Opa+ Neisseria gonorrhoeae exhibits reduced survival in human neutrophils via Src family kinase-mediated bacterial trafficking into mature phagolysosomes

Cellular Microbiology

Volumn 17, Issue 5, 2015, Pages 648-665

  Johnson, M Brittany ^a   Ball, Louise M ^a   Daily, Kylene P ^a   Martin, Jennifer N ^b   Columbus, Linda ^b   Criss, Alison K ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 4 AMINO 7 TERT BUTYL 5 (4 METHYLPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; BACTERIAL PROTEIN; BACTERICIDAL PERMEABILITY INCREASING PROTEIN; CARCINOEMBRYONIC ANTIGEN; CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 1; CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 6; CEACAM3 PROTEIN; CELL ADHESION MOLECULE; EHT 1864; ENZYME INHIBITOR; OPACITY ASSOCIATED PROTEIN; PICEATANNOL; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; OPA PROTEIN, NEISSERIA; OUTER MEMBRANE PROTEIN;

ARTICLE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; CONTROLLED STUDY; HUMAN; MIXED INFECTION; MOUSE; NEISSERIA GONORRHOEAE; NEUTROPHIL; NONHUMAN; PHAGOLYSOSOME; PHAGOSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; RESPIRATORY BURST; CELL CULTURE; IMMUNOLOGY; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); NEISSERIA GONORRHOEAE;

BACTERIAL OUTER MEMBRANE PROTEINS; CELL ADHESION MOLECULES; CELLS, CULTURED; HUMANS; MICROBIAL VIABILITY; NEISSERIA GONORRHOEAE; NEUTROPHILS; PHAGOSOMES; SIGNAL TRANSDUCTION;

EID: 84927743153     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12389     Document Type: Article

References (78)

1. Abdel-Latif, D., Steward, M., and Lacy, P. (2005) Neutrophil primary granule release and maximal superoxide generation depend on Rac2 in a common signalling pathway. Can J Physiol Pharmacol 83: 69-75.
2. Astarie-Dequeker, C., Nigou, J., Puzo, G., and Maridonneau-Parini, I. (2000) Lipoarabinomannans activate the protein tyrosine kinase Hck in human neutrophils. Infect Immun 68: 4827-4830.
3. Ball, L.M., and Criss, A.K. (2013) Constitutively Opa-expressing and opa-deficient Neisseria gonorrhoeae strains differentially stimulate and survive exposure to human neutrophils. J Bacteriol 195: 2982-2990.
4. Bhat, K.S., Gibbs, C.P., Barrera, O., Morrison, S.G., Jahnig, F., Stern, A., etal. (1991) The opacity proteins of Neisseria gonorrhoeae strain MS11 are encoded by a family of 11 complete genes. Mol Microbiol 5: 1889-1901.
5. Borregaard, N. (2010) Neutrophils, from marrow to microbes. Immunity 33: 657-670.
6. Borregaard, N., Sorensen, O.E., and Theilgaard-Monch, K. (2007) Neutrophil granules: a library of innate immunity proteins. Trends Immunol 28: 340-345.
7. Bos, M.P., Kuroki, M., Krop-Watorek, A., Hogan, D., and Belland, R.J. (1998) CD66 receptor specificity exhibited by neisserial Opa variants is controlled by protein determinants in CD66 N-domains. Proc Natl Acad Sci USA 95: 9584-9589.
8. Buntru, A., Roth, A., Nyffenegger-Jann, N.J., and Hauck, C.R. (2012) HemITAM signaling by CEACAM3, a human granulocyte receptor recognizing bacterial pathogens. Arch Biochem Biophys 524: 77-83.
9. 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.
10. 2-independent antimicrobial proteins from human polymorphonuclear granulocytes. Infect Immun 47: 401-407.
11. 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.
12. Chen, T., Bolland, S., Chen, I., Parker, J., Pantelic, M., Grunert, F., and Zimmermann, W. (2001) The CGM1a (CEACAM3/CD66d)-mediated phagocytic pathway of Neisseria gonorrhoeae expressing opacity proteins is also the pathway to cell death. J Biol Chem 276: 17413-17419.
13. Cole, J.G., Fulcher, N.B., and Jerse, A.E. (2010) Opacity proteins increase Neisseria gonorrhoeae fitness in the female genital tract due to a factor under ovarian control. Infect Immun 78: 1629-1641.
14. Connell, T.D., Shaffer, D., and Cannon, J.G. (1990) Characterization of the repertoire of hypervariable regions in the Protein II (opa) gene family of Neisseria gonorrhoeae. Mol Microbiol 4: 439-449.
15. 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.
16. Criss, A.K., and Seifert, H.S. (2008) Neisseria gonorrhoeae suppresses the oxidative burst of human polymorphonuclear leukocytes. Cell Microbiol 10: 2257-2270.
17. 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.
18. Dempsey, J.A., Litaker, W., Madhure, A., Snodgrass, T.L., and Cannon, J.G. (1991) Physical map of the chromosome of Neisseria gonorrhoeae FA1090 with locations of genetic markers, including opa and pil genes. J Bacteriol 173: 5476-5486.
19. Edwards, S.W. (2005) Biochemistry and Physiology of the Neutrophil. Cambridge, UK: Cambridge University Press.
20. Fensome, A., Cunningham, E., Prosser, S., Tan, S.K., Swigart, P., Thomas, G., etal. (1996) ARF and PITP restore GTP gamma S-stimulated protein secretion from cytosol-depleted HL60 cells by promoting PIP2 synthesis. Curr Biol 6: 730-738.
21. 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.
22. Fulcher, N.B. (2004) The role of Neisseria gonorrhoeae opacity proteins in host cell interactions and pathogenesis. PhD thesis, Department of Microbiology and Immunology, Chapel Hill, NC, University of North Carolina.
23. Fumagalli, L., Zhang, H., Baruzzi, A., Lowell, C.A., and Berton, G. (2007) The Src family kinases Hck and Fgr regulate neutrophil responses to N-formyl-methionyl-leucyl-phenylalanine. J Immunol 178: 3874-3885.
24. Gray-Owen, S.D., and Blumberg, R.S. (2006) CEACAM1: contact-dependent control of immunity. Nat Rev Immunol 6: 433-446.
25. Gray-Owen, S.D., Dehio, C., Haude, A., Grunert, F., and Meyer, T.F. (1997a) CD66 carcinoembryonic antigens mediate interactions between Opa-expressing Neisseria gonorrhoeae and human polymorphonuclear phagocytes. EMBO J 16: 3435-3445.
26. Gray-Owen, S.D., Lorenzen, D.R., Haude, A., Meyer, T.F., and Dehio, C. (1997b) Differential Opa specificities for CD66 receptors influence tissue interactions and cellular response to Neisseria gonorrhoeae. Mol Microbiol 26: 971-980.
27. Hauck, C.R., Meyer, T.F., Lang, F., and Gulbins, E. (1998) CD66-mediated phagocytosis of Opa52 Neisseria gonorrhoeae requires a Src-like tyrosine kinase- and Rac1-dependent signalling pathway. EMBO J 17: 443-454.
28. Hauck, C.R., Gulbins, E., Lang, F., and Meyer, T.F. (1999) Tyrosine phosphatase SHP-1 is involved in CD66-mediated phagocytosis of Opa52-expressing Neisseria gonorrhoeae. Infect Immun 67: 5490-5494.
29. Hobbs, M.M., Sparling, P.F., Cohen, M.S., Shafer, W.M., Deal, C.D., and Jerse, A.E. (2011) Experimental gonococcal infection in male volunteers: cumulative experience with Neisseria gonorrhoeae strains FA1090 and MS11mkC. Front Microbiol 2: 123.
30. 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.
31. Jerse, A.E. (1999) Experimental gonococcal genital tract infection and opacity protein expression in estradiol-treated mice. Infect Immun 67: 5699-5708.
32. Johnson, M.B., and Criss, A.K. (2013a) Neisseria gonorrhoeae phagosomes delay fusion with primary granules to enhance bacterial survival inside human neutrophils. Cell Microbiol 15: 1323-1340.
33. Johnson, M.B., and Criss, A.K. (2013b) Fluorescence microscopy methods for determining the viability of bacteria in association with mammalian cells. J Vis Exp. doi:10.3791/50729.
34. de Jonge, M.I., Hamstra, H.J., van Alphen, L., Dankert, J., and van der Ley, P. (2003) Mapping the binding domains on meningococcal Opa proteins for CEACAM1 and CEA receptors. Mol Microbiol 50: 1005-1015.
35. 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.
36. Kupsch, E.M., Knepper, B., Kuroki, T., Heuer, I., and Meyer, T.F. (1993) Variable opacity (Opa) outer membrane proteins account for the cell tropisms displayed by Neisseria gonorrhoeae for human leukocytes and epithelial cells. EMBO J 12: 641-650.
37. Lacy, P. (2006) Mechanisms of degranulation in neutrophils. Allergy Asthma Clin Immunol 2: 98-108.
38. McCaw, S.E., Schneider, J., Liao, E.H., Zimmermann, W., and Gray-Owen, S.D. (2003) Immunoreceptor tyrosine-based activation motif phosphorylation during engulfment of Neisseria gonorrhoeae by the neutrophil-restricted CEACAM3 (CD66d) receptor. Mol Microbiol 49: 623-637.
39. McCaw, S.E., Liao, E.H., and Gray-Owen, S.D. (2004) Engulfment of Neisseria gonorrhoeae: revealing distinct processes of bacterial entry by individual carcinoembryonic antigen-related cellular adhesion molecule family receptors. Infect Immun 72: 2742-2752.
40. Makino, S., van Putten, J.P., and Meyer, T.F. (1991) Phase variation of the opacity outer membrane protein controls invasion by Neisseria gonorrhoeae into human epithelial cells. EMBO J 10: 1307-1315.
41. Malorny, B., Morelli, G., Kusecek, B., Kolberg, J., and Achtman, M. (1998) Sequence diversity, predicted two-dimensional protein structure, and epitope mapping of neisserial Opa proteins. J Bacteriol 180: 1323-1330.
42. Mocsai, A., Jakus, Z., Vantus, T., Berton, G., Lowell, C.A., and Ligeti, E. (2000) Kinase pathways in chemoattractant-induced degranulation of neutrophils: the role of p38 mitogen-activated protein kinase activated by Src family kinases. J Immunol 164: 4321-4331.
43. Mohn, H., Le Cabec, V., Fischer, S., and Maridonneau-Parini, I. (1995) The src-family protein-tyrosine kinase p59hck is located on the secretory granules in human neutrophils and translocates towards the phagosome during cell activation. Biochem J 309 (Part 2): 657-665.
44. Murphy, G.L., Connell, T.D., Barritt, D.S., Koomey, M., and Cannon, J.G. (1989) Phase variation of gonococcal protein II: regulation of gene expression by slipped-strand mispairing of a repetitive DNA sequence. Cell 56: 539-547.
45. N'Diaye, E.N., Darzacq, X., Astarie-Dequeker, C., Daffe, M., Calafat, J., and Maridonneau-Parini, I. (1998) Fusion of azurophil granules with phagosomes and activation of the tyrosine kinase Hck are specifically inhibited during phagocytosis of mycobacteria by human neutrophils. J Immunol 161: 4983-4991.
46. Papayannopoulos, V., and Zychlinsky, A. (2009) NETs: a new strategy for using old weapons. Trends Immunol 30: 513-521.
47. Rest, R.F., and Pretzer, E. (1981) Degradation of gonococcal outer membrane proteins by human neutrophil lysosomal proteases. Infect Immun 34: 62-68.
48. Rest, R.F., and Shafer, W.M. (1989) Interactions of Neisseria gonorrhoeae with human neutrophils. Clin Microbiol Rev 2 (Suppl.): S83-S91.
49. 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.
50. Rest, R.F., Lee, N., and Bowden, C. (1985) Stimulation of human leukocytes by protein II+ gonococci is mediated by lectin-like gonococcal components. Infect Immun 50: 116-122.
51. Sadarangani, M., Pollard, A.J., and Gray-Owen, S.D. (2011) Opa proteins and CEACAMs: pathways of immune engagement for pathogenic Neisseria. FEMS Microbiol Rev 35: 498-514.
52. Sarantis, H., and Gray-Owen, S.D. (2007) The specific innate immune receptor CEACAM3 triggers neutrophil bactericidal activities via a Syk kinase-dependent pathway. Cell Microbiol 9: 2167-2180.
53. Sarantis, H., and Gray-Owen, S.D. (2012) Defining the roles of human carcinoembryonic antigen-related cellular adhesion molecules during neutrophil responses to Neisseria gonorrhoeae. Infect Immun 80: 345-358.
54. 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.
55. Sengelov, H., Kjeldsen, L., and Borregaard, N. (1993) Control of exocytosis in early neutrophil activation. J Immunol 150: 1535-1543.
56. 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.
57. Shafer, W.M., Onunka, V.C., and Martin, L.E. (1986) Antigonococcal activity of human neutrophil cathepsin G. Infect Immun 54: 184-188.
58. Shafer, W.M., Onunka, V.C., Jannoun, M., and Huthwaite, L.W. (1990) Molecular mechanism for the antigonococcal action of lysosomal cathepsin G. Mol Microbiol 4: 1269-1277.
59. 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.
60. Simms, A.N., and Jerse, A.E. (2006) In vivo selection for Neisseria gonorrhoeae opacity protein expression in the absence of human carcinoembryonic antigen cell adhesion molecules. Infect Immun 74: 2965-2974.
61. Simons, M.P., Nauseef, W.M., and Apicella, M.A. (2005) Interactions of Neisseria gonorrhoeae with adherent polymorphonuclear leukocytes. Infect Immun 73: 1971-1977.
62. Sintsova, A., Sarantis, H., Islam, E.A., Sun, C.X., Amin, M., Chan, C.H., etal. (2014) Global analysis of neutrophil responses to Neisseria gonorrhoeae reveals a self-propagating inflammatory program. PLoS Pathog 10: e1004341.
63. Smirnov, A., Daily, K.P., and Criss, A.K. (2014) Assembly of NADPH oxidase in human neutrophils is modulated by the opacity-associated protein expression state of Neisseria gonorrhoeae. Infect Immun 82: 1036-1044.
64. 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.
65. Stern, A., Brown, M., Nickel, P., and Meyer, T.F. (1986) Opacity genes in Neisseria gonorrhoeae: control of phase and antigenic variation. Cell 47: 61-71.
66. 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.
67. Stohl, E.A., Dale, E.M., Criss, A.K., and Seifert, H.S. (2013) Neisseria gonorrhoeae metalloprotease NGO1686 is required for full piliation, and piliation is required for resistance to H2O2- and neutrophil-mediated killing. MBio 4: e00399-13.
68. Swanson, J. (1978) Studies on gonococcus infection. XIV. Cell wall protein differences among color/opacity colony variants of Neisseria gonorrhoeae. Infect Immun 21: 292-302.
69. Van Ziffle, J.A., and Lowell, C.A. (2009) Neutrophil-specific deletion of Syk kinase results in reduced host defense to bacterial infection. Blood 114: 4871-4882.
70. Vandeputte-Rutten, L., Bos, M.P., Tommassen, J., and Gros, P. (2003) Crystal structure of neisserial surface protein A (NspA), a conserved outer membrane protein with vaccine potential. J Biol Chem 278: 24825-24830.
71. 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.
72. Virji, M., Makepeace, K., Ferguson, D.J., and Watt, S.M. (1996) Carcinoembryonic antigens (CD66) on epithelial cells and neutrophils are receptors for Opa proteins of pathogenic neisseriae. Mol Microbiol 22: 941-950.
73. Wang, J., Gray-Owen, S.D., Knorre, A., Meyer, T.F., and Dehio, C. (1998) Opa binding to cellular CD66 receptors mediates the transcellular traversal of Neisseria gonorrhoeae across polarized T84 epithelial cell monolayers. Mol Microbiol 30: 657-671.
74. Werner, E. (2004) GTPases and reactive oxygen species: switches for killing and signaling. J Cell Sci 117: 143-153.
75. Wiesner, P.J., and Thompson, S.E., 3rd (1980) Gonococcal diseases. Dis Mon 26: 1-44.
76. World Health Organization (2012) Global incidence and prevalence of selected curable sexually transmitted infections - 2008. Geneva, Switzerland WHO, Department of Reproductive Health and Research.
77. 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.
78. Zen, K., and Parkos, C.A. (2003) Leukocyte-epithelial interactions. Curr Opin Cell Biol 15: 557-564.