The target cell plasma membrane is a critical interface for Salmonella cell entry effector-host interplay

Molecular Microbiology

Volumn 54, Issue 4, 2004, Pages 887-904

  Cain, Robert J ^a   Hayward, Richard D ^a   Koronakis, Vassilis ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BACTERIAL PROTEIN; DIMETHYLALLYLTRANSFERASE; EPITOPE; F ACTIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; PROTEIN CDC42; PROTEIN SOPE; PROTEIN SPTP; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CELL INTERACTION; CELL MEMBRANE; CELL STRAIN 3T3; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; CYTOSOL; EFFECTOR CELL; ESCHERICHIA COLI; HOST CELL; IMMUNOFLUORESCENCE MICROSCOPY; IN VITRO STUDY; INTERNALIZATION; INTESTINE EPITHELIUM CELL; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; SALMONELLA TYPHIMURIUM; TARGET CELL;

ANIMALS; BACTERIAL PROTEINS; CDC42 GTP-BINDING PROTEIN; CELL FRACTIONATION; CELL MEMBRANE; CYTOPLASM; EPITHELIAL CELLS; IMMUNOHISTOCHEMISTRY; INTESTINAL MUCOSA; MICE; NIH 3T3 CELLS; RECOMBINANT FUSION PROTEINS; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION;

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

EID: 8544245668     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2004.04336.x     Document Type: Article

References (74)

1. Abdul-Manan, N., Aghazadeh, B., Liu, G.A., Majumdar, A., Ouerfelli, O., Siminovitch, K.A., and Rosen, M.K. (1999) Structure of Cdc42 in complex with the GTPase-binding domain of the Wiskott-Aldrich syndrome protein. Nature 399: 379-383.
2. Aepfelbacher, M., Trasak, C., Wilharm, G., Wiedemann, A., Truelzsch, K., Krauss, K., et al. (2003) Characterisation of YopT effects on Rho GTPases in Yersinia enterocolitica-infected cells. J Biol Chem 278: 33217-33223.
3. Andersen, J.S., Lyon, C.E., Fox, A.H., Leung, A.K., Lam, Y.W., Steen, H., et al. (2002) Directed proteomic analysis of the human nucleolus. Curr Biol 12: 1-11.
4. Bailey, M.J., Hughes, C., and Koronakis, V. (1996) Increased distal gene transcription by the elongation factor RfaH, a specialised homologue of NusG. Mol Microbiol 22: 729-737.
5. Beveridge, T.J. (1999) Structures of gram negative cell walls and their derived membrane vesicles. J Bacteriol 181: 4725-4733.
6. Brumell, J.H., Goosney, D.L., and Finlay, B.B. (2002) SifA, a type III secreted effector of Salmonella typhimurium, directs Salmonella-induced filament formation along microtubules. Traffic 3: 407-415.
7. Brumell, J.H., Kujat-Choy, S., Brown, N.F., Vallance, B.A., Knodler, L.A., and Finlay, B.B. (2003) SopD2 is a novel type III secreted effector of Salmonella typhimurium that targets late endocytic compartments upon delivery into host cells. Traffic 4: 36-48.
8. Buchwald, G., Friebel, A., Galán, J.E., Hardt, W.D., Wittinghofer, A., and Scheffzek, K. (2002) Structural basis for the reversible activation of a Rho protein by the bacterial toxin SopE. EMBO J 21: 3286-3295.
9. Cezanne, L., Navarro, L., and Tocanne, J.F. (1992) Isolation of the plasma membrane and organelles from Chinese hamster ovary cells. Biochem Biophys Acta 1112: 205-214.
10. Collazo, C.M., and Galán, J.E. (1997) The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host cell. Mol Microbiol 24: 747-756.
11. Conrad, P.A., Smart, E.J., Ying, Y.S., Anderson, R.S., and Bloom, G.S. (1995) Caveolin cycles between plasma membrane caveolae and the Golgi complex by microtubule-dependent and microtubule-independent steps. J Cell Biol 131: 1421-1433.
12. Crago, A.M., and Koronakis, V. (1998) Salmonella InvG forms a ring-like multimer that requires the InvH lipoprotein for outer membrane localisation. Mol Microbiol 30: 47-56.
13. Ehrbar, K., Friebel, A., Miller, S.I., and Hardt, W.-D. (2003) Role of the Salmonella pathogenicity island 1 (SPI-1) protein InvB in type III secretion of SopE and SopE2, two Salmonella effector proteins encoded outside of SPI-1. J Bacteriol 185: 6950-6967.
14. Feng, Y., Wente, S.R., and Majerus, P.W. (2001) Overexpression of the inositol phosphatase SopB in human 293 cells stimulates cellular chloride influx and inhibits nuclear mRNA export. Proc Natl Acad Sci USA 98: 875-879.
15. Finlay, B.B., and Falkow, S. (1997) Common themes in microbial pathogenicity revisited. Microbiol Mol Biol Rev 61: 136-169.
16. Fraser, G.M., Bennett, J.C., and Hughes, C. (1999) Substrate-specific binding of hook-associated proteins by FlgN and FliT, putative chaperones for flagellum assembly. Mol Microbiol 32: 569-580.
17. Freeman, U.A., Ohl, M.E., and Miller, S.I. (2003) The Salmonella enterica serovar Typhimurium translocated effectors SseJ and SifB are targeted to the Salmonella containing vacuole. Infect Immun 71: 418-427.
18. Frithz-Lindsten, E., Du, Y., Rosqvist, R., and Forsberg, A. (1997) Intracellular targeting of exoenzyme S of Pseudomonas aeruginosa via type III-dependent translocation induces phagocytosis resistance, cytotoxicity, and disruption of actin microfilaments. Mol Microbiol 25: 1125-1139.
19. Fu, Y., and Galán, J.E. (1998) The Salmonella typhimurium tyrosine phosphatase SptP is translocated into host cells and disrupts the actin cytoskeleton. Mol Microbiol 27: 359-368.
20. Fu, Y., and Galán, J.E. (1999) A Salmonella protein antagonises Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401: 293-297.
21. Fu, H.-W., Beese, L.S., and Casey, P.J. (1994) Kinetic analysis of zinc ligand mutants of mammalian protein farnesyl-transferase. Biochemistry 37: 4465-4472.
22. Galán, J.E., and Collmer, A. (1999) Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284: 1322-1328.
23. Galyov, E.E., Wood, M.W., Rosqvist, R., Mullan, P.B., Watson, P.R., Hedges, S., and Wallis, T.S. (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.
24. Garner, M.J., Hayward, R.D., and Koronakis, V. (2002) The Salmonella pathogenicity island 1 secretion system directs cellular cholesterol redistribution during mammalian cell entry and intracellular trafficking. Cell Microbiol 4: 153-165.
25. Gauthier, A., de Grado, M., and Finlay, B.B. (2000) Mechanical fractionation reveals structural requirements for enteropathogenic Escherichia coli Tir insertion into host membranes. Infect Immun 68: 4344-4348.
26. Gulig, P.A., and Curtiss, R., III (1987) Plasmid-associated virulence of Salmonella typhimurium. Infect Immun 55: 2891-2901.
27. Hardt, W.-D., Chen, L.-M., Scheubel, K.E., Bustelo, X.R., Galán, J., and E. (1998) Salmonella typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93: 815-826.
28. Hayward, R.D., and Koronakis, V. (1999) Direct nucleation and bundling of actin by the SipC protein of invasive Salmonella. EMBO J 18: 4926-4934.
29. Hayward, R.D., and Koronakis, V. (2002) Direct modulation of the host cell cytoskeleton by Salmonella actin-binding proteins. Trends Cell Biol 12: 15-20.
30. Hayward, R.D., McGhie, E.J., and Koronakis, V. (2000) Membrane fusion activity of purified SipB, a Salmonella surface protein essential for mammalian cell invasion. Mol Microbiol 37: 727-739.
31. Hernandez, L.D., Hueffer, K., Wenk, M.R., and Galán, J.E. (2004) Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science 304: 1805-1807.
32. Higashide, W., Dai, S., Hombs, V.P., and Zhou, D. (2002) Involvement of SipA in modulating actin dynamics during Salmonella invasion into cultured epithelial cells. Cell Microbiol 4: 357-365.
33. Jepson, M.A., Kenny, B., and Leard, A.D. (2001) Role of sipA in the early stages of Salmonella typhimurium entry into epithelial cells. Cell Microbiol 3: 417-426.
34. Journet, L., Agrain, C., Broz, P., and Cornells, G.R. (2003) The needle length of bacterial injectisomes is determined by a molecular ruler. Science 302: 1757-1760.
35. Juris, S.J., Rudolph, A.E., Huddler, D., Orth, K., and Dixon, J.E. (2000) A distinctive role for the Yersinia protein kinase: actin binding, kinase activation and cytoskeletal disruption. Proc Natl Acad Sci USA 97: 9431-9436.
36. Kaniga, K., Tucker, S., Trollinger, D., and Galán, J.E. (1995) Homologues of the Shigella IpaB and IpaC invasins are required for Salmonella typhimurium entry into cultured epithelial cells. J Bacteriol 177: 3965-3971.
37. Kenny, B., and Warawa, J. (2001) Enteropathogenic Escherichia coli (EPEC) Tir receptor molecule does not undergo full modification when introduced into host cells by EPEC-independent mechanisms. Infect Immun 69: 1444-1453.
38. Kenny, B., DeVinney, R., Stein, M., Reinscheid, D.J., Frey, E.A., and Finlay, B.B. (1997) Enteropathogenic E. coli (EPEC) transfers its own receptor for intimate adherence into mammalian cells. Cell 91: 511-520.
39. Knodler, L.A., Vallance, B.A., Hensel, M., Jackel, D., Finlay, B.B., and Steele-Mortimer, O. (2003) Salmonella type III effectors PipB and PipB2 are targeted to detergent-resistant microdomains on internal host cell membranes. Mol Microbiol 49: 685-704.
40. Knutton, S., Rosenshine, I., Pallen, M.J., Nisan, B.C., Neves, C., Bain, C., et al. (1998) A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. EMBO J 17: 2166-2176.
41. Koronakis, V., Li, J., Koronakis, E., and Stauffer, K. (1997) Structure of TolC, the outer membrane component of the bacterial type I efflux system, derived from two dimensional crystals. Mol Microbiol 23: 617-626.
42. Kranewitter, W.J., Danninger, C., and Gimona, M. (2001) GEF at work: Vav in protruding filopodia. Cell Motil Cytoskeleton 49: 154-160.
43. Kubori, T., and Galán, J.E. (2003) Temporal regulation of Salmonella virulence effector function by proteosome-dependent protein degradation. Cell 115: 333-342.
44. Lilic, M., Galkin, V.E., Orlova, A., VanLoock, M.S., Egelman, E.H., and Stebbins, C.E. (2003) Salmonella SipA polymerises actin by stapling filaments with nonglobular protein arms. Science 301: 1918-1921.
45. Lin, S.L., Le, T.X., and Cowan, D.S. (2003) SptP, a Salmonella typhimurium type III-secreted protein, inhibits the mitogen-activated protein kinase pathway by inhibiting Raf activation. Cell Microbiol 5: 267-275.
46. McGhie, E.J., Hayward, R.D., and Koronakis, V. (2001) Cooperation between actin-binding proteins of invasive Salmonella: SipA potentiates SipC nucleation and bundling of actin. EMBO J 20: 2131-2139.
47. McGhie, E.J., Hayward, R.D., and Koronakis, V. (2004) Control of actin turnover by a Salmonella invasion protein. Mol Cell 13: 497-510.
48. Marcus, S.L., Knodler, L.A., and Finlay, B.B. (2002) Salmonella enterica serovar Typhimurium effector SigD/SopB is membrane-associated and ubiquitinated inside host cells. Cell Microbiol 4: 435-446.
49. Muramoto, K., Makishima, S., Aizawa, S.-I., and Macnab, R.M. (1998) Effect of cellular level of FliK on flagellar hook and filament assembly in Salmonella typhimurium. Mol Microbiol 277: 871-882.
50. Murli, S., Watson, R.O., and Galán, J.E. (2001) Role of tyrosine kinases and the tyrosine phosphatase SptP in the interaction of Salmonella with host cells. Cell Microbiol 3: 795-810.
51. Nobles, C.A., and Hall, A. (1995) Rho, Rac and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibres, lamellipodia and filopodia. Cell 81: 53-62.
52. Norris, F.A., Wilson, M.P., Wallis, T.S., Galyov, E.E., and Majerus, P.W. (1998) SopB, a protein required for virulence in S. dublin, is an inositol phosphate phosphatase. Proc Natl Acad Sci USA 95: 14057-14059.
53. Oh, P., and Schnitzer, J.E. (1999) Immunoisolation of caveolae with high affinity antibody binding to the oligomeric caveolin cage. Toward understanding the basis of purification. J Biol Chem 274: 23144-23154.
54. Ohnishi, K., Fan, F., Schoenhals, G.J., Kihara, M., and Macnab, R.M. (1997) The FliO, FliP, FliQ, and FliR proteins of Salmonella typhimurium: putative components for flagellar assembly. J Bacteriol 179: 6092-6099.
55. Osborn, M.J., and Munson, R. (1974) Separation of the inner (cytoplasmic) and outer membranes of gram-negative bacteria. Methods Enzymol 31: 642-653.
56. Osborn, M.J., Gander, J.E., Parisi, E., and Carson, J. (1972) Mechanism of assembly of the outer membrane of Salmonella typhimurium. Isolation and characterisation of cytoplasmic and outer membrane. J Biol Chem 247: 3973-3986.
57. Ren, Y., Li, R., Zheng, Y., and Busch, H. (1998) Cloning and characterisation of GEF-H1, a microtubule-associated guanine nucleotide exchange factor for Rac and Rho GTPases. J Biol Chem 273: 34954-34960.
58. Rosqvist, R., Magnusson, K.E., and Wolf-Watz, H. (1994) Target cell contact triggers expression and polarised transfer of Yersina YopE cytotoxin into mammalian cells. EMBO J 13: 964-972.
59. Ruiz-Albert, J., Yu, X.J., Beuzon, C.R., Blakey, A.N., Galyov, E.E., and Holden, D.W. (2002) Complimentary activities of SseJ and SifA regulate dynamics of the Salmonella typhimurium vacuolar membrane. Mol Microbiol 44: 645-661.
60. Russo, C., Gao, Y., Mancini, P., Vanni, C., Porotto, M., Falasca, M., et al. (2001) Modulation of oncogenic Dbl activity by phosphoinositol phosphate binding to pleckstrin homology domain. J Biol Chem 276: 19524-19531.
61. Scherer, C.A., Cooper, E., and Miller, S.I. (2000) The Salmonella type III secretion translocon protein SspC is inserted into the epithelial plasma membrane upon infection. Mol Microbiol 37: 1133-1145.
62. Stebbins, C.E., and Galán, J.E. (2000) Modulation of host signalling by a bacterial mimic: structure of the Salmonella effector SptP bound to Rac1. Mol Cell 6: 1449-1460.
63. Slender, S., Friebel, A., Linder, S., Rohde, M., Mirold, S., and Hardt, W.-D. (2000) Identification of SopE2 from Salmonella typhimurium, a conserved guanine nucleotide exchange factor for Cdc42 of the host cell. Mol Microbiol 36: 1206-1021.
64. Stolz, D.B., and Jacobson, B.S. (1992) Examination of transcellular membrane protein polarity of bovine aortic endothelial cells in vitro using the cationic colloidal silica microbead membrane-isolation procedure. J Cell Sci 103: 39-51.
65. Studier, M., and Moffat, B.A. (1986) Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189: 113-130.
66. Terebiznik, M.R., Vieira, O.V., Marcus, S.L., Slade, A., Yip, C.M., Trimble, W.S., et al. (2002) Elimination of host cell Ptdlns(4,5)P(2) by bacterial SigD promotes membrane fission during invasion by Salmonella. Nat Cell Biol 4:766-773.
67. Thanabalu, T., Koronakis, E., Hughes, C., and Koronakis, V. (1998) Substrate-induced assembly of a contiguous channel for protein export from E. coli: reversible bridging of an inner membrane translocase to an outer membrane exit channel. EMBO J 17: 6487-6496.
68. Tran Van Nhieu, G., Caron, E., Hall, A., and Sansonetti, P.J. (1999) IpaC induces actin polymerisation and filopodia formation during Shigella entry into epithelial cells. EMBO J 18: 3249-3262.
69. Tucker, S.C., and Galán, J.E. (2000) Complex function for SicA, a Salmonella enterica serovar Typhimurium type III secretion-associated chaperone. J Bacteriol 182: 2262-2268.
70. Wood, M.W., Rosqvist, R., Mullan, P.B., Edwards, M.H., and Galyov, E.E. (1996) SopE, a secreted protein of Salmonella dublin is translocated into the eukaryotic cell via a sip-dependent mechanism and promotes bacterial entry. Mol Microbiol 22: 327-338.
71. Yamaguchi, S., Fujita, H., Sugata, K., Taira, T., and Iino, T. (1984) Genetic analysis of H2, the structural gene for phase-2 flagellin in Salmonella. J Gen Microbiol 130: 255-265.
72. Zhou, D., and Galán, J.E. (2000) Striking a balance: modulation of the actin cytoskeleton by Salmonella. Proc Natl Acad Sci USA 97: 8754-8761.
73. Zhou, D., Mooseker, M.S., and Galán, J.E. (1999) Role of the S. typhimurium actin-binding protein SipA in bacterial internalisation. Science 283: 2092-2095.
74. Zhou, D., Chen, L.-M., Hernandez, L., Shears, S.B., and Galán, J.E. (2001) A Salmonella inositol polyphosphatase acts in concert with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalisation. Mol Microbiol 39: 248-259.