1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Enterohemorrhagic Adhesins

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • PDF
    403.68 Kb
  • XML
    195.46 Kb
  • HTML
    188.56 Kb
  • Authors: Brian D. McWilliams1, Alfredo G. Torres2
  • Editors: Vanessa Sperandio3, Carolyn J. Hovde4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX 77555; 2: Department of Pathology and Sealy Center for Vaccine Development, University of Texas Medical Branch, Galveston, TX 77555; 3: University of Texas Southwestern Medical Center, Dallas, TX; 4: University of Idaho, Moscow, ID
    • Source: microbiolspec June 2014 vol. 2 no. 3 doi:10.1128/microbiolspec.EHEC-0003-2013
  • Received 30 April 2013 Accepted 29 July 2013 Published 20 June 2014
  • Alfredo G. Torres, [email protected]
image of Enterohemorrhagic <span class="jp-italic">Escherichia coli</span> Adhesins
    Preview this microbiology spectrum article:
    Preview Magnify
    Zoom in
    Zoomout

    Enterohemorrhagic Adhesins, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/2/3/EHEC-0003-2013-1.gif /docserver/preview/fulltext/microbiolspec/2/3/EHEC-0003-2013-2.gif

  • Abstract:

    Adhesins are a group of proteins in enterohemorrhagic (EHEC) that are involved in the attachment or colonization of this pathogen to abiotic (plastic or steel) and biological surfaces, such as those found in bovine and human intestines. This review provides the most up-to-date information on these essential adhesion factors, summarizing important historical discoveries and analyzing the current and future state of this research. In doing so, the proteins intimin and Tir are discussed in depth, especially regarding their role in the development of attaching and effacing lesions and in EHEC virulence. Further, a series of fimbrial proteins (Lpf1, Lpf2, curli, ECP, F9, ELF, Sfp, HCP, and type 1 fimbria) are also described, emphasizing their various contributions to adherence and colonization of different surfaces and their potential use as genetic markers in detection and classification of different EHEC serotypes. This review also discusses the role of several autotransporter proteins (EhaA-D, EspP, Saa and Sab, and Cah), as well as other proteins associated with adherence, such as flagella, EibG, Iha, and OmpA. While these proteins have all been studied to varying degrees, all of the adhesins summarized in this article have been linked to different stages of the EHEC life cycle, making them good targets for the development of more effective diagnostics and therapeutics.

  • Citation: McWilliams B, Torres A. 2014. Enterohemorrhagic Adhesins. Microbiol Spectrum 2(3):EHEC-0003-2013. doi:10.1128/microbiolspec.EHEC-0003-2013.

References

1. Francis DH, Collins JE, Duimstra JR. 1986. Infection of gnotobiotic pigs with an Escherichia coli O157:H7 strain associated with an outbreak of hemorrhagic colitis. Infect Immun 51:953–956. [PubMed]
2. Yu J, Kaper JB. 1992. Cloning and characterization of the eae gene of enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol 6:411–417. [PubMed][CrossRef]
3. Donnenberg MS, Tzipori S, McKee ML, O'Brien AD, Alroy J, Kaper JB. 1993. The role of the eae gene of enterohemorrhagic Escherichia coli in intimate attachment in vitro and in a porcine model. J Clin Invest 92:1418–1424. [PubMed][CrossRef]
4. Donnenberg MS, Tacket CO, James SP, Losonsky G, Nataro JP, Wasserman SS, Kaper JB, Levine MM. 1993. Role of the eaeA gene in experimental enteropathogenic Escherichia coli infection. J Clin Invest 92:1412–1417. [PubMed][CrossRef]
5. Torres AG, Kaper JB. 2002. Pathogenicity islands of intestinal E. coli. Pathogenicity islands (PAIs) and the evolution of pathogenic microbes. Curr Top Microbiol Immunol 264:31–48. [PubMed][CrossRef]
6. Stevens MP, Wallis TS. 29 August 2005, posting date Chapter 8.3.2.3, Adhesins of enterohemorrhagic Escherichia coli. In Böck A, et al. (ed), EcoSal— Escherichia coli and Salmonella: Cellular and Molecular Biology. ASM Press, Washington, DC. doi:10.1128/ecosal.8.3.2.3. [CrossRef]
7. McDaniel TK, Jarvis KG, Donnenberg MS, Kaper JB. 1995. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci USA 92:1664–1668. [PubMed][CrossRef]
8. Elliott SJ, Wainwright LA, McDaniel TK, Jarvis KG, Deng YK, Lai LC, McNamara BP, Donnenberg MS, Kaper JB. 1998. The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69. Mol Microbiol 28:1–4. [PubMed][CrossRef]
9. Perna NT, Mayhew GF, Posfai G, Elliott S, Donnenberg MS, Kaper JB, Blattner FR. 1998. Molecular evolution of a pathogenicity island from enterohemorrhagic Escherichia coli O157:H7. Infect Immun 66:3810–3817. [PubMed]
10. Zhu C, Agin TS, Elliott SJ, Johnson LA, Thate TE, Kaper JB, Boedeker EC. 2001. Complete nucleotide sequence and analysis of the locus of enterocyte effacement from rabbit diarrheagenic Escherichia coli RDEC-1. Infect Immun 69:2107–2115. [PubMed][CrossRef]
11. Tauschek M, Strugnell RA, Robins-Browne RM. 2002. Characterization and evidence of mobilization of the LEE pathogenicity island of rabbit-specific strains of enteropathogenic Escherichia coli. Mol Microbiol 44:1533–1550. [PubMed][CrossRef]
12. Deng W, Li Y, Vallance BA, Finlay BB. 2001. Locus of enterocyte effacement from Citrobacter rodentium: sequence analysis and evidence for horizontal transfer among attaching and effacing pathogens. Infect Immun 69:6323–6335. [PubMed][CrossRef]
13. Bretschneider G, Berberov EM, Moxley RA. 2007. Isotype-specific antibody responses against Escherichia coli O157:H7 locus of enterocyte effacement proteins in adult beef cattle following experimental infection. Vet Immunol Immunopathol 118:229–238. [PubMed][CrossRef]
14. Dean-Nystrom EA, Bosworth BT, Moon HW, O'Brien AD. 1998. Escherichia coli O157:H7 requires intimin for enteropathogenicity in calves. Infect Immun 66:4560–4563. [PubMed]
15. Judge NA, Mason HS, O'Brien AD. 2004. Plant cell-based intimin vaccine given orally to mice primed with intimin reduces time of Escherichia coli O157:H7 shedding in feces. Infect Immun 72:168–175. [PubMed][CrossRef]
16. Dziva F, van Diemen PM, Stevens MP, Smith AJ, Wallis TS. 2004. Identification of Escherichia coli O157:H7 genes influencing colonization of the bovine gastrointestinal tract using signature-tagged mutagenesis. Microbiology 150:3631–3645. [PubMed][CrossRef]
17. Cornick NA, Booher SL, Moon HW. 2002. Intimin facilitates colonization by Escherichia coli O157:H7 in adult ruminants. Infect Immun 70:2704–2707. [PubMed][CrossRef]
18. Ritchie JM, Thorpe CM, Rogers AB, Waldor MK. 2003. Critical roles for stx2, eae, and tir in enterohemorrhagic Escherichia coli-induced diarrhea and intestinal inflammation in infant rabbits. Infect Immun 71:7129–7139. [PubMed][CrossRef]
19. Abe A, Heczko U, Hegele RG, Brett FB. 1998. Two enteropathogenic Escherichia coli type III secreted proteins, EspA and EspB, are virulence factors. J Exp Med 188:1907–1916. [PubMed][CrossRef]
20. Ebel F, Deibel C, Kresse AU, Guzman CA, Chakraborty T. 1996. Temperature- and medium-dependent secretion of proteins by Shiga toxin-producing Escherichia coli. Infect Immun 64:4472–4479. [PubMed]
21. Kenny B, Finlay BB. 1995. Protein secretion by enteropathogenic Escherichia coli is essential for transducing signals to epithelial cells. Proc Natl Acad Sci USA 92:7991–7995. [PubMed][CrossRef]
22. Jarvis KG, Kaper JB. 1996. Secretion of extracellular proteins by enterohemorrhagic Escherichia coli via a putative type III secretion system. Infect Immun 64:4826–4829. [PubMed]
23. Hueck CJ. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62:379–433. [PubMed]
24. Gauthier A, Finlay BB. 2003. Translocated intimin receptor and its chaperone interact with ATPase of the type III secretion apparatus of enteropathogenic Escherichia coli. J Bacteriol 185:6747–6755. [CrossRef]
25. Garmendia J, Frankel G, Crepin VF. 2005. Enteropathogenic and enterohemorrhagic Escherichia coli infections: translocation, translocation, translocation. Infect Immun 73:2573–2585. [PubMed][CrossRef]
26. Sharp FC, Sperandio V. 2007. QseA directly activates transcription of LEE1 in enterohemorrhagic Escherichia coli. Infect Immun 75:2432–2440. [PubMed][CrossRef]
27. Atlung T, Ingmer H. 1997. H-NS: a modulator of environmentally regulated gene expression. Mol Microbiol 24:7–17. [PubMed][CrossRef]
28. Mellies JL, Elliott SJ, Sperandio V, Donnenberg MS, Kaper JB. 1999. The Per regulon of enteropathogenic Escherichia coli: identification of a regulatory cascade and a novel transcriptional activator, the locus of enterocyte effacement (LEE)-encoded regulator (Ler). Mol Microbiol 33:296–306. [PubMed][CrossRef]
29. Deng W, Puente JL, Gruenheid S, Li Y, Vallance BA, Vazquez A, Barba J, Ibarra JA, O'Donnell P, Metalnikov P, Ashman K, Lee S, Goode D, Pawson T, Finlay BB. 2004. Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci USA 101:3597–3602. [PubMed][CrossRef]
30. Kenny B, Abe A, Stein M, Finlay BB. 1997. Enteropathogenic Escherichia coli protein secretion is induced in response to conditions similar to those in the gastrointestinal tract. Infect Immun 65:2606–2612. [PubMed]
31. Bansal T, Jesudhasan P, Pillai S, Wood TK, Jayaraman A. 2008. Temporal regulation of enterohemorrhagic Escherichia coli virulence mediated by autoinducer-2. Appl Microbiol Biotechnol 78:811–819. [PubMed][CrossRef]
32. Sperandio V, Li CC, Kaper JB. 2002. Quorum-sensing Escherichia coli regulator A: a regulator of the LysR family involved in the regulation of the locus of enterocyte effacement pathogenicity island in enterohemorrhagic E. coli. Infect Immun 70:3085–3093. [CrossRef]
33. Abe H, Tatsuno I, Tobe T, Okutani A, Sasakawa C. 2002. Bicarbonate ion stimulates the expression of locus of enterocyte effacement-encoded genes in enterohemorrhagic Escherichia coli O157:H7. Infect Immun 70:3500–3509. [PubMed][CrossRef]
34. Yin X, Feng Y, Wheatcroft R, Chambers J, Gong J, Gyles CL. 2011. Adherence of Escherichia coli O157:H7 to epithelial cells in vitro and in pig gut loops is affected by bacterial culture conditions. Can J Vet Res 75:81–88. [PubMed]
35. Bansal T, Kim DN, Slininger T, Wood TK, Jayaraman A. 2012. Human intestinal epithelial cell-derived molecule(s) increase enterohemorrhagic Escherichia coli virulence. FEMS Immunol Med Microbiol 66:399–410. [PubMed][CrossRef]
36. Bhatt S, Edwards AN, Nguyen HT, Merlin D, Romeo T, Kalman D. 2009. The RNA binding protein CsrA is a pleiotropic regulator of the locus of enterocyte effacement pathogenicity island of enteropathogenic Escherichia coli. Infect Immun 77:3552–3568. [PubMed][CrossRef]
37. Russell RM, Sharp FC, Rasko DA, Sperandio V. 2007. QseA and GrlR/GrlA regulation of the locus of enterocyte effacement genes in enterohemorrhagic Escherichia coli. J Bacteriol 189:5387–5392. [PubMed][CrossRef]
38. Bustamante VH, Santana FJ, Calva E, Puente JL. 2001. Transcriptional regulation of type III secretion genes in enteropathogenic Escherichia coli: Ler antagonizes H-NS-dependent repression. Mol Microbiol 39:664–678. [PubMed][CrossRef]
39. Elliott SJ, Sperandio V, Giron JA, Shin S, Mellies JL, Wainwright L, Hutcheson SW, McDaniel TK, Kaper JB. 2000. The locus of enterocyte effacement (LEE)-encoded regulator controls expression of both LEE- and non-LEE-encoded virulence factors in enteropathogenic and enterohemorrhagic Escherichia coli. Infect Immun 68:6115–6126. [PubMed][CrossRef]
40. Friedberg D, Umanski T, Fang Y, Rosenshine I. 1999. Hierarchy in the expression of the locus of enterocyte effacement genes of enteropathogenic Escherichia coli. Mol Microbiol 34:941–952. [PubMed][CrossRef]
41. Njoroge JW, Nguyen Y, Curtis MM, Moreira CG, Sperandio V. 2012. Virulence meets metabolism: Cra and KdpE gene regulation in enterohemorrhagic Escherichia coli. MBio 3:e00280-12. [PubMed][CrossRef]
42. Laaberki MH, Janabi N, Oswald E, Repoila F. 2006. Concert of regulators to switch on LEE expression in enterohemorrhagic Escherichia coli O157:H7: interplay between Ler, GrlA, HNS and RpoS. Int J Med Microbiol 296:197–210. [PubMed][CrossRef]
43. Kendall MM, Gruber CC, Rasko DA, Hughes DT, Sperandio V. 2011. Hfq virulence regulation in enterohemorrhagic Escherichia coli O157:H7 strain 86-24. J Bacteriol 193:6843–6851. [PubMed][CrossRef]
44. Barba J, Bustamante VH, Flores-Valdez MA, Deng W, Finlay BB, Puente JL. 2005. A positive regulatory loop controls expression of the locus of enterocyte effacement-encoded regulators Ler and GrlA. J Bacteriol 187:7918–7930. [PubMed][CrossRef]
45. Dorman CJ. 2004. H-NS: a universal regulator for a dynamic genome. Nat Rev Microbiol 2:391–400. [PubMed][CrossRef]
46. Garcia J, Cordeiro TN, Prieto MJ, Pons M. 2012. Oligomerization and DNA binding of Ler, a master regulator of pathogenicity of enterohemorrhagic and enteropathogenic Escherichia coli. Nucleic Acids Res 40:10254–10262. [PubMed][CrossRef]
47. 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 USA 87:7839–7843. [PubMed][CrossRef]
48. Tzipori S, Gunzer F, Donnenberg MS, de Montigny L, Kaper JB, Donohue-Rolfe A. 1995. The role of the eaeA gene in diarrhea and neurological complications in a gnotobiotic piglet model of enterohemorrhagic Escherichia coli infection. Infect Immun 63:3621–3627. [PubMed]
49. McKee ML, Melton-Celsa AR, Moxley RA, Francis DH, O'Brien AD. 1995. Enterohemorrhagic Escherichia coli O157:H7 requires intimin to colonize the gnotobiotic pig intestine and to adhere to HEp-2 cells. Infect Immun 63:3739–3744. [PubMed]
50. Gansheroff LJ, Wachtel MR, O'Brien AD. 1999. Decreased adherence of enterohemorrhagic Escherichia coli to HEp-2 cells in the presence of antibodies that recognize the C-terminal region of intimin. Infect Immun 67:6409–6417. [PubMed]
51. Buist G, Steen A, Kok J, Kuipers OP. 2008. LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol Microbiol 68:838–847. [PubMed][CrossRef]
52. Touze T, Hayward RD, Eswaran J, Leong JM, Koronakis V. 2004. Self-association of EPEC intimin mediated by the beta-barrel-containing anchor domain: a role in clustering of the Tir receptor. Mol Microbiol 51:73–87. [PubMed][CrossRef]
53. Kelly G, Prasannan S, Daniell S, Fleming K, Frankel G, Dougan G, Connerton I, Matthews S. 1999. Structure of the cell-adhesion fragment of intimin from enteropathogenic Escherichia coli. Nat Struct Biol 6:313–318. [PubMed][CrossRef]
54. Batchelor M, Prasannan S, Daniell S, Reece S, Connerton I, Bloomberg G, Dougan G, Frankel G, Matthews S. 2000. Structural basis for recognition of the translocated intimin receptor (Tir) by intimin from enteropathogenic Escherichia coli. EMBO J 19:2452–2464. [PubMed][CrossRef]
55. Luo Y, Frey EA, Pfuetzner RA, Creagh AL, Knoechel DG, Haynes CA, Finlay BB, Strynadka NC. 2000. Crystal structure of enteropathogenic Escherichia coli intimin-receptor complex. Nature 405:1073–1077. [PubMed][CrossRef]
56. Rosenshine I, Ruschkowski S, Stein M, Reinscheid DJ, Mills SD, Finlay BB. 1996. A pathogenic bacterium triggers epithelial signals to form a functional bacterial receptor that mediates actin pseudopod formation. EMBO J 15:2613–2624. [PubMed]
57. Campellone KG, Leong JM. 2003. Tails of two Tirs: actin pedestal formation by enteropathogenic E. coli and enterohemorrhagic E. coli O157:H7. Curr Opin Microbiol 6:82–90. [PubMed][CrossRef]
58. Campellone KG, Brady MJ, Alamares JG, Rowe DC, Skehan BM, Tipper DJ, Leong JM. 2006. Enterohaemorrhagic Escherichia coli Tir requires a C-terminal 12-residue peptide to initiate EspF-mediated actin assembly and harbours N-terminal sequences that influence pedestal length. Cell Microbiol 8:1488–1503. [PubMed][CrossRef]
59. 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. [PubMed][CrossRef]
60. Ismaili A, Philpott DJ, Dytoc MT, Sherman PM. 1995. Signal transduction responses following adhesion of verocytotoxin-producing Escherichia coli. Infect Immun 63:3316–3326. [PubMed]
61. DeVinney R, Stein M, Reinscheid D, Abe A, Ruschkowski S, Finlay BB. 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. [PubMed]
62. Kenny B, 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. [PubMed][CrossRef]
63. de Groot JC, Schluter K, Carius Y, Quedenau C, Vingadassalom D, Faix J, Weiss SM, Reichelt J, Standfuss-Gabisch C, Lesser CF, Leong JM, Heinz DW, Bussow K, Stradal TE. 2011. Structural basis for complex formation between human IRSp53 and the translocated intimin receptor Tir of enterohemorrhagic E. coli. Structure 19:1294–1306. [PubMed][CrossRef]
64. Garmendia J, Phillips AD, Carlier MF, Chong Y, Schuller S, Marches O, Dahan S, Oswald E, Shaw RK, Knutton S, Frankel G. 2004. TccP is an enterhemorrhagic Escherichia coli O157:H7 type III effector protein that couples Tir to the actin cytoskeleton. Cell Microbiol 6:1167–1183. [PubMed][CrossRef]
65. Weiss SM, Ladwein M, Schmidt D, Ehinger J, Lommel S, Stading K, Beutling U, Disanza A, Frank R, Jansch L, Scita G, Gunzer F, Rottner K, Stradal TE. 2009. IRSp53 links the enterohemorrhagic E. coli effectors Tir and EspFU for actin pedestal formation. Cell Host Microbe 5:244–258. [PubMed][CrossRef]
66. Vingadassalom D, Kazlauskas A, Skehan B, Cheng HC, Magoun L, Robbins D, Rosen MK, Saksela K, Leong JM. 2009. Insulin receptor tyrosine kinase substrate links the E. coli O157:H7 actin assembly effectors Tir and EspF(U) during pedestal formation. Proc Natl Acad Sci USA 106:6754–6759. [PubMed][CrossRef]
67. Frankel G, Candy DC, Everest P, Dougan G. 1994. Characterization of the C-terminal domains of intimin-like proteins of enteropathogenic and enterohemorrhagic Escherichia coli, Citrobacter freundii, and Hafnia alvei. Infect Immun 62:1835–1842. [PubMed]
68. Frankel G, Candy DC, Fabiani E, Adu-Bobie J, Gil S, Novakova M, Phillips AD, Dougan G. 1995. Molecular characterization of a carboxy-terminal eukaryotic-cell-binding domain of intimin from enteropathogenic Escherichia coli. Infect Immun 63:4323–4328. [PubMed]
69. Frankel G, Lider O, Hershkoviz R, Mould AP, Kachalsky SG, Candy DC, Cahalon L, Humphries MJ, Dougan G. 1996. The cell-binding domain of intimin from enteropathogenic Escherichia coli binds to beta1 integrins. J Biol Chem 271:20359–20364. [PubMed][CrossRef]
70. Liu H, Magoun L, Leong JM. 1999. beta1-chain integrins are not essential for intimin-mediated host cell attachment and enteropathogenic Escherichia coli-induced actin condensation. Infect Immun 67:2045–2049. [PubMed]
71. Hartland EL, Batchelor M, Delahay RM, Hale C, Matthews S, Dougan G, Knutton S, Connerton I, Frankel G. 1999. Binding of intimin from enteropathogenic Escherichia coli to Tir and to host cells. Mol Microbiol 32:151–158. [PubMed][CrossRef]
72. Sinclair JF, Dean-Nystrom EA, O'Brien AD. 2006. The established intimin receptor Tir and the putative eucaryotic intimin receptors nucleolin and beta1 integrin localize at or near the site of enterohemorrhagic Escherichia coli O157:H7 adherence to enterocytes in vivo. Infect Immun 74:1255–1265. [PubMed][CrossRef]
73. Gu L, Wang H, Guo YL, Zen K. 2008. Heparin blocks the adhesion of E. coli O157:H7 to human colonic epithelial cells. Biochem Biophys Res Commun 369:1061–1064. [PubMed][CrossRef]
74. Sinclair JF, O'Brien AD. 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. [PubMed][CrossRef]
75. Sinclair JF, O'Brien AD. 2004. Intimin types alpha, beta, and gamma bind to nucleolin with equivalent affinity but lower avidity than to the translocated intimin receptor. J Biol Chem 279:33751–33758. [PubMed][CrossRef]
76. Liu B, Yin X, Feng Y, Chambers JR, Guo A, Gong J, Zhu J, Gyles CL. 2010. Verotoxin 2 enhances adherence of enterohemorrhagic Escherichia coli O157:H7 to intestinal epithelial cells and expression of {beta}1-integrin by IPEC-J2 cells. Appl Environ Microbiol 76:4461–4468. [PubMed][CrossRef]
77. Jenkins C, Chart H, Smith HR, Hartland EL, Batchelor M, Delahay RM, Dougan G, Frankel G. 2000. Antibody response of patients infected with verocytotoxin-producing Escherichia coli to protein antigens encoded on the LEE locus. J Med Microbiol 49:97–101. [PubMed]
78. Karpman D, Bekassy ZD, Sjogren AC, Dubois MS, Karmali MA, Mascarenhas M, Jarvis KG, Gansheroff LJ, O'Brien AD, Arbus GS, Kaper JB. 2002. Antibodies to intimin and Escherichia coli secreted proteins A and B in patients with enterohemorrhagic Escherichia coli infections. Pediatr Nephrol 17:201–211. [PubMed][CrossRef]
79. Li Y, Frey E, Mackenzie AM, Finlay BB. 2000. Human response to Escherichia coli O157:H7 infection: antibodies to secreted virulence factors. Infect Immun 68:5090–5095. [PubMed][CrossRef]
80. Adu-Bobie J, Frankel G, Bain C, Goncalves AG, Trabulsi LR, Douce G, Knutton S, Dougan G. 1998. Detection of intimins alpha, beta, gamma, and delta, four intimin derivatives expressed by attaching and effacing microbial pathogens. J Clin Microbiol 36:662–668. [PubMed]
81. Blanco M, Blanco JE, Blanco J, de Carvalho VM, Onuma DL, Pestana de Castro AF. 2004. Typing of intimin ( eae) genes in attaching and effacing Escherichia coli strains from monkeys. J Clin Microbiol 42:1382–1383. [PubMed][CrossRef]
82. China B, Goffaux F, Pirson V, Mainil J. 1999. Comparison of eae, tir, espA and espB genes of bovine and human attaching and effacing Escherichia coli by multiplex polymerase chain reaction. FEMS Microbiol Lett 178:177–182. [PubMed][CrossRef]
83. Oswald E, Schmidt H, Morabito S, Karch H, Marches O, Caprioli A. 2000. Typing of intimin genes in human and animal enterohemorrhagic and enteropathogenic Escherichia coli: characterization of a new intimin variant. Infect Immun 68:64–71. [PubMed][CrossRef]
84. Reid SD, Betting DJ, Whittam TS. 1999. Molecular detection and identification of intimin alleles in pathogenic Escherichia coli by multiplex PCR. J Clin Microbiol 37:2719–2722. [PubMed]
85. Zhang WL, Kohler B, Oswald E, Beutin L, Karch H, Morabito S, Caprioli A, Suerbaum S, Schmidt H. 2002. Genetic diversity of intimin genes of attaching and effacing Escherichia coli strains. J Clin Microbiol 40:4486–4492. [PubMed][CrossRef]
86. Ito K, Iida M, Yamazaki M, Moriya K, Moroishi S, Yatsuyanagi J, Kurazono T, Hiruta N, Ratchtrachenchai OA. 2007. Intimin types determined by heteroduplex mobility assay of intimin gene ( eae)-positive Escherichia coli strains. J Clin Microbiol 45:1038–1041. [PubMed][CrossRef]
87. Torres AG, Zhou X, Kaper JB. 2005. Adherence of diarrheagenic Escherichia coli strains to epithelial cells. Infect Immun 73:18–29. [PubMed][CrossRef]
88. Phillips AD, Frankel G. 2000. Intimin-mediated tissue specificity in enteropathogenic Escherichia coli interaction with human intestinal organ cultures. J Infect Dis 181:1496–1500. [PubMed][CrossRef]
89. Mundy R, Schuller S, Girard F, Fairbrother JM, Phillips AD, Frankel G. 2007. Functional studies of intimin in vivo and ex vivo: implications for host specificity and tissue tropism. Microbiology 153:959–967. [PubMed][CrossRef]
90. Ahmed S, Byrd W, Kumar S, Boedeker EC. 2013. A directed intimin insertion mutant of a rabbit enteropathogenic Escherichia coli (REPEC) is attenuated, immunogenic and elicits serogroup specific protection. Vet Immunol Immunopathol 152:146–155. [PubMed][CrossRef]
91. Guirro M, de Souza RL, Piazza RM, Guth BE. 2013. Antibodies to intimin and Escherichia coli-secreted proteins EspA and EspB in sera of Brazilian children with hemolytic uremic syndrome and healthy controls. Vet Immunol Immunopathol 152:121–125. [PubMed][CrossRef]
92. McKee ML, O'Brien AD. 1996. Truncated enterohemorrhagic Escherichia coli (EHEC) O157:H7 intimin (EaeA) fusion proteins promote adherence of EHEC strains to HEp-2 cells. Infect Immun 64:2225–2233. [PubMed]
93. Dean-Nystrom EA, Gansheroff LJ, Mills M, Moon HW, O'Brien AD. 2002. Vaccination of pregnant dams with intimin(O157) protects suckling piglets from Escherichia coli O157:H7 infection. Infect Immun 70:2414–2418. [PubMed][CrossRef]
94. Ghaem-Maghami M, Simmons CP, Daniell S, Pizza M, Lewis D, Frankel G, Dougan G. 2001. Intimin-specific immune responses prevent bacterial colonization by the attaching-effacing pathogen Citrobacter rodentium. Infect Immun 69:5597–5605. [PubMed][CrossRef]
95. Agin TS, Zhu C, Johnson LA, Thate TE, Yang Z, Boedeker EC. 2005. Protection against hemorrhagic colitis in an animal model by oral immunization with isogeneic rabbit enteropathogenic Escherichia coli attenuated by truncating intimin. Infect Immun 73:6608–6619. [PubMed][CrossRef]
96. Vilte DA, Larzabal M, Cataldi AA, Mercado EC. 2008. Bovine colostrum contains immunoglobulin G antibodies against intimin, EspA, and EspB and inhibits hemolytic activity mediated by the type three secretion system of attaching and effacing Escherichia coli. Clin Vaccine Immunol 15:1208–1213. [PubMed][CrossRef]
97. Rabinovitz BC, Gerhardt E, Tironi FC, Abdala A, Galarza R, Vilte DA, Ibarra C, Cataldi A, Mercado EC. 2012. Vaccination of pregnant cows with EspA, EspB, gamma-intimin, and Shiga toxin 2 proteins from Escherichia coli O157:H7 induces high levels of specific colostral antibodies that are transferred to newborn calves. J Dairy Sci 95:3318–3326. [PubMed][CrossRef]
98. Amani J, Mousavi SL, Rafati S, Salmanian AH. 2011. Immunogenicity of a plant-derived edible chimeric EspA, Intimin and Tir of Escherichia coli O157:H7 in mice. Plant Sci 180:620–627. [PubMed][CrossRef]
99. Hur J, Lee JH. 2011. Immune responses to new vaccine candidates constructed by a live attenuated Salmonella Typhimurium delivery system expressing Escherichia coli F4, F5, F6, F41 and intimin adhesin antigens in a murine model. J Vet Med Sci 73:1265–1273. [CrossRef]
100. Oliveira AF, Cardoso SA, Almeida FB, de Oliveira LL, Pitondo-Silva A, Soares SG, Hanna ES. 2012. Oral immunization with attenuated Salmonella vaccine expressing Escherichia coli O157:H7 intimin gamma triggers both systemic and mucosal humoral immunity in mice. Microbiol Immunol 56:513–522. [PubMed][CrossRef]
101. Dytoc MT, Ismaili A, Philpott DJ, Soni R, Brunton JL, Sherman PM. 1994. Distinct binding properties of eaeA-negative verocytotoxin-producing Escherichia coli of serotype O113:H21. Infect Immun 62:3494–3505. [PubMed]
102. Paton AW, Woodrow MC, Doyle RM, Lanser JA, Paton JC. 1999. Molecular characterization of a Shiga toxigenic Escherichia coli O113:H21 strain lacking eae responsible for a cluster of cases of hemolytic-uremic syndrome. J Clin Microbiol 37:3357–3361. [PubMed]
103. Fitzhenry RJ, Reece S, Trabulsi LR, Heuschkel R, Murch S, Thomson M, Frankel G, Phillips AD. 2002. Tissue tropism of enteropathogenic Escherichia coli strains belonging to the O55 serogroup. Infect Immun 70:4362–4368. [PubMed][CrossRef]
104. Hayashi T, Makino K, Ohnishi M, Kurokawa K, Ishii K, Yokoyama K, Han CG, Ohtsubo E, Nakayama K, Murata T, Tanaka M, Tobe T, Iida T, Takami H, Honda T, Sasakawa C, Ogasawara N, Yasunaga T, Kuhara S, Shiba T, Hattori M, Shinagawa H. 2001. Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res 8:11–22. [PubMed][CrossRef]
105. Perna NT, Plunkett G, III, Burland V, Mau B, Glasner JD, Rose DJ, Mayhew GF, Evans PS, Gregor J, Kirkpatrick HA, Posfai G, Hackett J, Klink S, Boutin A, Shao Y, Miller L, Grotbeck EJ, Davis NW, Lim A, Dimalanta ET, Potamousis KD, Apodaca J, Anantharaman TS, Lin J, Yen G, Schwartz DC, Welch RA, Blattner FR. 2001. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409:529–533. [PubMed][CrossRef]
106. Baumler AJ, Heffron F. 1995. Identification and sequence analysis of lpfABCDE, a putative fimbrial operon of Salmonella typhimurium. J Bacteriol 177:2087–2097. [PubMed]
107. Baumler AJ, Tsolis RM, Heffron F. 1996. The lpf fimbrial operon mediates adhesion of Salmonella typhimurium to murine Peyer's patches. Proc Natl Acad Sci USA 93:279–283. [PubMed][CrossRef]
108. Torres AG, Giron JA, Perna NT, Burland V, Blattner FR, Avelino-Flores F, Kaper JB. 2002. Identification and characterization of lpfABCC'DE, a fimbrial operon of enterohemorrhagic Escherichia coli O157:H7. Infect Immun 70:5416–5427. [PubMed][CrossRef]
109. Doughty S, Sloan J, Bennett-Wood V, Robertson M, Robins-Browne RM, Hartland EL. 2002. Identification of a novel fimbrial gene cluster related to long polar fimbriae in locus of enterocyte effacement-negative strains of enterohemorrhagic Escherichia coli. Infect Immun 70:6761–6769. [PubMed][CrossRef]
110. Torres AG, Kanack KJ, Tutt CB, Popov V, Kaper JB. 2004. Characterization of the second long polar (LP) fimbriae of Escherichia coli O157:H7 and distribution of LP fimbriae in other pathogenic E. coli strains. FEMS Microbiol Lett 238:333–344. [PubMed]
111. Osek J, Weiner M, Hartland EL. 2003. Prevalence of the lpfO113 gene cluster among Escherichia coli O157 isolates from different sources. Vet Microbiol 96:259–266. [PubMed][CrossRef]
112. Torres AG, Blanco M, Valenzuela P, Slater TM, Patel SD, Dahbi G, Lopez C, Barriga XF, Blanco JE, Gomes TA, Vidal R, Blanco J. 2009. Genes related to long polar fimbriae of pathogenic Escherichia coli strains as reliable markers to identify virulent isolates. J Clin Microbiol 47:2442–2451. [PubMed][CrossRef]
113. Galli L, Torres AG, Rivas M. 2010. Identification of the long polar fimbriae gene variants in the locus of enterocyte effacement-negative Shiga toxin-producing Escherichia coli strains isolated from humans and cattle in Argentina. FEMS Microbiol Lett 308:123–129. [PubMed]
114. Torres AG, Milflores-Flores L, Garcia-Gallegos JG, Patel SD, Best A, La Ragione RM, Martinez-Laguna Y, Woodward MJ. 2007. Environmental regulation and colonization attributes of the long polar fimbriae (LPF) of Escherichia coli O157:H7. Int J Med Microbiol 297:177–185. [PubMed][CrossRef]
115. Torres AG, Lopez-Sanchez GN, Milflores-Flores L, Patel SD, Rojas-Lopez M, Martinez de la Pena CF, Arenas-Hernandez MM, Martinez-Laguna Y. 2007. Ler and H-NS, regulators controlling expression of the long polar fimbriae of Escherichia coli O157:H7. J Bacteriol 189:5916–5928. [PubMed][CrossRef]
116. Rojas-Lopez M, Arenas-Hernandez MM, Medrano-Lopez A, Martinez de la Pena CF, Puente JL, Martinez-Laguna Y, Torres AG. 2011. Regulatory control of the Escherichia coli O157:H7 lpf1 operon by H-NS and Ler. J Bacteriol 193:1622–1632. [PubMed][CrossRef]
117. Torres AG, Slater TM, Patel SD, Popov VL, Arenas-Hernandez MM. 2008. Contribution of the Ler- and H-NS-regulated long polar fimbriae of Escherichia coli O157:H7 during binding to tissue-cultured cells. Infect Immun 76:5062–5071. [PubMed][CrossRef]
118. Farfan MJ, Cantero L, Vidal R, Botkin DJ, Torres AG. 2011. Long polar fimbriae of enterohemorrhagic Escherichia coli O157:H7 bind to extracellular matrix proteins. Infect Immun 79:3744–3750. [PubMed][CrossRef]
119. Jordan DM, Cornick N, Torres AG, Dean-Nystrom EA, Kaper JB, Moon HW. 2004. Long polar fimbriae contribute to colonization by Escherichia coli O157:H7 in vivo. Infect Immun 72:6168–6171. [PubMed][CrossRef]
120. Fitzhenry R, Dahan S, Torres AG, Chong Y, Heuschkel R, Murch SH, Thomson M, Kaper JB, Frankel G, Phillips AD. 2006. Long polar fimbriae and tissue tropism in Escherichia coli O157:H7. Microbes Infect 8:1741–1749. [PubMed][CrossRef]
121. Lloyd SJ, Ritchie JM, Rojas-Lopez M, Blumentritt CA, Popov VL, Greenwich JL, Waldor MK, Torres AG. 2012. A double, long polar fimbria mutant of Escherichia coli O157:H7 expresses curli and exhibits reduced in vivo colonization. Infect Immun 80:914–920. [PubMed][CrossRef]
122. Barnhart MM, Chapman MR. 2006. Curli biogenesis and function. Annu Rev Microbiol 60:131–147. [PubMed][CrossRef]
123. Fitzhenry RJ, Stevens MP, Jenkins C, Wallis TS, Heuschkel R, Murch S, Thomson M, Frankel G, Phillips AD. 2003. Human intestinal tissue tropism of intimin epsilon O103 Escherichia coli. FEMS Microbiol Lett 218:311–316. [PubMed][CrossRef]
124. Olsen A, Jonsson A, Normark S. 1989. Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338:652–655. [PubMed][CrossRef]
125. Olsen A, Wick MJ, Morgelin M, Bjorck L. 1998. Curli, fibrous surface proteins of Escherichia coli, interact with major histocompatibility complex class I molecules. Infect Immun 66:944–949. [PubMed]
126. Collinson SK, Clouthier SC, Doran JL, Banser PA, Kay WW. 1997. Characterization of the agfBA fimbrial operon encoding thin aggregative fimbriae of Salmonella enteritidis. Adv Exp Med Biol 412:247–248. [PubMed][CrossRef]
127. Romling U, Bian Z, Hammar M, Sierralta WD, Normark S. 1998. Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol 180:722–731. [PubMed]
128. Dong T, Schellhorn HE. 2009. Global effect of RpoS on gene expression in pathogenic Escherichia coli O157:H7 strain EDL933. BMC Genomics 10:349. [PubMed][CrossRef]
129. Olsen A, Arnqvist A, Hammar M, Sukupolvi S, Normark S. 1993. The RpoS sigma factor relieves H-NS-mediated transcriptional repression of csgA, the subunit gene of fibronectin-binding curli in Escherichia coli. Mol Microbiol 7:523–536. [PubMed][CrossRef]
130. Lee JH, Cho MH, Lee J. 2011. 3-indolylacetonitrile decreases Escherichia coli O157:H7 biofilm formation and Pseudomonas aeruginosa virulence. Environ Microbiol 13:62–73. [PubMed][CrossRef]
131. Hammar M, Arnqvist A, Bian Z, Olsen A, Normark S. 1995. Expression of two csg operons is required for production of fibronectin- and congo red-binding curli polymers in Escherichia coli K-12. Mol Microbiol 18:661–670. [PubMed][CrossRef]
132. Vidal O, Longin R, Prigent-Combaret C, Dorel C, Hooreman M, Lejeune P. 1998. Isolation of an Escherichia coli K-12 mutant strain able to form biofilms on inert surfaces: involvement of a new ompR allele that increases curli expression. J Bacteriol 180:2442–2449. [PubMed]
133. Dorel C, Vidal O, Prigent-Combaret C, Vallet I, Lejeune P. 1999. Involvement of the Cpx signal transduction pathway of E. coli in biofilm formation. FEMS Microbiol Lett 178:169–175. [PubMed][CrossRef]
134. Brown PK, Dozois CM, Nickerson CA, Zuppardo A, Terlonge J, Curtiss R, III. 2001. MlrA, a novel regulator of curli (AgF) and extracellular matrix synthesis by Escherichia coli and Salmonella enterica serovar Typhimurium. Mol Microbiol 41:349–363. [PubMed][CrossRef]
135. Saldana Z, Xicohtencatl-Cortes J, Avelino F, Phillips AD, Kaper JB, Puente JL, Giron JA. 2009. Synergistic role of curli and cellulose in cell adherence and biofilm formation of attaching and effacing Escherichia coli and identification of Fis as a negative regulator of curli. Environ Microbiol 11:992–1006. [PubMed][CrossRef]
136. Sharma VK, Bearson SM, Bearson BL. 2010. Evaluation of the effects of sdiA, a luxR homologue, on adherence and motility of Escherichia coli O157:H7. Microbiology 156:1303–1312. [PubMed][CrossRef]
137. Ryu JH, Beuchat LR. 2005. Biofilm formation by Escherichia coli O157:H7 on stainless steel: effect of exopolysaccharide and curli production on its resistance to chlorine. Appl Environ Microbiol 71:247–254. [PubMed][CrossRef]
138. Pawar DM, Rossman ML, Chen J. 2005. Role of curli fimbriae in mediating the cells of enterohaemorrhagic Escherichia coli to attach to abiotic surfaces. J Appl Microbiol 99:418–425. [PubMed][CrossRef]
139. Fink RC, Black EP, Hou Z, Sugawara M, Sadowsky MJ, Diez-Gonzalez F. 2012. Transcriptional responses of Escherichia coli K-12 and O157:H7 associated with lettuce leaves. Appl Environ Microbiol 78:1752–1764. [PubMed][CrossRef]
140. Low AS, Holden N, Rosser T, Roe AJ, Constantinidou C, Hobman JL, Smith DG, Low JC, Gally DL. 2006. Analysis of fimbrial gene clusters and their expression in enterohaemorrhagic Escherichia coli O157:H7. Environ Microbiol 8:1033–1047. [PubMed][CrossRef]
141. Rendon MA, Saldana Z, Erdem AL, Monteiro-Neto V, Vazquez A, Kaper JB, Puente JL, Giron JA. 2007. Commensal and pathogenic Escherichia coli use a common pilus adherence factor for epithelial cell colonization. Proc Natl Acad Sci USA 104:10637–10642. [PubMed][CrossRef]
142. Pouttu R, Westerlund-Wikstrom B, Lang H, Alsti K, Virkola R, Saarela U, Siitonen A, Kalkkinen N, Korhonen TK. 2001. matB, a common fimbrillin gene of Escherichia coli, expressed in a genetically conserved, virulent clonal group. J Bacteriol 183:4727–4736. [PubMed][CrossRef]
143. Saldana Z, Erdem AL, Schuller S, Okeke IN, Lucas M, Sivananthan A, Phillips AD, Kaper JB, Puente JL, Giron JA. 2009. The Escherichia coli common pilus and the bundle-forming pilus act in concert during the formation of localized adherence by enteropathogenic E. coli. J Bacteriol 191:3451–3461. [PubMed][CrossRef]
144. van Diemen PM, Dziva F, Stevens MP, Wallis TS. 2005. Identification of enterohemorrhagic Escherichia coli O26:H– genes required for intestinal colonization in calves. Infect Immun 73:1735–1743. [PubMed][CrossRef]
145. Low AS, Dziva F, Torres AG, Martinez JL, Rosser T, Naylor S, Spears K, Holden N, Mahajan A, Findlay J, Sales J, Smith DG, Low JC, Stevens MP, Gally DL. 2006. Cloning, expression, and characterization of fimbrial operon F9 from enterohemorrhagic Escherichia coli O157:H7. Infect Immun 74:2233–2244. [PubMed][CrossRef]
146. Vazquez-Juarez RC, Kuriakose JA, Rasko DA, Ritchie JM, Kendall MM, Slater TM, Sinha M, Luxon BA, Popov VL, Waldor MK, Sperandio V, Torres AG. 2008. CadA negatively regulates Escherichia coli O157:H7 adherence and intestinal colonization. Infect Immun 76:5072–5081. [PubMed][CrossRef]
147. Samadder P, Xicohtencatl-Cortes J, Saldana Z, Jordan D, Tarr PI, Kaper JB, Giron JA. 2009. The Escherichia coli ycbQRST operon encodes fimbriae with laminin-binding and epithelial cell adherence properties in Shiga-toxigenic E. coli O157:H7. Environ Microbiol 11:1815–1826. [PubMed][CrossRef]
148. Brunder W, Khan AS, Hacker J, Karch H. 2001. Novel type of fimbriae encoded by the large plasmid of sorbitol-fermenting enterohemorrhagic Escherichia coli O157:H(–). Infect Immun 69:4447–4457. [PubMed][CrossRef]
149. Bielaszewska M, Prager R, Vandivinit L, Musken A, Mellmann A, Holt NJ, Tarr PI, Karch H, Zhang W. 2009. Detection and characterization of the fimbrial sfp cluster in enterohemorrhagic Escherichia coli O165:H25/NM isolates from humans and cattle. Appl Environ Microbiol 75:64–71. [PubMed][CrossRef]
150. Musken A, Bielaszewska M, Greune L, Schweppe CH, Muthing J, Schmidt H, Schmidt MA, Karch H, 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. [PubMed][CrossRef]
151. Xicohtencatl-Cortes J, Monteiro-Neto V, Ledesma MA, Jordan DM, Francetic O, Kaper JB, Puente JL, Giron JA. 2007. Intestinal adherence associated with type IV pili of enterohemorrhagic Escherichia coli O157:H7. J Clin Invest 117:3519–3529. [PubMed][CrossRef]
152. Xicohtencatl-Cortes J, Monteiro-Neto V, Saldana Z, Ledesma MA, Puente JL, Giron JA. 2009. The type 4 pili of enterohemorrhagic Escherichia coli O157:H7 are multipurpose structures with pathogenic attributes. J Bacteriol 191:411–421. [PubMed][CrossRef]
153. Galfi P, Neogrady S, Semjen G, Bardocz S, Pusztai A. 1998. Attachment of different Escherichia coli strains to cultured rumen epithelial cells. Vet Microbiol 61:191–197. [PubMed][CrossRef]
154. Enami M, Nakasone N, Honma Y, Kakinohana S, Kudaka J, Iwanaga M. 1999. Expression of type I pili is abolished in verotoxin-producing Escherichia coli O157. FEMS Microbiol Lett 179:467–472. [PubMed][CrossRef]
155. Li B, Koch WH, Cebula TA. 1997. Detection and characterization of the fimA gene of Escherichia coli O157:H7. Mol Cell Probes 11:397–406. [PubMed][CrossRef]
156. Roe AJ, Currie C, Smith DG, Gally DL. 2001. Analysis of type 1 fimbriae expression in verotoxigenic Escherichia coli: a comparison between serotypes O157 and O26. Microbiology 147:145–152. [PubMed]
157. Cookson AL, Cooley WA, Woodward MJ. 2002. The role of type 1 and curli fimbriae of Shiga toxin-producing Escherichia coli in adherence to abiotic surfaces. Int J Med Microbiol 292:195–205. [PubMed][CrossRef]
158. Leyton DL, Sevastsyanovich YR, Browning DF, Rossiter AE, Wells TJ, Fitzpatrick RE, Overduin M, Cunningham AF, Henderson IR. 2011. Size and conformation limits to secretion of disulfide-bonded loops in autotransporter proteins. J Biol Chem 286:42283–42291. [PubMed][CrossRef]
159. Henderson IR, Nataro JP. 2001. Virulence functions of autotransporter proteins. Infect Immun 69:1231–1243. [PubMed][CrossRef]
160. Wells TJ, Sherlock O, Rivas L, Mahajan A, Beatson SA, Torpdahl M, Webb RI, Allsopp LP, Gobius KS, Gally DL, Schembri MA. 2008. EhaA is a novel autotransporter protein of enterohemorrhagic Escherichia coli O157:H7 that contributes to adhesion and biofilm formation. Environ Microbiol 10:589–604. [PubMed][CrossRef]
161. Wells TJ, McNeilly TN, Totsika M, Mahajan A, Gally DL, Schembri MA. 2009. The Escherichia coli O157:H7 EhaB autotransporter protein binds to laminin and collagen I and induces a serum IgA response in O157:H7 challenged cattle. Environ Microbiol 11:1803–1814. [PubMed][CrossRef]
162. Peterson JH, Tian P, Ieva R, Dautin N, Bernstein HD. 2010. Secretion of a bacterial virulence factor is driven by the folding of a C-terminal segment. Proc Natl Acad Sci USA 107:17739–17744. [PubMed][CrossRef]
163. Brunder W, Schmidt H, Karch H. 1997. EspP, a novel extracellular serine protease of enterohaemorrhagic Escherichia coli O157:H7 cleaves human coagulation factor V. Mol Microbiol 24:767–778. [PubMed][CrossRef]
164. Orth D, Ehrlenbach S, Brockmeyer J, Khan AB, Huber G, Karch H, Sarg B, Lindner H, Wurzner R. 2010. EspP, a serine protease of enterohemorrhagic Escherichia coli, impairs complement activation by cleaving complement factors C3/C3b and C5. Infect Immun 78:4294–4301. [PubMed][CrossRef]
165. Brockmeyer J, Aldick T, Soltwisch J, Zhang W, Tarr PI, Weiss A, Dreisewerd K, Muthing J, Bielaszewska M, Karch H. 2011. Enterohaemorrhagic Escherichia coli haemolysin is cleaved and inactivated by serine protease EspPalpha. Environ Microbiol 13:1327–1341. [PubMed][CrossRef]
166. Dziva F, Mahajan A, Cameron P, Currie C, McKendrick IJ, Wallis TS, Smith DG, Stevens MP. 2007. EspP, a Type V-secreted serine protease of enterohaemorrhagic Escherichia coli O157:H7, influences intestinal colonization of calves and adherence to bovine primary intestinal epithelial cells. FEMS Microbiol Lett 271:258–264. [PubMed][CrossRef]
167. Xicohtencatl-Cortes J, Saldana Z, Deng W, Castaneda E, Freer E, Tarr PI, Finlay BB, Puente JL, Giron JA. 2010. Bacterial macroscopic rope-like fibers with cytopathic and adhesive properties. J Biol Chem 285:32336–32342. [PubMed][CrossRef]
168. Paton AW, Srimanote P, Woodrow MC, Paton JC. 2001. Characterization of Saa, a novel autoagglutinating adhesin produced by locus of enterocyte effacement-negative Shiga-toxigenic Escherichia coli strains that are virulent for humans. Infect Immun 69:6999–7009. [PubMed][CrossRef]
169. Lucchesi PM, Kruger A, Parma AE. 2006. Distribution of saa gene variants in verocytotoxigenic Escherichia coli isolated from cattle and food. Res Microbiol 157:263–266. [PubMed][CrossRef]
170. Toma C, Nakasone N, Miliwebsky E, Higa N, Rivas M, Suzuki T. 2008. Differential adherence of Shiga toxin-producing Escherichia coli harboring saa to epithelial cells. Int J Med Microbiol 298:571–578. [PubMed][CrossRef]
171. Herold S, Paton JC, Paton AW. 2009. Sab, a novel autotransporter of locus of enterocyte effacement-negative shiga-toxigenic Escherichia coli O113:H21, contributes to adherence and biofilm formation. Infect Immun 77:3234–3243. [PubMed][CrossRef]
172. Torres AG, Perna NT, Burland V, Ruknudin A, Blattner FR, Kaper JB. 2002. Characterization of Cah, a calcium-binding and heat-extractable autotransporter protein of enterohaemorrhagic Escherichia coli. Mol Microbiol 45:951–966. [PubMed][CrossRef]
173. Torres AG, Jeter C, Langley W, Matthysse AG. 2005. Differential binding of Escherichia coli O157:H7 to alfalfa, human epithelial cells, and plastic is mediated by a variety of surface structures. Appl Environ Microbiol 71:8008–8015. [PubMed][CrossRef]
174. Giron JA, Torres AG, Freer E, Kaper JB. 2002. The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol Microbiol 44:361–379. [PubMed][CrossRef]
175. Best A, La Ragione RM, Sayers AR, Woodward MJ. 2005. Role for flagella but not intimin in the persistent infection of the gastrointestinal tissues of specific-pathogen-free chicks by shiga toxin-negative Escherichia coli O157:H7. Infect Immun 73:1836–1846. [PubMed][CrossRef]
176. Erdem AL, Avelino F, Xicohtencatl-Cortes J, Giron JA. 2007. Host protein binding and adhesive properties of H6 and H7 flagella of attaching and effacing Escherichia coli. J Bacteriol 189:7426–7435. [PubMed][CrossRef]
177. Mahajan A, Currie CG, Mackie S, Tree J, McAteer S, McKendrick I, McNeilly TN, Roe A, La Ragione RM, Woodward MJ, Gally DL, Smith DG. 2009. An investigation of the expression and adhesin function of H7 flagella in the interaction of Escherichia coli O157:H7 with bovine intestinal epithelium. Cell Microbiol 11:121–137. [PubMed][CrossRef]
178. Tarr PI, Bilge SS, Vary JC, Jr., Jelacic S, Habeeb RL, Ward TR, Baylor MR, Besser TE. 2000. Iha: a novel Escherichia coli O157:H7 adherence-conferring molecule encoded on a recently acquired chromosomal island of conserved structure. Infect Immun 68:1400–1407. [PubMed][CrossRef]
179. Herold S, Paton JC, Srimanote P, Paton AW. 2009. Differential effects of short-chain fatty acids and iron on expression of iha in Shiga-toxigenic Escherichia coli. Microbiology 155:3554–3563. [PubMed][CrossRef]
180. Yin X, Wheatcroft R, Chambers JR, Liu B, Zhu J, Gyles CL. 2009. 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. [PubMed][CrossRef]
181. Lu Y, Iyoda S, Satou H, Satou H, Itoh K, Saitoh T, Watanabe H. 2006. A new immunoglobulin-binding protein, EibG, is responsible for the chain-like adhesion phenotype of locus of enterocyte effacement-negative, shiga toxin-producing Escherichia coli. Infect Immun 74:5747–5755. [PubMed][CrossRef]
182. Merkel V, Ohder B, Bielaszewska M, Zhang W, Fruth A, Menge C, Borrmann E, Middendorf B, Muthing J, Karch H, Mellmann A. 2010. Distribution and phylogeny of immunoglobulin-binding protein G in Shiga toxin-producing Escherichia coli and its association with adherence phenotypes. Infect Immun 78:3625–3636. [PubMed][CrossRef]
183. Torres AG, Kaper JB. 2003. Multiple elements controlling adherence of enterohemorrhagic Escherichia coli O157:H7 to HeLa cells. Infect Immun 71:4985–4995. [CrossRef]
184. Torres AG, Li Y, Tutt CB, Xin L, Eaves-Pyles T, Soong L. 2006. Outer membrane protein A of Escherichia coli O157:H7 stimulates dendritic cell activation. Infect Immun 74:2676–2685. [PubMed][CrossRef]
185. Prasadarao NV, Wass CA, Weiser JN, Stins MF, Huang SH, Kim KS. 1996. Outer membrane protein A of Escherichia coli contributes to invasion of brain microvascular endothelial cells. Infect Immun 64:146–153. [PubMed]
186. Prasadarao NV. 2002. Identification of Escherichia coli outer membrane protein A receptor on human brain microvascular endothelial cells. Infect Immun 70:4556–4563. [PubMed][CrossRef]
187. Shin S, Lu G, Cai M, Kim KS. 2005. Escherichia coli outer membrane protein A adheres to human brain microvascular endothelial cells. Biochem Biophys Res Commun 330:1199–1204. [PubMed][CrossRef]
188. Gu J, Ji X, Qi J, Ma Y, Mao X, Zou Q. 2010. Crystallization and preliminary crystallographic studies of the C-terminal domain of outer membrane protein A from enterohaemorrhagic Escherichia coli. Acta Crystallogr Sect F Struct Biol Cryst Commun 66:929–931. [PubMed][CrossRef]
Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.EHEC-0003-2013
2014-06-20
2020-09-25

Abstract:

Adhesins are a group of proteins in enterohemorrhagic (EHEC) that are involved in the attachment or colonization of this pathogen to abiotic (plastic or steel) and biological surfaces, such as those found in bovine and human intestines. This review provides the most up-to-date information on these essential adhesion factors, summarizing important historical discoveries and analyzing the current and future state of this research. In doing so, the proteins intimin and Tir are discussed in depth, especially regarding their role in the development of attaching and effacing lesions and in EHEC virulence. Further, a series of fimbrial proteins (Lpf1, Lpf2, curli, ECP, F9, ELF, Sfp, HCP, and type 1 fimbria) are also described, emphasizing their various contributions to adherence and colonization of different surfaces and their potential use as genetic markers in detection and classification of different EHEC serotypes. This review also discusses the role of several autotransporter proteins (EhaA-D, EspP, Saa and Sab, and Cah), as well as other proteins associated with adherence, such as flagella, EibG, Iha, and OmpA. While these proteins have all been studied to varying degrees, all of the adhesins summarized in this article have been linked to different stages of the EHEC life cycle, making them good targets for the development of more effective diagnostics and therapeutics.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

/deliver/fulltext/microbiolspec/2/3/EHEC-0003-2013.html?itemId=/content/journal/microbiolspec/10.1128/microbiolspec.EHEC-0003-2013&mimeType=html&fmt=ahah

Figures

Enterohemorrhagic Adhesins
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.EHEC-0003-2013-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.EHEC-0003-2013-1,properties={foaf_givenname=Brian D., foaf_name=Brian D. McWilliams, foaf_surname=McWilliams, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.EHEC-0003-2013-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.EHEC-0003-2013-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.EHEC-0003-2013-2,properties={foaf_givenname=Alfredo G., foaf_name=Alfredo G. Torres, foaf_surname=Torres, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.EHEC-0003-2013-aff2]]}]]
Citation: McWilliams B, Torres A. 2014. Enterohemorrhagic adhesins. microbiolspec 2(3): doi:10.1128/microbiolspec.EHEC-0003-2013
/content/microbiolspec/10.1128/microbiolspec.EHEC-0003-2013.fig1
FIGURE 1
Illustration of the EHEC prototype strain EDL933 LEE pathogenicity island. The five LEE operons are depicted, specifically emphasizing gene-encoded proteins associated with adhesion and A/E lesion formation. They include the genes encoding the regulatory proteins Ler, GrlA, and GrlR; the translocated receptor protein Tir; and the adhesin protein intimin.
microbiolspec/2/3/EHEC-0003-2013-fig1_thmb.gif
microbiolspec/2/3/EHEC-0003-2013-fig1.gif
Image of FIGURE 1

Click to view

FIGURE 1

Illustration of the EHEC prototype strain EDL933 LEE pathogenicity island. The five LEE operons are depicted, specifically emphasizing gene-encoded proteins associated with adhesion and A/E lesion formation. They include the genes encoding the regulatory proteins Ler, GrlA, and GrlR; the translocated receptor protein Tir; and the adhesin protein intimin.

Source: microbiolspec June 2014 vol. 2 no. 3 doi:10.1128/microbiolspec.EHEC-0003-2013
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.EHEC-0003-2013.fig2
FIGURE 2
Time line and proposed roles of major fimbrial/afimbrial adhesin proteins in EHEC. In (A), Lpf is interacting with the extracellular membrane (ECM) proteins, such as laminin, collagen IV, and fibronectin. After the initial interaction with the intestine is established, EHEC is able to closely attach to the host cell (B) through an interaction of the surface protein intimin with the translocated receptor protein Tir and nucleolin. In (C), the interaction between Tir and intimin is established, initiating a host-cell actin rearrangement via participation of the translocated bacterial protein EspFu and the recruitment of several host proteins. In (D), ECP and HCP are proposed to interact with the surface of host intestinal cells, perhaps strengthening the colonization through the formation of microcolonies and/or biofilms. Further, curli is shown to contribute in the establishment of biofilms, though an interaction with ECP and HCP is not demonstrated. Finally in (E), dominant curli expression has been proposed as detrimental for the survival of EHEC in the intestine, suggesting that this surface structure might become important for the pathogen interaction with abiotic surfaces and during colonization of the surface of vegetable and plant leaves.
microbiolspec/2/3/EHEC-0003-2013-fig2_thmb.gif
microbiolspec/2/3/EHEC-0003-2013-fig2.gif
Image of FIGURE 2

Click to view

FIGURE 2

Time line and proposed roles of major fimbrial/afimbrial adhesin proteins in EHEC. In (A), Lpf is interacting with the extracellular membrane (ECM) proteins, such as laminin, collagen IV, and fibronectin. After the initial interaction with the intestine is established, EHEC is able to closely attach to the host cell (B) through an interaction of the surface protein intimin with the translocated receptor protein Tir and nucleolin. In (C), the interaction between Tir and intimin is established, initiating a host-cell actin rearrangement via participation of the translocated bacterial protein EspFu and the recruitment of several host proteins. In (D), ECP and HCP are proposed to interact with the surface of host intestinal cells, perhaps strengthening the colonization through the formation of microcolonies and/or biofilms. Further, curli is shown to contribute in the establishment of biofilms, though an interaction with ECP and HCP is not demonstrated. Finally in (E), dominant curli expression has been proposed as detrimental for the survival of EHEC in the intestine, suggesting that this surface structure might become important for the pathogen interaction with abiotic surfaces and during colonization of the surface of vegetable and plant leaves.

Source: microbiolspec June 2014 vol. 2 no. 3 doi:10.1128/microbiolspec.EHEC-0003-2013
Permissions and Reprints Request Permissions
Download as Powerpoint

Tables

Enterohemorrhagic Adhesins
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.EHEC-0003-2013-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.EHEC-0003-2013-1,properties={foaf_givenname=Brian D., foaf_name=Brian D. McWilliams, foaf_surname=McWilliams, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.EHEC-0003-2013-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.EHEC-0003-2013-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.EHEC-0003-2013-2,properties={foaf_givenname=Alfredo G., foaf_name=Alfredo G. Torres, foaf_surname=Torres, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.EHEC-0003-2013-aff2]]}]]
Citation: McWilliams B, Torres A. 2014. Enterohemorrhagic adhesins. microbiolspec 2(3): doi:10.1128/microbiolspec.EHEC-0003-2013
/content/microbiolspec/10.1128/microbiolspec.EHEC-0003-2013.T1
TABLE 1
Major characteristics of the EHEC fimbrial proteins
Generic image for table

Click to view

TABLE 1

Major characteristics of the EHEC fimbrial proteins

Source: microbiolspec June 2014 vol. 2 no. 3 doi:10.1128/microbiolspec.EHEC-0003-2013
/content/microbiolspec/10.1128/microbiolspec.EHEC-0003-2013.T2
TABLE 2
EHEC autotransporters and their functions
Generic image for table

Click to view

TABLE 2

EHEC autotransporters and their functions

Source: microbiolspec June 2014 vol. 2 no. 3 doi:10.1128/microbiolspec.EHEC-0003-2013

Supplemental Material

No supplementary material available for this content.

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error