Experimental infection of native human ureteral tissue with Neisseria gonorrhoeae: Adhesion, invasion, intracellular fate, exocytosis, and passage through a stratified epithelium

Infection and Immunity

Volumn 65, Issue 8, 1997, Pages 3391-3398

  Mosleh, Ibrahim M ^a,b   Boxberger, Hans Jürgen ^a   Sessler, Michael J ^c   Meyer, Thomas F ^a,b  

^a MAX PLANCK INST FÜR BIOLOGIE   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BACTERIUM ADHERENCE; BACTERIUM PILUS; ELECTRON MICROSCOPY; EPITHELIUM; EXPERIMENTAL INFECTION; GONORRHEA; HUMAN; HUMAN TISSUE; NEISSERIA GONORRHOEAE; NORMAL HUMAN; PRIORITY JOURNAL; URETER;

EID: 0030878294     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.65.8.3391-3398.1997     Document Type: Article

References (48)

1. Apicella, M. A., M. Ketterer, F. K. N. Lee, D. Zhuo, P. A. Rice, and M. S. Blake. 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. Bessen, D., and E. C. Gotschlich. 1986. Interactions of gonococci with HeLa cells: attachment, detachment, replication, penetration, and the role of protein II. Infect. Immun. 54:154-160.
3. Blake, M. S., and E. C. Gotschlich. 1987. Functional and immunological properties of pathogenic Neisseria surface proteins, p. 377-400. In M. Inouye (ed.), Bacterial outer membranes as model systems. John Wiley & Sons, Inc., New York, N.Y.
4. Boxberger, H.-J., M. J. Sessler, B. Maetzel, and T. F. Meyer. 1993. Highly polarized primary epithelial cells from human nasopharynx grown as spheroid-like vesicles. Eur. J. Cell Biol. 62:140-151.
5. Boxberger, H.-J., M. J. Sessler, B. Maetzel, I. M. Mosleh, H.-D. Becker, and T. F. Meyer. 1994. Highly polarized primary urothelial cells from human ureter grown as spheroid-like vesicles. Epithelial Cell Biol. 3:85-95.
6. Chen, T., R. J. Belland, J. Wilson, and J. Swanson. 1995 Adherence of pilus- Opa+ gonococci to epithelial cells in vitro involves heparan sulfate. J. Exp. Med. 182:511-517.
7. Chen, T., and E. C. Gotschlieh. 1996. CGM1a antigen of neutrophils, a receptor of gonococcal opacity protein. Proc. Natl. Acad. Sci. USA 93:14851-14856.
8. Evans, B. A. 1977. Ultrastructural study of cervical gonorrhea. J. Infect. Dis. 136:248-255.
9. Fujita, K., T. Yamamoto, and R. Kitagawa. 1991. Binding sites for P and/or 1-piliated Escherichia coli in human ureter. J. Urol. 146:217-222.
10. Fujita, K., T. Yamamato, T. Yokota, and R. Kitagawa. 1989. In vitro adherence of type 1-fimbriated uropathogenic Escherichia coli to human ureteral mucosa. Infect. Immun. 57:2574-2579.
11. Fujita, K., T. Yokota, T. Oguri, M. Fujime, and R. Kitagawa. 1992. In vitro adherence of Staphylococcus saprophyticus. Staphylococcus epidermidis, Staphylococcus haemolyticus, and Staphylococcus aureus to human ureter. Urol. Res. 20:399-402.
12. Granger, B. L., S. A. Green, C. A. Gabel, C. L. Howe, I. Mellman, and A. Helenius. 1990. Characterization and cloning of Igp 110, a lysosomal membrane glycoprotein from mouse and rat cells. J. Biol. Chem. 265:12036-12043.
13. Grassmé, H. U. C., R. M. Ireland, and J. P. M. van Putten. 1996. Gonococcal opacity protein promotes bacterial entry-associated rearrangements of the epithelial cell actin cytoskeleton. Infect. Immun. 64:1621-1630.
14. Gray-Owen, S. D., C. Dehio, A. Haude, F. Grunert, and T. F. Meyer. 1997. CD66 carcinoembryonic antigens mediate interactions between Opa-expressing Neisseria gonorrhoeae and human polymorphonuclear phagocytes. EMBO J. 16:3435-3445.
15. Gregg, C. R., M. A. Melly, C. G. Hellerqvist, J. G. Coniglio, and Z. A. McGee. 1981. Toxic activity of purified lipopolysaccharide of Neisseria gonorrhoeae for human fallopian tube mucosa. J. Infect. Dis. 143:432-439.
16. Gregg, C. R., M. A. Melly, and Z. A. McGee. 1980. Gonococcal lipopolysaccharide: a toxin for human fallopian tube mucosa. Am. J. Obstet. Gynecol. 138:981-984.
17. Harkness, A. H. 1948. The pathology of gonorrhoea. Br. J. Vener. Dis. 24:137-147.
18. Hauck, C. R., and T. F. Meyer. 1997. Lysosomal/phagosomal membrane protein h-lamp-1 is a target of the IgA1 protease of Neisseria gonorrhoeae. FEBS Lett. 405:86-90.
19. Kellogg, D. S., Jr., I. R. Cohen, L. C. Norins, A. L. Schroeter, and G. Reising. 1968. Neisseria gonorrhoeae. II. Colonial variation and pathogenicity during 35 months in vitro. J. Bacteriol. 96:596-605.
20. König, G. 1991. Polychloroprene glue as an adhesive for mounting specimens for SEM. J. Electron Microsc. Technol. 17:467-468.
21. Kupsch, E.-M., B. Knepper, T. Kuroki, I. Heuer, and T. F. Meyer. 1993. Variable opacity (Opa) outer membrane proteins account for cell tropism displayed by Neisseria gonorrhoeae for human leukocytes and epithelial cells. EMBO J. 12:641-650.
22. Lammel, C. J., N. P. Dekker, R. E. Mandrell, J. M. Griffiss, and G. F. Brooks. 1991. The role of Opa in adherence of gonococci to HEC-1-B cells and to human fallopian tube tissue, p. 615-620. In M. Achtman, P. Kohl, C. March, G. Morelli, A. Seiler, and B. Thiesen (ed.), Neisseria 1990: Proceedings of the Seventh International Pathogenic Neisseria Conference. Walter de Gruyer & Co., Berlin, Germany.
23. Makino, S.-I., J. P. M. van Putten, and T. F. Meyer. 1991. Phase variation of the opacity outer membrane protein controls invasion by Neisseria gonorrhoeae into human epithelial cells. EMBO J. 10:1307-1315.
24. Mårdh, P.-A., B. Baldetorp, C. H. Håkansson, H. Fritz, and L. Weström. 1979. Studies of ciliated epithelia of the human genital tract. 3. Mucociliary wave activity in organ cultures of human fallopian tubes challenged with Neisseria gonorrhoeae and gonococcal endotoxin. Br. J. Vener. Dis. 55:256-264.
25. McGee, Z. A., A. P. Johnson, and D. Taylor-Robinson. 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. 143:413-422.
26. McGee, Z. A., D. S. Stephens, L. H. Hoffman, W. F. Schlech III, and R. G. Horn. 1983. Mechanisms of mucosal invasion by pathogenic Neisseria. Rev. Infect. Dis. 5:S708-S714.
27. Melly, M. A., C. R. Gregg, and Z. A. McGee. 1981. Studies of toxicity of Neisseria gonorrhoeae for human fallopian tube mucosa. J. Infect. Dis. 143:423-131.
28. Meyer, T. F., N. Mlawer, and M. So. 1982. Pilus expression in Neisseria gonorrhoeae involves chromosomal rearrangement. Cell 30:45-52.
29. Nassif, X., J.-L. Beretti, J. Lowy, P. Stenberg, P. O'Gara, P. Pfeifer, S. Normark, and M. So. 1944. Roles of pilin and PilC in adhesion of Neisseria meningitidis to human epithelial cells. Proc. Natl. Acad. Sci. USA 91:3769-3773.
30. Richardson, W. P., and J. C. Sadoff. 1988. Induced engulfment of Neisseria gonorrhoeae by tissue culture cells. Infect. Immun. 56:2512-2514.
31. Rudel, T., J. P. M. van Putten, C. G. Gibbs, R. Haas, and T. F. Meyer. 1992. Interaction of two variable proteins (PilE and PilC) required for pilus mediated adherence of Neisseria gonorrhoeae to human epithelial cells. Mol. Microbiol. 6:3439-3450.
32. Rudel, T., I. Scheuerpflug, and T. F. Meyer. 1995. Neisserial pilC protein identified as type-4 pilus tip-located adhesin. Nature 373:357-359.
33. Salvers, A. A., and D. D. Whitt. 1994. Bacterial pathogenesis: a molecular approach, p. 244. ASM Press, Washington, D.C.
34. Shaw, J. H., and S. Falkow. 1988. Model for invasion of human tissue culture cells by Neisseria gonorrhoeae. Infect. Immun. 56:1625-1632.
35. Stephens, D. S., and M. M. Farley. 1991. Pathogenic events during infection of the human nasopharynx with Neisseria meningitidis and Haemophilus influenzae. Rev. Infect. Dis. 13:22-33.
36. Stephens, D. S., and Z. A. McGee. 1981. Attachment of Neisseria meningitidis to human mucosal surfaces: influence of pili and type of receptor cell. J. Infect. Dis. 143:524-532.
37. Stephens, D. S., Z. A. McGee, and M. D. Cooper. 1987. Cytopathic effects of pathogenic Neisseria. Studies using human fallopian tube organ cultures and human nasopharyngeal organ cultures. Antonic Leeuwenhoek 53:575-584.
38. Thompson, J. A., F. Grunert, and W. Zimmerman. 1991. Carcinoembryonic antigen gene family: molecular biology and clinical perspective. J. Clin. Lab. Anal. 5:344-366.
39. Tjia, K. F., J. P. M. van Putten, E. Pils, and H. I. Zanen. 1988. The interaction between Neisseria gonorrhoeae and the human cornea in organ culture: an electron microscopic study. Graefe's Arch. Clin. Exp. Ophthalmol. 226:341-345.
40. van Putten, J. P. M., and S. M. Paul. 1995. Binding of syndican-like cell surface proteoglycan receptor is required for Neisseria gonorrhoeae entry into human mucosal cells. EMBO J. 14:2144-2154.
41. Virji, M., and J. S. Everson. 1981. Comparative virulence of opacity variants of Neisseria gonorrhoeae strain P9. Infect. Immun. 31:965-970.
42. Virji, M., H. Kayhty, D. J. P. Ferguson, C. Alexandrescu, J. E. Heckels, and E. R. Moxon. 1991. The role of pili in the interactions of pathogenic Neisseria with cultured human endothelial cells. Mol. Microbiol. 5:1831-1841.
43. Virji, M., K. Makepeace, D. J. P. Ferguson, and S. M. Watt. 1996. Carcinoembryonic antigens (CD66) on epithelial cells and neutrophils are receptors for Opa proteins of pathogenic neisseriae. Mol. Microbiol. 22:941-950.
44. Virji, M., K. Makepeace, I. Peak, G. Payne, J. R. Saunders, J. P. Ferguson, and E. R. Moxon. 1995. Functional implications of the expression of PilC protein in meningococci. Mol. Microbiol. 16:1087-1097.
45. Ward, M. E., and P. J. Watt. 1972. Adherence of Neisseria gonorrhoeae to urethral mucosal cells: an electron-microscopic study of human gonorrhea. J. Infect. Dis. 126:601-605.
46. Ward, E. W., P. J. Watt, and J. N. Robertson. 1974. The human fallopian tube: a laboratory model for gonococcal infection. J. Infect. Dis. 129:650-659.
47. Weel, J. F. L., and J. P. M. van Putten. 1991. Fate of the major outer membrane protein PI.A in early and late events of gonococcal infection of epithelial cells. Res. Microbiol. 142:985-993.
48. Weel, J. F. L., C. T. P. Hopman, and J. P. M. van Putten. 1991. Bacterial entry and intracellular processing of Neisseria gonorrhoeae in epithelial cells: immunomorphological evidence for alterations in the major outer membrane protein PI.B. J. Exp. Med. 174:705-715.