The LysR-type transcriptional regulator QseD alters type three secretion in enterohemorrhagic Escherichia coli and motility in K-12 Escherichia coli

Journal of Bacteriology

Volumn 192, Issue 14, 2010, Pages 3699-3712

  Habdas, Benjamin J ^a   Smart, Jennifer ^b   Kaper, James B ^b   Sperandio, Vanessa ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

QUORUM SENSING ESCHERICHIA COLI REGULATOR D; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CONTROLLED STUDY; DNA BINDING; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI K 12; GENE EXPRESSION; GENE LOSS; GENE MUTATION; NONHUMAN; OPERON; PLASMID; PRIORITY JOURNAL; QUORUM SENSING; TRANSCRIPTION REGULATION;

ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI K12; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; QUORUM SENSING; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION, GENETIC;

ENTEROBACTERIACEAE; ESCHERICHIA COLI;

EID: 77954414667     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00382-10     Document Type: Article

References (88)

1. Allen, K. J., D. Lepp, R. C. McKellar, and M. W. Griffiths. 2008. Examination of stress and virulence gene expression in Escherichia coli O157:H7 using targeted microarray analysis. Foodborne Pathog. Dis. 5:437-447.
2. Alto, N. M., A. W. Weflen, M. J. Rardin, D. Yarar, C. S. Lazar, R. Tonikian, A. Koller, S. S. Taylor, C. Boone, S. S. Sidhu, S. L. Schmid, G. A. Hecht, and J. E. Dixon. 2007. The type III effector EspF coordinates membrane trafficking by the spatiotemporal activation of two eukaryotic signaling pathways. J. Cell Biol. 178:1265-1278.
3. Amberg, D. C., D. Burke, J. N. Strathern, and Cold Spring Harbor Laboratory. 2005. Methods in yeast genetics: a Cold Spring Harbor Laboratory course manual, 2005 ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
4. Anderson, G. G., C. C. Goller, S. Justice, S. J. Hultgren, and P. C. Seed. 2010. Polysaccharide capsule and sialic acid-mediated regulation promote biofilm-like intracellular bacterial communities during cystitis. Infect. Immun. 78:963-975.
5. Axler-Diperte, G. L., V. L. Miller, and A. J. Darwin. 2006. YtxR, a conserved LysR-like regulator that induces expression of genes encoding a putative ADP-ribosyltransferase toxin homologue in Yersinia enterocolitica. J. Bacteriol. 188:8033-8043.
6. Baba, T., T. Ara, M. Hasegawa, Y. Takai, Y. Okumura, M. Baba, K. A. Datsenko, M. Tomita, B. L. Wanner, and H. Mori. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006.0008.
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. Barker, C. S., B. M. Pruss, and P. Matsumura. 2004. Increased motility of Escherichia coli by insertion sequence element integration into the regulatory region of the flhD operon. J. Bacteriol. 186:7529-7537.
9. Basineni, S. R., R. Madhugiri, T. Kolmsee, R. Hengge, and G. Klug. 2009. The influence of Hfq and ribonucleases on the stability of the small noncoding RNA OxyS and its target rpoS in E. coli is growth phase dependent. RNA Biol. 6:584-594.
10. 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.
11. Chilcott, G. S., and K. T. Hughes. 2000. Coupling of flagellar gene expression to flagellar assembly in Salmonella enterica serovar typhimurium and Escherichia coli. Microbiol. Mol. Biol. Rev. 64:694-708.
12. Clarke, M. B., D. T. Hughes, C. Zhu, E. C. Boedeker, and V. Sperandio. 2006. The QseC sensor kinase: a bacterial adrenergic receptor. Proc. Natl. Acad. Sci. U. S. A. 103:10420-10425.
13. Clarke, M. B., and V. Sperandio. 2005. Transcriptional regulation of flhDC by QseBC and sigma (FliA) in enterohaemorrhagic Escherichia coli. Mol. Microbiol. 57:1734-1749.
14. 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. U. S. A. 97:6640-6645.
15. Deghmane, A. E., D. Giorgini, M. Larribe, J. M. Alonso, and M. K. Taha. 2002. Down-regulation of pili and capsule of Neisseria meningitidis upon contact with epithelial cells is mediated by CrgA regulatory protein. Mol. Microbiol. 43:1555-1564.
16. 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. U. S. A. 101:3597-3602.
17. De Silva, R. S., G. Kovacikova, W. Lin, R. K. Taylor, K. Skorupski, and F. J. Kull. 2005. Crystal structure of the virulence gene activator AphA from Vibrio cholerae reveals it is a novel member of the winged helix transcription factor superfamily. J. Biol. Chem. 280:13779-13783.
18. Dong, T., and H. E. Schellhorn. 2009. Control of RpoS in global gene expression of Escherichia coli in minimal media. Mol. Genet. Genomics 281:19-33.
19. Donnenberg, M. S., and T. S. Whittam. 2001. Pathogenesis and evolution of virulence in enteropathogenic and enterohemorrhagic Escherichia coli. J. Clin. Invest. 107:539-548.
20. 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.
21. Elliott, S. J., L. A. Wainwright, T. K. McDaniel, K. G. Jarvis, Y. K. Deng, L. C. Lai, B. P. McNamara, M. S. Donnenberg, and J. B. Kaper. 1998. The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69. Mol. Microbiol. 28:1-4.
22. 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.
23. Gibson, K. E., and T. J. Silhavy. 1999. The LysR homolog LrhA promotes RpoS degradation by modulating activity of the response regulator sprE. J. Bacteriol. 181:563-571.
24. Gietz, D., A. St. Jean, R. A. Woods, and R. H. Schiestl. 1992. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20:1425.
25. Griffin, P. M., S. M. Ostroff, R. V. Tauxe, K. D. Greene, J. G. Wells, J. H. Lewis, and P. A. Blake. 1988. Illnesses associated with Escherichia coli O157:H7. Ann. Intern. Med. 109:705-712.
26. 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.
27. Hansen, A. M., and J. B. Kaper. 2009. Hfq affects the expression of the LEE pathogenicity island in enterohaemorrhagic Escherichia coli. Mol. Microbiol. 73:446-465.
28. Honda, N., S. Iyoda, S. Yamamoto, J. Terajima, and H. Watanabe. 2009. LrhA positively controls the expression of the locus of enterocyte effacement genes in enterohemorrhagic Escherichia coli by differential regulation of their master regulators PchA and PchB. Mol. Microbiol. 74:1393-1411.
29. Hughes, D. T., M. B. Clarke, K. Yamamoto, D. A. Rasko, and V. Sperandio. 2009. The QseC adrenergic signaling cascade in Enterohemorrhagic E. coli (EHEC). PLoS Pathog. 5:e1000553.
30. Ieva, R., C. Alaimo, I. Delany, G. Spohn, R. Rappuoli, and V. Scarlato. 2005. CrgA is an inducible LysR-type regulator of Neisseria meningitidis, acting both as a repressor and as an activator of gene transcription. J. Bacteriol. 187:3421-3430. (Pubitemid 40628697)
31. 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.
32. Iyoda, S., and H. Watanabe. 2004. Positive effects of multiple pch genes on expression of the locus of enterocyte effacement genes and adherence of enterohaemorrhagic Escherichia coli O157:H7 to HEp-2 cells. Microbiology 150:2357-2571. (Pubitemid 39117647)
33. Janga, S. C., and E. Perez-Rueda. 2009. Plasticity of transcriptional machinery in bacteria is increased by the repertoire of regulatory families. Comput. Biol. Chem. 33:261-268.
34. Jarvis, K. G., J. A. Giron, A. E. Jerse, T. K. McDaniel, M. S. Donnenberg, and J. B. Kaper. 1995. Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc. Natl. Acad. Sci. U. S. A. 92:7996-8000.
35. Jozic, D., J. T. Kaiser, R. Huber, W. Bode, and K. Maskos. 2003. X-ray structure of isoaspartyl dipeptidase from E.coli: a dinuclear zinc peptidase evolved from amidohydrolases. J. Mol. Biol. 332:243-256.
36. Kaper, J. B., and M. A. Karmali. 2008. The continuing evolution of a bacterial pathogen. Proc. Natl. Acad. Sci. U. S. A. 105:4535-4536.
37. Kendall, M. M., D. A. Rasko, and V. Sperandio. 2007. Global effects of the cell-to-cell signaling molecules autoinducer-2, autoinducer-3, and epinephrine in a luxS mutant of enterohemorrhagic Escherichia coli. Infect. Immun. 75:4875-4884.
38. 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. (Pubitemid 27508240)
39. Kenny, B., S. Ellis, A. D. Leard, J. Warawa, H. Mellor, and M. A. Jepson. 2002. Co-ordinate regulation of distinct host cell signalling pathways by multifunctional enteropathogenic Escherichia coli effector molecules. Mol. Microbiol. 44:1095-1107.
40. 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.
41. Knutton, S., T. Baldwin, P. H. Williams, and A. S. McNeish. 1988. New diagnostic test for enteropathogenic Escherichia coli. Lancet i(8598):1337.
42. Konczy, P., K. Ziebell, M. Mascarenhas, A. Choi, C. Michaud, A. M. Kropinski, T. S. Whittam, M. Wickham, B. Finlay, and M. A. Karmali. 2008. Genomic O island 122, locus for enterocyte effacement, and the evolution of virulent verocytotoxin-producing Escherichia coli. J. Bacteriol. 190:5832-5840.
43. Kovacikova, G., W. Lin, and K. Skorupski. 2004. Vibrio cholerae AphA uses a novel mechanism for virulence gene activation that involves interaction with the LysR-type regulator AphB at the tcpPH promoter. Mol. Microbiol. 53:129-142.
44. Kovacikova, G., and K. Skorupski. 2001. Overlapping binding sites for the virulence gene regulators AphA, AphB and cAMP-CRP at the Vibrio cholerae tcpPH promoter. Mol. Microbiol. 41:393-407.
45. Kovacikova, G., and K. Skorupski. 1999. A Vibrio cholerae LysR homolog, AphB, cooperates with AphA at the tcpPH promoter to activate expression of the ToxR virulence cascade. J. Bacteriol. 181:4250-4256. (Pubitemid 29331382)
46. Lahiri, A., P. Das, and D. Chakravortty. 2008. The LysR-type transcriptional regulator Hrg counteracts phagocyte oxidative burst and imparts survival advantage to Salmonella enterica serovar Typhimurium. Microbiology 154:2837-2846.
47. Lange, R., and R. Hengge-Aronis. 1994. The cellular concentration of the sigma S subunit of RNA polymerase in Escherichia coli is controlled at the levels of transcription, translation, and protein stability. Genes Dev. 8:1600-1612. (Pubitemid 2116932)
48. Lehnen, D., C. Blumer, T. Polen, B. Wackwitz, V. F. Wendisch, and G. Unden. 2002. LrhA as a new transcriptional key regulator of flagella, motility and chemotaxis genes in Escherichia coli. Mol. Microbiol. 45:521-532.
49. Li, H., A. Granat, V. Stewart, and J. R. Gillespie. 2008. RpoS, H-NS, and DsrA influence EHEC hemolysin operon (ehxCABD) transcription in Escherichia coli O157:H7 strain EDL933. FEMS Microbiol. Lett. 285:257-262.
50. Maddocks, S. E., and P. C. Oyston. 2008. Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology 154:3609-3623.
51. McDaniel, T. K., K. G. Jarvis, M. S. Donnenberg, and J. B. Kaper. 1995. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc. Natl. Acad. Sci. U. S. A. 92:1664-1668.
52. 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.
53. Merrikh, H., A. E. Ferrazzoli, A. Bougdour, A. Olivier-Mason, and S. T. Lovett. 2009. A DNA damage response in Escherichia coli involving the alternative sigma factor, RpoS. Proc. Natl. Acad. Sci. U. S. A. 106:611-616.
54. Merrikh, H., A. E. Ferrazzoli, and S. T. Lovett. 2009. Growth phase and (p)ppGpp control of IraD, a regulator of RpoS stability, in Escherichia coli. J. Bacteriol. 191:7436-7446.
55. Nakanishi, N., H. Abe, Y. Ogura, T. Hayashi, K. Tashiro, S. Kuhara, N. Sugimoto, and T. Tobe. 2006. ppGpp with DksA controls gene expression in the locus of enterocyte effacement (LEE) pathogenicity island of enterohaemorrhagic Escherichia coli through activation of two virulence regulatory genes. Mol. Microbiol. 61:194-205.
56. Orth, K., L. E. Palmer, Z. Q. Bao, S. Stewart, A. E. Rudolph, J. B. Bliska, and J. E. Dixon. 1999. Inhibition of the mitogen-activated protein kinase kinase superfamily by a Yersinia effector. Science 285:1920-1923.
57. Peterson, C. N., V. J. Carabetta, T. Chowdhury, and T. J. Silhavy. 2006. LrhA regulates rpoS translation in response to the Rcs phosphorelay system in Escherichia coli. J. Bacteriol. 188:3175-3181.
58. Pratt, L. A., and T. J. Silhavy. 1996. The response regulator SprE controls the stability of RpoS. Proc. Natl. Acad. Sci. U. S. A. 93:2488-2492.
59. Rasko, D. A., M. J. Rosovitz, G. S. Myers, E. F. Mongodin, W. F. Fricke, P. Gajer, J. Crabtree, M. Sebaihia, N. R. Thomson, R. Chaudhuri, I. R. Henderson, V. Sperandio, and J. Ravel. 2008. The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J. Bacteriol. 190:6881-6893.
60. Reading, N. C., D. A. Rasko, A. G. Torres, and V. Sperandio. 2009. The two-component system QseEF and the membrane protein QseG link adrenergic and stress sensing to bacterial pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 106:5889-5894.
61. Reid, S. D., C. J. Herbelin, A. C. Bumbaugh, R. K. Selander, and T. S. Whittam. 2000. Parallel evolution of virulence in pathogenic Escherichia coli. Nature 406:64-67.
62. Rogers, M. F., L. D. Budnick, I. Kirson, E. S. Hurwitz, M. H. Hatch, C. A. Bopp, M. A. Karmali, G. W. Gary, R. Layne, and L. B. Schonberger. 1986. Hemolytic-uremic syndrome - an outbreak in Sacramento, California. West J. Med. 144:169-173.
63. Russell, R. M., F. C. Sharp, D. A. Rasko, and V. Sperandio. 2007. QseA and GrlR/GrlA regulation of the locus of enterocyte effacement genes in enterohemorrhagic Escherichia coli. J. Bacteriol. 189:5387-5392.
64. Sainsbury, D. C., G. Kessell, A. Guhan, A. Fall, V. Miller, M. R. Abouzeid, and T. Muir. 2009. Unexpected hyperpigmentation following intralesional bleomycin injection. J. Plast. Reconstr. Aesthet. Surg. 62:e497-e499.
65. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
66. Sánchez-SanMartín, C., V. H. Bustamante, E. Calva, and J. L. Puente. 2001. Transcriptional regulation of the orf19 gene and the tir-cesT-eae operon of enteropathogenic Escherichia coli. J. Bacteriol. 183:2823-2833.
67. Schell, M. A. 1993. Molecular biology of the LysR family of transcriptional regulators. Annu. Rev. Microbiol. 47:597-626.
68. Shakhnovich, E. A., B. M. Davis, and M. K. Waldor. 2009. Hfq negatively regulates type III secretion in EHEC and several other pathogens. Mol. Microbiol. 74:347-363.
69. Sharma, V. K., and R. L. Zuerner. 2004. Role of hha and ler in transcriptional regulation of the esp operon of enterohemorrhagic Escherichia coli O157:H7. J. Bacteriol. 186:7290-7301.
70. Sharp, F. C., and V. Sperandio. 2007. QseA directly activates transcription of LEE1 in enterohemorrhagic Escherichia coli. Infect. Immun. 75:2432-2440.
71. 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.
72. Sperandio, V., J. L. Mellies, R. M. Delahay, G. Frankel, J. A. Crawford, W. Nguyen, and J. B. Kaper. 2000. Activation of enteropathogenic Escherichia coli (EPEC) LEE2 and LEE3 operons by Ler. Mol. Microbiol. 38:781-793.
73. Sperandio, V., J. L. Mellies, W. Nguyen, S. Shin, and J. B. Kaper. 1999. Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 96:15196-15201.
74. 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.
75. 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. U. S. A. 100:8951-8956.
76. 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.
77. Surette, M. G., and B. L. Bassler. 1998. Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc. Natl. Acad. Sci. U. S. A. 95:7046-7050.
78. Surette, M. G., M. B. Miller, and B. L. Bassler. 1999. Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. Proc. Natl. Acad. Sci. U. S. A. 96:1639-1644.
79. Tu, X., T. Latifi, A. Bougdour, S. Gottesman, and E. A. Groisman. 2006. The PhoP/PhoQ two-component system stabilizes the alternative sigma factor RpoS in Salmonella enterica. Proc. Natl. Acad. Sci. U. S. A. 103:13503-13508.
80. Tu, X., I. Nisan, C. Yona, E. Hanski, and I. Rosenshine. 2003. EspH, a new cytoskeleton-modulating effector of enterohaemorrhagic and enteropathogenic Escherichia coli. Mol. Microbiol. 47:595-606.
81. Umanski, T., I. Rosenshine, and D. Friedberg. 2002. Thermoregulated expression of virulence genes in enteropathogenic Escherichia coli. Microbiology 148:2735-2744.
82. Vojtek, A. B., and S. M. Hollenberg. 1995. Ras-Raf interaction: two-hybrid analysis. Methods Enzymol. 255:331-342.
83. Wales, A. D., M. J. Woodward, and G. R. Pearson. 2005. Attaching-effacing bacteria in animals. J. Comp. Pathol. 132:1-26.
84. Walters, M., M. P. Sircili, and V. Sperandio. 2006. AI-3 synthesis is not dependent on luxS in Escherichia coli. J. Bacteriol. 188:5668-5681.
85. Walters, M., and V. Sperandio. 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.
86. Wang, Y., M. Rawlings, D. T. Gibson, D. Labbe, H. Bergeron, R. Brousseau, and P. C. Lau. 1995. Identification of a membrane protein and a truncated LysR-type regulator associated with the toluene degradation pathway in Pseudomonas putida F1. Mol. Gen. Genet. 246:570-579.
87. Yang, H., E. Wolff, M. Kim, A. Diep, and J. H. Miller. 2004. Identification of mutator genes and mutational pathways in Escherichia coli using a multicopy cloning approach. Mol. Microbiol. 53:283-295.
88. Zhang, L., R. R. Chaudhuri, C. Constantinidou, J. L. Hobman, M. D. Patel, A. C. Jones, D. Sarti, A. J. Roe, I. Vlisidou, R. K. Shaw, F. Falciani, M. P. Stevens, D. L. Gally, S. Knutton, G. Frankel, C. W. Penn, and M. J. Pallen. 2004. Regulators encoded in the Escherichia coli type III secretion system 2 gene cluster influence expression of genes within the locus for enterocyte effacement in enterohemorrhagic E. coli O157:H7. Infect. Immun. 72:7282-7293.