Fimbriation and curliation in escherichia coli O157:H7 a paradigm of intestinal and environmental colonization

Gut Microbes

Volumn 3, Issue 3, 2012, Pages 272-276

  Lloyd, Sonja J ^a,c   Ritchie, Jennifer M ^b   Torres, Alfredo G ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF SURREY   (United Kingdom)

^c NONE   (Canada)

Author keywords

Colonization; Curli; E. coli O157:H7; Enterohemorrhagic E. coli; Fimbria; Long polar fimbriae

Indexed keywords

ARTICLE; BACTERIAL COLONIZATION; ESCHERICHIA COLI O157; FIMBRIA; GASTROINTESTINAL DISEASE; GENE MUTATION; HUMAN; NONHUMAN; PATHOGENESIS; SHIGA TOXIN PRODUCING ESCHERICHIA COLI; ANIMAL; BACTERIUM ADHERENCE; BIOLOGICAL MODEL; EPITHELIUM CELL; GENETICS; INTESTINE; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; RABBIT; REVIEW;

ESCHERICHIA COLI; ORYCTOLAGUS CUNICULUS;

ADHESIN; BACTERIAL PROTEIN; CRL PROTEIN, BACTERIA; ESCHERICHIA COLI PROTEIN; FIMBRIA PROTEIN; VIRULENCE FACTOR;

ADHESINS, BACTERIAL; ANIMALS; BACTERIAL ADHESION; BACTERIAL PROTEINS; ENVIRONMENTAL MICROBIOLOGY; EPITHELIAL CELLS; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; FIMBRIAE PROTEINS; HUMANS; INTESTINES; MODELS, BIOLOGICAL; RABBITS; VIRULENCE FACTORS;

EID: 84930482564     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/gmic.20661     Document Type: Article

References (46)

1. Caprioli A, Morabito S, Brugère H, Oswald E. Enterohaemorrhagic Escherichia coli: emerging issues on virulence and modes of transmission. Vet Res 2005; 36:289-311. PMID:15845227; http://dx.doi.org/10.1051/vetres:2005002.
2. Farfan MJ, Torres AG. Molecular mechanisms that mediate colonization of Shiga toxin-producing Escherichia coli strains. Infect Immun 2012; 80:903-913. PMID:22144484; http://dx.doi.org/10.1128/IAI.05907-11.
3. Fitzhenry R, Dahan S, Torres AG, Chong Y, Heuschkel R, Murch SH, et al. Long polar fimbriae and tissue tropism in Escherichia coli O157:H7. Microbes Infect 2006; 8:1741-1749. PMID:16815722; http://dx.doi.org/10.1016/j.micinf.2006.02.012.
4. Mundy R, Schüller S, Girard F, Fairbrother JM, Phillips AD, Frankel G. Functional studies of intimin in vivo and ex vivo: implications for host specificity and tissue tropism. Microbiology 2007; 153:959-967. PMID:17379706; http://dx.doi.org/10.1099/mic.0.2006/003467-0.
5. Fitzhenry RJ, Pickard DJ, Hartland EL, Reece S, Dougan G, Phillips AD, et al. Intimin type influences the site of human intestinal mucosal colonisation by enterohaemorrhagic Escherichia coli O157:H7. Gut 2002; 50:180-185. PMID:11788556; http://dx.doi.org/10.1136/gut.50.2.180.
6. Bäumler AJ, Heffron F. Identification and sequence analysis of lpfABCDE, a putative fimbrial operon of Salmonella typhimurium. J Bacteriol 1995; 177:2087-2097. PMID:7721701.
7. Torres AG, Giron JA, Perna NT, Burland V, Blattner FR, Avelino-Flores F, et al. Identification and characterization of lpfABCC'DE, a fimbrial operon of enterohemorrhagic Escherichia coli O157:H7. Infect Immun 2002; 70:5416-5427. PMID:12228266; http://dx.doi.org/10.1128/IAI.70.10.5416-5427.2002.
8. Rojas-López M, Arenas-Hernández MM, Medrano-López A, Martínez de la Peña CF, Puente JL, Martínez-Laguna Y, et al. Regulatory control of the Escherichia coli O157:H7 lpf1 operon by H-NS and Ler. J Bacteriol 2011; 193:1622-1632. PMID:21278287; http://dx.doi.org/10.1128/JB.01082-10.
9. Torres AG, Kanack KJ, Tutt CB, Popov V, Kaper JB. 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 2004; 238:333-344; PMID:15358418.
10. Torres AG, Milflores-Flores L, Garcia-Gallegos JG, Patel SD, Best A, La Ragione RM, et al. Environmental regulation and colonization attributes of the long polar fimbriae (LPF) of Escherichia coli O157:H7. Int J Med Microbiol 2007; 297:177-185. PMID:17353147; http://dx.doi.org/10.1016/j.ijmm.2007.01.005.
11. Jordan DM, Cornick N, Torres AG, Dean-Nystrom EA, Kaper JB, Moon HW. Long polar fimbriae contribute to colonization by Escherichia coli O157:H7 in vivo. Infect Immun 2004; 72:6168-6171. PMID:15385526; http://dx.doi.org/10.1128/IAI.72.10.6168-6171.2004.
12. Lloyd SJ, Ritchie JM, Rojas-Lopez M, Blumentritt CA, Popov VL, Greenwich JL, et al. A double, long polar fimbria mutant of Escherichia coli O157:H7 expresses Curli and exhibits reduced in vivo colonization. Infect Immun 2012; 80:914-920. PMID:22232190; http://dx.doi.org/10.1128/IAI.05945-11.
13. Ritchie JM, Thorpe CM, Rogers AB, Waldor MK. Critical roles for stx2, eae, and tir in enterohemorrhagic Escherichia coli-induced diarrhea and intestinal inflammation in infant rabbits. Infect Immun 2003; 71:7129-7139. PMID:14638803; http://dx.doi.org/10.1128/IAI.71.12.7129-7139.2003.
14. Barnhart MM, Chapman MR. Curli biogenesis and function. Annu Rev Microbiol 2006; 60:131-147. PMID:16704339; http://dx.doi.org/10.1146/annurev.micro.60.080805.142106.
15. Prigent-Combaret C, Prensier G, Le Thi TT, Vidal O, Lejeune P, Dorel C. Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. Environ Microbiol 2000; 2:450-464. PMID:11234933; http://dx.doi.org/10.1046/j.1462-2920.2000.00128.x.
16. Brown PK, Dozois CM, Nickerson CA, Zuppardo A, Terlonge J, Curtiss R 3rd. MlrA, a novel regulator of curli (AgF) and extracellular matrix synthesis by Escherichia coli and Salmonella enterica serovar Typhimurium. Mol Microbiol 2001; 41:349-363; PMID:11489123; http://dx.doi.org/10.1046/j.1365-2958.2001.02529.x.
17. Chapman MR, Robinson LS, Pinkner JS, Roth R, Heuser J, Hammar M, et al. Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 2002; 295:851-855. PMID:11823641; http://dx.doi.org/10.1126/science.1067484.
18. Hammar M, Bian Z, Normark S. Nucleator dependent intercellular assembly of adhesive curli organelles in Escherichia coli. Proc Natl Acad Sci U S A 1996; 93:6562-6566. PMID:8692856; http://dx.doi.org/10.1073/pnas.93.13.6562.
19. Olsén A, Jonsson A, Normark S. Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 1989; 338:652-655. PMID:2649795; http://dx.doi.org/10.1038/338652a0.
20. Olsén A, Wick MJ, Mörgelin M, Björck L. Curli, fibrous surface proteins of Escherichia coli, interact with major histocompatibility complex class I molecules. Infect Immun 1998; 66:944-949. PMID:9488380.
21. Olsén A, Arnqvist A, Hammar M, Sukupolvi S, Normark S. The RpoS sigma factor relieves H-NSmediated transcriptional repression of csgA, the subunit gene of fibronectin-binding curli in Escherichia coli. Mol Microbiol 1993; 7:523-536. PMID:8459772; http://dx.doi.org/10.1111/j.1365-2958.1993.tb01143.x.
22. Pratt LA, Silhavy TJ. Crl stimulates RpoS activity during stationary phase. Mol Microbiol 1998; 29:1225-1236. PMID:9767590; http://dx.doi.org/10.1046/j.1365-2958.1998.01007.x.
23. Uhlich GA, Keen JE, Elder RO. Mutations in the csgD promoter associated with variations in curli expression in certain strains of Escherichia coli O157:H7. Appl Environ Microbiol 2001; 67:2367-2370. PMID:11319125; http://dx.doi.org/10.1128/AEM.67.5.2367-2370.2001.
24. Uhlich GA, Keen JE, Elder RO. Variations in the csgD promoter of Escherichia coli O157:H7 associated with increased virulence in mice and increased invasion of HEp-2 cells. Infect Immun 2002; 70:395-699. PMID:11748206; http://dx.doi.org/10.1128/IAI.70.1.395-399.2002.
25. Provence DL, Curtiss R 3rd. Role of crl in avian pathogenic Escherichia coli: a knockout mutation of crl does not affect hemagglutination activity, fibronectin binding, or Curli production. Infect Immun 1992; 60:4460-4467. PMID:1398960.
26. Torres AG, Jeter C, Langley W, Matthysse AG. 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 2005; 71:8008-8015. PMID:16332780; http://dx.doi.org/10.1128/AEM.71.12.8008-8015.2005.
27. Fink RC, Black EP, Hou Z, Sugawara M, Sadowsky MJ, Diez-Gonzalez F. Transcriptional responses of Escherichia coli K-12 and O157:H7 associated with lettuce leaves. Appl Environ Microbiol 2012; 78:1752-1764. PMID:22247152; http://dx.doi.org/10.1128/AEM.07454-11.
28. Macarisin D, Patel J, Bauchan G, Giron JA, Sharma VK. Role of curli and cellulose expression in adherence of Escherichia coli O157:H7 to spinach leaves. Foodborne Pathog Dis 2012; 9:160-167. PMID:22315954; http://dx.doi.org/10.1089/fpd.2011.1020.
29. Torres AG, Zhou X, Kaper JB. Adherence of diarrheagenic Escherichia coli strains to epithelial cells. Infect Immun 2005; 73:18-29. PMID:15618137; http://dx.doi.org/10.1128/IAI.73.1.18-29.2005.
30. Jubelin G, Vianney A, Beloin C, Ghigo JM, Lazzaroni JC, Lejeune P, et al. CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J Bacteriol 2005; 187:2038-2049. PMID:15743952; http://dx.doi.org/10.1128/JB.187.6.2038-2049.2005.
31. Chapman MR, Robinson LS, Pinkner JS, Roth R, Heuser J, Hammar M, et al. Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 2002; 295:851-855. PMID:11823641; http://dx.doi.org/10.1126/science.1067484.
32. Bian Z, Brauner A, Li Y, Normark S. Expression of and cytokine activation by Escherichia coli curli fibers in human sepsis. J Infect Dis 2000; 181:602-612. PMID:10669344; http://dx.doi.org/10.1086/315233.
33. Saldaña Z, Xicohtencatl-Cortes J, Avelino F, Phillips AD, Kaper JB, Puente JL, et al. 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 2009; 11:992-1006; PMID:19187284; http://dx.doi.org/10.1111/j.1462-2920.2008.01824.x.
34. Uhlich GA, Gunther NW 4th, Bayles DO, Mosier DA. The CsgA and Lpp proteins of an Escherichia coli O157:H7 strain affect HEp-2 cell invasion, motility, and biofilm formation. Infect Immun 2009; 77:1543-1552. PMID:19179421; http://dx.doi.org/10.1128/IAI.00949-08.
35. Carter MQ, Brandl MT, Louie JW, Kyle JL, Carychao DK, Cooley MB, et al. Distinct acid resistance and survival fitness displayed by Curli variants of enterohemorrhagic Escherichia coli O157:H7. Appl Environ Microbiol 2011; 77:3685-3695. PMID:21478320; http://dx.doi.org/10.1128/AEM.02315-10.
36. White AP, Sibley KA, Sibley CD, Wasmuth JD, Schaefer R, Surette MG, et al. Intergenic sequence comparison of Escherichia coli isolates reveals lifestyle adaptations but not host specificity. Appl Environ Microbiol 2011; 77:7620-7632. PMID:21908635; http://dx.doi.org/10.1128/AEM.05909-11.
37. Luo C, Walk ST, Gordon DM, Feldgarden M, Tiedje JM, Konstantinidis KT. Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species. Proc Natl Acad Sci U S A 2011; 108:7200-8205. PMID:21482770; http://dx.doi.org/10.1073/pnas.1015622108.
38. Holden NJ, Gally DL. Switches, cross-talk and memory in Escherichia coli adherence. J Med Microbiol 2004; 53:585-593. PMID:15184527; http://dx.doi.org/10.1099/jmm.0.05491-0.
39. Low AS, Holden N, Rosser T, Roe AJ, Constantinidou C, Hobman JL, et al. Analysis of fimbrial gene clusters and their expression in enterohaemorrhagic Escherichia coli O157:H7. Environ Microbiol 2006; 8:1033-1047. PMID:16689724; http://dx.doi.org/10.1111/j.1462-2920.2006.00995.x.
40. Schembri MA, Klemm P. Coordinate gene regulation by fimbriae-induced signal transduction. EMBO J 2001; 20:3074-3081. PMID:11406584; http://dx.doi.org/10.1093/emboj/20.12.3074.
41. Ogasawara H, Yamada K, Kori A, Yamamoto K, Ishihama A. Regulation of the Escherichia coli csgD promoter: interplay between five transcription factors. Microbiology 2010; 156:2470-2483. PMID:20466769; http://dx.doi.org/10.1099/mic.0.039131-0.
42. Lee JH, Kim YG, Cho MH, Wood TK, Lee J. Transcriptomic analysis for genetic mechanisms of the factors related to biofilm formation in Escherichia coli O157:H7. Curr Microbiol 2011; 62:1321-1330. PMID:21221972; http://dx.doi.org/10.1007/s00284-010-9862-4.
43. Torres AG, López-Sánchez GN, Milflores-Flores L, Patel SD, Rojas-López M, Martínez de la Peña CF, et al. Ler and H-NS, regulators controlling expression of the long polar fimbriae of Escherichia coli O157:H7. J Bacteriol 2007; 189:5916-5928. PMID:17586645; http://dx.doi.org/10.1128/JB.00245-07.
44. Torres AG, Slater TM, Patel SD, Popov VL, Arenas- Hernández MMP. Contribution of the Ler- and H-NS-regulated long polar fimbriae of Escherichia coli O157:H7 during binding to tissue-cultured cells. Infect Immun 2008; 76:5062-5071. PMID:18794291; http://dx.doi.org/10.1128/IAI.00654-08.
45. Dong T, Schellhorn HE. Global effect of RpoS on gene expression in pathogenic Escherichia coli O157:H7 strain EDL933. BMC Genomics 2009; 10:349. PMID:19650909; http://dx.doi.org/10.1186/1471-2164-10-349.
46. Eppinger M, Mammel MK, Leclerc JE, Ravel J, Cebula TA. Genomic anatomy of Escherichia coli O157:H7 outbreaks. Proc Natl Acad Sci U S A 2011; 108:20142-20147. PMID:22135463; http://dx.doi.org/10.1073/pnas.1107176108.