Membrane ruffling and invasion of human and avian cell lines is reduced for aflagellate mutants of Salmonella enterica serotype Enteritidis

International Journal of Medical Microbiology

Volumn 293, Issue 4, 2003, Pages 261-272

  La Ragione, Roberto M ^a   Cooley, William A ^a   Velge, Philippe ^b   Jepson, Mark A ^c   Woodward, Martin J ^a  

^a VETERINARY LABORATORIES AGENCY   (United Kingdom)

^b CEMAGREF   (France)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Adherence; Flagella; Invasion; Ruffles; Salmonella enterica serotype Enteritidis

Indexed keywords

ALLELE; ANIMAL CELL; ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL STRAIN; BACTERIUM MUTANT; CELL LINE; CONFOCAL MICROSCOPY; CYTOSKELETON; ELECTRON MICROSCOPY; FOWL; HUMAN; HUMAN CELL; HYPOTHESIS; NONHUMAN; PHENOTYPE; SALMONELLA ENTERICA; SALMONELLA ENTERITIDIS; SEROTYPE; WILD TYPE;

EID: 0041424879     PISSN: 14384221     EISSN: None     Source Type: Journal    
DOI: 10.1078/1438-4221-00263     Document Type: Article

References (41)

1. Adler, J., Templeton, B.: The effect of environmental conditions on the motility of Escherichia coli. J. Gen. Microbiol. 446, 175-184 (1967).
2. Allen-Vercoe, E., Woodward, M. J.: Adherence of Salmonella enterica serovar Enteritidis to chick gut explant; the role of flagella but not fimbriae. J. Med. Microbiol. 48, 771-780 (1999).
3. Allen-Vercoe, E. Sayers, A. R., Woodward, M. J.: Virulence of Salmonella enterica serovar Enteritidis aflagellate and afimbriate mutants in the day old chick. Epidemiol. Infect. 122, 395-402 (1999).
4. Carsiotis, M., Stocker, B. A. D., Weinstein, D. L., O'Brien, A. D.: A Salmonella virulence gene linked to flg. Infect. Immun. 57, 3276-3280 (1989).
5. Ciacci-Woolwine, F., Blomfield, I. C., Richardson, S. H., Mizel, S. B.: Salmonella flagellin induces tumor necrosis factor alpha in a human promonocytic cell line. Infect. Immun. 66, 1127-1134 (1998).
6. Clark, M. A., Hirst, B. H., Jepson, M. A.: Inoculum composition and Salmonella pathogenicity island 1 regulate M cell invasion and epithelial destruction by Salmonella typhimurium. Infect. Immun. 66, 724-731 (1998).
7. Dibb-Fuller, M., Allen-Vercoe, E., Thorns, C. J., Woodward, M. J.: Characterisation of fimbrial and flagella mediated adherence to and invasion of INT407 monolayers by Salmonella enterica serotype Enteritidis. Microbiology 145, 1023-1031 (1999).
8. Dorman, C. J.: DNA supercoiling and environmental regulation of gene expression of pathogenic bacteria. Infect. Immun. 59, 745-749 (1991).
9. Eaves-Pyles, T., Murthy, K., Liaudet, L., Virag, L., Ross, G., Soriano, F. G., Szabo, C., Salzman, A. L.: Flagellin, a novel mediator of Salmonella-induced epithelial activation and systemic inflammation: I kappa B alpha degradation, induction of nitric oxide synthase, induction of proinflammatory mediators, and cardiovascular dysfunction. J. Immunol. 166, 1248-1260 (2001).
10. Eaves-Pyles, T., Szabo, C., Salzman, A. L.: Bacterial invasion is not required for activation of NF-kappaB in enterocytes. Infect. Immun. 67, 800-804 (1999).
11. 28) regulates the expression of Salmonella genes associated with the centisome 63 type III secretion system. Infect. Immun. 68, 2735-2743 (2000).
12. Francis, C. L., Ryan, T. A., Jones, B. D., Smith, S. J., Falkow, S.: Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature 364, 639-642 (1993).
13. Galan, J. E., Curtiss, R. D.: Cloning and molecular characterisation of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc. Natl. Acad. Sci. USA 68, 6383-6387 (1989).
14. Galan, J. E., Zhou, D.: Striking a balance: Modulation of the actin cytoskeleton by Salmonella. Proc. Natl. Acad. Sci. USA 97, 8754-8761 (2000).
15. Gewirtz, A. T., Simon, P. O. Jr., Schmitt, C. K., Taylor, L. J., Hagedorn, C. H., O'Brien, A. D., Neish, A. S., Madara, J. L.: Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J. Clin. Invest. 107, 99-109 (2001a).
16. Gewirtz, A. T., Navas, T. A., Lyons, S., Godowski, P. J., Madara, J. L.: Cutting edge: bacterial flagellin activates basolaterally expressed tlr5 to induce epithelial proinflammatory gene expression. J. Immunol. 167, 1882-1885 (2001b).
17. Guard-Petter, J., Keller, L. H., Rahman, M. M., Carlson, R. W., Silvers, S.: A novel relationship between O-antigen variation, matrix formation and invasiveness of Salmonella enteritidis. Epidemiol. Infect. 117, 219-231 (1996).
18. Hansen-Wester, I., Hensel, M.: Salmonella pathogenicity islands encoding type III secretion systems. Microbes Infect. 3, 549-559 (2001).
19. Iyoda, S., Kamaidoi, T., Hirose, K., Kutsukake, K., Watanabe, H.: A flagellar gene fliZ regulates the expression of invasion genes and virulence phenotype in Salmonella enterica serovar Typhimurium. Microb. Pathog. 30, 81-90 (2001).
20. Jepson, M. A., Lang, T. F., Reed, K. A., Simmons, N. L.: Evidence for a rapid, direct effect on epithelial monolayer integrity and transepithelial transport in response to Salmonella invasion. Pflügers Archiv Eur. J. Physiol. 432, 225-233 (1996).
21. Jepson, M. A., Kenny, B., Leard, A. D.: Role of sipA in the early stages of Salmonella typhimurium entry into epithelial cells. Cell. Microbiol. 3, 417-426 (2001).
22. Jones, B. D., Lee, C. A., Falkow, S.: Invasion by Salmonella typhimurium is affected by the direction of flagellar rotation. Infect. Immun. 60, 2475-2480 (1992).
23. Jones, G. W., Richardson, L. A., Uhlman, D.: The invasion of HeLa cells by Salmonella typhimurium: reversible and irreversible bacterial attachment and the role of bacterial motility. J. Gen. Microbiol. 127, 351-360 (1981).
24. Kerridge, D.: The effect of the environment on the formation of bacterial flagella. In: Microbial reactions in the environment, Society of General Microbiology special publication. Cambridge University Press, Cambridge, UK, pp 41-68 (1961).
25. Khoramian-Falsafi, T., Harayama, S., Kutsukake, K., Pechere, J. C.: Effect of motility and chemotaxis on the invasion of Salmonella Typhimurium into HeLa cells. Microb. Pathog. 9, 47-53 (1990).
26. Komoriya, K., Shibano, N., Higano, T., Azuma, N., Yamaguchi, S., Aizawa, S. I.: Flagellar proteins and type III-exported virulence factors are the predominant proteins secreted into the culture media of Salmonella typhimurium. Mol. Microbiol. 34, 767-779 (1999).
27. Liu, S. L., Ezaki, T., Miura, H., Matsui, K., Yabuuchi, E.: Intact motility as a Salmonella typhi invasion-related factor. Infect. Immun. 56, 1967-1973 (1988).
28. Lillard, H. S.: Role of fimbriae and flagella in the attachment of Salmonella typhimurium to poultry skin. J. Food Sci. 51, 54-57 (1986).
29. Parker, C. T., Guard-Petter, J.: Contribution of flagella and invasion proteins to pathogenesis of Salmonella enterica serovar enteritidis in chicks. FEMS Microbiol. Lett. 204, 287-291 (2001).
30. Robertson, J. M. C., Grant, G., Allen-Vercoe, E., Woodward, M. J., Putsai, A., Flint, H. J.: Adhesion of Salmonella enterica var Enteritidis strains lacking fimbriae and flagella to rat ileal explants cultured at the air interface or submerged in tissue culture medium. J. Med. Microbiol. 49, 691-696 (2000).
31. Robertson, J. M. C., Grant, G., Allen-Vercoe, E., Woodward, M. J., Putzai, A., Flint, N. J.: Lack of functional flagella disadvantages Salmonella enterica var Enteritidis in the rat. J. Med. Microbiol. 52, 91-99 (2003).
32. Schechter, L. M., Lee, C. A.: Salmonella invasion of nonphagocytic cells. Subcell. Biochem. 33, 289-320 (2000).
33. Schmitt, C. K., Ikeda, J. S., Darnell, S. C., Watson, P. R., Bispham, J., Wallis, T. S., Weinstein, D. L., Metcalf, E. S., O'Brien, A. D.: Absence of all components of the flagellar export and synthesis machinery differentially alters virulence of Salmonella enterica serovar Typhimurium in models of typhoid fever, survival in macrophages, tissue culture invasiveness, and calf enterocolitis. Infect. Immun. 69, 5619-5625 (2001).
34. Steiner, T. S., Nataro, J. P., Poteet-Smith, C. E., Smith, J. A., Guerrant, R. L.: Enteroaggregative Escherichia coli expresses a novel flagellin that causes IL-8 release from intestinal epithelial cells. J. Clin. Invest. 105, 1769-1777 (2000).
35. Sukhan, A.: The invasion-associated type III secretion system of Salmonella typhimurium: common and unique features. Cell. Mol. Life Sci. 57, 1033-1049 (2000).
36. Uhlman, D., Jones, G. W.: Chemotaxis as a factor in the interactions between HeLa cells and Salmonella typhimurium. J. Gen. Microbiol. 128, 415-418 (1982).
37. Van Asten, F. J. A. M., Hendriks, H. G. C. J. M., Koninkx, J. F. J. G., Van der Zeijst, B. A. B., Gaastra, W.: Inactivation of the flagellin gene of Salmonella enterica serotype Enteritidis strongly reduces invasion into differentiated Caco-2 cells. FEMS Microbiol. Lett. 185, 175-179 (2000).
38. Velge, P., Bottreau, E., Quere, P., Pardon, P., Nicolle, J. C., Morrison, M., Bout, D., Dimier, I.: Establishment and characterisation of partially differentiated chicken enterocyte cell clones. Eur. J. Cell Biol. 81, 203-212 (2002).
39. Walker, S. L., Sojka, M., Dibb-Fuller, M., Woodward, M. J.: Effect of pH, temperature and surface contact on the elaboration of fimbriae and flagella by Salmonella enterica serotype Enteritidis. J. Med. Microbiol. 48, 1-9 (1999).
40. Weinstein, D. L., Carsiotis, M., Lissner, C. R., O'Brien, A. D.: Flagella help Salmonella typhimurium survive within murine macrophages. Infect. Immun. 46, 819-825 (1984).
41. Zhou, D., Mooseker, M. S., Galan, J. E.: Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science 283, 2092-2095 (1999).