Differences in gene expression between the classical and El Tor biotypes of Vibrio cholerae O1

Infection and Immunity

Volumn 74, Issue 6, 2006, Pages 3633-3642

  Beyhan, Sinem ^a   Tischler, Anna D ^b,c   Camilli, Andrew ^b   Yildiz, Fitnat H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; EXOPOLYSACCHARIDE; IRON; PEPTIDE; VIRULENCE FACTOR;

AMINO ACID TRANSPORT; ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BIOFILM; BIOTYPE; CARBOHYDRATE SYNTHESIS; CHEMOTAXIS; COMPARATIVE STUDY; CONTROLLED STUDY; CTXA GENE; GENE DELETION; GENE EXPRESSION; IRON TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; REGULON; TRANSCRIPTION REGULATION; VIBRIO CHOLERAE; VIEA GENE; VIEB GENE; VIES GENE;

AMINO ACIDS; BACTERIAL PROTEINS; BACTERIAL TYPING TECHNIQUES; CHEMOTAXIS; GENE EXPRESSION PROFILING; PURINE NUCLEOTIDES; PYRIMIDINE NUCLEOTIDES; REGULON; SIGMA FACTOR; TRANSCRIPTION FACTORS; VIBRIO CHOLERAE O1; VIRULENCE;

EID: 33646903239     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01750-05     Document Type: Article

References (58)

1. Ades, S. E. 2004. Control of the alternative sigma factor sigmaE in Escherichia coli. Curr. Opin. Microbiol. 7:157-162.
2. Alba, B. M., and C. A. Gross. 2004. Regulation of the Escherichia coli sigma-dependent envelope stress response. Mol. Microbiol. 52:613-619.
3. Attridge, S. R., P. A. Manning, J. Holmgren, and G. Jonson. 1996. Relative significance of mannose-sensitive hemagglutinin and toxin-coregulated pili in colonization of infant mice by Vibrio cholerae El Tor. Infect. Immun. 64: 3369-3373.
4. 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.
5. Camilli, A., and J. J. Mekalanos. 1995. Use of recombinase gene fusions to identify Vibrio cholerae genes induced during infection. Mol. Microbiol. 18:671-683.
6. 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.
7. 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.
8. Chiavelli, D. A., J. W. Marsh, and R. K. Taylor. 2001. The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl. Environ. Microbiol. 67:3220-3225.
9. 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.
10. Davis, B. M., H. H. Kimsey, A. V. Kane, and M. K. Waldor. 2002. A satellite phage-encoded antirepressor induces repressor aggregation and cholera toxin gene transfer. EMBO J. 21:4240-4249.
11. Davis, B. M., and M. K. Waldor. 2003. Filamentous phages linked to virulence of Vibrio cholerae. Curr. Opin. Microbiol. 6:35-42.
12. Ding, Y., B. M. Davis, and M. K. Waldor. 2004. Hfq is essential for Vibrio cholerae virulence and downregulates sigma expression. Mol. Microbiol. 53: 345-354.
13. DiRita, V. J. 1994. Multiple regulatory systems in Vibrio cholerae pathogenesis. Trends Microbiol. 2:37-38.
14. 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.
15. 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.
16. Duguay, A. R., and T. J. Silhavy. 2004. Quality control in the bacterial periplasm. Biochim. Biophys. Acta 1694:121-134.
17. Dziejman, M., E. Balon, D. Boyd, C. M. Fraser, J. F. Heidelberg, and J. J. Mekalanos. 2002. Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease. Proc. Natl. Acad. Sci. USA 99:1556-1561.
18. 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.
19. Gentleman, R. C., V. J. Carey, D. M. Bates, B. Bolstad, M. Dettling, S. Dudoit, B. Ellis, L. Gautier, V. Ge, J. Gentry, K. Hornik, T. Hothorn, W. Huber, S. Iacus, R. Irizarry, F. Leisch, C. Li, M. Maechler, A. J. Rossini, G. Sawitzki, C. Smith, G. Smyth, L. Tierney, J. Y. Yang, and J. Zhang. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5:R80.
20. -), and 569B. J. Bacteriol. 162:35-41.
21. Goldberg, S. L., and J. R. Murphy. 1984. Molecular cloning of the hemolysin determinant from Vibrio cholerae El Tor. J. Bacteriol. 160:239-244.
22. Gosink, K. K., R. Kobayashi, I. Kawagishi, and C. C. Hase. 2002. Analyses of the roles of the three cheA homologs in chemotaxis of Vibrio cholerae. J. Bacteriol. 184:1767-1771.
23. Hanne, L. F., and R. A. Finkelstein. 1982. Characterization and distribution of the hemagglutinins produced by Vibrio cholerae. Infect. Immun. 36:209-214.
24. 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.
25. Heidelberg, J. F., J. A. Eisen, W. C. Nelson, R. A. Clayton, M. L. Gwinn, R. J. Dodson, D. H. Haft, E. K. Hickey, J. D. Peterson, L. Umayam, S. R. Gill, K. E. Nelson, T. D. Read, H. Tettelin, D. Richardson, M. D. Ermolaeva, J. Vamathevan, S. Bass, H. Qin, I. Dragoi, P. Sellers, L. McDonald, T. Utterback, R. D. Fleishmann, W. C. Nierman, O. White, S. L. Salzberg, H. O. Smith, R. R. Colwell, J. J. Mekalanos, J. C. Venter, and C. M. Fraser. 2000. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406:477-483.
26. 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.
27. Kaper, J. B., J. G. Morris, Jr., and M. M. Levine. 1995. Cholera. Clin. Microbiol. Rev. 8:48-86.
28. Kirn, T. J., B. A. Jude, and R. K. Taylor. 2005. A colonization factor links Vibrio choleras environmental survival and human infection. Nature 438: 863-866.
29. 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.
30. 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.
31. 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.
32. 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.
33. Lee, S. H., M. J. Angelichio, J. J. Mekalanos, and A. Camilli. 1998. Nucleotide sequence and spatiotemporal expression of the Vibrio cholerae vieSAB genes during infection. J. Bacteriol. 180:2298-2305.
34. Li, X., and S. Roseman. 2004. The chitinolytic cascade in vibrios is regulated by chitin oligosaccharides and a two-component chitin catabolic sensor/kinase. Proc. Natl. Acad. Sci. USA 101:627-631.
35. Lipp, E. K., A. Huq, and R. R. Colwell. 2002. Effects of global climate on infectious disease: the cholera model. Clin. Microbiol. Rev. 15:757-770.
36. Manning, P. A., M. H. Brown, and M. W. Heuzenroeder. 1984. Cloning of the structural gene (hly) for the haemolysin of Vibrio cholerae El Tor strain 017. Gene 31:225-231.
37. 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.
38. 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.
39. Murley, Y. M., J. Behari, R. Griffin, and S. B. Calderwood. 2000. Classical and El Tor biotypes of Vibrio cholerae differ in timing of transcription of tcpPH during growth in inducing conditions. Infect. Immun. 68:3010-3014.
40. 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.
41. Parsot, C., and J. J. Mekalanos. 1991. Expression of the Vibrio cholerae gene encoding aldehyde dehydrogenase is under control of ToxR, the cholera toxin transcriptional activator. J. Bacteriol. 173:2842-2851.
42. Prouty, M. G., N. E. Correa, and K. E. Klose. 2001. The novel sigma54- and sigma28-dependent flagellar gene transcription hierarchy of Vibrio cholerae. Mol. Microbiol. 39:1595-1609.
43. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
44. Shaw, C. E., and R. K. Taylor. 1990. Vibrio cholerae O395 tcpA pilin gene sequence and comparison of predicted protein structural features to those of type 4 pilins. Infect. Immun. 58:3042-3049.
45. Tacket, C. O., R. K. Taylor, G. Losonsky, Y. Lim, J. P. Nataro, J. B. Kaper, and M. M. Levine. 1998. Investigation of the roles of toxin-coregulated pili and mannose-sensitive hemagglutinin pili in the pathogenesis of Vibrio cholerae O139 infection. Infect. Immun. 66:692-695.
46. 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.
47. 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.
48. Thelin, K. H., and R. K. Taylor. 1996. Toxin-coregulated pilus, but not mannose-sensitive hemagglutinin, is required for colonization by Vibrio cholerae O1 El Tor biotype and O139 strains. Infect. Immun. 64:2853-2856.
49. Tischler, A. D., and A. Camilli. 2004. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol. Microbiol. 53:857-869.
50. Tischler, A. D., and A. Camilli. 2005. Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect. Immun. 73:5873-5882.
51. 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.
52. Tusher, V. G., R. Tibshirani, and G. Chu. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98:5116-5121.
53. Watnick, P. I., K. J. Fullner, and R. Kolter. 1999. A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. J. Bacteriol. 181:3606-3609.
54. Watnick, P. I., and R. Kolter. 1999. Steps in the development of a Vibrio cholerae El Tor biofilm. Mol. Microbiol. 34:586-595.
55. 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.
56. 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.
57. Yildiz, F. H., and G. K. Schoolnik. 1998. Role of rpoS in stress survival and virulence of Vibrio cholerae. J. Bacteriol. 180:773-784.
58. 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.