Regulatory networks controlling Vibrio cholerae virulence gene expression

Infection and Immunity

Volumn 75, Issue 12, 2007, Pages 5542-5549

  Matson, Jyl S ^a   Withey, Jeffrey H ^a,b   DiRita, Victor J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; CHITIN;

BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; BIOFILM; CELL MOTILITY; CHEMOTAXIS; GENE CONTROL; GENE EXPRESSION REGULATION; NONHUMAN; PRIORITY JOURNAL; QUORUM SENSING; REGULATORY MECHANISM; SECOND MESSENGER; SHORT SURVEY; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; VIBRIO CHOLERAE;

ANIMALS; BACTERIAL PROTEINS; CHOLERA; CHOLERA TOXIN; FIMBRIAE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; TRANSCRIPTION FACTORS; VIBRIO CHOLERAE; VIRULENCE FACTORS;

EID: 36749079251     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01094-07     Document Type: Short Survey

References (102)

1. Alba, B. M., and C. A. Gross. 2004. Regulation of the Escherichia coli sigma-dependent envelope stress response. Mol. Microbiol. 52:613-619.
2. Alba, B. M., J. A. Leeds, C. Onufryk, C. Z. Lu, and C. A. Gross. 2002. DegS and YaeL participate sequentially in the cleavage of RseA to activate the sigma(E)-dependent extracytoplasmic stress response. Genes Dev. 16:2156-2168.
3. Ausmees, N., R. Mayer, H. Weinhouse, G. Volman, D. Amikam, M. Benziman, and M. Lindberg. 2001. Genetic data indicate that proteins containing the GGDEF domain possess diguanylate cyclase activity. FEMS Microbiol. Lett. 204:163-167.
4. 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.
5. Beck, N. A., E. S. Krukonis, and V. J. DiRita. 2004. TcpH influences virulence gene expression in Vibrio cholerae by inhibiting degradation of the transcription activator TcpP. J. Bacteriol. 186:8309-5316.
6. Behari, J., L. Stagon, and S. B. Calderwood. 2001. pepA, a gene mediating pH regulation of virulence genes in Vibrio cholerae. J. Bacteriol. 183:178-188.
7. Beyhan, S., A. D. Tischler, A. Camilli, and F. H. Yildiz. 2006. Differences in gene expression between the classical and El Tor biotypes of Vibrio cholerae O1. Infect. Immun. 74:3633-3642.
8. Bik, E. M., A. E. Bunschoten, R. D. Gouw, and F. R. Mooi. 1995. Genesis of the novel epidemic Vibrio cholerae O139 strain: evidence for horizontal transfer of genes involved in polysaccharide synthesis. EMBO J. 14:209 216.
9. Blokesch, M., and G. K. Schoolnik. 2007. Serogroup conversion of Vibrio cholerae in aquatic reservoirs. PLoS Pathog. 3:e81.
10. Brown, M. S., and J. L. Goldstein. 1999. A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood. Proc. Natl. Acad. Sci. USA 96:11041-11048.
11. Busby, S., and R. H. Ebright. 1994. Promoter structure, promoter recognition, and transcription activation in prokaryotes. Cell 79:743-746.
12. 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.
13. 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.
14. Camilli, A., and B. L. Bassler. 2006. Bacterial small-molecule signaling pathways. Science 311:1113-1116.
15. 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.
16. 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.
17. Chen, X., S. Schauder, N. Potier, A. Van Dorsselaer, I. Pelczer, B. L. Bassler, and F. M. Hughson. 2002. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415:545-549.
18. Childers, B. M., G. G. Weber, M. G. Prouty, M. M. Castaneda, F. Peng, and K. E. Klose. 2007. Identification of residues critical for the function of the Vibrio cholerae virulence regulator ToxT by scanning alanine mutagenesis. J. Mol. Biol. 367:1413-1430.
19. 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. 29:235-246.
20. 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.
21. 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.
22. 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 Vibrio cholerae is due to biotype-specific control over toxT expression. Proc. Natl. Acad. Sci. USA 93:7991-7995.
23. 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.
24. Faruque, S. M., M. Kamruzzaman, I. M. Meraj, N. Chowdhury, G. B. Nair, R. B. Sack, R. R. Colwell, and D. A. Sack. 2003. Pathogenic potential of environmental Vibrio cholerae strains carrying genetic variants of the toxin-coregulated pilus pathogenicity island. Infect. Immun. 71:1020-1025.
25. Finkelstein, R. A., M. Boesman-Finkelstein, Y. Chang, and C. C. Hase. 1992. Vibrio cholerae hemagglutinin/protease, colonial variation, virulence, and detachment. Infect. Immun. 60:472-478.
26. Freeman, J. A., and B. L. Bassler. 1999. A genetic analysis of the function of LuxO, a two-component response regulator involved in quorum sensing in Vibrio harveyi. Mol. Microbiol. 31:665-677.
27. Freeman, J. A., and B. L. Bassler. 1999. Sequence and function of LuxU: a two-component phosphorelay protein that regulates quorum sensing in Vibrio harveyi. J. Bacteriol. 181:899-906.
28. Freter, R. 1981. Mechanisms of association of bacteria with mucosal surfaces. CIBA Found. Symp. 80:36-55.
29. Freter, R., and P. C. O'Brien. 1981. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: chemotactic responses of Vibrio cholerae and description of motile nonchemotactic mutants. Infect. Immun. 34:215-221.
30. Freter, R., P. C. O'Brien, and M. S. Macsai. 1981. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vivo studies. Infect. Immun. 34:234-240.
31. 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.
32. 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.
33. Ghosh, A., K. Paul, and R. Chowdhury. 2006. Role of the histone-like nucleoid structuring protein in colonization, motility, and bile-dependent repression of virulence gene expression in Vibrio cholerae. Infect. Immun. 74:3060-3064.
34. Gupta, S., and R. Chowdhury. 1997. Bile affects production of virulence factors and motility of Vibrio cholerae. Infect. Immun. 65:1131-1134.
35. Hase, C. C. 2001. Analysis of the role of flagellar activity in virulence gene expression in Vibrio cholerae. Microbiology 147:831-837.
36. Hase, 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.
37. Hase, 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.
38. Haugo, A. J., and P. I. Watnick. 2002. Vibrio cholerae CytR is a repressor of biofilm development. Mol. Microbiol. 45:471-483.
39. 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.
40. 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.
41. 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.
42. Hung, D. T., and J. J. Mekalanos. 2005. Bile acids induce cholera toxin expression in Vibrio cholerae in a ToxT-independent manner. Proc. Natl. Acad. Sci. USA 102:3028-3033.
43. Hung, D. T., E. A. Shakhnovich, E. Pierson, and J. J. Mekalanos. 2005. Small-molecule inhibitor of Vibrio cholerae virulence and intestinal colonization. Science 310:670-674.
44. 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.
45. 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.
46. 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.
47. 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.
48. Kovacikova, G., W. Lin, and K. Skorapski. 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.
49. Kovacikova, G., and K. Skorupski. 2002. 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.
50. 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.
51. Kovacikova, G., and K. Skorapski. 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.
52. Kovacikova, G., and K. Skorapski. 2002. Regulation of virulence gene expression in Vibrio cholerae by quorum sensing: HapR functions at the aphA promoter. Mol. Microbiol. 46:1135-1147.
53. 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.
54. 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.
55. 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.
56. Lenz, D. H., M. B. Miller, J. Zhu, R. V. Kulkarni, and B. L. Bassler. 2005. CsrA and three redundant small RNAs regulate quorum sensing in Vibrio cholerae. Mol. Microbiol. 58:1186-1202.
57. 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.
58. 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.
59. 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.
60. Lilley, B. N., and B. L. Bassler. 2000. Regulation of quorum sensing in Vibrio harveyi by LuxO and sigma-54. Mol. Microbiol. 36:940-954.
61. Lin, W., G. Kovacikova, and K. Skorapski. 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.
62. Makinoshima, H., and M. S. Glickman. 2006. Site-2 proteases in prokaryotes: regulated intramembrane proteolysis expands to microbial pathogenesis. Microbes Infect. 8:1882-1888.
63. Martin, R. G., and J. L. Rosner. 2001. The AraC transcriptional activators. Curr. Opin. Microbiol. 4:132-137.
64. Martinez-Hackert, E., and A. M. Stock. 1997. Structural relationships in the OmpR family of winged-helix transcription factors. J. Mol. Biol. 269:301-312.
65. 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.
66. 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.
67. Meibom, K. L., M. Blokesch, N. A. Dolganov, C. Y. Wu, and G. K. Schoolnik. 2005. Chitin induces natural competence in Vibrio cholerae. Science 310:1824-1827.
68. 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.
69. 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.
70. 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.
71. 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.
72. Mooi, F. R., and E. M. Bik. 1997. The evolution of epidemic Vibrio cholerae strains. Trends Microbiol. 5:161-165.
73. Morris, J. G., Jr., M. B. Sztein, E. W. Rice, J. P. Nataro, G. A. Losonsky, P. Panigrahi, C. O. Tacket, and J. A. Johnson. 1996. Vibrio cholerae O1 can assume a chlorine-resistant rugose survival form that is virulent for humans. J. Infect. Dis. 174:1364-1368.
74. Murley, Y. M., P. A. Carroll, K. Skorupski, R. K. Taylor, and S. B. Calderwood. 1999. Differential transcription of the tcpPH operon confers biotype-specific control of the Vibrio cholerae ToxR virulence regulon. Infect. Immun. 67:5117-5123.
75. 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.
76. Nye, M. B., J. D. Pfau, K. Skorapski, 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.
77. 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.
78. Pfau, J. D., and R. K. Taylor. 1998. Mutations in toxR and toxS that separate transcriptional activation from DNA binding at the cholera toxin gene promoter. J. Bacteriol. 180:4724-4733.
79. 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.
80. 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.
81. Reguera, G., and R. Kolter. 2005. Virulence and the environment: a novel role for Vibrio cholerae toxin-coregulated pili in biofilm formation on chitin. J. Bacteriol. 187:3551-3555.
82. Rice, E. W., C. J. Johnson, R. M. Clark, K. R. Fox, D. J. Reasoner, M. E. Dunnigan, P. Panigrahi, J. A. Johnson, and J. G. Morris, Jr. 1992. Chlorine and survival of "rugose" Vibrio cholerae. Lancet 340:740.
83. Richardson, K. 1991. Roles of motility and flagellar structure in pathogenicity of Vibrio cholerae: analysis of motility mutants in three animal models. Infect. Immun. 59:2727-2736.
84. Schuhmacher, D. A., and K. E. Klose. 1999. Environmental signals modulate ToxT-dependent virulence factor expression in Vibrio cholerae. J. Bacteriol. 181:1508-1514.
85. 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.
86. 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.
87. Skorapski, K., and R. K. Taylor. 1997. Control of the ToxR virulence regulon in Vibrio cholerae by environmental stimuli. Mol. Microbiol. 25:1003-1009.
88. Sperandio, V., J. A. Giron, W. D. Silveira, and J. B. Kaper. 1995. The OmpU outer membrane protein, a potential adherence factor of Vibrio cholerae. Infect. Immun. 63:4433-4438.
89. 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.
90. Teppema, J. S., P. A. Guinee, A. A. Ibrahim, M. Paques, and E. J. Ruitenberg. 1987. In vivo adherence and colonization of Vibrio cholerae strains that differ in hemagglutinating activity and motility. Infect. Immun. 55:2093-2102.
91. Tischler, A. D., and A. Camilli. 2005. Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect. Immun. 73:5873-5882.
92. Wai, S. N., Y. Mizunoe, A. Takade, S. I. Kawabata, and S. I. Yoshida. 1998. Vibrio cholerae O1 strain TSI-4 produces the exopolysaccharide materials that determine colony morphology, stress resistance, and biofilm formation. Appl. Environ. Microbiol. 64:3648-3655.
93. Withey, J. H., and V. J. DiRita. 2005. 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.
94. 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.
95. Withey, J. H., and V. J. Dirita. 2005. Vibrio cholerae ToxT independently activates the divergently transcribed aldA and tagA genes. J. Bacteriol. 187:7890-7900.
96. Yancey, R. J., and L. J. Berry. 1978. Motility of the pathogen and intestinal immunity of the host in experimental cholera. Adv. Exp. Med. Biol. 107:447-455.
97. Yancey, R. J., D. L. Willis, and L. J. Berry. 1978. Role of motility in experimental cholera in adult rabbits. Infect. Immun. 22:387-392.
98. 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.
99. 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.
100. Yoon, S. S., and J. J. Mekalanos. 2006. 2,3-Butanediol synthesis and the emergence of the Vibrio cholerae El Tor biotype. Infect. Immun. 74:6547-6556.
101. 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.
102. 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.