Salmonella maintains the integrity of its intracellular vacuole through the action of SifA

EMBO Journal

Volumn 19, Issue 13, 2000, Pages 3235-3249

  Beuzón, Carmen R ^a   Méresse, Stéphane ^c   Unsworth, Kate E ^a   Ruíz Albert, Javier ^a   Garvis, Steve ^a   Waterman, Scott R ^a   Ryder, Timothy A ^b   Boucrot, Emmanuel ^c   Holden, David W ^a  

^a IMPERIAL COLLEGE SCHOOL OF MEDICINE   (United Kingdom)

^b QUEEN CHARLOTTE S AND CHELSEA HOSPITAL   (United Kingdom)

^c INSERM   (France)

Author keywords

Competitive Index; SPI 2; Trafficking; Type III secretion; Vacuole

Indexed keywords

ADENOSINE TRIPHOSPHATASE; GLYCOPROTEIN;

ARTICLE; BACTERIAL GENE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; CELL VACUOLE; CONTROLLED STUDY; ENDOCYTOSIS; EPITHELIUM CELL; HUMAN; HUMAN CELL; MACROPHAGE; MUTANT; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; SALMONELLA TYPHIMURIUM;

ANIMALIA; BACTERIA (MICROORGANISMS); NEGIBACTERIA; SALMONELLA; SALMONELLA TYPHIMURIUM; TYPHIMURIUM;

EID: 0343517154     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.13.3235     Document Type: Article

References (61)

1. Altschul, S., Madden, T., Schaffer, A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. (1997) Gapped blast and PSI-blast: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402.
2. Baumler, A., Tsolis, R., Valentine, P., Ficht, T. and Heffron, F. (1997) Synergistic effect of mutations in invA and lpfC on the ability of Salmonella typhimurium to cause murine typhoid. Infect. Immun., 65, 2254-2259.
3. Beuzón, C., Banks, G., Deiwick, J., Hensel, M. and Holden, D.W. (1999) pH-dependent secretion of SseB, a product of the SPI-2 type III secretion system of Salmonella typhimurium. Mol. Microbiol., 33, 806-816.
4. Blanc-Potard, A. and Groisman, E. (1997) The Salmonella selC locus contains a pathogenicity island mediating intramacrophage survival. EMBO J., 16, 5376-5385.
5. Chang, A.C. and Cohen, S.N. (1978) Construction and characterisation of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J. Bacteriol., 134, 1141-1156.
6. Chatfield, S., Dorman, C., Hayward, C. and Dougan, G. (1991) Role of ompR dependent genes in Salmonella typhimurium virulence: mutants deficient in both OmpC and OmpF are attenuated in vivo. Infect. Immun., 59, 449-452.
7. Cirillo, D., Valdivia, R., Monack, D. and Falkow, S. (1998) Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol. Microbiol., 30, 175-188.
8. Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res., 16, 10881-10890.
9. Davis, R.H., Botstein, D. and Roth, J.R. (1980) Advanced Bacterial Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
10. de Chastellier, C. and Berche, P. (1994) Fate of Listeria monocytogenes in murine macrophages: evidence for simultaneous killing and survival of intracellular bacteria. Infect. Immun., 62, 543-553
11. Deiwick, J., Nikolaus, T., Erdogan, S. and Hensel, M. (1999) Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol. Microbiol., 31, 1759-1773.
12. Dorman, C., Chatfield, S., Higgins, C., Hayward, C. and Dougan, G. (1989) Characterization of porin and ompR mutants of a virulent strain of Salmonella typhimurium: ompR mutants are attenuated in vivo. Infect. Immun., 57, 2136-2140.
13. Finlay, B.B. (1994) Molecular and cellular mechanisms of Salmonella pathogenesis Curr. Top. Microbiol. Immunol., 192, 163-185.
14. Freter, R., O'Brien, P. and Macsai, M. (1981) Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vivo studies. Infect. Immun., 34, 234-240.
15. Galán, J.E. (1996) Molecular genetic bases of Salmonella entry into host cells. Mol. Microbiol., 20, 263-271.
16. Galán, J.E. and Curtiss, R., III (1989) Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc. Natl Acad. Sci. USA, 86, 6383-6387
17. Garcia-del Portillo, F. and Finlay, B.B. (1995) Targeting of Salmonella typhimurium to vesicles containing lysosomal membrane glycoproteins bypasses compartments with mannose-6-phosphate receptors. J. Cell Biol., 129, 81-97.
18. Garcia-del Portillo, .F., Zwick, M.B., Leung, K.Y. and Finlay, B.B. (1993a) Intracellular replication of Salmonella within epithelial cells is associated with filamentous structures containing lysosomal membrane glycoproteins. Infect. Agents Dis., 2, 227-231.
19. Garcia-del Portillo, F., Zwick, M.B., Leung, K.Y. and Finlay, B.B. (1993b) Salmonella induces the formation of filamentous structures containing lysosomal membrane glycoproteins in epithelial cells. Proc. Natl Acad. Sci. USA. 90, 10544-10548.
20. Gentschev, I., Sokolovic, Z., Mollenkopf, H.J., Hess, J., Kaufmann, S.H., Kuhn, M., Krohne, G.F. and Goebel, W. (1995) Salmonella strain secreting active listeriolysin changes its intracellular localization. Infect. Immun., 63, 4202-4205.
21. Glaser, P., Ladant, D., Sezer, O., Pichot, F., Ullmann, A. and Danchin, A. (1988) The calmodulin-sensitive adenylate cyclase of Bordetella pertussis: cloning and expression in Escherichia coli. Mol. Microbiol., 2, 19-30.
22. Groisman, E. and Ochman, H. (1997) How Salmonella became a pathogen. Trends Microbiol., 5, 343-349.
23. Hardt, W.-D., Urlaub, H. and Galán, J.E. (1998) A substrate of the centisome 63 type III protein secretion system of Salmonella typhimurium is encoded by a cryptic bacteriophage. Proc. Natl Acad. Sci. USA, 95, 2574-2579.
24. Hensel, M., Shea, J.E., Gleeson, C., Jones, M.D., Dalton, E. and Holden, D. W. (1995) Simultaneous identification of bacterial virulence genes by negative selection. Science, 269, 400-403.
25. Hensel, M., Shea, J.E., Raupach, B., Monack, D., Falkow, S., Gleeson, C. and Holden, D.W. (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. Hensel, M. et al. (1998) Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol. Microbiol., 30, 163-174.
27. Heyde, M. and Portalier, R. (1987) Regulation of major outer membrane porin proteins of Escherichia coli K 12 by pH. Mol. Gen. Genet., 208, 511-517.
28. Hueck, C.J. (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev., 62, 379-433.
29. Hunziker, W. and Geuze, H.J. (1996) Intracellular trafficking of lysosomal membrane proteins. BioEssays, 18, 379-389.
30. Jones, M.A., Wood, M.W., Mullan, P.B., Watson, P.R., Wallis, T.S. and Galyov, E.E. (1998) Secreted effector proteins of Salmonella dublin act in concert to induce enteritis. Infect. Immun., 66, 5799-5804.
31. Lee, A., Detweiler, C. and Falkow, S. (2000) OmpR regulates the two-component system SsrA-SsrB in Salmonella pathogenicity island 2. J. Bacteriol, 182, 771-781.
32. Méresse, S., Steele-Mortimer, O., Finlay, B.B. and Gorvel, J.P. (1999a) The rab7 GTPase controls the maturation of Salmonella typhimurium-containing vacuoles in HeLa cells. EMBO J., 18, 4394-4403.
33. Méresse, S., Steele-Mortimer, O., Moreno, E., Desjardins, M., Finlay, B.B. and Gorvel, J.P (1999b) Controlling the maturation of pathogen-containing vacuoles: a matter of life and death. Nature Cell Biol., 1, 183-188.
34. Miao, E., Scherer, C., Tsolis, R., Kingsley, R., Adams, L., Baumler, A. and Miller, S. (1999) Salmonella typhimurium leucine-rich repeat proteins are targeted to the SPI1 and SPI2 type III secretion systems. Mol. Microbiol., 34, 850-864.
35. Miller, S.I. and Mekalanos, J.J. (1990) Constitutive expression of the phoP regulon attenuates Salmonella virulence and survival within macrophages. J. Bacteriol., 172, 2485-2490.
36. 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.
37. Mills, D.M., Bajaj, V. and Lee, C.A. (1995) A 40 kb chromosomal fragment encoding Salmonella typhimurium invasion genes is absent from the corresponding region of the Escherichia coli K-12 chromosome. Mol. Microbiol., 15, 749-759.
38. Mills, S., Ruschkowski, S., Stein, M. and Finlay, B. (1998) Trafficking of porin-deficient Salmonella typhimurium mutants inside HeLa cells: ompR and envZ mutants are defective for the formation of Salmonella-induced filaments. Infect. Immun., 66, 1806-1811.
39. 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.
40. Pearson, W. and Lipman, D. (1988) Improved tools for biological sequence analysis. Proc. Natl Acad. Sci. USA, 85, 2444-2448.
41. 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.
42. Rathman, M., Sjaastad, M.D. and Falkow, S. (1996) Acidification of phagosomes containing Salmonella typhimurium in murine macrophages. Infect. Immun., 64, 2765-2773.
43. Rathman, M., Barker, L.P. and Falkow, S. (1997) The unique trafficking pattern of Salmonella typhimurium-containing phagosomes in murine macrophages is independent of the mechanism of bacterial entry. Infect. Immun., 65, 1475-1485.
44. Richter-Dahlfors, A., Buchan, A. and Finlay, B. (1997) Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J. Exp. Med., 186, 569-580.
45. Rothman, J.E. and Wieland, F.T. (1996) Protein sorting by transport vesicles. Science, 272, 227-234.
46. Ryder, T.A. and Mackenzie, M.L. (1981) The routine preparation of seminal fluid specimens for transmission electron microscopy. J. Clin. Pathol., 34, 1006-1009.
47. Sato, S.B. and Toyama, S. (1994) Interference with the endosomal acidification by a monoclonal antibody directed toward the 116 (100)-kD subunit of the vacuolar type proton pump. J. Cell Biol. 127, 39-53.
48. Schimmoller, F., Simon, I. and Pfeffer, S.R. (1998) Rab GTPases, directors of vesicle docking. J. Biol. Chem., 273, 22161-22164.
49. 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.
50. Shea, J., Beuzón, C., Gleeson, C., Mundy, R. and Holden, D.W. (1999) Influence of the Salmonella typhimurium pathogenicity island 2 type III secretion system on bacterial growth in the mouse. Infect. Immun., 67, 213-219.
51. Sinai, A.P. and Joiner, K.A. (1997) Safe haven: the cell biology of nonfusogenic pathogen vacuoles. Annu. Rev. Microbiol., 51, 415-462.
52. Steele-Mortimer, O., Méresse, S., Gorvel, J.P. and Finlay, B.B. (1999) Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathways. Cell Microbiol., 1, 33-49.
53. Stein, M., Leung, K., Zwick, M., Garcia-del Portillo, F. and Finlay, B. (1996) Identification of a Salmonella virulence gene required for formation of filamentous structures containing lysosomal membrane glycoproteins within epithelial cells. Mol. Microbiol., 20, 151-164.
54. Taylor, R., Miller, V., Furlong, D. and Mekalanos, J. (1987) Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc. Natl Acad. Sci. USA, 84, 2833-2837.
55. Thomas, A.D. and Booth, I.R. (1992) The regulation of expression of the porin gene ompC by acid pH. J. Gen. Microbiol., 138, 1829-1835
56. Thompson, J., Higgins, D. and Gibson, T. (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res., 22, 4673-4680.
57. Tsolis, R.M., Townsend, S.M., Miao, E.A., Miller, S.I., Ficht, T.A., Adams, L.G. and Baumler, A.J. (1999) Identification of a putative Salmonella enterica serotype typhimurium host range factor with homology to lpaH and YopM by signature-tagged mutagenesis. Infect. Immun., 67, 6385-6393.
58. Uchiya, K., Barbieri, M., Funato, K., Shah, A., Stahl, P. and Groisman, A. (1999) A Salmonella virulence protein that inhibits cellular trafficking. EMBO J., 18, 3924-3933.
59. Valdivia, R. and Falkow, S. (1997) Fluorescence-based isolation of bacterial genes expressed within host cells. Science, 277, 2007-2011.
60. Vazquez-Torres, A., Xu, Y., Jones-Carson, J., Holden, D.W., Lucia, S.M., Dinauer, M.C., Mastroeni, P. and Fang, F.C. (2000) Salmonella Pathogenicity Island 2-dependent evasion of the phagocyte NADPH oxidase. Science, 287, 1655-1658.
61. Wood, M., Jones, M., Watson, P., Hedges, S., Wallis, T. and Galyov, E. (1998) Identification of a pathogenicity island required for Salmonella enteropathogenicity. Mol. Microbiol., 29, 883-891.