Neisseria gonorrhoeae suppresses the oxidative burst of human polymorphonuclear leukocytes

Cellular Microbiology

Volumn 10, Issue 11, 2008, Pages 2257-2270

  Criss, Alison K ^a,b   Seifert, H Steven ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; OPACITY ASSOCIATED PROTEIN; OPACITY ASSOCIATED PROTEIN B; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIUM CULTURE; CELL VIABILITY; CONTROLLED STUDY; CULTURE MEDIUM; GONORRHEA; HUMAN; HUMAN CELL; INFLAMMATION; MICROBIAL ACTIVITY; NEISSERIA GONORRHOEAE; NEUTROPHIL; NONHUMAN; OPSONIZATION; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RESPIRATORY BURST; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS;

ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; CELLS, CULTURED; GONORRHEA; HUMANS; NEISSERIA GONORRHOEAE; NEUTROPHILS; REACTIVE OXYGEN SPECIES; RESPIRATORY BURST; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); NEISSERIA GONORRHOEAE; STAPHYLOCOCCUS AUREUS;

EID: 54049127365     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2008.01205.x     Document Type: Article

References (80)

1. Allen, L.A., Beecher, B.R., Lynch, J.T., Rohner, O.V., and Wittine, L.M. (2005) Helicobacter pylori disrupts NADPH oxidase targeting in human neutrophils to induce extracellular superoxide release. J Immunol 174: 3658-3667.
2. Archibald, F.S., and Duong, M.N. (1986) Superoxide dismutase and oxygen toxicity defenses in the genus Neisseria. Infect Immun 51: 631-641.
3. Bauer, F.J., Rudel, T., Stein, M., and Meyer, T.F. (1999) Mutagenesis of the Neisseria gonorrhoeae porin reduces invasion in epithelial cells and enhances phagocyte responsiveness. Mol Microbiol 31: 903-913.
4. Belland, R.J., Chen, T., Swanson, J., and Fischer, S.H. (1992) Human neutrophil response to recombinant neisserial Opa proteins. Mol Microbiol 6: 1729-1737.
5. 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: 160-167.
6. Black, W.J., Schwalbe, R.S., Nachamkin, I., and Cannon, J.G. (1984) Characterization of Neisseria gonorrhoeae protein II phase variation by use of monoclonal antibodies. Infect Immun 45: 453-457.
7. Britigan, B.E., Klapper, D., Svendsen, T., and Cohen, M.S. (1988) Phagocyte-derived lactate stimulates oxygen consumption by Neisseria gonorrhoeae. An unrecognized aspect of the oxygen metabolism of phagocytosis. J Clin Invest 81: 318-324.
8. Carlyon, J.A., and Fikrig, E. (2003) Invasion and survival strategies of Anaplasma phagocytophilum. Cell Microbiol 5: 743-754.
9. Carlyon, J.A., Chan, W.T., Galan, J., Roos, D., and Fikrig, E. (2002) Repression of rac2 mRNA expression by Anaplasma phagocytophila is essential to the inhibition of superoxide production and bacterial proliferation. J Immunol 169: 7009-7018.
10. Carlyon, J.A., Abdel-Latif, D., Pypaert, M., Lacy, P., and Fikrig, E. (2004) Anaplasma phagocytophilum utilizes multiple host evasion mechanisms to thwart NADPH oxidase-mediated killing during neutrophil infection. Infect Immun 72: 4772-4783.
11. Chen, C.J., Tobiason, D.M., Thomas, C.E., Shafer, W.M., Seifert, H.S., and Sparling, P.F. (2004) A mutant form of the Neisseria gonorrhoeae pilus secretin protein PilQ allows increased entry of heme and antimicrobial compounds. J Bacteriol 186: 730-739.
12. Chen, T., and Gotschlich, E.C. (1996) CGM1a antigen of neutrophils, a receptor of gonococcal opacity proteins. Proc Natl Acad Sci USA 93: 14851-14856.
13. Crawford, M.A., Aylott, C.V., Bourdeau, R.W., and Bokoch, G.M. (2006) Bacillus anthracis toxins inhibit human neutrophil NADPH oxidase activity. J Immunol 176: 7557-7565.
14. Criss, A.K., and Seifert, H.S. (2006) Gonococci exit apically and basally from polarized epithelial cells and exhibit dynamic changes in type IV pili. Cell Microbiol 8: 1430-1443.
15. Dahlgren, C., and Karlsson, A. (1999) Respiratory burst in human neutrophils. J Immunol Methods 232: 3-14.
16. Dehio, C., Gray-Owen, S.D., and Meyer, T.F. (1998) The role of neisserial Opa proteins in interactions with host cells. Trends Microbiol 6: 489-495.
17. Dillard, J.P., and Seifert, H.S. (2001) A variable genetic island specific for Neisseria gonorrhoeae is involved in providing DNA for natural transformation and is found more often in disseminated infection isolates. Mol Microbiol 41: 263-277.
18. Edwards, J.L., and Apicella, M.A. (2004) The molecular mechanisms used by Neisseria gonorrhoeae to initiate infection differ between men and women. Clin Microbiol Rev 17: 965-981.
19. Edwards, J.L., Entz, D.D., and Apicella, M.A. (2003) Gonococcal phospholipase D modulates the expression and function of complement receptor 3 in primary cervical epithelial cells. Infect Immun 71: 6381-6391.
20. Elkins, C., and Rest, R.F. (1990) Monoclonal antibodies to outer membrane protein PII block interactions of Neisseria gonorrhoeae with human neutrophils. Infect Immun 58: 1078-1084.
21. Elmros, T., Burman, L.G., and Bloom, G.D. (1976) Autolysis of Neisseria gonorrhoeae. J Bacteriol 126: 969-976.
22. Fang, F.C. (2004) Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol 2: 820-832.
23. Fischer, S.H., and Rest, R.F. (1988) Gonococci possessing only certain P.II outer membrane proteins interact with human neutrophils. Infect Immun 56: 1574-1579.
24. Fisette, P.L., Ram, S., Andersen, J.M., Guo, W., and Ingalls, R.R. (2003) The Lip lipoprotein from Neisseria gonorrhoeae stimulates cytokine release and NF-kappaB activation in epithelial cells in a Toll-like receptor 2-dependent manner. J Biol Chem 278: 46252-46260.
25. Frangipane, J.V., and Rest, R.F. (1992) Anaerobic growth of gonococci does not alter their Opa-mediated interactions with human neutrophils. Infect Immun 60: 1793-1799.
26. Fulcher, N.B. (2004) The role of Neisseria Gonorrhoeae opacity proteins in host cell interactions and pathogenesis. Thesis. Chapel Hill, NC: Department of Microbiology and Immunology, University of North Carolina, pp. 1-202.
27. Gallois, A., Klein, J.R., Allen, L.A., Jones, B.D., and Nauseef, W.M. (2001) Salmonella pathogenicity island 2-encoded type III secretion system mediates exclusion of NADPH oxidase assembly from the phagosomal membrane. J Immunol 166: 5741-5748.
28. Gray-Owen, S.D., Lorenzen, D.R., Haude, A., Meyer, T.F., and Dehio, C. (1997) Differential Opa specificities for CD66 receptors influence tissue interactions and cellular response to Neisseria gonorrhoeae. Mol Microbiol 26: 971-980.
29. Hagman, K.E., Pan, W., Spratt, B.G., Balthazar, J.T., Judd, R.C., and Shafer, W.M. (1995) Resistance of Neisseria gonorrhoeae to antimicrobial hydrophobic agents is modulated by the mtrRCDE efflux system. Microbiology 141: 611-622.
30. Hamilton, H.L., Dominguez, N.M., Schwartz, K.J., Hackett, K.T., and Dillard, J.P. (2005) Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Mol Microbiol 55: 1704-1721.
31. Hampton, M.B., Kettle, A.J., and Winterbourn, C.C. (1998) Inside the neutrophil phagosome: Oxidants, myeloperoxidase, and bacterial killing. Blood 92: 3007-3017.
32. Harkness, A.H. (1948) The pathology of gonorrhoea. Br J Vener Dis 24: 137-147.
33. 2-mediated toxicity in Neisseria gonorrhoeae. J Bacteriol 172: 7293-7296.
34. Hebeler, B.H., and Young, F.E. (1975) Autolysis of Neisseria gonorrhoeae. J Bacteriol 122: 385-392.
35. Hook, E.W., and Holmes, K.K. (1985) Gonococcal infections. Ann Intern Med 102: 229-243.
36. James, J.F., and Swanson, J. (1978) Studies on gonococcus infection. XIII. Occurrence of color/opacity colonial variants in clinical cultures. Infect Immun 19: 332-340.
37. Jerse, A.E., Cohen, M.S., Drown, P.M., Whicker, L.G., Isbey, S.F., Seifert, H.S., and Cannon, J.G. (1994) Multiple gonococcal opacity proteins are expressed during experimental urethral infection in the male. J Exp Med 179: 911-920.
38. Jerse, A.E., Sharma, N.D., Simms, A.N., Crow, E.T., Snyder, L.A., and Shafer, W.M. (2003) A gonococcal efflux pump system enhances bacterial survival in a female mouse model of genital tract infection. Infect Immun 71: 5576-5582.
39. Kellogg, D.S., Jr, Peacock, W.L., Deacon, W.E., Brown, L., and Pirkle, C.I. (1963) Neisseria gonorrhoeae. I. Virulence genetically linked to clonal variation. J Bacteriol 85: 1274-1279.
40. Koomey, M., Gotschlich, E.C., Robbins, K., Bergstrom, S., and Swanson, J. (1987) Effects of recA mutations on pilus antigenic variation and phase transitions in Neisseria gonorrhoeae. Genetics 117: 391-398.
41. Le, Y., Murphy, P.M., and Wang, J.M. (2002) Formyl-peptide receptors revisited. Trends Immunol 23: 541-548.
42. Lodge, R., Diallo, T.O., and Descoteaux, A. (2006) Leishmania donovani lipophosphoglycan blocks NADPH oxidase assembly at the phagosome membrane. Cell Microbiol 8: 1922-1931.
43. Long, C.D., Tobiason, D.M., Lazio, M.P., Kline, K.A., and Seifert, H.S. (2003) Low-level pilin expression allows for substantial DNA transformation competence in Neisseria gonorrhoeae. Infect Immun 71: 6279-6291.
44. Lorenzen, D.R., Gunther, D., Pandit, J., Rudel, T., Brandt, E., and Meyer, T.F. (2000) Neisseria gonorrhoeae porin modifies the oxidative burst of human professional phagocytes. Infect Immun 68: 6215-6222.
45. Massari, P., Henneke, P., Ho, Y., Latz, E., Golenbock, D.T., and Wetzler, L.M. (2002) Cutting edge: Immune stimulation by neisserial porins is toll-like receptor 2 and MyD88 dependent. J Immunol 168: 1533-1537.
46. McCaffrey, R.L., and Allen, L.A. (2006) Francisella tularensis LVS evades killing by human neutrophils via inhibition of the respiratory burst and phagosome escape. J Leukoc Biol 80: 1224-1230.
47. Massari, P., Ram, S., Macleod, H., and Wetzler, L.M. (2003) The role of porins in neisserial pathogenesis and immunity. Trends Microbiol 11: 87-93.
48. Mogensen, T.H., Paludan, S.R., Kilian, M., and Ostergaard, L. (2006) Live Streptococcus pneumoniae, Haemophilus influenzae, and Neisseria meningitidis activate the inflammatory response through Toll-like receptors 2, 4, and 9 in species-specific patterns. J Leukoc Biol 80: 267-277.
49. Morse, S.A., and Bartenstein, L. (1980) Purine metabolism in Neisseria gonorrhoeae: The requirement for hypoxanthine. Can J Microbiol 26: 13-20.
50. Mott, J., and Rikihisa, Y. (2000) Human granulocytic ehrlichiosis agent inhibits superoxide anion generation by human neutrophils. Infect Immun 68: 6697-6703.
51. Mott, J., Rikihisa, Y., and Tsunawaki, S. (2002) Effects of Anaplasma phagocytophila on NADPH oxidase components in human neutrophils and HL-60 cells. Infect Immun 70: 1359-1366.
52. Naids, F.L., and Rest, R.F. (1991) Stimulation of human neutrophil oxidative metabolism by nonopsonized Neisseria gonorrhoeae. Infect Immun 59: 4383-4390.
53. Nauseef, W.M., Volpp, B.D., McCormick, S., Leidal, K.G., and Clark, R.A. (1991) Assembly of the neutrophil respiratory burst oxidase. Protein kinase C promotes cytoskeletal and membrane association of cytosolic oxidase components. J Biol Chem 266: 5911-5917.
54. O'Brien, J.P., Goldenberg, D.L., and Rice, P.A. (1983) Disseminated gonococcal infection: A prospective analysis of 49 patients and a review of pathophysiology and immune mechanisms. Medicine 62: 395-406.
55. Qu, X.D., Harwig, S.S., Oren, A.M., Shafer, W.M., and Lehrer, R.I. (1996) Susceptibility of Neisseria gonorrhoeae to protegrins. Infect Immun 64: 1240-1245.
56. Rest, R.F., and Pretzer, E. (1981) Degradation of gonococcal outer membrane proteins by human neutrophil lysosomal proteases. Infect Immun 34: 62-68.
57. Rest, R.F., Fischer, S.H., Ingham, Z.Z., and Jones, J.F. (1982) Interactions of Neisseria gonorrhoeae with human neutrophils: Effects of serum and gonococcal opacity on phagocyte killing and chemiluminescence. Infect Immun 36: 737-744.
58. Roos, D., van Bruggen, R., and Meischl, C. (2003) Oxidative killing of microbes by neutrophils. Microbes Infect 5: 1307-1315.
59. Segal, A.W. (2005) How neutrophils kill microbes. Ann Rev Immunol 23: 197-223.
60. Segal, E., Billyard, E., So, M., Storzbach, S., and Meyer, T.F. (1985) Role of chromosomal rearrangement in N. gonorrhoeae pilus phase variation. Cell 40: 293-300.
61. Seib, K.L., Simons, M.P., Wu, H.J., McEwan, A.G., Nauseef, W.M., Apicella, M.A., and 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.
62. Seib, K.L., Wu, H.J., Kidd, S.P., Apicella, M.A., Jennings, M.P., and 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.
63. Seifert, H.S., Wright, C.J., Jerse, A.E., Cohen, M.S., and Cannon, J.G. (1994) Multiple gonococcal pilin antigenic variants are produced during experimental human infections. J Clin Invest 93: 2744-2749.
64. Shafer, W.M., and Rest, R.F. (1989) Interactions of gonococci with phagocytic cells. Annu Rev Microbiol 43: 121-145.
65. Shafer, W.M., Onunka, V.C., and Martin, L.E. (1986) Antigonococcal activity of human neutrophil cathepsin G. Infect Immun 54: 184-188.
66. Shafer, W.M., Qu, X., Waring, A.J., and Lehrer, R.I. (1998) Modulation of Neisseria gonorrhoeae susceptibility to vertebrate antibacterial peptides due to a member of the resistance/nodulation/division efflux pump family. Proc Natl Acad Sci USA 95: 1829-1833.
67. Simons, M.P., Nauseef, W.M., and Apicella, M.A. (2005) Interactions of Neisseria gonorrhoeae with adherent polymorphonuclear leukocytes. Infect Immun 73: 1971-1977.
68. Soler-Garcia, A.A., and Jerse, A.E. (2004) A Neisseria gonorrhoeae catalase mutant is more sensitive to hydrogen peroxide and paraquat, an inducer of toxic oxygen radicals. Microb Pathog 37: 55-63.
69. Soler-Garcia, A.A., and 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.
70. Staali, L., Bauer, S., Morgelin, M., Bjorck, L., and Tapper, H. (2006) Streptococcus pyogenes bacteria modulate membrane traffic in human neutrophils and selectively inhibit azurophilic granule fusion with phagosomes. Cell Microbiol 8: 690-703.
71. Stohl, E.A., Criss, A.K., and Seifert, H.S. (2005) The transcriptome response of Neisseria gonorrhoeae to hydrogen peroxide reveals genes with previously uncharacterized roles in oxidative damage protection. Mol Microbiol 58: 520-532.
72. Swanson, J., Barrera, O., Sola, J., and Boslego, J. (1988) Expression of outer membrane protein II by gonococci in experimental gonorrhea. J Exp Med 168: 2121-2129.
73. Terada, L.S., Johansen, K.A., Nowbar, S., Vasil, A.I., and Vasil, M.L. (1999) Pseudomonas aeruginosa hemolytic phospholipase C suppresses neutrophil respiratory burst activity. Infect Immun 67: 2371-2376.
74. Tobiason, D.M., and Seifert, H.S. (2006) The obligate human pathogen, Neisseria gonorrhoeae, is polyploid. PLoS Biol 4: 1069-1078.
75. Ulsen, P., and Tommassen, J. (2006) Protein secretion and secreted proteins in pathogenic Neisseriaceae. FEMS Microbiol Rev 30: 292-319.
76. Vazquez-Torres, A., Xu, Y., Jones-Carson, J., Holden, D.W., Lucia, S.M., Dinauer, M.C., etal. (2000) Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 287: 1655-1658.
77. Virji, M., and Heckels, J.E. (1986) The effect of protein II and pili on the interaction of Neisseria gonorrhoeae with human polymorphonuclear leucocytes. J Gen Microbiol 132: 503-512.
78. Warner, D.M., Folster, J.P., Shafer, W.M., and Jerse, A.E. (2007) Regulation of the MtrC-MtrD-MtrE efflux-pump system modulates the in vivo fitness of Neisseria gonorrhoeae. J Infect Dis 196: 1804-1812.
79. WHO (2001) Global Prevalence and Incidence of Selected Curable Sexually Transmitted Infections: Overview and Estimates. Geneva: WHO.
80. Zak, K., Diaz, J.-L., Jackson, D., and Heckels, J.E. (1984) Antigenic variation during infection with Neisseria gonorrhoeae: Detection of antibodies to surface proteins in sera of patients with gonorrhea. J Infect Dis 149: 166-174.