This Article Full Text Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Reprints and Permissions Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Wilks, K. E. Articles by Kroll, J. S. Search for Related Content PubMed PubMed Citation Articles by Wilks, K. E. Articles by Kroll, J. S.

 Previous Article  |  Next Article 

Infect. Immun., Jan 1998, 213-217, Vol 66, No. 1
Copyright © 1998, American Society for Microbiology

Periplasmic superoxide dismutase in meningococcal pathogenicity

KE Wilks, KL Dunn, JL Farrant, KM Reddin, AR Gorringe, PR Langford and JS Kroll
Department of Paediatrics, Imperial College, School of Medicine at St. Mary's Hospital, London, United Kingdom.

Meningococcal sodC encodes periplasmic copper- and zinc-cofactored superoxide dismutase (Cu,Zn SOD) which catalyzes the conversion of the superoxide radical anion to hydrogen peroxide, preventing a sequence of reactions leading to production of toxic hydroxyl free radicals. From its periplasmic location, Cu,Zn SOD was inferred to acquire its substrate from outside the bacterial cell and was speculated to play a role in preserving meningococci from the action of microbicidal oxygen free radicals produced in the context of host defense. A sodC mutant was constructed by allelic exchange and was used to investigate the role of Cu,Zn SOD in pathogenicity. Wild-type and mutant meningococci grew at comparable rates and survived equally long in aerobic liquid culture. The mutant showed no increased sensitivity to paraquat, which generates superoxide within the cytosol, but was approximately 1,000- fold more sensitive to the toxicity of superoxide generated in solution by the xanthine/xanthine oxidase system. These data support a role for meningococcal Cu,Zn SOD in protection against exogenous superoxide. In experiments to translate this into a role in pathogenicity, wild-type and mutant organisms were used in an intraperitoneal mouse infection model. The sodC mutant was significantly less virulent. We conclude that periplasmic Cu,Zn SOD contributes to the virulence of Neisseria meningitidis, most likely by reducing the effectiveness of toxic oxygen host defenses.

This article has been cited by other articles:

• Sjolinder, H., Mogensen, T. H., Kilian, M., Jonsson, A.-B., Paludan, S. R. (2008). Important Role for Toll-Like Receptor 9 in Host Defense against Meningococcal Sepsis. Infect. Immun. 76: 5421-5428 [Abstract] [Full Text]  
• Ammendola, S., Pasquali, P., Pacello, F., Rotilio, G., Castor, M., Libby, S. J., Figueroa-Bossi, N., Bossi, L., Fang, F. C., Battistoni, A. (2008). Regulatory and Structural Differences in the Cu,Zn-Superoxide Dismutases of Salmonella enterica and Their Significance for Virulence. J. Biol. Chem. 283: 13688-13699 [Abstract] [Full Text]  
• Balashova, N. V., Park, D. H., Patel, J. K., Figurski, D. H., Kachlany, S. C. (2007). Interaction between Leukotoxin and Cu,Zn Superoxide Dismutase in Aggregatibacter actinomycetemcomitans. Infect. Immun. 75: 4490-4497 [Abstract] [Full Text]  
• Keith, K. E., Valvano, M. A. (2007). Characterization of SodC, a Periplasmic Superoxide Dismutase from Burkholderia cenocepacia. Infect. Immun. 75: 2451-2460 [Abstract] [Full Text]  
• Fung, W. W. M., O'Dwyer, C. A., Sinha, S., Brauer, A. L., Murphy, T. F., Kroll, J. S., Langford, P. R. (2006). 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. J. Clin. Microbiol. 44: 4222-4226 [Abstract] [Full Text]  
• Seib, K. L., Wu, H.-J., Kidd, S. P., Apicella, M. A., Jennings, M. P., McEwan, A. G. (2006). Defenses against Oxidative Stress in Neisseria gonorrhoeae: a System Tailored for a Challenging Environment. Microbiol. Mol. Biol. Rev. 70: 344-361 [Abstract] [Full Text]  
• Wu, H.-J., Seib, K. L., Edwards, J. L., Apicella, M. A., McEwan, A. G., Jennings, M. P. (2005). Azurin of Pathogenic Neisseria spp. Is Involved in Defense against Hydrogen Peroxide and Survival within Cervical Epithelial Cells. Infect. Immun. 73: 8444-8448 [Abstract] [Full Text]  
• Newcombe, J., Eales-Reynolds, L.-J., Wootton, L., Gorringe, A. R., Funnell, S. G. P., Taylor, S. C., McFadden, J. J. (2004). Infection with an Avirulent phoP Mutant of Neisseria meningitidis Confers Broad Cross-Reactive Immunity. Infect. Immun. 72: 338-344 [Abstract] [Full Text]  
• Plewes, K. A., Barr, S. D., Gedamu, L. (2003). Iron Superoxide Dismutases Targeted to the Glycosomes of Leishmania chagasi Are Important for Survival. Infect. Immun. 71: 5910-5920 [Abstract] [Full Text]  
• Dunn, K. L. R., Farrant, J. L., Langford, P. R., Kroll, J. S. (2003). Bacterial [Cu,Zn]-Cofactored Superoxide Dismutase Protects Opsonized, Encapsulated Neisseria meningitidis from Phagocytosis by Human Monocytes/Macrophages. Infect. Immun. 71: 1604-1607 [Abstract] [Full Text]  
• Tseng, H.-J., McEwan, A. G., Apicella, M. A., Jennings, M. P. (2003). OxyR Acts as a Repressor of Catalase Expression in Neisseria gonorrhoeae. Infect. Immun. 71: 550-556 [Abstract] [Full Text]  
• Hwang, C.-S., Rhie, G.-e., Oh, J.-H., Huh, W.-K., Yim, H.-S., Kang, S.-O. (2002). Copper- and zinc-containing superoxide dismutase (Cu/ZnSOD) is required for the protection of Candida albicans against oxidative stresses and the expression of its full virulence. Microbiology 148: 3705-3713 [Abstract] [Full Text]  
• Skaar, E. P., Tobiason, D. M., Quick, J., Judd, R. C., Weissbach, H., Etienne, F., Brot, N., Seifert, H. S. (2002). The outer membrane localization of the Neisseria gonorrhoeae MsrA/B is involved in survival against reactive oxygen species. Proc. Natl. Acad. Sci. USA 99: 10108-10113 [Abstract] [Full Text]  
• Bong, C. T. H., Fortney, K. R., Katz, B. P., Hood, A. F., Mateo, L. R. S., Kawula, T. H., Spinola, S. M. (2002). A Superoxide Dismutase C Mutant of Haemophilus ducreyi Is Virulent in Human Volunteers. Infect. Immun. 70: 1367-1371 [Abstract] [Full Text]  
• Sansone, A., Watson, P. R., Wallis, T. S., Langford, P. R., Kroll, J. S. (2002). The role of two periplasmic copper- and zinc-cofactored superoxide dismutases in the virulence of Salmonella choleraesuis. Microbiology 148: 719-726 [Abstract] [Full Text]  
• Langford, P. R., Sheehan, B. J., Shaikh, T., Kroll, J. S. (2002). Active Copper- and Zinc-Containing Superoxide Dismutase in the Cryptic Genospecies of Haemophilus Causing Urogenital and Neonatal Infections Discriminates Them from Haemophilus influenzae Sensu Stricto. J. Clin. Microbiol. 40: 268-270 [Abstract] [Full Text]  
• Tullius, M. V., Harth, G., Horwitz, M. A. (2001). High Extracellular Levels of Mycobacterium tuberculosis Glutamine Synthetase and Superoxide Dismutase in Actively Growing Cultures Are Due to High Expression and Extracellular Stability Rather than to a Protein-Specific Export Mechanism. Infect. Immun. 69: 6348-6363 [Abstract] [Full Text]  
• Piddington, D. L., Fang, F. C., Laessig, T., Cooper, A. M., Orme, I. M., Buchmeier, N. A. (2001). Cu,Zn Superoxide Dismutase of Mycobacterium tuberculosis Contributes to Survival in Activated Macrophages That Are Generating an Oxidative Burst. Infect. Immun. 69: 4980-4987 [Abstract] [Full Text]  
• Poyart, C., Pellegrini, E., Gaillot, O., Boumaila, C., Baptista, M., Trieu-Cuot, P. (2001). Contribution of Mn-Cofactored Superoxide Dismutase (SodA) to the Virulence of Streptococcus agalactiae. Infect. Immun. 69: 5098-5106 [Abstract] [Full Text]  
• West, D., Reddin, K., Matheson, M., Heath, R., Funnell, S., Hudson, M., Robinson, A., Gorringe, A. (2001). Recombinant Neisseria meningitidis Transferrin Binding Protein A Protects against Experimental Meningococcal Infection. Infect. Immun. 69: 1561-1567 [Abstract] [Full Text]  
• Dussurget, O., Stewart, G., Neyrolles, O., Pescher, P., Young, D., Marchal, G. (2001). Role of Mycobacterium tuberculosis Copper-Zinc Superoxide Dismutase. Infect. Immun. 69: 529-533 [Abstract] [Full Text]  
• Lefebre, M. D., Valvano, M. A. (2001). In vitro resistance of Burkholderia cepacia complex isolates to reactive oxygen species in relation to catalase and superoxide dismutase production. Microbiology 147: 97-109 [Abstract] [Full Text]  
• Bandyopadhyay, P., Steinman, H. M. (2000). Catalase-Peroxidases of Legionella pneumophila: Cloning of the katA Gene and Studies of KatA Function. J. Bacteriol. 182: 6679-6686 [Abstract] [Full Text]  
• Sheehan, B. J., Langford, P. R., Rycroft, A. N., Kroll, J. S. (2000). [Cu,Zn]-Superoxide Dismutase Mutants of the Swine Pathogen Actinobacillus pleuropneumoniae Are Unattenuated in Infections of the Natural Host. Infect. Immun. 68: 4778-4781 [Abstract] [Full Text]  
• Yesilkaya, H., Kadioglu, A., Gingles, N., Alexander, J. E., Mitchell, T. J., Andrew, P. W. (2000). Role of Manganese-Containing Superoxide Dismutase in Oxidative Stress and Virulence of Streptococcus pneumoniae. Infect. Immun. 68: 2819-2826 [Abstract] [Full Text]  
• Battistoni, A., Pacello, F., Folcarelli, S., Ajello, M., Donnarumma, G., Greco, R., Grazia Ammendolia, M., Touati, D., Rotilio, G., Valenti, P. (2000). Increased Expression of Periplasmic Cu,Zn Superoxide Dismutase Enhances Survival of Escherichia coli Invasive Strains within Nonphagocytic Cells. Infect. Immun. 68: 30-37 [Abstract] [Full Text]  
• Ha, U., Jin, S. (1999). Expression of the soxR Gene of Pseudomonas aeruginosa Is Inducible during Infection of Burn Wounds in Mice and Is Required To Cause Efficient Bacteremia. Infect. Immun. 67: 5324-5331 [Abstract] [Full Text]  
• Clements, M. O., Watson, S. P., Foster, S. J. (1999). Characterization of the Major Superoxide Dismutase of Staphylococcus aureus and Its Role in Starvation Survival, Stress Resistance, and Pathogenicity. J. Bacteriol. 181: 3898-3903 [Abstract] [Full Text]  
• Fang, F. C., DeGroote, M. A., Foster, J. W., Baumler, A. J., Ochsner, U., Testerman, T., Bearson, S., Giard, J.-C., Xu, Y., Campbell, G., Laessig, T. (1999). Virulent Salmonella typhimurium has two periplasmic Cu, Zn-superoxide dismutases. Proc. Natl. Acad. Sci. USA 96: 7502-7507 [Abstract] [Full Text]  
• Kroll, J. S., Wilks, K. E., Farrant, J. L., Langford, P. R. (1998). Natural genetic exchange between Haemophilus and Neisseria: Intergeneric transfer of chromosomal genes between major human pathogens. Proc. Natl. Acad. Sci. USA 95: 12381-12385 [Abstract] [Full Text]  
• Pacello, F., Langford, P. R., Kroll, J. S., Indiani, C., Smulevich, G., Desideri, A., Rotilio, G., Battistoni, A. (2001). A Novel Heme Protein, the Cu,Zn-Superoxide Dismutase from Haemophilus ducreyi. J. Biol. Chem. 276: 30326-30334 [Abstract] [Full Text]  
• Battistoni, A., Pacello, F., Mazzetti, A. P., Capo, C., Kroll, J. S., Langford, P. R., Sansone, A., Donnarumma, G., Valenti, P., Rotilio, G. (2001). A Histidine-rich Metal Binding Domain at the N Terminus of Cu,Zn-Superoxide Dismutases from Pathogenic Bacteria. A NOVEL STRATEGY FOR METAL CHAPERONING. J. Biol. Chem. 276: 30315-30325 [Abstract] [Full Text]