Cholera toxin expression by El Tor Vibrio cholerae in shallow culture growth conditions

Microbial Pathogenesis

Volumn 66, Issue , 2014, Pages 5-13

  Cobaxin, Mayra ^a   Martínez, Haydee ^a   Ayala, Guadalupe ^b   Holmgren, Jan ^c   Sjöling, Åsa ^c   Sánchez, Joaquín ^a  

^a UNIVERSIDAD AUTÓNOMA DEL ESTADO DE MORELOS   (Mexico)

^b INSTITUTO NACIONAL DE SALUD PÚBLICA   (Mexico)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

El Tor vibrios; Endogenous bicarbonate; Low oxygen and AphB regulation; Model for cholera toxin expression; Shallow cultures; ToxT regulator

Indexed keywords

BICARBONATE; CARBON DIOXIDE; CHOLERA TOXIN; DISSOLVED OXYGEN;

ANAEROBIC GROWTH; APHB GENE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIOSTASIS; BACTERIUM CULTURE; CONTROLLED STUDY; CTXAB GENE; GENE ACTIVATION; GENE SYNTHESIS; NONHUMAN; OZONE DEPLETION; PH; PRIORITY JOURNAL; TCPP GENE; TOXT GENE; VIBRIO CHOLERAE;

VIBRIO CHOLERAE;

EL TOR VIBRIOS; ENDOGENOUS BICARBONATE; LOW OXYGEN AND APHB REGULATION; MODEL FOR CHOLERA TOXIN EXPRESSION; SHALLOW CULTURES; TOXT REGULATOR;

BACTERIAL PROTEINS; CARBON DIOXIDE; CHOLERA TOXIN; CULTURE MEDIA; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN-ION CONCENTRATION; OXYGEN; VIBRIO CHOLERAE;

EID: 84888427472     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2013.11.002     Document Type: Article

References (76)

1. De S.N., Chatterje D.N. An experimental study of the mechanism of action of Vibrio cholerae on the intestinal mucous membrane. JPathol Bacteriol 1953, 66:559-562.
2. Finkelstein R.A. Cholera enterotoxin (choleragen): a historical perspective. Cholera 1992, 155-187. Plenum Medical Book Company, New York. D. Barua, W.B. Greenough (Eds.).
3. Kaper J.B., Morris J.G., Levine M.M. Cholera. Clin Microbiol Rev 1995, 8:48-86.
4. Miller M.B., Bassler B.L. Quorum sensing in bacteria. Annu Rev Microbiol 2001, 55:165-199.
5. Sánchez J., Holmgren J. Cholera toxin-a foe & a friend. Indian J Med Res 2011, 133:153-163.
6. Gill D.M. The arrangement of subunits in cholera toxin. Biochemistry 1976, 15:1242-1248.
7. Lönnroth I., Holmgren J. Subunit structure of cholera toxin. JGen Microbiol 1973, 76:417-427.
8. Waldor M.K., Mekalanos J.J. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 1996, 272:1910-1914.
9. Fando R., Pérez J., Rodríguez B., Campos J., Robert A., García L., et al. Promoter activities in Vibrio cholerae ctxφ prophage. Infect Immun 1997, 65:1561-1565.
10. DiRita V.J., Parsot C., Jander G., Mekalanos J.J. Regulatory cascade controls virulence in Vibrio cholerae. Proc Natl Acad Sci U S A 1991, 88:5403-5407.
11. Matson J.S., Withey J.H., DiRita V.J. Regulatory networks controlling Vibrio cholerae virulence gene expression. Infect Immun 2007, 75:5542-5549.
12. Miller M.B., Skorupski K., Lenz D.H., Taylor R.K., Bassler B.L. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 2002, 110:303-304.
13. Ng W.L., Bassler B.L. Bacterial quorum-sensing network architectures. Annu Rev Genet 2009, 43:197-222.
14. Cámara M.A., Hardman A., Williams P., Milton D. Quorum sensing in Vibrio cholerae. Nat Genet 2002, 32:217-218.
15. Jobling M.G., Holmes R.K. Characterization of hapR, a positive regulator of the Vibrio cholerae HA/protease gene hap, and its identification as a functional homologue of the Vibrio harveyi luxR gene. Mol Microbiol 1997, 26:1023-1034.
16. Zhu J., Miller M.B., Vance R.E., Dziejman M., Bassler B.L., Mekalanos J.J. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci U S A 2002, 99:3129-3134.
17. Bassler B.L., Greenberg E.P., Stevens A.M. Cross-species induction of luminescence in the quorum-sensing bacterium Vibrio harveyi. JBacteriol 1997, 179:4043-4045.
18. Higgins D.A., Pomianek M.E., Kraml C.M., Taylor R.K., Semmelhack M.F., Bassler B.L. The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature 2007, 450:883-886.
19. Kovacikova G., Skorupski K. Regulation of virulence gene expression in Vibrio cholerae by quorum sensing: HapR functions at the aphA promoter. Mol Microbiol 2002, 46:1135-1147.
20. Joelsson A., Liu Z., Zhu J. Genetic and phenotypic diversity of quorum-sensing systems in clinical and environmental isolates of Vibrio cholerae. Infect Immun 2006, 74:1141-1147.
21. Hammer B.K., Bassler B.L. Regulatory small RNAs circumvent the conventional quorum sensing pathway in pandemic Vibrio cholerae. Proc Natl Acad Sci U S A 2007, 104:11145-11149.
22. Lenz D.H., Mok K.C., Lilley B.N., Kulkarni R.V., Wingreen N.S., Bassler B.L. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 2004, 118:69-82.
23. Lin W., Kovacikova G., Skorupski K. Requirements for Vibrio cholerae HapR binding and transcriptional repression at the hapR promoter are distinct from those at the aphA promoter. JBacteriol 2005, 187:3013-3019.
24. Skorupski K., Taylor R.K. Anew level in the Vibrio cholerae ToxR virulence cascade: AphA is required for transcriptional activation of the tcpPH operon. Mol Microbiol 1999, 31:763-771.
25. De Silva R.S., Kovacikova G., Lin W., Taylor R.K., Skorupski K., Kull F.J. Crystal structure of the virulence gene activator AphA from Vibrio cholerae reveals it is a novel member of the winged helix transcription factor superfamily. JBiol Chem 2005, 280:13779-13783.
26. Kovacikova G., Skorupski K. AVibrio cholerae LysR homolog AphB cooperates with AphA at the tcpPH promoter to activate expression of the ToxR virulence cascade. JBacteriol 1999, 181:4250-4256.
27. 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 2004, 53:129-142.
28. Kovacikova G., Lin W., Skorupski K. The LysR-type virulence activator AphB regulates the expression of genes in Vibrio cholerae in response to low pH and anaerobiosis. JBacteriol 2010, 192:4181-4191.
29. Liu Z., Yang M., Peterfreund G.L., Tsou A.M., Selamoglu N., Daldal F., et al. Vibrio cholerae anaerobic induction of virulence gene expression is controlled by thiol-based switches of virulence regulator AphB. Proc Natl Acad Sci U S A 2011, 108:810-815.
30. Taylor J.L., De Silva R.S., Kovacikova G., Lin W., Taylor R.K., Skorupski K., et al. The crystal structure of AphB, a virulence gene activator from Vibrio cholerae, reveals residues that influence its response to oxygen and pH. Mol Microbiol 2012, 83:457-470.
31. Häse C.C., Mekalanos J.J. TcpP protein is a positive regulator of virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci U S A 1998, 95:730-734.
32. Krukonis E.S., Yu R.R., DiRita V.J. The Vibrio cholerae ToxR/TcpP/ToxT virulence cascade: distinct roles for two membrane-localized transcriptional activators on a single promoter. Mol Microbiol 2000, 38:67-84.
33. Carroll P.A., Tashima K.T., Rogers M.B., DiRita V.J., Calderwood S.B. Phase variation in tcpH modulates expression of the ToxR regulon in Vibrio cholerae. Mol Microbiol 1997, 25:1099-1111.
34. Goss T.J., Seaborn C.P., Gray M.D., Krukonis E.S. Identification of the TcpP-binding site in the toxT promoter of Vibrio cholerae and the role of ToxR in TcpP-mediated activation. Infect Immun 2010, 78:4122-4133.
35. Higgins D.E., DiRita V.J. Transcriptional control of toxT, a regulatory gene in the ToxR regulon of Vibrio cholerae. Mol Microbiol 1994, 14:17-29.
36. Miller V.L., Mekalanos J.J. Synthesis of cholera toxin is positively regulated at the transcriptional level by ToxR. Proc Natl Acad Sci U S A 1984, 81:3471-3475.
37. Miller V.L., Taylor R.K., Mekalanos J.J. Cholera toxin transcriptional activator ToxR is a transmembrane DNA binding protein. Cell 1987, 48:271-279.
38. Miller V.L., DiRita V.J., Mekalanos J.J. Identification of toxS, a regulatory gene whose product enhances toxR-mediated activation of the cholera toxin promoter. JBacteriol 1989, 171:1288-1293.
39. Goss T.J., Morgan S.J., French E.L., Krukonis E.S. ToxR recognizes a direct repeat element in the toxT, ompU, ompT, and ctxA promoters of Vibrio cholerae to regulate transcription. Infect Immun 2013, 81:884-895.
40. Champion G.A., Neely M.N., Brennan M.A., DiRita V.J. Abranch in the ToxR regulatory cascade of Vibrio cholerae revealed by characterization of toxT mutant strains. Mol Microbiol 1997, 23:323-331.
41. Hung D.T., Mekalanos J.J. Bile acids induce cholera toxin expression in Vibrio cholerae in a ToxT-independent manner. Proc Natl Acad Sci U S A 2005, 102:3028-3033.
42. Lee S.H., Hava D.L., Waldor M.K., Camilli A. Regulation and temporal expression patterns of Vibrio cholerae virulence genes during infection. Cell 1999, 99:625-634.
43. Higgins D.E., Nazareno E., DiRita V.J. The virulence gene activator ToxT from Vibrio cholerae is a member of the AraC family of transcriptional activators. JBacteriol 1992, 174:6974-6980.
44. Lowden M.J., Skorupski K., Pellegrini M., Chiorazzo M.G., Taylor R.K., Kull J.F. Structure of Vibrio cholerae ToxT reveals a mechanism for fatty acid regulation of virulence genes. Proc Natl Acad Sci U S A 2010, 107:2860-2865.
45. Hulbert R.R., Taylor R.K. Mechanism of ToxT-dependent transcriptional activation at the Vibrio cholerae tcpA Promoter. JBacteriol 2002, 184:5533-5544.
46. Withey J.H., DiRita V.J. The toxbox: specific DNA sequence requirements for activation of Vibrio cholerae virulence genes by ToxT. Mol Microbiol 2006, 59:1779-1789.
47. Withey J.H., DiRita V.J. Activation of both acfA and acfD transcription by Vibrio cholerae ToxT requires binding to two centrally located DNA sites in an inverted repeat conformation. Mol Microbiol 2005, 56:1062-1077.
48. Bellair M., Withey J.H. Flexibility of Vibrio cholerae ToxT in transcription activation of genes having altered promoter spacing. JBacteriol 2008, 190:7925-7931.
49. Prouty M.G., Osorio C.R., Klose K.E. Characterization of functional domains of the Vibrio cholerae virulence regulator ToxT. Mol Microbiol 2005, 58:1143-1156.
50. Childers B.M., Weber G.G., Prouty M.G., Castaneda M.M., Peng F., Klose K.E. Identification of residues critical for the function of the Vibrio cholerae virulence regulator ToxT by scanning alanine mutagenesis. JMol Biol 2007, 367:1413-1430.
51. Dittmer J.B., Withey J.H. Identification and characterization of the functional toxboxes in the Vibrio cholerae cholera toxin promoter. JBacteriol 2012, 194:5255-5256.
52. Shakhnovich E.A., Hung D.T., Pierson E., Lee K., Mekalanos J.J. Virstatin inhibits dimerization of the transcriptional activator ToxT. Proc Natl Acad Sci U S A 2007, 104:2372-2377.
53. Nye M.B., Pfau J.D., Skorupski K., Taylor R.K. Vibrio cholerae H-NS silences virulence gene expression at multiple steps in the ToxR regulatory cascade. JBacteriol 2000, 182:4295-4303.
54. Stonehouse E.A., Hulbert R.R., Nye M.B., Skorupski K., Taylor R.K. H-NS binding and repression of the ctx promoter in Vibrio cholerae. JBacteriol 2011, 193:979-988.
55. Yu R.R., DiRita V.J. Regulation of gene expression in Vibrio cholerae by ToxT involves both antirepression and RNA polymerase stimulation. Mol Microbiol 2002, 43:119-134.
56. Yu R.R., DiRita V.J. Analysis of an autoregulatory loop controlling ToxT, cholera toxin, and toxin-coregulated pilus production in Vibrio cholerae. JBacteriol 1999, 181:2584-2592.
57. Chatterjee A.P., Dutta K., Chowdhury R. Effect of fatty acids and cholesterol present in bile on expression of virulence factors and motility of Vibrio cholerae. Infect Immun 2007, 75:1946-1953.
58. Abuaita B.H., Withey J.H. Bicarbonate induces Vibrio cholerae virulence gene expression by enhancing ToxT activity. Infect Immun 2009, 77:4111-4120.
59. Nielsen A.T., Dolganov N.A., Rasmussen T., Otto G., Miller M.C., Felt S.A., et al. Abistable switch and anatomical site control Vibrio cholerae virulence gene expression in the intestine. PLoS Pathog 2010, 6:e1001102.
60. Iwanaga M., Yamamoto K. New medium for the production of cholera toxin by Vibrio cholerae O1 biotype El Tor. JClin Microbiol 1985, 22:405-408.
61. Iwanaga M., Yamamoto K., Higa N., Ichinose Y., Nakasone N., Tanabe M. Culture conditions for stimulating cholera toxin production by Vibrio cholerae O1 El Tor. Microbiol Immunol 1986, 30:1075-1083.
62. Iwanaga M., Kuyyakanond T. Large production of cholera toxin by Vibrio cholerae O1 in yeast extract peptone water. JClin Microbiol 1987, 25:2314-2316.
63. DiRita V.J., Neely M., Taylor R.K., Bruss P.M. Differential expression of ToxR regulon in classical and El Tor biotypes of Vibrio cholerae is due to biotype-specific control over ToxT expression. Proc Natl Acad Sci U S A 1996, 93:7991-7995.
64. Gardel C.L., Mekalanos J.J. Regulation of cholera toxin by temperature, pH, and osmolarity. Methods Enzymol 1994, 235:517-526.
65. Murley Y.M., Carroll P.A., Skorupski K., Taylor R.K., Calderwood S.B. Differential transcription of the tcpPH operon confers biotype-specific control of the Vibrio cholerae ToxR virulence regulon. Infect Immun 1999, 67:5117-5123.
66. Murley Y.M., Behari J., Griffin R., Calderwood S.B. Classical and El Tor biotypes of Vibrio cholerae differ in timing of transcription of tcpPH during growth in inducing conditions. Infect Immun 2000, 68:3010-3014.
67. Kovacikova G., Skorupski K. Differential activation of the tcpPH promoter by AphB determines biotype specificity of virulence gene expression in Vibrio cholerae. JBacteriol 2000, 182:3228-3238.
68. Kovacikova G., Skorupski K. Binding site requirements of the gene regulator AphB: differential affinities for the Vibrio cholerae classical and El Tor tcpPH promoters. Mol Microbiol 2002, 44:533-547.
69. Sánchez J., Medina G., Buhse T., Holmgren J., Soberon-Chavez G. Expression of cholera toxin under non-AKI conditions in Vibrio cholerae El Tor induced by increasing the exposed surface of cultures. JBacteriol 2004, 186:1355-1361.
70. Craig J.P., Yamamoto K., Takeda Y., Miwatani T. Production of cholera-like enterotoxin by a Vibrio cholerae non-O1 strain isolated from the environment. Infect Immun 1981, 34:90-97.
71. Svennerholm A.M., Holmgren J. Identification of Escherichia coli heat-labile enterotoxin by means of a ganglioside immunosorbent assay (GM1-ELISA) procedure. Curr Microbiol 1978, 1:19-23.
72. Medrano A.I., DiRita V.J., Castillo G., Sánchez J. Transient transcriptional activation of the Vibrio cholerae El Tor virulence regulator ToxT in response to culture conditions. Infect Immun 1999, 67:2178-2183.
73. 2 may inhibit bacterial growth and induce virulence gene expression in enteropathogenic Escherichia coli. Microb Pathog 2012, 53:49-55.
74. Kolter R., Siegele D.A., Tormo A. The stationary phase of the bacterial life cycle. Annu Rev Microbiol 1993, 47:855-874.
75. Navarro-Llorens J.M., Tormo A., Martínez-García E. Stationary phase in gram-negative bacteria. FEMS Microbiol Rev 2010, 34:476-495.
76. Casey J.R. Why bicarbonate?. Biochem Cell Biol 2006, 84:930-939.