The RcsB-RcsC regulatory system of Salmonella typhi differentially modulates the expression of invasion proteins, flagellin and Vi antigen in response to osmolarity

Molecular Microbiology

Volumn 29, Issue 3, 1998, Pages 835-850

  Arricau, Nathalie ^a   Hermant, Daniel ^a   Waxin, Hervé ^a   Ecobichon, Chantal ^a   Duffey, Paul S ^b   Popoff, Michel Y ^a  

^a INSTITUT PASTEUR   (France)

^b CALIFORNIA DEPARTMENT OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLIN;

ANTIGENICITY; ARTICLE; GENE EXPRESSION REGULATION; INTESTINE EPITHELIUM CELL; OSMOLARITY; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN SECRETION; SALMONELLA TYPHI;

ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CELL MEMBRANE; FLAGELLIN; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; MULTIENZYME COMPLEXES; OSMOLAR CONCENTRATION; PHOSPHOPROTEIN PHOSPHATASE; POLYSACCHARIDES, BACTERIAL; PROTEIN KINASES; SALMONELLA TYPHI; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; VIRULENCE FACTORS;

NEGIBACTERIA; SALMONELLA TYPHI;

EID: 0031928463     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1998.00976.x     Document Type: Article

References (76)

1. Alpuche-Aranda, C.M., Swanson, J.A., Loomis, W.P., and Miller, S.I. (1992) Salmonella typhimurium activates virulence gene transcription within acidified macrophage phagosomes. Proc Natl Acad Sci USA 89: 10079-10083.
2. Altmeyer, R.M., McNern, J.K., Bossio, J.C., Rosenshine, I., Finlay, B.B., and Galan, J.E. (1993) Cloning and molecular characterization of a gene involved in Salmonella adherence and invasion of cultured epithelial cells. Mol Microbiol 7: 89-98.
3. Arricau, N., Hermant, D., Waxin, H., and Popoff, M.Y. (1997) Molecular characterization of the Salmonella typhi StpA protein that is related to both Yersinia YopE cytotoxin and YopH tyrosine phosphatase. Res Microbiol 148: 21-26.
4. Bajaj, V., Hwang, C., and Lee, C.A. (1995) hilA is a novel ompR/toxR family member that activates the expression of Salmonella typhimurium invasion genes. Mol Microbiol 18: 715-727.
5. Bajaj, V., Lucas, R.L., Hwang, C., and Lee, C.A. (1996) Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol Microbiol 22: 703-714.
6. Behlau, I., and Miller, S.I. (1993) A PhoP-repressed gene promotes Salmonella typhimurium invasion of epithelial cells. J Bacteriol 175: 4475-4484.
7. Betts, J., and Finlay, B.B. (1992) Identification of Salmonella typhimurium invasiveness loci. Can J Microbiol 38: 852-857.
8. Birnboim, H.C., and Doly, J. (1979) A rapid alkaline procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7: 1513-1523.
9. Casadaban, M., and Cohen, S.N. (1980) Analysis of a gene control signal by DNA fusion and cloning in E. coli. J Mol Biol 138: 179-207.
10. Cerquetti, M.C., and Hooke, A.M. (1993) Vi I typing phage for generalized transduction of Salmonella typhi. J Bacteriol 175: 5294-5296.
11. Chen, L.M., Kaniga, K., and Galan, J.E. (1996) Salmonella spp. are cytotoxic for cultured macrophages. Mol Microbiol 21: 1101-1115.
12. Collazo, C.M., and Galan, J.E. (1996) Requirement for exported proteins in secretion through the invasion-associated type III system of Salmonella typhimurium. Infect Immun 64: 3524-3531.
13. Duffey, P.S., Kani, J.C., Lee, J.O., Hill, W.J., and Kokka, R. (1992) Salmonella serogroups C2 and C3 identified by agglutination using an immunoglobulin G3 (κ) monoclonal antibody (32-1-E3) reactive with somatic factor-8-like polysaccharide antigen. J Clin Microbiol 30: 3050-3057.
14. Eichelberg, K., Kaniga, K., and Galan, J.E. (1996) Transcriptional regulation of Salmonella secreted virulence-determinants. In 96th General Meeting of the American Society for Microbiology. New Orleans: American Society for Microbiology Press, p. 161.
15. Finlay, B.B., and Falkow, S. (1989) Salmonella as an intracellular parasite. Mol Microbiol 3: 1833-1841.
16. Forst, S.A., and Roberts, D.L. (1994) Signal transduction by the EnvZ-OmpR phosphotransfer system in bacteria. Res Microbiol 145: 363-373.
17. Galan, J.E. (1995) Molecular and cellular bases of Salmonella entry into host cells. Curr Topics Microbiol Immunol 209: 43-60.
18. Galan, J.E. (1996) Molecular genetic bases of Salmonella entry into host cells. Mol Microbiol 20: 263-271.
19. Galan, J.E., and Curtiss, III, R. (1990) Expression of Salmonella typhimurium genes required for invasion is regulated by changes in DNA supercoiling. Infect Immun 58: 1879-1885.
20. Galyov, E.E., Wood, M.W., Rosqvist, R., Mullan, P.B., Watson, P.R., Hedges, S., et al. (1997) A secreted effector protein of Salmonella dublin is translocated into eukaryotic cells and mediates inflammation and fluid secretion in infected ileal mucosa. Mol Microbiol 25: 903-912.
21. 2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84: 165-174.
22. Hardt, W.D., and Galan, J.E. (1997) A secreted Salmonella protein with homology to an avirulence determinant of plant pathogenic bacteria. Proc Natl Acad Sci USA 94: 9887-9892.
23. Hashimoto, Y., Li, N., Yokoyama, H., and Ezaki, T. (1993) Complete nucleotide sequence and molecular characterization of ViaB region encoding Vi antigen in Salmonella typhi. J Bacteriol 175: 4456-4465.
24. Hashimoto, Y., Khan, A.Q., and Ezaki, T. (1996) Positive autoregulation of vipR expression in ViaB region-encoded Vi antigen of Salmonella typhi. J Bacteriol 178: 1430-1436.
25. Hensel, M., Shea, J.E., Raupach, B., Monack, D., Falkow, S., Gleeson, C., et al. (1997) Functional analysis of ssaJ and the ssaK/U operon, 13 genes encoding components of the type III secretion apparatus of Salmonella pathogenicity island 2. Mol Microbiol 24: 155-167.
26. Hermant, D., Ménard, R., Arricau, N., Parsot, C., and Popoff, M.Y. (1995) Functional conservation of the Salmonella and Shigella effectors of entry into epithelial cells. Mol Microbiol 17: 781-789.
27. Hornick, R.B., Greisman, S.E., Wooward, I.E., Dupont, H.L., Dawkins, A.T., and Snyder, M.J. (1970) Typhoid fever: pathogenesis and immunologic control N Engl J Med 293: 686-691.
28. Houng, H.H., Noon, K.F., Ou, J.T., and Baron, L.S. (1992) Expression of Vi antigen in Escherichia coli K-12: characterization of ViaB from Citrobacter freundii and identity of ViaA with RcsB. J Bacteriol 174: 5910-5915.
29. Hueck, C.J., Hantman, M.J., Bajaj, V., Johnston, C., Lee, C.A., and Miller, S.I. (1995) Salmonella typhimurium secreted invasion determinants are homologous to Shigella Ipa proteins. Mol Microbiol 18: 479-490.
30. Johnson, E.M., and Baron, L.S. (1969) Genetic transfer of the Vi antigen from Salmonella typhosa to Escherichia coli. J Bacteriol 99: 355-359.
31. Johnston, C., Pegues, D.A., Hueck, C.J., Lee, C.A., and Miller, S.I. (1996) Transcriptional activation of Salmonella typhimurium invasion genes by a member of the phosphorylated response-regulator superfamily. Mol Microbiol 22: 715-727.
32. Jones, B.D. (1996) Salmonellosis: host immune responses and bacterial virulence determinants. Annu Rev Immunol 14: 533-561.
33. Jones, B.D., Lee, C.A., and Falkow, S. (1992) Invasion by Salmonella typhimurium is affected by the direction of flagellar rotation. Infect Immun 60: 2475-2480.
34. Kado, C.I., and Liu, S.T. (1981) A rapid procedure for detection and isolation of large and small plasmids. J Bacteriol 145: 1365-1373.
35. Kaniga, K., Trollinger, D., and Galan, J.E. (1995a) Identification of two targets of the type III secretion system encoded in the inv and spa loci of Salmonella typhimurium that share homology to IpaD and IpaA proteins. J Bacteriol 177: 7078-7085.
36. Kaniga, K., Tucker, S.C., Trollinger, D., and Galan, J.E. (1995b) Homologs of the Shigella invasins IpaB and IpaC are required for Salmonella typhimurium entry into cultured cells. J Bacteriol 177: 3965-3971.
37. Klarsfeld, A.D., Goossens, P.L., and Cossart, P. (1994) Five Listeria monocytogenes genes preferentially expressed in infected mammalian cells: plcA, purH, purD, pyrE and an arginine ABC transporter gene arpJ. Mol Microbiol 13: 585-597.
38. Kohbata, S., Yokoyama, H., and Yabuuchi, E. (1986) Cylopathogenic effect of Salmonella typhi GIFU 10007 on M cells of murine Peyer's patches in ligated ileal loops: an ultrastructural study. Microbiol Immunol 30: 1225-1237.
39. Kolyva, S., Waxin, H., and Popoff, M.Y. (1992) The Vi antigen of Salmonella typhi: molecular analysis of the viaB locus. J Gen Microbiol 138: 297-304.
40. Kossack, R.E., Guerrant, R.L., Densen, P., Schadelin, J., and Mandell, G.L. (1981) Diminished neutrophil oxidative metabolism after phagocytosis of virulent Salmonella typhi. Infect Immun 31: 674-678.
41. Kutsukake, K., Ohya, Y., and Iino, T. (1990) Transcriptional analysis of the flagellar regulon of Salmonella typhimurium. J Bacteriol 172: 741-747.
42. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
43. Leclerc, G.J., Tartera, C., and Metcalf, E.S. (1998) Environmental regulation of Salmonella typhi invasion-defective mutants. Infect Immun 66: 682-691.
44. Lee, C.A., and Falkow, S. (1990) The ability of Salmonella to enter mammalian cells is affected by bacterial growth state. Proc Natl Acad Sci USA 87: 4304-4308.
45. Lee, C.A., Jones, B.D., and Falkow, S. (1992) Identification of a Salmonella typhimurium invasion locus by selection for hyperinvasive mutants. Proc Natl Acad Sci USA 89: 1847-1851.
46. Liu, S.L., and Sanderson, K.E. (1995) Genomic cleavage map of Salmonella typhi Ty2. J Bacteriol 177: 5099-5107.
47. Liu, S.L., Ezaki, T., Miura, H., Matsui, K., and Yabuuchi, E. (1988) Intact motility as a Salmonella typhi invasion-related factor. Infect Immun 56: 1967-73.
48. Lockman, H.A., and Curtiss, III, R. (1990) Salmonella typhimurium mutants lacking flagella or motility remain virulent in BALB/c mice. Infect Immun 58: 137-143.
49. Looney, R.J., and Steigbigel, R.T. (1986) Role of the Vi antigen of Salmonella typhi in resistance to host defense in vitro. J Lab Clin Med 108: 506-516.
50. Mesnage, S., Tosi-Couture, E., Gounon, P., Mock, M., and Fouet, A. (1998) The capsule and S-layer: two independent and yet compatible macromolecular structures in Bacillus anthracis. J Bacteriol 180: 52-58.
51. Miller, R.M., Garbus, J., and Hornick, R.B. (1972) Lack of enhanced oxygen consumption by polymorphonuclear leukocytes on phagocytosis of virulent Salmonella typhi. Science 175: 1010-1011.
52. Miller, S.I., Kukral, A.M., and Mekalanos, J.J. (1989) A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. Proc Natl Acad Sci USA 86: 5054-5058.
53. Miller, V.L., and Mekalanos, J.J. (1988) A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 170: 2575-2583.
54. Mills, S.D., and Finlay, B.B. (1994) Comparison of Salmonella typhi and S. typhimurium invasion, intracellular growth and localization in cultured human epithelial cells. Microb Pathog 17: 409-423.
55. Miras, I., Hermant, D., Arricau, N., and Popoff, M.Y. (1995) Nucleotide sequence of iagA and iagB genes involved in invasion of HeLa cells by Salmonella enterica ssp. enterica ser. Typhi. Res Microbiol 146: 17-20.
56. Ochman, H., Soncini, F.C., Solomon, F., and Groisman, E.A. (1996) Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci USA 93: 7800-7804.
57. Pardon, P., Popoff, M.Y., Coynault, C., Marly, J., and Miras, I. (1986) Virulence-associated plasmids of Salmonella serotype Typhimurium in experimental murine infection. Ann Inst Pasteur/Microbiol 137B: 47-60.
58. Pegues, D.A., Hantman, M.J., Behlau, I., and Miller, S.I. (1995) PhoP/PhoQ transcriptional repression of Salmonella typhimurium invasion genes: evidence for a role in protein secretion. Mol Microbiol 17: 169-181.
59. Phalipon, A., Arondel, J., Nato, F., Rouyre, S., Mazie, J.-C., and Sansonetti, P.J. (1992) Identification and characterization of B-cell epitopes of IpaC, an invasion-associated protein of Shigella flexneri. Infect Immun 60: 1919-26.
60. Pickard, D., Li, J., Roberts, M., Maskell, D., Hone, D., Levine, M., et al. (1994) Characterization of defined ompR mutants of Salmonella typhi: ompR is involved in the regulation of Vi polysaccharide expression. Infect Immun 62: 3984-3993.
61. s, SpvR and growth phase in the control of spvR, the regulatory gene of the Salmonella plasmid virulence operon. Mol Gen Genet 256: 333-47.
62. Robbins, J.D., and Robbins, J.B. (1984) Reexamination of the protective role of the capsular polysaccharide (Vi antigen) of Salmonella typhi. J Infect Dis 150: 436-449.
63. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
64. Schmeiger, H. (1972) Phage P22-mutants with increased or decreased transduction abilities. Mol Gen Genet 119: 74-88.
65. Shea, J.E., Hensel, M., Gleeson, C., and Holden, D.W. (1996) Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc Natl Acad Sci USA 93: 2593-2597.
66. Sledjeski, D.D., and Gottesman, S. (1996) Osmotic shock induction of capsule synthesis in Escherichia coli K-12. J Bacteriol 178: 1204-1206.
67. Stout, V. (1994) Regulation of capsule synthesis includes interactions of the RcsC/RcsB regulatory pair. Res Microbiol 145: 389-392.
68. Takeuchi, A. (1967) Electron microscopic studies of experimental Salmonella infection. Am J Pathol 50: 109-136.
69. Tartera, C., and Metcalf, E.S. (1993) Osmolarity and growth phase overlap in regulation of Salmonella typhi adherence to and invasion of human intestinal cells. Infect Immun 61: 3084-3089.
70. Tsang, R.S.W., and Chau, P.Y. (1987) Production of Vi monoclonal antibodies and their application as diagnostic reagents. J Clin Microbiol 25: 531-535.
71. Vieira, J., and Messing, J. (1982) The pUC plasmids, an M13 mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene 19: 259-268.
72. Virlogeux, I., Waxin, H., Ecobichon, C., and Popoff, M.Y. (1995) Role of the viaB locus in synthesis, transport and expression of Salmonella typhi Vi antigen. Microbiology 141: 3039-3047.
73. Virlogeux, I., Waxin, H., Ecobichon, C., Lee, J.O., and Popoff, M.Y. (1996) Characterization of the rcsA and rcsB genes from Salmonella typhi: rcsB through tviA is involved in regulation of Vi antigen synthesis. J Bacteriol 178: 1691-1698.
74. Virlogeux-Payant, I., and Popoff, M.Y. (1996) The Vi antigen of Salmonella typhi. Bull Inst Pasteur 94: 237-250.
75. Wood, M.W., Rosqvist, R., Mullan, P.B., Edwards, M.E., and Galyov, E.E. (1996) SopE, a secreted protein of Salmonella dublin, is translocated into the target eukaryotic cell via a sip-dependent mechanism and promotes bacterial entry. Mol Microbiol 22: 327-338.
76. Zierler, M., and Galan, J.E. (1995) Contact with cultured epithelial cells induces the secretion of the Salmonella typhimurium invasion protein InvJ. Infect Immun 63: 4024-4028.