Enhanced actin pedestal formation by enterohemorrhagic Escherichia coli O157:H7 adapted to the mammalian host

Frontiers in Microbiology

Volumn 2, Issue NOV, 2011, Pages

  Brady, Michael John ^a   Radhakrishnan, Padhma ^a   Liu, Hui ^a   Magoun, Loranne ^a   Murphy, Kenan C ^a   Mukherjee, Jean ^b   Donohue Rolfe, Arthur ^b   Tzipori, Saul ^b   Leong, John M ^a,c  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b TUFTS UNIVERSITY   (United States)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Actin assembly; EHEC; Host adaptation; Intimin; Tir; Translocation

Indexed keywords

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MAMMALIA;

EID: 84874924977     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2011.00226     Document Type: Article

References (74)

1. Acheson, D. W., De Breucker, S. A., Jacewicz, M., Lincicome, L. L., Donohue-Rolfe, A., Kane, A. V., and Keusch, G. T. (1995). Expression and purification of Shiga-like toxin II B subunits. Infect. Immun. 63, 301-308.
2. Agin, T. S., and Wolf, M. K. (1997). Identification of a family of intimins common to Escherichia coli causing attaching-effacing lesions in rabbits, humans, and swine. Infect. Immun. 65, 320-326.
3. Ando, H., Abe, H., Sugimoto, N., and Tobe, T. (2007). Maturation of functional type III secretion machinery by activation of anaerobic respiration in enterohaemor-rhagic Escherichia coli. Microbiology 153,464-473.
4. Antunes, L. C., Ferreira, R. B., Buckner, M. M.,andFinlay,B. B. (2010). Quorum sensing in bacterial virulence. Microbiology 156,2271-2282.
5. Bhatt, S., Romeo, T., and Kalman, D. (2011). Honing the message: post-transcriptional and post-translational control in attaching and effacing pathogens. Trends Microbiol. 19,217-224.
6. Bishop, A. L., Wiles, S., Dougan, G., and Frankel, G. (2007). Cell attachment properties and infectiv-ity of host-adapted and environmentally adapted Citrobacter roden-tium. Microbes Infect. 9,1316-1324.
7. Campellone, K. G. (2010). Cytoskeleton-modulating effectors of enteropathogenic, and enterohaemorrhagic Escherichia coli: Tir, EspFU, and actin pedestal assembly. FEBSJ. 277, 2390-2402.
8. Campellone, K. G., Giese, A., Tipper, D J., and Leong, J. M. (2002). A tyrosine-phosphorylated 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.
9. Campellone, K. G., and Leong, J. M. (2003). Tails of two Tirs: actin pedestal formation by enteropathogenic E. coli and enterohemorrhagic E. coli O157:H7. Curr. Opin. Micro biol. 6, 82-90.
10. Campellone, K. G., Robbins, D., and Leong, J. M. (2004). EspFU is a translocated EHEC effector that interacts with Tir and N-WASP and promotes Nck-independent actin assembly. Dev. Cell 7, 217-228.
11. Campellone, K. G., Roe, A. J., Lobner-Olesen, A., Murphy, K. C., Magoun, L., Brady, M. J., Donohue-Rolfe, A., Tzipori, S., Gally, D. L., Leong, J. M., and Marinus, M. G. (2007). Increased adherence and actin pedestal formation by dam-deficient enterohaemorrhagic Escherichia coli O157:H7. Mol. Microbiol. 63, 1468-1481.
12. Cantey, R. J., and Moseley, S. L. (1991). HeLa cell adherence, actin aggregation, and invasion by noneteropath-ogenic Escherichia coli possessing the eae gene. Infect. Immun. 59, 3924-3929.
13. Casadaban, M. J., and Cohen, S. N. (1980). Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J. Mol. Biol. 138, 179-207.
14. Celli, J., Deng, W., and Finlay, B. B. (2000). Enteropathogenic Escherichia coli (EPEC) attachment to epithelial cells: exploiting the host cell cytoskeleton from the outside. Cell. Microbiol. 2,1-9.
15. Crepin, V. F., Girard, F., Schüller, S., Phillips, A. D., Mousnier, A., and Frankel, G. (2010). Dissecting the role of the Tir:Nck and Tir:IRTKS/IRSp53 signalling pathways in vivo. Mol. Microbiol. 75, 308-323.
16. DeVinney, R., Stein, M., Reinscheid, D., Abe, A., Ruschkowski, S., and Finlay,B. B. (1999). Enterohemorrhagic Escherichia coli O157:H7 produces Tir, which is translocated to the host cell membrane but is not tyrosine phosphorylated. Infect. Immun. 67, 2389-2398.
17. Donnenberg, M. S., Giron, J. A., Nataro, J. P., and Kaper, J. B. (1992). A plasmid-encoded type IV fimbrial gene of enteropathogenic Escherichia coli associated with localized adherence. Mol. Microbiol. 6, 3427-3437.
18. Donnenberg, M. S., Lai, L. C., Taylor, K. A. (1997). The locus of entero-cyte effacement pathogenicity island of enteropathogenic Escherichia coli encodes secretion functions and remnants of transposons at its extreme right end. Gene. 184, 107-114.
19. Donnenberg, M. S., Yu, J., and Kaper, J. B. (1993). A second chromosomal gene necessary for intimate attachment of enteropatho-genic Escherichia coli to epithelial cells. J. Bacteriol. 175, 4670-4680.
20. Donohue-Rolfe, A., Kondova, I., Oswald, S., Hutto, D., and Tzipori, S. (2000). Escherichia coli O157:H7 strains that express Shiga toxin (Stx) 2 alone are more neurotropic for gnotobiotic piglets than are isotypes producing only Stx1 or both Stx1 and Stx2. J. Infect. Dis. 181,1825-1829.
21. Ebel, F., Deibel, C., Kresse, A. U., Guzman, C. A., and Chakraborty, T. (1996). Temperature- and medium-dependent secretion of proteins by Shiga toxin- producing Escherichia coli. Infect. Immun. 64, 4472-4479.
22. Ebel, F., Podzadel, T., Rohde, M., Kresse, A. U., Kramer, S., Deibel, C., Guzman, C. A., and Chakraborty, T. (1998). Initial binding of Shiga toxin-producing Escherichia coli to host cells and subsequent induction of actin rearrangements depend on filamentous EspA-containing surface appendages. Mol. Microbiol. 30, 147-161.
23. Frankel, G., Lider, O., Hershkoviz, R., Mould, A. P., Kachalsky, S. G., Candy, D., Cahalon, L., Humphries, M. J., and Dougan, G. (1996). The cell-binding domain of intimin from enteropathogenic Escherichia coli binds to beta1 integrins. J. Biol. Chem. 271,20359-20364.
24. Frankel, G., Philips, A. D., Novakova, M., Batchelor, M., Hicks, S., and Dougan, G. (1998). Generation of Escherichia coli intimin derivatives with differing biological activities using site-directed mutagenesis of the intimin C-terminus domain. Mol. Microbiol. 29,559-570.
25. Frankel, G., and Phillips, A. D. (2008). Attaching effacing Escherichia coli and paradigms of Tir-triggered actin polymerization: getting off the pedestal. Cell. Microbiol. 10, 549-556.
26. Garmendia, J., Phillips, A. D., Carlier, M. F., Chong, Y., Schuller, S., Marches, O., Dahan, S., Oswald, E., Shaw, R. K., Knutton, S., and Frankel, G. (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.
27. Hansen, A. M., and Kaper, J. B. (2009). Hfq affects the expression of the LEE pathogenicity island in enterohaemorrhagic Escherichia coli. Mol. Microbiol. 73, 446-465.
28. Hayward, R. D., Leong, J. M., Koronakis, V., and Campellone, K. G. (2006). Exploiting pathogenic Escherichia coli to model transmembrane receptor signalling. Nat. Rev. Microbiol. 4, 358-370.
29. House, B., Kus, J. V., Prayitno, N., Mair, R., Que, L., Chingcuanco, F., Gannon, V., Cvitkovitch, D. G., and Barnett Foster, D. (2009). Acid-stress-induced changes in enterohaemorrhagic Escherichia coli O157: H7 virulence. Microbiology 155, 2907-2918.
30. Jerse, A. E., Yu, J., Tall, B. D., and Kaper, J. B. (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. USA 87, 7839-7843.
31. Karch, H., Heesemann, J., Laufs, R., O'Brien, A. D., Tacket, C. O., and Levine, M. M. (1987). A plasmid of enterohemorrhagic Escherichia coli O157:H7 is required for expression of a new fimbrial antigen and for adhesion to epithelial cells. Infect. Immun. 55, 455-461.
32. Karmali, M. A. (1989). Infection by verocytotoxin-producing Escherichia coli. Clin. Microbiol. Rev. 2, 15-38.
33. Kenny, B. (1999). Phosphorylation of tyrosine 474 of the enteropathogenic Escherichia coli (EPEC) Tir receptor molecule is essential for actin nucleating activity and is preceded by additional host modifications. Mol. Microbiol. 31, 1229-1241.
34. Kenny, B., Devinney, R., Stein, M., Reinscheid, D. J., Frey, E. A., and Finlay, B. B. (1997). Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91, 511-520.
35. Knutton, S., Baldwin, T., Williams, P. H., and Mcneish, A. S. (1989). Actin accumulation at sites of bacterial adhesion to tissue culture cells: basis of a new diagnostic test for enteropathogenic and enterohemorrhagic Escherichia coli. Infect. Immun. 57, 1290-1298.
36. Labigne-Roussel, A. F., Lark, D., School-nik, G., and Falkow, S. (1984). Cloning and expression of an afim-brial adhesin (AFA-I) responsible for P blood group-independent, mannose-resistant hemag-glutination from a pyelonephritic Escherichia coli strain. Infect. Immun. 46,251-259.
37. Liu, H., Magoun, L., and Leong, J. M. (1999a). β1-Chain integrins are not essential for intimin-mediated host cell attachment and enteropatho-genic Escherichia coli-mediated actin polymerization. Infect. Immun. 67, 2045-2049.
38. Liu, H., Magoun, L., Luperchio, S., Schauer, D. B., and Leong, J. M. (1999b). The Tir-binding region of enterohaemorrhagic Escherichia coli intimin is sufficient to trigger actin condensation after bacterial-induced host cell signalling. Mol. Microbiol. 34,67-81.
39. Liu, H., Radhakrishnan, P., Magoun, L., Prabu, M., Campellone, K. G., Savage, P., He, F., Schiffer, C. A., and Leong, J. M. (2002). Point mutants of EHEC intimin that diminish Tir recognition and actin pedestal formation highlight a putative Tir binding pocket. Mol Microbiol. 45, 1557-1573.
40. McDaniel, T. K., Jarvis, K. G., Don-nenberg, M. S., and Kaper, J. B. (1995). A genetic locus of entero-cyte effacement conserved among diverse enterobacterial pathogens. Proc. Natl. Acad. Sci. U.S.A. 92, 1664-1668.
41. McDaniel, T. K., and Kaper, J. B. (1997). A cloned pathogenicity island from enteropathogenic Escherichia coli confers the attaching and effacing phenotype on E. coli K-12. Mol. Microbiol. 23, 399-407.
42. McKee, M. L., and O'Brien, A. D. (1996). Truncated enterohem-orrhagic Escherichia coli (EHEC) O157:H7 intimin (EaeA) fusion proteins promote adherence of EHEC strains to HEp-2 cells. Infect. Immun. 64,2225-2233.
43. Mellies, J. L., Barron, A. M., and Carmona,A. M. (2007). Enteropathogenic and enterohemorrhagic Escherichia coli virulence gene regulation. Infect. Immun. 75, 4199-4210.
44. Merrell, D. S., Butler, S. M., Qadri, F., Dolganov, N. A., Alam, A., Cohen, M. B., Calderwood, S. B., School-nik, G. K., and Camilli, A. (2002). Host-induced epidemic spread of the cholera bacterium. Nature 417, 642-645.
45. Mundy, R., Pickard, D., Wilson, R. K., Simmons, C. P., Dougan, G., and Frankel, G. (2003). Identification of a novel type IV pilus gene cluster required for gastrointestinal colonization of Citrobacter rodentium. Mol. Microbiol. 48, 795-809.
46. Murphy, K. C., and Campellone, K. G. (2003). Lambda red-mediated recombinogenic engineering of enterohemorrhagic and enteropathogenic E. coli. BMCMol. Biol. 4, 11. doi:10.1186/1471-2199-4-11
47. Murphy, K. C., Ritchie, J. M., Waldor, M. K., Lobner-Olesen, A., and Marinus, M. G. (2008). Dam methyltrans-ferase is required for stable lysogeny of the Shiga toxin (Stx2)-encoding bacteriophage 933W of enterohemorrhagic Escherichia coli O157:H7. J. Bacteriol. 190,438-441.
48. Musken, A., Bielaszewska, M., Greune, L., Schweppe, C. H., Muthing, J., Schmidt, H., Schmidt, M. A., Karch, H., and Zhang, W. (2008). Anaerobic conditions promote expression of Sfp fimbriae and adherence of sorbitol-fermenting enterohemorrhagic Escherichia coli O157:NM to human intestinal epithelial cells. Appl. Environ. Microbiol. 74, 1087-1093.
49. Nataro, J. P., and Kaper, J. B. (1998). Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11, 142-201.
50. Noel, J. M., and Boedeker, E. C. (1997). Enterohemorrhagic Escherichia coli: a family of emerging pathogens. Dig. Dis. 15,67-91. [Review].
51. Pai, C. H., Kelly, J. K., and Meyers, G. L. (1986). Experimental infection of infant rabbits with verotoxin-producing Escherichia coli. Infect. Immun. 51, 16-23.
52. Puente, J. L., Bieber, D., Ramer, S. W., Murray, W., and Schoolnik, G. K. (1996). The bundle-forming pili of enteropathogenic Escherichia coli: transcriptional regulation by environmental signals. Mol. Microbiol. 20, 87-100.
53. Riley, L. W., Remis, R. S., Helgerson, S. D., Mcgee, H. B., Wells, J. G., Davis, B. R., Hebert, R. J., Olcott, E. S., Johnson, L. M., Hargrett, N. T., Blake, P. A., and Cohen, M. L. (1983). Hem-orrhagic colitis associated with a rare Escherichia coli serotype. N. Engl. J. Med. 308,681-685.
54. Ritchie, J. M., Brady, M. J., Riley, K. N., Ho, T. D., Campellone, K. G., Herman, I. M., Donohue-Rolfe, A., Tzi-pori, S., Waldor, M. K., and Leong, J. M. (2008). EspFU, a type III-translocated effector of actin assembly, fosters epithelial association and late-stage intestinal colonization by E. coli O157:H7. Cell. Microbiol. 10, 836-847.
55. Rosenshine, I., Ruschkowski, S., and Finlay, B. B. (1996). Expression of attaching/effacing activity by enteropathogenic Escherichia coli depends on growth phase, temperature, and protein synthesis upon contact with epithelial cells. Infect. Immun. 64, 966-973.
56. Sanchez-SanMartin, C., Bustamante, V. H., Calva, E., and Puente, J. L. (2001). Transcriptional regulation of the orf19 gene and the tir-cesT-eae operon of enteropathogenic Escherichia coli. J. Bacteriol. 183,2823-2833.
57. Shakhnovich, E. A., Davis, B. M., and Waldor, M. K. (2009). Hfqnegatively regulates type III secretion in EHEC and several other pathogens. Mol. Microbiol. 74, 347-363.
58. Sinclair, J. F., and O'Brien, A. D. (2002). Cell surface-localized nucleolin is a eukaryotic receptor for the adhesin intimin-gamma of enterohemorrhagic Escherichia coli O157:H7. J. Biol. Chem. 277, 2876-2885.
59. Spears, K. J., Roe, A. J., and Gally, D. L. (2006). A comparison of enteropathogenic and enterohaemorrhagic Escherichia coli pathogen-esis. FEMS Microbiol. Lett. 255, 187-202.
60. Sperandio, V., Mellies, J. L., Nguyen, W., Shin, S., and Kaper, J. B. (1999). Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 96, 15196-15201.
61. Teel, L. D., Steinberg, B. R., Aronson, N. E., and O'Brien, A. D. (2003). Shiga toxin-producing Escherichia coli-associated kidney failure in a 40-year-old patient and late diagnosis by novel bacteriologic and toxin detection methods. J. Clin. Microbiol. 41,3438-3440.
62. Tzipori, S., Gunzer, F., Donnenberg, M. S., De Montigny L., Kaper, J. B., and Donohue-Rolfe, A. (1995). The role of the eaeA gene in diarrhea and neurological complications in a gno-tobiotic piglet model of enterohemorrhagic Escherichia coli infection. Infect. Immun. 63, 3621-3627.
63. Tzipori, S., Karch, H., Wachsmuth, K. I., Robins-Browne, R. M., O'Brien, A. D., Lior, H., Cohen, M. L., Smithers, J., and Levine, M. M. (1987). Role of a 60-megadalton plasmid and Shiga-like toxins in the pathogenesis of infection caused by enterohemorrhagic Escherichia coli O157:H7 in gnotobiotic piglets. Infect. Immun. 55,3117-3125.
64. Tzipori, S., Montanaro, J., Robins-Browne, R. M., Vial, P., Gibson, R., and Levine, M. M. (1992). Studies with enteroaggregative Escherichia coli in the gnotobiotic piglet gastroenteritis model. Infect. Immun. 60, 5302-5306.
65. Vingadassalom, D., Campellone, K. G., Brady, M. J., Skehan, B., Battle, S. E., Robbins, D., Kapoor, A., Hecht, G., Snapper, S. B., and Leong, J. M. (2010). Enterohemorrhagic E. coli requires N-WASP for efficient type III translocation but not for EspFU-mediated actin pedestal formation. PLoS Pathog. 6, e1001056. doi:10.1371/journal.ppat.1001056
66. Vlisidou, I., Dziva, F., La Ragione, R. M., Best, A., Garmendia, J., Hawes, P., Monaghan, P., Cawthraw, S. A., Frankel, G., Woodward, M. J., and Stevens, M. P. (2006). Role of intimin-tir interactions and the tir-cytoskeleton coupling protein in the colonization of calves and lambs by Escherichia coli O157:H7. Infect. Immun. 74, 758-764.
67. Warawa, J., and Kenny, B. (2001). Phosphoserine modification of the enteropathogenic Escherichia coli Tir molecule is required to trigger con-formational changes in Tir and efficient pedestal elongation. Mol. Microbiol. 42, 1269-1280.
68. Wiles, S., Dougan, G., and Frankel, G. (2005). Emergence of a "hyperin-fectious" bacterial state after passage of Citrobacter rodentium through the host gastrointestinal tract. Cell. Microbiol. 7, 1163-1172.
69. Xicohtencatl-Cortes, J., Monteiro-Neto, V., Ledesma, M. A., Jordan, D. M., Francetic, O., Kaper, J. B., Puente, J. L., and Giron, J. A. (2007). Intestinal adherence associated with type IV pili of enterohemorrhagic Escherichia coli O157:H7. J. Clin. Invest. 117,3519-3529.
70. Xicohtencatl-Cortes, J., Monteiro-Neto, V., Saldana, Z., Ledesma, M. A., Puente, J. L., and Giron, J. A. (2009). The type 4 pili of enterohemorrhagic Escherichia coli O157:H7 are multipurpose structures with pathogenic attributes. J. Bacteriol. 191, 411-421.
71. Yin, X., Chambers, J. R., Wheatcroft, R., Johnson, R. P., Zhu, J., Liu, B., and Gyles, C. L. (2009a). Adherence of Escherichia coli O157:H7 mutants in vitro and in ligated pig intestines. Appl. Environ. Microbiol. 75,4975-4983.
72. Yin, X., Wheatcroft, R., Chambers, J. R., Liu, B., Zhu, J., and Gyles, C. L. (2009b). Contributions of O island 48 to adherence of enterohemorrhagic Escherichia coli O157:H7 to epithelial cells in vitro and in ligated pig ileal loops. Appl. Environ. Microbiol. 75, 5779-5786.
73. Yin, X., Zhu, J., Feng, Y., Chambers, J. R., Gong, J., and Gyles, C. L. (2011). Differential gene expression and adherence of Escherichia coli O157:H7 in vitro and in ligated pig intestines. PLoS ONE 6, e17424. doi:10.1371/journal.pone.00 17424
74. Zahavi, E. E., Lieberman, J. A., Donnenberg, M. S., Nitzan, M., Baruch, K., Rosenshine, I., Turner, J. R., Melamed-Book, N., Feinstein, N., Zlotkin-Rivkin, E., and Aroeti, B. (2011). Bundle forming pilus retraction enhances enteropathogenic Escherichia coli infectivity. Mol. Biol. Cell. 22, 2436-2447.