Neisseria gonorrhoeae phagosomes delay fusion with primary granules to enhance bacterial survival inside human neutrophils

Cellular Microbiology

Volumn 15, Issue 8, 2013, Pages 1323-1340

  Johnson, M Brittany ^a   Criss, Alison K ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYSOPHOSPHATIDYLCHOLINE; SERINE PROTEINASE;

ARTICLE; BACTERIAL SURVIVAL; BACTERIAL VIABILITY; CONTROLLED STUDY; ELECTRON MICROSCOPY; EX VIVO STUDY; GONORRHEA; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE MICROSCOPY; NEISSERIA GONORRHOEAE; NEUTROPHIL; NONHUMAN; OPSONIZATION; PHAGOLYSOSOME; PHAGOSOME; PRIORITY JOURNAL;

ANIMALS; CYTOPLASMIC GRANULES; HUMANS; IMMUNOGLOBULIN G; INTERLEUKIN-8; MALE; MEMBRANE FUSION; MICROBIAL VIABILITY; NEISSERIA GONORRHOEAE; NEUTROPHILS; PEPTIDE HYDROLASES; PHAGOSOMES; SERINE PROTEASES;

BACTERIA (MICROORGANISMS); NEISSERIA GONORRHOEAE;

EID: 84880330691     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12117     Document Type: Article

References (57)

1. Balthazar, J.T., Gusa, A., Martin, L.E., Choudhury, B., Carlson, R., and Shafer, W.M. (2011) Lipooligosaccharide structure is an important determinant in the resistance of Neisseria gonorrhoeae to antimicrobial agents of innate host defense. Front Microbiol 2: 30.
2. Bangalore, N., Travis, J., Onunka, V.C., Pohl, J., and Shafer, W.M. (1990) Identification of the primary antimicrobial domains in human neutrophil cathepsin G. J Biol Chem 265: 13584-13588.
3. 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.
4. 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.
5. Cahoon, L.A., and Seifert, H.S. (2009) An alternative DNA structure is necessary for pilin antigenic variation in Neisseria gonorrhoeae. Science 325: 764-767.
6. 2-independent antimicrobial proteins from human polymorphonuclear granulocytes. Infect Immun 47: 401-407.
7. Chen, A., and Seifert, H.S. (2011) Neisseria gonorrhoeae-mediated inhibition of apoptotic signalling in polymorphonuclear leukocytes. Infect Immun 79: 4447-4458.
8. Cougoule, C., Constant, P., Etienne, G., Daffe, M., and Maridonneau-Parini, I. (2002) Lack of fusion of azurophil granules with phagosomes during phagocytosis of Mycobacterium smegmatis by human neutrophils is not actively controlled by the bacterium. Infect Immun 70: 1591-1598.
9. Criss, A.K., and Seifert, H.S. (2008) Neisseria gonorrhoeae suppresses the oxidative burst of human polymorphonuclear leukocytes. Cell Microbiol 10: 2257-2270.
10. Criss, A.K., and Seifert, H.S. (2012) A bacterial siren song: intimate interactions between Neisseria and neutrophils. Nat Rev Microbiol 10: 178-190.
11. Criss, A.K., Katz, B.Z., and Seifert, H.S. (2009) Resistance of Neisseria gonorrhoeae to non-oxidative killing by adherent human polymorphonuclear leucocytes. Cell Microbiol 11: 1074-1087.
12. Densen, P., and Mandell, G.L. (1978) Gonococcal interactions with polymorphonuclear neutrophils: importance of the phagosome for bactericidal activity. J Clin Invest 62: 1161-1171.
13. Desjardins, M., and Descoteaux, A. (1997) Inhibition of phagolysosomal biogenesis by the Leishmania lipophosphoglycan. J Exp Med 185: 2061-2068.
14. Faurschou, M., and Borregaard, N. (2003) Neutrophil granules and secretory vesicles in inflammation. Microbes Infect 5: 1317-1327.
15. Fratti, R.A., Backer, J.M., Gruenberg, J., Corvera, S., and Deretic, V. (2001) Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J Cell Biol 154: 631-644.
16. Geier, H., and Celli, J. (2011) Phagocytic receptors dictate phagosomal escape and intracellular proliferation of Francisella tularensis. Infect Immun 79: 2204-2214.
17. Hedges, S.R., Sibley, D.A., Mayo, M.S., Hook, E.W., 3rd, and Russell, M.W. (1998) Cytokine and antibody responses in women infected with Neisseria gonorrhoeae: effects of concomitant infections. J Infect Dis 178: 742-751.
18. Hong, C.W., Kim, T.K., Ham, H.Y., Nam, J.S., Kim, Y.H., Zheng, H., etal. (2010) Lysophosphatidylcholine increases neutrophil bactericidal activity by enhancement of azurophil granule-phagosome fusion via glycine.GlyR alpha 2/TRPM2/p38 MAPK signaling. J Immunol 184: 4401-4413.
19. Johnson, M.B., and Criss, A.K. (2011) Resistance of Neisseria gonorrhoeae to neutrophils. Front Microbiol 2: 77.
20. Kellogg, D.S., Jr, Peacock, W.L., Jr, Deacon, W.E., Brown, L., and Pirkle, D.I. (1963) Neisseria gonorrhoeae. I. Virulence genetically linked to clonal variation. J Bacteriol 85: 1274-1279.
21. Kirkcaldy, R.D., Ballard, R.C., and Dowell, D. (2011) Gonococcal resistance: are cephalosporins next? Curr Infect Dis Rep 13: 196-204.
22. Lee, E.H., and Shafer, W.M. (1999) The farAB-encoded efflux pump mediates resistance of gonococci to long-chained antibacterial fatty acids. Mol Microbiol 33: 839-845.
23. Lee, W.L., Harrison, R.E., and Grinstein, S. (2003) Phagocytosis by neutrophils. Microbes Infect 5: 1299-1306.
24. Lewis, L.A., Choudhury, B., Balthazar, J.T., Martin, L.E., Ram, S., Rice, P.A., etal. (2009) Phosphoethanolamine substitution of lipid A and resistance of Neisseria gonorrhoeae to cationic antimicrobial peptides and complement-mediated killing by normal human serum. Infect Immun 77: 1112-1120.
25. Lin, L., Ayala, P., Larson, J., Mulks, M., Fukuda, M., Carlsson, S.R., etal. (1997) The Neisseria type 2 IgA1 protease cleaves LAMP1 and promotes survival of bacteria within epithelial cells. Mol Microbiol 24: 1083-1094.
26. 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.
27. Mollinedo, F., Janssen, H., Iglesia-Vicente, J., Villa-Pulgarin, J.A., and Calafat, J. (2010) Selective fusion of azurophilic granules with Leishmania-containing phagosomes in human neutrophils. J Biol Chem 285: 34528-34536.
28. Morse, S.A., and Bartenstein, L. (1980) Purine metabolism in Neisseria gonorrhoeae: the requirement for hypoxanthine. Can J Microbiol 26: 13-20.
29. Munafo, D.B., Johnson, J.L., Ellis, B.A., Rutschmann, S., Beutler, B., and Catz, S.D. (2007) Rab27a is a key component of the secretory machinery of azurophilic granules in granulocytes. Biochem J 402: 229-239.
30. Ndowa, F., and Lusti-Narasimhan, M. (2012) The threat of untreatable gonorrhoea: implications and consequences for reproductive and sexual morbidity. Reprod Health Matters 20: 76-82.
31. Perera, N.C., Schilling, O., Kittel, H., Back, W., Kremmer, E., and Jenne, D.E. (2012) NSP4, an elastase-related protease in human neutrophils with arginine specificity. Proc Natl Acad Sci USA 109: 6229-6234.
32. 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.
33. Ramsey, K.H., Schneider, H., Cross, A.S., Boslego, J.W., Hoover, D.L., Staley, T.L., etal. (1995) Inflammatory cytokines produced in response to experimental human gonorrhea. J Infect Dis 172: 186-191.
34. Rest, R.F. (1979) Killing of Neisseria gonorrhoeae by human polymorphonuclear neutrophil granule extracts. Infect Immun 25: 574-579.
35. Rest, R.F., and Pretzer, E. (1981) Degradation of gonococcal outer membrane proteins by human neutrophil lysosomal proteases. Infect Immun 34: 62-68.
36. Rock, J.P., and Rest, R.F. (1988) Rapid damage to membranes of Neisseria gonorrhoeae caused by human neutrophil granule extracts. J Gen Microbiol 134: 509-519.
37. Segal, A.W. (2005) How neutrophils kill microbes. Annu Rev Immunol 23: 197-223.
38. 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.
39. Shafer, W.M., and Morse, S.A. (1987) Cleavage of the protein III and major iron-regulated protein of Neisseria gonorrhoeae by lysosomal cathepsin G. J Gen Microbiol 133: 155-162.
40. Shafer, W.M., Onunka, V., and Hitchcock, P.J. (1986a) A spontaneous mutant of Neisseria gonorrhoeae with decreased resistance to neutrophil granule proteins. J Infect Dis 153: 910-917.
41. Shafer, W.M., Onunka, V.C., and Martin, L.E. (1986b) Antigonococcal activity of human neutrophil cathepsin G. Infect Immun 54: 184-188.
42. 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.
43. Silliman, C.C., Elzi, D.J., Ambruso, D.R., Musters, R.J., Hamiel, C., Harbeck, R.J., etal. (2003) Lysophosphatidylcholines prime the NADPH oxidase and stimulate multiple neutrophil functions through changes in cytosolic calcium. J Leukoc Biol 73: 511-524.
44. Simons, M.P., Nauseef, W.M., and Apicella, M.A. (2005) Interactions of Neisseria gonorrhoeae with adherent polymorphonuclear leukocytes. Infect Immun 73: 1971-1977.
45. Simons, M.P., Nauseef, W.M., Griffith, T.S., and Apicella, M.A. (2006) Neisseria gonorrhoeae delays the onset of apoptosis in polymorphonuclear leukocytes. Cell Microbiol 8: 1780-1790.
46. Sorensen, O.E., Follin, P., Johnsen, A.H., Calafat, J., Tjabringa, G.S., Hiemstra, P.S., and Borregaard, N. (2001) Human cathelicidin, hCAP-18, is processed to the antimicrobial peptide LL-37 by extracellular cleavage with proteinase 3. Blood 97: 3951-3959.
47. 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.
48. 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.
49. Stuart, L.M., and Ezekowitz, R.A. (2005) Phagocytosis: elegant complexity. Immunity 22: 539-550.
50. van Ulsen, P., and Tommassen, J. (2006) Protein secretion and secreted proteins in pathogenic Neisseriaceae. FEMS Microbiol Rev 30: 292-319.
51. Unemo, M., and Shafer, W.M. (2011) Antibiotic resistance in Neisseria gonorrhoeae: origin, evolution, and lessons learned for the future. Ann N Y Acad Sci 1230: E19-E28.
52. Urban, C.F., Lourido, S., and Zychlinsky, A. (2006) How do microbes evade neutrophil killing? Cell Microbiol 8: 1687-1696.
53. Voyich, J.M., Braughton, K.R., Sturdevant, D.E., Whitney, A.R., Said-Salim, B., Porcella, S.F., etal. (2005) Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J Immunol 175: 3907-3919.
54. Wiesner, P.J., and Thompson, S.E., 3rd (1980) Gonococcal diseases. Dis Mon 26: 1-44.
55. Workowski, K.A., and Berman, S. (2010) Sexually transmitted diseases treatment guidelines, 2010. MMWR Recomm Rep 59: 1-110.
56. Wu, H., Soler-Garcia, A.A., and Jerse, A.E. (2009) A strain-specific catalase mutation and mutation of the metal-binding transporter gene mntC attenuate Neisseria gonorrhoeae in vivo but not by increasing susceptibility to oxidative killing by phagocytes. Infect Immun 77: 1091-1102.
57. Zhu, W., Chen, C.J., Thomas, C.E., Anderson, J.E., Jerse, A.E., and Sparling, P.F. (2011) Vaccines for gonorrhea: can we rise to the challenge? Front Microbiol 2: 124.