vttRa and vttRB encode ToxR family proteins that mediate bile-induced expression of type three secretion system genes in a non-O1/non-O139 Vibrio cholerae strain

Infection and Immunity

Volumn 78, Issue 6, 2010, Pages 2554-2570

  Alam, Ashfaqul ^a   Tam, Vincent ^b,c   Hamilton, Elaine ^a   Dziejman, Michelle ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BETA GALACTOSIDASE; PROTEIN; PROTEIN VOPF; PROTEIN VTTRA; PROTEIN VTTRB; RNA; SPACER DNA; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; DNA BINDING PROTEIN; TOXR PROTEIN, VIBRIO CHOLERAE; TRANSCRIPTION FACTOR;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BILE; CHROMOSOME; CONTROLLED STUDY; GENE CONTROL; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUSION; GENE LOCUS; GENETIC CODE; IN VIVO STUDY; NONHUMAN; OPERON; PRIORITY JOURNAL; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; TRANSCRIPTION REGULATION; VIBRIO CHOLERAE; ANIMAL; BIOSYNTHESIS; DRUG EFFECT; GENETICS; METABOLISM; MOUSE; PHYSIOLOGICAL STRESS; VIRULENCE;

ANIMALS; ANTI-BACTERIAL AGENTS; ARTIFICIAL GENE FUSION; BACTERIAL PROTEINS; BETA-GALACTOSIDASE; BILE; DNA-BINDING PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; MICE; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; VIBRIO CHOLERAE NON-O1; VIRULENCE;

EID: 77952681705     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01073-09     Document Type: Article

References (79)

1. Abreu-Goodger, C., and E. Merino. 2005. RibEx: a web server for locating riboswitches and other conserved bacterial regulatory elements. Nucleic Acids Res. 33:W690-W692. (Pubitemid 44530011)
2. 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.
3. Anderson, A. M., J. B. Varkey, C. A. Petti, R. A. Liddle, R. Frothingham, and C. W. Woods. 2004. Non-O1 Vibrio cholerae septicemia: case report, discussion of literature, and relevance to bioterrorism. Diagn. Microbiol. Infect. Dis. 49:295-297.
4. Bag, P. K., P. Bhowmik, T. K. Hajra, T. Ramamurthy, P. Sarkar, M. Majumder, G. Chowdhury, and S. C. Das. 2008. Putative virulence traits and pathogenicity of Vibrio cholerae non-O1, non-O139 isolates from surface waters in Kolkata, India. Appl. Environ. Microbiol. 74:5635-5644.
5. Bagchi, K., P. Echeverria, J. D. Arthur, O. Sethabutr, O. Serichantalergs, and C. W. Hoge. 1993. Epidemic of diarrhea caused by Vibrio cholerae non-O1 that produced heat-stable toxin among Khmers in a camp in Thailand. J. Clin. Microbiol. 31:1315-1317.
6. Begum, K., C. R. Ahsan, M. Ansaruzzaman, D. K. Dutta, Q. S. Ahmad, and K. A. Talukder. 2006. Toxin(s), other than cholera toxin, produced by environmental non O1 non O139 Vibrio cholerae. Cell. Mol. Immunol. 3:115-121.
7. Bhattacharya, M. K., D. Dutta, S. K. Bhattacharya, A. Deb, A. K. Mukhopadhyay, G. B. Nair, T. Shimada, Y. Takeda, A. Chowdhury, and D. Mahalanabis. 1998. Association of a disease approximating cholera caused by Vibrio cholerae of serogroups other than O1 and O139. Epidemiol. Infect. 120:1-5.
8. Bina, J., J. Zhu, M. Dziejman, S. Faruque, S. Calderwood, and J. Mekalanos. 2003. ToxR regulon of Vibrio cholerae and its expression in vibrios shed by cholera patients. Proc. Natl. Acad. Sci. U. S. A. 100:2801-2806.
9. Bina, J. E., D. Provenzano, C. Wang, X. R. Bina, and J. J. Mekalanos. 2006. Characterization of the Vibrio cholerae vexAB and vexCD efflux systems. Arch. Microbiol. 186:171-181.
10. Bina, X. R., D. Provenzano, N. Nguyen, and J. E. Bina. 2008. Vibrio cholerae RND family efflux systems are required for antimic robial resistance, optimal virulence factor production, and colonization of the infant mouse small intestine. Infect. Immun. 76:3595-3605.
11. Brickman, E., and J. Beckwith. 1975. Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and φ80 transducing phages. J. Mol. Biol. 96:307-316.
12. 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.
13. 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.
14. Chatterjee, S. N., and K. Chaudhuri. 2003. Lipopolysaccharides of Vibrio cholerae. I. Physical and chemical characterization. Biochim. Biophys. Acta 1639:65-79.
15. Chatterjee, S. N., and K. Chaudhuri. 2004. Lipopolysaccharides of Vibrio cholerae II. Genetics of biosynthesis. Biochim. Biophys. Acta 1690:93-109.
16. Chen, Y., J. A. Johnson, G. D. Pusch, J. G. Morris, Jr., and O. C. Stine. 2007. The genome of non-O1 Vibrio cholerae NRT36S demonstrates the presence of pathogenic mechanisms that are distinct from those of O1 Vibrio. cholerae. Infect. Immun. 75:2645-2647. (Pubitemid 46744360)
17. Cornelis, G. R., and F. Van Gijsegem. 2000. Assembly and function of type III secretory systems. Annu. Rev. Microbiol. 54:735-774.
18. 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.
19. Dalsgaard, A., M. J. Albert, D. N. Taylor, T. Shimada, R. Meza, O. Serichantalergs, and P. Echeverria. 1995. Characterization of Vibrio cholerae non-O1 serogroups obtained from an outbreak of diarrhea in Lima, Peru. J. Clin. Microbiol. 33:2715-2722.
20. Dalsgaard, A., A. Forslund, L. Bodhidatta, O. Serichantalergs, C. Pitarangsi, L. Pang, T. Shimada, and P. Echeverria. 1999. A high proportion of Vibrio cholerae strains isolated from children with diarrhoea in Bangkok, Thailand are multiple antibiotic resistant and belong to heterogenous non-O1, non-O139 O-serotypes. Epidemiol. Infect. 122:217-226.
21. Dalsgaard, A., O. Serichantalergs, A. Forslund, W. Lin, J. Mekalanos, E. Mintz, T. Shimada, and J. G. Wells. 2001. Clinical and environmental isolates of Vibrio cholerae serogroup O141 carry the CTX phage and the genes encoding the toxin-coregulated pili. J. Clin. Microbiol. 39:4086-4092.
22. DiRita, V. J., C. Parsot, G. Jander, and J. J. Mekalanos. 1991. Regulatory cascade controls virulence in Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 88:5403-5407.
23. Donnenberg, M. S., and J. B. Kaper. 1991. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect. Immun. 59:4310-4317.
24. Dziejman, M., H. Kolmar, H.-J. Fritz, and J. J. Mekalnaos. 1999. ToxR oligomeric interactions are not modulated by environmental conditions or periplasmic domain conformation. Mol. Microbiol. 31:305-317.
25. Dziejman, M., D. Serruto, V. C. Tam, D. Sturtevant, P. Diraphat, S. M. Faruque, M. H. Rahman, J. F. Heidelberg, J. Decker, L. Li, K. T. Montgomery, G. Grills, R. Kucherlapati, and J. J. Mekalanos. 2005. Genomic characterization of non-O1, non-O139 Vibrio cholerae reveals genes for a type III secretion system. Proc. Natl. Acad. Sci. U. S. A. 102:3465-3470.
26. 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.
27. Faruque, S. M., N. Chowdhury, M. Kamruzzaman, M. Dziejman, M. H. Rahman, D. A. Sack, G. B. Nair, and J. J. Mekalanos. 2004. Genetic diversity and virulence potential of environmental Vibrio cholerae population in a cholera-endemic area. Proc. Natl. Acad. Sci. U. S. A. 101:2123-2128.
28. Faruque, S. M., and J. J. Mekalanos. 2003. Pathogenicity islands and phages in Vibrio cholerae evolution. Trends Microbiol. 11:505-510.
29. Francis, M. S., H. Wolf-Watz, and A. Forsberg. 2002. Regulation of type III secretion systems. Curr. Opin. Microbiol. 5:166-172.
30. Gardel, C. L., and J. J. Mekalanos. 1994. Modus operandi of Vibrio cholerae: swim to arrive stop to kill. The relationship among chemotaxis, motility and virulence. J. Cell. Biochem. 18A:65.
31. Gunn, J. S. 2000. Mechanisms of bacterial resistance and response to bile. Microbes Infect. 2:907-913. (Pubitemid 30483186)
32. Gupta, S., and R. Chowdhury. 1997. Bile affects production of virulence factors and motility of Vibrio cholerae. Infect. Immun. 65:1131-1134.
33. Henke, J. M., and B. L. Bassler. 2004. Quorum sensing regulates type III secretion in Vibrio harveyi and Vibrio parahaemolyticus. J. Bacteriol. 186: 3794-3805.
34. Honda, T., M. Arita, T. Takeda, M. Yoh, and T. Miwatani. 1985. Non-O1 Vibrio cholerae produces two newly identified toxins related to Vibrio parahaemolyticus haemolysin and Escherichia coli heat-stable enterotoxin. Lancet 2(8447):163-164.
35. Horton, R. M., H. D. Hunt, S. N. Ho, J. K. Pullen, and L. R. Pease. 1989. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77:61-68.
36. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379-433.
37. 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. U. S. A. 102:3028-3033.
38. Ichinose, Y., K. Yamamoto, N. Nakasone, M. J. Tanabe, T. Takeda, T. Miwatani, and M. Iwanaga. 1987. Enterotoxicity of El Tor-like hemolysin of non-01 Vibrio cholerae. Infect. Immun. 55:1090-1093.
39. Johnson, J., P. Panigrahi, and J. G. Morris. 1992. Non-O1 Vibrio cholerae NRT36S produces a polysaccharide capsule that determines colony morphology, serum resistance, and virulence in mice. Infect. Immun. 60:864-869.
40. Kazmierczak, M. J., M. Wiedmann, and K. J. Boor. 2005. Alternative sigma factors and their roles in bacterial virulence. Microbiol. Mol. Biol. Rev. 69:527-543.
41. Krukonis, E. S., and V. J. DiRita. 2003. From motility to virulence: sensing and responding to environmental signals in Vibrio cholerae. Curr. Opin. Microbiol. 6:186-190. (Pubitemid 36628664)
42. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
43. Larocque, R. C., J. B. Harris, M. Dziejman, X. Li, A. I. Khan, A. S. 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.
44. 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.
45. 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.
46. Makino, K., K. Oshima, K. Kurokawa, K. Yokoyama, T. Uda, K. Tagomori, Y. Iijima, M. Najima, M. Nakano, A. Yamashita, Y. Kubota, S. Kimura, T. Yasunaga, T. Honda, H. Shinagawa, M. Hattori, and T. Iida. 2003. Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V. cholerae. Lancet 361:743-749. (Pubitemid 36293629)
47. Manoil, C., and J. Beckwith. 1986. A genetic approach to analyzing membrane protein topology. Science 233:1403-1407. (Pubitemid 17169373)
48. Matson, J. S., J. H. Withey, and V. J. Dirita. 2007. Regulatory networks controlling Vibrio cholerae virulence gene expression. Infect. Immun. 75: 5542-5549.
49. Mekalanos, J. J. 1992. Environmental signals controlling expression of virulence determinants in bacteria. J. Bacteriol. 174:1-7.
50. Miller, V. L., and J. J. Mekalanos. 1984. Synthesis of cholera toxin is positively regulated at the transcriptional level by toxR. Proc. Natl. Acad. Sci. U. S. A. 81:3471-3475.
51. Miller, V. L., and J. J. Mekalanos. 1985. Genetic analysis of the cholera toxin-positive regulatory gene toxR. J. Bacteriol. 163:580-585.
52. 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.
53. Morris, J. G. 1990. Non-O group 1 Vibrio cholerae: a look at the epidemiology of an occasional pathogen. Epidemiol. Rev. 12:179-191.
54. Mukhopadhyay, A. K., S. Garg, R. Mitra, A. Basu, K. Rajendran, D. Dutta, S. K. Bhattacharya, T. Shimada, T. Takeda, Y. Takeda, and G. B. Nair. 1996. Temporal shifts in traits of Vibrio cholerae strains isolated from hospitalized patients in Calcutta: a 3-year (1993 to 1995) analysis. J. Clin. Microbiol. 34:2537-2543.
55. Okada, N., T. Iida, K.-S. Park, N. Goto, T. Yasunaga, H. Hiyoshi, S. Matsuda, T. Kodama, and T. Honda. 2009. Identification and characterization of a novel type III secretion system in trh-positive Vibrio parahaemolyticus strain TH3996 reveal genetic lineage and diversity of pathogenic machinery beyond the species level. Infect. Immun. 77:904-913.
56. Osawa, R., E. Arakawa, T. Okitsu, S. Yamai, and H. Watanabe. 2002. Levels of thermostable direct hemolysin produced by Vibrio parahaemolyticus O3:K6 and other serovars grown anaerobically with the presence of a bile acid. Curr. Microbiol. 44:302-305.
57. Ottemann, K. M., V. J. DiRita, and J. J. Mekalanos. 1992. ToxR proteins with substitutions in residues conserved with OmpR fail to activate transcription from the cholera toxin promoter. J. Bacteriol. 174:6807-6814.
58. Peterson, K. M. 2002. Expression of Vibrio cholerae virulence genes in response to environmental signals. Curr. Issues Intest. Microbiol. 3:29-38.
59. Pope, L. M., K. E. Reed, and S. M. Payne. 1995. Increased protein secretion and adherence to HeLa cells by Shigella spp. following growth in the presence of bile salts. Infect. Immun. 63:3642-3648.
60. Prouty, A. M., I. E. Brodsky, J. Manos, R. Belas, S. Falkow, and J. S. Gunn. 2004. Transcriptional regulation of Salmonella enterica serovar Typhimurium genes by bile. FEMS Immunol. Med. Microbiol. 41:177-185.
61. Prouty, A. M., and J. S. Gunn. 2000. Salmonella enterica serovar Typhimurium invasion is repressed in the presence of bile. Infect. Immun. 68: 6763-6769.
62. Provenzano, D., and K. K. 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. U. S. A. 97:10220-10224.
63. Provenzano, D., D. A. Schuhmacher, J. Barker, and K. K. Klose. 2000. The virulence regulatory protein ToxR mediates enhanced bile resistance in Vibrio cholerae and other pathogenic Vibrio species. Infect. Immun. 68:1491-1497. (Pubitemid 30108549)
64. Rahman, M. H., K. Biswas, M. A. Hossain, R. B. Sack, J. J. Mekalanos, and S. M. Faruque. 2008. Distribution of genes for virulence and ecological fitness among diverse Vibrio cholerae population in a cholera endemic area: tracking the evolution of pathogenic strains. DNA Cell Biol. 27:347-355.
65. Reidl, J., and K. E. Klose. 2002. Vibrio cholerae and cholera: out of the water and into the host. FEMS. Microbiol. Rev. 26:125-139.
66. Rivera, I. N., J. Chun, A. Huq, R. B. Sack, and R. R. Colwell. 2001. Genotypes associated with virulence in environmental isolates of Vibrio cholerae. Appl. Environ. Microbiol. 67:2421-2429.
67. Rudra, S., R. Mahajan, M. Mathur, K. Kathuria, and V. Talwar. 1996. Cluster of cases of clinical cholera due to Vibrio cholerae 010 in east Delhi. Indian J. Med. Res. 103:71-73.
68. Sack, D. A., R. B. Sack, G. B. Nair, and A. K. Siddique. 2004. Cholera. Lancet 363:223-233.
69. Saka, H. A., C. Bidinost, C. Sola, P. Carranza, C. Collino, S. Ortiz, J. R. Echenique, and J. L. Bocco. 2008. Vibrio cholerae cytolysin is essential for high enterotoxicity and apoptosis induction produced by a cholera toxin gene-negative V. cholerae non-O1, non-O139 strain. Microb. Pathog. 44:118-128.
70. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, second ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
71. Schuhmacher, D. A., and K. E. Klose. 1999. Environmental signals modulate ToxT-dependent virulence factor expression in Vibrio cholerae. J. Bacteriol. 181:1508-1514.
72. 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.
73. Slauch, J. M., and T. J. Silhavy. 1991. cis-acting ompF mutations that result in OmpR-dependent constitutive expression. J. Bacteriol. 173:4039-4048.
74. Stensrud, K. F., P. R. Adam, C. D. La Mar, A. J. Olive, G. H. Lushington, R. Sudharsan, N. L. Shelton, R. S. Givens, W. L. Picking, and W. D. Picking. 2008. Deoxycholate interacts with IpaD of Shigella flexneri in inducing the recruitment of IpaB to the type III secretion apparatus needle tip. J. Biol. Chem. 283:18646-18654.
75. Tam, V. C., D. Serruto, M. Dziejman, W. Brieher, and J. J. Mekalanos. 2007. A type III secretion system in Vibrio cholerae translocates a formin/spire hybrid-like actin nucleator to promote intestinal colonization. Cell Host Microbe 1:95-107.
76. Tampakaki, A. P., V. E. Fadouloglou, A. D. Gazi, N. J. Panopoulos, and M. Kokkinidis. 2004. Conserved features of type III secretion. Cell. Microbiol. 6:805-816.
77. Wachsmuth, I. K., Ø. Olsvik, G. M. Evins, and T. Popovic. 1994. Molecular epidemiology of cholera, p. 357-370. In I. K. Wachsmuth, P. A. Blake, and Ø. Olsvik (ed.), Vibrio cholerae and cholera: molecular to global perspectives. American Society for Microbiology, Washington, D.C.
78. Reference deleted.
79. Yahr, T. L., and M. C. Wolfgang. 2006. Transcriptional regulation of the Pseudomonas aeruginosa type III secretion system. Mol. Microbiol. 62:631-640.