SseG, a virulence protein that targets Salmonella to the Golgi network

EMBO Journal

Volumn 22, Issue 19, 2003, Pages 5003-5014

  Salcedo, Suzana P ^a   Holden, David W ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Golgi; Salmonella; SseG; Trafficking; Type III secretion

Indexed keywords

BACTERIAL PROTEIN; PROTEIN SSEG; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL REPRODUCTION; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CELL INVASION; CELL MATURATION; CELL SECRETION; CELL VACUOLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOCYTOSIS; EPITHELIUM CELL; GOLGI COMPLEX; HUMAN; HUMAN CELL; MEMBRANE BINDING; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; SALMONELLA CONTAINING VACUOLE; SALMONELLA ENTERICA;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; GOLGI APPARATUS; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; SALMONELLA TYPHIMURIUM; VACUOLES;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; SALMONELLA; SALMONELLA ENTERICA; STRAWBERRY CRINKLE VIRUS;

EID: 0141642027     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg517     Document Type: Article

References (40)

1. Berger, E.G., Aegerter, E., Mandel, T. and Hauri, H.P. (1986) Monoclonal antibodies to soluble, human milk galactosyltransferase (lactose synthase A protein). Carbohydr. Res., 149, 23-33.
2. Beuzón, C.R., Méresse, S., Unsworth, K.E., Ruiz-Albert, J., Garvis, S., Waterman, S.R., Ryder, T.A., Boucrot, E. and Holden, D.W. (2000) Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J., 19, 3235-3249.
3. Beuzón, C.R., Salcedo, S.P. and Holden, D.W. (2002) Growth and killing of a Salmonella enterica serovar Typhimurium sifA mutant strain in the cytosol of different host cell lines. Microbiology, 148, 2705-2715.
4. Bispham, J., Tripathi, B.N., Watson, P.R. and Wallis, T.S. (2001) Salmonella pathogenicity island 2 influences both systemic salmonellosis and Salmonella-induced enteritis in calves. Infect. Immun., 69, 367-377.
5. Brumell, J.H., Tang, P., Mills, S.D. and Finlay, B.B. (2001) Characterization of Salmonella-induced filaments (Sifs) reveals a delayed interaction between Salmonella-containing vacuoles and late endocytic compartments. Traffic, 2, 643-653.
6. Chardin, P. and McCormick, F. (1999) Brefeldin A: the advantage of being uncompetitive. Cell, 97, 153-155.
7. 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.
8. Cole, N.B., Sciaky, N., Marotta, A., Song, J. and Lippincott-Schwartz, J. (1996) Golgi dispersal during microtubule disruption: regeneration of Golgi stacks at peripheral endoplasmic reticulum exit sites. Mol. Biol. Cell, 7, 631-650.
9. Dascher, C. and Balch, W.E. (1994) Dominant inhibitory mutants of ARF1 block endoplasmic reticulum to Golgi transport and trigger disassembly of the Golgi apparatus. J. Biol. Chem., 269, 1437-1448.
10. Deiwick, J., Nikolaus, T., Shea, J.E., Gleeson, C., Holden, D.W. and Hensel, M. (1998) Mutations in Salmonella pathogenicity island 2 (SPI2) genes affecting transcription of SPI1 genes and resistance to antimicrobial agents. J. Bacteriol., 180, 4775-4780.
11. 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.
12. Garcia-del Portillo, F., Zwick, M.B., Leung, K.Y. and Finlay, B.B. (1993) Salmonella induces the formation of filamentous structures containing lysosomal membrane glycoproteins in epithelial cells. Proc. Natl Acad. Sci. USA, 90, 10544-10548.
13. Gleeson, P.A. (1998) Targeting of proteins to the Golgi apparatus. Histochem. Cell. Biol., 109, 517-532.
14. Guy, R.L., Gonias, L.A. and Stein, M.A. (2000) Aggregation of host endosomes by Salmonella requires SPI2 translocation of SseFG and involves SpvR and the fms-aroE intragenic region. Mol. Microbiol., 37, 1417-1435.
15. Hackstadt, T., Rockey, D.D., Heinzen, R. A. and Scidmore, M.A. (1996) Chlamydia trachomatis interrupts an exocytic pathway to acquire endogenously synthesized sphingomyelin in transit from the Golgi apparatus to the plasma membrane. EMBO J., 15, 964-977.
16. Hackstadt, T., Fischer, E.R., Scidmore, M.A., Rockey, D.D. and Heinzen, R.A. (1997) Origins and functions of the chlamydial inclusion. Trends Microbiol., 5, 288-293.
17. Hensel, M., Shea, J.E., Waterman, S.R., Mundy, R., Nikolaus, T., Banks, G., Vazquez-Torres, A., Gleeson, C., Fang, F.C. and Holden, D.W. (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.
18. Holden, D.W. (2002) Trafficking of the Salmonella vacuole in macrophages. Traffic, 3, 161-169.
19. Kagan, J.C. and Roy, C.R. (2002) Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat. Cell Biol., 4, 945-954.
20. Kuhle, V. and Hensel, M. (2002) SseF and SseG are translocated effectors of the type III secretion system of Salmonella pathogenicity island 2 that modulate aggregation of endosomal compartments. Cell. Microbiol., 4, 813-824.
21. Lippincott-Schwartz, J., Yuan, L.C., Bonifacino, J.S. and Klausner, R.D. (1989) Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell, 56, 801-813.
22. Lippincott-Schwartz, J., Donaldson, J.G., Schweizer, A., Berger, E.G., Hauri, H.P., Yuan, L.C. and Klausner, R.D. (1990) Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway. Cell, 60, 821-836.
23. Lippincott-Schwartz, J., Yuan, L., Tipper, C., Amherdt, M., Orci, L. and Klausner, R.D. (1991) Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell, 67, 601-616.
24. Méresse, S., Steele-Mortimer, O., Finlay, B.B. and Gorvel, J.P. (1999) The rab7 GTPase controls the maturation of Salmonella typhimurium-containing vacuoles in HeLa cells. EMBO J., 18, 4394-4403.
25. 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.
26. Paesold, G., Guiney, D.G., Eckmann, L. and Kagnoff, M.F. (2002) Genes in the Salmonella pathogenicity island 2 and the Salmonella virulence plasmid are essential for Salmonella-induced apoptosis in intestinal epithelial cells. Cell. Microbiol., 4, 771-781.
27. Persson, B. and Argos, P. (1994) Prediction of transmembrane segments in proteins utilising multiple sequence alignments. J. Mol. Biol., 237, 182-192.
28. Plutner, H., Davidson, H.W., Saraste, J. and Balch, W.E. (1992) Morphological analysis of protein transport from the ER to Golgi membranes in digitonin-permeabilized cells: role of the P58 containing compartment. J. Cell Biol., 119, 1097-1116.
29. Ponnambalam, S., Girotti, M., Yaspo, M.L., Owen, C.E., Perry, A.C., Suganuma, T., Nilsson, T., Fried, M., Banting, G. and Warren, G. (1996) Primate homologues of rat TGN38: primary structure, expression and functional implications. J. Cell Sci., 109, 675-685.
30. 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.
31. Ruiz-Albert, J., Yu, X.J., Beuzón, C.R., Blakey, A.N., Galyov, E.E. and Holden, D.W. (2002) Complementary activities of SseJ and SifA regulate dynamics of the Salmonella typhimurium vacuolar membrane. Mol. Microbiol., 44, 645-661.
32. Steele-Mortimer, O., Méresse, S., Gorvel, J.P., Toh, B.H. and Finlay, B.B. (1999) Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell. Microbiol., 1, 33-49.
33. Stein, M.A., Leung, K.Y., Zwick, M., García-del Portillo, F. and Finlay, B.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.
34. Thyberg, J. and Moskalewski, S. (1999) Role of microtubules in the organization of the Golgi complex. Exp. Cell Res., 246, 263-279.
35. Uchiya, K., Barbieri, M.A., Funato, K., Shah, A.H., Stahl, P.D. and Groisman, E.A. (1999) A Salmonella virulence protein that inhibits cellular trafficking. EMBO J., 18, 3924-3933.
36. Valdivia, R.H. and Falkow, S. (1997) Fluorescence-based isolation of bacterial genes expressed within host cells. Science, 277, 2007-2011.
37. Ward, T.H., Polishchuk, R.S., Caplan, S., Hirschberg, K. and Lippincott-Schwartz, J. (2001) Maintenance of Golgi structure and function depends on the integrity of ER export. J. Cell Biol., 155, 557-570.
38. Waterman, S.R. and Holden, D.W. (2003) Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell. Microbiol., 5, 501-511.
39. Wood, S.A. and Brown, W.J. (1992) The morphology but not the function of endosomes and lysosomes is altered by brefeldin A. J. Cell Biol., 119, 273-285.
40. Wyrick, P.B. (2000) Intracellular survival by Chlamydia. Cell. Microbiol., 2, 275-282.