Superoxide reduction by a superoxide reductase lacking the highly conserved lysine residue

Teixeira, Miguel; Cabelli, Diane; Pinto, Ana F.; Romao, Celia V.; Pinto, Liliana C.; Huber, Harald; Saraiva, Ligia M.; Todorovic, Smilja

doi:10.1007/s00775-014-1222-6

Title: Superoxide reduction by a superoxide reductase lacking the highly conserved lysine residue

Journal Article · Fri Dec 05 00:00:00 EST 2014 · JBIC Journal of Biological Inorganic Chemistry

DOI:https://doi.org/10.1007/s00775-014-1222-6· OSTI ID:1182506

Teixeira, Miguel ^[1]; Cabelli, Diane ^[2]; Pinto, Ana F. ^[3]; Romao, Celia V. ^[1]; Pinto, Liliana C. ^[1]; Huber, Harald ^[4]; Saraiva, Ligia M. ^[1]; Todorovic, Smilja ^[1]

Univ. Nova de Lisboa, Oeiras (Portugal)
Brookhaven National Lab. (BNL), Upton, NY (United States)
Univ. Nova de Lisboa, Oeiras (Portugal); Karolinska Inst., Stockholm (Sweden)
Univ. Regensburg, Regensburg (Germany)

Superoxide reductases (SORs) are the most recently identified superoxide detoxification systems, being found in microorganisms from the three domains of life. These enzymes are characterized by a catalytic mononuclear iron site, with one cysteine and four histidine ligands of the ferrous active form. A lysine residue in the –EKHVP– motif, located close to the active site, has been considered to be essential for the enzyme function, by contributing to the positive surface patch that attracts the superoxide anion and by controlling the chemistry of the catalytic mechanism through a hydrogen bond network. However, we show here that this residue is substituted by non-equivalent amino acids in several putative SORs from Archaea and unicellular Eukarya. In this work, we focus on mechanistic and spectroscopic studies of one of these less common enzymes, the SOR from the hyperthermophilic crenarchaeon Ignicoccus hospitalis. We employ pulse radiolysis fast kinetics and spectroscopic approaches to study the wild-type enzyme (₋E₂₃T₂₄HVP₋), and two mutants, T24K and E23A, the later mimicking enzymes lacking both the lysine and glutamate (a ferric ion ligand) of the motif. The efficiency of the wild type protein and mutants in reducing superoxide is comparable to other SORs, revealing the robustness of these enzymes to single mutations.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

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

Grant/Contract Number:: SC00112704

OSTI ID:: 1182506

Report Number(s):: BNL-107428-2015-JA; R&D Project: CO-004; KC0304030

Journal Information:: JBIC Journal of Biological Inorganic Chemistry, Vol. 20, Issue 1; ISSN 0949-8257

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 5 works

Citation information provided by
Web of Science

References (38)

Avoiding high-valent iron intermediates: Superoxide reductase and rubrerythrin Kurtz, Donald M. Journal of Inorganic Biochemistry, Vol. 100, Issue 4 https://doi.org/10.1016/j.jinorgbio.2005.12.017	journal	April 2006
Reductive elimination of superoxide: Structure and mechanism of superoxide reductases Pinto, Ana Filipa; Rodrigues, João V.; Teixeira, Miguel Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1804, Issue 2 https://doi.org/10.1016/j.bbapap.2009.10.011	journal	February 2010
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
Methanoferrodoxin represents a new class of superoxide reductase containing an iron-sulfur cluster: Superoxide reductase from Methanosarcina mazei Krätzer, Christian; Welte, Cornelia; Dörner, Katerina FEBS Journal, Vol. 278, Issue 3 https://doi.org/10.1111/j.1742-4658.2010.07964.x	journal	December 2010
A Blue Non-Heme Iron Protein from Desulfovibrio gigas Chen, Liang; Sharma, Pardeep; Gall, Jean European Journal of Biochemistry, Vol. 226, Issue 2 https://doi.org/10.1111/j.1432-1033.1994.tb20087.x	journal	December 1994
SORGOdb: Superoxide Reductase Gene Ontology curated DataBase Lucchetti-Miganeh, Céline; Goudenège, David; Thybert, David BMC Microbiology, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2180-11-105	journal	January 2011
Reaction of the Desulfoferrodoxin from Desulfoarculus baarsii with Superoxide Anion: EVIDENCE FOR A SUPEROXIDE REDUCTASE ACTIVITY Lombard, Murielle; Fontecave, Marc; Touati, Danièle Journal of Biological Chemistry, Vol. 275, Issue 1 https://doi.org/10.1074/jbc.275.1.115	journal	January 2000
Oxygen detoxification in the strict anaerobic archaeon Archaeoglobus fulgidus: superoxide scavenging by Neelaredoxin Abreu, Isabel A.; Saraiva, Ligia M.; Carita, Joao Molecular Microbiology, Vol. 38, Issue 2 https://doi.org/10.1046/j.1365-2958.2000.02121.x	journal	October 2000
Superoxide Reductase from Desulfoarculus baarsii : Reaction Mechanism and Role of Glutamate 47 and Lysine 48 in Catalysis ^† Lombard, Murielle; Houée-Levin, Chantal; Touati, Danièle Biochemistry, Vol. 40, Issue 16 https://doi.org/10.1021/bi0023908	journal	April 2001
Fe3+–η2–peroxo species in superoxide reductase from Treponema pallidum. Comparison with Desulfoarculus baarsii Mathé, Christelle; Nivière, Vincent; Houée-Levin, Chantal Biophysical Chemistry, Vol. 119, Issue 1 https://doi.org/10.1016/j.bpc.2005.06.013	journal	January 2006
Superoxide Reductase from Desulfoarculus baarsii : Identification of Protonation Steps in the Enzymatic Mechanism ^† Nivière, Vincent; Asso, Marcel; Weill, Claire O. Biochemistry, Vol. 43, Issue 3 https://doi.org/10.1021/bi035698i	journal	January 2004
Superoxide reductase from Desulfoarculus baarsii Nivière, Vincent; Lombard, Murielle Methods in Enzymology https://doi.org/10.1016/S0076-6879(02)49328-7	book	January 2002
Pulse radiolysis studies on superoxide reductase from Treponema pallidum Nivière, Vincent; Lombard, Murielle; Fontecave, Marc FEBS Letters, Vol. 497, Issue 2-3 https://doi.org/10.1016/S0014-5793(01)02468-1	journal	May 2001
Superoxide Reduction Mechanism of Archaeoglobus fulgidus One-Iron Superoxide Reductase ^† Rodrigues, João V.; Abreu, Isabel A.; Cabelli, Diane Biochemistry, Vol. 45, Issue 30 https://doi.org/10.1021/bi052489k	journal	August 2006
Superoxide reduction by Archaeoglobus fulgidus desulfoferrodoxin: comparison with neelaredoxin Rodrigues, João V.; Saraiva, Lígia M.; Abreu, Isabel A. JBIC Journal of Biological Inorganic Chemistry, Vol. 12, Issue 2 https://doi.org/10.1007/s00775-006-0182-x	journal	October 2006
Superoxide reduction by Nanoarchaeum equitans neelaredoxin, an enzyme lacking the highly conserved glutamate iron ligand Rodrigues, João V.; Victor, Bruno L.; Huber, Harald JBIC Journal of Biological Inorganic Chemistry, Vol. 13, Issue 2 https://doi.org/10.1007/s00775-007-0313-z	journal	October 2007
Control of the Evolution of Iron Peroxide Intermediate in Superoxide Reductase from Desulfoarculus baarsii. Involvement of Lysine 48 in Protonation Bonnot, Florence; Molle, Thibaut; Ménage, Stéphane Journal of the American Chemical Society, Vol. 134, Issue 11 https://doi.org/10.1021/ja209297n	journal	March 2012
Computational Study of the Non-Heme Iron Active Site in Superoxide Reductase and Its Reaction with Superoxide Silaghi-Dumitrescu, Radu; Silaghi-Dumitrescu, Ioan; Coulter, Eric D. Inorganic Chemistry, Vol. 42, Issue 2 https://doi.org/10.1021/ic025684l	journal	January 2003
Oxidation State Changes and Electron Flow in Enzymatic Catalysis and Electrocatalysis through Wannier-Function Analysis Sit, Patrick H. -L.; Zipoli, Federico; Chen, Jia Chemistry - A European Journal, Vol. 17, Issue 43 https://doi.org/10.1002/chem.201101916	journal	September 2011
Sulfur K-Edge X-ray Absorption Spectroscopy and Density Functional Theory Calculations on Superoxide Reductase: Role of the Axial Thiolate in Reactivity Dey, Abhishek; Jenney,, Francis E.; Adams, Michael W. W. Journal of the American Chemical Society, Vol. 129, Issue 41 https://doi.org/10.1021/ja064167p	journal	October 2007
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
The Mechanism of Superoxide Scavenging by Archaeoglobus fulgidus Neelaredoxin Abreu, Isabel A.; Saraiva, Lı́gia M.; Soares, Cláudio M. Journal of Biological Chemistry, Vol. 276, Issue 42 https://doi.org/10.1074/jbc.M103232200	journal	August 2001
Kinetics and Mechanism of Superoxide Reduction by Two-Iron Superoxide Reductase from Desulfovibrio vulgaris ^† Emerson, Joseph P.; Coulter, Eric D.; Cabelli, Diane E. Biochemistry, Vol. 41, Issue 13 https://doi.org/10.1021/bi0119159	journal	April 2002
Raman-Assisted Crystallography Reveals End-On Peroxide Intermediates in a Nonheme Iron Enzyme Katona, G.; Carpentier, P.; Niviere, V. Science, Vol. 316, Issue 5823 https://doi.org/10.1126/science.1138885	journal	April 2007
A genomic analysis of the archaeal system Ignicoccus hospitalis-Nanoarchaeum equitans Podar, Mircea; Anderson, Iain; Makarova, Kira S. Genome Biology, Vol. 9, Issue 11 https://doi.org/10.1186/gb-2008-9-11-r158	journal	January 2008
The superoxide reductase from the early diverging eukaryote Giardia intestinalis Testa, Fabrizio; Mastronicola, Daniela; Cabelli, Diane E. Free Radical Biology and Medicine, Vol. 51, Issue 8 https://doi.org/10.1016/j.freeradbiomed.2011.07.017	journal	October 2011
Cloning, purification, crystallization and X-ray crystallographic analysis of Ignicoccus hospitalis neelaredoxin Pinho, Filipa G.; Romão, Célia V.; Pinto, Ana F. Acta Crystallographica Section F Structural Biology and Crystallization Communications, Vol. 66, Issue 5 https://doi.org/10.1107/S1744309110012030	journal	April 2010
Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 Laemmli, U. K. Nature, Vol. 227, Issue 5259, p. 680-685 https://doi.org/10.1038/227680a0	journal	August 1970
Measurement of protein using bicinchoninic acid Smith, P. K.; Krohn, R. I.; Hermanson, G. T. Analytical Biochemistry, Vol. 150, Issue 1 https://doi.org/10.1016/0003-2697(85)90442-7	journal	October 1985
Enzyme activity as an indicator of red cell age Sass, Martin D.; Vorsanger, Eric; Spear, Paul W. Clinica Chimica Acta, Vol. 10, Issue 1 https://doi.org/10.1016/0009-8981(64)90210-4	journal	July 1964
Reactions of Hydrogen Peroxide with Familial Amyotrophic Lateral Sclerosis Mutant Human Copper-Zinc Superoxide Dismutases Studied by Pulse Radiolysis Goto, Joy J.; Gralla, Edith Butler; Valentine, Joan Selverstone Journal of Biological Chemistry, Vol. 273, Issue 46 https://doi.org/10.1074/jbc.273.46.30104	journal	November 1998
Spectroscopic Studies of Pyrococcus furiosus Superoxide Reductase: Implications for Active-Site Structures and the Catalytic Mechanism Clay, Michael D.; Jenney,, Francis E.; Hagedoorn, Peter L. Journal of the American Chemical Society, Vol. 124, Issue 5 https://doi.org/10.1021/ja016889g	journal	February 2002
Fe ³⁺ -Hydroxide Ligation in the Superoxide Reductase from Desulfoarculus b aarsii Is Associated with pH Dependent Spectral Changes Mathé, Christelle; Nivière, Vincent; Mattioli, Tony A. Journal of the American Chemical Society, Vol. 127, Issue 47 https://doi.org/10.1021/ja053808y	journal	November 2005
Resonance Raman study of the superoxide reductase from Archaeoglobus fulgidus, E12 mutants and a ‘natural variant’ Todorovic, Smilja; Rodrigues, João V.; Pinto, Ana F. Physical Chemistry Chemical Physics, Vol. 11, Issue 11 https://doi.org/10.1039/b815489a	journal	January 2009
Assessing the Role of the Active-site Cysteine Ligand in the Superoxide Reductase from Desulfoarculus baarsii Mathé, Christelle; Weill, Claire O.; Mattioli, Tony A. Journal of Biological Chemistry, Vol. 282, Issue 30 https://doi.org/10.1074/jbc.M700279200	journal	June 2007
Resonance Raman Characterization of the Mononuclear Iron Active-Site Vibrations and Putative Electron Transport Pathways in Pyrococcus furiosus Superoxide Reductase Clay, Michael D.; Jenney, Francis E.; Noh, Hak Joon Biochemistry, Vol. 41, Issue 31 https://doi.org/10.1021/bi025833b	journal	July 2002
Electrode potentials of partially reduced oxygen species, from dioxygen to water Koppenol, Willem H.; Stanbury, David M.; Bounds, Patricia L. Free Radical Biology and Medicine, Vol. 49, Issue 3 https://doi.org/10.1016/j.freeradbiomed.2010.04.011	journal	August 2010
The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools Thompson, J. Nucleic Acids Research, Vol. 25, Issue 24 https://doi.org/10.1093/nar/25.24.4876	journal	December 1997

Cited By (1)

Rational redox tuning of transition metal sites: learning from superoxide reductase Horch, Marius Chemical Communications, Vol. 55, Issue 62 https://doi.org/10.1039/c9cc04004h	journal	January 2019

Similar Records

Nickel Superoxide Dismutase: Structural and Functional Roles of Cys2 and Cys6

Journal Article · Fri Jan 01 00:00:00 EST 2010 · Journal of Biological Inorganic Chemistry · OSTI ID:1182506

Ryan, K; Johnson, O; Cabelli, D; +2 more

Nickel Superoxide Dismutase: Structural and Functional Roles of Cys2 and Cys6

Journal Article · Tue Jun 01 00:00:00 EDT 2010 · Journal of Biological Inorganic Chemistry · OSTI ID:1182506

Maroney, M J; Cabelli, D; Ryan, K C; +2 more

Role of Lysine-54 in determining cofactor specificity and binding in human dihydrofolate reductase

Journal Article · Tue Sep 04 00:00:00 EDT 1990 · Biochemistry; (USA) · OSTI ID:1182506

Huang, Shaoming; Tan, Xuehai; Thompson, P D; +5 more

Related Subjects

38 RADIATION CHEMISTRY, RADIOCHEMISTRY, AND NUCLEAR CHEMISTRY
laser electron accelerator facility
superoxide
oxidative stress
superoxide reductase
Ignicoccus

Title: Superoxide reduction by a superoxide reductase lacking the highly conserved lysine residue

Citation Formats

References (38)

Cited By (1)

Similar Records

Related Subjects