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7 - N. gonorrhoeae: The varying mechanism of pathogenesis in males and females

Published online by Cambridge University Press:  21 August 2009

Jennifer L. Edwards
Affiliation:
Department of Microbiology, The University of Iowa, Iowa City, Iowa 52242, USA
Hillery A. Harvey
Affiliation:
Department of Microbiology, The University of Iowa, Iowa City, Iowa 52242, USA
Michael A. Apicella
Affiliation:
Department of Microbiology, The University of Iowa, Iowa City, Iowa 52242, USA
Richard J. Lamont
Affiliation:
University of Florida
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Summary

Neisseria gonorrhoeae, the gonococcus, is the causative agent of gonorrhea, one of the oldest human diseases on record. Biblical references to gonorrhea in Leviticus (15:1–15:19) showed that the infectious nature of the disease was recognized even at that time. Probably, the best description of gonorrhea in a man in the preantibiotic era can be found in the writings of Boswell, who described in detail each of his 19 episodes of infection (Ober, 1970). These descriptions also allude to the asymptomatic nature of the disease in women, as many of the contacts from whom he acquired the infection were without symptoms of disease. Today, it is estimated that greater than 1 million cases of N. gonorrhoeae infection occur in the United States, and 60 million cases are reported annually worldwide. Hence, N. gonorrhoeae infection remains prevalent in the general population, despite the fact that antibiotic therapy is readily available. The high incidence of this disease remains a major concern in lower socioeconomic groups in the United States; however, the highest incidence of infection and of complications resulting from infection occur in developing countries. In underdeveloped nations it has been shown that patients with gonorrhea are at much higher risk for contracting human immunodeficiency virus (HIV). It is proposed that this increased susceptibility to HIV infection results from the inflammatory response generated by infecting gonococci with the subsequent disruption and shedding of the mucosal epithelium.

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Publisher: Cambridge University Press
Print publication year: 2004

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References

Apicella, M. A., Ketterer, M., Lee, F. K. N., Zhou, D., Rice, P. A., and Blake, M. S. (1996). The pathogenesis of gonococcal urethritis in men: confocal and immunoelectron microscopic analysis of urethral exudates from men infected with Neisseria gonorrhoeae. J. Infect. Dis. 173, 636–646CrossRefGoogle ScholarPubMed
Apicella, M.., Mandrell, R. E., Shero, M., Wilson, M. E., Griffiss, J. M., Brooks, G. F., Lammel, C., Breen, J. F., and Rice, P. A. (1990). Modification by sialic acid of Neisseria gonorrhoeae lipooligosaccharide epitope expression in human urethral exudates: an immunoelectron microscopic analysis. J. Infect. Dis. 162, 506–512CrossRefGoogle ScholarPubMed
Aral, S. O., Mosher, W. D., and Cates, W. (1991). Self-reported pelvic inflammatory disease in the United States. JAMA 266,, 2570–2573CrossRefGoogle Scholar
Bjerknes, R., Guttormsen, H.-K., Solberg, C. O., and Wetzler, L. M. (1995). Neisserial porins inhibit human neutrophil actin polymerization, degranulation, opsonin receptor expression, and phagocytosis but prime the neutrophils to increase their oxidative burst. Infect. Immun. 63, 160–167Google ScholarPubMed
Bolan, G., Ehrhardt, A. A., and Wasserheit, J. N. (1999). Gender perspectives and STDs. In Sexually Transmitted Diseases, ed. K. K. Holmes, P.-A. Mardh, P. F. Sparling, S. M. Lemon, W. E. Stamm, P. Piot, and J. N. Wasserheit, 3rd ed., pp. 117–127. New York: McGraw-Hill
Campagnari, A. A., Spinola, S. M., Lesse, A. J., Kwaik, Y. A., Mandrell, R. E., and Apicella, M. A. (1990). Lipooligosaccharide epitopes shared among gram-negative non-enteric mucosal pathogens. Microb. Pathog. 8, 353–362CrossRefGoogle ScholarPubMed
Chen, C. J., Thomas, C. E., McLean, D. S., Rouquette-Loughlin, C., Shafer, W. M., and Sparling, P. F. (2002). PilQ point mutation results in hemoglobin utilization in the absence of HpuA/B. In Abstracts of the 13th International Pathogenic Neisseria Conference, ed. D. A. Caugant and E. Wedege, p. 103. Oslo: Nordberg Aksidenstrykkeri AS
Chen, T. C., Swanson, J., Wilson, J., and Belland, R. J. (1995). Heparin protects Opa+Neisseria gonorrhoeae from the bactericidal action of normal human serum. Infect. Immun. 63, 1790–1795Google ScholarPubMed
Clark, V. L., Campbell, L. A., Palermo, D. A., Evans, T. M., and Klimpel, K. W. (1987). Induction and repression of outer membrane proteins by anaerobic growth of Neisseria gonorrhoeae. Infect. Immun. 55, 1359–1364Google ScholarPubMed
Cooke, S. J., Jolley, K., Ison, C. A., Young, H., and Heckels, J. E. (1998). Naturally occurring isolates of Neisseria gonorrhoeae, which display anomalous serovar properties, express PIA/PIB hybrid porins, deletions in PIB or novel PIA molecules. FEMS Microbiol. Lett. 162, 75–82CrossRefGoogle ScholarPubMed
Cornelissen, C. N., Kelley, M., Hobbs, M. M., Anderson, J. E., Cannon, J. G., Cohen, M. S., and Sparling, P. F. (1998). The transferrin receptor expressed by gonococcal strain FA1090 is required for experimental infection of human male volunteers. Mol. Microbiol. 27, 611–616CrossRefGoogle ScholarPubMed
Dehio, C., Gray-Owen, S. D., and Meyer, T. F. (2000). Host cell invasion by pathogenic Neisseriae. In Subcellular Biochemistry, Vol. 33: Bacterial Invasion into Eukaryotic Cells, ed. T. A. Oelschlaeger and J. Hacker, pp. 61–96. New York: PlenumCrossRef
Densen, P., MacKeen, L. A., and Clark, R. A. (1982). Dissemination of gonococcal infection is associated with delayed stimulation of complement-dependent neutrophil chemotaxis in vitro. Infect. Immun. 38, 563–572Google ScholarPubMed
Dilworth, J. A., Hendley, J. O., and Mandell, G. L. (1975). Attachment and ingestion of gonococci by human neutrophils. Infect. Immun. 11, 512–516Google ScholarPubMed
Edwards, J. L. and Apicella, M. A. (2002). The role of lipooligosaccharide in Neisseria gonorrhoeae pathogenesis of cervical epithelia: lipid A serves as a C3 acceptor molecule. Cell. Microbiol. 4, 585–598CrossRefGoogle ScholarPubMed
Edwards, J. L., Brown, E. J., Ault, K. A., and Apicella, M. A. (2001). The role of complement receptor 3 (CR3) in Neisseria gonorrhoeae infection of human cervical epithelia. Cell. Microbiol. 3, 611–622CrossRefGoogle ScholarPubMed
Edwards, J. L., Brown, E. J., Uk-Nham, S., Cannon, J. G., Blake, M. S., and Apicella, M. A. (2002). A co-operative interaction between Neisseria gonorrhoeae and complement receptor 3 mediates infection of primary cervical epithelial cells. Cell. Microbiol. 4, 571–584CrossRefGoogle ScholarPubMed
Edwards, J. L., Shao, J. Q., Ault, K. A., and Apicella, M. A. (2000). Neisseria gonorrhoeae elicits membrane ruffling and cytoskeletal rearrangements upon infection of primary human endocervical and ectocervical cells. Infect. Immun. 68, 5354–5363CrossRefGoogle ScholarPubMed
Estabrook, M. M., Griffiss, J. M., and Jarvis, G. A. (1997). Sialylation of Neisseria meningitidis lipooligosaccharide inhibits serum bactericidal activity by masking lacto-N-neotetraose. Infect. Immun. 65, 4436–4444Google ScholarPubMed
Evans, B. A. (1977). Ultrastructure study of cervical gonorrhea. J. Infect. Dis. 136, 248–255CrossRefGoogle ScholarPubMed
Farrell, C. F. and Rest, R. F. (1990). Up-regulation of human neutrophil receptors for Neisseria gonorrhoeae expressing PII outer membrane proteins. Infect Immun. 58, 2777–2784Google ScholarPubMed
Forest, K. T., Dunham, S. A., Koomey, M., and Tainer, J. A. (1999). Crystallographic structure reveals phosphorylated pilin from Neisseria: phosphoserine sites modify type IV pilus surface chemistry and fiber morphology. Mol. Microbiol. 31, 743–752CrossRefGoogle Scholar
Forest, K. T. and Tainer, J. A. (1997). Type-4 pilus-structure: outside to inside and top to bottom – a minireview. Gene 192, 165–169CrossRefGoogle Scholar
Giardina, P. C., Williams, R., Lubaroff, D., and Apicella, M. A. (1998). Neisseria gonorrhoeae induces focal polymerization of actin in primary human urethral epithelium. Infect. Immun. 66, 3416–3419Google ScholarPubMed
Gorby, G. L., Clemens, C. M., Barley, L. R., and McGee, Z. A. (1991). Effect of human chorionic gonadotropin (hCG) on Neisseria gonorrhoeae invasion of and IgA secretion by human fallopian tube mucosa. Microb. Pathogen. 10, 373–384CrossRefGoogle ScholarPubMed
Haines, K. A., Reibman, J., Tang, X., Blake, M. S., and Weissmann, G. (1991). Effects of protein I of Neisseria gonorrhoeae on neutrophil activation: generation of diacylglycerol from phosphatidylcholine via a specific phospholipase C is associated with exocytosis. J. Cell Biol. 114, 433–442CrossRefGoogle Scholar
Haines, K. A., Yeh, L., Blake, M. S., Cristello, P., Korchak, H., and Weissmann, G. (1988). Protein I, a translocatable ion channel from Neisseria gonorrhoeae, selectively inhibits exocytosis from human neutrophils without inhibiting O2– generation. J. Biol. Chem. 263, 945–951Google ScholarPubMed
Harvey, H. A., Jennings, M. P., Campbell, C. A., Williams, R., and Apicella, M. A. (2001). Receptor-mediated endocytosis of Neisseria gonorrhoeae into primary human urethral epithelial cells: the role of the asialoglycoprotein receptor. Mol. Microbiol. 42, 659–672CrossRefGoogle ScholarPubMed
Harvey, H. A., Porat, N., Campbell, C. A., Jennings, M. P., Gibson, B. W., Phillips, N. J., Apicella, M. A., and Blake, M. S. (2000). Gonococcal lipooligosaccharide is a ligand for the asialoglycoprotein receptor on human sperm. Mol. Microbiol. 36, 1059–1070CrossRefGoogle ScholarPubMed
Harvey, H. A., Ketterer, M. R., Preston, A., Lubaroff, D., Williams, R., and Apicella, M. A. (1997). Ultrastructure analysis of primary human urethral epithelial cell cultures infected with Neisseria gonorrhoeae. Infect. Immun. 65, 2420–2427Google ScholarPubMed
Hedges, S. R., Sibley, D. A., Mayo, M. S., Hook, E. W. III, and Russell, M. W. (1998). Cytokine and antibody responses in women infected with Neisseria gonorrhoeae: effects of concomitant infections. J. Infect. Dis. 178, 742–751CrossRefGoogle ScholarPubMed
Householder, T. C., Belli, W. A., Lissenden, S., Cole, J. A., and Clark, V. L. (1999). cis- and trans-acting elements involved in regulation of aniA, the gene encoding the major anaerobically induced outer membrane protein in Neisseria gonorrhoeae. J. Bacteriol. 181, 541–551Google ScholarPubMed
Jarvis, G. A. (1995). Recognition and control of neisserial infection by antibody and complement. Trends Microbiol. 3, 198–201CrossRefGoogle ScholarPubMed
Jones, S. L., Knaus, U. G., Bokoch, G. M., and Brown, E. J. (1998). Two signaling mechanisms for activation of αMβ2 avidity in polymorphonuclear neutrophils. J. Biol. Chem. 273, 10,556–10,566CrossRefGoogle Scholar
Källström, H., Islam, Md.S., Berggren, P.-O., and Jonsson, A.-B. (1998). Cell signaling by the type IV pili of pathogenic Neisseria. J. Biol. Chem. 273, 21,777–21,782CrossRefGoogle ScholarPubMed
Källström, H., Liszewski, M. K., Atkinson, J. P., and Jonsson, A.-B. (1997). Membrane cofactor protein (MCP or CD46) is a cellular pilus receptor for pathogenic Neisseria. Mol. Microbiol. 25, 639–647CrossRefGoogle ScholarPubMed
Lemon, S. M. and Sparling, P. F. (1999). Pathogenesis of sexually transmitted viral and bacterial infections. In Sexually Transmitted Diseases, ed. K. K. Holmes, P.-A. Mardh, P. F. Sparling, S. M. Lemon, W. E. Stamm, P. Piot, and J. N. Wasserheit, pp. 433–449. New York: McGraw-Hill.
Mandrell, R. E. and Apicella, M. A. (1993). Lipo-oligosaccharides (LOS) of mucosal pathogens: molecular mimicry and host-modification of LOS. Immunobiology 187, 382–402CrossRefGoogle ScholarPubMed
Marceau, M., Forest, K., Béretti, J.-L., Tainer, J., and Nassif, X. (1998). Consequences of the loss of O-linked glycosylation of meningococcal type IV pilin on piliation and pilus-mediated adhesion. Mol. Microbiol. 27, 705–715CrossRefGoogle ScholarPubMed
McGee, Z. A., Johnson, A. P., and Taylor-Robinson, D. (1981). Pathogenic mechanisms of Neisseria gonorrhoeae: observations on damage to human fallopian tubes in organ culture by gonococci of colony type 1 or type 4. J. Infect. Dis. 143, 413–422CrossRefGoogle ScholarPubMed
Ober, W. B. (1970). Boswell's clap. JAMA 212, 91–95CrossRefGoogle ScholarPubMed
Parge, H. E., Forest, K. T., Hickey, M. J., Christensen, D., Getzoff, E. D., and Tainer, J. A. (1995). Structure of the fibre-forming protein pilin at 2.6 A resolution. Nature 378, 32–38CrossRefGoogle ScholarPubMed
Putten, J. P. M., Duensing, T. D., and Carlson, J. (1998). Gonococcal invasion of epithelial cells driven by P.IA, a bacterial ion channel with GTP binding properties. J. Exp. Med. 188, 941–952CrossRefGoogle ScholarPubMed
Putten, J. P. M., Duensing, T. D., and Cole, R. L. (1998). Entry of Opa+ gonococci into Hep-2 cells requires concerted action of glycosaminoglycans, fibronectin and integrin receptors. Mol. Microbiol. 29, 369–379CrossRefGoogle ScholarPubMed
Putten, J. P. M. and Robertson, B. D. (1995). Molecular mechanisms and implications for infection of lipopolysaccharide variation in Neisseria. Mol. Microbiol. 16, 847–853CrossRefGoogle ScholarPubMed
Rahman, M., Källström, H., Normark, S., and Jonsson, A.-B. (1997). PilC of pathogenic Neisseria is associated with the bacterial cell surface. Mol. Microbiol. 25, 11–25CrossRefGoogle ScholarPubMed
Ram, S., Cullinane, M., Blom, A. M., Gulati, S., McQuillen, D. P., Boden, R., Monks, B. G., O'Connell, C., Elkins, C., Pangburn, M. K., Dahlback, B., and Rice, P. A. (2001). C4bp binding to porin mediates stable serum resistance of Neisseria gonorrhoeae. Intl. Immunopharmacol. 1, 423–432CrossRefGoogle ScholarPubMed
Ram, S., McQuillen, D. P., Gulati, S., Elkins, C., Pangburn, M. K., and Rice, P. A. (1998). Binding of complement factor H to loop 5 of porin protein 1A: a molecular mechanism of serum resistance of nonsialylated Neisseria gonorrhoeae. J. Exp. Med. 187, 743–752CrossRefGoogle Scholar
Ram, S., Sharma, A. K., Simpson, S. D., Gulati, S., McQuillen, D. P., Pangburn, M. K., and Rice, P. A. (1998). A novel sialic acid binding site on factor H mediates serum resistance of sialylated Neisseria gonorrhoeae. J. Exp. Med. 187, 743–752CrossRefGoogle ScholarPubMed
Schneider, H., Cross, A. S., Kuschner, R. A., Taylor, D. N., Sandoff, J. C., Boslego, J. W., and Deal, C. D. (1995). Experimental human gonococcal urethritis: 250 Neisseria gonorrhoeae MS11mkC are infective. J. Infect. Dis. 172, 180–185CrossRefGoogle ScholarPubMed
Schneider, H., Schmidt, K. A., Skillman, D. R., Verg, L., Warren, R. L., Wylie, H. J., Sandoff, J. C., Deal, C. D., and Cross, A. S. (1996). Sialylation lessens the infectivity of Neisseria gonorrhoeae MS11mkC. J. Infect. Dis. 173, 1422–1427CrossRefGoogle ScholarPubMed
Schryvers, A. B. and Stojiljkovic, I. (1999). Iron acquisition systems in the pathogenic Neisseria. Mol. Microbiol. 32, 1117–1123CrossRefGoogle ScholarPubMed
Snyder, L. A. S., Butcher, S. A., and Saunders, N. J. (2001). Comparative whole-genome analyses reveal over 100 putative phase variable genes in the pathogenic Neisseria spp. Microbiology 147, 2321–2332CrossRefGoogle ScholarPubMed
Spence, J. M., Chen, J. C.-R., and Clark, V. L. (1997). A proposed role for the lutropin receptor in contact-inducible gonococcal invasion of Hec1B cells. Infect. Immun. 65, 3736–3742Google ScholarPubMed
Stimson, E., Virji, M., Makepeace, K., Dell, A., Morris, H. R., Payne, G., Saunders, J. R., Jennings, M. P., Barker, S., Panico, M., Bcench, I., and Moxon, E. R. (1995). Meningococcal pilin: a glycoprotein substituted with digalaactosyl 2,4-diacetamido-2,4,6-trideoxyhexose. Mol. Microbiol. 17, 1201–1214CrossRefGoogle ScholarPubMed
Sweet, R. L., Blankfort-Doyle, M., Robbie, M. O., and Schacter, J. (1986). The occurrence of chlamydial and gonococcal salpingitis during the menstrual cycle. JAMA 255, 2062–2064CrossRefGoogle ScholarPubMed
Tobiason, D. M. and Seifert, H. S. (2001). Inverse relationship between pilus-mediated gonococcal adherence and surface expression of the pilus receptor, CD46. Microbiology 147, 2333–2340CrossRefGoogle ScholarPubMed
Vogel, U. and Frosch, M. (1999). Mechanisms of neisserial serum resistance. Mol. Microbiol. 32, 1133–1139CrossRefGoogle ScholarPubMed
Weiser, J. N., Goldberg, J. B., Pan, N., Wilson, L., and Virji, M. (1998). The phosphorylcholine epitope undergoes phase variation on a 43-kilodalton protein in Pseudomonas aeruginosa and on pili of Neisseria meningitidis and Neisseria gonorrhoeae. Infect. Immun. 66, 4263–4267Google ScholarPubMed
Wen, K.-K., Giardina, P. C., Blake, M. S., Edwards, J. L., Apicella, M. A., and Rubenstein, P. A. (2000). Interaction of the gonococcal porin P.IB with G-and F-actin. Biochemistry 39, 8638–8647CrossRefGoogle ScholarPubMed
Williams, J. M., Chen, G.-C., Zhu, L., and Rest, R. F. (1998). Using the yeast two-hybrid system to identify human epithelial cell proteins that bind gonococcal Opa proteins: intracellular gonococci bind pyruvate kinase via their Opa proteins and require host pyruvate for growth. Mol. Microbiol. 27, 171–186CrossRefGoogle ScholarPubMed
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