The T3SS effector EspT defines a new category of invasive enteropathogenic E. coli (EPEC) which form intracellular actin pedestals

PLoS Pathogens

Volumn 5, Issue 12, 2009, Pages

  Bulgin, Richard ^a   Arbeloa, Ana ^a   Goulding, David ^b   Dougan, Gordon ^b   Crepin, Valerie F ^a   Raymond, Benoit ^a   Frankel, Gad ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; GUANOSINE TRIPHOSPHATASE; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; P21 ACTIVATED KINASE; PROTEIN ABI1; PROTEIN CDC42; PROTEIN WAVE 2; RAC1 PROTEIN; UNCLASSIFIED DRUG; ESCHERICHIA COLI PROTEIN; ESPT PROTEIN, E COLI; WISKOTT ALDRICH SYNDROME PROTEIN;

ACTIN POLYMERIZATION; BACTERIAL CELL; BACTERIAL STRAIN; BACTERIUM ADHERENCE; CELL INVASION; CELL VACUOLE; CITROBACTER RODENTIUM; CONFERENCE PAPER; ENTEROPATHOGENIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI INFECTION; MEMBRANE FORMATION; NONHUMAN; PLASMID; TONOPLAST; TYPE III SECRETION SYSTEM; ANIMAL; ARTICLE; CELL MEMBRANE; CELL STRAIN 3T3; CELL STRAIN CACO 2; CONFOCAL MICROSCOPY; ESCHERICHIA COLI INFECTION; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TRANSFECTION; HELA CELL; HUMAN; METABOLISM; MICROBIOLOGY; MOUSE; PATHOGENICITY; PHYSIOLOGY; PSEUDOPODIUM; SCANNING ELECTRON MICROSCOPY; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY; VIRULENCE;

ESCHERICHIA COLI;

3T3 CELLS; ACTINS; ANIMALS; CACO-2 CELLS; CELL MEMBRANE; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HUMANS; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; PSEUDOPODIA; RAC1 GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; TRANSFECTION; VACUOLES; VIRULENCE; WISKOTT-ALDRICH SYNDROME PROTEIN FAMILY;

EID: 74549169867     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000683     Document Type: Conference Paper

References (69)

1. Nataro JP, Kaper JB (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11: 142-201.
2. Mundy R, MacDonald TT, Dougan G, Frankel G, Wiles S (2005) Citrobacter rodentium of mice and man. Cell Microbiol 7: 1697-1706.
3. Frankel G, Phillips AD (2008) Attaching effacing Escherichia coli and paradigms of Tir-triggered actin polymerization: getting off the pedestal. Cell Microbiol 10: 549-556.
4. Knutton S, Lloyd DR, McNeish AS (1987) Adhesion of enteropathogenic Escherichia coli to human intestinal enterocytes and cultured human intestinal mucosa. Infect Immun 55: 69-77.
5. Frankel G, Phillips AD, Rosenshine I, Dougan G, Kaper JB, et al. (1998) Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements. Mol Microbiol 30: 911-921.
6. Garmendia J, Frankel G, Crepin VF (2005) Enteropathogenic and enterohemorrhagic Escherichia coli infections: translocation, translocation, translocation. Infect Immun 73: 2573-2585.
7. Tobe T, Beatson SA, Taniguchi H, Abe H, Bailey CM, et al. (2006) An extensive repertoire of type III secretion effectors in Escherichia coli O157 and the role of lambdoid phages in their dissemination. Proc Natl Acad Sci U S A 103: 14941-14946.
8. Iguchi A, Thomson NR, Ogura Y, Saunders D, Ooka T, et al. (2009) Complete genome sequence and comparative genome analysis of enteropathogenic Escherichia coli O127:H6 strain E2348/69. J Bacteriol 191: 347-354.
9. Galan JE, Wolf-Watz H (2006) Protein delivery into eukaryotic cells by type III secretion machines. Nature 444: 567-573.
10. Coburn B, Sekirov I, Finlay BB (2007) Type III secretion systems and disease. Clin Microbiol Rev 20: 535-549.
11. Kenny B, DeVinney R, Stein M, Reinscheid DJ, Frey EA, et al. (1997) k. Cell 91: 511-520.
12. Frankel G, Phillips AD, Trabulsi LR, Knutton S, Dougan G, et al. (2001) Intimin and the host cell-is it bound to end in Tir(s)? Trends Microbiol 9: 214-218.
13. Matsuzawa T, Kuwae A, Yoshida S, Sasakawa C, Abe A (2004) Enteropathogenic Escherichia coli activates the RhoA signaling pathway via the stimulation of GEF-H1. Embo J 23: 3570-3582.
14. Kenny B, Jepson M (2000) Targeting of an enteropathogenic Escherichia coli (EPEC) effector protein to host mitochondria. Cell Microbiol 2: 579-590.
15. Arbeloa A, Bulgin RR, MacKenzie G, Shaw RK, Pallen MJ, et al. (2008) Subversion of actin dynamics by EspM effectors of attaching and effacing bacterial pathogens. Cell Microbiol 10: 1429-1441.
16. Alto NM, Shao F, Lazar CS, Brost RL, Chua G, et al. (2006) Identification of a bacterial type III effector family with G protein mimicry functions. Cell 124: 133-145.
17. Berger CN, Crepin VF, Jepson MA, Arbeloa A, Frankel G (2009) The mechanisms used by enteropathogenic Escherichia coli to control filopodia dynamics. Cell Microbiol 11: 309-322.
18. Jaffe AB, Hall A (2002) Rho GTPases in transformation and metastasis. Adv Cancer Res 84: 57-80.
19. Etienne-Manneville S, Hall A (2002) Rho GTPases in cell biology. Nature 420: 629-635.
20. Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21: 247-269.
21. Arbeloa A, Blanco M, Moreira FC, Bulgin R, Lopez C, et al. (2009) Distribution of espM and espT among enteropathogenic and enterohaemorrhagic Escherichia coli. J Med Microbiol 58: 988-995.
22. Viljanen MK, Peltola T, Junnila SY, Olkkonen L, Jarvinen H, et al. (1990) Outbreak of diarrhoea due to Escherichia coli O111:B4 in schoolchildren and adults: association of Vi antigen-like reactivity. Lancet 336: 831-834.
23. Bulgin RR, Arbeloa A, Chung JC, Frankel G (2009) EspT triggers formation of lamellipodia and membrane ruffles through activation of Rac-1 and Cdc42. Cell Microbiol 11: 217-229.
24. Buccione R, Orth JD, McNiven MA (2004) Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nat Rev Mol Cell Biol 5: 647-657.
25. Chhabra ES, Higgs HN (2007) The many faces of actin: matching assembly factors with cellular structures. Nat Cell Biol 9: 1110-1121.
26. Cossart P, Sansonetti PJ (2004) Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304: 242-248.
27. Yoshida S, Sasakawa C (2003) Exploiting host microtubule dynamics: a new aspect of bacterial invasion. Trends Microbiol 11: 139-143.
28. Hardt WD, Chen LM, Schuebel KE, Bustelo XR, Galan JE (1998) S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93: 815-826.
29. Patel JC, Galan JE (2006) Differential activation and function of Rho GTPases during Salmonella-host cell interactions. J Cell Biol 175: 453-463.
30. Tran Van Nhieu G, Caron E, Hall A, Sansonetti PJ (1999) IpaC induces actin polymerization and filopodia formation during Shigella entry into epithelial cells. Embo J 18: 3249-3262.
31. Mounier J, Popoff MR, Enninga J, Frame MC, Sansonetti PJ, et al. (2009) The IpaC carboxyterminal effector domain mediates Src-dependent actin polymerization during Shigella invasion of epithelial cells. PLoS Pathog 5: e1000271. doi:10.1371/journal.ppat.1000271.
32. Burton EA, Plattner R, Pendergast AM (2003) Abl tyrosine kinases are required for infection by Shigella flexneri. Embo J 22: 5471-5479.
33. Handa Y, Suzuki M, Ohya K, Iwai H, Ishijima N, et al. (2007) Shigella IpgB1 promotes bacterial entry through the ELMO-Dock180 machinery. Nat Cell Biol 9: 121-128.
34. Drucker MM, Polliack A, Yeivin R, Sacks TG (1970) Immunofluorescent demonstration of enteropathogenic Escherichia coli in tissues of infants dying with enteritis. Pediatrics 46: 855-864.
35. Donnenberg MS, Kaper JB (1992) Enteropathogenic Escherichia coli. Infect Immun 60: 3953-3961.
36. Hernandes RT, Silva RM, Carneiro SM, Salvador FA, Fernandes MC, et al. (2008) The localized adherence pattern of an atypical enteropathogenic Escherichia coli is mediated by intimin omicron and unexpectedly promotes HeLa cell invasion. Cell Microbiol 10: 415-425.
37. Ohya K, Handa Y, Ogawa M, Suzuki M, Sasakawa C (2005) IpgB1 is a novel Shigella effector protein involved in bacterial invasion of host cells. Its activity to promote membrane ruffling via Rac1 and Cdc42 activation. J Biol Chem 280: 24022-24034.
38. Jerse AE, Yu J, Tall BD, Kaper JB (1990) A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc Natl Acad Sci U S A 87: 7839-7843.
39. Miki H, Yamaguchi H, Suetsugu S, Takenawa T (2000) IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature 408: 732-735.
40. Legg JA, Bompard G, Dawson J, Morris HL, Andrew N, et al. (2007) N-WASP involvement in dorsal ruffle formation in mouse embryonic fibroblasts. Mol Biol Cell 18: 678-687.
41. Machuy N, Campa F, Thieck O, Rudel T (2007) c-Abl-binding protein interacts with p21-activated kinase 2 (PAK-2) to regulate PDGF-induced membrane ruffles. J Mol Biol 370: 620-632.
42. Innocenti M, Zucconi A, Disanza A, Frittoli E, Areces LB, et al. (2004) Abi1 is essential for the formation and activation of a WAVE2 signalling complex. Nat Cell Biol 6: 319-327.
43. Suetsugu S, Kurisu S, Oikawa T, Yamazaki D, Oda A, et al. (2006) Optimization of WAVE2 complex-induced actin polymerization by membrane-bound IRSp53, PIP(3), and Rac. J Cell Biol 173: 571-585.
44. Suetsugu S, Miki H, Takenawa T (1999) Identification of two human WAVE/ SCAR homologues as general actin regulatory molecules which associate with the Arp2/3 complex. Biochem Biophys Res Commun 260: 296-302.
45. Takenawa T, 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.
46. Kumar Y, Valdivia RH (2009) Leading a sheltered life: intracellular pathogens and maintenance of vacuolar compartments. Cell Host Microbe 5: 593-601.
47. Celli J, Deng W, Finlay BB (2000) Enteropathogenic Escherichia coli (EPEC) attachment to epithelial cells: exploiting the host cell cytoskeleton from the outside. Cell Microbiol 2: 1-9.
48. Donnenberg MS, Donohue-Rolfe A, Keusch GT (1989) Epithelial cell invasion: an overlooked property of enteropathogenic Escherichia coli (EPEC) associated with the EPEC adherence factor. J Infect Dis 160: 452-459.
49. Ladwein M, Rottner K (2008) On the Rho'd: the regulation of membrane protrusions by Rho-GTPases. FEBS Lett 582: 2066-2074.
50. Shi J, Scita G, Casanova JE (2005) WAVE2 signaling mediates invasion of polarized epithelial cells by Salmonella typhimurium. J Biol Chem 280: 29849-29855.
51. Steffen A, Rottner K, Ehinger J, Innocenti M, Scita G, et al. (2004) Sra-1 and Nap1 link Rac to actin assembly driving lamellipodia formation. Embo J 23: 749-759.
52. Schroeder GN, Hilbi H (2008) Molecular pathogenesis of Shigella spp.: controlling host cell signaling, invasion, and death by type III secretion. Clin Microbiol Rev 21: 134-156.
53. Steele-Mortimer O (2008) The Salmonella-containing vacuole: moving with the times. Curr Opin Microbiol 11: 38-45.
54. Campellone KG, Giese A, Tipper DJ, Leong JM (2002) A tyrosinephosphorylated 12-amino-acid sequence of enteropathogenic Escherichia coli Tir binds the host adaptor protein Nck and is required for Nck localization to actin pedestals. Mol Microbiol 43: 1227-1241.
55. Gruenheid S, DeVinney R, Bladt F, Goosney D, Gelkop S, et al. (2001) Enteropathogenic E. coli Tir binds Nck to initiate actin pedestal formation in host cells. Nat Cell Biol 3: 856-859.
56. Lommel S, Benesch S, Rottner K, Franz T, Wehland J, et al. (2001) Actin pedestal formation by enteropathogenic Escherichia coli and intracellular
57. Cossart P (1995) Actin-based bacterial motility. Curr Opin Cell Biol 7: 94-101.
58. Frischknecht F, Moreau V, Rottger S, Gonfloni S, Reckmann I, et al. (1999) Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signalling. Nature 401: 926-929.
59. Guiney DG, Lesnick M (2005) Targeting of the actin cytoskeleton during infection by Salmonella strains. Clin Immunol 114: 248-255.
60. Yam PT, Theriot JA (2004) Repeated cycles of rapid actin assembly and disassembly on epithelial cell phagosomes. Mol Biol Cell 15: 5647-5658.
61. Miyake K, McNeil PL, Suzuki K, Tsunoda R, Sugai N (2001) An actin barrier to resealing. J Cell Sci 114: 3487-3494.
62. Rodriguez A, Rioult MG, Ora A, Andrews NW (1995) A trypanosome-soluble factor induces IP3 formation, intracellular Ca2+ mobilization and microfilament rearrangement in host cells. J Cell Biol 129: 1263-1273.
63. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640-6645.
64. Schlosser-Silverman E, Elgrably-Weiss M, Rosenshine I, Kohen R, Altuvia S (2000) Characterization of Escherichia coli DNA lesions generated within J774 macrophages. J Bacteriol 182: 5225-5230.
65. Charpentier X, Oswald E (2004) Identification of the secretion and translocation domain of the enteropathogenic and enterohemorrhagic Escherichia coli effector Cif, using TEM-1 beta-lactamase as a new fluorescence-based reporter. J Bacteriol 186: 5486-5495.
66. Levine MM, Bergquist EJ, Nalin DR, Waterman DH, Hornick RB, et al. (1978) Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet 1: 1119-1122.
67. Garmendia J, Phillips AD, Carlier MF, Chong Y, Schuller S, et al. (2004) TccP is an enterohaemorrhagic Escherichia coli O157:H7 type III effector protein that couples Tir to the actin-cytoskeleton. Cell Microbiol 6: 1167-1183.
68. Hueck CJ, Hantman MJ, Bajaj V, Johnston C, Lee CA, et al. (1995) Salmonella typhimurium secreted invasion determinants are homologous to Shigella Ipa proteins. Mol Microbiol 18: 479-490.
69. Pelletier S, Julien C, Popoff MR, Lamarche-Vane N, Meloche S (2005) Cyclic AMP induces morphological changes of vascular smooth muscle cells by inhibiting a Rac-dependent signaling pathway. J Cell Physiol 204: 412-422.