Salmonella type III secretion effectors: Pulling the host cell's strings

Current Opinion in Microbiology

Volumn 9, Issue 1, 2006, Pages 46-54

  Schlumberger, Markus C ^a   Hardt, Wolf Dietrich ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN;

CELL INVASION; EFFECTOR CELL; HOST CELL; IMMUNE RESPONSE; INTESTINE CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; REVIEW; SALMONELLA;

ANIMALS; BACTERIAL PROTEINS; CYTOPLASMIC VESICLES; HUMANS; PROTEIN TRANSPORT; SALMONELLA; SALMONELLA INFECTIONS; SALMONELLA INFECTIONS, ANIMAL; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); SALMONELLA;

EID: 31844438569     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2005.12.006     Document Type: Review

References (86)

1. M.E. Ohl, and S.I. Miller Salmonella: a model for bacterial pathogenesis Annu Rev Med 52 2001 259 274
2. I. Hansen-Wester, and M. Hensel Salmonella pathogenicity islands encoding type III secretion systems Microbes Infect 3 2001 549 559
3. J.E. Galan Salmonella interactions with host cells: type III secretion at work Annu Rev Cell Dev Biol 17 2001 53 86
4. T.S. Wallis, and E.E. Galyov Molecular basis of Salmonella-induced enteritis Mol Microbiol 36 2000 997 1005
5. S. Hapfelmeier, and W.D. Hardt A mouse model for S. typhimurium-induced enterocolitis Trends Microbiol 13 2005 497 503
6. S.R. Waterman, and D.W. Holden Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system Cell Microbiol 5 2003 501 511
7. V. Kuhle, and M. Hensel Cellular microbiology of intracellular Salmonella enterica: functions of the type III secretion system encoded by Salmonella pathogenicity island 2 Cell Mol Life Sci 61 2004 2812 2826
8. C. Cheminay, A. Mohlenbrink, and M. Hensel Intracellular Salmonella inhibit antigen presentation by dendritic cells J Immunol 174 2005 2892 2899
9. J. Bispham, B.N. Tripathi, P.R. Watson, and T.S. Wallis Salmonella pathogenicity island 2 influences both systemic salmonellosis and Salmonella-induced enteritis in calves Infect Immun 69 2001 367 377
10. S. Hapfelmeier, B. Stecher, M. Barthel, M. Kremer, A. Müller, M. Heikenwalder, T. Stallmach, M. Hensel, K. Pfeffer, and S. Akira The Salmonella pathogenicity island (SPI)-1 and SPI-2 type III secretion systems allow Salmonella Serovar typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms J Immunol 174 2005 1675 1685
11. B. Coburn, Y. Li, D. Owen, B.A. Vallance, and B.B. Finlay Salmonella enterica Serovar Typhimurium pathogenicity island 2 is necessary for complete virulence in a mouse model of infectious enterocolitis Infect Immun 73 2005 3219 3227
12. I. Hautefort, M.J. Proenca, and J.C. Hinton Single-copy green fluorescent protein gene fusions allow accurate measurement of Salmonella gene expression in vitro and during infection of mammalian cells Appl Environ Microbiol 69 2003 7480 7491
13. M.C. Schlumberger, A.J. Muller, K. Ehrbar, B. Winnen, I. Duss, B. Stecher, and W.D. Hardt Real-time imaging of type III secretion: Salmonella SipA injection into host cells Proc Natl Acad Sci USA 102 2005 12548 12553 Using time-lapse microscopy, this study visualizes the type III injection of SipA in real-time. Coupled with quantitative measurements of SipA levels and localization, it provides new insights into spatio-temporal aspects of effector protein interplay and illustrates the efficiency of type III secretion.
14. T. Kubori, Y. Matsushima, D. Nakamura, J. Uralil, M. Lara-Tejero, A. Sukhan, J.E. Galan, and S.I. Aizawa Supramolecular structure of the Salmonella typhimurium type III protein secretion system Science 280 1998 602 605
15. M.K. Zierler, and J.E. Galan Contact with cultured epithelial cells stimulates secretion of Salmonella typhimurium invasion protein InvJ Infect Immun 63 1995 4024 4028
16. R. Menard, P. Sansonetti, and C. Parsot The secretion of the Shigella flexneri Ipa invasins is activated by epithelial cells and controlled by IpaB and IpaD EMBO J 13 1994 5293 5302
17. M. Watarai, T. Tobe, M. Yoshikawa, and C. Sasakawa Contact of Shigella with host cells triggers release of Ipa invasins and is an essential function of invasiveness EMBO J 14 1995 2461 2470
18. R. Rosqvist, K.E. Magnusson, and H. Wolf-Watz Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells EMBO J 13 1994 964 972
19. L.J. Mota, L. Journet, I. Sorg, C. Agrain, and G.R. Cornelis Bacterial injectisomes: needle length does matter Science 307 2005 1278
20. M.A. Jepson, B. Kenny, and A.D. Leard Role of sipA in the early stages of Salmonella typhimurium entry into epithelial cells Cell Microbiol 3 2001 417 426
21. D. Buttner, and U. Bonas Port of entry - the type III secretion translocon Trends Microbiol 10 2002 186 192
22. D. Roy, D.R. Liston, V.J. Idone, A. Di, D.J. Nelson, C. Pujol, J.B. Bliska, S. Chakrabarti, and N.W. Andrews A process for controlling intracellular bacterial infections induced by membrane injury Science 304 2004 1515 1518
23. K. Kaniga, S. Tucker, D. Trollinger, and J.E. Galan Homologs of the Shigella IpaB and IpaC invasins are required for Salmonella typhimurium entry into cultured epithelial cells J Bacteriol 177 1995 3965 3971
24. M.W. Wood, R. Rosqvist, P.B. Mullan, M.H. Edwards, and E.E. Galyov 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 1996 327 338
25. C.M. Collazo, and J.E. Galan The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host cell Mol Microbiol 24 1997 747 756
26. R.D. Hayward, E.J. McGhie, and V. Koronakis Membrane fusion activity of purified SipB, a Salmonella surface protein essential for mammalian cell invasion Mol Microbiol 37 2000 727 739
27. C.A. Scherer, E. Cooper, and S.I. Miller The Salmonella type III secretion translocon protein SspC is inserted into the epithelial cell plasma membrane upon infection Mol Microbiol 37 2000 1133 1145
28. E.J. McGhie, P.J. Hume, R.D. Hayward, J. Torres, and V. Koronakis Topology of the Salmonella invasion protein SipB in a model bilayer Mol Microbiol 44 2002 1309 1321
29. W.L. Picking, H. Nishioka, P.D. Hearn, M.A. Baxter, A.T. Harrington, A. Blocker, and W.D. Picking IpaD of Shigella flexneri is independently required for regulation of Ipa protein secretion and efficient insertion of IpaB and IpaC into host membranes Infect Immun 73 2005 1432 1440
30. R.D. Hayward, R.J. Cain, E.J. McGhie, N. Phillips, M.J. Garner, and V. Koronakis Cholesterol binding by the bacterial type III translocon is essential for virulence effector delivery into mammalian cells Mol Microbiol 56 2005 590 603 This study describes the direct binding of SipB and its Shigella homologue IpaB to cholesterol in the host plasma membrane, and highlights the importance of this interaction for translocon assembly and subsequent effector protein delivery into the host cell.
31. M.J. Garner, R.D. Hayward, and V. Koronakis The Salmonella pathogenicity island 1 secretion system directs cellular cholesterol redistribution during mammalian cell entry and intracellular trafficking Cell Microbiol 4 2002 153 165
32. F.G. van der Goot, G. Tran van Nhieu, A. Allaoui, P. Sansonetti, and F. Lafont Rafts can trigger contact-mediated secretion of bacterial effectors via a lipid-based mechanism J Biol Chem 279 2004 47792 47798
33. J.C. Patel, and J.E. Galan Manipulation of the host actin cytoskeleton by Salmonella - all in the name of entry Curr Opin Microbiol 8 2005 10 15
34. M. Lilic, and C.E. Stebbins Re-structuring the host cell: up close with Salmonella's molecular machinery Microbes Infect 6 2004 1205 1211
35. D.G. Guiney, and M. Lesnick Targeting of the actin cytoskeleton during infection by Salmonella strains Clin Immunol 114 2005 248 255
36. D. Zhou, M.S. Mooseker, and J.E. Galan Role of the S. typhimurium actin-binding protein SipA in bacterial internalization Science 283 1999 2092 2095
37. E.J. McGhie, R.D. Hayward, and V. Koronakis Cooperation between actin-binding proteins of invasive Salmonella: SipA potentiates SipC nucleation and bundling of actin EMBO J 20 2001 2131 2139
38. M. Lilic, V.E. Galkin, A. Orlova, M.S. VanLoock, E.H. Egelman, and C.E. Stebbins Salmonella SipA polymerizes actin by stapling filaments with nonglobular protein arms Science 301 2003 1918 1921
39. E.J. McGhie, R.D. Hayward, and V. Koronakis Control of actin turnover by a salmonella invasion protein Mol Cell 13 2004 497 510 This study illustrates how the direct interaction of SipA with F-actin affects the function of host actin depolimerizing factors ADF/cofilin and gelsolin, highlighting the ability of SipA to locally modulate the host machinery of actin reorganization.
40. R.D. Hayward, and V. Koronakis Direct nucleation and bundling of actin by the SipC protein of invasive Salmonella EMBO J 18 1999 4926 4934
41. J. Chang, J. Chen, and D. Zhou Delineation and characterization of the actin nucleation and effector translocation activities of Salmonella SipC Mol Microbiol 55 2005 1379 1389 This is the first study to delineate the actin nucleating activity of SipC from its general role in TTSS-1 effector protein translocation, providing the first insights into the role of SipC in actin remodelling in vivo.
42. W. Higashide, S. Dai, V.P. Hombs, and D. Zhou Involvement of SipA in modulating actin dynamics during Salmonella invasion into cultured epithelial cells Cell Microbiol 4 2002 357 365
43. D. Zhou, L.M. Chen, L. Hernandez, S.B. Shears, and J.E. Galan A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization Mol Microbiol 39 2001 248 260
44. S. Mirold, K. Ehrbar, A. Weissmüller, R. Prager, H. Tschäpe, H. Rüssmann, and W.D. Hardt Salmonella host cell invasion emerged by acquisition of a mosaic of separate genetic elements, including Salmonella pathogenicity island 1 (SPI1), SPI5, and sopE2 J Bacteriol 183 2001 2348 2358
45. W.D. Hardt, L.M. Chen, K.E. Schuebel, X.R. Bustelo, and J.E. Galan S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells Cell 93 1998 815 826
46. M.G. Rudolph, C. Weise, S. Mirold, B. Hillenbrand, B. Bader, A. Wittinghofer, and W.D. Hardt Biochemical analysis of SopE from Salmonella typhimurium, a highly efficient guanosine nucleotide exchange factor for RhoGTPases J Biol Chem 274 1999 30501 30509
47. S. Stender, A. Friebel, S. Linder, M. Rohde, S. Mirold, and W.D. Hardt Identification of SopE2 from Salmonella typhimurium, a conserved guanine nucleotide exchange factor for Cdc42 of the host cell Mol Microbiol 36 2000 1206 1221
48. G. Buchwald, A. Friebel, J.E. Galan, W.D. Hardt, A. Wittinghofer, and K. Scheffzek Structural basis for the reversible activation of a Rho protein by the bacterial toxin SopE EMBO J 21 2002 3286 3295
49. M.C. Schlumberger, A. Friebel, G. Buchwald, K. Scheffzek, A. Wittinghofer, and W.D. Hardt Amino acids of the bacterial toxin SopE involved in G-nucleotide exchange on Cdc42 J Biol Chem 278 2003 27149 27159
50. C. Williams, E.E. Galyov, and S. Bagby solution structure, backbone dynamics, and interaction with Cdc42 of Salmonella guanine nucleotide exchange factor SopE2 Biochemistry 43 2004 11998 12008
51. A. Friebel, H. Ilchmann, M. Aelpfelbacher, K. Ehrbar, W. Machleidt, and W.D. Hardt SopE and SopE2 from Salmonella typhimurium activate different sets of RhoGTPases of the host cell J Biol Chem 276 2001 34035 34040
52. A.K. Criss, D.M. Ahlgren, T.S. Jou, B.A. McCormick, and J.E. Casanova The GTPase Rac1 selectively regulates Salmonella invasion at the apical plasma membrane of polarized epithelial cells J Cell Sci 114 2001 1331 1341
53. F.A. Norris, M.P. Wilson, T.S. Wallis, E.E. Galyov, and P.W. Majerus SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase Proc Natl Acad Sci USA 95 1998 14057 14059
54. A. Aleman, I. Rodriguez-Escudero, G.V. Mallo, V.J. Cid, M. Molina, and R. Rotger The amino-terminal non-catalytic region of Salmonella typhimurium SigD affects actin organization in yeast and mammalian cells Cell Microbiol 7 2005 1432 1446
55. A.K. Criss, and J.E. Casanova Coordinate regulation of Salmonella enterica serovar Typhimurium invasion of epithelial cells by the Arp2/3 complex and Rho GTPases Infect Immun 71 2003 2885 2891
56. H.N. Higgs, and T.D. Pollard Regulation of actin filament network formation through ARP2/3 complex: activation by a diverse array of proteins Annu Rev Biochem 70 2001 649 676
57. K.E. Unsworth, M. Way, M. McNiven, L. Machesky, and D.W. Holden Analysis of the mechanisms of Salmonella-induced actin assembly during invasion of host cells and intracellular replication Cell Microbiol 6 2004 1041 1055
58. J. Shi, G. Scita, and J.E. Casanova WAVE2 signaling mediates invasion of polarized epithelial cells by Salmonella typhimurium J Biol Chem 280 2005 29849 29855
59. T.E. Stradal, K. Rottner, A. Disanza, S. Confalonieri, M. Innocenti, and G. Scita Regulation of actin dynamics by WASP and WAVE family proteins Trends Cell Biol 14 2004 303 311
60. T. Kubori, and J.E. Galan Temporal regulation of salmonella virulence effector function by proteasome-dependent protein degradation Cell 115 2003 333 342
61. Y. Fu, and J.E. Galan A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion Nature 401 1999 293 297
62. S.L. Marcus, M.R. Wenk, O. Steele-Mortimer, and B.B. Finlay A synaptojanin-homologous region of Salmonella typhimurium SigD is essential for inositol phosphatase activity and Akt activation FEBS Lett 494 2001 201 207
63. M.R. Terebiznik, O.V. Vieira, S.L. Marcus, A. Slade, C.M. Yip, W.S. Trimble, T. Meyer, B.B. Finlay, and S. Grinstein Elimination of host cell PtdIns(4,5)P(2) by bacterial SigD promotes membrane fission during invasion by Salmonella Nat Cell Biol 4 2002 766 773
64. D. Drecktrah, L.A. Knodler, and O. Steele-Mortimer Modulation and utilization of host cell phosphoinositides by Salmonella spp Infect Immun 72 2004 4331 4335
65. L.D. Hernandez, K. Hueffer, M.R. Wenk, and J.E. Galan Salmonella modulates vesicular traffic by altering phosphoinositide metabolism Science 304 2004 1805 1807
66. L.A. Knodler, B.B. Finlay, and O. Steele-Mortimer The Salmonella effector protein SopB protects epithelial cells from apoptosis by sustained activation of Akt J Biol Chem 280 2005 9058 9064
67. D. Drecktrah, L.A. Knodler, K. Galbraith, and O. Steele-Mortimer The Salmonella SPI1 effector SopB stimulates nitric oxide production long after invasion Cell Microbiol 7 2005 105 113 This study describes the prolonged presence of SopB inside the host cell after injection and its role in stimulation of nitric oxide production hours after bacterial invasion. It demonstrates that TTSS-1 effectors can still be active after induction of TTSS-2 and highlights the multiple roles of SopB.
68. D. Chakravortty, I. Hansen-Wester, and M. Hensel Salmonella pathogenicity island 2 mediates protection of intracellular Salmonella from reactive nitrogen intermediates J Exp Med 195 2002 1155 1166
69. A. Tierrez, and F. Garcia-del Portillo New concepts in Salmonella virulence: the importance of reducing the intracellular growth rate in the host Cell Microbiol 7 2005 901 909
70. E. Boucrot, T. Henry, J.P. Borg, J.P. Gorvel, and S. Meresse The intracellular fate of Salmonella depends on the recruitment of kinesin Science 308 2005 1174 1178 This study demonstrates that the TTSS-2 effector SifA targets the host protein SKIP to control the association of the SCV with kinesin. This provides a molecular mechanism of how TTSS-2 effectors delicately balance the activity of microtubule motors to create and maintain a replication-permissive intracellular niche.
71. R.E. Harrison, J.H. Brumell, A. Khandani, C. Bucci, C.C. Scott, X. Jiang, B.B. Finlay, and S. Grinstein Salmonella impairs RILP recruitment to Rab7 during maturation of invasion vacuoles Mol Biol Cell 15 2004 3146 3154
72. M. Marsman, I. Jordens, C. Kuijl, L. Janssen, and J. Neefjes Dynein-mediated vesicle transport controls intracellular Salmonella replication Mol Biol Cell 15 2004 2954 2964
73. J.H. Brumell, S. Kujat-Choy, N.F. Brown, B.A. Vallance, L.A. Knodler, and B.B. Finlay SopD2 is a novel type III secreted effector of Salmonella typhimurium that targets late endocytic compartments upon delivery into host cells Traffic 4 2003 36 48
74. X. Jiang, O.W. Rossanese, N.F. Brown, S. Kujat-Choy, J.E. Galan, B.B. Finlay, and J.H. Brumell The related effector proteins SopD and SopD2 from Salmonella enterica serovar Typhimurium contribute to virulence during systemic infection of mice Mol Microbiol 54 2004 1186 1198
75. J. Ruiz-Albert, X.J. Yu, C.R. Beuzon, A.N. Blakey, E.E. Galyov, and D.W. Holden Complementary activities of SseJ and SifA regulate dynamics of the Salmonella typhimurium vacuolar membrane Mol Microbiol 44 2002 645 661
76. J.A. Freeman, M.E. Ohl, and S.I. Miller The Salmonella enterica serovar typhimurium translocated effectors SseJ and SifB are targeted to the Salmonella-containing vacuole Infect Immun 71 2003 418 427
77. L.A. Knodler, and O. Steele-Mortimer The Salmonella effector PipB2 affects Late endosome/lysosome distribution to mediate Sif extension Mol Biol Cell 16 2005 4108 4123
78. R.L. Guy, L.A. Gonias, and M.A. Stein Aggregation of host endosomes by Salmonella requires SPI2 translocation of SseFG and involves SpvR and the fms-aroE intragenic region Mol Microbiol 37 2000 1417 1435
79. V. Kuhle, and M. Hensel 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 2002 813 824
80. V. Kuhle, D. Jackel, and M. Hensel Effector proteins encoded by Salmonella pathogenicity island 2 interfere with the microtubule cytoskeleton after translocation into host cells Traffic 5 2004 356 370
81. D. Chakravortty, M. Rohde, L. Jager, J. Deiwick, and M. Hensel Formation of a novel surface structure encoded by Salmonella pathogenicity Island 2 EMBO J 24 2005 2043 2052
82. S. Dai, P.D. Sarmiere, O. Wiggan, J.R. Bamburg, and D. Zhou Efficient Salmonella entry requires activity cycles of host ADF and cofilin Cell Microbiol 6 2004 459 471
83. C.A. Mueller, P. Broz, S.A. Muller, P. Ringler, F. Erne-Brand, I. Sorg, M. Kuhn, A. Engel, and G.R. Cornelis The V-antigen of Yersinia forms a distinct structure at the tip of injectisome needles Science 310 2005 674 676
84. J. Enninga, J. Mounier, P. Sansonetti, and G.T. Nhieu Secretion of type III effectors into host cells in real time Nat Methods 2 2005 959 965
85. B.K. Coombes, M.E. Wickham, N.F. Brown, S. Lemire, L. Bossi, W.W. Hsiao, F.S. Brinkman, and B.B. Finlay Genetic and molecular analysis of GogB, a phage-encoded type III-secreted substrate in Salmonella enterica serovar typhimurium with autonomous expression from its associated phage J Mol Biol 348 2005 817 830
86. K. Geddes, M. Worley, G. Niemann, and F. Heffron Identification of new secreted effectors in Salmonella enterica serovar Typhimurium Infect Immun 73 2005 6260 6271