Hfq affects the expression of the LEE pathogenicity island in enterohaemorrhagic Escherichia coli

Molecular Microbiology

Volumn 73, Issue 3, 2009, Pages 446-465

  Hansen, Anne Marie ^a   Kaper, James B ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; RNA;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI K 12; GENE EXPRESSION REGULATION; INTESTINE EPITHELIUM CELL; LOCUS OF ENTEROCYTE EFFACEMENT PATHOGENICITY ISLAND; NONHUMAN; PATHOGENICITY ISLAND; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION;

ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENOMIC ISLANDS; HOST FACTOR 1 PROTEIN; PHOSPHOPROTEINS; REPRESSOR PROTEINS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, BACTERIAL; TRANS-ACTIVATORS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 67651204873     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06781.x     Document Type: Article

References (114)

1. Abe, H., Miyahara, A., Oshima, T., Tashiro, K., Ogura, Y., Kuhara, S., et al. (2008) Global regulation by horizontally transferred regulators establishes the pathogenicity of Escherichia coli. DNA Res 15 : 25 38.
2. Aiba, H. (2007) Mechanism of RNA silencing by Hfq-binding small RNAs. Curr Opin Microbiol 10 : 134 139.
3. Ali, A.T., Iwata, A., Nishimura, A., Ueda, S. Ishihama, A. (1999) Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol 181 : 6361 6370.
4. Atlung, T. Ingmer, H. (1997) H-NS: a modulator of environmentally regulated gene expression. Mol Microbiol 24 : 7 17.
5. Attia, A.S., Sedillo, J.L., Wang, W., Liu, W., Brautigam, C.A., Winkler, W. Hansen, E.J. (2008) Moraxella catarrhalis expresses an unusual Hfq protein. Infect Immun 76 : 2520 2530.
6. Barba, J., Bustamante, V.H., Flores-Valdez, M.A., Deng, W., Finlay, B.B. Puente, J.L. (2005) A positive regulatory loop controls expression of the locus of enterocyte effacement-encoded regulators Ler and GrlA. J Bacteriol 187 : 7918 7930.
7. Bertin, P., Terao, E., Lee, E.H., Lejeune, P., Colson, C., Danchin, A. Collatz, E. (1994) The H-NS protein is involved in the biogenesis of flagella in Escherichia coli. J Bacteriol 176 : 5537 5540.
8. Blattner, F.R., Plunkett, G., III, Bloch, C.A., Perna, N.T., Burland, V., Riley, M., et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277 : 1453 1474.
9. Bolivar, F., Rodriguez, R.L., Greene, P.J., Betlach, M.C., Heyneker, H.L. Boyer, H.W. (1977) Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene 2 : 95 113. (Pubitemid 9021046)
10. Brennan, R.G. Link, T.M. (2007) Hfq structure, function and ligand binding. Curr Opin Microbiol 10 : 125 133.
11. Brescia, C.C., Mikulecky, P.J., Feig, A.L. Sledjeski, D.D. (2003) Identification of the Hfq-binding site on DsrA RNA: Hfq binds without altering DsrA secondary structure. RNA 9 : 33 43.
12. Brown, L. Elliott, T. (1996) Efficient translation of the RpoS sigma factor in Salmonella typhimurium requires host factor I, an RNA-binding protein encoded by the hfq gene. J Bacteriol 178 : 3763 3770.
13. Bustamante, V.H., Santana, F.J., Calva, E. Puente, J.L. (2001) Transcriptional regulation of type III secretion genes in enteropathogenic Escherichia coli: Ler antagonizes H-NS-dependent repression. Mol Microbiol 39 : 664 678.
14. Campellone, K.G., Roe, A.J., Løbner-Olesen, A., Murphy, K.C., Magoun, L., Brady, M.J., et al. (2007) Increased adherence and actin pedestal formation by dam-deficient enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol 63 : 1468 1481.
15. R cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158 : 9 14.
16. Christiansen, J.K., Nielsen, J.S., Ebersbach, T., Valentin-Hansen, P., Søgaard-Andersen, L. Kallipolitis, B.H. (2006) Identification of small Hfq-binding RNAs in Listeria monocytogenes. RNA 12 : 1383 1396.
17. Creasey, E.A., Delahay, R.M., Daniell, S.J. Frankel, G. (2003) Yeast two-hybrid system survey of interactions between LEE-encoded proteins of enteropathogenic Escherichia coli. Microbiology 149 : 2093 2106.
18. Dam Mikkelsen, N. Gerdes, K. (1997) Sok antisense RNA from plasmid R1 is functionally inactivated by RNaseE and polyadenylated by poly(A) polymerase I. Mol Microbiol 26 : 311 320.
19. Datsenko, K.A. Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97 : 6640 6645.
20. Deng, W., Li, Y., Vallance, B.A. Finlay, B.B. (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.
21. Deng, W., Puente, J.L., Gruenheid, S., Li, Y., Vallance, B.A., Vazquez, A., et al. (2004) Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci USA 101 : 3597 3602.
22. Ding, Y., Davis, B.M. Waldor, M.K. (2004) Hfq is essential for Vibrio cholerae virulence and downregulates sigma expression. Mol Microbiol 53 : 345 354.
23. Donohue-Rolfe, A., Kondova, I., Oswald, S., Hutto, D. 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.
24. Elliott, S.J., Wainwright, L.A., McDaniel, T.K., Jarvis, K.G., Deng, Y.K., Lai, L.C., et al. (1998) The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69. Mol Microbiol 28 : 1 4.
25. Elliott, S.J., Sperandio, V., Giron, J.A., Shin, S., Mellies, J.L., Wainwright, L., et al. (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.
26. Fantappiè, L., Metruccio, M.M., Seib, K.L., Oriente, F., Cartocci, E., Ferlicca, F., et al. (2009) The RNA chaperone Hfq is involved in stress response and virulence in Neisseria meningitidis and is a pleiotropic regulator of protein expression. Infect Immun 77 : 1842 1853.
27. Frankel, G., Phillips, A.D., Rosenshine, I., Dougan, G., Kaper, J.B. Knutton, S. (1998) Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements. Mol Microbiol 30 : 911 921.
28. Franze de Fernandez, M.T., Eoyang, L. August, J.T. (1968) Factor fraction required for the synthesis of bacteriophage Qbeta-RNA. Nature 219 : 588 590.
29. 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.
30. Garmendia, J., Frankel, G. Crepin, V.F. (2005) Enteropathogenic and enterohemorrhagic Escherichia coli infections: translocation, translocation, translocation. Infect Immun 73 : 2573 2585. (Pubitemid 40570322)
31. Geissmann, T.A. Touati, D. (2004) Hfq, a new chaperoning role: binding to messenger RNA determines access for small RNA regulator. EMBO J 23 : 396 405.
32. 32-mediated cytoplasmic stress response in Escherichia coli. J Bacteriol 189 : 1963 1973.
33. Haack, K.R., Robinson, C.L., Miller, K.J., Fowlkes, J.W. Mellies, J.L. (2003) Interaction of Ler at the LEE5 (tir) operon of enteropathogenic Escherichia coli. Infect Immun 71 : 384 392.
34. Hansen, A.M., Qiu, Y., Yeh, N., Blattner, F.R., Durfee, T. Jin, D.J. (2005) SspA is required for acid resistance in stationary phase by downregulation of H-NS in Escherichia coli. Mol Microbiol 56 : 719 734.
35. Hirakawa, H., Kodama, T., Takumi-Kobayashi, A., Honda, T. Yamaguchi, A. (2009) Secreted indole serves as a signal for expression of type III secretion system translocators in enterohaemorrhagic Escherichia coli O157:H7. Microbiology 155 : 541 550.
36. Huang, L.H. Syu, W.J. (2008) GrlA of enterohemorrhagic Escherichia coli O157:H7 activates LEE1 by binding to the promoter region. J Microbiol Immunol Infect 41 : 9 16.
37. Huys, G., Cnockaert, M., Janda, J.M. Swings, J. (2003) Escherichia albertii sp. nov., a diarrhoeagenic species isolated from stool specimens of Bangladeshi children. Int J Syst Evol Microbiol 53 : 807 810.
38. Iyoda, S., Koizumi, N., Satou, H., Lu, Y., Saitoh, T., Ohnishi, M. Watanabe, H. (2006) The GrlR-GrlA regulatory system coordinately controls the expression of flagellar and LEE-encoded type III protein secretion systems in enterohemorrhagic Escherichia coli. J Bacteriol 188 : 5682 5692.
39. Jerse, A.E., Yu, J., Tall, B.D. 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.
40. Jobichen, C., Li, M., Yerushalmi, G., Tan, Y.W., Mok, Y.K., Rosenshine, I., et al. (2007) Structure of GrlR and the implication of its EDED motif in mediating the regulation of type III secretion system in EHEC. PLoS Pathog 3 : e69.
41. Kaper, J.B., Nataro, J.P. Mobley, H.L. (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2 : 123 140.
42. Kawamoto, H., Koide, Y., Morita, T. Aiba, H. (2006) Base-pairing requirement for RNA silencing by a bacterial small RNA and acceleration of duplex formation by Hfq. Mol Microbiol 61 : 1013 1022.
43. Knutton, S., Baldwin, T., Williams, P.H. 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.
44. Kulesus, R.R., Diaz-Perez, K., Slechta, E.S., Eto, D.S. Mulvey, M.A. (2008) Impact of the RNA chaperone Hfq on the fitness and virulence potential of uropathogenic Escherichia coli. Infect Immun 76 : 3019 3026.
45. Laaberki, M.H., 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.
46. Lease, R.A. Belfort, M. (2000) Riboregulation by DsrA RNA: trans-actions for global economy. Mol Microbiol 38 : 667 672.
47. Lease, R.A., Cusick, M.E. Belfort, M. (1998) Riboregulation in Escherichia coli: DsrA RNA acts by RNA:RNA interactions at multiple loci. Proc Natl Acad Sci USA 95 : 12456 12461.
48. Lenz, D.H., Mok, K.C., Lilley, B.N., Kulkarni, R.V., Wingreen, N.S. Bassler, B.L. (2004) The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118 : 69 82.
49. Levine, M.M., Bergquist, E.J., Nalin, D.R., Waterman, D.H., Hornick, R.B., Young, C.R. Sotman, S. (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.
50. Lin, J., Lee, I.S., Frey, J., Slonczewski, J.L. Foster, J.W. (1995) Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli. J Bacteriol 177 : 4097 4104.
51. T method. Methods 25 : 402 408.
52. Lodato, P.B. Kaper, J.B. (2008) Post-transcriptional processing of the LEE4 operon in enterohaemorrhagic Escherichia coli. Mol Microbiol 71 : 273 290.
53. McDaniel, T.K., Jarvis, K.G., Donnenberg, M.S. Kaper, J.B. (1995) A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci USA 92 : 1664 1668.
54. McNealy, T.L., Forsbach-Birk, V., Shi, C. Marre, R. (2005) The Hfq homolog in Legionella pneumophila demonstrates regulation by LetA and RpoS and interacts with the global regulator CsrA. J Bacteriol 187 : 1527 1532.
55. Majdalani, N., Vanderpool, C.K. Gottesman, S. (2005) Bacterial small RNA regulators. Crit Rev Biochem Mol Biol 40 : 93 113.
56. Masuda, N. Church, G.M. (2002) Escherichia coli gene expression responsive to levels of the response regulator EvgA. J Bacteriol 184 : 6225 6234.
57. Meibom, K.L., Forslund, A.L., Kuoppa, K., Alkhuder, K., Dubail, I., Dupuis, M., et al. (2009) Hfq, a novel pleiotropic regulator of virulence-associated genes in Francisella tularensis. Infect Immun 77 : 1866 1880.
58. Mellies, J.L., Elliott, S.J., Sperandio, V., Donnenberg, M.S. Kaper, J.B. (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.
59. Mellies, J.L., Barron, A.M. Carmona, A.M. (2007) Enteropathogenic and enterohemorrhagic Escherichia coli virulence gene regulation. Infect Immun 75 : 4199 4210.
60. Mellies, J.L., Larabee, F.J., Zarr, M.A., Horback, K.L., Lorenzen, E. Mavor, D. (2008) Ler interdomain linker is essential for anti-silencing activity in enteropathogenic Escherichia coli. Microbiology 154 : 3624 3638.
61. Miller, J.F. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press.
62. Mitobe, J., Morita-Ishihara, T., Ishihama, A. Watanabe, H. (2008) Involvement of RNA-binding protein Hfq in the post-transcriptional regulation of invE gene expression in Shigella sonnei. J Biol Chem 283 : 5738 5747.
63. Mohanty, B.K., Maples, V.F. Kushner, S.R. (2004) The Sm-like protein Hfq regulates polyadenylation dependent mRNA decay in Escherichia coli. Mol Microbiol 54 : 905 920.
64. Moll, I., Leitsch, D., Steinhauser, T. Bläsi, U. (2003) RNA chaperone activity of the Sm-like Hfq protein. EMBO Rep 4 : 284 289.
65. Møller, T., Franch, T., Højrup, P., Keene, D.R., Bächinger, H.P., Brennan, R.G. Valentin-Hansen, P. (2002) Hfq: a bacterial Sm-like protein that mediates RNA-RNA interaction. Mol Cell 9 : 23 30.
66. Morita, T., Maki, K. Aiba, H. (2005) RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Dev 19 : 2176 2186.
67. Muffler, A., Fischer, D. Hengge-Aronis, R. (1996) The RNA-binding protein HF-I, known as a host factor for phage Qbeta RNA replication, is essential for rpoS translation in Escherichia coli. Genes Dev 10 : 1143 1151.
68. Murphy, K.C. Campellone, K.G. (2003) Lambda Red-mediated recombinogenic engineering of enterohemorrhagic and enteropathogenic E. coli. BMC Mol Biol 4 : 11.
69. Nakao, H., Watanabe, H., Nakayama, S. Takeda, T. (1995) yst gene expression in Yersinia enterocolitica is positively regulated by a chromosomal region that is highly homologous to Escherichia coli host factor 1 gene (hfq). Mol Microbiol 18 : 859 865.
70. Nataro, J.P. Kaper, J.B. (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11 : 142 201.
71. Navarre, W.W., Porwollik, S., Wang, Y., McClelland, M., Rosen, H., Libby, S.J. Fang, F.C. (2006) Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313 : 236 238.
72. Opdyke, J.A., Kang, J.G. Storz, G. (2004) GadY, a small-RNA regulator of acid response genes in Escherichia coli. J Bacteriol 186 : 6698 6705. (Pubitemid 39332106)
73. Perna, N.T., Mayhew, G.F., Posfai, G., Elliott, S., Donnenberg, M.S., Kaper, J.B. Blattner, F.R. (1998) Molecular evolution of a pathogenicity island from enterohemorrhagic Escherichia coli O157:H7. Infect Immun 66 : 3810 3817.
74. Porter, M.E., Mitchell, P., Roe, A.J., Free, A., Smith, D.G. Gally, D.L. (2004) Direct and indirect transcriptional activation of virulence genes by an AraC-like protein, PerA from enteropathogenic Escherichia coli. Mol Microbiol 54 : 1117 1133.
75. Porter, M.E., Mitchell, P., Free, A., Smith, D.G. Gally, D.L. (2005) The LEE1 promoters from both enteropathogenic and enterohemorrhagic Escherichia coli can be activated by PerC-like proteins from either organism. J Bacteriol 187 : 458 472.
76. Posfai, G., Koob, M.D., Kirkpatrick, H.A. Blattner, F.R. (1997) Versatile insertion plasmids for targeted genome manipulations in bacteria: isolation, deletion, and rescue of the pathogenicity island LEE of the Escherichia coli O157:H7 genome. J Bacteriol 179 : 4426 4428.
77. Poteete, A.R. Fenton, A.C. (1984) Lambda red-dependent growth and recombination of phage P22. Virology 15 : 161 167.
78. Price, S.B., Cheng, C.M., Kaspar, C.W., Wright, J.C., DeGraves, F.J., Penfound, T.A., et al. (2000) Role of rpoS in acid resistance and fecal shedding of Escherichia coli O157:H7. Appl Environ Microbiol 66 : 632 637.
79. Rasko, D.A., Rosovitz, M.J., Myers, G.S., Mongodin, E.F., Fricke, W.F., Gajer, P., et al. (2008) The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bacteriol 190 : 6881 6893.
80. Repoila, F. Darfeuille, F. (2009) Small regulatory non-coding RNAs in bacteria: physiology and mechanistic aspects. Biol Cell 101 : 117 131.
81. Repoila, F. Gottesman, S. (2003) Temperature sensing by the dsrA promoter. J Bacteriol 185 : 6609 6614.
82. Robertson, G.T. Roop, R.M., Jr (1999) The Brucella abortus host factor I (HF-I) protein contributes to stress resistance during stationary phase and is a major determinant of virulence in mice. Mol Microbiol 34 : 690 700.
83. Roe, A.J., Yull, H., Naylor, S.W., Woodward, M.J., Smith, D.G. Gally, D.L. (2003) Heterogeneous surface expression of EspA translocon filaments by Escherichia coli O157:H7 is controlled at the posttranscriptional level. Infect Immun 71 : 5900 5909.
84. Roe, A.J., Naylor, S.W., Spears, K.J., Yull, H.M., Dransfield, T.A., Oxford, M., et al. (2004) Co-ordinate single-cell expression of LEE4- and LEE5-encoded proteins of Escherichia coli O157:H7. Mol Microbiol 54 : 337 352.
85. Roe, A.J., Tysall, L., Dransfield, T., Wang, D., Fraser-Pitt, D., Mahajan, A., et al. (2007) Analysis of the expression, regulation and export of NleA-E in Escherichia coli O157:H7. Microbiology 153 : 1350 1360.
86. Russell, R.M., Sharp, F.C., Rasko, D.A. Sperandio, V. (2007) QseA and GrlR/GrlA regulation of the locus of enterocyte effacement genes in enterohemorrhagic Escherichia coli. J Bacteriol 189 : 5387 5392.
87. Saitoh, T., Iyoda, S., Yamamoto, S., Lu, Y., Shimuta, K., Ohnishi, M., et al. (2008) Transcription of the ehx enterohemolysin gene is positively regulated by GrlA, a global regulator encoded within the locus of enterocyte effacement in enterohemorrhagic Escherichia coli. J Bacteriol 190 : 4822 4830.
88. Sambrook, J. Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press.
89. Sanchez-SanMartin, C., Bustamante, V.H., Calva, E. 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. (Pubitemid 32319285)
90. Schumacher, M.A., Pearson, R.F., Møller, T., Valentin-Hansen, P. Brennan, R.G. (2002) Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: a bacterial Sm-like protein. EMBO J 21 : 3546 3556.
91. Sharp, F.C. Sperandio, V. (2007) QseA directly activates transcription of LEE1 in enterohemorrhagic Escherichia coli. Infect Immun 75 : 2432 2440.
92. Shifrin, Y., Peleg, A., Ilan, O., Nadler, C., Kobi, S., Baruch, K., et al. (2008) Transient shielding of intimin and the type III secretion system of enterohemorrhagic and enteropathogenic Escherichia coli by a group 4 capsule. J Bacteriol 190 : 5063 5074. (Pubitemid 351991074)
93. Shin, S., Castanie-Cornet, M.P., Foster, J.W., Crawford, J.A., Brinkley, C. Kaper, J.B. (2001) An activator of glutamate decarboxylase genes regulates the expression of enteropathogenic Escherichia coli virulence genes through control of the plasmid-encoded regulator, Per. Mol Microbiol 41 : 1133 1150.
94. Sittka, A., Pfeiffer, V., Tedin, K. Vogel, J. (2007) The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium. Mol Microbiol 63 : 193 217.
95. Sledjeski, D.D., Whitman, C. Zhang, A. (2001) Hfq is necessary for regulation by the untranslated RNA DsrA. J Bacteriol 183 : 1997 2005.
96. Sonnleitner, E., Hagens, S., Rosenau, F., Wilhelm, S., Habel, A., Jäger, K.E. Bläsi, U. (2003) Reduced virulence of a hfq mutant of Pseudomonas aeruginosa O1. Microb Pathog 35 : 217 228.
97. Soper, T.J. Woodson, S.A. (2008) The rpoS mRNA leader recruits Hfq to facilitate annealing with DsrA sRNA. RNA 14 : 1907 1917.
98. Sperandio, V., Mellies, J.L., Nguyen, W., Shin, S. 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 USA 96 : 15196 15201.
99. Sperandio, V., Mellies, J.L., Delahay, R.M., Frankel, G., Crawford, J.A., Nguyen, W. Kaper, J.B. (2000) Activation of enteropathogenic Escherichia coli (EPEC) LEE2 and LEE3 operons by Ler. Mol Microbiol 38 : 781 793.
100. Sperandio, V., Li, C.C. Kaper, J.B. (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.
101. Sperandio, V., Torres, A.G., Jarvis, B., Nataro, J.P. Kaper, J.B. (2003) Bacteria-host communication: the language of hormones. Proc Natl Acad Sci USA 100 : 8951 8956.
102. Stoebel, D.M., Free, A. Dorman, C.J. (2008) Anti-silencing: overcoming H-NS-mediated repression of transcription in Gram-negative enteric bacteria. Microbiology 154 : 2533 2545.
103. Torres, A.G., Lopez-Sanchez, G.N., Milflores-Flores, L., Patel, S.D., Rojas-Lopez, M., Martinez de la Pena, C.F., et al. (2007) Ler and H-NS, regulators controlling expression of the long polar fimbriae of Escherichia coli O157:H7. J Bacteriol 189 : 5916 5928. (Pubitemid 47236144)
104. Tsai, N.P., Wu, Y.C., Chen, J.W., Wu, C.F., Tzeng, C.M. Syu, W.J. (2006) Multiple functions of l0036 in the regulation of the pathogenicity island of enterohaemorrhagic Escherichia coli O157:H7. Biochem J 393 : 591 599.
105. Tsui, H.C., Leung, H.C. Winkler, M.E. (1994) Characterization of broadly pleiotropic phenotypes caused by an hfq insertion mutation in Escherichia coli K-12. Mol Microbiol 13 : 35 49.
106. Umanski, T., Rosenshine, I. Friedberg, D. (2002) Thermoregulated expression of virulence genes in enteropathogenic Escherichia coli. Microbiology 148 : 2735 2744.
107. Updegrove, T., Wilf, N., Sun, X. Wartell, R.M. (2008) Effect of Hfq on RprA-rpoS mRNA pairing: Hfq-RNA binding and the influence of the 5′ rpoS mRNA leader region. Biochemistry 47 : 11184 11195.
108. Valentin-Hansen, P., Eriksen, M. Udesen, C. (2004) The bacterial Sm-like protein Hfq: a key player in RNA transactions. Mol Microbiol 51 : 1525 1533.
109. Valentin-Hansen, P., Johansen, J. Rasmussen, A.A. (2007) Small RNAs controlling outer membrane porins. Curr Opin Microbiol 10 : 152 155.
110. Walters, M. Sperandio, V. (2006) Autoinducer 3 and epinephrine signaling in the kinetics of locus of enterocyte effacement gene expression in enterohemorrhagic Escherichia coli. Infect Immun 74 : 5445 5455.
111. Waters, L.S. Storz, G. (2009) Regulatory RNAs in bacteria. Cell 136 : 615 628.
112. Wilson, J.W., Ott, C.M., Honer zu, B.K., Ramamurthy, R., Quick, L., Porwollik, S., et al. (2007) Space flight alters bacterial gene expression and virulence and reveals a role for global regulator Hfq. Proc Natl Acad Sci USA 104 : 16299 16304.
113. Yerushalmi, G., Nadler, C., Berdichevski, T. Rosenshine, I. (2008) Mutational analysis of the locus of enterocyte effacement-encoded regulator (Ler) of enteropathogenic Escherichia coli. J Bacteriol 190 : 7808 7818.
114. Zhang, A., Wassarman, K.M., Ortega, J., Steven, A.C. Storz, G. (2002) The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Mol Cell 9 : 11 22.