Previous Article | Next Article 
Infection and Immunity, April 2005, p. 1971-1977, Vol. 73, No. 4
0019-9567/05/$08.00+0 doi:10.1128/IAI.73.4.1971-1977.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.
Interactions of Neisseria gonorrhoeae with Adherent Polymorphonuclear Leukocytes
Mark P. Simons,1
William M. Nauseef,1,2,3 and
Michael A. Apicella1*
Department of Microbiology, Inflammation Program, and Molecular, Biology Program,1
Department of Medicine, University of Iowa,2
Veterans Affairs Medical Center, Iowa City, Iowa3
Received 29 September 2004/
Returned for modification 10 November 2004/
Accepted 20 December 2004
Neisseria gonorrhoeae causes severe exudative urethritis. The exudates from infected individuals contain large numbers of polymorphonuclear leukocytes (PMN) with ingested gonococci. The fate of N. gonorrhoeae within PMN has been a topic of debate for years. In this study, we examined the interactions of N. gonorrhoeae with PMN adherent to surfaces as a system that better models events during clinical disease. Using chemiluminescence to measure reactive oxygen species (ROS), we found that N. gonorrhoeae stimulated PMN to produce a respiratory burst. Different kinetics were seen when PMN were stimulated with opsonized zymosan particles. In addition, ROS were produced predominantly inside the PMN in response to gonococci. Laser scanning confocal microscopy and transmission electron microscopy showed that N. gonorrhoeae rapidly associated with PMN under these experimental conditions and was internalized. Some gonococci were cleared in the first 30 to 60 min after phagocytosis, but a majority of the population persisted for 6 h after phagocytosis. Quantification of viable organisms showed that a significant portion of the population resisted killing. The viability of this subpopulation remained unchanged for 2 h after phagocytosis. A significant increase of viable gonococci from 1 to 6 h was also observed, suggesting intracellular replication. Four different N. gonorrhoeae strains demonstrated the same capacity to resist PMN-mediated killing, whereas Escherichia coli was rapidly killed by PMN under the same conditions. Taken together, these findings suggest that a subpopulation of N. gonorrhoeae resists killing and replicates within PMN phagosomes in spite of NADPH oxidase activation.
* Corresponding author. Mailing address: Department of Microbiology, 3-403 Bowen Science Building, University of Iowa, 51 Newton Rd., Iowa City, IA 52242. Phone: (319) 335-7807. Fax: (319) 335-9006. E-mail:
michael-apicella{at}uiowa.edu.
Editor: J. N. Weiser
Infection and Immunity, April 2005, p. 1971-1977, Vol. 73, No. 4
0019-9567/05/$08.00+0 doi:10.1128/IAI.73.4.1971-1977.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.
This article has been cited by other articles:
-
Barth, K. R., Isabella, V. M., Wright, L. F., Clark, V. L.
(2009). Resistance to peroxynitrite in Neisseria gonorrhoeae. Microbiology
155: 2532-2545
[Abstract]
[Full Text]
-
Cloud-Hansen, K. A., Hackett, K. T., Garcia, D. L., Dillard, J. P.
(2008). Neisseria gonorrhoeae Uses Two Lytic Transglycosylases To Produce Cytotoxic Peptidoglycan Monomers. J. Bacteriol.
190: 5989-5994
[Abstract]
[Full Text]
-
Simons, M. P., Leidal, K. G., Nauseef, W. M., Griffith, T. S.
(2008). TNF-related apoptosis-inducing ligand (TRAIL) is expressed throughout myeloid development, resulting in a broad distribution among neutrophil granules. J. Leukoc. Biol.
83: 621-629
[Abstract]
[Full Text]
-
Smith, H., Tang, C. M., Exley, R. M.
(2007). Effect of Host Lactate on Gonococci and Meningococci: New Concepts on the Role of Metabolites in Pathogenicity. Infect. Immun.
75: 4190-4198
[Full Text]
-
Nazareth, H., Genagon, S. A., Russo, T. A.
(2007). Extraintestinal Pathogenic Escherichia coli Survives within Neutrophils. Infect. Immun.
75: 2776-2785
[Abstract]
[Full Text]
-
Soler-Garcia, A. A., Jerse, A. E.
(2007). Neisseria gonorrhoeae Catalase Is Not Required for Experimental Genital Tract Infection despite the Induction of a Localized Neutrophil Response. Infect. Immun.
75: 2225-2233
[Abstract]
[Full Text]
-
Stohl, E. A., Seifert, H. S.
(2006). Neisseria gonorrhoeae DNA Recombination and Repair Enzymes Protect against Oxidative Damage Caused by Hydrogen Peroxide. J. Bacteriol.
188: 7645-7651
[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]
-
Lerm, M., Holm, A., Seiron, A., Sarndahl, E., Magnusson, K.-E., Rasmusson, B.
(2006). Leishmania donovani Requires Functional Cdc42 and Rac1 To Prevent Phagosomal Maturation.. Infect. Immun.
74: 2613-2618
[Abstract]
[Full Text]
-
Seib, K. L., Simons, M. P., Wu, H.-J., McEwan, A. G., Nauseef, W. M., Apicella, M. A., Jennings, M. P.
(2005). Investigation of Oxidative Stress Defenses of Neisseria gonorrhoeae by Using a Human Polymorphonuclear Leukocyte Survival Assay. Infect. Immun.
73: 5269-5272
[Abstract]
[Full Text]