The RNA binding protein CsrA is a pleiotropic regulator of the locus of enterocyte effacement pathogenicity island of enteropathogenic Escherichia coli

Infection and Immunity

Volumn 77, Issue 9, 2009, Pages 3552-3568

  Bhatt, Shantanu ^a,b   Edwards, Adrianne Nehrling ^b   Nguyen, Hang Thi Thu ^a   Merlin, Didier ^a   Romeo, Tony ^b,c   Kalman, Daniel ^a,b,d  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

^d Department of Pathology ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; ESCHERICHIA COLI SECRETED PROTEIN A; MESSENGER RNA; PROTEIN ESPB; PROTEIN ESPD; RNA BINDING PROTEIN; RNA BINDING PROTEIN CSRA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANIMAL CELL; ARTICLE; BACTERIAL GENE; CSRA GENE; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCD GENE; GENE CONTROL; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; GRLRA GENE; INTESTINE CELL; LEE1 GENE; LEE2 GENE; LEE4 GENE; LEE5 GENE; NONHUMAN; PATHOGENICITY ISLAND; PRIORITY JOURNAL; TYPE III SECRETION SYSTEM;

3T3 CELLS; ANIMALS; BACTERIAL ADHESION; BINDING SITES; CELL POLARITY; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENOMIC ISLANDS; GLYCOGEN; MICE; OPERON; PHOSPHOPROTEINS; RECEPTORS, CELL SURFACE; REPRESSOR PROTEINS; RNA-BINDING PROTEINS; TRANS-ACTIVATORS;

EID: 69049116272     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00418-09     Document Type: Article

References (100)

1. Abe, H., I. Tatsuno, T. Tobe, A. Okutani, and C. Sasakawa. 2002. Bicarbonate ion stimulates the expression of locus of enterocyte effacementencoded genes in enterohemorrhagic Escherichia coli O157:H7. Infect. Immun. 70:3500-3509.
2. Altier, C., M. Suyemoto, and S. D. Lawhon. 2000. Regulation of Salmonella enterica serovar Typhimurium invasion genes by csrA. Infect. Immun. 68:6790-6797.
3. Anyanful, A., J. Dolan-Livengood, T. Lewis, S. Sheth, M. N. DeZalia, M. Sherman, L. V. Kalman, G. M. Benian, and D. Kalman. 2005. Paralysis and killing of Caenorhabditis elegans by enteropathogenic Escherichia coli requires the bacterial tryptophanase gene. Mol. Microbiol. 57:988-1007.
4. Babitzke, P., and T. Romeo. 2007. CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr. Opin. Microbiol. 10:156-163.
5. Baker, C. S., L. A. Eory, H. Yakhnin, J. Mercante, T. Romeo, and P. Babitzke. 2007. CsrA inhibits translation initiation of Escherichia coli hfq by binding to a single site overlapping the Shine-Dalgarno sequence. J. Bacteriol. 189:5472-5481.
6. Baker, C. S., I. Morozov, K. Suzuki, T. Romeo, and P. Babitzke. 2002. CsrA regulates glycogen biosynthesis by preventing translation of glgC in Escherichia coli. Mol. Microbiol. 44:1599-1610.
7. Barba, J., V. H. Bustamante, M. A. Flores-Valdez, W. Deng, B. B. Finlay, and J. L. Puente. 2005. A positive regulatory loop controls expression of the locus of enterocyte effacement-encoded regulators Ler and GrlA. J. Bacteriol. 187:7918-7930.
8. Barnard, F. M., M. F. Loughlin, H. P. Fainberg, M. P. Messenger, D. W. Ussery, P. Williams, and P. J. Jenks. 2004. Global regulation of virulence and the stress response by CsrA in the highly adapted human gastric pathogen Helicobacter pylori. Mol. Microbiol. 51:15-32.
9. Bommarius, B., D. Maxwell, A. Swimm, S. Leung, A. Corbett, W. Bornmann, and D. Kalman. 2007. Enteropathogenic Escherichia coli Tir is an SH2/3 ligand that recruits and activates tyrosine kinases required for pedestal formation. Mol. Microbiol. 63:1748-1768.
10. Burrowes, E., C. Baysse, C. Adams, and F. O'Gara. 2006. Influence of the regulatory protein RsmA on cellular functions in Pseudomonas aeruginosa PAO1, as revealed by transcriptome analysis. Microbiology 152:405-418.
11. Bustamante, V. H., F. J. Santana, E. Calva, and J. L. Puente. 2001. Transcriptional regulation of type III secretion genes in enteropathogenic Escherichia coli: Ler antagonizes H-NS-dependent repression. Mol. Microbiol. 39:664-678.
12. Canil, C., I. Rosenshine, S. Ruschkowski, M. S. Donnenberg, J. B. Kaper, and B. B. Finlay. 1993. Enteropathogenic Escherichia coli decreases the transepithelial electrical resistance of polarized epithelial monolayers. Infect. Immun. 61:2755-2762.
13. Chen, H. D., and G. Frankel. 2005. Enteropathogenic Escherichia coli: unravelling pathogenesis. FEMS Microbiol. Rev. 29:83-98.
14. Cleary, J., L. C. Lai, R. K. Shaw, A. Straatman-Iwanowska, M. S. Donnenberg, G. Frankel, and S. Knutton. 2004. Enteropathogenic Escherichia coli (EPEC) adhesion to intestinal epithelial cells: role of bundle-forming pili (BFP), EspA filaments and intimin. Microbiology 150:527-538.
15. Creasey, E. A., R. M. Delahay, S. J. Daniell, and G. Frankel. 2003. Yeast two-hybrid system survey of interactions between LEE-encoded proteins of enteropathogenic Escherichia coli. Microbiology 149:2093- 2106.
16. Cui, Y., A. Chatterjee, Y. Liu, C. K. Dumenyo, and A. K. Chatterjee. 1995. Identification of a global repressor gene, rsmA, of Erwinia carotovora subsp. carotovora that controls extracellular enzymes, N-(3-oxohexanoyl)-L-homoserine lactone, and pathogenicity in soft-rotting Erwinia spp. J. Bacteriol. 177:5108-5115.
17. Daniell, S. J., N. Takahashi, R. Wilson, D. Friedberg, I. Rosenshine, F. P. Booy, R. K. Shaw, S. Knutton, G. Frankel, and S. Aizawa. 2001. The filamentous type III secretion translocon of enteropathogenic Escherichia coli. Cell. Microbiol. 3:865-871.
18. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
19. Dean, P., and B. Kenny. 2004. Intestinal barrier dysfunction by enteropathogenic Escherichia coli is mediated by two effector molecules and a bacterial surface protein. Mol. Microbiol. 54:665-675.
20. Deng, W., Y. Li, P. R. Hardwidge, E. A. Frey, R. A. Pfuetzner, S. Lee, S. Gruenheid, N. C. Strynakda, J. L. Puente, and B. B. Finlay. 2005. Regulation of type III secretion hierarchy of translocators and effectors in attaching and effacing bacterial pathogens. Infect. Immun. 73:2135-2146.
21. Deng, W., J. L. Puente, S. Gruenheid, Y. Li, B. A. Vallance, A. Vazquez, J. Barba, J. A. Ibarra, P. O'Donnell, P. Metalnikov, K. Ashman, S. Lee, D. Goode, T. Pawson, and B. B. Finlay. 2004. Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc. Natl. Acad. Sci. USA 101:3597-3602.
22. Donnenberg, M. S., J. Yu, and J. B. Kaper. 1993. A second chromosomal gene necessary for intimate attachment of enteropathogenic Escherichia coli to epithelial cells. J. Bacteriol. 175:4670-4680.
23. Dubey, A. K., C. S. Baker, T. Romeo, and P. Babitzke. 2005. RNA sequence and secondary structure participate in high-affinity CsrA-RNA interaction. RNA 11:1579-1587.
24. Dubey, A. K., C. S. Baker, K. Suzuki, A. D. Jones, P. Pandit, T. Romeo, and P. Babitzke. 2003. CsrA regulates translation of the Escherichia coli carbon starvation gene, cstA, by blocking ribosome access to the cstA transcript. J. Bacteriol. 185:4450-4460.
25. Elliott, S. J., S. W. Hutcheson, M. S. Dubois, J. L. Mellies, L. A. Wainwright, M. Batchelor, G. Frankel, S. Knutton, and J. B. Kaper. 1999. Identification of CesT, a chaperone for the type III secretion of Tir in enteropathogenic Escherichia coli. Mol. Microbiol. 33:1176-1189.
26. Elliott, S. J., V. Sperandio, J. A. Giron, S. Shin, J. L. Mellies, L. Wainwright, S. W. Hutcheson, T. K. McDaniel, and J. B. Kaper. 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.
27. Forsbach-Birk, V., T. McNealy, S. Chunwei, D. Lynch, and R. Marre. 2004. Reduced expression of the global regulator protein CsrA in Legionella pneumophila affects virulence-associated regulators and growth in Acanthamoeba castellanii. Int. J. Med. Microbiol. 294:15-25.
28. Foubister, V., I. Rosenshine, M. S. Donnenberg, and B. B. Finlay. 1994. The eaeB gene of enteropathogenic Escherichia coli is necessary for signal transduction in epithelial cells. Infect. Immun. 62:3038-3040.
29. Friedberg, D., T. Umanski, Y. Fang, and I. Rosenshine. 1999. Hierarchy in the expression of the locus of enterocyte effacement genes of enteropathogenic Escherichia coli. Mol. Microbiol. 34:941-952.
30. Goldberg, M. D., M. Johnson, J. C. Hinton, and P. H. Williams. 2001. Role of the nucleoid-associated protein Fis in the regulation of virulence properties of enteropathogenic Escherichia coli. Mol. Microbiol. 41:549-559.
31. Grant, A. J., M. Farris, P. Alefounder, P. H. Williams, M. J. Woodward, and C. D. O'Connor. 2003. Co-ordination of pathogenicity island expression by the BipA GTPase in enteropathogenic Escherichia coli (EPEC). Mol. Microbiol. 48:507-521.
32. Gruenheid, S., R. DeVinney, F. Bladt, D. Goosney, S. Gelkop, G. D. Gish, T. Pawson, and B. B. Finlay. 2001. Enteropathogenic E. coli Tir binds Nck to initiate actin pedestal formation in host cells. Nat. Cell Biol. 3:856-859.
33. Gutiérrez, P., Y. Li, M. J. Osborne, E. Pomerantseva, Q. Liu, and K. Gehring. 2005. Solution structure of the carbon storage regulator protein CsrA from Escherichia coli. J. Bacteriol. 187:3496-3501.
34. Guttman, J. A., Y. Li, M. E. Wickham, W. Deng, A. W. Vogl, and B. B. Finlay. 2006. Attaching and effacing pathogen-induced tight junction disruption in vivo. Cell. Microbiol. 8:634-645.
35. Haack, K. R., C. L. Robinson, K. J. Miller, J. W. Fowlkes, and J. L. Mellies. 2003. Interaction of Ler at the LEE5 (tir) operon of enteropathogenic Escherichia coli. Infect. Immun. 71:384-392.
36. Heeb, S., S. A. Kuehne, M. Bycroft, S. Crivii, M. D. Allen, D. Haas, M. Camara, and P. Williams. 2006. Functional analysis of the post-transcriptional regulator RsmA reveals a novel RNA-binding site. J. Mol. Biol. 355:1026-1036.
37. Heroven, A. K., K. Bohme, M. Rohde, and P. Dersch. 2008. A Csr-type regulatory system, including small non-coding RNAs, regulates the global virulence regulator RovA of Yersinia pseudotuberculosis through RovM. Mol. Microbiol. 68:1179-1195.
38. Huang, L. H., and W. J. Syu. 2008. GrlA of enterohemorrhagic Escherichia coli O157:H7 activates LEE1 by binding to the promoter region. J. Microbiol. Immunol. Infect. 41:9-16.
39. Ide, T., S. Laarmann, L. Greune, H. Schillers, H. Oberleithner, and M. A. Schmidt. 2001. Characterization of translocation pores inserted into plasma membranes by type III-secreted Esp proteins of enteropathogenic Escherichia coli. Cell. Microbiol. 3:669-679.
40. Iyoda, S., and H. Watanabe. 2005. ClpXP protease controls expression of the type III protein secretion system through regulation of RpoS and GrlR levels in enterohemorrhagic Escherichia coli. J. Bacteriol. 187:4086-4094.
41. Jobichen, C., M. Li, G. Yerushalmi, Y. W. Tan, Y. K. Mok, I. Rosenshine, K. Y. Leung, and J. Sivaraman. 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.
42. Kalman, D., O. D. Weiner, D. L. Goosney, J. W. Sedat, B. B. Finlay, A. Abo, and J. M. Bishop. 1999. Enteropathogenic E. coli acts through WASP and Arp2/3 complex to form actin pedestals. Nat. Cell Biol. 1:389-391.
43. Kenny, B., A. Abe, M. Stein, and B. B. Finlay. 1997. Enteropathogenic Escherichia coli protein secretion is induced in response to conditions similar to those in the gastrointestinal tract. Infect. Immun. 65:2606-2612.
44. Kenny, B., R. Devinney, M. Stein, D. J. Reinscheid, E. A. Frey, and B. B. Finlay. 1997. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91:511-520.
45. Kenny, B., and B. B. Finlay. 1995. Protein secretion by enteropathogenic Escherichia coli is essential for transducing signals to epithelial cells. Proc. Natl. Acad. Sci. USA 92:7991-7995.
46. Kenny, B., L. C. Lai, B. B. Finlay, and M. S. Donnenberg. 1996. EspA, a protein secreted by enteropathogenic Escherichia coli, is required to induce signals in epithelial cells. Mol. Microbiol. 20:313-323.
47. Kerrinnes, T., Z. B. Zelas, W. Streckel, F. Faber, E. Tietze, H. Tschape, and S. Yaron. 2009. CsrA and CsrB are required for the post-transcriptional control of the virulence-associated effector protein AvrA of Salmonella enterica. Int. J. Med. Microbiol. 299:333-341.
48. Knutton, S., M. M. Baldini, J. B. Kaper, and A. S. McNeish. 1987. Role of plasmid-encoded adherence factors in adhesion of enteropathogenic Escherichia coli to HEp-2 cells. Infect. Immun. 55:78-85.
49. Knutton, S., T. Baldwin, P. H. Williams, and A. S. McNeish. 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.
50. Knutton, S., I. Rosenshine, M. J. Pallen, I. Nisan, B. C. Neves, C. Bain, C. Wolff, G. Dougan, and G. Frankel. 1998. A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. EMBO J. 17:2166-2176.
51. Kraiss, A., J. Blass, and J. Reidl. 1998. A suicide plasmid (pJR lacZins) for targeted integration for non-native genes into the chromosome of Escherichia coli. Tech. Tips Online 1:TO1249.
52. Kresse, A. U., F. Beltrametti, A. Muller, F. Ebel, and C. A. Guzman. 2000. Characterization of SepL of enterohemorrhagic Escherichia coli. J. Bacteriol. 182:6490-6498.
53. Laaberki, M., N. Janabi, E. Oswald, and F. Repoila. 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.
54. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
55. Lai, L. C., L. A. Wainwright, K. D. Stone, and M. S. Donnenberg. 1997. A third secreted protein that is encoded by the enteropathogenic Escherichia coli pathogenicity island is required for transduction of signals and for attaching and effacing activities in host cells. Infect. Immun. 65:2211-2217.
56. Lawhon, S. D., J. G. Frye, M. Suyemoto, S. Porwollik, M. McClelland, and C. Altier. 2003. Global regulation by CsrA in Salmonella typhimurium. Mol. Microbiol. 48:1633-1645.
57. Leverton, L. Q., and J. B. Kaper. 2005. Temporal expression of enteropathogenic Escherichia coli virulence genes in an in vitro model of infection. Infect. Immun. 73:1034-1043.
58. Liu, M. Y., G. Gui, B. Wei, J. F. Preston, 3rd, L. Oakford, U. Yuksel, D. P. Giedroc, and T. Romeo. 1997. The RNA molecule CsrB binds to the global regulatory protein CsrA and antagonizes its activity in Escherichia coli. J. Biol. Chem. 272:17502-17510.
59. Liu, M. Y., and T. Romeo. 1997. The global regulator CsrA of Escherichia coli is a specific mRNA-binding protein. J. Bacteriol. 179:4639-4642.
60. Lodato, P. B., and J. B. Kaper. 2009. Post-transcriptional processing of the LEE4 operon in enterohaemorrhagic Escherichia coli. Mol. Microbiol. 71:273-290.
61. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
62. Lucchetti-Miganeh, C., E. Burrowes, C. Baysse, and G. Ermel. 2008. The post-transcriptional regulator CsrA plays a central role in the adaptation of bacterial pathogens to different stages of infection in animal hosts. Microbiology 154:16-29.
63. McDaniel, T. K., and J. B. Kaper. 1997. A cloned pathogenicity island from enteropathogenic Escherichia coli confers the attaching and effacing phenotype on E. coli K-12. Mol. Microbiol. 23:399-407.
64. McNamara, B. P., A. Koutsouris, C. B. O'Connell, J. P. Nougayrede, M. S. Donnenberg, and G. Hecht. 2001. Translocated EspF protein from enteropathogenic Escherichia coli disrupts host intestinal barrier function. J. Clin. Investig. 107:621-629.
65. Mellies, J. L., A. M. Barron, and A. M. Carmona. 2007. Enteropathogenic and enterohemorrhagic Escherichia coli virulence gene regulation. Infect. Immun. 75:4199-4210.
66. Mellies, J. L., A. M. Barron, K. R. Haack, A. S. Korson, and D. A. Oldridge. 2006. The global regulator Ler is necessary for enteropathogenic Escherichia coli colonization of Caenorhabditis elegans. Infect. Immun. 74:64-72.
67. Mellies, J. L., S. J. Elliott, V. Sperandio, M. S. Donnenberg, and J. B. Kaper. 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.
68. Mercante, J., K. Suzuki, X. Cheng, P. Babitzke, and T. Romeo. 2006. Comprehensive alanine-scanning mutagenesis of Escherichia coli CsrA defines two subdomains of critical functional importance. J. Biol. Chem. 281:31832-31842.
69. Moon, H. W., S. C. Whipp, R. A. Argenzio, M. M. Levine, and R. A. Giannella. 1983. Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect. Immun. 41:1340-1351.
70. Murphy, K. C., and K. G. Campellone. 2003. Lambda Red-mediated recombinogenic engineering of enterohemorrhagic and enteropathogenic E. coli. BMC Mol. Biol. 4:11.
71. Nataro, J. P., and J. B. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
72. O'Connell, C. B., E. A. Creasey, S. Knutton, S. Elliott, L. J. Crowther, W. Luo, M. J. Albert, J. B. Kaper, G. Frankel, and M. S. Donnenberg. 2004. SepL, a protein required for enteropathogenic Escherichia coli type III translocation, interacts with secretion component SepD. Mol. Microbiol. 52:1613-1625.
73. Ogino, T., R. Ohno, K. Sekiya, A. Kuwae, T. Matsuzawa, T. Nonaka, H. Fukuda, S. Imajoh-Ohmi, and A. Abe. 2006. Assembly of the type III secretion apparatus of enteropathogenic Escherichia coli. J. Bacteriol. 188:2801-2811.
74. Pernestig, A. K., D. Georgellis, T. Romeo, K. Suzuki, H. Tomenius, S. Normark, and O. Melefors. 2003. The Escherichia coli BarA-UvrY two-component system is needed for efficient switching between glycolytic and gluconeogenic carbon sources. J. Bacteriol. 185:843-853.
75. Pessi, G., F. Williams, Z. Hindle, K. Heurlier, M. T. Holden, M. Camara, D. Haas, and P. Williams. 2001. The global posttranscriptional regulator RsmA modulates production of virulence determinants and N-acylhomoserine lactones in Pseudomonas aeruginosa. J. Bacteriol. 183:6676-6683.
76. Poteete, A. R., and A. C. Fenton. 1984. Lambda red-dependent growth and recombination of phage P22. Virology 134:161-167.
77. Rife, C., R. Schwarzenbacher, D. McMullan, P. Abdubek, E. Ambing, H. Axelrod, T. Biorac, J. M. Canaves, H. J. Chiu, A. M. Deacon, M. DiDonato, M. A. Elsliger, A. Godzik, C. Grittini, S. K. Grzechnik, J. Hale, E. Hampton, G. W. Han, J. Haugen, M. Hornsby, L. Jaroszewski, H. E. Klock, E. Koesema, A. Kreusch, P. Kuhn, S. A. Lesley, M. D. Miller, K. Moy, E. Nigoghossian, J. Paulsen, K. Quijano, R. Reyes, E. Sims, G. Spraggon, R. C. Stevens, H. van den Bedem, J. Velasquez, J. Vincent, A. White, G. Wolf, Q. Xu, K. O. Hodgson, J. Wooley, and I. A. Wilson. 2005. Crystal structure of the global regulatory protein CsrA from Pseudomonas putida at 2.05 Å resolution reveals a new fold. Proteins 61:449-453.
78. Roe, A. J., H. Yull, S. W. Naylor, M. J. Woodward, D. G. Smith, and D. L. Gally. 2003. Heterogeneous surface expression of EspA translocon filaments by Escherichia coli O157:H7 is controlled at the posttranscriptional level. Infect. Immun. 71:5900-5909.
79. Romeo, T. 1998. Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule CsrB. Mol. Microbiol. 29:1321-1330.
80. Romeo, T., M. Gong, M. Y. Liu, and A. M. Brun-Zinkernagel. 1993. Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties. J. Bacteriol. 175:4744-4755.
81. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
82. Sekiya, K., M. Ohishi, T. Ogino, K. Tamano, C. Sasakawa, and A. Abe. 2001. Supermolecular structure of the enteropathogenic Escherichia coli type III secretion system and its direct interaction with the EspA-sheath-like structure. Proc. Natl. Acad. Sci. USA 98:11638-11643.
83. Sharp, F. C., and V. Sperandio. 2007. QseA directly activates transcription of LEE1 in enterohemorrhagic Escherichia coli. Infect. Immun. 75:2432-2440.
84. Simon, R., U. Priefer, and A. Pühler. 1983. A broad host range mobilisation system for in vivo genetic engineering: transposon mutagenesis in gram-negative bacteria. Bio/Technology 1:784-791.
85. Sircili, M. P., M. Walters, L. R. Trabulsi, and V. Sperandio. 2004. Modulation of enteropathogenic Escherichia coli virulence by quorum sensing. Infect. Immun. 72:2329-2337.
86. Sperandio, V., C. C. Li, and J. B. Kaper. 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.
87. Sperandio, V., J. L. Mellies, W. Nguyen, S. Shin, and J. B. Kaper. 1999. Quorum sensing controls expressionof the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc. Natl. Acad. Sci. USA 96:15196-15201.
88. Sperandio, V., A. G. Torres, J. A. Giron, and J. B. Kaper. 2001. Quorum sensing is a global regulatory mechanism in enterohemorrhagic Escherichia coli O157:H7. J. Bacteriol. 183:5187-5197.
89. Sperandio, V., A. G. Torres, B. Jarvis, J. P. Nataro, and J. B. Kaper. 2003. Bacteria-host communication: the language of hormones. Proc. Natl. Acad. Sci. USA 100:8951-8956.
90. Sperandio, V., A. G. Torres, and J. B. Kaper. 2002. Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol. Microbiol. 43:809-821.
91. Suzuki, K., P. Babitzke, S. R. Kushner, and T. Romeo. 2006. Identification of a novel regulatory protein (CsrD) that targets the global regulatory RNAs CsrB and CsrC for degradation by RNase E. Genes Dev. 20:2605-2617.
92. Suzuki, K., X. Wang, T. Weilbacher, A. K. Pernestig, O. Melefors, D. Georgellis, P. Babitzke, and T. Romeo. 2002. Regulatory circuitry of the CsrA/CsrB and BarA/UvrY systems of Escherichia coli. J. Bacteriol. 184:5130-5140.
93. Swimm, A., B. Bommarius, Y. Li, D. Cheng, P. Reeves, M. Sherman, D. Veach, W. Bornmann, and D. Kalman. 2004. Enteropathogenic Escherichia coli use redundant tyrosine kinases to form actin pedestals. Mol. Biol. Cell 15:3520-3529.
94. Umanski, T., I. Rosenshine, and D. Friedberg. 2002. Thermoregulated expression of virulence genes in enteropathogenic Escherichia coli. Microbiology 148:2735-2744.
95. Uzzau, S., N. Figueroa-Bossi, S. Rubino, and L. Bossi. 2001. Epitope tagging of chromosomal genes in Salmonella. Proc. Natl. Acad. Sci. USA 98:15264-15269.
96. Wachter, C., C. Beinke, M. Mattes, and M. A. Schmidt. 1999. Insertion of EspD into epithelial target cell membranes by infecting enteropathogenic Escherichia coli. Mol. Microbiol. 31:1695-1707.
97. Wang, X., A. K. Dubey, K. Suzuki, C. S. Baker, P. Babitzke, and T. Romeo. 2005. CsrA post-transcriptionally represses pgaABCD, responsible for synthesis of a biofilm polysaccharide adhesin of Escherichia coli. Mol. Microbiol. 56:1648-1663.
98. Wei, B. L., A. M. Brun-Zinkernagel, J. W. Simecka, B. M. Pruss, P. Babitzke, and T. Romeo. 2001. Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol. Microbiol. 40:245-256.
99. Weilbacher, T., K. Suzuki, A. K. Dubey, X. Wang, S. Gudapaty, I. Morozov, C. S. Baker, D. Georgellis, P. Babitzke, and T. Romeo. 2003. A novel sRNA component of the carbon storage regulatory system of Escherichia coli. Mol. Microbiol. 48:657-670.
100. Wilson, R. K., R. K. Shaw, S. Daniell, S. Knutton, and G. Frankel. 2001. Role of EscF, a putative needle complex protein, in the type III protein translocation system of enteropathogenic Escherichia coli. Cell. Microbiol. 3:753-762.