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Chapter 12 : Toxin and Virulence Regulation in

Authors: Karen Skorupski1, Ronald K. Taylor1
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Affiliations: 1: Department of Microbiology and Immunology, Dartmouth Medical School, Hanover, NH 03755
Content Type: Monograph
Publication Year: 2013

Category: Bacterial Pathogenesis

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Abstract:

Of the more than 200 different serogroups of that have been isolated, only two of these, O1 and O139, have been found to have epidemic and pandemic potential. CTXφ carries the genes for CT () and the VPI contains the genes () responsible for the synthesis and assembly of the essential colonization factor toxin-coregulated pilus (TCP). As part of the acetoin operon, AphA represses the expression of two PhoB-activated genes, and , that encode proteins which influence motility and biofilm formation by altering c-di-GMP levels in the cell. Bicarbonate may be an important in vivo signal that increases the activity of ToxT during infection and induces virulence gene expression. Once has disseminated out of the host and virulence gene expression is no longer required, TcpP and ToxT levels are decreased by proteolysis and H-NS reestablishes repression at the various promoters. Thus, like GbpA, FrhA plays an important role in in both the host and in the aquatic environment. A model for infection involves motile bacteria attaching to the intestinal cell surface, after which they upregulate virulence factor expression and downregulate motility. The flagellar regulatory hierarchy also influences virulence gene expression in through the quorum sensing system. Recent advances in the development of cDNA sequencing (RNA-seq) have facilitated the generation of comprehensive transcriptome profiles of during infection in both the rabbit and mouse models of cholera.

Citation: Skorupski K, Taylor R. 2013. Toxin and Virulence Regulation in , p 241-261. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch12
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Toxin and Virulence Regulation in Vibrio cholerae
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Citation: Skorupski K, Taylor R. 2013. Toxin and Virulence Regulation in , p 241-261. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch12
/content/10.1128/9781555818524.chap12.fig12-1
Figure 1

The virulence cascade. The VPI is shown by a blue line, CTXΦ by a red line, and the ancestral genome by black lines. At low cell density, in the absence of CAI-1 and AI-2, CqsS and LuxPQ phosphorylate LuxO, which, together with σ, activates the expression of to . The resulting small RNAs, together with Hfq, destabilize the message, leading to activation of expression by Lrp and VpsR. AphA cooperates with AphB to activate the promoter. TcpPH cooperates with ToxRS to activate the promoter. ToxT then activates the and promoters. At low cell density, AphA also represses the expression of to - and . At high cell density, in the presence of CAI-1 and AI-2, LuxO is not phosphorylated and to are not expressed. This allows for the accumulation of HapR, which binds to a site in the promoter overlapping the VpsR binding site, repressing its expression and turning off the virulence cascade. doi:10.1128/9781555818524.ch12f1

10.1128/9781555818524/fig12-1_thmb.gif
10.1128/9781555818524/fig12-1.gif
Image of Figure 1
Figure 1

The virulence cascade. The VPI is shown by a blue line, CTXΦ by a red line, and the ancestral genome by black lines. At low cell density, in the absence of CAI-1 and AI-2, CqsS and LuxPQ phosphorylate LuxO, which, together with σ, activates the expression of to . The resulting small RNAs, together with Hfq, destabilize the message, leading to activation of expression by Lrp and VpsR. AphA cooperates with AphB to activate the promoter. TcpPH cooperates with ToxRS to activate the promoter. ToxT then activates the and promoters. At low cell density, AphA also represses the expression of to - and . At high cell density, in the presence of CAI-1 and AI-2, LuxO is not phosphorylated and to are not expressed. This allows for the accumulation of HapR, which binds to a site in the promoter overlapping the VpsR binding site, repressing its expression and turning off the virulence cascade. doi:10.1128/9781555818524.ch12f1

Citation: Skorupski K, Taylor R. 2013. Toxin and Virulence Regulation in , p 241-261. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch12
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References

/content/book/10.1128/9781555818524.chap12
1. Abuaita, B. H.,, and J. H. Withey. 2009. Bicarbonate induces Vibrio cholerae virulence gene expression by enhancing ToxT activity. Infect. Immun. 77: 4111– 4120.
2. Abuaita, B. H.,, and J. H. Withey. 2011. Termination of Vibrio cholerae virulence gene expression is mediated by proteolysis of the major virulence activator, ToxT. Mol. Microbiol. 81: 1640– 1653.
3. Alam, A.,, R. C. LaRocque,, J. B. Harris,, C. Vanderspurt,, E. T. Ryan,, F. Qadri,, and S. B. Calderwood. 2005. Hyperinfectivity of human-passaged Vibrio cholerae can be modeled by growth in the infant mouse. Infect. Immun. 73: 6674– 6679.
4. Alekshun, M. N.,, S. B. Levy,, T. R. Mealy,, B. A. Seaton,, and J. F. Head. 2001. The crystal structure ofMarR, a regulator of multiple antibiotic resistance, at 2.3 Å resolution. Nat. Struct. Biol. 8: 710– 714.
5. Atlung, T.,, and H. Ingmer. 1997. H-NS: a modulator of environmentally regulated gene expression. Mol. Microbiol. 24: 7– 17.
6. Barthelmebs, L.,, B. Lecomte,, C. Divies,, and J.-F. Cavin. 2000. Inducible metabolism of phenolic acids in Pediococcus pentosaceus is encoded by an autoregulated operon which involves a new class of negative transcriptional regulator. J. Bacteriol. 182: 6724– 6731.
7. Beck, N. A.,, E. S. Krukonis,, and V. J. DiRita. 2004. TcpH influences virulence gene expression in Vibrio cholerae by inhibiting the degradation of the transcription activator TcpP. J. Bacteriol. 186: 8309– 8316.
8. Bellair, M.,, and J. H. Withey. 2008. Flexibility of Vibrio cholerae ToxT in transcription activation of genes having altered promoter spacing. J. Bacteriol. 190: 7925– 7931.
9. Beyhan, S.,, A. D. Tischler,, A. Camilli,, and F. H. Yildiz. 2006. Differences in gene expression between the classical and El Torbiotypes of Vibrio cholerae O1. Infect. Immun. 74: 3633– 3642.
10. Bina, J.,, Z. Zhu,, M. Dziejman,, S. Faruque,, S. Calderwood,, and J. J. Mekalanos. 2003. ToxR regulon of Vibrio cholerae and its expression in vibrios shed by cholera patients. Proc. Natl. Acad. Sci. USA 100: 2801– 2806.
11. Bradley, E. S.,, K. Bodi,, A. M. Ismail,, and A. Camilli. 2011. A genome-wide approach to discovery of small RNAs involved in regulation of virulence in Vibrio cholerae. PLoS Pathog. 7: e1002126.
12. Brinkman, A. B.,, T. J. G. Ettema,, W. M. deVos,, and J. van der Oost. 2003. The Lrp family of transcriptional regulators. Mol. Microbiol. 48: 287– 294.
13. Brown, R. C.,, and R. K. Taylor. 1995. Organization of tcp, acf, and toxT genes within a ToxT-dependent operon. Mol. Microbiol. 16: 425– 439.
14. Butler, S. M.,, and A. Camilli. 2004. Both chemotaxis and net motility greatly influence the infectivity of Vibrio cholerae. Proc. Natl. Acad. Sci. USA 101: 5018– 5023.
15. Butler, S. M.,, and A. Camilli. 2005. Going against the grain: chemotaxis and infection in Vibrio cholerae. Nat. Rev. Microbiol. 3: 611– 620.
16. Butler, S. M.,, E. J. Nelson,, N. Chowdhury,, S. M. Faruque,, S. B. Calderwood,, and A. Camilli. 2006. Cholera stool bacteria repress chemotaxis to increase infectivity. Mol. Microbiol. 60: 417– 426.
17. Calvo, J. M.,, and R. G. Matthews. 1994. The leucine-responsive regulatory protein, a global regulator of metabolism in Escherichia coli. Microbiol. Rev. 58: 466– 490.
18. Carroll, P. A.,, K. T. Tashima,, M. B. Rogers,, V. J. DiRita,, and S. B. Calderwood. 1997. Phase variation in tcpH modulates expression of the ToxR regulon in Vibrio cholerae. Mol. Microbiol. 25: 1099– 1111.
19. Casper-Lindley, C.,, and F. H. Yildiz. 2004. VpsT is a transcriptional regulator required for expression of vps biosynthesis genes and the development of rugose colonial morphology in Vibrio cholerae O1 El Tor. J. Bacteriol. 186: 1574– 1578.
20. Cerda-Maira, F. A.,, C. S. Ringelberg,, and R. K. Taylor. 2008. The bile response repressor BreR regulates expression of the Vibrio cholerae breAB efflux system operon. J. Bacteriol. 190: 7441– 7452.
21. Champion, G. A.,, M. N. Neely,, M. A. Brennan,, and V. J. DiRita. 1997. A branch in the ToxR regulatory cascade of Vibrio cholerae revealed by characterization of toxT mutant strains. Mol. Microbiol. 23: 323– 331.
22. Chaparro, A. P.,, S. K. Ali,, and K. E. Klose. 2010. The ToxT-dependent methyl-accepting chemoreceptors AcfB and TcpI contribute to Vibrio cholerae intestinal colonization. FEMS Microbiol. Lett. 302: 99– 105.
23. Chatterjee, A.,, P. K. Dutta,, and R. Chowdhury. 2007. Effect of fatty acids and cholesterol present in bile on expression of virulence factors and motility of Vibrio cholerae. Infect. Immun. 75: 1946– 1953.
24. Childers, B. M.,, X. Cao,, G. G. Weber,, B. Demeler,, P. J. Hart,, and K. E. Klose. 2011. N-terminal residues of the Vibrio cholerae virulence regulatory protein ToxT involved in dimerization and modulation by fatty acids. J. Biol. Chem. 286: 28644– 28655.
25. Correa, N. E.,, J. R. Barker,, and K. E. Klose. 2004. The Vibrio cholerae FlgM homologue is an anti-s 28 factor that is secreted through the sheathed polar flagellum. J. Bacteriol. 186: 4613– 4619.
26. Correa, N. E.,, C. M. Lauriano,, R. McGee,, and K. E. Klose. 2000. Phosphorylation of the flagellar regulatory protein FlrC is necessary for Vibrio cholerae motility and enhanced colonization. Mol. Microbiol. 35: 743– 755.
27. Craig, L.,, R. K. Taylor,, M. E. Pique,, B. D. Adair,, A. S. Arvai,, M. Singh,, S. J. Lloyd,, D. S. Shin,, E. D. Getzoff,, M. Yeager,, K. T. Forest,, and J. A. Tainer. 2003. Type IV pilin structure and assembly: X-ray and EM analyses of Vibrio cholerae toxin-coregulated pilus and Pseudomonas aeruginosa PAK pilin. Mol. Cell 11: 1139– 1150.
28. Crawford, J. A.,, J. B. Kaper,, and V. J. DiRita. 1998. Analysis of ToxR-dependent transcription activation of ompU, the gene encoding a major envelope protein in Vibrio cholerae. Mol. Microbiol. 29: 235– 256.
29. Crawford, J. A.,, E. S. Krukonis,, and V. J. DiRita. 2003. Membrane localization of the ToxR winged-helix domain is required for TcpP-mediated virulence gene activation in Vibrio cholerae. Mol. Microbiol. 47: 1459– 1473.
30. 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.
31. De Silva, R. S.,, G. Kovacikova,, W. Lin,, R. K. Taylor,, K. Skorupski,, and F. J. Kull. 2007. Crystal structure of the Vibrio cholerae quorum-sensing regulatory protein HapR. J. Bacteriol. 189: 5683– 5691.
32. Deutscher, J.,, C. Francke,, and P. W. Postma. 2006. How phosphotransferase system-related protein phosphorylation regulates carbon metabolism in bacteria. Microbiol. Mol. Biol. Rev. 70: 939– 1031.
33. Ding, Y.,, and M. K. Waldor. 2003. Deletion of a Vibrio cholerae ClC channel results in acid sensitivity and enhanced intestinal colonization. Infect. Immun. 71: 4197– 4200.
34. DiRita, V. J.,, and J. J. Mekalanos. 1991. Periplasmic interaction between two membrane regulatory proteins, ToxR and ToxS, results in signal transduction and transcriptional activation. Cell 64: 29– 37.
35. DiRita, V. J.,, C. Parsot,, G. Jander,, and J. J. Mekalanos. 1991. Regulatory cascade controls virulence in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 88: 5403– 5407.
36. DiRita, V. J.,, M. Neely,, R. K. Taylor,, and P. M. Bruss. 1996. Differential expression of the ToxR regulon in classical and El Tor biotypes of V. cholerae is due to biotype-specific control over toxT expression. Proc. Natl. Acad. Sci. USA 93: 7991– 7995.
37. Dorman, C. J. 2007. H-NS, the genome sentinel. Nat. Rev. Microbiol. 5: 157– 161.
38. Dutzler, R. 2006. The ClC family of chloride channels and transporters. Curr. Opin. Struct. Biol. 16: 439– 446.
39. Dziejman, M.,, and J. J. Mekalanos. 1994. Analysis of membrane protein interaction: ToxR can dimerize the amino terminus of phage lambda repressor. Mol. Microbiol. 13: 485– 494.
40. Fang, F. C.,, and S. Rimsky. 2008. New insights into transcriptional regulation by H-NS. Curr. Opin. Microbiol. 11: 113– 120.
41. Faruque, S. M.,, M. J. Albert,, and J. J. Mekalanos. 1998. Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae. Microbiol. Mol. Biol. Rev. 62: 1301– 1314.
42. Faruque, S. M.,, K. Biswas,, S. M. N. Udden,, Q. S. Ahmad,, D. A. Sack,, G. B. Nair,, and J. J. Mekalanos. 2006. Transmissibility of cholera: in vivo-formed biofilms and their relationship to infectivity and persistence in the environment. Proc. Natl. Acad. Sci. USA 103: 6350– 6355.
43. Finkelstein, R. A.,, M. Boesman-Finkelstein,, Y. Chang,, and C. C. Häse. 1992. Vibrio cholerae hemagglutinin/protease, colonial variation, virulence, and detachment. Infect. Immun. 60: 472– 478.
44. Finkelstein, R. A.,, M. Boesman-Finkelstein,, and P. Holt. 1983. Vibrio cholerae hemagglutinin/lectin/protease hydrolyzes fibronectin and ovomucin: F. M. Burnet revisited. Proc. Natl. Acad. Sci. USA 80: 1092– 1095.
45. Finne, J.,, M. E. Breimer,, G. C. Hansson,, K.-A. Karlsson,, H. Leffler,, J. F. G. Vliegenthart,, and H. van Halbeek. 1989. Novel polyfucosylated N-linked glycopeptides with blood group A, H, X, and Y determinants from human small intestinal epithelial cells. J.Biol. Chem. 264: 5720– 5735.
46. Fong, J. C. N.,, and F. H. Yildiz. 2008. Interplay between cyclic AMP-cyclic AMP receptor protein and cyclic di-GMP signaling in Vibrio cholerae biofilm formation. J. Bacteriol. 190: 6646– 6659.
47. Fong, J. C. N.,, K. A. Syed,, K. E. Klose,, and F. H. Yildiz. 2010. Role of Vibrio polysaccharide ( vps) genes in VPS production, biofilm formation and Vibrio cholerae pathogenesis. Microbiology 156: 2757– 2769.
48. Gallegos, M.-T.,, R. Schleif,, A. Bairoch,, K. Hofmann,, and J. L. Ramos. 1997. AraC/XylS family of transcriptional regulators. Microbiol. Mol. Biol. Rev. 61: 393– 410.
49. Galperin, M. Y.,, A. N. Nikolskaya,, and E. V. Koonin. 2001. Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol. Lett. 203: 11– 21.
50. Gardel, C. L.,, and J. J. Mekalanos. 1996. Alterations in Vibrio cholerae motility phenotypes correlate with changes in virulence factor expression. Infect. Immun. 64: 2246– 2255.
51. Goosen, N.,, and P. van de Putte. 1995. The regulation of transcription initiation by integration host factor. Mol. Microbiol. 16: 1– 7.
52. Goss, T. J.,, C. P. Seaborn,, M. D. Gray,, and E. S. Krukonis. 2010. Identification of the TcpP binding site in the toxT promoter of Vibrio cholerae and the role of ToxR in TcpP-mediated activation. Infect. Immun. 78: 4122– 4133.
53. Gunn, J. S. 2000. Mechanisms of bacterial resistance and response to bile. Microbes Infect. 2: 907– 913.
54. Gupta, S.,, and R. Chowdhury. 1997. Bile affects production of virulence factors and motility of Vibrio cholerae. Infect. Immun. 65: 1131– 1134.
55. Hammer, B. K.,, and B. L. Bassler. 2003. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol. Microbiol. 50: 101– 114.
56. Häse, C. C. 2001. Analysis of the role of flagellar activity in virulence gene expression in Vibrio cholerae. Microbiology 147: 831– 837.
57. Häse, C. C.,, and B. Barquera. 2001. Role of sodium bioenergetics in Vibrio cholerae. Biochem. Biophys. Acta 1505: 169– 178.
58. Häse, C. C.,, and J. J. Mekalanos. 1998. TcpP protein is a positive regulator of virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 95: 730– 734.
59. Häse, C. C.,, and J. J. Mekalanos. 1999. Effects of changes in membrane sodium flux on virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 96: 3183– 3187.
60. Hengge, R. 2009. Principles of c-di-GMP signalling in bacteria. Nat. Rev. Microbiol. 7: 263– 273.
61. Herrington, D. A.,, R. H. Hall,, G. Losonsky,, J. J. Mekalanos,, R. K. Taylor,, and M. M. Levine. 1988. Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae colonization in humans J. Exp. Med. 168: 1487– 1492.
62. Herz, K.,, S. Vimont,, E. Padan,, and P. Berche. 2003. Roles of NhaA, NhaB, and NhaD Na +/H + antiporters in survival of Vibrio cholerae in a saline environment. J. Bacteriol. 185: 1236– 1244.
63. Higgins, D. E.,, and V. J. DiRita. 1994. Transcriptional control of toxT, a regulatory gene in the ToxR regulon of Vibrio cholerae. Mol. Microbiol. 14: 17– 29.
64. Higgins, D. E.,, E. Nazareno,, and V. J. DiRita. 1992. The virulence gene activator ToxT from Vibrio cholerae is a member of the AraC family of transcriptional activators. J. Bacteriol. 174: 6974– 6980.
65. Hsiao, A.,, Z. Liu,, A. Joelsson,, and J. Zhu. 2006. Vibrio cholerae virulence regulator-coordinated evasion of host immunity. Proc. Natl. Acad. Sci. USA 103: 14542– 14547.
66. Hsiao, A.,, X. Xu,, B. Kan,, R. V. Kulkarni,, and J. Zhu. 2009. Direct regulation by the Vibrio cholerae regulator ToxT to modulate colonization and anticolonization pilus expression. Infect. Immun. 77: 1383– 1388.
67. Hsieh, Y.-J.,, and B. L. Wanner. 2010. Global regulation by the seven-component P i signaling system. Curr. Opin. Microbiol. 13: 198– 203.
68. Hulbert, R. R.,, and R. K. Taylor. 2002. Mechanism of ToxT-dependent transcriptional activation at the Vibrio cholerae tcpA promoter. J. Bacteriol. 184: 5533– 5544.
69. Hung, D. T.,, J. Zhu,, D. Sturtevant,, and J. J. Mekalanos. 2006. Bile acids stimulate biofilm formation in Vibrio cholerae. Mol. Microbiol. 59: 193– 201.
70. Iwanaga, M.,, K. Yamamoto,, N. Higa,, Y. Ichinose,, N. Nakasone,, and M. Tanabe. 1986. Culture conditions for stimulating cholera toxin production by Vibrio cholerae O1 El Tor. Microbiol. Immunol. 30: 1075– 1083.
71. Jobling, M. G.,, and R. K. Holmes. 1997. Characterization of hapR, a positive regulator of the Vibrio cholerae HA/protease gene hap, and its identification as a functional homologue of the Vibrio harveyi luxR gene. Mol. Microbiol. 26: 1023– 1034.
72. Jude, B. A.,, R. M. Martinez,, K. Skorupski,, and R. K. Taylor. 2009. Levels of the secreted Vibrio cholerae attachment factor GbpA are modulated by quorum-sensing-induced proteolysis. J.Bacteriol. 191: 6911– 6917.
73. Jude, B. A.,, and R. K. Taylor. 2011. The physical basis of type 4 pilus-mediated microcolony formation by Vibrio cholerae O1. J.Struct. Biol. 175: 1– 9.
74. Kamruzzaman, M.,, S. M. N. Udden,, D. E. Cameron,, S. B. Calderwood,, G. B. Nair,, J. J. Mekalanos,, and S. M. Faruque. 2010. Quorum-regulated biofilms enhance the development of conditionally viable, environmental Vibrio cholerae. Proc. Natl. Acad. Sci. USA 107: 1588– 1593.
75. Kanjilal, S.,, R. Citorik,, R. C. LaRocque,, M. F. Ramoni,, and S. B. Calderwood. 2010. A systems biology approach to modeling Vibrio cholerae gene expression under virulence-inducing conditions. J. Bacteriol. 192: 4300– 4310.
76. Kaper, J. B.,, J. G. Morris, Jr.,, and M. M. Levine. 1995. Cholera. Clin. Microbiol. Rev. 8: 48– 86.
77. Karaolis, D. K. R.,, J. A. Johnson,, C. C. Bailey,, E. C. Boedeker,, J. Kaper,, and P. R. Reeves. 1998. A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proc. Natl. Acad. Sci. USA 95: 3134– 3139.
78. Kirn, T. J.,, N. Bose,, and R. K. Taylor. 2003. Secretion of a soluble colonization factor by the TCP type 4 pilus biogenesis pathway for V. cholerae. Mol. Microbiol. 49: 81– 92.
79. Kirn, T. J.,, B. A. Jude,, and R. K. Taylor. 2005. A colonization factor links Vibrio cholerae environmental survival and human infection. Nature 438: 863– 866.
80. Kirn, T.J.,, M. J. Lafferty,, C. M. P. Sandoe,, and R. K. Taylor. 2000. Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. Mol. Microbiol. 35: 896– 910.
81. Klose, K. E.,, and J. J. Mekalanos. 1998. Distinct roles of an alternative sigma factor during both free-swimming and colonizing phases of the Vibrio cholerae pathogenic cycle. Mol. Microbiol. 28: 501– 520.
82. Kolb, A.,, S. Busby,, H. Buc,, S. Garges,, and S. Adhya. 1993. Transcriptional regulation by cAMP and its receptor protein. Annu. Rev. Biochem. 62: 749– 795.
83. 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.
84. Kovacikova, G.,, and K. Skorupski. 2000. Differential activation of the tcpPH promoter by AphB determines biotype specificity of virulence gene expression in Vibrio cholerae. J. Bacteriol. 182: 3228– 3238.
85. 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.
86. Kovacikova, G.,, and K. Skorupski. 2002a. Binding site requirements of the virulence gene regulator AphB: differential affinities for the Vibrio cholerae classical and El Tor tcpPH promoters. Mol. Microbiol. 44: 533– 547.
87. Kovacikova, G.,, and K. Skorupski. 2002b. Regulation of virulence gene expression in Vibrio cholerae by quorum sensing: HapR functions at the aphA promoter. Mol. Microbiol. 46: 1135– 1147.
88. Kovacikova, G.,, W. Lin,, and K. Skorupski. 2003. The virulence activator AphA links quorum sensing to pathogenesis and physiology in Vibrio cholerae by repressing the expression of a penicillin amidase gene on the small chromosome. J. Bacteriol. 185: 4825– 4836.
89. 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.
90. Kovacikova, G.,, W. Lin,, and K. Skorupski. 2005. Dual regulation of genes involved in acetoin biosynthesis and motility/biofilm formation by the virulence activator AphA and the acetate-responsive LysR-type regulator AlsR in Vibrio cholerae. Mol. Microbiol. 57: 420– 433.
91. Kovacikova, G.,, W. Lin,, and K. Skorupski. 2010. The LysR-type virulence activator AphB regulates the expression of genes in Vibrio cholerae in response to low pH and anaerobiosis. J. Bacteriol. 192: 4181– 4191.
92. Krasteva, P. V.,, J. C. N. Fong,, N. J. Shikuma,, S. Beyhan,, M. V. A. S. Navarro,, F. H. Yildiz,, and H. Sondermann. 2010. Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327: 866– 868.
93. Krukonis, E. S.,, R. R. Yu,, and V. J. DiRita. 2000. The Vibrio cholerae ToxR/TcpP/ToxT virulence cascade: distinct roles for two membrane-localized transcriptional activators on a single promoter. Mol. Microbiol. 38: 67– 84.
94. Krukonis, E. S.,, and V. J. DiRita. 2003. DNA binding and ToxR responsiveness by the wing domain of TcpP, an activator of virulence gene expression in Vibrio cholerae. Mol. Cell 12: 157– 165.
95. LaRocque, R. C.,, J. B. Harris,, M. Dziejman,, X. Li,, A. I. Khan,, A. S. G. Faruque,, S. M. Faruque,, G. B. Nair,, E. T. Ryan,, F. Qadri,, J. J. Mekalanos,, and S. B. Calderwood. 2005. Transcriptional profiling of Vibrio cholerae recovered directly from patient specimens during early and late stages of human infection. Infect. Immun. 73: 4488– 4493.
96. Lee, S. H.,, D. L. Hava,, M. K. Waldor,, and A. Camilli. 1999. Regulation and temporal expression patterns of Vibrio cholerae virulence genes during infection. Cell 99: 625– 634.
97. Lee, S. H.,, S. M. Butler,, and A. Camilli. 2001. Selection for in vivo regulators of bacterial virulence. Proc. Natl. Acad. Sci. USA 98: 6889– 6894.
98. Lenz, D. H.,, K. C. Mok,, B. N. Lilley,, R. V. Kulkarni,, N. S. Wingreen,, and B. L. Bassler. 2004. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118: 69– 82.
99. Li, C. C.,, J. A. Crawford,, V. J. DiRita,, and J. B. Kaper. 2000. Molecular cloning and transcriptional regulation of ompT, a ToxR-repressed gene in Vibrio cholerae. Mol. Microbiol. 35: 189– 203.
100. Li, C. C.,, D. S. Merrell,, A. Camilli,, and J. B. Kaper. 2002. ToxR interferes with CRP-dependent transcriptional activation of ompT in Vibrio cholerae. Mol. Microbiol. 43: 1577– 1589.
101. Lin, W.,, G. Kovacikova,, and K. Skorupski. 2005. Requirements for Vibrio cholerae HapR binding and transcriptional repression at the hapR promoter are distinct from those at the aphA promoter. J. Bacteriol. 187: 3013– 3019.
102. Lin, W.,, G. Kovacikova,, and K. Skorupski. 2007. The quorum sensing regulator HapR downregulates the expression of the virulence gene transcription factor AphA in Vibrio cholerae by antagonizing Lrp- and VpsR-mediated activation. Mol. Microbiol. 64: 953– 967.
103. Liu, X.,, S. Beyhan,, B. Lim,, R. G. Linington,, and F. H. Yildiz. 2010. Identification and characterization of a phosphodiesterase that inversely regulates motility and biofilm formation in Vibrio cholerae. J. Bacteriol. 192: 4541– 4552.
104. Liu, Z.,, T. Miyashiro,, A. Tsou,, A. Hsiao,, M. Goulian,, and J. Zhu. 2008. Mucosal penetration primes Vibrio cholerae for host colonization by repressing quorum sensing. Proc. Natl. Acad. Sci. USA 105: 9769– 9774.
105. Liu, Z.,, M. Yang,, G. L. Peterfreund,, A. M. Tsou,, N. Selamoglu,, F. Daldal,, Z. Zhong,, B. Kan,, and J. Zhu. 2011. Vibrio cholerae anaerobic induction of virulence gene expression is controlled by thiol-based switches of virulence regulator AphB. Proc. Natl. Acad. Sci. USA 108: 810– 815.
106. Lowden, M. J.,, K. Skorupski,, M. Pellegrini,, M. G. Chiorazzo,, R. K. Taylor,, and J. F. Kull. 2010. Structure of Vibrio cholerae ToxT reveals a mechanism for fatty acid regulation of virulence genes. Proc. Natl. Acad. Sci. USA 107: 2860– 2865.
107. Maddocks, S. E.,, and P. C. F. Oyston. 2008. Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology 154: 3609– 3623.
108. Makinoshima, H.,, and M. S. Glickman. 2006. Site-2 proteases in prokaryotes: regulated intramembrane proteolysis expands to microbial pathogenesis. Microbes Infect. 8: 1882– 1888.
109. Mandlik, A.,, J. Livny,, W. P. Robins,, J. M. Ritchie,, J. J. Mekalanos,, and M. K. Waldor. 2011. RNA-seq-based monitoring of infection-linked changes in Vibrio cholerae gene expression. Cell Host Microbe 10: 165– 174.
110. Marcus, E. A.,, A. P. Moshfegh,, G. Sachs,, and D. R. Scott. 2005. The periplasmic –-carbonic anhydrase activity of Helicobacter pylori is essential for acid acclimation. J. Bacteriol. 187: 729– 738.
111. Martinez, R. M.,, M. N. Dharmasena,, T. J. Kirn,, and R. K. Taylor. 2009. Characterization of two outer membrane proteins, FlgO and FlgP, that influence Vibrio cholerae motility. J. Bacteriol. 191: 5669– 5679.
112. Martinez-Hackert, E.,, and A. M. Stock. 1997. The DNA-binding domain of OmpR: crystal structures of a winged helix transcription factor. Structure 5: 109– 124.
113. Martinez-Wilson, H. F.,, R. Tamayo,, A. D. Tischler,, D. W. Lazinski,, and A. Camilli. 2008. The Vibrio cholerae hybrid sensor kinase VieS contributes to motility and biofilm regulation by altering the cyclic diguanylate level. J. Bacteriol. 190: 6439– 6447.
114. Mathur, J.,, and M. K. Waldor. 2004. The Vibrio cholerae ToxR-regulated porin OmpU confers resistance to antimicrobial peptides. Infect. Immun. 72: 3577– 3583.
115. Mathur, J.,, B. M. Davis,, and M. K. Waldor. 2007. Antimicrobial peptides activate the Vibrio cholerae σ E regulon through an OmpU-dependent signalling pathway. Mol. Microbiol. 63: 848– 858.
116. Matson, J. S.,, and V. J. DiRita. 2005. Degradation of the membrane-localized virulence activator TcpP by the YaeL protease in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 102: 16403– 16408.
117. McCarter, L. L. 2001. Polar flagellar motility of Vibrionaceae. Microbiol. Mol. Biol. Rev. 65: 445– 462.
118. Megli, C. J.,, A. S. W. Yuen,, S. Kolappan,, M. R. Richardson,, M. N. Dharmasena,, S. J. Krebs,, R. K. Taylor,, and L. Craig. 2011. Crystal structure of the Vibrio cholerae colonization factor TcpF and identification of a functional immunogenic site. J. Mol. Biol 409: 146– 158.
119. Meibom, K. L.,, X. B. Li,, A. T. Nielsen,, C.-Y. Wu,, S. Roseman,, and G. K. Schoolnik. 2004. The Vibrio cholerae chitin utilization program. Proc. Natl. Acad. Sci. USA 101: 2524– 2529.
120. Merrell, D. S.,, S. M. Butler,, F. Qadri,, N. A. Dolganov,, A. Alam,, M. B. Cohen,, S. B. Calderwood,, G. K. Schoolnik,, and A. Camilli. 2002. Host-induced epidemic spread of the cholera bacterium. Nature 417: 642– 645.
121. Merrell, D. S.,, and A. Camilli. 1999. The cadA gene of Vibrio cholerae is induced during infection and plays a role in acid tolerance. Mol. Microbiol. 34: 836– 849.
122. Merrell, D. S.,, and A. Camilli. 2000. Regulation of Vibrio cholerae genes required for acid tolerance by a member of the “ToxR-like” family of transcriptional regulators. J. Bacteriol. 182: 5342– 5350.
123. Merrell, D. S.,, C. Bailey,, J. B. Kaper,, and A. Camilli. 2001. The ToxR-mediated organic acid tolerance response of Vibrio cholerae requires OmpU. J. Bacteriol. 183: 2746– 2754.
124. Miller, M. B.,, K. Skorupski,, D. H. Lenz,, R. K. Taylor,, and B. L. Bassler. 2002. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110: 303– 314.
125. Miller, V. L.,, R. K. Taylor,, and J. J. Mekalanos. 1987. Cholera toxin transcriptional activator ToxR is a transmembrane DNA binding protein. Cell 48: 271– 279.
126. Miller, V. L.,, and J. J. Mekalanos. 1988. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170: 2575– 2583.
127. Miller, V. L.,, V. J. DiRita,, and J. J. Mekalanos. 1989. Identification of toxS, a regulatory gene whose product enhances ToxR-mediated activation of the cholera toxin promoter. J. Bacteriol. 171: 1288– 1293.
128. Morgan, S. J.,, S. Felek,, S. Gadwal,, N. M. Koropatkin,, J. W. Perry,, A. B. Bryson,, and E. S. Krukonis. 2011. The two faces of ToxR: activator of ompU, co-regulator of toxT in Vibrio cholerae. Mol. Microbiol. 81: 113– 128.
129. Morris, D. C.,, F. Peng,, J. R. Barker,, and K. E. Klose. 2008. Lipidation of an FlrC-dependent protein is required for enhanced intestinal colonization by Vibrio cholerae. J. Bacteriol. 190: 231– 239.
130. Ng, W.-L.,, and B. L. Bassler. 2009. Bacterial quorum-sensing network architectures. Annu. Rev. Genet. 43: 197– 222.
131. Nielsen, A. T.,, N. A. Dolganov,, G. Otto,, M. C. Miller,, C. Y. Wu,, and G. K. Schoolnik. 2006. RpoS controls the Vibrio cholerae mucosal escape response. PLoS Pathog. 2: e109.
132. Nielsen, A. T.,, N. A. Dolganov,, T. Rasmussen,, G. Otto,, M. C. Miller,, S. A. Felt,, S. Torreilles,, and G. K. Schoolnik. 2010. A bistable switch and anatomical site control Vibrio cholerae virulence gene expression in the intestine. PLoS Pathog. 6: e1001102.
133. Nye, M. B.,, J. D. Pfau,, K. Skorupski,, and R. K. Taylor. 2000. Vibrio cholerae H-NS silences virulence gene expression at multiple steps in the ToxR regulatory cascade. J. Bacteriol. 182: 4295– 4303.
134. Ou, G.,, P. K. Rompikuntal,, A. Bitar,, B. Lindmark,, K. Vaitkevicius,, S. N. Wai,, and M.-L. Hammarstrom. 2009. Vibrio cholerae cytolysin causes an inflammatory response in human intestinal epithelial cells that is modulated by the PrtV protease. PloS One 4: e7806.
135. Peterson, K. M.,, and J. J. Mekalanos. 1988. Characterization of the Vibrio cholerae toxR regulon: identification of novel genes involved in intestinal colonization. Infect. Immun. 56: 2822– 2829.
136. Pokutta, S.,, and W. I. Weis. 2007. Structure and mechanism of cadherins and catenins in cell-cell contacts. Annu. Rev. Cell Dev. Biol. 23: 237– 261.
137. Porter, S. L.,, G. H. Wadhams,, and J. P. Armitage. 2011. Signal processing in complex chemotaxis pathways. Nat. Rev. Microbiol. 9: 153– 165.
138. Pratt, J. T.,, A. M. Ismail,, and A. Camilli. 2010. PhoB regulates both environmental and virulence gene expression in Vibrio cholerae. Mol. Microbiol. 77: 1595– 1605.
139. Pratt, J. T.,, E. McDonough,, and A. Camilli. 2009. PhoB regulates motility, biofilms and cyclic di-GMP in Vibrio cholerae. J.Bacteriol. 191: 6632– 6642.
140. Prouty, M. G.,, N. E. Correa,, and K. E. Klose. 2001. The novel σ 54- and σ 28-dependent flagellar gene transcription hierarchy of Vibrio cholerae. Mol. Microbiol. 39: 1595– 1609.
141. Prouty, M. G.,, C. R. Osorio,, and K. E. Klose. 2005. Characterization of functional domains of the Vibrio cholerae virulence regulator ToxT. Mol. Microbiol. 58: 1143– 1156.V
142. Provenzano, D.,, and K. E. Klose. 2000. Altered expression of the ToxR-regulated porins OmpU and OmpT diminishes Vibrio cholerae bile resistance, virulence factor expression, and intestinal colonization. Proc. Natl. Acad. Sci. USA 97: 10220– 10224.
143. Provenzano, D.,, D. A. Schuhmacher,, J. L. Barker,, and K. E. Klose. 2000. The virulence regulatory protein ToxR mediates enhanced bile resistance in Vibrio cholerae and other pathogenic Vibrio species. Infect. Immun. 68: 1491– 1497.
144. Rao, N. N.,, and A. Torriani. 1990. Molecular aspects of phosphate transport in Escherichia coli. Mol. Microbiol. 4: 1083– 1090.
145. Richard, A. L.,, J. H. Withey,, S. Beyhan,, F. Yildiz,, and V. J. DiRita. 2010. The Vibrio cholerae virulence regulatory cascade controls glucose uptake through activation of TarA, a small regulatory RNA. Mol. Microbiol. 78: 1171– 1181.
146. Rutherford, S. T.,, J. C. van Kessel,, Y. Shao,, and B. L. Bassler. 2011. AphA and LuxR/HapR reciprocally control quorum sensing in vibrios. Genes Dev. 25: 397– 408.
147. Ryan, R. P.,, Y. Fouhy,, J. F. Lucey,, L. C. Crossman,, S. Spiro,, Y.-W. He,, L.-H. Zhang,, S. Heeb,, M. Camara,, P. Williams,, and J. M. Dow. 2006. Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc. Natl. Acad. Sci. USA 103: 6712– 6717.
148. Ryjenkov, D. A.,, R. Simm,, U. Romling,, and M. Gomelsky. 2006. The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ domain protein YcgR controls motility in enterobacteria. J. Biol. Chem. 281: 30310– 30314.
149. Ryjenkov, D. A.,, M. Tarutina,, O. V. Moskvin,, and M. Gomelsky. 2005. Cyclic diguanylate is a ubiquitous signalling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J. Bacteriol. 187: 1792– 1798.
150. Sanchez, J.,, and J. Holmgren. 2005. Virulence factors, pathogenesis and vaccine protection in cholera and ETEC diarrhea. Curr. Opin. Immunol. 17: 388– 398.
151. Sanchez, J.,, and J. Holmgren. 2008. Cholera toxin structure, gene regulation and pathophysiological and immunological aspects. Cell. Mol. Life Sci. 65: 1347– 1360.
152. Satchell, K. J. F. 2011. Structure and function of MARTX toxins and other large repetitive RTX proteins. Annu. Rev. Microbiol. 65: 71– 90.
153. Schild, S.,, R. Tamayo,, E. J. Nelson,, F. Qadri,, S. B. Calderwood,, and A. Camilli. 2007. Genes induced late in infection increase fitness of Vibrio cholerae after release into the environment. Cell Host Microbe 2: 264– 277.
154. Schmidt, A. J.,, D. A. Ryjenkov,, and M. Gomelsky. 2005. The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J. Bacteriol. 187: 4774– 4781.
155. Schuhmacher, D. A.,, and K. E. Klose. 1999. Environmental signals modulate ToxT-dependent virulence factor expression in Vibrio cholerae. J. Bacteriol. 181: 1508– 1514.
156. Shakhnovich, E. A.,, D. T. Hung,, E. Pierson,, K. Lee,, and J. J. Mekalanos. 2007. Virstatin inhibits dimerization of the transcriptional activator ToxT. Proc. Natl. Acad. Sci. USA 104: 2372– 2377.
157. Silva, A. J.,, G. J. Leitch,, A. Camilli,, and J. A. Benitez. 2006. Contribution of hemagglutinin/protease and motility to the pathogenesis of El Tor biotype cholera. Infect. Immun. 74: 2072– 2079.
158. Skorupski, K.,, and R. K. Taylor. 1997. Cyclic AMP and its receptor protein negatively regulate the coordinate expression of cholera toxin and toxin-coregulated pilus in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 94: 265– 270.
159. Skorupski, K.,, and R. K. Taylor. 1999. A new level in the Vibrio cholerae ToxR virulence cascade: AphA is required for transcriptional activation of the tcpPH operon. Mol. Microbiol. 31: 763– 771.
160. Srivastava, D.,, R. C. Harris,, and C. M. Waters. 2011. Integration of cyclic di-GMP and quorum sensing in the control of vpsT and aphA in Vibrio cholerae. J. Bacteriol. 193: 6331– 6341.
161. Stonehouse, E.,, G. Kovacikova,, R. K. Taylor,, and K. Skorupski. 2008. Integration host factor positively regulates virulence gene expression in Vibrio cholerae. J. Bacteriol. 190: 4736– 4748.
162. Stonehouse, E. A.,, R. R. Hulbert,, M. B. Nye,, K. Skorupski,, and R. K. Taylor. 2011. H-NS binding and repression of the ctx promoter in Vibrio cholerae. J. Bacteriol. 193: 979– 988.
163. Syed, K. A.,, S. Beyhan,, N. Correa,, J. Queen,, J. Liu,, F. Peng,, K. J. F. Satchell,, \ Yildiz,, and K. E. Klose. 2009. The Vibrio cholerae flagellar regulatory hierarchy controls expression of virulence factors. J. Bacteriol. 191: 6555– 6570.
164. Szabady, R. L.,, J. H. Yanta,, D. K. Halladin,, M. J. Schofield,, and R. A. Welch. 2011. TagA is a secreted protease of Vibrio cholerae that specifically cleaves mucin glycoproteins. Microbiology 157: 516– 525.
165. Tamayo, R.,, A. D. Tischler,, and A. Camilli. 2005. The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J. Biol. Chem. 280: 33324– 33330.
166. Tamayo, R.,, B. Patimalla,, and A. Camilli. 2010. Growth in a biofilm induces a hyperinfectious phenotype in Vibrio cholerae. Infect. Immun. 78: 3560– 3569.
167. Tamayo, R.,, S. Schild,, J. T. Pratt,, and A. Camilli. 2008. Role of cyclic di-GMP during El Tor biotype Vibrio cholerae infection: characterization of the in vivo-induced cyclic di-GMP phosphodiesterase CdpA. Infect. Immun. 76: 1617– 1627.
168. Tamplin, M. L.,, A. L. Gauzens,, A. Huq,, D. A. Sack,, and R. R. Colwell. 1990. Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters. Appl. Environ. Microbiol. 56: 1977– 1980.
169. Taylor, J. L.,, R. S. De Silva,, G. Kovacikova,, W. Lin,, R. K. Taylor,, K. Skorupski,, and F. J. Kull. 2012. The crystal structure of AphB, a virulence gene activator from Vibrio cholerae, reveals residues that influence its response to oxygen and pH. Mol. Microbiol. 83: 457– 470.
170. Taylor, R. K.,, V. L. Miller,, D. B. Furlong,, and J. J. Mekalanos. 1987. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc. Natl. Acad. Sci. USA 84: 2833– 2837.
171. Tischler, A. D.,, and A. Camilli. 2004. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol. Microbiol. 53: 857– 869.
172. Tischler, A. D.,, and A. Camilli. 2005. Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect. Immun. 73: 5873– 5882.
173. Tischler, A. D.,, S. H. Lee,, and A. Camilli. 2002. The Vibrio cholerae vieSAB locus encodes a pathway contributing to cholera toxin production. J. Bacteriol. 184: 4104– 4113.
174. Vaitkevicius, K.,, B. Lindmark,, G. Ou,, T. Song,, C. Toma,, M. Iwanaga,, J. Zhu,, A. Andersson,, M.-L. Hammarstrom,, S. Tuck,, and S. N. Wai. 2006. A Vibrio cholerae protease needed for killing of Caenorhabditis elegans has a role in protection from natural predator grazing. Proc. Natl. Acad. Sci. USA 103: 9280– 9285.
175. van Ulsen, P.,, M. Hillebrand,, L. Zulianello,, P. van de Putte,, and N. Goosen. 1996. Integration host factor alleviates the H-NS-mediated repression of the early promoter of bacteriophage Mu. Mol. Microbiol. 21: 567– 578.
176. Waldor, M. K.,, and J. J. Mekalanos. 1996. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272: 1910– 1914.
177. Waters, C. M.,, W. Lu,, J. D. Rabinowitz,, and B. L. Bassler. 2008. Quorum sensing controls biofilm formation in Vibrio cholerae through modulation of cyclic di-GMP levels and repression of vpsT. J. Bacteriol. 190: 2527– 2536.
178. Withey, J. H.,, and V. J. DiRita. 2005a. Activation of both acfA and acfD transcription by Vibrio cholerae ToxT requires binding to two centrally located DNA sites in an inverted repeat conformation. Mol. Microbiol. 56: 1062– 1077.
179. Withey, J. H.,, and V. J. DiRita. 2005b. Vibrio cholerae ToxT independently activates the divergently transcribed aldA and tagA genes. J. Bacteriol. 187: 7890– 7900.
180. Withey, J. H.,, and V. J. DiRita. 2006. The toxbox: specific DNA sequence requirements for activation of Vibrio cholerae virulence genes by ToxT. Mol. Microbiol. 59: 1779– 1789.
181. Yang, J.,, M. Tauschek,, and R. M. Robins-Browne. 2011. Control of bacterial virulence by AraC-like regulators that respond to chemical signals. Trends Microbiol. 19: 128– 135.
182. Yang, M.,, E. M. Frey,, Z. Liu,, R. Bishar,, and J. Zhu. 2010. The virulence transcriptional activator AphA enhances biofilm formation by Vibrio cholerae by activating the expression of the biofilm regulator VpsT. Infect. Immun. 78: 697– 703.
183. Yildiz, F. H.,, and G. K. Schoolnik. 1999. Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance and biofilm formation. Proc. Natl. Acad. Sci. USA 96: 4028– 4033.
184. Yildiz, F. H.,, N. A. Dolganov,, and G. K. Schoolnik. 2001. VpsR, a member of the response regulators of the two-component regulatory systems, is required for expression of vps biosynthesis genes and EPS ETr-associated phenotypes in Vibrio cholerae O1 El Tor. J. Bacteriol. 183: 1716– 1726.
185. Yildiz, F. H.,, X. S. Liu,, A. Heydorn,, and G. K. Schoolnik. 2004. Molecular analysis of rugosity in a Vibrio cholerae O1 El Tor phase variant. Mol. Microbiol. 53: 497– 515.
186. Yu, R. R.,, and V. J. DiRita. 1999. Analysis of an autoregulatory loop controlling ToxT, cholera toxin, and toxin-coregulated pilus production in Vibrio cholerae. J. Bacteriol. 181: 2584– 2592.
187. Yu, R. R.,, and V. J. DiRita. 2002. Regulation of gene expression in Vibrio cholerae by ToxT involves both antirepression and RNA polymerase stimulation. Mol. Microbiol. 43: 119– 134.
188. Zheng, J.,, O. S. Shin,, D. E. Cameron,, and J. J. Mekalanos. 2010. Quorum sensing and a global regulator TsrA control expression of type VI secretion and virulence in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 107: 21128– 21133.
189. Zhu, J.,, M. B. Miller,, R. E. Vance,, M. Dziejman,, B. L. Bassler,, and J. J. Mekalanos. 2002. Quorum sensing regulators control virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 99: 3129– 3134.
190. Zhu, J.,, and J. J. Mekalanos. 2003. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev. Cell 5: 647– 656.

Tables

Toxin and Virulence Regulation in Vibrio cholerae
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Citation: Skorupski K, Taylor R. 2013. Toxin and Virulence Regulation in , p 241-261. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch12
/content/10.1128/9781555818524.chap12.tab12-1
Table 1

Environmental factors influencing virulence gene expression

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10.1128/9781555818524/tab12-1.gif
Generic image for table
Table 1

Environmental factors influencing virulence gene expression

Citation: Skorupski K, Taylor R. 2013. Toxin and Virulence Regulation in , p 241-261. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch12

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