Analysis of the mechanisms of Salmonella-induced actin assembly during invasion of host cells and intracellular replication

Cellular Microbiology

Volumn 6, Issue 11, 2004, Pages 1041-1055

  Unsworth, Kate E ^a   Way, Michael ^b   McNiven, Mark ^c   Machesky, Laura ^d   Holden, David W ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^c MAYO CLINIC   (United States)

^d UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN 3; BACTERIAL PROTEIN; CORTACTIN; DYNAMIN; F ACTIN; GUANOSINE TRIPHOSPHATASE; METHENAMINE; PROTEIN CDC42; RAC PROTEIN; RHO FACTOR;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; BACTERIAL VIRULENCE; CELL INVASION; CELL SPREADING; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOSKELETON; EUKARYOTE; GENETIC TRANSFECTION; HELA CELL; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INTRACELLULAR SPACE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DETERMINATION; PROTEIN EXPRESSION; RNA INTERFERENCE; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; SEROTYPE; SIGNAL TRANSDUCTION;

ACTIN-RELATED PROTEIN 2; ACTIN-RELATED PROTEIN 3; ACTINS; BACTERIAL PROTEINS; CYTOSKELETAL PROTEINS; GENE EXPRESSION REGULATION; GTP-BINDING PROTEINS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICROFILAMENT PROTEINS; NERVE TISSUE PROTEINS; PROTEINS; SALMONELLA TYPHIMURIUM; WISKOTT-ALDRICH SYNDROME PROTEIN FAMILY; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

BACTERIA (MICROORGANISMS); EUKARYOTA; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM;

EID: 6344241120     PISSN: 14625814     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2004.00417.x     Document Type: Article

References (64)

1. Bakshi, C.S., Singh, V.P., Wood, M.W., Jones, P.W., Wallis, T.S., and Galyov, E.E. (2000) Identification of SopE2, a Salmonella secreted protein which is highly homologous to SopE and involved in bacterial invasion of epithelial cells. J Bacteriol 182: 2341-2344.
2. Beuzon, C.R., Meresse, S., Unsworth, K.E., Ruiz-Albert, J., Garvis, S., Waterman, S.R., et al. (2000) Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J 19: 3235-3249.
3. Bierne, H., Gouin, E., Roux, P., Caroni, P., Yin, H.L., and Cossart, P. (2001) A role for cofilin and LIM kinase in Listeria induced phagocytosis. J Cell Biol 155: 101-112.
4. Burbelo, P.D., Drechsel, D., and Hall, A. (1995) A conserved binding motif defines numerous candidate target proteins for both Cdc42 and Rac GTPases. J Biol Chem 270: 29071-29074.
5. Cantarelli, V.V., Takahashi, A., Akeda, Y., Nagayama, K., and Honda, T. (2000) Interaction of enteropathogenic or enterohemorrhagic Escherichia coli with HeLa cells results in translocation of cortactin to the bacterial adherence site. Infect Immun 68: 382-386.
6. Cantarelli, V.V., Takahashi, A., Yanagihara, I., Akeda, Y., Imura, K., Kodama, T., et al. (2002) Cortactin is necessary for F-actin accumulation in pedestal structures induced by enteropathogenic Escherichia coli infection. Infect Immun 70: 2206-2209.
7. Cao, H., Garcia, F., and McNiven, M.A. (1998) Differential distribution of dynamin isoforms in mammalian cells. Mol Biol Cell 9: 2595-2609.
8. Cao, H., Thompson, H.M., Krueger, E.W., and McNiven, M.A. (2000) Disruption of Golgi structure and function in mammalian cells expressing a mutant dynamin. J Cell Sci 113: 1993-2002.
9. Chen, L.M., Hobbie, S., and Galan, J.E. (1996b) Requirement of cdc42 for Salmonella-induced cytoskeletal and nuclear responses. Science 274: 2115-2118.
10. Chen, L.M., Kaniga, K., and Galan, J.E. (1996a) Salmonella spp. are cytotoxic for cultured macrophages. Mol Microbiol 21 1101-1115.
11. Criss, A.K., Ahlgren, D.M., Jou, T.S., McCormick, B.A., and Casanova, J.E. (2001) The GTPase Rac1 selectively regulates Salmonella invasion at the apical plasma membrane of polarized epithelial cells. J Cell Sci 114: 1331-1341.
12. Criss, A.K., and Casanova, J.E. (2003) Coordinate regulation of Salmonella enterica serovar Typhimurium invasion of epithelial cells by the Arp2/3 complex and Rho GTPases. Infect Immun 71: 2885-2891.
13. Elbashir, S.M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K., and Tuschl, T. (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411: 494-498.
14. Friebel, A., Ilchmann, H., Aepfelbacher, M., Ehrbar, K., Machleidt, W., and Hardt, W.D. (2001) SopE and SopE2 from Salmonella typhimurium activate different sets of Rho GTPases of the host cell. J Biol Chem 276: 34035-34040.
15. Frischknecht, F., and Way, M. (2001) Surfing pathogens and the lessons learned for actin polymerization. Trends Cell Biol 11: 30-38.
16. Fu, Y., and Galan, J.E. (1999) A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401: 293-297.
17. 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.
18. Hardt, W.D., Chen, L.M., Schuebel, K.E., Bustelo, X.R., and Galan, J.E. (1998b) S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93: 815-826.
19. Hardt, W.D., Urlaub, H., and Galan, J.E. (1998a) 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.
20. 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.
21. 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.
22. Hensel, M., Shea, J.E., Waterman, S.R., Mundy, R., Nikolaus, T., Banks, G., 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.
23. 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.
24. Huang, C., Ni, Y., Wang, T., Gao, Y., Haudenschild, C.C., and Zhan, X. (1997) Down-regulation of the filamentous actin cross-linking activity of cortactin by Src-mediated tyrosine phosphorylation. J Biol Chem 272: 13911-13915.
25. 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.
26. Just, I., Selzer, J., Wilm, M., von Eichel-Streiber, C., Mann, M., and Aktories, K. (1995) Glucosylation of Rho proteins by Clostridium difficile toxin B. Nature 375: 500-503.
27. Kalman, D., Weiner, O.D., Goosney, D.L., Sedat, J.W., Finlay, B.B., Abo, A., and Bishop, J.M. (1999) Enteropathogenic E. coli acts through WASP and Arp2/3 complex to form actin pedestals. Nat Cell Biol 1: 389-391.
28. Launay, S., Brown, G., and Machesky, L.M. (2003) Expression of WASP and Scar1/WAVE1 actin-associated proteins is differentially modulated during differentiation of HL-60 cells. Cell Motil Cytoskeleton 54: 274-285.
29. Levine, M.M., Nataro, J.P., Karch, H., Baldini, M.M., Kaper, J.B., Black, R.E., et al. (1985) The diarrheal response of humans to some classic serotypes of enteropathogenic Escherichia coli is dependent on a plasmid encoding an enteroadhesiveness factor. J Infect Dis 152: 550-559.
30. Lilic, M., Galkin, V.E., Orlova, A., VanLoock, M.S., Egelman, E.H., and Stebbins, C.E. (2003) Salmonella SipA polymerizes actin by stapling filaments with nonglobular protein arms. Science 301 1918-1921.
31. Machesky, L.M., and Insall, R.H. (1998) Scar1 and the related Wiskott-Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex. Curr Biol 8: 1347-1356.
32. McGee, K., Zettl, M., Way, M., and Fallman, M. (2001) A role for N-WASP in invasin-promoted internalisation. FEBS Lett 509 59-65.
33. 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.
34. McNiven, M.A., Kim, L., Krueger, E.W., Orth, J.D., Cao, H., and Wong, T.W. (2000) Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J Cell Biol 151: 187-198.
35. Meresse, S., Unsworth, K.E., Habermann, A., Griffiths, G., Fang, F., Martinez-Lorenzo, M.J., et al. (2001) Remodelling of the actin cytoskeleton is essential for replication of intravacuolar Salmonella. Cell Microbiol 3: 567-577.
36. Miao, E.A., Brittnacher, M., Haraga, A., Jeng, R.L., Welch, M.D., and Miller, S.I. (2003) Salmonella effectors translocated across the vacuolar membrane interact with the actin cytoskeleton. Mol Microbiol 48: 401-415.
37. Miki, H., Sasaki, T., Takai, Y., and Takenawa, T. (1998) Induction of filopodium formation by a WASP-related actin-depolymerizing protein N-WASP. Nature 391: 93-96.
38. Moreau, V., Frischknecht, F., Reckmann, I., Vincentelli, R., Rabut, G., Stewart, D., and Way, M. (2000) A complex of N-WASP and WIP integrates signalling cascades that lead to actin polymerization. Nat Cell Biol 2: 441-448.
39. Mukherjee, K., Parashuraman, S., Raje, M., and Mukhopadhyay, A. (2001) SopE acts as an Rab5-specific nucleotide exchange factor and recruits non-prenylated Rab5 on Salmonella-containing phagosomes to promote fusion with early endosomes. J Biol Chem 276: 23607-23615.
40. Mullins, R.D., Heuser, J.A., and Pollard, T.D. (1998) The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc Natl Acad Sci USA 95: 6181-6186.
41. Pruyne, D., Evangelista, M., Yang, C., Bi, E., Zigmond, S., Bretscher, A., and Boone, C. (2002) Role of formins in actin assembly: nucleation and barbed-end association. Science 297: 612-615.
42. Ruiz-Albert, J., Yu, X.J., Beuzon, 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.
43. Sagot, I., Rodal, A.A., Moseley, J., Goode, B.L., and Pellman, D. (2002) An actin nucleation mechanism mediated by Bni1 and Profilin. Nat Cell Biol 4: 626-631.
44. Satoh, S., and Tominaga, T. (2001) mDia-interacting protein acts downstream of Rho-mDia and modifies Src activation and stress fiber formation. J Biol Chem 276: 39290-39294.
45. Scherer, C.A., Cooper, E., and Miller, S.I. (2000) The Salmonella type III secretion translocon protein SspC is inserted into the epithelial cell plasma membrane upon infection. Mol Microbiol 37: 1133-1145.
46. Stender, 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: 1206-1221.
47. Svitkina, T.M., and Borisy, G.G. (1999) Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J Cell Biol 145: 1009-1026.
48. Takenawa, T., and Miki, H. (2001) WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J Cell Sci 114: 1801-1809.
49. Thompson, H.M., and McNiven, M.A. (2001) Dynamin: switch or pinchase? Curr Biol 11: R850.
50. Tominaga, T., Sahai, E., Chardin, P., McCormick, F., Courtneidge, S.A., and Alberts, A.S. (2000) Diaphanous-related formins bridge Rho GTPase and Src tyrosine kinase signaling. Mol Cell 5 13-25.
51. Tsuji, T., Ishizaki, T., Okamoto, M., Higashida, C., Kimura, K., Furuyashiki, T., et al. (2002) ROCK and mDia1 antagonize in Rho-dependent Rac activation in Swiss 3T3 fibroblasts. J Cell Biol 157: 819-830.
52. Uruno, T., Liu, J., Yansong, L., Smith, N., and Zhan, X. (2003) Sequential interaction of Actin-related Proteins 2 and 3 (Arp2/3) Complex with Neural Wiscott-Aldrich Syndrome Protein (N-WASP) and cortactin during branched actin filament network formation. J Biol Chem 278: 26086-26093.
53. Uruno, T., Liu, J., Zhang, P., Fan, Y., Egile, C., Li, R., et al. (2001) Activation of Arp2/3 complex-mediated actin polymerization by cortactin. Nat Cell Biol 3: 259-266.
54. Valdivia, R.H., and Falkow, S. (1996) Bacterial genetics by flow cytometry: rapid isolation of Salmonella typhimurium acid-inducible promoters by differential fluorescence induction. Mol Microbiol 22: 367-378.
55. Watanabe, N., Kato, T., Fujita, A., Ishizaki, T., and Narumiya, S. (1999) Cooperation between mDia1 and ROCK in Rho-induced actin reorganization. Nat Cell Biol 1: 136-143.
56. Weaver, A.M., Heuser, J.E., Karginov, A.V., Lee, W.L., Parsons, J.T., and Cooper, J.A. (2002) Interaction of cortactin and N-WASp with Arp2/3 complex. Curr Biol 12: 1270-1278.
57. Weaver, A.M., Karginov, A.V., Kinley, A.W., Weed, S.A., Li, Y., Parsons, J.T., and Cooper, J.A. (2001) Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr Biol 11: 370-374.
58. Weed, S.A., Karginov, A.V., Schafer, D.A., Weaver, A.M., Kinley, A.W., Cooper, J.A., and Parsens, J.T. (2000) Cortactin localization to sites of actin assembly in lamellipodia requires interactions with F-actin and the Arp2/3 complex. J Cell Biol 151: 29-40.
59. Welch, M.D., Iwamatsu, A., and Mitchison, T.J. (1997) Actin polymerization is induced by Arp2/3 protein complex at the surface of Listeria monocytogenes. Nature 385: 265-269.
60. Wray, C., and Sojka, W.J. (1978) Experimental Salmonella typhimurium infection in calves. Res Vet Sci 25: 139-143.
61. Yu, X.J., Ruiz-Albert, J., Unsworth, K.E., Garvis, S., Liu, M., and Holden, D.W. (2002) SpiC is required for secretion of Salmonella Pathogenicity Island 2 type III secretion system proteins. Cell Microbiol 4: 531-540.
62. Zhou, D. (2001) Collective efforts to modulate the host actin cytoskeleton by Salmonella type III-secreted effector proteins. Trends Microbiol 9: 567-569; discussion 569-570.
63. Zhou, D., Mooseker, M.S., and Galan, J.E. (1999a) An invasion-associated Salmonella protein modulates the actin-bundling activity of plastin. Proc Natl Acad Sci USA 96: 10176-10181.
64. Zhou, D., Mooseker, M.S., and Galan, J.E. (1999b) Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science 283: 2092-2095.