A Salmonella virulence protein that inhibits cellular trafficking

EMBO Journal

Volumn 18, Issue 14, 1999, Pages 3924-3933

  Uchiya, Kei Ichi ^a   Barbieri, M Alejandro ^a   Funato, Kouichi ^a   Shah, Ankur H ^a   Stahl, Philip D ^a   Groisman, Eduardo A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Endosome; Intracellular trafficking; Phagosome; Salmonella; Type III secretion

Indexed keywords

BACTERIAL PROTEIN; TRANSFERRIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; CONTROLLED STUDY; CYTOSOL; FEMALE; HOST CELL; HUMAN; HUMAN CELL; LYSOSOME; MACROPHAGE; MEMBRANE TRANSPORT; MOUSE; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN TRANSPORT; SALMONELLA ENTERICA; SINDBIS VIRUS;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CELL LINE; CELL SURVIVAL; CYTOSOL; ENDOSOMES; GENES, BACTERIAL; GTP-BINDING PROTEINS; INHIBITORY CONCENTRATION 50; LETHAL DOSE 50; LYSOSOMES; MACROPHAGES; MEMBRANE FUSION; MICE; MOLECULAR SEQUENCE DATA; MUTATION; PHAGOSOMES; RAB5 GTP-BINDING PROTEINS; RECEPTORS, TRANSFERRIN; SALMONELLA ENTERICA; VIRULENCE;

EID: 0033565304     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.14.3924     Document Type: Article

References (51)

1. Alexander, J. and Vickerman, K. (1975) Fusion of host cell secondary lysosomes with the parasitophorous vacuoles of Leishmania mexicana-infected macrophages. J. Protozol., 22, 502-508.
2. Allen, P.M., Beller, D.I., Braun, J. and Unanue, E.R. (1984) The handling of Listeria monocytogenes by macrophages: the search for an immunogenic molecule in antigen presentation. J. Immunol., 132, 323-331.
3. Barbieri, M.A., Li, G., Colombo, M.I. and Stahl, P.D. (1994) Rab5, an early acting endosomal GTPase supports in vitro endosome fusion without GTP hydrolysis. J. Biol. Chem., 269, 18720-18722.
4. Blanc-Potard, A.-B. and Groisman, E.A. (1997) The Salmonella selC locus contains a pathogenicity island mediating intramacrophage survival. EMBO J., 16, 5376-5385.
5. Boquet, P., Munro, P., Fiorentini, C. and Just, I. (1998) Toxins from anaerobic bacteria: specificity and molecular mechanisms of action. Curr. Opin. Microbiol., 1, 66-74.
6. Brown, W.J., DeWald, D.B., Emr, S.D., Plutner, H. and Balch, W.E. (1995) Role for phosphatidylinositol 3-kinase in the sorting and transport of newly synthesized lysosomal enzymes in mammalian cells. J. Cell Biol., 130, 781-796.
7. Buchmeier, N.A. and Heffron, F. (1991) Inhibition of macrophage phagosome-lysosome fusion by Salmonella typhimurium. Infect. Immun., 59, 2232-2238.
8. Cirillo, D.M., Valdivia, R.H., Monack, D.M. 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.
9. Davis, R.W., Bolstein, D. and Roth, J.R. (1980) Advanced Bacterial Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
10. Diaz, R., Mayorga, L. and Stahl, P. (1988) In vitro fusion of endosomes following receptor-mediated endocytosis. J. Biol. Chem., 263, 6093-6100.
11. Diaz, R., Mayorga, L.S., Weidman, P.I., Rothman, J.E. and Stahl, P.D. (1989) Vesicle fusion following receptor-mediated endocytosis requires a protein active in Golgi transport. Nature, 339, 398-400.
12. Fields, P.I., Swanson, R.V., Haidaris, C.G. and Heffron, F. (1986) Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc. Natl Acad. Sci. USA, 83, 5189-5193.
13. Fortier, A.H., Leiby, D.A., Narayanan, R.B., Asafoadjei, E., Crawford, R.M., Nacy, C.A. and Meltzer, M.S. (1995) Growth of Francisella tularensis LVS in macrophages: the acidic intracellular compartment provides essential iron required for growth. Infect. Immun., 63, 1478-1483.
14. Fraker, P.J. and Speck, J.C., Jr (1978) Protein and cell membrane iodinations with a sparingly soluble chloroamide, 1,3,4,6-tetrachloro-3a,6a-diphrenylglycoluril. Biochem. Biophys. Res. Commun., 80, 849-857.
15. Galán, J.E. (1996) Molecular genetic basis of Salmonella entry into host cells. Mol. Microbiol., 20, 263-272.
16. Garcia-del Portillo, F. and Finlay, B.B. (1995a) Targeting of Salmonella typhimurium to vesicles containing lysosomal membrane glycoproteins bypasses compartments with mannose 6-phosphate receptors. J. Cell Biol., 129, 81-97.
17. Garcia-del Portillo, F. and Finlay, B.B. (1995b) The varied lifestyles of intracellular pathogens within eukaryotic vacuolar compartments. Trends Microbiol., 3, 373-380.
18. Groisman, E.A. and Ochman, H. (1996) Pathogenicity islands: bacterial evolution in quantum leaps. Cell, 87, 791-794.
19. Groisman, E.A., Sturmoski, M.A., Solomon, F., Lin, R. and Ochman, H. (1993) Molecular, functional and evolutionary analysis of sequences specific to Salmonella. Proc. Natl Acad. Sci. USA, 90, 1033-1037.
20. Hacker, J., Blum-Oehler, G., Mühldorfer, I. and Tschäpe, H. (1997) Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol. Microbiol., 23, 1089-1098.
21. Heinzen, R.A., Scidmore, M.A., Rockey, D.D. and Hackstadt, T. (1996) Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnetti and Chlamydia trachomatis. Infect. Immun., 64, 796-809.
22. Hensel, M., Shea, J.E., Bäumler, A.J., Gleeson, C., Blattner, F. and Holden, D.W. (1997a) Analysis of the boundaries of Salmonella pathogenicity island 2 and the corresponding chromosomal region of Escherichia coli K-12. J. Bacteriol., 179, 1105-1111.
23. Hensel, M., Shea, J.E., Raupach, B., Monack, D., Falkow, S., Gleeson, C., Kubo, T. and Holden, D.F. (1997b) 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.
24. 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.
25. Hensel, M., Nikolaus, T. and Egelseer, C. (1999) Molecular and functional analysis indicates a mosaic structure of Salmonella pathogenicity island 2. Mol. Microbiol., 31, 489-498.
26. Horwitz, M.A. (1983) The Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J. Exp. Med., 158, 2108-2126.
27. Hsia, R., Pannekoek, Y., Ingerowski, E. and Bavoil, P.M. (1997) Type III secretion genes identify a putative virulence locus of Chlamydia. Mol. Microbiol., 25, 351-359.
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. Ishibashi, Y. and Arai, T. (1990) Specific inhibition of phagosome-lysosome fusion in murine macrophages mediated by Salmonella typhimurium infection. FEMS Microbiol. Immunol., 64, 35-44.
30. Joiner, K.A., Fuhrman, S.A., Miettinen, H.M., Kasper, L.H. and Mellman, I. (1990) Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science, 249, 641-646.
31. Lavin, M.F. and Shiloh, Y. (1997) The genetic defect in ataxiatelangiectasia. Annu. Rev. Immunol., 15, 177-202.
32. Lee, C.A. (1997) Type III secretion systems: machines to deliver bacterial proteins into eukaryotic cells? Trends Microbiol., 5, 148-156.
33. Li, G. and Stahl, P.D. (1993) Structure-function relationship of the small GTPase rab5. J. Biol. Chem., 268, 24475-24480.
34. Lim, D.-S., Kirsch, D.G., Canman, C.E., Ahn, J.-H., Ziv, Y., Newman, L.S., Darnell, R.B., Shiloh, Y. and Kastan, M.B. (1998) ATM binds to β-adaptin in cytoplasmic vesicles. Proc. Natl Acad. Sci. USA, 95, 10146-10151.
35. Mayorga, L.S., Diaz, R., Colombo, M.I. and Stahl, P.D. (1989) GTP γS stimulation of endosome fusion suggests a role for a GTP-binding protein in the priming of vesicles before fusion. Cell Regul., 1, 113-124.
36. Mayorga, L.S., Colombo, M.I., Lennartz, M., Brown, E.J., Rahman, K.H., Weiss, R., Lennon, P.J. and Stahl, P.D. (1993) Inhibition of endosome fusion by phospholipase A2 (PLA2) inhibitors points to a role for PLA2 in endocytosis. Proc. Natl Acad. Sci. USA, 90, 10255-10259.
37. 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.
38. Montecucco, C. (1998) Protein toxins and membrane transport. Curr. Opin. Cell Biol., 10, 530-536.
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. Portnoy, D.A. and Jones, S. (1994) The cell biology of Listeria monocytogenes infection (escape from a vacuole). Ann. NY Acad. Sci., 730, 15-25.
41. 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.
42. Richter-Dahlfors, A., Buchan, A.M.J. and Finlay, B.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.
43. Rodriguez, L., Stirling, C.J. and Woodman, P.G. (1994) Multiple N-ethylmaleimide-sensitive components are required for endosomal vesicle fusion. Mol. Biol. Cell, 5, 773-783.
44. Roth, J. (1983) The colloidal gold marker system for light and electron microscopy cytochemistry. In Bullock, G. and Petrusz, P. (eds), Techniques in Immunochemistry. Vol. 2. Academic Press, London, UK, pp. 217-284.
45. Russell, D.G., Xu, S. and Chakraborty, P. (1992) Intracellular trafficking and the parasitophorous vacuole of Leishmania mexicana-infected macrophages. J. Cell Sci., 103, 1193-1210.
46. 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.
47. Shea, J.E., Beuzon, C.R., 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.
48. Sheehan, B., Kocks, C., Dramsi, S., Gouin, E., Klarsfeld, A.D., Mengaud, J. and Cossart, P. (1994) Molecular and genetics determinants of Listeria monocytogenes. Curr. Top. Microbiol. Immunol., 192, 187-216.
49. Shizuya, H., Birren, B., Kim, U.-J., Mancino, V., Slepak, T., Tachiri, Y. and Simon, M. (1992) Cloning and stable maintenance of 300-kilobase-pair fragments of human DNA in Escherichia coli using an F-factor-based vector. Prof. Natl Acad. Sci. USA, 89, 8794-8797.
50. Stenmark, H., Parton, R.G., Steele-Mortimer, O., Lutcke, A., Gruenberg, J. and Zerial, M. (1994) Inhibition of Rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J., 13, 1287-1296.
51. Valdivia, R.H. and Falkow, S. (1997) Fluorescence-based isolation of bacterial genes expressed within host cells. Science, 277, 2007-2010.