Role of the histone-like nucleoid structuring protein in the regulation of rpoS and RpoS-dependent genes in Vibrio cholerae

Journal of Bacteriology

Volumn 190, Issue 22, 2008, Pages 7335-7345

  Silva, Anisia J ^a   Sultan, Syed Zafar ^a   Liang, Weili ^b   Benitez, Jorge A ^a  

^a MOREHOUSE SCHOOL OF MEDICINE   (United States)

^b CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLERA TOXIN; HISTONE LIKE NUCLEOID STRUCTURING PROTEIN; HYDROGEN PEROXIDE; MESSENGER RNA; PROTEINASE; SIGMA FACTOR RPOS;

ALLELE; ARTICLE; BIOTYPE; ESCHERICHIA COLI; GENE DELETION; GENE EXPRESSION; OSMOLARITY; PH MEASUREMENT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIBRIO CHOLERAE; VIRULENCE; WILD TYPE;

BACTERIAL PROTEINS; CHEMOTAXIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; MUTAGENESIS, INSERTIONAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE DELETION; SIGMA FACTOR; SIGNAL TRANSDUCTION; VIBRIO CHOLERAE;

ESCHERICHIA COLI; ORYCTOLAGUS CUNICULUS; VIBRIO CHOLERAE;

EID: 55549106104     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00360-08     Document Type: Article

References (64)

1. Atlung, T., and H. Ingmer. 1997. H-NS: a modulator of environmentally regulated gene expression. Mol. Microbiol. 24:7-17.
2. Becker, G., E. Klauck, and R. Hengge-Aronis. 1999. Regulation of RpoS proteolysis in Escherichia coli: the response regulator RssB is a recognition factor that interacts with the turnover element in RpoS. Proc. Natl. Acad. Sci. USA 96:6439-6444.
3. Benitez, J. A., A. J. Silva, and R. A. Finkelstein. 2001. Environmental signals controlling production of hemagglutinin/protease in Vibrio cholerae. Infect. Immun. 69:6549-6553.
4. Benítez, J. A., L. Garcia, A. J. Silva, H. Garcia, R. Fando, B. Cedre, A. Perez, J. Campos, B. L. Rodriguez, J. L. Perez, T. Valmaseda, O. Perez, A. Perez, M. Ramirez, T. Ledon, M. Diaz, M. Lastre, L. Bravo, and G. Sierra. 1999. Preliminary assessment of the safety and immunogenicity of a new CTXφ-negative hemagglutinin/protease-defective El Tor strain as a cholera vaccine candidate. Infect. Immun. 67:539-545.
5. Boin, M. A., M. J. Austin, and C. C. Hase. 2004. Chemotaxis in Vibrio cholerae. FEMS Microbiol. Lett. 239:1-8.
6. Brescia, C. C., M. K. Kaw, and D. D. Sledjeski. 2004. The DNA binding protein H-NS binds to and alters the stability of RNA in vitro and in vivo. J. Mol. Biol. 339:505-514.
7. Brosius, J., A. Ullrich, M. A. Raker, A. Gray, T. J. Dull, R. R. Gutell, and H. F. Noller. 1981. Construction and fine mapping of recombinant plasmids containing the rrnB ribosomal RNA operon of E. coli. Plasmid 6:112-118.
8. Chiang, S. L., R. K. Taylor, M. Koomey, and J. J. Mekalanos. 1995. Single amino acid substitutions in the N-terminus of Vibrio cholerae TcpA affect colonization, autoagglutination, and serum resistance. Mol. Microbiol. 17:1133-1142.
9. q/Ptrp-lac plasmids and transposons that confer conditional phenotypes. Gene 123:17-24.
10. Ding, Y., B. M. Davis, and M. K. Waldor. 2004. Hfq is essential for Vibrio cholerae virulence and down regulates sigma expression. Mol. Microbiol. 53:345-354.
11. Donnenberg, M. S., and J. B. Kaper. 1991. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive selection suicide vector. Infect. Immun. 59:4310-4317.
12. Dorman, C. 2004. H-NS: a universal regulator for a dynamic genome. Nat. Rev. Microbiol. 2:391-400.
13. Finkelstein, R. A. 1992. Cholera enterotoxin (choleragen): a historical perspective, p. 155-187. In D. Barua and W. B. Greenough (ed.), Cholera. Plenum Medical Book Company, New York, NY.
14. Finkelstein, R. A., M. Boesman-Finkelstein, and P. Holt. 1983. Vibrio cholerae hemagglutinin/lectin/protease hydrolyzes fibronectin and ovomucin: F.M. Burnet revisited. Proc. Natl. Acad. Sci. USA 80:1092-1095.
15. García, L., M. D. Jidy, H. Garcia, B. L. Rodriguez, R. Fernández, G. Ano, B. Cedre, T. Valmaseda, E. Suzarte, M. Ramirez, Y. Pino, J. Campos, J. Menéndez, R. Valera, D. González, I. González, O. Perez, T. Serrano, M. Lastre, F. Miralles, J. Del Campo, J. L. Maestre, J. L. Perez, A. Talavera, A. Perez, K. Marrero, T. Ledon, and R. Fando. 2005. The vaccine candidate Vibrio cholerae 638 is protective against cholera in healthy volunteers. Infect. Immun. 73:3018-3024.
16. Ghosh, A., K. Paul, and R. Chowdhury. 2006. Role of the histone-like nucleoid structuring protein in colonization, motility, and bile-dependent repression of virulence gene expression in Vibrio cholerae. Infect. Immun. 74:3060-3064.
17. Gosink, K. K., R. Kobayashi, I. Kawagishi, and C. C. Häse. 2002. Analysis of the role of the three cheA homologs in chemotaxis of Vibrio cholerae. J. Bacteriol. 184:1767-1771.
18. Häse, C. C., and R. A. Finkelstein. 1991. Cloning and nucleotide sequence of the Vibrio cholerae hemagglutinin/protease (HA/protease) gene and construction of an HA/protease-negative strain. J. Bacteriol. 173:3311-3317.
19. S (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev. 66:373-395.
20. S-selective? Curr. Opin. Microbiol. 5:591-595.
21. Hommais, F., E. Krin, C. Laurent-Winter, O. Soutourina, A. Malpertuy, J.-P. Le Caer, A. Danchin, and P. Bertin. 2001. Large-scale monitoring of pleiotropic regulation of gene expression by the prokaryotic nucleoid-associated protein, H-NS. Mol. Microbiol. 40:20-36.
22. Hyakutake, A., M. Homma, M. J. Austin, M. A. Boin, C. C. Häse, and I. Kawagishi. 2005. Only one of the five CheY homologs in Vibrio cholerae directly switches flagellar rotation. J. Bacteriol. 187:8403-8410.
23. 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.
24. Jahid, I. K., A. J. Silva, and J. A. Benitez. 2006. Polyphosphate stores enhance the ability of Vibrio cholerae to overcome environmental stresses in a low-phosphate environment. Appl. Environ. Microbiol. 72:7043-7049.
25. Jobling, M. G., and R. K. Holmes. 1997. 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. 26:1023-1034.
26. Johansson, J., B. Dagberg, E. Richet, and B. E. Uhlin. 1998. H-NS and StpA proteins stimulate expression of the maltose regulon in Escherichia coli. J. Bacteriol. 180:6117-6125.
27. Kaper, J. B., G. Morris, Jr., and M. M. Levine. 1995. Cholera. Clin. Microbiol. Rev. 8:48-86.
28. Klose, K. E., and J. J. Mekalanos. 1998. Differential expression of multiple flagellins in Vibrio cholerae. J. Bacteriol. 180:303-316.
29. Kovacikova, G., and K. Skorupski. 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.
30. Krishnan, H. H., A. Ghosh, K. Paul, and R. Chowdhury. 2004. Effect of anaerobiosis on expression of virulence factors in Vibrio cholerae. Infect. Immun. 72:3961-3967.
31. Liang, W., A. Pascual-Montano, A. J. Silva, and J. A. Benitez. 2007. The cyclic AMP receptor protein modulates quorum sensing, motility and multiple genes that affect intestinal colonization in Vibrio cholerae. Microbiology 153:2964-2975.
32. Majdalani, N., S. Chen, J. Murrow, K. St. John, and S. Gottesman. 2001. Regulation of RpoS by a novel small RNA: the characterization of RprA. Mol. Microbiol. 39:1382-1394.
33. Marcus, H., J. M. Ketley, J. B. Kaper, and R. K. Holmes. 1990. Effect of DNase production, plasmid size, and restriction barriers on transformation of Vibrio cholerae by electroporation and osmotic shock. FEMS Microbiol. Lett. 56:149-154.
34. Mel, S. F., K. J. Fullner, S. Wimer-Mackin, W. L. Lencer, and J. J. Mekalanos. 2000. Association of protease activity in Vibrio cholerae vaccine strains with decrease in transcellular epithelial resistance of polarized T84 intestinal cells. Infect. Immun. 68:6487-6492.
35. Merrell, D. S., C. Bailey, J. B. Kaper, and A. Camilli. 2001. The ToxR-mediated organic acid tolerance response of Vibrio cholerae requires OmpU. J. Bacteriol. 183:2746-2754.
36. Merrell, D. S., and A. Camilli. 1999. The cadA gene of Vibrio cholerae is induced during infection and plays a role in acid tolerance. Mol. Microbiol. 34:836-849.
37. Merrell, D. S., and A. Camilli. 2002. Acid tolerance of gastrointestinal pathogens. Curr. Opin. Microbiol. 5:51-55.
38. Merrell, D. S., D. L. Hava, and A. Camilli. 2002. Identification of novel factors involved in colonization and acid tolerance of Vibrio cholerae. Mol. Microbiol. 43:1471-1491.
39. Merrell, D. S., A. D. Tischler, S. H. Lee, and A. Camilli. 2000. Vibrio cholerae requires rpoS for efficient intestinal colonization. Infect. Immun. 68:6691-6696.
40. Miller, J. H. 1971. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. Miller, M. B., K. Skorupski, D. H. Lenz, R. K. Taylor, and B. L. Bassler. 2002. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110:303-314.
42. Nielsen, A. T., N. A. Dolganov, G. Otto, M. C. Miller, C. Y. Wu, and G. K. Schoolnik. 2006. RpoS controls the Vibrio cholerae mucosal escape response. PLoS Pathog. 2:e109.
43. Nogueira, T., and M. Springer. 2000. Post-transcriptional control by global regulators of gene expression in bacteria. Curr. Opin. Microbiol. 3:154-158.
44. Nye, M. B., and R. K. Taylor. 2003. Vibrio cholerae H-NS domain structure and function with respect to transcriptional repression of ToxR regulon genes reveals differences among H-NS family members. Mol. Microbiol. 50:427-444.
45. Nye, M. B., J. D. Pfau, K. Skorupski, and R. K. Taylor. 2000. Vibrio cholerae H-NS silences virulence gene expression at multiple steps in the ToxR regulatory cascade. J. Bacteriol. 182:4295-4303.
46. Owen-Hughes, T. A., G. D. Pavitt, D. S. Santos, J. M. Sidebotham, C. S. J. Hulton, J. C. D. Hinton, and C. F. Higgins. 1992. The chromatin-associated protein H-NS interacts with curved DNA to influence DNA topology and gene expression. Cell 71:255-265.
47. 28-dependent flagellar gene transcription hierarchy of Vibrio cholerae. Mol. Microbiol. 39:1595-1609.
48. Rothmel, R. D., D. Shinabarger, M. Parsek, T. Aldrich, and A. M. Chakrabarty. 1991. Functional analysis of the Pseudomonas putida regulatory protein CatR: transcriptional studies and determination of the CatR DNA binding site by hydroxyl-radical footprinting. J. Bacteriol. 173:4717-4724.
49. Silva, A. J., and J. A. Benitez. 2004. Transcriptional regulation of Vibrio cholerae hemagglutinin/protease by the cyclic AMP receptor protein and RpoS. J. Bacteriol. 186:6374-6382.
50. Silva, A. J., and J. A. Benitez. 2006. A Vibrio cholerae relaxed (relA) mutant expresses major virulence factors, exhibits biofilm formation and motility, and colonizes the suckling mouse intestine. J. Bacteriol. 188:794-800.
51. Silva, A. J., G. J. Leitch, A. Camilli, and J. A. Benitez. 2006. Contribution of hemagglutinin/protease and motility to the pathogenesis of El Tor biotype cholera. Infect. Immun. 74:2072-2079.
52. Silva, A. J., K. Pham, and J. A. Benitez. 2003. Hemagglutinin/protease expression and mucin gel penetration in El Tor biotype Vibrio cholerae. Microbiology 149:1883-1891.
53. Skorupski, K., and R. K. Taylor. 1997. Cyclic AMP and its receptor protein negatively regulate the coordinate expression of cholera toxin and toxin co-regulated pilus in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 94:265-270.
54. Spurio, R., M. Falconi, A. Brandi, C. L. Pon, and C. O. Gualerzi. 1997. The oligomeric structure of the nucleoid protein H-NS is necessary for recognition of intrinsically curved DNA and for DNA binding. EMBO J. 16:1795-1805.
55. Starks, M. J. 1987. Multicopy expression vectors carrying the lac repressor for regulated high-level expression of genes in Escherichia coli. Gene 51:255-267.
56. Tendeng, C., C. Badaut, E. Krin, P. Gounon, S. Ngo, A. Danchin, S. Rimsky, and P. Bertin. 2000. Isolation and characterization of vicH, encoding a new pleiotropic regulator in Vibrio cholerae. J. Bacteriol. 182:2026-2032.
57. Ueguchi, C., and T. Mizuno. 1993. The Escherichia coli nucleoid protein H-NS functions directly as a transcriptional repressor. EMBO J. 12:1039-1046.
58. Vicente, M., K. F. Chater, and V. De Lorenzo. 1999. Bacterial transcription factors involved in global regulation. Mol. Microbiol. 33:8-17.
59. Wu, Z., D. Milton, P. Nybom, A. Sjö, and K. E. Magnusson. 1996. Vibrio cholerae hemagglutinin/protease (HA/protease) causes morphological changes in cultured epithelial cells and perturbs their paracellular barrier function. Microb. Pathog. 21:111-123.
60. Wu, Z., P. Nybom, and K. E. Magnusson. 2000. Distinct effects of Vibrio cholerae haemagglutinin/protease on the structure and localization of the tight junction-associated proteins occludin and ZO-1. Cell. Microbiol. 2:11-17.
61. Wu, Z., P. Nybom, T. Sundqvist, and K. E. Magnusson. 1998. Endogenous nitric oxide in MDCK-I cells modulates the Vibrio cholerae haemagglutinin/ protease (HA/P)-mediated cytotoxicity. Microb. Pathog. 24:321-326.
62. Yildiz, F. H., and G. K. Schoolnik. 1998. Role of rpoS in stress survival and virulence of Vibrio cholerae. J. Bacteriol. 180:773-784.
63. Yu, R. R., and V. J. DiRita. 2002. Regulation of gene expression in Vibrio cholerae by toxT involves both antirepression and RNA polymerase stimulation. Mol. Microbiol. 43:119-134.
64. Zhou, Y., and S. Gottesman. 2006. Modes of regulation of RpoS by H-NS. J. Bacteriol. 188:7022-7025.