Interactions of pathogenic Neisseria with host cells. Is it possible to assemble the puzzle?

Molecular Microbiology

Volumn 32, Issue 6, 1999, Pages 1124-1132

  Nassif, Xavier ^a   Pujol, Céline ^a   Morand, Philippe ^a   Eugène, Emmanuel ^a  

^a INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GLYCOPROTEIN; PORIN;

BACTERIAL INFECTION; BACTERIUM PILUS; CELL INTERACTION; DISEASE COURSE; GONORRHEA; HUMAN; LIFE CYCLE; MENINGOCOCCOSIS; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; HUMANS; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS; PILI, SEX; PORINS;

EID: 0033028556     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1999.01416.x     Document Type: Review

References (60)

1. Apicella, M.A., Ketterer, M., Lee, F.K., 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: 636-646
2. Ayala, P., Lin, L., Hopper, S., Fukuda, M., and So, M. (1998) Infection of epithelial cells by pathogenic neisseriae reduces the levels of multiple lysosomal constituents. Infect Immun 66: 5001-5007
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. + Neisseria gonorrhoeae by limited availability of normal human serum. Infect Immun 65: 645-650
5. 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
6. Cannon, J.G., Johannsen, D., Hobbs, J.D., Hoffman, N., Dempsey, J.A.F., Johnston, D., et al. (1998) Studies of the human challenge model of gonococcal infection: population dynamics of gonococci during experimental infection, and infectivity of isogenic mutants. In Abstracts of the Eleventh International Pathogenic Neisseria Conference. Nassif, X., Quentin-Millet, M.J., and Taha, M.K. (eds). Paris: EDIMARK, pp. 48
7. Chen, T., Grunert, F., Medina-Marino, A., and Gotschlich, E.C. (1997) Several carcinoembryonic antigens (CD66) serve as receptors for goncoccal opacity proteins. J Exp Med 185: 1557-1564
8. v integrin receptors. FEBS Lett 424: 84-88
9. Duensing, T.D., and van Putten, J.P.M. (1997) Vitronectin mediates internalization of Neisseria gonorrhoeae by Chinese hamster ovary cells. Infect Immun 65: 964-970
10. Feavers, I.M., and Maiden, M.C.J. (1998) A gonococcal porA pseudogene: implications for understanding the evolution and pathogenicity of Neisseria gonorrhoeae. Mol Microbiol 30: 647-656
11. 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
12. Forest, K., Dunham, S.T., Koomey, M., and Tainer, J. (1999). Crystallographic structure reveals phosphorylated pilin from Neisseria: phosphoserine sites modify type IV pilus surface chemistry and fibre morphology. Mol Microbiol 31: 743-752
13. Giardina, P.C., Wen, K.K., Williams, R., Lubaroff, D., Blake, M.S., Rubenstein, P.A., and Apicella, M.A. (1998) Neisseria-encoded porins influence actin dynamics, in vitro. In Abstracts of the Eleventh International Pathogenic Neisseria Conference Nassif, X., Quentin-Millet, M.J., and Taha, M.K. (eds). Paris: EDK, p. 36
14. Gomez-Duarte, O.G., Dehio, M., Guzman, C.A., Chhatwal, G.S., Dehio, C., and Meyer, T.F. (1997) Binding of vitronectin to Opa-expressing Neisseria gonorrhoeae mediates invasion of HeLa cells. Infect Immun 65: 3857-3866
15. Grassmé, H., Gulbins, E., Brenner, B., Ferlinz, K., Sandhoff, K., Harzer, K., et al. (1997) Acidic sphingomyelinase mediates entry of N. gonorrhoeae into nonphagocytic cells. Cell 91: 605-615
16. 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
17. 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
18. Guibourdenche, M., Popoff, M.Y., and Riou, J.Y. (1986) Deoxyribonucleic acid relatedness among Neisseria gonorrhoeae. N. meningitidis, N. lactamica, N. cinema and Neisseria polysaccharea. Ann Inst Pasteur/Microbiol 137B: 177-185
19. Harvey, H.A., Ketterer, M.R., Preston, A., Lubaroff, D., Williams, R., and Apicella, M.A. (1997) Ultrastructural analysis of primary human urethral epithelial cell cultures infected with Neisseria gonorrhoeae. Infect Immun 65: 2420-2427
20. 52 Neisseria gonorrhoeae requires a Src-like tyrosine kinase- and Rac1-dependent signalling pathway. EMBO J 17: 443-454
21. Jones, B.D., Ghori, N., and Falkow, S. (1994) Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J Exp Med 180: 15-23
22. Källström, H., and Jonsson, A.-B. (1998) Characterization of the region downstream of the pilus biogenesis gene pilC1 in Neisseria gonorrhoeae. Biochim Biophys Acta 1397: 137-140
23. 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
24. Lin, L., Ayala, P., Larson, J., Mulks, M., Fukuda, M., Carisson, S.R., et al. (1997) The Neisseria type 2 IgA1 protease cleaves LAMP1 and promotes survival of bacteria within epithelial cells. Mol Microbiol 24: 1083-1094
25. McGee, Z., Johnson, A., and Taylor-Robinson, D. (1981) Pathogenic Mechanisms of Neisseria gonorrhoeae: observations on damage to human fallopian tubes in organ culture by Bonococci of colony type 1 or type 4. J Infect Dis 143: 413-422
26. McGee, Z., Stephens, D., Hoffman, L., Schlech, W. III, and Horn, R. (1983) Mechanisms of mucosal invasion by pathogenic Neisseria. Rev Infect Dis 5: S708-S714
27. Marceau, M., and Nassif, X. (1999) S-pilin production by Neisseria gonorrhoeae does not require post-traductional modification of Ser63, as is the case for Neisseria meningitidis. J Bacteriol 181: 656-661
28. Marceau, M., Beretti, J.-L., and Nassif, X. (1995) High adhesiveness of encapsulated Neisseria meningitidis to epithelial cells is associated with the formation of bundles of pili. Mol Microbiol 17: 855-863
29. 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: 705-715
30. Merz, A.J., and So, M. (1997) Attachment of piliated, Opa (-) and Opc (-) gonococci and meningococci to epithelial cells elicits cortical actin rearrangements and clustering of tyrosine-phosphorylated proteins. Infect Immun 65: 4341-4349
31. Merz, A.J., Rifenbery, D.B., Arvidson, C.G., and So, M. (1996) Traversal of a polarized epithelium by pathogenic Neisseriae: facilitation by type IV pili and maintenance of epithelial barrier function. Mol Med 2: 745-754
32. Nassif, X., Beretti, J.-L., Lowy, J., Stenberg, P., O'Gaora, P., Pfeifer, J., et al. (1994) Roles of pilin and PilC in adhesion of Neisseria meningitidis to human epithelial and endothelial cells. Proc Natl Acad Sci, USA 91: 3769-3773
33. Naumann, M., Wessler, S., Bartsch, C., Wieland, B., and Meyer, T.F. (1997) Neisseria gonorrhoeae epithelial cell interaction leads to the activation of the transcription factors nuclear factor kappaB and activator protein 1 and the induction of inflammatory cytokines. J Exp Med 186: 247-258
34. Parge, H.E., Forest, K.T., Hickey, M.J., Christensen, D.A., Getzoff, E.D., and Tainer, J.A. (1995) Structure of the fibre-forming protein pilin at 2.6 A resolution. Nature 378: 32-38
35. Paruchuri, D.K., Seifert, H.S., Ajioka, R.S., Karlson, K.-A., and So, M. (1990) Identification and characterization of a Neisseria gonorrhoeae gene encoding a glycolipid-binding adhesin. Proc Natl Acad Sci USA 87: 333-337
36. Pron, B., Taha, M.-K., Rambaud, C., Fournet, J.-C., Pattey, N., Monnet, J.-P., et al. (1997) Interaction of Neisseria meningitidis with the components of the blood-brain barrier correlates with an increased expression of PilC. J Infect Dis 176: 1285-1292
37. Pujol, C., Eugène, E., de Saint Martin, L., and Nassif, X. (1997) Interaction of Neisseria meningitidis with a polarized monolayer of epithelial cells. Infect Immun 65: 4836-4842
38. Pujol, C., Eugène, E., Marceau, M., and Nassif, X. (1999) The meningococcal PilT protein is required for induction of intimate attachment to epithelial cells following pilus-mediated adhesion. Proc Natl Acad Sci USA 96: 4017-4022
39. van Putten, J.P.M. (1993) Phase variation of lipopolysaccharide directs interconversion of invasive and immuno-resistant phenotypes of Neisseria gonorrhoeae. EMBO J 12: 4043-4051
40. van Putten, J.P., and Paul, S.M. (1995) Binding of syndecan like cell surface proteoglycan receptors is required for Neisseria gonorrhoeae entry into human mucosal cells. EMBO J 14: 2144-2154
41. + gonococci into HEp-2 cells requires concerted action of glycosaminoglycans, fibronectin and integrin receptors. Mol Microbiol 29: 369-379
42. van Putten, J.P.M., Duensing, T.D., and Carlson, J. (1998b) Gonococcal invasion of epithelial cells driven by PIA., a bacterial ion channel with GTP binding properties. J Exp Med 188: 941-952
43. Rudel, T., Scheuerpflug, I., and Meyer, T.F. (1995) Neisseria PilC protein identified as type-4 pilus tip-located adhesin. Nature 373: 357-362
44. Sarkari, J., Pandt, N., Moxon, E.R., and Achtman, M. (1994) Variable expression of the Opc outer membrane protein in Neisseria meningitidis is caused by size variation of a promoter containing poly-cytidine. Mol Microbiol 13: 207-217
45. Schwan, E.T., Eickerjäger, S., Fischer, E., Maier, J., Manning, P.A., and Meyer, T.F. (1998) Identification and characterization of genomic loci of both pathogenic Neisseria mediating independent recognition of glycolipids and binding to human epithelial cells. In Abstracts of the Eleventh International Pathogenic Neisseria Conference Nassif, X., Quentin-Millet, M.J., and Taha, M.K. (eds). Paris: EDK, p. 387
46. Spence, J.M.J.C.R., C., and Clark, V.L. (1997) A proposed role for the lutropin receptor in contact-inducible gonococcal invasion of Hec1B cells. Infect Immun 65: 3736-3742
47. Stimson, E., Virji, M., Barker, S., Panico, M., Blench, I., Saunder, J., et al. (1996) Discovery of a novel protein modification: alpha-glycerophosphate is a substituent of meningococcal pilin. Biochem J 316: 29-33
48. Stimson, E., Virji, M., Makepeace, K., Dell, A., Morris, H.R., Payne, G., et al. (1995) Meningococcal pilin: a glycoprotein substituted with digalactosyl 2,4-diacetamido-2,4,6-trideoxyhexose. Mol Microbiol 17: 1201-1214
49. 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
50. Taha, M.-K., Morand, P., Pereira, Y., Eugène, E., Giorgini, D., Larribe, M., and Nassif, X. (1998) Pilus-mediated adhesion of Neisseria meningitidis - the essential role of cell contact-dependent transcriptional upregulation of the PilC1 protein. Mol Microbiol 28: 1153-1163
51. Ulmer, J.B., Burke, C.J., Shi, C., Friedman, A., Donnelly, J.J., and Liu, M.A. (1992) Pore formation and mitogenicity in blood cells by the class 2 protein of Neisseria meningitidis. J Biol Chem 267: 19266-19271
52. Virji, M., Makepeace, K., Ferguson, D.J.P., Achtman, M., Sarkari, J., and Moxon, E.R. (1992) Expression of the Opc protein correlates with invasion of epithelial and endothelial cells by Neisseria meningitidis. Mol Microbiol 6: 2785-2795
53. Virji, M., Makepeace, K., Ferguson, D.J.P., Achtman, M., and Moxon, E.R. (1993) Meningococcal Opa and Opc proteins: their role in colonization and invasion of human epithelial and endothelial cells. Mol Microbiol 10: 499-510
54. Virji, M., Makepeace, K., and Moxon, E.R. (1994) Distinct mechanisms of interactions of Opc-expressing meningococci at apical and basolateral surfaces of human endothelial cells; the role of integrins in apical interactions. Mol Microbiol 14: 173-184
55. Virji, M., Makepeace, K., Ferguson, D.J.P., and Watt, S.M. (1996a) Carcinoembryonic antigens (CD66) on epithelial cells and neutrophils are receptors for Opa proteins of pathogenic neisseriae. Mol Microbiol 22: 941-950
56. Virji, M., Watt, S.M., Barker, S., Makepeace, K., and Doyonnas, R. (1996b) The N-domain of the humain CD66a adhesion molecule is a target for Opa proteins of Neisseria meningitidis and Neisseria gonorrhoeae. Mol Microbiol 22: 929-939
57. de Vries, F.P., Cole, R., Dankert, J., Frosch, M., and van Putten, J.P.M. (1998) Neisseria meningitidis producing the Opc adhesin binds epithelial cell proteoglycan receptors. Mol Microbiol 27: 1203-1212
58. 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
59. 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: 4263-4267
60. 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: 171-186