Acid-induced activation of the urease promoters is mediated directly by the ArsRS two-component system of Helicobacter pylori

Infection and Immunity

Volumn 73, Issue 10, 2005, Pages 6437-6445

  Pflock, Michael ^a   Kennard, Simone ^a   Delany, Isabel ^b   Scarlato, Vincenzo ^b   Beier, Dagmar ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b CHIRON VACCINES   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACID; BACTERIAL PROTEIN; MUTANT PROTEIN; NICKEL; NIKR PROTEIN; UNCLASSIFIED DRUG; UREASE;

ACID RESPONSIVE SIGNALING; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIUM MUTANT; BINDING SITE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA FOOTPRINTING; ENZYME ACTIVITY; GENE ACTIVATION; GENE CONTROL; GENE DELETION; GENE SEQUENCE; HELICOBACTER PYLORI; NONHUMAN; OPERON; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; REGULATOR GENE; SIGNAL TRANSDUCTION; STOMACH PH; TRANSCRIPTION REGULATION; WILD TYPE;

EID: 25444522923     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.10.6437-6445.2005     Document Type: Article

References (43)

1. Akada, J. K., M. Shirai, H. Takeuchi, M. Tsuda, and T. Nakazawa. 2000. Identification of the urease operon in Helicobacter pylori and its control by mRNA decay in response to pH. Mol. Microbiol. 36:1071-1084.
2. Bauerfeind, P., R. Garner, B. E. Dunn, and H. L. Mobley. 1997. Synthesis and activity of Helicobacter pylori urease and catalase at low pH. Gut 40:25-30.
3. Beier, D., G. Spohn, R. Rappuoli, and V. Scarlato. 1997. Identification and characterization of an operon of Helicobacter pylori that is involved in motility and stress adaptation. J. Bacteriol. 179:4676-4683.
4. Beier, D., and R. Frank. 2000. Molecular characterization of two-component systems of Helicobacter pylori. J. Bacteriol. 182:2068-2076.
5. Bijlsma, J. J. E., M. M. Gerrits, R. Imamdi, C. M. J. E. Vandenbroucke-Grauls, and J. G. Kusters. 1998. Urease-positive, acid-sensitive mutants of Helicobacter pylori: urease-independent acid resistance involved in growth at low pH. FEMS Microbiol. Lett. 167:309-313.
6. Bijlsma, J. J. E., A. L. M. Lie, I. C. Nootenboom, C. M. Vandenbroucke-Grauls, and J. G. Kusters. 2000. Identification of loci essential for the growth of Helicobacter pylori under acidic conditions. J. Infect. Dis. 182:1566-1569.
7. Bijlsma, J. J. E., B. Waidner, A. H. M. van Vliet, N. J. Hughes, S. Häg, S. Bereswill, D. J. Kelly, C. M. J. E. Vandenbroucke-Grauls, M. Kist, and J. G. Kusters. 2002. The Helicobacter pylori homologue of the ferric uptake regulator is involved in acid resistance. Infect. Immun. 70:606-611.
8. Blaser, M. J. 1992. Helicobacter pylori: its role in disease. Clin. Infect. Dis. 15:386-391.
9. Bury-Moné, S., J.-M. Thiberge, M. Contreras, A. Maitournam, A. Labigne, and H. de Reuse. 2004. Responsiveness to acidity via metal ion regulators mediates virulence in the gastric pathogen Helicobacter pylori. Mol. Microbiol. 53:623-638.
10. Contreras, M., J.-M. Thiberge, M.-A. Mandrand-Berthelot, and A. Labigne. 2003. Characterization of the roles of NikR, a nickel-responsive pleiotropic autoregulator of Helicobacter pylori. Mol. Microbiol. 49:947-963.
11. Davies, B. J., N. de Vries, S. G. Rijpkema, A. H. M. van Vliet, and C. W. Penn. 2002. Transcriptional and mutational analysis of the Helicobacter pylori urease promoter. FEMS Microbiol. Lett. 213:27-32.
12. Delany, I., G. Spohn, R. Rappuoli, and V. Scarlato. 2001. The Fur repressor controls transcription of iron-activated and -repressed genes in Helicobacter pylori. Mol. Microbiol. 42:1297-1309.
13. Delany, I., R. Ieva, A. Soragni, M. Hilleringman, R. Rappuoli, and V. Scarlato. In vitro analysis of protein-operator interactions of the NikR and Fur metal-responsive regulators in overlapping sets of genes in Helicobacter pylori. Submitted for publication.
14. dePina, K., V. Desjardin, M. A. Mandrand-Berthelot, G. Giordano, and L. F. Wu. 1999. Isolation and characterization of the nikR gene encoding a nickel-responsive regulator in Escherichia coli. J. Bacteriol. 181:670-674.
15. Dietz, P., G. Gerlach, and D. Beier. 2002. Identification of target genes regulated by the two-component system HP166-HP165 of Helicobacter pylori. J. Bacteriol. 184:350-362.
16. Eaton, K. A., and S. Krakowka. 1994. Effect of gastric pH on urease-dependent colonization of gnotobiotic piglets by Helicobacter pylori. Infect. Immun. 62:3604-3607.
17. Ernst, F. D., S. Bereswill, B. Waidner, J. Stoof, U. Mäder, J. G. Kusters, E. J. Kuipers, M. Kist, A. H. M. van Vliet, and G. Homuth. 2005. Transcriptional profiling of Helicobacter pylori Fur- and iron-regulated gene expression. Microbiology 151:533-546.
18. Ferrero, R. L., V. Cussac, P. Courcoux, and A. Labigne. 1992. Construction of isogenic urease-negative mutants of Helicobacter pylori by allelic exchange. J. Bacteriol. 174:4212-4217.
19. Forsyth, M. H., P. Cao, P. P. Garcia, J. D. Hall, and T. L. Cover. 2002. Genome-wide transcriptional profiling in a histidine kinase mutant of Helicobacter pylori identifies members of a regulon. J. Bacteriol. 184:4630-4635.
20. Kinnear, S. M., P. E. Boucher, S. Stibitz, and N. H. Carbonetti. 1999. Analysis of BvgA activation of the pertactin gene promoter in Bordetella pertussis. J. Bacteriol. 181:5234-5241.
21. Labigne-Roussel, A., P. Courcoux, and L. Tompkins. 1988. Gene disruption and replacement as feasible approach for mutagenesis of Campylobacter jejuni. J. Bacteriol. 170:1704-1708.
22. Maxam, A. M., and W. Gilbert. 1977. A new method for sequencing DNA. Proc. Natl. Acad. Sci. USA 74:560-564.
23. 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.
24. Mollenhauer-Rektorschek, M., G. Hanauer, G. Sachs, and K. Melchers. 2002. Expression of UreI is required for intragastric transit and colonization of gerbil gastric mucosa by Helicobacter pylori. Res. Microbiol. 153:659-666.
25. Panthel, K., P. Dietz, R. Haas, and D. Beier. 2003. Two-component systems of Helicobacter pylori contribute to virulence in a mouse infection model. Infect. Immun. 71:5381-5385.
26. Peterson, W. L. 1991. Helicobacter pylori and peptic ulcer disease. N. Engl. J. Med. 324:1043-1048.
27. Pflock, M., P. Dietz, J. Schär, and D. Beier. 2004. Genetic evidence for histidine kinase HP165 being an acid sensor of Helicobacter pylori. FEMS Microbiol. Lett. 234:51-61.
28. Rektorschek, M., D. Weeks, G. Sachs, and K. Melchers. 1998. Influence of pH on metabolism and urease activity of Helicobacter pylori. Gastroenterology 115:628-641.
29. Scott, D. R., E. A. Marcus, D. L. Weeks, A. Lee, K. Melchers, and G. Sachs. 2000. Expression of the Helicobacter pylori ureI gene is required for acidic pH activation of cytoplasmic urease. Infect. Immun. 68:470-477.
30. Scott, D. R., E. A. Marcus, D. L. Weeks, and G. Sachs. 2002. Mechanisms of acid resistance due to the urease system of Helicobacter pylori. Gastroenterology 123:187-195.
31. Skouloubris, S., J.-M. Thiberge, A. Labigne, and H. De Reuse. 1998. The Helicobacter pylori UreI protein is not involved in urease activity but is essential for bacterial survival in vivo. Infect. Immun. 66:4517-4521.
32. Spohn, G., and V. Scarlato. 1999. Motility of Helicobacter pylori is coordinately regulated by the transcriptional activator FlgR, an NtrC homolog. J. Bacteriol. 181:593-599.
33. Tomb, J.-F., O. White, A. R. Kerlavage, R. 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, E. K. Hickey, D. E. Berg, J. D. Gocayne, T. R. Utterback, J. D. Peterson, J. M. Kelley, M. D. Cotton, J. M. Weidman, C. Fujii, C. Bowman, L. Watthey, E. Wallin, W. S. Hayes, M. Borodovsky, P. D. Karp, H. O. Smith, C. M. Fraser, and J. C. Venter. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547.
34. Uemura, N. S., S. Okamoto, S. Yamamoto, N. Matsumura, S. Yamaguchi, M. Yamakido, K. Taniyama, N. Sasaki, and R. J. Schlemper. 2001. Helicobacter pylori infection and the development of gastric cancer. N. Engl. J. Med. 345:784-789.
35. van Vliet, A. H. M., E. J. Kuipers, B. Waidner, B. J. Davies, N. de Vries, C. W. Penn, C. M. J. E. Vandenbroucke-Grauls, M. Kist, S. Bereswill, and J. G. Kusters. 2001. Nickel-responsive induction of urease expression in Helicobacter pylori is mediated at the transcriptional level. Infect. Immun. 69:4891-4897.
36. van Vliet, A. H. M., S. W. Poppelaars, B. J. Davies, J. Stoof, S. Bereswill, M. Kist, C. W. Penn, E. J. Kuipers, and J. G. Kusters. 2002. NikR mediates nickel-responsive transcriptional induction of urease expression in Helicobacter pylori. Infect. Immun. 70:2846-2852.
37. van Vliet, A. H. M., J. Stoof, S. W. Poppelaars, S. Bereswill, G. Homuth, M. Kist, E. J. Kuipers, and J. G. Kusters. 2003. Differential regulation of amidase- and formamidase-mediated ammonia production by the Helicobacter pylori Fur repressor. J. Biol. Chem. 278:9052-9057.
38. van Vliet, A. H. M., E. J. Kuipers, J. Stoof, S. W. Poppelaars, and J. G. Kusters. 2004. Acid-responsive gene induction of ammonia-producing enzymes in Helicobacter pylori is mediated via a metal-responsive repressor cascade. Infect. Immun. 72:766-773.
39. van Vliet, A. H. M, F. D. Ernst, and J. G. Kusters. 2004. NikR-mediated regulation of Helicobacter pylori acid adaptation. Trends Microbiol. 12:489-494.
40. Wang, Y., and D. E. Taylor. 1990. Chloramphenicol resistance in Campylobacter coli: nucleotide sequence, expression, and cloning vector construction. Gene 94:23-28.
41. + gated urea channel: the link between Helicobacter pylori urease and gastric colonization. Science 287:482-485.
42. Wen, Y., E. A. Marcus, U. Matrubutham, M. A. Gleeson, D. R. Scott, and G. Sachs. 2003. Acid-adaptive genes of Helicobacter pylori. Infect. Immun. 71:5921-5939.
43. Xiang, Z., S. Censini, P. F. Bayeli, J. L. Telford, N. Figura, R. Rappuoli, and A. Covacci. 1995. Analysis of expression of CagA and VacA virulence factors in 43 strains of Helicobacter pylori reveals that clinical isolates can be divided into two major types and that CagA is not necessary for expression of the vacuolating cytotoxin. Infect. Immun. 63:94-98.