The development of a FACS-based strategy for the isolation of Shigella flexneri mutants that are deficient in intercellular spread

Molecular Microbiology

Volumn 35, Issue 5, 2000, Pages 974-990

  Rathman, Michelle ^a   Jouirhi, Noureddine ^b   Allaoui, Abdelmounaaïm ^b   Sansonetti, Philippe ^a   Parsot, Claude ^a   Van Nhieu, Guy Tran ^a  

^a INSERM   (France)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIUM LIPOPOLYSACCHARIDE;

ARTICLE; BACTERIAL GROWTH; BACTERIUM MUTANT; CELL INVASION; CILIARY MOTILITY; COLON MUCOSA; CONTROLLED STUDY; DISEASE COURSE; EPITHELIUM CELL; FLUORESCENCE ACTIVATED CELL SORTER; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; SHIGELLA FLEXNERI;

CACO-2 CELLS; CELL SEPARATION; FLOW CYTOMETRY; HUMANS; MICROSCOPY, ELECTRON; MUTATION; O ANTIGENS; SHIGELLA FLEXNERI;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; SHIGELLA FLEXNERI;

EID: 0034058860     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2000.01770.x     Document Type: Article

References (56)

1. Adam, T., Arpin, M., Prévost, M.-C., Gounon, P., and Sansonetti, P.J. (1995) Cytoskeletal rearrangements during entry of Shigella flexneri into HeLa cells. J Cell Biol 129: 367-381.
2. Alexander, D.C., and Valvano, M.A. (1994) Role of the rfe gene in the biosynthesis of the Escherichia coli O7-specific lipopolysaccharide and other O-specific polysaccharides containing N-acetylglucosamine. J Bacteriol 176: 7079-7084.
3. Alexeyev, M.F., and Shokolenko, I.N. (1995) Mini-Tn 10 transposon derivatives for insertion mutagenesis and gene delivery into the chromosome of Gram-negative bacteria. Gene 160: 59-62.
4. Allaoui, A., Ménard, R., Sansonetti, P.J., and Parsot, C. (1992) icsB: a Shigella flexneri virulence gene necessary for the lysis of protrusions during intercellular spread. Mol Microbiol 6: 1605-1616.
5. Anderson, D.M., and Schneewind, O. (1999) Type III machines of gram-negative pathogens: injecting virulence factors into host cells and more. Curr Opin Microbiol 2: 18-24.
6. Bârzu, S., Nato, F., Rouyre, S., Mazie, M.-C., Sansonetti, P., and Phallipon, A. (1993) Characterization of B-cell epitopes on IpaB, an invasion-associated antigen of Shigella flexneri: identification of an immunodominant domain recognized during natural infection. Infect Immun 61: 3825-3831.
7. Bernardini, M.L., Mounier, J., d'Hauteville, H., Coquis-Rondon, M., and Sansonetti, P.J. (1989) Identification of icsA, a plasmid locus of Shigella flexneri that governs bacterial intra-and intercellular spread through interaction with F-actin. Proc Natl Acad Sci USA 86: 3867-3871.
8. Bernardini, M.L., Sanna, M.G., Fontaine, A., and Sansonetti, P.J. (1993) OmpC is involved in invasion of epithelial cells by Shigella flexneri. Infect Immun 61: 3625-3635.
9. Bhuna, A.K., Ball, P.M., Fuad, A.T., Kurz, B.W., Emerson, J.W., and Johnson, M.G. (1991) Development and characterization of a monoclonal antibody specific for Listeria monocytogenes and Listeria innocua. Infect Immun 59: 3176-3184.
10. Blocker, A., Gounon, P., Larquet, E., Niehbuhr, K., Cabiaux, V., Parsot, C., and Sansonetti, P. (1999) The tripartite type III secretion of Shigella flexneri inserts IpaB and IpaC into host membranes. J Cell Biol 147: 683-693.
11. Bosch, L.V.D., Manning, P.A., and Morona, R. (1997) Regulation of O antigen chain length is required for Shigella flexneri virulence. Mol Microbiol 23: 765-775.
12. Clerc, P., and Sansonetti, P.J. (1987) Entry of Shigella flexneri into HeLa cells: evidence for directed phagocytosis involving actin polymerization and myosin accumulation. Infect Immun 55: 2681-2688.
13. Demers, B., Sansonetti, P.J., and Parsot, C. (1998) Induction of type III secretion in Shigella flexneri is associated with differential control of transcription of genes encoding secreted proteins. EMBO J 17: 2894-2903.
14. Heinrichs, D.E., Yethon, J.A., and Whitfield, C. (1998) Molecular basis for structural diversity in the core regions of the lipopolysaccharides of Escherichia coli and Salmonella enterica. Mol Microbiol 30: 221-232.
15. Hitchcock, P.J., and Brown, T.M. (1983) Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J Bacteriol 154: 269-277.
16. Hong, M., and Payne, S.M. (1997) Effect of mutations in Shigella flexneri chromosomal and plasmid-encoded lipopolysaccharide genes on invasion and serum resistance. Mol Microbiol 24: 779-791.
17. Kadurugamuwa, J.L., Rohde, M., Wehland, J., and Timmis, K.N. (1991) Intercellular spread of Shigella flexneri through a monolayer mediated by membranous protrusions and associated with reorganization of the cytoskeletal protein vinculin. Infect Immun 59: 3463-3471.
18. Kato, J., Ito, K., Nakamura, A., and Watanabe, H. (1989) Cloning of regions required for contact hemolysis and entry into LLC-MK2 cells from Shigella sonnei form I plasmid: VirF is a positive regulator gene for these phenotypes. Infect Immun 57: 1391-1398.
19. LaBrec, E.H., Schneider, H., Magnani, T.J., and Formal, S.B. (1964) Epithelial cell penetration as an essential step in the pathogenesis of bacillary dysentery. J Bacteriol 88: 1503-1518.
20. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
21. Lett, M.-C., Sasakawa, C., Okada, N., Sakai, T., Makino, S., Yamada, M., et al. (1989) virG, a plasmid-coded virulence gene of Shigella flexneri: identification of the virG protein and determination of the complete coding sequence. J Bacteriol 171: 353-359.
22. Makino, S., Sasakawa, C., Kamata, K., Kurata, T., and Yoshikawa, M. (1986) A genetic determinant required for continuous reinfection of adjacent cells on the large plasmid in S. flexneri 2a. Cell 46: 551-555.
23. Maurelli, A.T., Baudry, B., d'Hauteville, H., Hale, T.L., and Sansonetti, P.J. (1985) Cloning of plasmid DNA sequences involved in invasion of HeLa cells by Shigella flexneri. Infect Immun 49: 164-171.
24. Mecsas, J.J., and Strauss, E.J. (1996) Molecular mechanisms of bacterial virulence: type III secretion and pathogenicity islands. Emerg Infect Dis 2: 270-288.
25. Ménard, R., Sansonetti, P.J., and Parsot, C. (1993) Non polar mutagenesis of the ipa gene defines IpaB, IpaC and IpaD as effectors of Shigella flexneri entry into epithelial cells. J Bacteriol 175: 5899-5906.
26. Ménard, R., Sansonetti, P.J., and Parsot, C. (1994a) The secretion of the Shigella flexneri Ipa invasins is induced by epithelial cells and controlled by IpaB and IpaD. EMBO J 13: 5293-5302.
27. Ménard, R., Sansonetti, P.J., Parsot, C., and Vasselon, T. (1994b) The IpaB and IpaC invasins of Shigella flexneri associate in the extracellular medium and are partitioned in the cytoplasm by a specific chaperone. Cell 79: 515-525.
28. Ménard, R., Sansonetti, P.J., Parsot, C., and Vasselon, T. (1994c) Extracellular association and cytoplasmic partitioning of the IpaB and IpaC invasins of Shigella flexneri. Cell 79: 515-525.
29. Ménard, R., Dehio, C., and Sansonetti, P.J. (1996) Bacterial entry into epithelial cells: the paradigm of Shigella. Trends Microbiol 4: 220-226.
30. Mounier, J., Tyter, A., Coquis-Rondon, M., and Sansonetti, P.J. (1990) Intracellular spread of Listeria monocytogenes involves interaction with F-actin in the enterocyte cell line Caco-2. Infect Immun 58: 1048-1058.
31. Nakata, N., Sasakawa, C., Okada, N., Tobe, T., Fukuda, I., Suzuki, T., et al. (1992) Identification and characterization of virK, a virulence-associated large plasmid gene essential for intercellular spreading of Shigella flexneri. Mol Microbiol 6: 2387-2395.
32. Oaks, E., Wingfield, M., and Formal, S. (1985) Plaque formation by virulent Shigella flexneri. Infect Immun 48: 124-129.
33. Okada, N., Sasakawa, C., Tobe, T., Yamada, M., Nagai, S., Talukder, K.A., et al. (1991) Virulence-associated chromosomal loci of Shigella flexneri identified by random Tn5 insertion mutagenesis. Mol Microbiol 5: 187-195.
34. Okamura, N., Nagal, T., Nakaya, R., Kondo, S., Murakami, M., and Hisatsune, K. (1983) HeLa cell invasiveness and O antigen of Shigella flexneri as separate and prerequisite attributes of virulence to evoke keratoconjunctivitis in guinea pigs. Infect Immun 39: 505-512.
35. Page, A.-L., Ohayon, H., Sansonetti, P.J., and Parsot, C. (1999) The secreted IpaB and IpaC invasins and their cytoplasmic chaperone, IpgC, are required for intercellular dissemination of Shigella flexneri. Cell Microbiol 1: 183-193.
36. Phalipon, A., Arondel, J., Nato, F., Rouyre, S., Mazie, J.-C., and Sansonetti, P.J. (1992) Identification and characterizaion of B-cell epitopes of IpaC, an invasion-associated protein of Shigella flexneri. Infect Immun 60: 1919-1926.
37. Prévost, M.-C., Lesourd, M., Arpin, M., Vernel, F., Mounier, J., Hellio, R., and Sansonetti, P.J. (1992) Unipolar reorganization of F-actin layer at bacterial division and bundling of actin filaments by plastin correlate with movement of Shigella flexneri within HeLa cells. Infect Immun 60: 4088-4099.
38. Rajakumar, K., Jost, B.H., Sasakawa, C., Okada, N., Yoshikawa, M., and Adler, B. (1994) Nucleotide sequence of the rhamnose biosynthetic operon of Shigella flexneri 2a and role of lipopolysaccharide in virulence. J Bacteriol 176: 2362-2373.
39. Rick, P.D., Hubbard, G.L., and Barr, K. (1994) Role of the rfe gene in the synthesis of the O8 antigen in Escherichia coli K-12. J Bacteriol 176: 2877-2884.
40. Sakai, T., Sasakawa, C., and Yoshikawa, M. (1988) Expression of four virulence antigens of Shigella flexneri is positively regulated at the transcriptional level by the 30 kiloDalton VirF protein. Mol Microbiol 2: 589-597.
41. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual, 2nd edn. Ford, N., Nolan, C., and Ferguson, M. (eds). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
42. Sandlin, R.A., Lampel, K.A., Keasler, S.P., Goldberg, M.B., Stolzer, A.L., and Maurelli, A.T. (1995) Avirulence of rough mutants of Shigella flexneri: requirement of O antigen for correct unipolar localization of IcsA in the bacterial outer membrane. Infect Immun 63: 229-237.
43. Sansonetti, P.J., Mournier, J., Prévost, M.C., and Mège, R.M. (1994) Cadherin expression is required for the spread of Shigella flexneri between epithelial cells. Cell 76: 829-839.
44. Sasakawa, C., Kamata, K., Sakai, T., Makino, S., Yamada, M., Okada, N., and Yoshikawa, M. (1988) Virulence-associated genetic regions comprising 31 kilobases of the 230-kilobase plasmid in Shigella flexneri 2a. J Bacteriol 170: 2480-2484.
45. Schnaitman, C.A., and Klena, J.D. (1993) Genetics of lipopolysaccharide biosynthesis in enteric bacteria. Microbiol Rev 57: 655-682.
46. Sprott, G.D., Koval, S.F., and Schnaitman, C.A. (1994a) Generalized transduction in E. coli with phage P1. In Methods for General and Molecular Bacteriology. Gerhardt, P., Murray, R.G.E., Wood, WA, Krieg, N.R. (eds). Washington, DC: American Society of Microbiology, pp. 332-334.
47. Sprott, G.D., Koval, S.F., and Schnaitman, C.A. (1994b) Lipopolysachharide. In Methods for General and Molecular Bacteriology. Gerhardt, P., Murray, R.G.E., Wood, W.A., Krieg, N.R. (eds). Washington, DC: American Society of Microbiology, pp. 89-90.
48. Susuki, T., Murai, T., Fukuda, I., Tobe, T., Yoshikawa, M., and Sasakawa, C. (1994) Identification and characterization of a chromosomal virulence gene, vacJ, required for intercellular spreading of Shigella flexneri. Mol Microbiol 11: 31-41.
49. Takeuchi, S., Formal, S.B., and Sprinz, H. (1968) Experimental acute coliis in the rhesus monkey following peroral infection with Shigella flexneri. An electron microscope study. Am J Pathol 52: 503-529.
50. Tran Van Nhieu, G., Ben-Ze'ev, A., and Sansonetti, P.J. (1997) Modulation of bacterial entry into epithelial cells by association between vinvulin and the shigella IpaA invasin EMBO J 16: 2717-2729.
51. Tran Van Nhieu, G., Caron, E., Hall, A., and Sansonetti, P.J. (1999) IpaC induces actin polymerization and filopodia formation during Shigella entry into epithelial cells. EMBO J 18: 3249-3262.
52. Uchiya, K., Tobe, T., Komatsu, K., Suzuki, T., Watarai, M., Fukuda, I., et al. (1995) Identification of a novel virulence gene, virA, on the large plasmid of Shigella involved in invasion and intercellular spreading. Mol Microbiol 17: 241-250.
53. Valdivia, R.H., and Falkow, S. (1996) Bacterial genetics by flow cytometry: rapid isolation of Salmonella typhimurium acid-inducible promoters by differential fluorescence induction. Mol Microbiol 22: 367-378.
54. Vasselon, T.J., Mounier, M., Prevost, M.C., Hellio, R., and Sansonetti, P.J. (1991) Stress fiber-based movement of Shigella flexneri within cells. Infect Immun 59: 1723-1732.
55. Vasselon, T., Mounier, J., Hellio, R., and Sansonetti, P.J. (1992) Movement along actin filaments of the perijunctional area and de novo polymerization of cellular actin are required for Shigella flexneri colonizaion of epithelial Caco-2 cell monolayers. Infect Immun 60: 1031-1040.
56. Watarai, M., Tobe, T., Yoshikawa, M., and Sasakawa, C. (1995) Contact of Shigella with host cells triggers release of Ipa invasins and is an essential function of invasiveness. EMBO J 14: 2461-2470.