January 2012
Superoxide Dismutases and Superoxide Reductases Sheng, Yuewei; Abreu, Isabel A.; Cabelli, Diane E. Chemical Reviews, Vol. 114, Issue 7 https://doi.org/10.1021/cr4005296	journal	January 2014
Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans Murphy, Coleen T.; McCarroll, Steven A.; Bargmann, Cornelia I. Nature, Vol. 424, Issue 6946 https://doi.org/10.1038/nature01789	journal	June 2003
Catalytic Properties of Human Manganese Superoxide Dismutase Hsu, Jan-Ling; Hsieh, Yunsheng; Tu, Chingkuang Journal of Biological Chemistry, Vol. 271, Issue 30 https://doi.org/10.1074/jbc.271.30.17687	journal	July 1996
Superoxide dismutases—a review of the metal-associated mechanistic variations Abreu, Isabel A.; Cabelli, Diane E. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1804, Issue 2 https://doi.org/10.1016/j.bbapap.2009.11.005	journal	February 2010
Transcriptional outputs of the Caenorhabditis elegans forkhead protein DAF-16 McElwee, Joshua; Bubb, Kerry; Thomas, James H. Aging Cell, Vol. 2, Issue 2 https://doi.org/10.1046/j.1474-9728.2003.00043.x	journal	April 2003
The integration of macromolecular diffraction data Leslie, Andrew G. W. Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1 https://doi.org/10.1107/S0907444905039107	journal	December 2005
Tetramerization Reinforces the Dimer Interface of MnSOD Sheng, Yuewei; Durazo, Armando; Schumacher, Mikhail PLoS ONE, Vol. 8, Issue 5 https://doi.org/10.1371/journal.pone.0062446	journal	May 2013
Effects of Substrate Analogues and pH on Manganese Superoxide Dismutases ^† Tabares, Leandro C.; Cortez, Néstor; Hiraoka, B. Yukihiro Biochemistry, Vol. 45, Issue 6 https://doi.org/10.1021/bi051947m	journal	February 2006

Cited By (5)

Mechanism of Different Stereoisomeric Astaxanthin in Resistance to Oxidative Stress in Caenorhabditis elegans: Mechanism of astaxanthin stereoisomers… Liu, Xiaojuan; Luo, Qingxin; Cao, Yong Journal of Food Science, Vol. 81, Issue 9 https://doi.org/10.1111/1750-3841.13417	journal	August 2016
A Review of the Catalytic Mechanism of Human Manganese Superoxide Dismutase Azadmanesh, Jahaun; Borgstahl, Gloria Antioxidants, Vol. 7, Issue 2 https://doi.org/10.3390/antiox7020025	journal	January 2018
The first crystal structure of manganese superoxide dismutase from the genus Staphylococcus Retnoningrum, Debbie S.; Yoshida, Hiromi; Arumsari, Sekar Acta Crystallographica Section F Structural Biology Communications, Vol. 74, Issue 3 https://doi.org/10.1107/s2053230x18001036	journal	February 2018
Redox manipulation of the manganese metal in human manganese superoxide dismutase for neutron diffraction Azadmanesh, Jahaun; Lutz, William E.; Weiss, Kevin L. Acta Crystallographica Section F Structural Biology Communications, Vol. 74, Issue 10 https://doi.org/10.1107/s2053230x18011299	journal	September 2018
Optimization in continuous phase‐transition extraction of crude flavonoids from finger citron fruit and evaluation on their antiaging activities Chen, Haiqiang; Wang, Jing; Liu, Xiaojuan Food Science & Nutrition, Vol. 8, Issue 3 https://doi.org/10.1002/fsn3.1450	journal	February 2020

Similar Records

Six-coordinate manganese(3+) in catalysis by yeast manganese superoxide dismutase

Journal Article · Wed Oct 10 00:00:00 EDT 2012 · Proc. Natl. Acad. Sci. USA · OSTI ID:1221758

Sheng, Yuewei; Gralla, Edith Butler; Schumacher, Mikhail; +3 more

Copper, zinc superoxide dismutase (Cu, ZnSOD) and manganese superoxide dismutase (MnSOD): Developmental changes in erythroleukemia cells (ELC)

Conference · Mon Mar 11 00:00:00 EST 1991 · FASEB Journal (Federation of American Societies for Experimental Biology); (United States) · OSTI ID:1221758

Yano, S; Clerch, L; Massaro, D

Human mitochondrial manganese superoxide dismutase polymorphic variant Ile58Thr reduces activity by destabilizing the tetrameric interface

Journal Article · Tue Apr 09 00:00:00 EDT 1996 · Biochemistry (Eaton) · OSTI ID:1221758

Borgstahl, G E.O.; Hickey, M J; Johnson, M J

Related Subjects

38 RADIATION CHEMISTRY, RADIOCHEMISTRY, AND NUCLEAR CHEMISTRY
Laser Electron Accelerator Facility (LEAF)
superoxide dismutase
conformational variation
MnSOD-3-azide complex
catalytic mechanism
product inhibition

Title: The structure of the Caenorhabditis elegans manganese superoxide dismutase MnSOD-3-azide complex

Citation Formats

References (84)

Cited By (5)

Similar Records

Related Subjects