Phosphorylation of the flagellar regulatory protein FlrC is necessary for Vibrio cholerae motility and enhanced colonization

Molecular Microbiology

Volumn 35, Issue 4, 2000, Pages 743-755

  Correa, Nidia E ^a   Lauriano, Crystal M ^a   McGee, Raynia ^a   Klose, Karl E ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FLAGELLIN; MUTANT PROTEIN; PHOSPHATE; REGULATOR PROTEIN; SIGMA FACTOR;

ARTICLE; BACTERIAL COLONIZATION; BACTERIUM MUTANT; CELL MOTILITY; FLAGELLUM; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SMALL INTESTINE ABSORPTION; TRANSCRIPTION REGULATION; VIBRIO CHOLERAE;

ANIMALS; ASPARTIC ACID; BACTERIAL ADHESION; BACTERIAL PROTEINS; CELL DIVISION; DNA-BINDING PROTEINS; DNA-DIRECTED RNA POLYMERASES; FLAGELLA; FLAGELLIN; GENE EXPRESSION REGULATION, BACTERIAL; HEMOLYSIN PROTEINS; HUMANS; MICE; MOVEMENT; MUTATION; PHOSPHATES; PHOSPHORYLATION; PHOSPHOTRANSFERASES; RNA POLYMERASE SIGMA 54; SIGMA FACTOR; TRANSCRIPTION, GENETIC; VIBRIO CHOLERAE;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; VIBRIO CHOLERAE;

EID: 0033962752     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2000.01745.x     Document Type: Article

References (43)

1. Akerley, B.J., Cotter, P.A., and Miller, J.F. (1995) Ectopic expression of the flagellar regulon alters development of the Bordetella-host interaction. Cell 80: 611-620.
2. Coster, T.S., Killeen, K.P., Waldor, M.K., Beattie, D., Spriggs, D., Kenner, J.R., et al. (1995) Safety, immunogenicity and efficacy of a live attenuated Vibrio cholerae 0139 vaccine prototype, Bengal-15. Lancet 345: 949-952.
3. DiRita, V.J., Parsot, C., Jander, G., and Mekalanos, J.J. (1991) Regulatory cascade controls virulence in Vibrio cholerae. Proc Natl Acad Sci USA 88: 5403-5407.
4. Donnenberg, M.S., and Kaper, J.B. (1991) Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun 59: 4310-4317.
5. Eaton, K.A., Suerbaum, S., Josenhans, C., and Krakowka, S. (1996) Colonization of gnotobiotic piglets by Helicobacter pylori deficient in two flagellin genes. Infect Immun 64: 2445-2448.
6. Freter, R., and O'Brien, P.C.M. (1981) Role of chemotaxis in the association of motile bacteria with intestinal mucosa: chemotactic responses of Vibrio cholerae and description of motile nonchemotactic mutants. Infect Immun 34: 215-221.
7. Gardel, C.L., and Mekalanos, J.J. (1996) Alterations in Vibrio cholerae motility phenotypes correlate with changes in virulence factor expression. Infect Immun 64: 2246-2255.
8. Hanahan, D. (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Sol 166: 577-580.
9. Harshey, R.M., and Toguchi, A. (1996) Spinning tails: homologies among bacterial flagellar systems. Trends Microbiol 4: 226-231.
10. Hase, C.C., and Mekalanos, J.J. (1998) TcpP protein is a positive regulator of virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci USA 95: 730-734.
11. Hase, C.C., and Mekalanos, J.J. (1999) Effects of changes in membrane sodium flux on virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci USA 96: 3183-3187.
12. Hess, F., Oosawa, K., Kaplan, N., and Simon, M. (1988) Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis. Cell 53: 79-87.
13. Holmgren, J., and Svennerholm, A.M. (1989) Mechanisms of disease and immunity in cholera: a review. J Infect Dis 136: S105-S112.
14. Keener, J., and Kustu, S. (1988) Protein kinase and phospho-protein phosphatase activities of nitrogen regulatory proteins NTRB and NTRC of enteric bacteria: roles of the conserved amino-terminal domain of NTRC. Proc Natl Acad Sci USA 85: 4976-4980.
15. Kenner, J.R., Coster, T.S., Taylor, D.N., Trofa, A.F., Barrera-Oro, M., Hyman, T., et al. (1995) Peru-15, an improved live attenuated vaccine candidate for Vibrio cholerae 01. J Infect Dis 172: 1126-1129.
16. 54, a vital protein for Myxococcus xanthus. Proc Natl Acad Sci USA 94: 1979-1984.
17. Klose, K.E. (1993) Studies of the structure and function of the nitrogen-regulatory protein NTRC from Salmonella typhimurium. PhD Thesis, Berkeley, CA, University of California.
18. Klose, K.E., and Mekalanos, J.J. (1997) Simultaneous prevention of glutamine synthesis and high-affinity transport attenuates Salmonella typhimurium virulence. Infect Immun 65: 587-596.
19. Klose, K.E., and Mekalanos, J.J. (1998a) Distinct roles of an alternative sigma factor during both free-swimming and colonizing phases of the Vibrio cholerae pathogenic cycle. Mol Microbiol 28: 501-520.
20. Klose, K.E., and Mekalanos, J.J. (1998b) Differential regulation of multiple flagellins in V. cholerae. J Bacteriol 180: 303-316.
21. Klose, K.E., Weiss, D.S., and Kustu, S. (1993) Glutamate at the site of phosphorylation of nitrogen-regulatory protein NTRC mimics aspartyl-phosphate and activates the protein. J Mol Biol 232: 67-78.
22. 54-dependent transcriptional activators in Vibrio cholerae. J Bacteriol 180: 5256-5259.
23. Kojima, S., Yamamoto, K., Kawagishi, I., and Homma, M. (1999) The polar flagellar motor of Vibrio cholerae is driven by an Na + motive force. J Bacteriol 181: 1927-1930.
24. Lospalluto, J.J., and Finkelstein, R.A. (1972) Chemical and physical properties of cholera exo-enterotoxin (choleragen) and its spontaneously formed toxoid (choleragenoid). Biochim Biophys Acta 257: 158-166.
25. Lukat, G.S., McCleary, W.R., Stock, A.M., and Stock, J.B. (1992) Phosphorylation of bacterial response regulator proteins by low molecular weight phosphodonors. Proc Natl Acad Sci USA 89: 718-722.
26. Mead, D.A., Szczesna-Skorupa, E., and Kemper, B. (1986) Single-stranded DNA 'blue' T7 promoter plasmids: a versatile tandem promoter system for cloning and protein engineering. Protein Eng 1: 67-74.
27. Mekalanos, J.J., Collier, R.J., and Romig, W.R. (1979) Enzymic activity of cholera toxin. II. Relationships to proteolytic processing, disulfide bond reduction, and subunit composition. J Biol Chem 254: 5855-5861.
28. Mekalanos, J.J., Swartz, D.J., Pearson, G.D., Harford, N., Groyne, F., and de Wilde, M. (1983) Cholera toxin genes: nucleotide sequence, deletion analysis and vaccine development. Nature 306: 551-557.
29. Miller, J.H. (1992) A Short Course in Bacterial Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
30. Miller, V.L., and Mekalanos, J.J. (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.
31. Miller, V.L., Taylor, R.K., and Mekalanos, J.J. (1987) Cholera toxin transcriptional activator ToxR is a transmembrane DNA binding protein. Cell 48: 271-279.
32. Ninfa, A.J., Ninfa, E.G., Lupas, A.N., Stock, A., Magasanik, B., and Stock, J. (1988) Crosstalk between bacterial chemotaxis signal transduction proteins and the regulators of transcription of the Ntr regulon: evidence that nitrogen assimilation and chemotaxis are controlled by a common phosphotransfer mechanism. Proc Natl Acad Sci USA 85: 5492-5496.
33. Richardson, K. (1991) Roles of motility and flagellar structure in pathogenicity of Vibrio cholerae: analysis of motility mutants in three animal models. Infect Immun 59: 2727-2736.
34. Sanders, D.A., Gillece-Castro, B.L., Burlingame, A.L., and Koshland, Jr, D.E. (1992) Phosphorylation site of NtrC, a protein phosphatase whose covalent intermediate activates transcription. J Bacteriol 174: 5117-5122.
35. Sanders, D.A., Gillece-Castro, B.L., Stock, A.M., Burlingame, A.L., and Koshland, Jr, D.E. (1989) Identification of the site of phosphorylation of the chemotaxis response regulator protein, CheY. J Biol Chem 264: 21770-21778.
36. Stock, J.B., Surette, M.G., Levit, M., and Park, P. (1995) Two-component signal transduction systems: structure-function relationships and mechanisms of catalysis. In Two-Component Signal Transduction. Hoch, J.A., and Silhavy, T.J. (eds). Washington, DC: American Society for Microbiology Press, pp. 25-51.
37. 1-ELISA) procedure. Curr Microbiol 1: 19-23.
38. Taylor, R.K., Miller, V.L., Furlong, D.B., and Mekalanos, J.J. (1987) Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc Natl Acad Sci USA 84: 2833-2837.
39. Waldor, M.K., and Mekalanos, J.J. (1996) Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272: 1910-1914.
40. Wang, R.F., and Kushner, S. (1991) Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100: 195-199.
41. Wassenaar, T.M., van der Zeijst, B.A., Ayling, R., and Newell, D.G. (1993) Colonization of chicks by motility mutants of Campylobacter jejuni demonstrates the importance of flagellin A expression. J Gen Microbiol 139: 1171-1175.
42. Weiss, D.S., Batut, J., Klose, K.E., Keener, J., and Kustu, S. (1991) The phosphorylated form of the enhancer-binding protein NTRC has an ATPase activity that is essential for activation of transcription. Cell 67: 155-167.
43. 1) of Escherichia coli. Proc Natl Acad Sci USA 85: 8919-8923.