Structural, functional and immunogenic insights on Cu,Zn superoxide dismutase pathogenic virulence factors from Neisseria meningitidis and Brucella abortus
Abstract
Bacterial pathogens Neisseria meningitidis and Brucella abortus pose threats to human and animal health worldwide, causing meningococcal disease and brucellosis, respectively. Mortality from acute N. meningitidis infections remains high despite antibiotics, and brucellosis presents alimentary and health consequences. Superoxide dismutases are master regulators of reactive oxygen and general pathogenicity factors and are therefore therapeutic targets. Cu,Zn superoxide dismutases (SODs) localized to the periplasm promote survival by detoxifying superoxide radicals generated by major host antimicrobial immune responses. We discovered that passive immunization with an antibody directed at N. meningitidis SOD (NmSOD) was protective in a mouse infection model. To define the relevant atomic details and solution assembly states of this important virulence factor, we report high-resolution and X-ray scattering analyses of NmSOD and of SOD from B. abortus (BaSOD). The NmSOD structures revealed an auxiliary tetrahedral Cu-binding site bridging the dimer interface; mutational analyses suggested that this metal site contributes to protein stability, with implications for bacterial defense mechanisms. Biochemical and structural analyses informed us about electrostatic substrate guidance, dimer assembly, and an exposed C-terminal epitope in the NmSOD dimer. In contrast, the monomeric BaSOD structure provided insights for extending immunogenic peptide epitopes derived from the protein. These collective results revealmore »
- Authors:
-
- The Scripps Research Institute, La Jolla, CA (United States); Lawrence Berkeley National Lab., Berkeley, CA (United States)
- The Scripps Research Institute, La Jolla, CA (United States)
- Brookhaven National Lab. (BNL), Upton, NY (United States)
- National Animal Disease Center, Ames, IA (United States)
- Public Health England (previously The Health Protection Agency), Salisbury (United Kingdom)
- Imperial College, London (United Kingdom)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of Texas M.D. Anderson Cancer Center, Houston, TX (United States)
- Publication Date:
- Research Org.:
- Brookhaven National Laboratory (BNL), Upton, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1224775
- Alternate Identifier(s):
- OSTI ID: 1235891
- Report Number(s):
- BNL-108508-2015-JA; BNL-111744-2016-JA
Journal ID: ISSN 0021-9193; R&D Project: CO004; KC0304030
- Grant/Contract Number:
- SC0012704
- Resource Type:
- Journal Article: Accepted Manuscript
- Journal Name:
- Journal of Bacteriology
- Additional Journal Information:
- Journal Volume: 197; Journal Issue: 24; Journal ID: ISSN 0021-9193
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 38 RADIATION CHEMISTRY, RADIOCHEMISTRY, AND NUCLEAR CHEMISTRY; Laser Electron Accelerator Facility (LEAF)
Citation Formats
Pratt, Ashley J., DiDonato, Michael, Shin, David S., Cabelli, Diane E., Bruns, Cami K., Belzer, Carol A., Gorringe, Andrew R., Langford, Paul R., Tabatabai, Louisa B., Kroll, J. Simon, Tainer, John A., and Getzoff, Elizabeth D. Structural, functional and immunogenic insights on Cu,Zn superoxide dismutase pathogenic virulence factors from Neisseria meningitidis and Brucella abortus. United States: N. p., 2015.
Web. doi:10.1128/JB.00343-15.
Pratt, Ashley J., DiDonato, Michael, Shin, David S., Cabelli, Diane E., Bruns, Cami K., Belzer, Carol A., Gorringe, Andrew R., Langford, Paul R., Tabatabai, Louisa B., Kroll, J. Simon, Tainer, John A., & Getzoff, Elizabeth D. Structural, functional and immunogenic insights on Cu,Zn superoxide dismutase pathogenic virulence factors from Neisseria meningitidis and Brucella abortus. United States. https://doi.org/10.1128/JB.00343-15
Pratt, Ashley J., DiDonato, Michael, Shin, David S., Cabelli, Diane E., Bruns, Cami K., Belzer, Carol A., Gorringe, Andrew R., Langford, Paul R., Tabatabai, Louisa B., Kroll, J. Simon, Tainer, John A., and Getzoff, Elizabeth D. 2015.
"Structural, functional and immunogenic insights on Cu,Zn superoxide dismutase pathogenic virulence factors from Neisseria meningitidis and Brucella abortus". United States. https://doi.org/10.1128/JB.00343-15. https://www.osti.gov/servlets/purl/1224775.
@article{osti_1224775,
title = {Structural, functional and immunogenic insights on Cu,Zn superoxide dismutase pathogenic virulence factors from Neisseria meningitidis and Brucella abortus},
author = {Pratt, Ashley J. and DiDonato, Michael and Shin, David S. and Cabelli, Diane E. and Bruns, Cami K. and Belzer, Carol A. and Gorringe, Andrew R. and Langford, Paul R. and Tabatabai, Louisa B. and Kroll, J. Simon and Tainer, John A. and Getzoff, Elizabeth D.},
abstractNote = {Bacterial pathogens Neisseria meningitidis and Brucella abortus pose threats to human and animal health worldwide, causing meningococcal disease and brucellosis, respectively. Mortality from acute N. meningitidis infections remains high despite antibiotics, and brucellosis presents alimentary and health consequences. Superoxide dismutases are master regulators of reactive oxygen and general pathogenicity factors and are therefore therapeutic targets. Cu,Zn superoxide dismutases (SODs) localized to the periplasm promote survival by detoxifying superoxide radicals generated by major host antimicrobial immune responses. We discovered that passive immunization with an antibody directed at N. meningitidis SOD (NmSOD) was protective in a mouse infection model. To define the relevant atomic details and solution assembly states of this important virulence factor, we report high-resolution and X-ray scattering analyses of NmSOD and of SOD from B. abortus (BaSOD). The NmSOD structures revealed an auxiliary tetrahedral Cu-binding site bridging the dimer interface; mutational analyses suggested that this metal site contributes to protein stability, with implications for bacterial defense mechanisms. Biochemical and structural analyses informed us about electrostatic substrate guidance, dimer assembly, and an exposed C-terminal epitope in the NmSOD dimer. In contrast, the monomeric BaSOD structure provided insights for extending immunogenic peptide epitopes derived from the protein. These collective results reveal unique contributions of SOD to pathogenic virulence, refine predictive motifs for distinguishing SOD classes, and suggest general targets for antibacterial immune responses. Furthermore, the identified functional contributions, motifs, and targets distinguishing bacterial and eukaryotic SOD assemblies presented here provide a foundation for efforts to develop SOD-specific inhibitors of or vaccines against these harmful pathogens.},
doi = {10.1128/JB.00343-15},
url = {https://www.osti.gov/biblio/1224775},
journal = {Journal of Bacteriology},
issn = {0021-9193},
number = 24,
volume = 197,
place = {United States},
year = {Mon Oct 12 00:00:00 EDT 2015},
month = {Mon Oct 12 00:00:00 EDT 2015}
}
Web of Science
Works referenced in this record:
Identification of Francisella tularensis Live Vaccine Strain CuZn Superoxide Dismutase as Critical for Resistance to Extracellularly Generated Reactive Oxygen Species
journal, August 2009
- Melillo, A. A.; Mahawar, M.; Sellati, T. J.
- Journal of Bacteriology, Vol. 191, Issue 20
Novel dimeric interface and electrostatic recognition in bacterial Cu,Zn superoxide dismutase
journal, November 1996
- Bourne, Y.; Redford, S. M.; Steinman, H. M.
- Proceedings of the National Academy of Sciences, Vol. 93, Issue 23
Changes in crystallographic structure and thermostability of a Cu,Zn superoxide dismutase mutant resulting from the removal of a buried cysteine.
journal, August 1990
- McRee, D. E.; Redford, S. M.; Getzoff, E. D.
- Journal of Biological Chemistry, Vol. 265, Issue 24
DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering
journal, January 2009
- Franke, Daniel; Svergun, Dmitri I.
- Journal of Applied Crystallography, Vol. 42, Issue 2, p. 342-346
The Megavirus Chilensis Cu,Zn-Superoxide Dismutase: the First Viral Structure of a Typical Cellular Copper Chaperone-Independent Hyperstable Dimeric Enzyme
journal, October 2014
- Lartigue, Audrey; Burlat, Bénédicte; Coutard, Bruno
- Journal of Virology, Vol. 89, Issue 1
The Structure of Human Extracellular Copper–Zinc Superoxide Dismutase at 1.7 Å Resolution: Insights into Heparin and Collagen Binding
journal, May 2009
- Antonyuk, Svetlana V.; Strange, Richard W.; Marklund, Stefan L.
- Journal of Molecular Biology, Vol. 388, Issue 2
Amyloid-like filaments and water-filled nanotubes formed by SOD1 mutant proteins linked to familial ALS
journal, May 2003
- Elam, Jennifer Stine; Taylor, Alexander B.; Strange, Richard
- Nature Structural & Molecular Biology, Vol. 10, Issue 6
Single mutations at the subunit interface modulate copper reactivity in Photobacterium leiognathi Cu,Zn superoxide dismutase
journal, May 2001
- Stroppolo, M. E.; Pesce, A.; D’Orazio, M.
- Journal of Molecular Biology, Vol. 308, Issue 3
Developing master keys to brain pathology, cancer and aging from the structural biology of proteins controlling reactive oxygen species and DNA repair
journal, April 2007
- Perry, J. J. P.; Fan, L.; Tainer, J. A.
- Neuroscience, Vol. 145, Issue 4
Neisseria meningitidis: Biology, Microbiology, and Epidemiology
book, September 2011
- Rouphael, Nadine G.; Stephens, David S.
- Methods in Molecular Biology
The role of arginine 143 in the electrostatics and mechanism of Cu, Zn superoxide dismutase: Computational and experimental evaluation by mutational analysis
journal, May 1994
- Fisher, Cindy L.; Cabelli, Diane E.; Tainer, John A.
- Proteins: Structure, Function, and Genetics, Vol. 19, Issue 1
The reactivity of anti-peptide antibodies is a function of the atomic mobility of sites in a protein
journal, November 1984
- Tainer, John A.; Getzoff, Elizabeth D.; Alexander, Hannah
- Nature, Vol. 312, Issue 5990
Active-site Copper and Zinc Ions Modulate the Quaternary Structure of Prokaryotic Cu,Zn Superoxide Dismutase
journal, March 2003
- Cioni, P.; Pesce, A.; Morozzo della Rocca, B.
- Journal of Molecular Biology, Vol. 326, Issue 5
Super-Resolution in Solution X-Ray Scattering and Its Applications to Structural Systems Biology
journal, May 2013
- Rambo, Robert P.; Tainer, John A.
- Annual Review of Biophysics, Vol. 42, Issue 1
Copper at the Front Line of the Host-Pathogen Battle
journal, September 2012
- Festa, Richard A.; Thiele, Dennis J.
- PLoS Pathogens, Vol. 8, Issue 9
[16] SHELXL: High-resolution refinement
book, January 1997
- Sheldrick, George M.; Schneider, Thomas R.
- Methods in Enzymology
Candida albicans SOD5 represents the prototype of an unprecedented class of Cu-only superoxide dismutases required for pathogen defense
journal, April 2014
- Gleason, J. E.; Galaleldeen, A.; Peterson, R. L.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 16
Cloning, expression, and occurrence of the Brucella Cu-Zn superoxide dismutase.
journal, January 1990
- Bricker, B. J.; Tabatabai, L. B.; Judge, B. A.
- Infection and Immunity, Vol. 58, Issue 9
The role of innate immune signals in immunity to Brucella abortus
journal, January 2012
- Gomes, Marco Túlio R.; Campos, Priscila C.; de Almeida, Leonardo A.
- Frontiers in Cellular and Infection Microbiology, Vol. 2
The Good and the Bad of Antibiotics
journal, July 2013
- Chandel, N. S.; Budinger, G. R. S.
- Science Translational Medicine, Vol. 5, Issue 192
History of biological metal utilization inferred through phylogenomic analysis of protein structures
journal, May 2010
- Dupont, C. L.; Butcher, A.; Valas, R. E.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 23
Differential contribution of sodC1 and sodC2 to intracellular survival and pathogenicity of Salmonella enterica serovar Choleraesuis
journal, April 2005
- Ammendola, Serena; Ajello, Maria; Pasquali, Paolo
- Microbes and Infection, Vol. 7, Issue 4
Over-expression of homologous antigens in a leucine auxotroph of Brucella abortus strain RB51 protects mice against a virulent B. suis challenge
journal, April 2011
- Rajasekaran, Parthiban; Surendran, Naveen; Seleem, Mohamed N.
- Vaccine, Vol. 29, Issue 17
UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004
- Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C.
- Journal of Computational Chemistry, Vol. 25, Issue 13
Genetically Engineered Polymers of Human CuZn Superoxide Dismutase
journal, March 1989
- Hallewell, R. A.; Laria, I.; Tabrizi, A.
- Journal of Biological Chemistry, Vol. 264, Issue 9
Treatment strategies for central nervous system infections: an update
journal, October 2014
- Tan, Ying Ching; Gill, Arshdeep Kaur; Kim, Kwang Sik
- Expert Opinion on Pharmacotherapy, Vol. 16, Issue 2
Unique Features of the sodC -encoded Superoxide Dismutase from Mycobacterium tuberculosis , a Fully Functional Copper-containing Enzyme Lacking Zinc in the Active Site
journal, May 2004
- Spagnolo, Laura; Törö, Imre; D'Orazio, Melania
- Journal of Biological Chemistry, Vol. 279, Issue 32
Superoxide Stress Decreases Expression of srfA through Inhibition of Transcription of the comQXP Quorum-Sensing Locus in Bacillus subtilis
journal, February 2006
- Ohsawa, Taku; Tsukahara, Kensuke; Sato, Tsutomu
- The Journal of Biochemistry, Vol. 139, Issue 2
How does the oxidative burst of macrophages kill bacteria? Still an open question: How do phagocytic ROS kill bacteria?
journal, March 2011
- Slauch, James M.
- Molecular Microbiology, Vol. 80, Issue 3
Superoxide Dismutase from the Eukaryotic Thermophile Alvinella pompejana: Structures, Stability, Mechanism, and Insights into Amyotrophic Lateral Sclerosis
journal, February 2009
- Shin, David S.; DiDonato, Michael; Barondeau, David P.
- Journal of Molecular Biology, Vol. 385, Issue 5
A vaccine against serogroup B Neisseria meningitidis: dealing with uncertainty
journal, May 2014
- Andrews, Sophie M.; Pollard, Andrew J.
- The Lancet Infectious Diseases, Vol. 14, Issue 5
AMoRe : an automated package for molecular replacement
journal, March 1994
- Navaza, J.
- Acta Crystallographica Section A Foundations of Crystallography, Vol. 50, Issue 2
Brucella as a Potential Agent of Bioterrorism
journal, February 2013
- D. Doganay, Gizem; Doganay, Mehmet
- Recent Patents on Anti-Infective Drug Discovery, Vol. 8, Issue 1
PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
The changing and dynamic epidemiology of meningococcal disease
journal, May 2012
- Halperin, Scott A.; Bettinger, Julie A.; Greenwood, Brian
- Vaccine, Vol. 30
Detection and Quantification of Superoxide Formed within the Periplasm of Escherichia coli
journal, August 2006
- Korshunov, S.; Imlay, J. A.
- Journal of Bacteriology, Vol. 188, Issue 17
Current Perspectives on Rabies Postexposure Prophylaxis
journal, April 2015
- Blaise, Agathe; Gautret, Philippe
- Infectious Disorders - Drug Targets, Vol. 15, Issue 1
Faster superoxide dismutase mutants designed by enhancing electrostatic guidance
journal, July 1992
- Getzoff, Elizabeth D.; Cabelli, Diane E.; Fisher, Cindy L.
- Nature, Vol. 358, Issue 6384
The Solution Structure of the Monomeric Copper, Zinc Superoxide Dismutase from Salmonella enterica : Structural Insights To Understand the Evolution toward the Dimeric Structure †
journal, December 2008
- Mori, Mirko; Jiménez, Beatriz; Piccioli, Mario
- Biochemistry, Vol. 47, Issue 49
Mechanisms of Oxidative Protein Folding in the Bacterial Cell Envelope
journal, October 2010
- Kadokura, Hiroshi; Beckwith, Jon
- Antioxidants & Redox Signaling, Vol. 13, Issue 8
A protein isolated from Brucella abortus is a copper-zinc superoxide dismutase
journal, January 1990
- Beck, Bonnie L.; Tabatabai, Louisa B.; Mayfield, John E.
- Biochemistry, Vol. 29, Issue 2
Physiological Roles of Mitochondrial Reactive Oxygen Species
journal, October 2012
- Sena, Laura A.; Chandel, Navdeep S.
- Molecular Cell, Vol. 48, Issue 2
Structural Characterization of the Active Site of Brucella abortus Cu-Zn Superoxide Dismutase: A 15N and 1H NMR Investigation
journal, September 1995
- Chen, Yen-Liang; Park, Sanggyu; Thornburg, Robert W.
- Biochemistry, Vol. 34, Issue 38
Accurate assessment of mass, models and resolution by small-angle scattering
journal, April 2013
- Rambo, Robert P.; Tainer, John A.
- Nature, Vol. 496, Issue 7446
The structural biochemistry of the superoxide dismutases
journal, February 2010
- Perry, J. J. P.; Shin, D. S.; Getzoff, E. D.
- Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1804, Issue 2
SOD2 to SOD1 Switch in Breast Cancer
journal, January 2014
- Papa, Luena; Hahn, Mary; Marsh, Ellen L.
- Journal of Biological Chemistry, Vol. 289, Issue 9
Determination and analysis of the 2 Å structure of copper, zinc superoxide dismutase
journal, September 1982
- Tainer, John A.; Getzoff, Elizabeth D.; Beem, Karl M.
- Journal of Molecular Biology, Vol. 160, Issue 2
Bacterial species exhibit diversity in their mechanisms and capacity for protein disulfide bond formation
journal, August 2008
- Dutton, R. J.; Boyd, D.; Berkmen, M.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 33
Uniqueness of ab initio shape determination in small-angle scattering
journal, April 2003
- Volkov, Vladimir V.; Svergun, Dmitri I.
- Journal of Applied Crystallography, Vol. 36, Issue 3, p. 860-864
Clinical Manifestations of Human Brucellosis: A Systematic Review and Meta-Analysis
journal, December 2012
- Dean, Anna S.; Crump, Lisa; Greter, Helena
- PLoS Neglected Tropical Diseases, Vol. 6, Issue 12
Bacterial redox sensors
journal, December 2004
- Green, Jeffrey; Paget, Mark S.
- Nature Reviews Microbiology, Vol. 2, Issue 12
Presence of Copper- and Zinc-Containing Superoxide Dismutase in Commensal Haemophilus haemolyticus Isolates Can Be Used as a Marker To Discriminate Them from Nontypeable H. influenzae Isolates
journal, September 2006
- Fung, W. W. M.; O'Dwyer, C. A.; Sinha, S.
- Journal of Clinical Microbiology, Vol. 44, Issue 11
Assembly and antigenicity of the Neisseria gonorrhoeae pilus mapped with antibodies.
journal, January 1996
- Forest, K. T.; Bernstein, S. L.; Getzoff, E. D.
- Infection and immunity, Vol. 64, Issue 2
On the possible roles of N-terminal His-rich domains of Cu,Zn SODs of some Gram-negative bacteria
journal, January 2012
- Árus, Dávid; Jancsó, Attila; Szunyogh, Dániel
- Journal of Inorganic Biochemistry, Vol. 106, Issue 1
The new global map of human brucellosis
journal, February 2006
- Pappas, Georgios; Papadimitriou, Photini; Akritidis, Nikolaos
- The Lancet Infectious Diseases, Vol. 6, Issue 2
Structure and mechanism of copper, zinc superoxide dismutase
journal, November 1983
- Tainer, John A.; Getzoff, Elizabeth D.; Richardson, Jane S.
- Nature, Vol. 306, Issue 5940
Evolution of CuZn superoxide dismutase and the Greek Key β-barrel structural motif
journal, January 1989
- Getzoff, Elizabeth D.; Tainer, John A.; Stempien, Michelle M.
- Proteins: Structure, Function, and Genetics, Vol. 5, Issue 4
A Histidine-rich and Cysteine-rich Metal-binding Domain at the C Terminus of Heat Shock Protein A from Helicobacter pylori : IMPLICATION FOR NICKEL HOMEOSTASIS AND BISMUTH SUSCEPTIBILITY
journal, March 2008
- Cun, Shujian; Li, Hongyan; Ge, Ruiguang
- Journal of Biological Chemistry, Vol. 283, Issue 22
Crystallography & NMR System: A New Software Suite for Macromolecular Structure Determination
journal, September 1998
- Brünger, A. T.; Adams, P. D.; Clore, G. M.
- Acta Crystallographica Section D Biological Crystallography, Vol. 54, Issue 5
Conquering the Meningococcus
journal, January 2007
- Stephens, David S.
- FEMS Microbiology Reviews, Vol. 31, Issue 1
Function of the Greek key connection analysed using circular permutants of superoxide dismutase
journal, May 1997
- Boissinot, M.; Karnas, S.; Lepock, J. R.
- The EMBO Journal, Vol. 16, Issue 9
ElNemo: a normal mode web server for protein movement analysis and the generation of templates for molecular replacement
journal, July 2004
- Suhre, K.; Sanejouand, Y. -H.
- Nucleic Acids Research, Vol. 32, Issue Web Server
Chlorovirus PBCV-1 Encodes an Active Copper-Zinc Superoxide Dismutase
journal, August 2014
- Kang, M.; Duncan, G. A.; Kuszynski, C.
- Journal of Virology, Vol. 88, Issue 21
X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution
journal, August 2007
- Putnam, Christopher D.; Hammel, Michal; Hura, Greg L.
- Quarterly Reviews of Biophysics, Vol. 40, Issue 3
A Histidine-rich Metal Binding Domain at the N Terminus of Cu,Zn-Superoxide Dismutases from Pathogenic Bacteria: A NOVEL STRATEGY FOR METAL CHAPERONING
journal, May 2001
- Battistoni, Andrea; Pacello, Francesca; Mazzetti, Anna Paola
- Journal of Biological Chemistry, Vol. 276, Issue 32
Co-immunization with interlukin-18 enhances the protective efficacy of liposomes encapsulated recombinant Cu–Zn superoxide dismutase protein against Brucella abortus
journal, June 2011
- Singha, Harisankar; Mallick, Amirul Islam; Jana, Chandrakanta
- Vaccine, Vol. 29, Issue 29-30
A History of the Development of Brucella Vaccines
journal, January 2013
- Avila-Calderón, Eric Daniel; Lopez-Merino, Ahidé; Sriranganathan, Nammalwar
- BioMed Research International, Vol. 2013
Aggregation propensities of superoxide dismutase G93 hotspot mutants mirror ALS clinical phenotypes
journal, October 2014
- Pratt, A. J.; Shin, D. S.; Merz, G. E.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 43
The Brucella abortus Cu,Zn Superoxide Dismutase Is Required for Optimal Resistance to Oxidative Killing by Murine Macrophages and Wild-Type Virulence in Experimentally Infected Mice
journal, April 2005
- Gee, J. M.; Valderas, M. W.; Kovach, M. E.
- Infection and Immunity, Vol. 73, Issue 5
A prokaryotic superoxide dismutase paralog lacking two Cu ligands: From largely unstructured in solution to ordered in the crystal
journal, May 2005
- Banci, L.; Bertini, I.; Calderone, V.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 21
Robust, high-throughput solution structural analyses by small angle X-ray scattering (SAXS)
journal, July 2009
- Hura, Greg L.; Menon, Angeli L.; Hammel, Michal
- Nature Methods, Vol. 6, Issue 8
Selenocysteine's mechanism of incorporation and evolution revealed in cDNAs of three glutathione peroxidases
journal, January 1988
- Mullenbach, Guy T.; Tabrizi, Azita; Irvine, Bruce D.
- "Protein Engineering, Design and Selection", Vol. 2, Issue 3
X-ray Absorption Investigation of a Unique Protein Domain Able To Bind both Copper(I) and Copper(II) at Adjacent Sites of the N-Terminus of Haemophilus ducreyi Cu,Zn Superoxide Dismutase †
journal, October 2005
- D'Angelo, Paola; Pacello, Francesca; Mancini, Giordano
- Biochemistry, Vol. 44, Issue 39
Periplasmic Superoxide Dismutase in Meningococcal Pathogenicity
journal, January 1998
- Wilks, Kathryn E.; Dunn, Kate L. R.; Farrant, Jayne L.
- Infection and Immunity, Vol. 66, Issue 1
Unusual Trigonal-Planar Copper Configuration Revealed in the Atomic Structure of Yeast Copper−Zinc Superoxide Dismutase † , ‡
journal, January 1996
- Ogihara, Nancy L.; Parge, Hans E.; Hart, P. John
- Biochemistry, Vol. 35, Issue 7
Meningococcal carriage and disease—Population biology and evolution
journal, June 2009
- Caugant, Dominique A.; Maiden, Martin C. J.
- Vaccine, Vol. 27
The Chemistry and Mechanism of Antibody Binding to Protein Antigens
book, January 1988
- Getzoff, Elizabeth D.; Tainer, John A.; Lerner, Richard A.
- Advances in Immunology
Cloning and analysis of sodC, encoding the copper-zinc superoxide dismutase of Escherichia coli.
journal, May 1996
- Imlay, K. R.; Imlay, J. A.
- Journal of Bacteriology, Vol. 178, Issue 9
Progress in Brucella vaccine development
journal, March 2012
- Yang, Xinghong; Skyberg, Jerod A.; Cao, Ling
- Frontiers in Biology, Vol. 8, Issue 1
Modulation of immune responses in Balb/c mice vaccinated with Brucella abortus CuZn superoxide dismutase synthetic peptide vaccine
journal, January 1994
- Tabatabai, Louisa B.; Pugh, George W.
- Vaccine, Vol. 12, Issue 10
GNOM – a program package for small-angle scattering data processing
journal, October 1991
- Semenyuk, A. V.; Svergun, D. I.
- Journal of Applied Crystallography, Vol. 24, Issue 5
Use of S -[2,3-Bispalmitoyiloxy-(2 R )-Propyl]- R -Cysteinyl-Amido-Monomethoxy Polyethylene Glycol as an Adjuvant Improved Protective Immunity Associated with a DNA Vaccine Encoding Cu,Zn Superoxide Dismutase of Brucella abortus in Mice
journal, August 2014
- Retamal-Díaz, Angello; Riquelme-Neira, Roberto; Sáez, Darwin
- Clinical and Vaccine Immunology, Vol. 21, Issue 11
Towards a Brucella vaccine for humans
journal, May 2010
- Perkins, Stuart D.; Smither, Sophie J.; Atkins, Helen S.
- FEMS Microbiology Reviews, Vol. 34, Issue 3
Implementation and performance of SIBYLS: a dual endstation small-angle X-ray scattering and macromolecular crystallography beamline at the Advanced Light Source
journal, January 2013
- Classen, Scott; Hura, Greg L.; Holton, James M.
- Journal of Applied Crystallography, Vol. 46, Issue 1
Antimicrobial Resistance and Virulence: a Successful or Deleterious Association in the Bacterial World?
journal, April 2013
- Beceiro, A.; Tomas, M.; Bou, G.
- Clinical Microbiology Reviews, Vol. 26, Issue 2
A Novel Heme Protein, the Cu,Zn-Superoxide Dismutase from Haemophilus ducreyi
journal, May 2001
- Pacello, Francesca; Langford, Paul R.; Kroll, J. Simon
- Journal of Biological Chemistry, Vol. 276, Issue 32
Cu, Zn superoxide dismutase structure from a microbial pathogen establishes a class with a conserved dimer interface 1 1Edited by D. C. Rees
journal, February 2000
- Forest, Katrina T.; Langford, Paul R.; Kroll, J. Simon
- Journal of Molecular Biology, Vol. 296, Issue 1
Bacterial manipulation of innate immunity to promote infection
journal, February 2010
- Diacovich, Lautaro; Gorvel, Jean-Pierre
- Nature Reviews Microbiology, Vol. 8, Issue 2
ALS Mutants of Human Superoxide Dismutase Form Fibrous Aggregates Via Framework Destabilization
journal, September 2003
- DiDonato, Michael; Craig, Lisa; Huff, Mary E.
- Journal of Molecular Biology, Vol. 332, Issue 3
Advances in treatment of bacterial meningitis
journal, November 2012
- van de Beek, Diederik; Brouwer, Matthijs C.; Thwaites, Guy E.
- The Lancet, Vol. 380, Issue 9854
Human copper-zinc superoxide dismutase complements superoxide dismutase-deficient Escherichia coli mutants.
journal, October 1987
- Natvig, D. O.; Imlay, K.; Touati, D.
- Journal of Biological Chemistry, Vol. 262, Issue 30
FoXS: a web server for rapid computation and fitting of SAXS profiles
journal, May 2010
- Schneidman-Duhovny, D.; Hammel, M.; Sali, A.
- Nucleic Acids Research, Vol. 38, Issue Web Server
Functional and crystallographic characterization of Salmonella typhimurium Cu,Zn superoxide dismutase coded by the sodCI virulence gene 1 1Edited by R. Huber
journal, September 2000
- Pesce, Alessandra; Battistoni, Andrea; Stroppolo, Maria Elena
- Journal of Molecular Biology, Vol. 302, Issue 2
Electrostatic recognition between superoxide and copper, zinc superoxide dismutase
journal, November 1983
- Getzoff, Elizabeth D.; Tainer, John A.; Weiner, Paul K.
- Nature, Vol. 306, Issue 5940
Comprehensive macromolecular conformations mapped by quantitative SAXS analyses
journal, April 2013
- Hura, Greg L.; Budworth, Helen; Dyer, Kevin N.
- Nature Methods, Vol. 10, Issue 6
Virulent Salmonella typhimurium has two periplasmic Cu, Zn-superoxide dismutases
journal, June 1999
- Fang, F. C.; DeGroote, M. A.; Foster, J. W.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 13
Bacterial [Cu,Zn]-superoxide dismutase: phylogenetically distinct from the eukaryotic enzyme, and not so rare after all!
journal, September 1995
- Kroll, J. S.; Langford, P. R.; Wilks, K. E.
- Microbiology, Vol. 141, Issue 9
Adverse events in humans associated with accidental exposure to the livestock brucellosis vaccine RB51
journal, September 2004
- Ashford, David A.; di Pietra, Jennifer; Lingappa, Jairam
- Vaccine, Vol. 22, Issue 25-26
In vivo copper-mediated free radical production: an ESR spin-trapping study
journal, April 2002
- Kadiiska, Maria B.; Mason, Ronald P.
- Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, Vol. 58, Issue 6
Either periplasmic tethering or protease resistance is sufficient to allow a SodC to protect Salmonella enterica serovar Typhimurium from phagocytic superoxide: A tethered SodCII functions in the phagosome
journal, October 2011
- Rushing, Marcus D.; Slauch, James M.
- Molecular Microbiology, Vol. 82, Issue 4
Structural Basis of Heme Binding in the Cu,Zn Superoxide Dismutase from Haemophilus ducreyi
journal, February 2009
- Törő, Imre; Petrutz, Cristiana; Pacello, Francesca
- Journal of Molecular Biology, Vol. 386, Issue 2
XtalView/Xfit—A Versatile Program for Manipulating Atomic Coordinates and Electron Density
journal, April 1999
- McRee, Duncan E.
- Journal of Structural Biology, Vol. 125, Issue 2-3
Construction of Cu-Zn superoxide dismutase deletion mutants of Brucella abortus: analysis of survival in vitro in epithelial and phagocytic cells and in vivo in mice.
journal, January 1992
- Tatum, F. M.; Detilleux, P. G.; Sacks, J. M.
- Infection and Immunity, Vol. 60, Issue 7
Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase
journal, December 1997
- De Groote, M. A.; Ochsner, U. A.; Shiloh, M. U.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 25
Unique structural features of the monomeric Cu,Zn superoxide dismutase from Escherichia coli, revealed by X-ray crystallography
journal, December 1997
- Pesce, Alessandra; Capasso, Clemente; Battistoni, Andrea
- Journal of Molecular Biology, Vol. 274, Issue 3
Direct Oxidation of the [2Fe-2S] Cluster in SoxR Protein by Superoxide: DISTINCT DIFFERENTIAL SENSITIVITY TO SUPEROXIDE-MEDIATED SIGNAL TRANSDUCTION
journal, August 2012
- Fujikawa, Mayu; Kobayashi, Kazuo; Kozawa, Takahiro
- Journal of Biological Chemistry, Vol. 287, Issue 42
Conserved Enzyme-Substrate Electrostatic Attraction in Prokaryotic Cu,Zn Superoxide Dismutases
journal, March 1998
- Folcarelli, Silvia; Battistoni, Andrea; Falconi, Mattia
- Biochemical and Biophysical Research Communications, Vol. 244, Issue 3
Characterizing flexible and intrinsically unstructured biological macromolecules by SAS using the Porod-Debye law
journal, April 2011
- Rambo, Robert P.; Tainer, John A.
- Biopolymers, Vol. 95, Issue 8
Carbon monoxide binding to the heme group at the dimeric interface modulates structure and copper accessibility in the Cu,Zn superoxide dismutase from Haemophilus ducreyi : in silico and in vitro evidences
journal, July 2012
- Chillemi, Giovanni; De Santis, Serena; Falconi, Mattia
- Journal of Biomolecular Structure and Dynamics, Vol. 30, Issue 3
The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium
journal, May 2013
- Imlay, James A.
- Nature Reviews Microbiology, Vol. 11, Issue 7
Atomic structures of wild-type and thermostable mutant recombinant human Cu,Zn superoxide dismutase.
journal, July 1992
- Parge, H. E.; Hallewell, R. A.; Tainer, J. A.
- Proceedings of the National Academy of Sciences, Vol. 89, Issue 13
[Cu,Zn]-Superoxide Dismutase Mutants of the Swine Pathogen Actinobacillus pleuropneumoniae Are Unattenuated in Infections of the Natural Host
journal, August 2000
- Sheehan, B. J.; Langford, P. R.; Rycroft, A. N.
- Infection and Immunity, Vol. 68, Issue 8
Phagocytic Superoxide Specifically Damages an Extracytoplasmic Target to Inhibit or Kill Salmonella
journal, March 2009
- Craig, Maureen; Slauch, James M.
- PLoS ONE, Vol. 4, Issue 3
Evolutionary constraints for dimer formation in prokaryotic Cu,Zn superoxide dismutase 1 1Edited by R. Huber
journal, January 1999
- Bordo, Domenico; Matak, Dijana; Djinovic-Carugo, Kristina
- Journal of Molecular Biology, Vol. 285, Issue 1
Reconciling the chemistry and biology of reactive oxygen species
journal, April 2008
- Winterbourn, Christine C.
- Nature Chemical Biology, Vol. 4, Issue 5
Bacterial [Cu,Zn]-Cofactored Superoxide Dismutase Protects Opsonized, Encapsulated Neisseria meningitidis from Phagocytosis by Human Monocytes/Macrophages
journal, March 2003
- Dunn, K. L. R.; Farrant, J. L.; Langford, P. R.
- Infection and Immunity, Vol. 71, Issue 3
Microbial metalloproteomes are largely uncharacterized
journal, July 2010
- Cvetkovic, Aleksandar; Menon, Angeli Lal; Thorgersen, Michael P.
- Nature, Vol. 466, Issue 7307
Neisseria meningitidis factor H-binding protein fHbp: a key virulence factor and vaccine antigen
journal, February 2015
- Seib, Kate L.; Scarselli, Maria; Comanducci, Maurizio
- Expert Review of Vaccines, Vol. 14, Issue 6
Oral immunization of mice with recombinant Lactococcus lactis expressing Cu,Zn superoxide dismutase of Brucella abortus triggers protective immunity
journal, February 2012
- Sáez, Darwin; Fernández, Pablo; Rivera, Alejandra
- Vaccine, Vol. 30, Issue 7
Works referencing / citing this record:
Antibiotic treatment modulates protein components of cytotoxic outer membrane vesicles of multidrug-resistant clinical strain, Acinetobacter baumannii DU202
journal, August 2018
- Yun, Sung Ho; Park, Edmond Changkyun; Lee, Sang-Yeop
- Clinical Proteomics, Vol. 15, Issue 1
Mining of potential drug targets through the identification of essential and analogous enzymes in the genomes of pathogens of Glycine max, Zea mays and Solanum lycopersicum
journal, May 2018
- Silva, Rangeline Azevedo da; Pereira, Leandro de Mattos; Silveira, Melise Chaves
- PLOS ONE, Vol. 13, Issue 5
Immune Response to Mucosal Brucella Infection
journal, August 2019
- López-Santiago, Rubén; Sánchez-Argáez, Ana Beatriz; De Alba-Núñez, Liliana Gabriela
- Frontiers in Immunology, Vol. 10
Antigenicity of Brucella Proteins by the Elisa test
journal, March 2019
- Bulashev, A. K.; Syzdykova, A. S.; Suranshiyev, Zh. A.
- Bulletin of NSAU (Novosibirsk State Agrarian University), Issue 1