Regulation of virulence in Vibrio cholerae: the ToxR regulon

Bibliography

• 1  Chen LF, Woolley IJ, Visvanathan K, Korman TM: Hypovolemic shock and metabolic acidosis in a refugee secondary to O1 serotype Vibrio cholerae enteritis. Commun. Dis. Intell.30(2),233–235 (2006).
  MedlineGoogle Scholar
• 2  Wang F, Butler T, Rabbani GH, Jones PK: The acidosis of cholera. Contributions of hyperproteinemia, lactic acidemia, and hyperphosphatemia to an increased serum anion gap. N. Engl. J. Med.315(25),1591–1595 (1986).
  Medline CASGoogle Scholar
• 3  Sanyal SC: Cholera in its present day scenario. J. Indian Med. Assoc.98(7),371–376 (2000).
  Medline CASGoogle Scholar
• 4  Ries AA, Vugia DJ, Beingolea L et al.: Cholera in Piura, Peru: a modern urban epidemic. J. Infect. Dis.166(6),1429–1433 (1992).
  Medline CASGoogle Scholar
• 5  Barua D, Greenough WB: Cholera. Plenum Medical Book Co. NY, USA (1992).
  Google Scholar
• 6  Rosenberg CE: The Cholera Years; the United States in 1832, 1849, and 1866. Univ. of Chicago Press, Chicago, USA (1962).
  Google Scholar
• 7  Ramamurthy T, Garg S, Sharma R et al.: Emergence of novel strain of Vibrio cholerae with epidemic potential in southern and eastern India. Lancet341,703–704 (1993).
  Medline CASGoogle Scholar
• 8  Research ICfDD: Large epidemic of cholera-like disease in Bangladesh caused by Vibrio cholerae O139 synonym Bengal. Cholera Working Group, International Centre for Diarrhoeal Diseases Research, Bangladesh. Lancet342,387–390 (1993).
  MedlineGoogle Scholar
• 9  Redmond JW: The structure of the O-antigenic side chain of the lipopolysaccharide of Vibrio cholerae 569B (Inaba). Biochim. Biophys. Acta584(2),346–352 (1979).
  Medline CASGoogle Scholar
• 10  Kenne L, Lindberg B, Unger P, Gustafsson B, Holme T: Structural studies of the Vibrio cholerae O-antigen. Carbohydr. Res.100,341–349 (1982).
  Medline CASGoogle Scholar
• 11  Roy C, Mukerjee S: Variability in the haemolytic property of El Tor vibrios. Ann. Biochem. Exp. Med.22,295–296 (1962).
  Medline CASGoogle Scholar
• 12  Feeley JC: Classification of Vibrio cholerae (Vibrio comma), including el tor Vibrios, by infrasubspecific characteristics. J. Bacteriol.89,665–670 (1965).
  Medline CASGoogle Scholar
• 13  Barrett TJ, Blake PA: Epidemiological usefulness of changes in hemolytic activity of Vibrio cholerae biotype El Tor during the seventh pandemic. J. Clin. Microbiol.13(1),126–129 (1981).
  Medline CASGoogle Scholar
• 14  Dziejman M, Balon E, Boyd D, Fraser CM, Heidelberg JF, Mekalanos JJ: Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease. Proc. Natl Acad. Sci. USA99(3),1556–1561 (2002).
  Medline CASGoogle Scholar
• 15  Higa N, Honma Y, Albert MJ, Iwanaga M: Characterization of Vibrio cholerae O139 synonym Bengal isolated from patients with cholera-like disease in Bangladesh. Microbiol. Immunol.37(12),971–974 (1993).
  Medline CASGoogle Scholar
• 16  Prager R, Beer W, Voigt W et al.: Genomic and biochemical relatedness between Vibrio cholerae serovar O139 and serovar O1 eltor strains. Zentralbl Bakteriol283(1),14–28 (1995).
  Medline CASGoogle Scholar
• 17  Knirel YA, Paredes L, Jansson PE, Weintraub A, Widmalm G, Albert MJ: Structure of the capsular polysaccharide of Vibrio cholerae O139 synonym Bengal containing D-galactose4,6-cyclophosphate. Eur. J. Biochem.232(2),391–396 (1995).
  Medline CASGoogle Scholar
• 18  Knirel YA, Widmalm G, Senchenkova SN, Jansson PE, Weintraub A: Structural studies on the short-chain lipopolysaccharide of Vibrio cholerae O139 Bengal. Eur. J. Biochem.247(1),402–410 (1997).
  Medline CASGoogle Scholar
• 19  DePaola A: Vibrio cholerae in marine foods and environmental waters: a literature review. J. Food Sci.46,66–70 (1981).
  Google Scholar
• 20  Hornick RB, Music SI, Wenzel R et al.: The Broad Street pump revisited: response of volunteers to ingested cholera vibrios. Bull. NY Acad. Med.47(10),1181–1191 (1971).
  Medline CASGoogle Scholar
• 21  Sack DA, Tacket CO, Cohen MB et al.: Validation of a volunteer model of cholera with frozen bacteria as the challenge. Infect. Immun.66(5),1968–1972 (1998).
  Medline CASGoogle Scholar
• 22  Holmgren J, Svennerholm AM: Mechanisms of disease and immunity in cholera: a review. J. Infect. Dis.136(Suppl.) S105–S112 (1977).
  Medline CASGoogle Scholar
• 23  Taylor RK, Miller VL, Furlong DB, Mekalanos JJ: Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc. Natl Acad. Sci. USA84(9),2833–2837 (1987).
  Medline CASGoogle Scholar
• 24  Koch R, Carter KC: Essays of Robert Koch. Greenwood Press, NY, USA (1987).
  Google Scholar
• 25  De SN, Chatterje DN: An experimental study of the mechanism of action of Vibrioid cholerae on the intestinal mucous membrane. J. Pathol. Bacteriol.66,559–562 (1953).
  Medline CASGoogle Scholar
• 26  Dutta NK, Habbu MK: Experimental cholera in infant rabbits: a method for chemotherapeutic investifation. Br. J. Pharmacol.10,209–221 (1955).
  Google Scholar
• 27  Finkelstein RA, LoSpalluto JJ: Pathogenesis of experimental cholera. Preparation and isolation of choleragen and choleragenoid. J. Exp. Med.130(1),185–202 (1969).
  Medline CASGoogle Scholar
• 28  King CA, Van Heyningen WE: Deactivation of cholera toxin by a sialidase-resistant monosialosylganglioside. J. Infect. Dis.127(6),639–47 (1973).
  Medline CASGoogle Scholar
• 29  Gill DM, King CA: The mechanism of action of cholera toxin in pigeon erythrocyte lysates. J. Biol. Chem.250(16),6424–6432 (1975).
  Medline CASGoogle Scholar
• 30  Simons K, Ikonen E: Functional rafts in cell membranes. Nature387(6633),569–572 (1997).
  Medline CASGoogle Scholar
• 31  London E, Brown DA: Insolubility of lipids in triton X-100: physical origin and relationship to sphingolipid/cholesterol membrane domains (rafts). Biochim. Biophys. Acta1508(1–2),182–195 (2000).
  Medline CASGoogle Scholar
• 32  Gill DM, Rappaport RS: Origin of the enzymatically active A1 fragment of cholera toxin. J. Infect. Dis.139(6),674–680 (1979).
  Medline CASGoogle Scholar
• 33  Majoul I, Sohn K, Wieland FT et al.: KDEL receptor (Erd2p)-mediated retrograde transport of the cholera toxin A subunit from the Golgi involves COPI, p23, and the COOH terminus of Erd2p. J. Cell Biol.143(3),601–612 (1998).
  Medline CASGoogle Scholar
• 34  Majoul IV, Bastiaens PI, Soling HD: Transport of an external Lys-Asp-Glu-Leu (KDEL) protein from the plasma membrane to the endoplasmic reticulum: studies with cholera toxin in Vero cells. J. Cell Biol.133(4),777–789 (1996).
  Medline CASGoogle Scholar
• 35  Richards AA, Stang E, Pepperkok R, Parton RG: Inhibitors of COP-mediated transport and cholera toxin action inhibit simian virus 40 infection. Mol. Biol. Cell.13(5),1750–64 (2002).
  Medline CASGoogle Scholar
• 36  Teter K, Holmes RK: Inhibition of endoplasmic reticulum-associated degradation in CHO cells resistant to cholera toxin, Pseudomonas aeruginosa exotoxin A, and ricin. Infect. Immun.70(11),6172–6179 (2002).
  Medline CASGoogle Scholar
• 37  Dickinson BL, Lencer WI: Trancytosis of bacterial toxins across mucosal barriers. In: Bacterial Protein Toxins. Burns DL, Iglewski BH, Rappouli R (Eds). ASM Press, Washington DC, USA 173–186 (2003).
  Google Scholar
• 38  Mekalanos JJ, Collier RJ, Romig WR: Enzymic activity of cholera toxin. I. New method of assay and the mechanism of ADP-ribosyl transfer. J. Biol. Chem.254(13),5849–5854 (1979).
  Medline CASGoogle Scholar
• 39  Field M: Mechanisms of action of cholera and Escherichia coli enterotoxins. Am. J. Clin. Nutr.32(1),189–196 (1979).
  Medline CASGoogle Scholar
• 40  Jodal M, Lungren O: Enterotoxin-induced fluid secretion and the enteric nervous system. In: Development of Vaccines and Drugs against Diarrhea. Holmgren JAL, Molby R (Eds). Student litteratur, Lund, Sweden 278 (1985).
  Google Scholar
• 41  Field M, Fromm D, Wallace CK, Greenough WB: Stimulation of active chloride secretion in small intestine by cholera exotoxin. J. Clin. Invest.48,24a (1965).
  Google Scholar
• 42  Waldor MK, Mekalanos JJ: Lysogenic conversion by a filamentous phage encoding cholera toxin. Science272(5270),1910–1914 (1996).
  Medline CASGoogle Scholar
• 43  Kaper JB, Moseley SL, Falkow S: Molecular characterization of environmental and nontoxigenic strains of Vibrio cholerae. Infect. Immun.32(2),661–667 (1981).
  Medline CASGoogle Scholar
• 44  Mukhopadhyay AK, Chakraborty S, Takeda Y, Nair GB, Berg DE: Characterization of VPI pathogenicity island and CTXφ prophage in environmental strains of Vibrio cholerae. J. Bacteriol.183(16),4737–4746 (2001).
  Medline CASGoogle Scholar
• 45  Davis BM, Kimsey HH, Chang W, Waldor MK: The Vibrio cholerae O139 Calcutta bacteriophage CTXφ is infectious and encodes a novel repressor. J. Bacteriol.181(21),6779–6787 (1999).
  Medline CASGoogle Scholar
• 46  Shaw CE, Taylor RK: Vibrio cholerae O395 tcpA pilin gene sequence and comparison of predicted protein structural features to those of type 4 pilins. Infect. Immun.58(9),3042–3049 (1990).
  Medline CASGoogle Scholar
• 47  Manning PA: The tcp gene cluster of Vibrio cholerae. Gene192(1),63–70 (1997).
  Medline CASGoogle Scholar
• 48  Karaolis DK, Johnson JA, Bailey CC, Boedeker EC, Kaper JB, Reeves PR: A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proc. Natl Acad. Sci. USA95(6),3134–3139 (1998).
  Medline CASGoogle Scholar
• 49  Karaolis DK, Somara S, Maneval DR Jr, Johnson JA, Kaper JB: A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria. Nature399(6734),375–379 (1999).
  Medline CASGoogle Scholar
• 50  Faruque SM, Zhu J, Asadulghani, Kamruzzaman M, Mekalanos JJ: Examination of diverse toxin-coregulated pilus-positive Vibrio cholerae strains fails to demonstrate evidence for Vibrio pathogenicity island phage. Infect. Immun.71(6),2993–2999 (2003).
  Medline CASGoogle Scholar
• 51  Rajanna C, Wang J, Zhang D, Xu Z, Ali A, Hou YM et al.: The vibrio pathogenicity island of epidemic Vibrio cholerae forms precise extrachromosomal circular excision products. J. Bacteriol.185(23),6893–6901 (2003).
  Medline CASGoogle Scholar
• 52  Herrington DA, Hall RH, Losonsky G, Mekalanos JJ, Taylor RK, Levine MM: Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans. J. Exp. Med.168(4),1487–1492 (1988).
  Medline CASGoogle Scholar
• 53  Kirn TJ, Lafferty MJ, Sandoe CM, Taylor RK: Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. Mol. Microbiol.35(4),896–910 (2000).
  Medline CASGoogle Scholar
• 54  Kirn TJ, Bose N, Taylor RK: Secretion of a soluble colonization factor by the TCP type 4 pilus biogenesis pathway in Vibrio cholerae. Mol. Microbiol.49(1),81–92 (2003).
  Medline CASGoogle Scholar
• 55  Peterson KM, Mekalanos JJ: Characterization of the Vibrio cholerae ToxR regulon: identification of novel genes involved in intestinal colonization. Infect. Immun.56(11),2822–2829 (1988).
  Medline CASGoogle Scholar
• 56  Everiss KD, Hughes KJ, Kovach ME, Peterson KM: The Vibrio cholerae ACFb colonization determinant encodes an inner membrane protein that is related to a family of signal-transducing proteins. Infect. Immun.62(8),3289–3298 (1994).
  Medline CASGoogle Scholar
• 57  Miller VL, Mekalanos JJ: Synthesis of cholera toxin is positively regulated at the transcriptional level by toxR. Proc. Natl Acad. Sci. USA81(11),3471–3475 (1984).
  Medline CASGoogle Scholar
• 58  Miller VL, Mekalanos JJ: Genetic analysis of the cholera toxin-positive regulatory gene toxR. J. Bacteriol.163(2),580–5 (1985).
  Medline CASGoogle Scholar
• 59  Higgins DE, Nazareno E, DiRita VJ: The virulence gene activator ToxT from Vibrio cholerae is a member of the AraC family of transcriptional activators. J. Bacteriol.174(21),6974–6980 (1992).
  Medline CASGoogle Scholar
• 60  DiRita VJ, Parsot C, Jander G, Mekalanos JJ: Regulatory cascade controls virulence in Vibrio cholerae. Proc. Natl Acad. Sci. USA88(12),5403–5407 (1991).
  Medline CASGoogle Scholar
• 61  Bina J, Zhu J, Dziejman M, Faruque S, Calderwood S, Mekalanos J: ToxR regulon of Vibrio cholerae and its expression in vibrios shed by cholera patients. Proc. Natl Acad. Sci. USA100(5),2801–2806 (2003).
  Medline CASGoogle Scholar
• 62  Yu RR, DiRita VJ: Analysis of an autoregulatory loop controlling ToxT, cholera toxin, and toxin-coregulated pilus production in Vibrio cholerae. J. Bacteriol.181(8),2584–2592 (1999).
  Medline CASGoogle Scholar
• 63  Champion GA, Neely MN, Brennan MA, DiRita VJ: A branch in the ToxR regulatory cascade of Vibrio cholerae revealed by characterization of toxT mutant strains. Mol. Microbiol.23(2),323–331 (1997).
  Medline CASGoogle Scholar
• 64  Withey JH, DiRita VJ: The toxbox: specific DNA sequence requirements for activation of Vibrio cholerae virulence genes by ToxT. Mol. Microbiol.59(6),1779–1789 (2006).
  Medline CASGoogle Scholar
• 65  Hsiao A, Liu Z, Joelsson A, Zhu J: Vibrio cholerae virulence regulator-coordinated evasion of host immunity. Proc. Natl Acad. Sci. USA103(39),14542–14547 (2006).
  Medline CASGoogle Scholar
• 66  Prouty MG, Osorio CR, Klose KE: Characterization of functional domains of the Vibrio cholerae virulence regulator ToxT. Mol. Microbiol.58(4),1143–1156 (2005).
  Medline CASGoogle Scholar
• 67  Childers BM, Weber GG, Prouty MG, Castaneda MM, Peng F, Klose KE: Identification of residues critical for the function of the Vibrio cholerae virulence regulator ToxT by scanning alanine mutagenesis. J. Mol. Biol.367(5),1413–1430 (2007).
  Medline CASGoogle Scholar
• 68  Hung DT, Shakhnovich EA, Pierson E, Mekalanos JJ: Small-molecule inhibitor of Vibrio cholerae virulence and intestinal colonization. Science310(5748),670–674 (2005).
  Medline CASGoogle Scholar
• 69  Shakhnovich EA, Hung DT, Pierson E, Lee K, Mekalanos JJ: Virstatin inhibits dimerization of the transcriptional activator ToxT. Proc. Natl Acad. Sci. USA104(7),2372–2377 (2007).
  Medline CASGoogle Scholar
• 70  Schuhmacher DA, Klose KE: Environmental signals modulate ToxT-dependent virulence factor expression in Vibrio cholerae. J. Bacteriol.181(5),1508–1514 (1999).
  Medline CASGoogle Scholar
• 71  Gupta S, Chowdhury R: Bile affects production of virulence factors and motility of Vibrio cholerae. Infect. Immun.65(3),1131–1134 (1997).
  Medline CASGoogle Scholar
• 72  Lee SH, Hava DL, Waldor MK, Camilli A: Regulation and temporal expression patterns of Vibrio cholerae virulence genes during infection. Cell99(6),625–634 (1999).
  Medline CASGoogle Scholar
• 73  Tischler AD, Camilli A: Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol. Microbiol.53(3),857–869 (2004).
  Medline CASGoogle Scholar
• 74  Tischler AD, Camilli A: Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect. Immun.73(9),5873–5882 (2005).
  Medline CASGoogle Scholar
• 75  Hase CC, Mekalanos JJ: TcpP protein is a positive regulator of virulence gene expression in Vibrio cholerae. Proc. Natl Acad. Sci. USA95(2),730–734 (1998).
  Medline CASGoogle Scholar
• 76  Krukonis ES, Yu RR, Dirita VJ: The Vibrio cholerae ToxR/TcpP/ToxT virulence cascade: distinct roles for two membrane-localized transcriptional activators on a single promoter. Mol. Microbiol.38(1),67–84 (2000).
  Medline CASGoogle Scholar
• 77  Miller VL, Taylor RK, Mekalanos JJ: Cholera toxin transcriptional activator toxR is a transmembrane DNA binding protein. Cell48(2),271–279 (1987).
  MedlineGoogle Scholar
• 78  Martinez-Hackert E, Stock AM: Structural relationships in the OmpR family of winged-helix transcription factors. J. Mol. Biol.269(3),301–312 (1997).
  Medline CASGoogle Scholar
• 79  Murley YM, Carroll PA, Skorupski K, Taylor RK, Calderwood SB: Differential transcription of the tcpPH operon confers biotype-specific control of the Vibrio cholerae ToxR virulence regulon. Infect. Immun.67(10),5117–5123 (1999).
  Medline CASGoogle Scholar
• 80  Krukonis ES, DiRita VJ: DNA binding and ToxR responsiveness by the wing domain of TcpP, an activator of virulence gene expression in Vibrio cholerae. Mol. Cell12(1),157–165 (2003).
  Medline CASGoogle Scholar
• 81  Crawford JA, Krukonis ES, DiRita VJ: Membrane localization of the ToxR winged-helix domain is required for TcpP-mediated virulence gene activation in Vibrio cholerae. Mol. Microbiol.47(5),1459–1473 (2003).
  Medline CASGoogle Scholar
• 82  DiRita VJ, Mekalanos JJ: Periplasmic interaction between two membrane regulatory proteins, ToxR and ToxS, results in signal transduction and transcriptional activation. Cell64(1),29–37 (1991).
  Medline CASGoogle Scholar
• 83  Pfau JD, Taylor RK: Mutations in toxR and toxS that separate transcriptional activation from DNA binding at the cholera toxin gene promoter. J. Bacteriol.180(17),4724–4733 (1998).
  Medline CASGoogle Scholar
• 84  Beck NA, Krukonis ES, DiRita VJ: TcpH influences virulence gene expression in Vibrio cholerae by inhibiting degradation of the transcription activator TcpP. J. Bacteriol.186(24),8309–8316 (2004).
  Medline CASGoogle Scholar
• 85  Matson JS, DiRita VJ: Degradation of the membrane-localized virulence activator TcpP by the YaeL protease in Vibrio cholerae. Proc. Natl Acad. Sci. USA102(45),16403–16408 (2005).
  Medline CASGoogle Scholar
• 86  Carroll PA, Tashima KT, Rogers MB, DiRita VJ, Calderwood SB: Phase variation in tcpH modulates expression of the ToxR regulon in Vibrio cholerae. Mol. Microbiol.25(6),1099–1111 (1997).
  Medline CASGoogle Scholar
• 87  DiRita VJ: Co-ordinate expression of virulence genes by ToxR in Vibrio cholerae. Mol. Microbiol.6(4),451–458 (1992).
  Medline CASGoogle Scholar
• 88  Lin Z, Kumagai K, Baba K, Mekalanos JJ, Nishibuchi M: Vibrio parahaemolyticus has a homolog of the Vibrio cholerae toxRS operon that mediates environmentally induced regulation of the thermostable direct hemolysin gene. J. Bacteriol.175(12),3844–3855 (1993).
  Medline CASGoogle Scholar
• 89  Reich KA, Schoolnik GK: The light organ symbiont Vibrio fischeri possesses a homolog of the Vibrio cholerae transmembrane transcriptional activator ToxR. J. Bacteriol.176(10),3085–3088 (1994).
  Medline CASGoogle Scholar
• 90  Provenzano D, Lauriano CM, Klose KE: Characterization of the role of the ToxR-modulated outer membrane porins OmpU and OmpT in Vibrio cholerae virulence. J. Bacteriol.183(12),3652–3662 (2001).
  Medline CASGoogle Scholar
• 91  Provenzano D, Klose KE: 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. USA97(18),10220–10224 (2000).
  Medline CASGoogle Scholar
• 92  Miller VL, Mekalanos JJ: 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(6),2575–2583 (1988).
  Medline CASGoogle Scholar
• 93  Crawford JA, Kaper JB, DiRita VJ: Analysis of ToxR-dependent transcription activation of ompU, the gene encoding a major envelope protein in Vibrio cholerae. Mol. Microbiol.29(1),235–246 (1998).
  Medline CASGoogle Scholar
• 94  Li CC, Merrell DS, Camilli A, Kaper JB: ToxR interferes with CRP-dependent transcriptional activation of ompT in Vibrio cholerae. Mol. Microbiol.43(6),1577–1589 (2002).
  Medline CASGoogle Scholar
• 95  Simonet VC, Basle A, Klose KE, Delcour AH: The Vibrio cholerae porins OmpU and OmpT have distinct channel properties. J. Biol. Chem.278(19),17539–17545 (2003).
  Medline CASGoogle Scholar
• 96  Duret G, Delcour AH: Deoxycholic acid blocks Vibrio cholerae OmpT but not OmpU porin. J. Biol. Chem.281(29),19899–19905 (2006).
  Medline CASGoogle Scholar
• 97  Merrell DS, Bailey C, Kaper JB, Camilli A: The ToxR-mediated organic acid tolerance response of Vibrio cholerae requires OmpU. J. Bacteriol.183(9),2746–2754 (2001).
  Medline CASGoogle Scholar
• 98  Mathur J, Waldor MK: The Vibrio cholerae ToxR-regulated porin OmpU confers resistance to antimicrobial peptides. Infect. Immun.72(6),3577–3583 (2004).
  Medline CASGoogle Scholar
• 99  Mathur J, Davis BM, Waldor MK: Antimicrobial peptides activate the Vibrio choleraesigma regulon through an OmpU-dependent signalling pathway. Mol. Microbiol. (2007).
  MedlineGoogle Scholar
• 100  Hung DT, Mekalanos JJ: Bile acids induce cholera toxin expression in Vibrio cholerae in a ToxT-independent manner. Proc.  Natl Acad. Sci. USA102(8),3028–3033 (2005).
  Medline CASGoogle Scholar
• 101  Skorupski K, Taylor RK: A new level in the Vibrio cholerae ToxR virulence cascade: AphA is required for transcriptional activation of the tcpPH operon. Mol. Microbiol.31(3),763–771 (1999).
  Medline CASGoogle Scholar
• 102  Kovacikova G, Skorupski K: A Vibrio cholerae LysR homolog, AphB, cooperates with AphA at the tcpPH promoter to activate expression of the ToxR virulence cascade. J. Bacteriol.181(14),4250–4256 (1999).
  Medline CASGoogle Scholar
• 103  De Silva RS, Kovacikova G, Lin W, Taylor RK, Skorupski K, Kull FJ: Crystal structure of the virulence gene activator AphA from Vibrio cholerae reveals it is a novel member of the winged helix transcription factor superfamily. J. Biol. Chem.280(14),13779–13783 (2005).
  Medline CASGoogle Scholar
• 104  Kovacikova G, Lin W, Skorupski K: 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(1),129–142 (2004).
  Medline CASGoogle Scholar
• 105  Kovacikova G, Skorupski K: Differential activation of the tcpPH promoter by AphB determines biotype specificity of virulence gene expression in Vibrio cholerae. J. Bacteriol.182(11),3228–3238 (2000).
  Medline CASGoogle Scholar
• 106  Kovacikova G, Skorupski K: Regulation of virulence gene expression in Vibrio cholerae by quorum sensing: HapR functions at the aphA promoter. Mol. Microbiol.46(4),1135–1147 (2002).
  Medline CASGoogle Scholar
• 107  Kovacikova G, Skorupski K: Overlapping binding sites for the virulence gene regulators AphA, AphB and cAMP-CRP at the Vibrio cholerae tcpPH promoter. Mol. Microbiol.41(2),393–407 (2001).
  Medline CASGoogle Scholar
• 108  Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL, Mekalanos JJ: Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc. Natl Acad. Sci. USA99(5),3129–3134 (2002).
  Medline CASGoogle Scholar
• 109  Miller MB, Skorupski K, Lenz DH, Taylor RK, Bassler BL: Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell110(3),303–314 (2002).
  Google Scholar
• 110  Lilley BN, Bassler BL: Regulation of quorum sensing in Vibrio harveyi by LuxO and sigma-54. Mol. Microbiol.36(4),940–954 (2000).
  Medline CASGoogle Scholar
• 111  Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, Bassler BL: The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell118(1), 69–82 (2004).
  Google Scholar
• 112  Lenz DH, Miller MB, Zhu J, Kulkarni RV, Bassler BL: CsrA and three redundant small RNAs regulate quorum sensing in Vibrio cholerae. Mol. Microbiol.58(4),1186–202 (2005).
  Medline CASGoogle Scholar
• 113  Kovacikova G, Lin W, Skorupski K: 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(2),420–433 (2005).
  Medline CASGoogle Scholar
• 114  Kovacikova G, Lin W, Skorupski K: The virulence activator AphA links quorum sensing to pathogenesis and physiology in Vibrio cholerae by repressing the expression of a penicillin amidase gene on the small chromosome. J. Bacteriol.185(16),4825–4836 (2003).
  Medline CASGoogle Scholar
• 115  Skorupski K, Taylor RK: Cyclic AMP and its receptor protein negatively regulate the coordinate expression of cholera toxin and toxin-coregulated pilus in Vibrio cholerae. Proc. Natl Acad. Sci. USA94(1),265–270 (1997).
  Medline CASGoogle Scholar