Natural proteoglycan receptor analogs determine the dynamics of Opa adhesin-mediated gonococcal infection of Chang epithelial cells

Infection and Immunity

Volumn 65, Issue 12, 1997, Pages 5028-5034

  Van Putten, Jos P M ^a   Hayes, Stanley F ^a   Duensing, Thomas D ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; HEPARIN BINDING PROTEIN;

ARTICLE; BACTERIUM ADHERENCE; ELECTRON MICROSCOPY; EPITHELIUM CELL; GENETIC VARIABILITY; GONORRHEA; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; RECEPTOR BINDING;

EID: 0030780595     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.65.12.5028-5034.1997     Document Type: Article

References (47)

1. Apicella, M. A., M. Ketterer, F. K. N. Lee, D. Zhou, 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. 162:636-646.
2. Barritt, D. S., R. S. Schwalbe, D. G. Klapper, and J. G. Cannon. 1987. Antigenic and structural differences among six proteins II expressed by a single strain of Neisseria gonorrhoeae. Infect. Immun. 55:2026-2031.
3. 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.
4. Bos, M. P., F. Grunert, and R. J. Belland. 1997. Differential recognition of members of the carcinoembryonic antigen family by Opa variants of Neisseria gonorrhoeae. Infect. Immun. 65:2353-2361.
5. Chen, J. C. R., P. Bavoil, and V. L. Clark. 1991. Enhancement of the invasive ability of Neisseria gonorrhoeae by contact with Hec1B, an adenocarcinoma endometrial cell line. Mol. Microbiol. 5:1531-1538.
6. Chen, T., and E. C. Gotschlich. 1996. CGM1a antigen of neutrophils, a receptor of gonococcal opacity proteins. Proc. Natl. Acad. Sci. USA 93:14851-14856.
7. Chen, T., F. Grunert, A. Medina-Marino, and E. C. Gotschlich. 1997. Several carcinoembryonic antigens (CD66) serve as receptors for gonococcal opacity proteins. J. Exp. Med. 185:1557-1564.
8. 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.
9. Connell, T. D., D. Shaffer, and J. G. Cannon. 1990. Characterization of the repertoire of hypervariable regions in the protein II (opa) gene family of Neisseria gonorrhoeae. Mol. Microbiol. 4:439-449.
10. Dalton, J. P., D. Hudson, J. H. Adams, and L. H. Miller. 1991. Blocking of the receptor-mediated invasion of erythrocytes by Plasmodium knowlesi malaria with sulfated polysaccharides and glycosaminoglycans. Eur. J. Biochem. 195:789-794.
11. De Moreno, M. R., J. F. Smith, and R. V. Smith. 1985. Silver staining of proteins in polyacrylamide gels: increased sensitivity through a combined Coomassie blue-silver stain procedure. Anal. Biochem. 151:466-470.
12. De Vries, F. P., A. van den Ende, J. P. M. van Putten, and J. Dankert. 1996. Invasion of primary nasopharyngeal cells by Neisseria meningitidis is controlled by phase variation of multiple surface antigens. Infect. Immun. 64:2998-3006.
13. Duckworth, M., and W. Yaphe. 1971. The structure of agar. Carbohydr. Res. 16:189-197.
14. Ernst, R. K., D. M. Dombroski, and J. M. Merrick. 1990. Anaerobiosis, type 1 fimbriae, and growth phase are factors that affect invasion of HEp-2 cells by Salmonella typhimurium. Infect. Immun. 58:2014-2016.
15. Evans, B. A. 1977. Ultrastructural study of cervical gonorrhoea. J. Infect. Dis. 136:248-255.
16. Francis, C. L., M. N. Starnbach, and S. Falkow. 1992. Morphological and cytoskeletal changes in epithelial cells occur immediately upon interaction with Salmonella typhimurium grown under low-oxygen conditions. Mol. Microbiol. 6:3077-3087.
17. Gill, M., D. P. McQuillen, J. P. M. van Putten, L. M. Wetzler, J. Bramley, H. Crooke, N. J. Parsons, J. A. Cole, and H. Smith. 1996. Functional characterization of a sialyltransferase-deficient mutant of Neisseria gonorrhoeae. Infect. Immun. 64:3374-3378.
18. Ginocchio, C. C., S. B. Olmsted, C. L. Wells, and J. E. Galan. 1994. Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium. Cell 76:717-724.
19. 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.
20. Hendley, J. O., K. R. Powell, R. D. Odenwald, H. H. Holzgrefe, and R. Lyles. 1977. Demonstration of a capsule on Neisseria gonorrhoeae. N. Engl. J. Med. 296:608-611.
21. James, J. F., and J. Swanson. 1977. The capsule of the gonococcus. J. Exp. Med. 145:1082-1086.
22. Jarvis, G. A., and N. A. Vedros. 1987. Sialic acid of group B Neisseria meningitidis regulates alternative complement pathway activation. Infect. Immun. 55:174-180.
23. Kahrs, A. F., A. Bihlmaier, D. Facius, and T. F. Meyer. 1994. Generalized transposon shuttle mutagenesis in Neisseria gonorrhoeae: a method for isolating epithelial cell invasion-defective mutants. Mol. Microbiol. 12:819-831.
24. Kupsch, E. M., B. Knepper, T. Kuroki, I. Heuer, and T. F. Meyer. 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.
25. Lee, C. A., and S. Falkow. 1990. The ability of Salmonella to enter mammalian cells is affected by bacterial growth state. Proc. Natl. Acad. Sci. USA 87:4304-4308.
26. Makino, S., 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.
27. Meyer, T. F., J. Pohlner, and J. P. M. van Putten. 1994. Biology of the pathogenic neisseriae. Curr. Top. Microbiol. Immunol. 192:283-317.
28. Murphy, G. L., T. D. Connell, D. S. Barrit, M. Koomey, and J. G. Cannon. 1989. Phase variation of gonococcal protein II: regulation of a gene expression by slipped-strand mispairing of a repetitive DNA sequence. Cell 56:539-547.
29. Nassif, X., and M. So. 1995. Interaction of pathogenic neisseriae with nonphagocytic cells. Clin. Microbiol. Rev. 8:376-388.
30. Neyts, J., R. Snoeck, D. Schols, J. Balzarini, J. D. Esko, A. Van Schepdael, and E. De Clercq. 1992. Sulfated polymers inhibit the interaction of human cytomegalovirus with cell surface heparan sulfate. Virology 189:48-58.
31. Rudel, T., I. Scheuerpflug, and T. F. Meyer. 1995. Neisseria PilC protein identified as type-4 pilus tip-located adhesin. Nature 373:357-359.
32. Schiemann, D. A. 1995. Association with MDCK epithelial cells by Salmonella typhimurium is reduced during utilization of carbohydrates. Infect. Immun. 63:1462-1467.
33. Simon, D., and R. F. Rest. 1992. Escherichia coli expressing Neisseria gonorrhoeae opacity-associated outer membrane protein invade human cervical and endometrial epithelial cells. Proc. Natl. Acad. Sci. USA 89:5512-5516.
34. Stern, A., M. Brown, P. Nickel, and T. F. Meyer. 1987. Opacity genes in Neisseria gonorrhoeae: control of phase and antigenic variation. Cell 47:61-72.
35. Swanson, J., S. A. Hill, and S. H. Fischer. 1994. Growth on different solid media markedly affects the properties and behaviors of Opa+ gonococci, p. 771-776. In C. J. Conde-Glez, S. Morse, P. Rice, F. Sparling, and E. Caldéron (ed.), Pathobiology and immunobiology of Neisseriaceae. Instituto Nacional de Salud Publica, Cuernavaca, Mexico.
36. Swanson, J. 1994. Some Opa+ gonococci acquire a DNA 'capsule,' p. 587-593. In C. J. Conde-Glez, S. Morse, P. Rice, F. Sparling, and E. Caldéron (ed.), Pathobiology and immunobology of Neisseriaceae. Instituto Nacional de Salud Publica, Cuernavaca, Mexico.
37. Swanson, J. 1991. Effects of Opa proteins and lipooligosaccharides on surface charge and biological behavior of gonococci, p. 109-125. In C. I. Kado and J. H. Crosa (ed.), Molecular mechanisms of bacterial virulence. Kluwer Academic Publishers, Dordrecht, The Netherlands.
38. 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.
39. van Putten, J. P. M., J. F. L. Weel, and H. U. C. Grassmé. 1994. Measurements of invasion by antibody labeling and electron microscopy. Methods Enzymol. 236:420-437.
40. van Putten, J. P. M., and S. M. Paul. 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. van Putten, J. P. M., and T. D. Duensing. 1997. Infection of mucosal epithelial cells by Neisseria gonorrhoeae. Rev. Med. Microbiol. 8:51-59.
42. Virji, M., K. Makepeace, D. J. Ferguson, M. Achtman, and E. R. Moxon. 1993. Meningococcal Opa and Ope proteins: their role in colonization and invasion of human epithelial and endothelial cells. Mol. Microbiol. 10:499-510.
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. 29:941-950.
44. Ward, M. E., J. N. Robertson, P. M. Englefield, and P. J. Watt. 1975. Gonococcal infection: invasion of the mucosal surfaces of the genital tract, p. 188-199. In D. Schlessinger (ed.). Microbiology - 1975. American Society for Microbiology, Washington, D.C.
45. Weel, J. F. L., C. T. P. Hopman, and J. P. M. van Putten. 1991. In situ expression and localization of Neisseria gonorrhoeae opacity proteins in infected epithelial cells: apparent role of Opa proteins in cellular invasion. J. Exp. Med. 173:1395-1405.
46. Young, V. B., S. Falkow, and G. K. Schoolnik. 1992. The invasin protein of Yersinia enterocolitica: internalization of invasin-bearing bacteria by eukaryotic cells is associated with reorganization of the cytoskeleton. J. Cell Biol. 116:197-207.
47. Zaretsky, F. R., R. Pearce-Pratt, and D. M. Phillips. 1995. Sulfated polyanions block Chlamydia trachomatis infection of cervix-derived human epithelia. Infect. Immun. 63:3520-3526.