Physical limitations on Salmonella typhi entry into cultured human intestinal epithelial cells

Infection and Immunity

Volumn 66, Issue 6, 1998, Pages 2928-2937

  Huang, Xiao Zhe ^a   Tall, Ben ^b   Schwan, William R ^a,d   Kopecko, Dennis J ^a,c  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; INTERNALIZATION; INTESTINE BRUSH BORDER; INTESTINE EPITHELIUM CELL; PRIORITY JOURNAL; SALMONELLA TYPHI; SCANNING ELECTRON MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY;

EID: 0031812340     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.66.6.2928-2937.1998     Document Type: Article

References (46)

1. Alpuche-Aranda, C. M., E. L. Kacoosin, J. A. Swanson, and S. I. Miller. 1994. Salmonella stimulate macrophage macropinocytosis and persist within spacious phagosomes. J. Exp. Med. 179:601-608.
2. Behlau, I., and S. I. Miller. 1993. A PhoP-repressed gene promotes Salmonella typhimurium invasion of epithelial cells. J. Bacteriol. 175:4475-4484.
3. Clark, E. A., and J. S. Brugge. 1995. Integrins and signal transduction pathway: the road taken. Science 268:232-239.
4. Elsinghorst, E., L. S. Baron, and D. J. Kopecko. 1989. Penetration of human intestinal epithelial cells by Salmonella: molecular cloning and expression of S. typhi invasion determinants in Escherichia coli. Proc. Natl. Acad. Sci. USA 86:5173-5177.
5. Finlay, B. B. 1994. Molecular and cellular mechanisms of Salmonella pathogenesis. Curr. Top. Microbiol. 192:163-185.
6. Finlay, B. B. 1995. Interactions between Salmonella typhimurium, enteropathogenic Escherichia coli (EPEC), and host epithelial cells. Adv. Dent. Res. 9:31-36.
7. Finlay, B. B., and S. Falkow. 1990. Salmonella interactions with polarized human intestinal Caco-2 epithelial cells. J. Infect. Dis. 162:1096-1106.
8. Finlay, B. B., B. Gumbiner, and S. Falkow. 1988. Penetration of Salmonella through a polarized Madin-Darby canine kidney epithelial cell monolayer. J. Cell Biol. 107:221-230.
9. Finlay, B. B., S. Chatfield, K. Y. Leung, G. Dougan, and S. Falkow. 1991. Characterization of a Salmonella choleraesuis mutant that can not multiply within epithelial cells. Can. J. Microbiol. 37:568-672.
10. Francis, C. L., T. A. Ryan, B. D. Jones, S. J. Smith, and S. Falkow. 1993. Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature 364:639-642.
11. Galán, J. E. 1994. Interaction of bacteria with non-phagocytic cells. Curr. Opin. Immunol. 6:590-595.
12. Galán, J. E. 1996. Molecular genetic bases of Salmonella entry into host cells. Mol. Microbiol. 20:263-271.
13. Galán, J. E., and R. Curtiss III. 1991. Distribution of the invA, -B, -C, and -D genes of Salmonella typhimurium among other Salmonella serovars: invA mutants of Salmonella typhi are deficient for entry into mammalian cells. Infect. Immun. 59:2901-2908.
14. Ginocchio, C., J. Pace, and J. E. Galán. 1992. Identification and molecular characterization of a Salmonella typhimurium gene involved in triggering the internalization of Salmonella into cultured epithelial cells. Proc. Natl. Acad. Sci. USA 89:5976-5980.
15. Ginocchio, C. C., S. B. Olmsted, C. L. Wells, and J. E. Galán. 1994. Contact with epithelial cells induces the formation of surface appendages on S. typhimurium. Cell 76:717-724.
16. Holt, J. G., N. R. Krieg, P. H. A. Sneath, J. T. Staley, and S. T. Williams. 1994. Genus Salmonella, p. 175-289. In W. R. Hensyl (ed.), Bergey's manual of determinative bacteriology, 9th ed. The Williams & Wilkins Co., Baltimore. Md.
17. Hueck, C. J., M. J. Hantman, V. Bajaj, C. Johnston, C. A. Lee, and S. Miller. 1995. Salmonella typhimurium secreted invasion determinants are homologous to Shigella Ipa proteins. Mol. Microbiol. 18:479-490.
18. Isberg, R. R., and J. M. Leong. 1990. Multiple β1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration in mammalian cells. Cell 60:861-871.
19. Isberg, R. R., and G. T. V. Nhieu. 1994. Two mammalian cell internalization strategies used by pathogenic bacteria. Annu. Rev. Genet. 27:395-422.
20. Kihlstrom, E. 1977. Infection of HeLa cells with Salmonella typhimurium 395 MS and MR10 bacteria. Infect. Immun. 17:290-295.
21. Kohbata, S., H. Yokoyama, and E. Yabuuchi. 1986. Cytopathogenic effect of Salmonella typhi GIFU 10007 on M cells of murine ileal Peyer's patches in ligated ileal loops: an ultrastructural study. Microbiol. Immunol. 30:1225-1237.
22. Kusters, J. G., G. A. W. M. Mulders-Kremers, C. E. M. van Doornik, and B. A. M. van der Zeijst. 1993. Effects of multiplicity of infection, bacterial protein synthesis, and growth phase on adhesion to and invasion of human cell lines by Salmonella typhimurium. Infect. Immun. 61:5013-5020.
23. 21a.Lamont, R. J., A. Chan, C. M. Belton, K. T. Izutsu, D. Vasel, and A. Weinberg. 1995. Porphyromonas gingivalis invasion of gingival epithelial cells. Infect. Immun. 63:3878-3885.
24. Lee, C. A., B. D. Jones, and S. Falkow. 1992. Identification of a Salmonella typhimurium invasion locus by selection for hyperinvasive mutant. Proc. Natl. Acad. Sci. USA 89:1847-1851.
25. Makino, S., J. P. 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.
26. Mengaud, J., H. Ohayon, P. Gounon, R.-M. Mege, and P. Cossart. 1996. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84:923-932.
27. Miliotis, M. D. 1991. Acridine orange stain for determining intracellular enteropathogens in HeLa cell. J. Clin. Microbiol. 29:830-831.
28. Miliotis, M. D., H. J. Koornhof, and J. I. Phillips. 1989. Invasive potential of noncytotoxic enteropathogenic Escherichia coli in an in vitro Henle 407 cell model. Infect. Immun. 57:1928-1935.
29. Miliotis, M. D., B. D. Tall, and R. T. Gray. 1995. Adherence to and invasion of tissue culture cells by Vibrio hollisae. Infect. Immun. 63:4959-4963.
30. Mills, S. D., and B. B. Finlay. 1994. Comparison of Salmonella typhi and Salmonella typhimurium invasion, intracellular growth and localization in cultured human epithelial cells. Microb. Pathog. 17:409-423.
31. Monack, D. M., B. Raupach, A. E. Hromockyj, and S. Falkow. 1996. Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc. Natl. Acad. Sci. USA 93:9833-9838.
32. Mroczenski-Wildey, M. J., J. L. Di Fabio, and F. C. Cabello. 1989. Invasion analysis of Hela cell monolayers by Salmonella typhi: the role of lipopolysaccharide. Microb. Pathog. 6:143-152.
33. Oelschlaeger, T. A., and B. D. Tall. 1996. Uptake pathways of clinical isolates of Proteus mirabilis into human epithelial cells. Microb. Pathog. 20:1-16.
34. Oelschlaeger, T. A., T. J. Barrett, and D. J. Kopecko. 1994. Some structures and processes of human epithelial cells involved in uptake of enterohemorrhagic Escherichia coli O157:H7 strains. Infect. Immun. 62:5142-5150.
35. Oelschlaeger, T. A., P. Guerry, and D. J. Kopecko. 1993. Unusual microtubule-dependent endocytosis mechanisms triggered by Campylobacter jejuni and Citrobacter freundii. Proc. Natl. Acad. Sci. USA 90:6684-6688.
36. Ogawa, H., A. Nakamura, and R. Nakaya. 1968. Cinemicrographic study of tissue cell cultures infected with Shigella flexneri. Jpn. J. Med. Sci. Biol. 21:259-273.
37. Pang, T., Z. A. Bhutta, B. B. Finlay, and M. Altwegg. 1995. Typhoid fever and other salmonelloses: a continuing challenge. Trends Microbiol. 3:253-255.
38. Pegues, D. A., M. J. Hantman, I. Behlau, and S. I. Miller. 1995. PhoP/PhoQ transcriptional repression of Salmonella typhimurium invasion genes: evidence for a role in protein secretion. Mol. Microbiol. 17:169-181.
39. Portillo, F. G., and B. B. Finlay. 1994. Salmonella invasion of nonphagocytic cells induces formation of macropinosomes in the host cell. Infect. Immun. 62:4641-4645.
40. Takeuchi, A. 1967. Electron microscope studies of experimental Salmonella infection. Penetration into the intestinal epithelium by Salmonella typhimurium. Am. J. Pathol. 50:109-136.
41. Tall, B. D., R. T. Gray, and D. B. Shah. 1993. Bacterial adherence and biofilm behavior of Vibrio vulnificus, p. 378-379. In G. W. Bailey and C. L. Rieder (ed.), Proceedings of the Annual Meeting of the Microscopy Society of America. San Francisco Press, Inc., San Francisco, Calif.
42. Tartera, C., and E. Metcalf. 1993. Osmolarity and growth phase overlap in regulation of Salmonella typhi adherence to and invasion of human intestinal cells. Infect. Immun. 61:3084-3089.
43. Watarai, M., S. Funato, and C. Sasakawa. 1996. Interaction of Ipa proteins of Shigella flexneri with α5β1 integrin promotes entry of the bacteria into mammalian cells. J. Exp. Med. 183:991-999.
44. Yabuuchi, E., M. Ikedo, and T. Ezaki. 1986. Invasiveness of Salmonella typhi strains in Hela S3 monolayer cells. Microbiol. Immunol. 30:1213-1224.
45. Yokoyama, H., M. Ikedo, and S. Kohbata. 1987. An ultrastructural study of Hela cell invasion with Salmonella typhi GIFU 10007. Microbiol. Immunol. 31:1-11.
46. Zaidi, T. S., M. Grout, C. Lee, and G. B. Pier. 1997. Salmonella typhi, but not S. typhimurium, enters epithelial cells via the cystic fihrosis transmembrane conductance regulator (CFTR), abstr. D-98, p. 225. In Abstracts of the 97th General Meeting of the American Society for Microbiology 1997. American Society for Microbiology, Washington, D.C.