The quorum-sensing molecule autoinducer 2 regulates motility and flagellar morphogenesis in Helicobacter pylori

Journal of Bacteriology

Volumn 189, Issue 17, 2007, Pages 6109-6117

  Rader, Bethany A ^a   Campagna, Shawn R ^b   Semmelhack, Martin F ^b   Bassler, Bonnie L ^b   Guillemin, Karen ^a  

^a UNIVERSITY OF OREGON   (United States)

^b PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4,5 DIHYDROXY 2,3 PENTANEDIONE; ACETYLACETONE; AGAR; AUTOINDUCER 2; GENE PRODUCT; PHOSPHOTRANSFERASE; PROTEIN FLHA; SIGMA FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; CELL FREE SYSTEM; CONTROLLED STUDY; CYCLIZATION; FLGM GENE; FLGS GENE; FLIA GENE; GENE DELETION; GENE EXPRESSION; HELICOBACTER PYLORI; LUXS GENE; MORPHOGENESIS; MORPHOLOGY; MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; QUORUM SENSING; REGULATORY MECHANISM; SUPERNATANT; SYNTHESIS; TRANSCRIPTION REGULATION; WILD TYPE;

BACTERIAL PROTEINS; CARBON-SULFUR LYASES; FLAGELLA; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; HELICOBACTER PYLORI; HOMOSERINE; LACTONES; LOCOMOTION; MEMBRANE PROTEINS; MORPHOGENESIS; PENTANES; QUORUM SENSING; RNA, BACTERIAL; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

HELICOBACTER PYLORI;

EID: 34548503623     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00246-07     Document Type: Article

References (53)

1. Alm, R. A., L. S. Ling, D. T. Moir, B. L. King, E. D. Brown, P. C. Doig, D. R. Smith, B. Noonan, B. C. Guild, B. L. deJonge, G. Carmel, P. J. Tummino, A. Caruso, M. Uria-Nickelsen, D. M. Mills, C. Ives, R. Gibson, D. Merberg, S. D. Mills, Q. Jiang, D. E. Taylor, G. F. Vovis, and T. J. Trust. 1999. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397:176-180.
2. Baltrus, D. A., and K. Guillemin. 2006. Multiple phases of competence occur during the Helicobacter pylori growth cycle. FEMS Microbiol. Lett. 255:148-155.
3. Bassler, B. L., E. P. Greenberg, and A. M. Stevens. 1997. Cross-species induction of luminescence in the quorum-sensing bacterium Vibrio harveyi. J. Bacteriol. 179:4043-4045.
4. Bassler, B. L., and R. Losick. 2006. Bacterially speaking. Cell 125:237-246.
5. Bassler, B. L., M. Wright, R. E. Showalter, and M. R. Silverman. 1993. Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol. Microbiol. 9:773-786.
6. Beier, D., and R. Frank. 2000. Molecular characterization of two-component systems of Helicobacter pylori. J. Bacteriol. 182:2068-2076.
7. Bergara, F., C. Ibarra, J. Iwamasa, J. C. Patarroyo, R. Aguilera, and L. M. Marquez-Magana. 2003. CodY is a nutritional repressor of flagellar gene expression in Bacillus subtilis. J. Bacteriol. 185:3118-3126.
8. Bik, E. M., P. B. Eckburg, S. R. Gill, K. E. Nelson, E. A. Purdom, F. Francois, G. Perez-Perez, M. J. Blaser, and D. A. Relman. 2006. Molecular analysis of the bacterial microbiota in the human stomach. Proc. Natl. Acad. Sci. USA 103:732-737.
9. Blaser, M. J., and J. C. Atherton. 2004. Helicobacter pylori persistence: biology and disease. J. Clin. Investig. 113:321-333.
10. Cole, S. P., J. Harwood, R. Lee, R. She, and D. G. Guiney. 2004. Characterization of monospecies biofilm formation by Helicobacter pylori. J. Bacteriol. 186:3124-3132.
11. Colland, F., J. C. Rain, P. Gounon, A. Labigne, P. Legrain, and H. De Reuse. 2001. Identification of the Helicobacter pylori anti-sigma28 factor. Mol. Microbiol. 41:477-487.
12. Copass, M., G. Grandi, and R. Rappuoli. 1997. Introduction of unmarked mutations in the Helicobacter pylori vacA gene with a sucrose sensitivity marker. Infect. Immun. 65:1949-1952.
13. Corless, C. E., M. Guiver, R. Borrow, V. Edwards-Jones, E. B. Kaczmarski, and A. J. Fox. 2000. Contamination and sensitivity issues with a real-time universal 16S rRNA PCR. J. Clin. Microbiol. 38:1747-1752.
14. Covacci, A., S. Censini, M. Bugnoli, R. Petracca, D. Burroni, G. Macchia, A. Massone, E. Papini, Z. Xiang, N. Figura, et al. 1993. Molecular characterization of the 128-kDa immunodominant antigen of Helicobacter pylori associated with cytotoxicity and duodenal ulcer. Proc. Natl. Acad. Sci. USA 90:5791-5795.
15. De Keersmaecker, S. C., K. Sonck, and J. Vanderleyden. 2006. Let LuxS speak up in AI-2 signaling. Trends Microbiol. 14:114-119.
16. Eaton, K. A., S. Suerbaum, C. Josenhans, and S. Krakowka. 1996. Colonization of gnotobiotic piglets by Helicobacter pylori deficient in two flagellin genes. Infect. Immun. 64:2445-2448.
17. Elvers, K. T., and S. F. Park. 2002. Quorum sensing in Campylobacter jejuni: detection of a luxS encoded signalling molecule. Microbiology 148:1475-1481.
18. Federle, M. J., and B. L. Bassler. 2003. Interspecies communication in bacteria. J. Clin. Investig. 112:1291-1299.
19. Forsyth, M. H., and T. L. Cover. 2000. Intercellular communication in Helicobacter pylori: luxS is essential for the production of an extracellular signaling molecule. Infect. Immun. 68:3193-3199.
20. Freeman, J. A., and B. L. Bassler. 1999. A genetic analysis of the function of LuxO, a two-component response regulator involved in quorum sensing in Vibrio harveyi. Mol. Microbiol. 31:665-677.
21. Freeman, J. A., B. N. Lilley, and B. L. Bassler. 2000. A genetic analysis of the functions of LuxN: a two-component hybrid sensor kinase that regulates quorum sensing in Vibrio harveyi. Mol. Microbiol. 35:139-149.
22. Gonzalez Barrios, A. F., R. Zuo, Y. Hashimoto, L. Yang, W. E. Bentley, and T. K. Wood. 2006. Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022). J. Bacteriol. 188:305-316.
23. Greenberg, E. P., J. W. Hastings, and S. Ulitzer. 1979. Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria. Arch. Microbiol. 120:87-91.
24. Jeon, B., K. Itoh, N. Misawa, and S. Ryu. 2003. Effects of quorum sensing on flaA transcription and autoagglutination in Campylobacter jejuni. Microbiol. Immunol. 47:833-839.
25. Josenhans, C., E. Niehus, S. Amersbach, A. Horster, C. Betz, B. Drescher, K. T. Hughes, and S. Suerbaum. 2002. Functional characterization of the antagonistic flagellar late regulators FliA and FlgM of Helicobacter pylori and their effects on the H. pylori transcriptome. Mol. Microbiol. 43:307-322.
26. Joyce, E. A., B. L. Bassler, and A. Wright. 2000. Evidence for a signaling system in Helicobacter pylori: detection of a luxS-encoded autoinducer. J. Bacteriol. 182:3638-3643.
27. Kim, N., E. A. Marcus, Y. Wen, D. L. Weeks, D. R. Scott, H. C. Jung, I. S. Song, and G. Sachs. 2004. Genes of Helicobacter pylori regulated by attachment to AGS cells. Infect. Immun. 72:2358-2368.
28. Lee, W. K., K. Ogura, J. T. Loh, T. L. Cover, and D. E. Berg. 2006. Quantitative effect of luxS gene inactivation on the fitness of Helicobacter pylori. Appl. Environ Microbiol. 72:6615-6622.
29. Lilley, B. N., and B. L. Bassler. 2000. Regulation of quorum sensing in Vibrio harveyi by LuxO and sigma-54. Mol. Microbiol. 36:940-954.
30. Loh, J. T., M. H. Forsyth, and T. L. Cover. 2004. Growth phase regulation of flaA expression in Helicobacter pylori is luxS dependent. Infect. Immun. 72:5506-5510.
31. McAdams, H. H., and L. Shapiro. 2003. A bacterial cell-cycle regulatory network operating in time and space. Science 301:1874-1877.
32. McCarter, L. L. 2006. Regulation of flagella. Curr. Opin. Microbiol. 9:180-186.
33. McGee, D. J., C. Coker, T. L. Testerman, J. M. Harro, S. V. Gibson, and H. L. Mobley. 2002. The Helicobacter pylori flbA flagellar biosynthesis and regulatory gene is required for motility and virulence and modulates urease of H. pylori and Proteus mirabilis. J. Med. Microbiol. 51:958-970.
34. Menard, R., P. J. Sansonetti, and C. Parsot. 1993. Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J. Bacteriol. 175:5899-5906.
35. Merrell, D. S., M. L. Goodrich, G. Otto, L. S. Tompkins, and S. Falkow. 2003. pH-regulated gene expression of the gastric pathogen Helicobacter pylori. Infect. Immun. 71:3529-3539.
36. Mouery, K., B. A. Rader, E. C. Gaynor, and K. Guillemin. 2006. The stringent response is required for Helicobacter pylori survival of stationary phase, exposure to acid, and aerobic shock. J. Bacteriol. 188:5494-5500.
37. Niehus, E., H. Gressmann, F. Ye, R. Schlapbach, M. Dehio, C. Dehio, A. Stack, T. F. Meyer, S. Suerbaum, and C. Josenhans. 2004. Genome-wide analysis of transcriptional hierarchy and feedback regulation in the flagellar system of Helicobacter pylori. Mol. Microbiol. 52:947-961.
38. Osaki, T., T. Hanawa, T. Manzoku, M. Fukuda, H. Kawakami, H. Suzuki, H. Yamaguchi, X. Yan, H. Taguchi, S. Kurata, and S. Kamiya. 2006. Mutation of luxS affects motility and infectivity of Helicobacter pylori in gastric mucosa of a Mongolian gerbil model. J. Med. Microbiol. 55:1477-1485.
39. O'Toole, P. W., M. C. Lane, and S. Porwollik. 2000. Helicobacter pylori motility. Microbes Infect. 2:1207-1214.
40. Ottemann, K. M., and A. C. Lowenthal. 2002. Helicobacter pylori uses motility for initial colonization and to attain robust infection. Infect. Immun. 70:1984-1990.
41. Schauder, S., K. Shokat, M. G. Surette, and B. L. Bassler. 2001. The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol. Microbiol. 41:463-476.
42. Schmitz, A., C. Josenhans, and S. Suerbaum. 1997. Cloning and characterization of the Helicobacter pylori flbA gene, which codes for a membrane protein involved in coordinated expression of flagellar genes. J. Bacteriol. 179:987-997.
43. Semmelhack, M. F., S. R. Campagna, M. J. Federle, and B. L. Bassler. 2005. An expeditious synthesis of DPD and boron binding studies. Org. Lett. 7:569-572.
44. Smeets, L. C., J. J. Bijlsma, S. Y. Boomkens, C. M. Vandenbroucke-Grauls, and J. G. Kusters. 2000. comH, a novel gene essential for natural transformation of Helicobacter pylori. J. Bacteriol. 182:3948-3954.
45. Suerbaum, S. 1995. The complex flagella of gastric Helicobacter species. Trends Microbiol. 3:168-171.
46. Surette, M. G., and B. L. Bassler. 1998. Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 95:7046-7050.
47. Surette, M. G., and B. L. Bassler. 1999. Regulation of autoinducer production in Salmonella typhimurium. Mol. Microbiol. 31:585-595.
48. Surette, M. G., M. B. Miller, and B. L. Bassler. 1999. Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. Proc. Natl. Acad. Sci. USA 96:1639-1644.
49. Thompson, L. J., D. S. Merrell, B. A. Neilan, H. Mitchell, A. Lee, and S. Falkow. 2003. Gene expression profiling of Helicobacter pylori reveals a growth-phase-dependent switch in virulence gene expression. Infect. Immun. 71:2643-2655.
50. Tomb, J. F., O. White, A. R. Kerlavage, R. A. Clayton, G. G. Sutton, R. D. Fleischmann, K. A. Ketchum, H. P. Klenk, S. Gill, B. A. Dougherty, K. Nelson, J. Quackenbush, L. Zhou, E. F. Kirkness, S. Peterson, B. Loftus, D. Richardson, R. Dodson, H. G. Khalak, A. Glodek, K. McKenney, L. M. Fitzegerald, N. Lee, M. D. Adams, J. C. Venter, et al. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547.
51. Vendeville, A., K. Winzer, K. Heurlier, C. M. Tang, and K. R. Hardie. 2005. Making "sense" of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat. Rev. Microbiol. 3:383-396.
52. Walters, M., M. P. Sircili, and V. Sperandio. 2006. AI-3 synthesis is not dependent on luxS in Escherichia coli. J. Bacteriol. 188:5668-5681.
53. Waters, C. M., and B. L. Bassler. 2005. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21:319-346.