ToxR recognizes a direct repeat element in the toxT, ompU, ompT, and ctxA promoters of Vibrio cholerae to regulate transcription

Infection and Immunity

Volumn 81, Issue 3, 2013, Pages 884-895

  Goss, Thomas J ^a   Morgan, Sarah J ^b   French, Emily L ^a   Krukonisa, Eric S ^a,b  

^a UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BINDING SITE; CTXA PROMOTER; DNA BINDING; GENE ACTIVATION; GENE DISRUPTION; GENE MUTATION; GENE SEQUENCE; NONHUMAN; OMPT PROMOTER; OMPU PROMOTER; PRIORITY JOURNAL; PROMOTER REGION; TOXR GENE; TOXT PROMOTER; TRANSCRIPTION INITIATION; VIBRIO CHOLERAE;

ADHESINS, BACTERIAL; BACTERIAL PROTEINS; BASE SEQUENCE; BINDING SITES; DNA FOOTPRINTING; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; PORINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; TRANSCRIPTION FACTORS; VIBRIO CHOLERAE;

EID: 84874701109     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00889-12     Document Type: Article

References (50)

1. Herrington DA, Hall RH, Losonsky G, Mekalanos JJ, Taylor RK, Levine MM. 1988. Toxin, toxin-coregulated pili, and the ToxR regulon are essential for Vibrio cholerae pathogenesis in humans. J. Exp. Med. 168:1487-1492.
2. Champion GA, Neely MN, Brennan MA, DiRita VJ. 1997. A branch in the ToxR regulatory cascade of Vibrio cholerae revealed by characterization of toxT mutant strains. Mol. Microbiol. 23:323-331.
3. DiRita VJ, Parsot C, Jander G, Mekalanos JJ. 1991. Regulatory cascade controls virulence in Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 88: 5403-5407.
4. Häse CC, Mekalanos JJ. 1998. TcpP protein is a positive regulator of virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 95:730-734.
5. Higgins DE, DiRita VJ. 1994. Transcriptional control of toxT, a regulatory gene in the ToxR regulon of Vibrio cholerae. Mol. Microbiol. 14:17-29.
6. Krukonis ES, Yu RR, Dirita VJ. 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.
7. Murley YM, Carroll PA, Skorupski K, Taylor RK, Calderwood SB. 1999. Differential transcription of the tcpPH operon confers biotype-specific control of the Vibrio cholerae ToxR virulence regulon. Infect. Immun. 67:5117-5123.
8. Kovacikova G, Lin W, Skorupski K. 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.
9. Kovacikova G, Skorupski K. 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.
10. Kovacikova G, Skorupski K. 2002. Regulation of virulence gene expression in Vibrio cholerae by quorum sensing: HapR functions at the aphA promoter. Mol. Microbiol. 46:1135-1147.
11. Kovacikova G, Skorupski K. 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.
12. Skorupski K, Taylor RK. 1997. Cyclic AMP and its receptor protein negatively regulate the coordinate expression of cholera toxin and toxincoregulated pilus in Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 94:265-270.
13. Skorupski K, Taylor RK. 1999. A new level in the Vibrio cholerae virulence cascade: AphA is required for transcriptional activation of the tcpPH operon. Mol. Microbiol. 31:763-771.
14. Beck NA, Krukonis ES, DiRita VJ. 2004. TcpH influences virulence gene expression in Vibrio cholerae by inhibiting degradation of the transcription activator TcpP. J. Bacteriol. 186:8309-8316.
15. Matson JS, DiRita VJ. 2005. Degradation of the membrane-localized virulence activator TcpP by the YaeL protease in Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 102:16403-16408.
16. Abuaita BH, Withey JH. 2009. Bicarbonate induces Vibrio cholerae virulence gene expression by enhancing ToxT activity. Infect. Immun. 77: 4111-4120.
17. Schuhmacher DA, Klose KE. 1999. Environmental signals modulate ToxT-dependent virulence factor expression in Vibrio cholerae. J. Bacteriol. 181:1508-1514.
18. Abuaita BH, Withey JH. 2011. Termination of Vibrio cholerae virulence gene expression is mediated by proteolysis of the major virulence activator, ToxT. Mol. Microbiol. 81:1640-1653.
19. Nye MB, Pfau JD, Skorupski K, Taylor RK. 2000. Vibrio cholerae H-NS silences virulence gene expression at multiple steps in the ToxR regulatory cascade. J. Bacteriol. 182:4295-4303.
20. Yu RR, DiRita VJ. 2002. Regulation of gene expression in Vibrio cholerae by ToxT involves both antirepression and RNA polymerase stimulation. Mol. Microbiol. 43:119-134.
21. Liang W, Silva AJ, Benitez JA. 2007. The cyclic AMP receptor protein modulates colonial morphology in Vibrio cholerae. Appl. Environ. Microbiol. 73:7482-7487.
22. Martinez-Hackert E, Stock AM. 1997. Structural relationships in the OmpR family of winged-helix transcription factors. J. Mol. Biol. 269:301-312.
23. Blanco AG, Sola M, Gomis-Ruth FX, Coll M. 2002. Tandem DNA recognition by PhoB, a two-component signal transduction transcriptional activator. Structure 10:701-713.
24. Yoshida T, Qin L, Egger LA, Inouye M. 2006. Transcription regulation of ompF and ompC by a single transcription factor, OmpR. J. Biol. Chem. 281:17114-17123.
25. Goss TJ, Seaborn CP, Gray MD, Krukonis ES. 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.
26. Crawford JA, Krukonis ES, DiRita VJ. 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.
27. Ottemann KM, Mekalanos JJ. 1995. Analysis of Vibrio cholerae ToxR function by construction of novel fusion proteins. Mol. Microbiol. 15: 719-731.
28. Morgan SJ, Felek S, Gadwal S, Koropatkin NM, Perry JW, Bryson AB, Krukonis ES. 2011. The two faces of ToxR: activator of ompU, coregulator of toxT in Vibrio cholerae. Mol. Microbiol. 81:113-128.
29. Krukonis ES, DiRita VJ. 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.
30. Bina J, Zhu J, Dziejman M, Faruque S, Calderwood S, Mekalanos J. 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.
31. Crawford JA, Kaper JB, DiRita VJ. 1998. Analysis of ToxR-dependent transcription activation of ompU, the gene encoding a major envelope protein in Vibrio cholerae. Mol. Microbiol. 29:235-246.
32. Li CC, Crawford JA, DiRita VJ, Kaper JB. 2000. Molecular cloning and transcriptional regulation of ompT, a ToxR-repressed gene in Vibrio cholerae. Mol. Microbiol. 35:189-203.
33. Miller VL, Mekalanos JJ. 1984. Synthesis of cholera toxin is positively regulated at the transcriptional level by ToxR. Proc. Natl. Acad. Sci. U. S. A. 81:3471-3475.
34. Withey JH, DiRita VJ. 2006. The toxbox: specific DNA sequence requirements for activation of Vibrio cholerae virulence genes by ToxT. Mol. Microbiol. 59:1779-1789.
35. Yu RR, DiRita VJ. 1999. Analysis of an autoregulatory loop controlling ToxT, cholera toxin, and toxin-coregulated pilus production in Vibrio cholerae. J. Bacteriol. 181:2584-2592.
36. Miller VL, Taylor RK, Mekalanos JJ. 1987. Cholera toxin transcriptional activator ToxR is a transmembrane DNA binding protein. Cell 48:271-279. 37. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
38. Figurski DH, Helinski DR. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. U. S. A. 76:1648-1652.
39. Higuchi R. 1990. Recombinant PCR, p 177-183. In Innis MA, Gelfand DH, Sninsky JJ, White TJ (ed), PCR protocols: a guide to methods and applications. Academic Press, Inc., San Diego, CA.
40. Linn T, Pierre RS. 1990. Improved vector system for constructing transcriptional fusions that ensure independent translation of lacZ. J. Bacteriol. 172:1077-1084.
41. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
42. Higgins DE, DiRita VJ. 1996. Genetic analysis of the interaction between Vibrio cholerae transcription activator ToxR and toxT promoter DNA. J. Bacteriol. 178:1080-1087.
43. Miller VL, DiRita VJ, Mekalanos JJ. 1989. Identification of toxS, a regulatory gene whose product enhances ToxR-mediated activation of the cholera toxin promoter. J. Bacteriol. 171:1288-1293.
44. Koo HS, Wu HM, Crothers DM. 1986. DNA bending at adeninethymine tracts. Nature 320:501-506.
45. Diniz MM, Goulart CL, Barbosa LC, Farache J, Lery LM, Pacheco AB, Bisch PM, von Kruger WM. 2011. Fine-tuning control of phoBR expression in Vibrio cholerae by binding of PhoB to multiple pho boxes. J. Bacteriol. 193:6929-6938.
46. Mekalanos JJ, Swartz DJ, Pearson GD, Harford N, Groyne F, de Wilde M. 1983. Cholera toxin genes: nucleotide sequence, deletion analysis and vaccine development. Nature 306:551-557.
47. Dittmer JB, Withey JH. 2012. Identification and characterization of the functional toxboxes in the Vibrio cholerae cholera toxin promoter. J. Bacteriol. 194:5255-5263.
48. Marsden I, Chen Y, Jin C, Liao X. 1997. Evidence that the DNA binding specificity of winged helix proteins is mediated by a structural change in the amino acid sequence adjacent to the principal DNA binding helix. Biochemistry 36:13248-13255.
49. Overdier DG, Porcella A, Costa RH. 1994. The DNA-binding specificity of the hepatocyte nuclear factor 3/forkhead domain is influenced by amino- acid residues adjacent to the recognition helix. Mol. Cell. Biol. 14: 2755-2766.
50. Higgins DE, Nazareno E, DiRita VJ. 1992. The virulence gene activator ToxT from Vibrio cholerae is a member of the AraC family of transcriptional activators. J. Bacteriol. 174:6974-6980.