Disulfide Bond Formation and ToxR Activity in Vibrio cholerae

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Fengler, Vera H I ^a   Boritsch, Eva C ^a   Tutz, Sarah ^a   Seper, Andrea ^a   Ebner, Hanna ^a   Roier, Sandro ^a   Schild, Stefan ^a   Reidl, Joachim ^a  

^a UNIVERSITY OF GRAZ   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; DSBAB PROTEIN; HETERODIMER; HOMODIMER; OLIGOMER; OUTER MEMBRANE PORIN OMPT; OUTER MEMBRANE PORIN OMPU; PORIN; SERINE; TOXR PROTEIN; TOXS PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIUM MUTANT; CONTROLLED STUDY; DIMERIZATION; DISULFIDE BOND; GENE CONTROL; HETERODIMERIZATION; MOUSE; NONHUMAN; OLIGOMERIZATION; OXIDATION REDUCTION STATE; PROTEIN PROTEIN INTERACTION; VIBRIO CHOLERAE;

ANIMALS; BACTERIAL PROTEINS; CHOLERA; CYSTEINE; DISULFIDES; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; IMMUNOBLOTTING; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MUTATION; PERIPLASM; PORINS; PROTEIN DISULFIDE-ISOMERASES; PROTEIN MULTIMERIZATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS; VIBRIO CHOLERAE; VIRULENCE;

VIBRIO CHOLERAE;

EID: 84868091760     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047756     Document Type: Article

References (73)

1. Faruque SM, Albert MJ, Mekalanos JJ, (1998) Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae. Microbiol and Mol Biol Rev 62: 1301-1314.
2. Pruzzo C, Vezzulli L, Colwell RR, (2008) Global impact of Vibrio cholerae interactions with chitin. Environ Microbiol 10: 1400-1410.
3. Reidl J, Klose KE, (2002) Vibrio cholerae and cholera: Out of the water and into the host. FEMS-Microbiol Rev 26: 125-139.
4. Andoh A, Fujiyama Y, Sakumoto H, Uchihara H, Kimura T, et al. (1998) Detection of complement C3 and factor B gene expression in normal colorectal mucosa, adenomas and carcinomas. Clin Exp Immunol 111: 477-483.
5. Mallow EB, Harris A, Salzman N, Russell JP, DeBerardinis RJ, et al. (1996) Human enteric defensins. J Biol Chem 271: 4038-4045.
6. Herrington DA, Hall RH, Losonsky G, Mekalanos JJ, Taylor RK, et al. (1988) Toxin, toxin-coregulated pili and the toxR regulation are essential for Vibrio cholerae pathogenesis in humans. J Exp Med 168: 1487-1492.
7. DiRita VJ, Parsot C, Jander G, Mekalanos JJ, (1991) Regulatory cascade controls virulence in Vibrio cholerae. Proc Natl Acad Sci 88: 5403-5407.
8. Faruque SM, Nair GB, Mekalanos JJ, (2004) Genetics of stress adaptation and virulence in toxigenic Vibrio cholerae. DNA Cell Biol 23: 723-741.
9. Matson JS, Withey JH, DiRita VJ, (2007) Regulatory networks controlling Vibrio cholerae virulence gene expression. Infect Immun pp. 5542-5549.
10. Karaolis DK, Johnson JA, Bailey CC, Boedeker EC, Kaper JB, et al. (1998) A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proc Natl Acad Sci USA 95: 3134-3139.
11. Kovach ME, Shaffer MD, Peterson KM, (1996) A putative integrase gene defines the distal end of a large cluster of ToxR-regulated colonization genes in Vibrio cholerae. Microbiology 142: 2165-2174.
12. Miller VL, Mekalanos JJ, (1984) Synthesis of cholera toxin is positively regulated at the transcriptional level by toxR. Proc Nat Acad Sci USA 81: 3471-3475.
13. Osorio CR, Klose KE, (2000) A region of the transmembrane regulatory protein ToxR That tethers the transcriptional activation domain to the cytoplasmic membrane displays wide divergence among Vibrio species. J Bacteriol 182: 526-528.
14. Skorupski K, Taylor RK, (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.
15. Xu X, Stern AM, Liu Z, Kan B, Zhu J, (2010) Virulence regulator AphB enhances toxR transcription in Vibrio cholerae. BMC Microbiology doi:101186/1471-2180-10-3.
16. Bina J, Zhu J, Dziejman M, Faruque S, Calderwood S, et al. (2003) ToxR regulon of Vibrio cholerae and its expression in vibrios shed by cholera patients. Proc Natl Acad Sci USA 100: 2801-2806.
17. Childers BM, Klose KE, (2007) Regulation of virulence in Vibrio cholerae: the ToxR regulon. Future Microbiol 2: 335-344.
18. Hase CC, Mekalanos JJ, (1998) TcpP protein is a positive regulator of virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci USA 95: 730-734.
19. Higgins DE, DiRita VJ, (1994) Transcriptional control of toxT, a regulatory gene in the ToxR regulon of Vibrio cholerae. Mol Microbiol 14: 17-29.
20. DiRita VJ, (1994) Multiple regulatory systems in Vibrio cholerae pathogenesis. Trends Microbiol 2: 37-38.
21. Miller V, 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.
22. 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.
23. 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.
24. Li CC, Merrell DS, Camilli A, Kaper JB, (2002) ToxR interferes with CRP-dependent transcriptional activation of ompT in Vibrio cholerae. Mol Microbiol 43: 1577-1589.
25. Miller VL, Mekalanos JJ, (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.
26. Provenzano D, Klose KE, (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.
27. 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.
28. 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.
29. Morgan SJ, Felek S, Gadwal S, Koropatkin NM, Perry JW, et al. (2011) The two faces of ToxR: activator of ompU, co-regulator of toxT in Vibrio cholerae. Mol Microbiol 81: 113-128.
30. Miller VL, Taylor RK, Mekalanos JJ, (1987) Cholera toxin transcriptional activator ToxR is a transmembrane DNA binding protein. Cell 48: 271-279.
31. Dziejman M, Mekalanos JJ, (1994) Analysis of membrane protein interaction: ToxR can dimerize the amino terminus of phage lambda repressor. Mol Microbiol 13: 485-494.
32. Kolmar H, Hennecke F, Götz K, Janzer B, Vogt B, et al. (1995) Membrane insertion of the bacterial signal transduction protein ToxR and requirements of transcriptional activation studied by modular replacement of different protein substructures. EMBO J 14: 3895-3904.
33. Ottemann KM, Mekalanos JJ, (1995) Analysis of Vibrio cholerae ToxR function by construction of novel fusion proteins. Mol Microbiol 15: 719-731.
34. Ottemann KM, Mekalanos JJ, (1996) The ToxR protein of Vibrio cholerae forms homodimers and heterodimers. J Bacteriol 178: 156-162.
35. 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.
36. Dziejman M, Kolmar H, Fritz HJ, Mekalanos JJ, (1999) ToxR co-operative interactions are not modulated by environmental conditions or periplasmic domain conformation. Mol Microbiol 31: 305-317.
37. Hung DT, Mekalanos JJ, (2005) Bile acids induce cholera toxin expression in Vibrio cholerae in a ToxT-independent manner. Proc Natl Acad Sci, USA 22: 3028-3033.
38. DiRita VJ, Mekalanos JJ, (1991) Periplasmic interaction between two membrane regulatory proteins, ToxR and ToxS, results in signal transduction and transcriptional activation. Cell 64: 29-37.
39. Pfau JD, Taylor RK, (1998) Mutations in toxR and toxS that separate transcriptional activation from DNA binding at the cholera toxin gene promoter. J Bacteriol 180: 4724-4733.
40. Pearson GDN, Woods A, Chiang SL, Mekalanos JJ, (1993) CTX genetic element encodes a site-specific recombination system and an intestinal colonization factor. Proc Natl Acad Sci USA 90: 3750-3754.
41. Mekalanos JJ, (1983) Duplication and amplification of toxin genes in Vibrio cholerae. Cell 35: 253-263.
42. Iwanaga M, Yamamoto K, (1985) New medium for the production of cholera toxin by Vibrio cholerae O1 Biotype El Tor. J Clin Microbiol 22: 405-408.
43. Grimberg J, Maguire S, Belluscio L, (1989) A simple method for the preparation of plasmid and chromosomal E. coli DNA. Nucleic Acids Res 17: 8893.
44. Sanger F, Nicklen S, Coulson AR, (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463-5467.
45. Donnenberg MS, Kaper JB, (1991) Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun 59: 4310-4317.
46. Horton RM, Hunt HD, Ho SN, Pullen JK, Pease LR, (1989) Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77: 61-68.
47. Carlone ACY, Myrtle LT, Rumschlag HS, Sottner FO, (1986) Rapid microprocedure for isolating detergent-insoluble outer membrane proteins from Haemophilus-species. J Clin Microbiol 24: 330-332.
48. Warburg O, Christian W, (1941) Isolierung und Kristallisation des Gärungsferments Enolase. Biochem Z 310: 384-423.
49. Kang D, Gho YS, Suh M, Kang C, (2002) Highly sensitive and fast protein detection with Coomassie Brilliant Blue in sodium dodecyl sulfate-polyacrylamide gel electrophoresis. BKCS 23: 11.
50. Schild S, Nelson EJ, Camilli A, (2008) Immunization with Vibrio cholerae outer membrane vesicles induces protective immunity in mice. Infect Immun 76: 4554-4563.
51. Schild S, Tamayo R, Nelson EJ, Qadri F, Calderwood SB, et al. (2007) Genes induced late in infection increase fitness of Vibrio cholerae after release into the environment. Cell Host Microbe 2: 264-277.
52. Waldor KW, Mekalanos JJ, (1996) Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272: 1910-1914.
53. Svennerholm AM, Holmgren J, (1978) Identification of Escherichia coli heat-labile enterotoxin by means of a ganglioside immunosorbant assay (GM1-ELISA) procedure. Curr Microbiol 1: 19-23.
54. Moisi M, Jenul C, Butler SM, New A, Tutz S, et al. (2009) A novel regulatory protein involved in motility of Vibrio cholerae. J Bacteriol 191: 7027-7038.
55. Kadokura H, Beckwith J, (2010) Mechanisms of oxidative protein folding in the bacterial cell envelope. Antioxid Redox Signal 13: 1231-1246.
56. Bardwell JC, Lee JO, Jander G, Martin N, Belin D, et al. (1993) A pathway for disulfide bond formation in vivo. Proc Natl Acad Sci USA 90: 1038-1042.
57. Mey AR, Craig SA, Payne SM, (2012) Effects of amino acid supplementation on porin expression and ToxR levels in Vibrio cholerae. Infect Immun 80: 518-528.
58. 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.
59. Chatterjee A, Dutta PK, Chowdhury R, (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.
60. Yu J, Webb H, Hirst TR, (1992) A homologue of the Escherichia coli DsbA protein involved in disulphide bond formation is required for enterotoxin biogenesis in Vibrio cholerae. Mol Microbiol 6: 1949-1958.
61. Segatori L, Murphy L, Arredondo S, Kadokura H, Gilbert H, et al. (2006) Conserved role of the linker alpha-helix of the bacterial disulfide isomerase DsbC in the avoidance of misoxidation by DsbB. J Biol Chem 281: 4911-4919.
62. Salahpour A, Angers S, Bouvier M, (2000) Functional significance of oligomerization of G-protein-coupled receptors. TEM 11: 163-168.
63. Gentile F, Amodeo P, Febbraio F, Picaro F, Motta A, et al. (2002) SDS-resistant active and thermostable dimers are obtained from the dissociation of homotetrameric beta-glycosidase from hyperthermophilic Sulfolobus solfataricus in SDS. Stabilizing role of the A-C intermonomeric interface. J Biol Chem 277: 44050-44060.
64. Lueders J, Pyrowolakis G, Jentsch S, (2003) The ubiquitin-like protein HUB1 forms SDS-resistant complexes with cellular proteins in the absence of ATP. EMBO Rep 4: 1169-1174.
65. Akiyama Y, Ito K, (1993) Folding and assembly of bacterial alkaline phosphatase in vitro and in vivo. J Biol Chem 268: 8146-8150.
66. Ding Y, Davis BM, Waldor MK, (2004) Hfq is essential for Vibrio cholerae virulence and downregulates SigmaE expression. Mol Microbiol 53: 345-354.
67. Danese PN, Silhavy TJ, (1997) The sigma(E) and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes in Escherichia coli. Genes Dev 11: 1183-1193.
68. Pogliano J, Lynch AS, Belin D, Lin EC, Beckwith J, (1997) Regulation of Escherichia coli cell envelope proteins involved in protein folding and degradation by the Cpx two-component system. Genes Dev 11: 1169-1182.
69. Hanahan D, (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557-580.
70. Correa NE, Lauriano CM, McGee R, Klose KE, (2000) Phosphorylation of the flagellar regulatory protein FlrC is necessary for Vibrio cholerae motility and enhanced colonization. Mol Microbiol 35: 743-755.
71. Oka A, Sugisaki H, Takanami M, (1981) Nucleotide sequence of the kanamycin resistance transposon Tn903. J Mol Biol 147: 217-226.
72. Guzman LM, Belin D, Carson MJ, Beckwith J, (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
73. Quinones M, Kimsey HH, Waldor MK, (2005) LexA cleavage is required for CTX prophage induction. Mol Cell 17: 291-300.