Responsiveness to activity via metal ion regulators mediates virulense in the gastric pathogen Helicobacter pylori

Molecular Microbiology

Volumn 53, Issue 2, 2004, Pages 623-638

  Bury Moné, Stéphanie ^a   Thiberge, Jean Michel ^a   Contreras, Monica ^a   Maitournam, Aboubakar ^b   Labigne, Agnès ^a   De Reuse, Hilde ^a  

^a INSTITUT PASTEUR   (France)

^b Parc Scientifique de Luminy   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACID; AMIDASE; AMMONIA; FORMAMIDASE; METAL ION; PROTEIN FUR; PROTEIN NIKR; PROTEIN SUBUNIT; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REGULATOR PROTEIN; SODIUM PROTON EXCHANGE PROTEIN; UNCLASSIFIED DRUG; UREASE; VIRULENCE FACTOR; BACTERIAL PROTEIN; BUFFER; IRON UPTAKE REGULATION PROTEIN, BACTERIA; IRON-UPTAKE REGULATION PROTEIN, BACTERIA; METAL; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; REPRESSOR PROTEIN;

ACIDITY; ANALYTIC METHOD; ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; COMPARATIVE STUDY; CONTROLLED STUDY; DATA ANALYSIS; DOWN REGULATION; ENZYME ASSAY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ANALYSIS; GENETIC CODE; GENETIC REGULATION; GENETIC SELECTION; HELICOBACTER PYLORI; HOMEOSTASIS; METAL METABOLISM; MODEL; MUTANT; NONHUMAN; PATHOGENESIS; PH; PRIORITY JOURNAL; PROTECTION; PROTON TRANSPORT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STOMACH; SYNTHESIS; UPREGULATION; VALIDATION PROCESS; ADAPTATION; ANIMAL; BACTERIAL GENE; DISEASE MODEL; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; HELICOBACTER INFECTION; METABOLISM; MICROBIOLOGY; MOUSE; PATHOGENICITY; PHYSIOLOGY; VIRULENCE;

BACTERIA (MICROORGANISMS); HELICOBACTER; HELICOBACTER PYLORI; HELICOBACTER PYLORI 26695; PRIMATES;

ACIDS; ADAPTATION, PHYSIOLOGICAL; AMIDOHYDROLASES; AMMONIA; ANIMALS; BACTERIAL PROTEINS; BUFFERS; DISEASE MODELS, ANIMAL; DOWN-REGULATION; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HYDROGEN-ION CONCENTRATION; METALS; MICE; PROTON-TRANSLOCATING ATPASES; REPRESSOR PROTEINS; SODIUM-HYDROGEN ANTIPORTER; UP-REGULATION; UREASE; VIRULENCE; VIRULENCE FACTORS;

EID: 3242881125     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2004.04137.x     Document Type: Article

References (71)

1. Akada, J.K., Shirai, M., Takeuchi, H., Tsuda, M., and Nakazawa, T. (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. Allan, E., Clayton, C.L., McLaren, A., Wallace, D.M., and Wren, B.W. (2001) Characterization of low-pH responses of Helicobacter pylori using genomic DNA arrays. Microbiol 147: 2285-2292.
3. Ang, S., Lee, C.-Z., Peck, K., Sindici, M., Matrubutham, U., Gleeson, M.A., and Wang, J.-T. (2001) Acid-induced expression in Helicobacter pylori: study in genomic scale by microarray. Infect Immun 69: 1679-1686.
4. Arfin, S.M., Long, A.D., Ito, E.T., Tolleri, L., Riehle, M.M., Paegle, E.S., and Hatfield, G.W. (2000) Global gene expression profiling in Escherichia coli K12. The effects of integration host factor. J Biol Chem 275: 29672-29684.
5. Audia, J.P., Webb, C.C., and Foster, J.W. (2001) Breaking through the acid barrier: an orchestrated response to proton stress by enteric bacteria. Int J Med Microbiol 291: 97-106.
6. Bang, I.S., Audia, J.P., Park, Y.-K., and Foster, J.W. (2002) Autoregulation of the ompR response regulator by acid shock and control of the Salmonella enterica acid tolerance response. Mol Microbiol 44: 1235-1250.
7. Bijlsma, J.J.E., Waidner, B., Van Vliet, A.H.M., Hugues, N.J., Hag, S., Bereswill, S., et al. (2002) The Helicobacter pylori homologue of the ferric uptake regulator is involved in acid resistance. Infect Immun 70: 606-611.
8. Boneca, I.G., De Reuse, H., Epinat, J.-C., Pupin, M., Labigne, A., and Moszer, I. (2003) A revised annotation and comparative analysis of Helicobacter pylori genomes. Nucleic Acid Res 31: 1704-1714.
9. Bury-Moné, S., Skouloubris, S., Labigne, A., and De Reuse, H. (2001) The Helicobacter pylori Urel protein: role in adaptation to acidity and identification of residues essential for its activity and for acid activation. Mol Microbiol 42: 1021-1034.
10. Bury-Moné, S., Skouloubris, S., Dauga, C., Thiberge, J.-M., Dailidiene, D., Berg, D.E., et al. (2003) Presence of active aliphatic amidases in Helicobacter species able to colonize the stomach. Infect Immun 71: 5613-5622.
11. Callow, M.J., Duboit, S., Gong, E.L., Speed, T.P., and Rubin, E.M. (2000) Microarray expression profiling identifies genes with altered expression in HDL-deficient mice. Genome Res 10: 2022-2029.
12. Casadaban, M., and Cohen, S.N. (1980) Analysis of gene control signals by DNA fusions and cloning in E. coli. J Mol Biol 138: 179-207.
13. Chu, S., Tanaka, S., Kaunitz, J.D., and Montrose, M.H. (1999) Dynamic regulation of gastric surface pH by luminal pH. J Clin Invest 103: 605-612.
14. Colland, F., Rain, J.-C., Gounon, P., Labigne, A., Legrain, P., and De Reuse, H. (2001) Identification of the Helicobacter pylori anti-σ28 factor. Mol Microbiol 41: 477-487.
15. Contreras, M., Thiberge, J.-M., Mandrand-Berthelot, M.-A., and Labigne, A. (2003) Characterization of the roles of NikR, a nickel-responsive pleiotropic autoregulator of Helicobacter pylori. Mol Microbiol 49: 947-963.
16. Delany, I., Spohn, G., Pacheco, A.B.F., Leva, R., Alaimo, C., Rappuoli, R., and Scarlato, V. (2002) Autoregulation of Helicobacter pylori Fur revealed by functional analysis of the iron-binding site. Mol Microbiol 46: 1107-1122.
17. Dietz, P., Gerlach, G., and Beier, D. (2002) Identification of target genes regulated by the two-component system HP166-HP165 of Helicobacter pylori. J Bacteriol 184: 350-362.
18. Dong, Q., Hyde, D., Herra, C., Kean, C., Murphy, P., O'Morain, C.A., and Buckley, M. (2001) Identification of genes regulated by prolonged acid exposure in Helicobacter pylori. FEMS Microbiol Lett 196: 245-249.
19. Duboit, S., Yang, Y.H., Callow, M.J., and Speed, T.P. (2000) Statistical methods for identifying differentially expressed genes in replicated cDNA microarray experiments. In Technical Reports no. 578. Berkeley: University of California, pp. 1-38.
20. Eisen, M.B., Spellmen, P.T., Brown, D., and Botstein, D. (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95: 14863-14868.
21. Ernst, P.B., and Gold, B.D. (2000) The disease spectrum of Helicobacter pylori: the immunopathogenesis of gastroduodenal ulcer and gastric cancer. Annu Rev Microbiol 54: 615-640.
22. Forsyth, M.H., Cao, P., Garcia, P.P., Hall, J.D., and Cover, T.L. (2002) Genome-wide transcriptional profiling in a histidine kinase mutant of Helicobacter pylori identifies members of a regulon. J Bacteriol 184: 4630-4635.
23. Foster, J.W. (1999) When protons attack: microbial strategies of acid adaptation. Curr Opin Microbiol 2: 170-174.
24. Grant, G.R., Manduchi, E., and Stoeckert, C.J.J. (2002) Using non parametric methods in the context of multiple testing to determine differentially expressed genes. In Methods of Microarrays Data Analysis. Lin, S.M., and Johnson, K.F. (eds). Boston: Kluwer Academic Publishers.
25. Hatfield, G.W., Hung, S.-P., and Baldi, P. (2003) Differential analysis of DNA microarray gene expression data. Mol Microbiol 47: 871-877.
26. Heimer, S.R., Welch, R.A., Perna, N.T., Posfai, G., Evans, P.S., Kaper, J.B., et al. (2002) Urease of enterohemorrhagic Escherichia coli: evidence for regulation by Fur and a trans-acting factor. J Bacteriol 70: 1027-1031.
27. Herrmann, L., Schwan, D., Garner, R., Mobley, H., Haas, R., Schaefer, K.P., and Melchers, K. (1999) Helicobacter pylori cadA encodes an essential Cd(II)-Zn(II)-Co(II) resistance factor influencing urease activity. Mol Microbiol 33: 524-536.
28. Hommais, F., Krin, E., Laurent-Winter, C., Soutourina, O., Malpertuy, A., Le Caer, J.L., et al. (2001) Large-scale monitoring of pleiotropic regulation of gene expression by the prokaryotic nucleoid-associated protein, H-NS. Mol Microbiol 40: 20-36.
29. + antiporter of alkaliphilic Bacillus firmus OF4. J Bacteriol 179: 3851-3857.
30. Jungblut, P.R., Bumann, D., Haas, G., Zimny-Arndt, U., Holland, P., Lamer, S., et al. (2000) Comparative proteome analysis of Helicobacter pylori. Mol Microbiol 36: 710-725.
31. Kavermann, H., Burns, B.P., Angermuller, K., Odenbreit, S., Fischer, W., Melchers, K., and Haas, R. (2003) Identification and characterization of Helicobacter pylori genes essential for gastric colonization. J Exp Med 197: 813-822.
32. Kobayashi, H., Saito, H., and Kakegawa, T. (2000) Bacterial strategies to inhabit acidic environments. J Gen Appl Microbiol 46: 235-243.
33. Krishnaswamy, R., and Wilson, D.B. (2000) Construction and characterization of an Escherichia coli strain genetically engineered for Ni(II) bioaccumulation. Appl Environ Microbiol 66: 5383-5386.
34. Labigne, A., Cussac, V., and Courcoux, P. (1991) Shuttle cloning and nucleotide sequence of Helicobacter pylori genes responsible for urease activity. J Bacteriol 173: 1920-1931.
35. Lee, A., O'Rourke, J., Corazon De Ungria, M., Robertson, B., Daskalopoulos, G., and Dixon, M.F. (1997) A standardized mouse model of Helicobacter pylori infection: introducing the Sydney strain. Gastroenterology 112: 1386-1397.
36. McGee, D.J., Radcliff, F., Mendz, G.L., Ferrero, R.L., and Mobley, H.L.T. (1999) H. pylori rocF is required for arginase activity and acid protection in vitro but is not essential for colonization of mice or for urease activity. J Bacteriol 181: 7314-7322.
37. 1 ATPase from Helicobacter pylori. Infect Immun 65: 2640-2647.
38. Mahdavi, J., Sonden, B., Hurtig, M., Farzad, O., Forsberg, L., Roche, N., et al. (2002) Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 297: 573-578.
39. Manduchi, E., Grant, G.R., McKenzie, S.E., Overton, G.G., Surrey, S., and Stoeckert, C.J.J. (2000) Generation of patterns from gene expression data by assigning confidence to differentially expressed genes. Bioinformatics 16: 685-698.
40. Massé, E., and Gottesman, S. (2002) A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci USA 99: 4620-4625.
41. Menard, R., Sansonetti, P.J., and Parsot, C. (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.
42. Merrell, D.S., and Camilli, A. (2002) Acid tolerance of gastrointestinal pathogens. Curr Opin Microbiol 5: 51-55.
43. Merrell, D.S., Goodrich, M.L., Otto, G., Tompkins, L.S., and Falkow, S. (2003a) pH-regulated gene expression of the gastric pathogen Helicobacter pylori. Infect Immun 71: 3529-3539.
44. Merrell, D.S., Thompson, L.J., Kim, C.C., Mitchell, H., Tompkins, L.S., Lee, A., and Falkow, S. (2003b) Growth phase-dependent response of Helicobacter pylori to iron starvation. Infect Immun 71: 6510-6525.
45. Mobley, H.L.T., Mendz, G.L., and Hazell, S.L. (2001) Helicobacter pylori: Physiology and Genetics. Washington, DC: American Society for Microbiology Press.
46. Moran, A.P., Knirel, Y.A., Senchenkova, S.N., Widmalm, G., Hynes, S.O., and Jansson, P.-E. (2002) Phenotypic variation in molecular mimicry between Helicobacter pylori lipopolysaccharides and human gastric epithelial cell surface glycoforms. J Biol Chem 277: 5785-5795.
47. Olson, J.W., Mehta, N.S., and Maier, R.J. (2001) Requirement of nickel metabolism proteins HypA and HypB for full activity of both hydrogenase and urease in Helicobacter pylori. Mol Microbiol 39: 176-182.
48. Panthel, K., Dietz, P., Haas, R., and Beier, D. (2003) Two-component systems of Helicobacter pylori contribute to virulence in a mouse model infection model. Infect Immun 71: 5381-5385.
49. Rain, J.-C., Selig, L., De Reuse, H., Battaglia, V., Reverdy, C., Simon, S., et al. (2001) The protein-protein interaction map of the bacterial pathogen Helicobacter pylori. Nature 409: 211-215.
50. Schade, C., Flemstrom, G., and Holm, L. (1994) Hydrogen ion concentration in the mucus layer on top of acid-stimulated and -inhibited rat acid gastric mucosa. Gastroenterology 107: 180-188.
51. Schreiber, S., Stueben, M., Josenhans, C., Scheid, P., and Suerbaum, S. (1999) In vivo distribution of Helicobacter felis in the gastric mucus of the mouse: experimental method and results. Infect Immun 67: 5151-5156.
52. Schreiber, S., Nguyen, T.-H., Stuben, M., and Scheid, P. (2000) Demonstration of a pH gradient in the gastric gland of the acid-secreting guinea pig mucosa. Am J Physiol Gastrointest Liver Physiol 279: G597-G604.
53. Scott, D.R., Marcus, E.A., Weeks, D.L., and Sachs, G. (2002) Mechanisms of acid resistance due to the urease system of Helicobacter pylori. Gastroenterology 123: 187-195.
54. Skouloubris, S., Labigne, A., and De Reuse, H. (1997) Identification and characterization of an aliphatic amidase in Helicobacter pylori. Mol Microbiol 25: 989-998.
55. Skouloubris, S., Thiberge, J.-M., Labigne, A., and De Reuse, H. (1998) The Helicobacter pylori Urel protein is not involved in urease activity but is essential for bacterial survival in vivo. Infect Immun 66: 4517-4521.
56. Skouloubris, S., Labigne, A., and De Reuse, H. (2001) The AmiE aliphatic amidase and AmiF formamidase of Helicobacter pylori: natural evolution of two enzyme paralogs. Mol Microbiol 40: 596-609.
57. Slonczewski, J.L., McGee, D.J., Philips, J., Kirkpatrick, C., and Mobley, H.L.T. (2000) pH-dependent protein profile of Helicobacter pylori analyzed by two-dimensional gels. Helicobacter 5: 240-247.
58. Soutourina, O.A., Krin, E., Laurent-Winter, C., Hommais, F., Danchin, A., and Bertin, P.N. (2002) Regulation of bacterial motility in response to low pH in Escherichia coli: the role of H-NS protein. Microbiology 148: 1543-1551.
59. Szczebara, F., Dhaenens, L., Armand, S., and Husson, M.O. (1999) Regulation of the transcription of genes encoding different virulence factors in Helicobacter pylori by free iron. FEMS Microbiol Lett 175: 165-170.
60. Tahar, R., Boudin, C., Thiery, I., and Bourgouin, C. (2002) Immune response of Anopheles gambiae to the early sporogonic stages of the human malaria parasite Plasmodium falciparum. EMBO J 21: 6673-6680.
61. Thompson, L., Merrell, D.S., Neilan, B.A., Mitchell, H., Lee, A., and Falkow, S. (2003) Gene expression profiling of Helicobacter pylori reveals a growth-phase-dependent switch in virulence gene expression. Infect Immun 71: 2643-2655.
62. Tomb, J.-F., White, O., Kerlavage, A.R., Clayton, R.A., Sutton, G.G., Fleischmann, R.D., et al. (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388: 539-547.
63. Van Vliet, A.H.M., Kuipers, E., Waidner, B., Davies, B.J., De Vries, N., Penn, C.W., et al. (2001) Nickel-responsive induction of urease expression in Helicobacter pylori is mediated at the transcriptional level. Infect Immun 69: 4891-4897.
64. Van Vliet, A.H.M., Poppelaars, S.W., Davies, B.J., Stoof, J., Bereswill, S., Kist, M., et al. (2002a) NikR mediates nickel-responsive transcriptional induction of urease in Helicobacter pylori. Infect Immun 70: 2846-2852.
65. Van Vliet, A.H.M., Stoof, J., Vlasblom, R., Wainwright, S.A., Hugues, N.J., Kelly, D.J., et al. (2002b) The role of the ferric uptake regulator (Fur) in regulation of Helicobacter pylori iron uptake. Helicobacter 4: 237-244.
66. Van Vliet, A.H.M., Stoof, J., Poppelaars, S.W., Bereswill, S., Homuth, G., Kist, M., et al. (2003) Differential regulation of amidase- and formamidase-mediated ammonia production by the Helicobacter pylori Fur repressor. J Biol Chem 278: 9052-9057.
67. +-gated urea channel: the link between Helicobacter pylori urease and gastric colonization. Science 287: 482-485.
68. Wen, Y., Marcus, E.A., Matrubutham, U., Gleeson, M.A., Scott, D.R., and Sachs, G. (2003) Acid-adaptive genes of Helicobacter pylori. Infect Immun 71: 5921-5939.
69. Worku, M.L., Sidebotham, R.L., Walker, M.M., Keshavarz, T., and Karim, Q.N. (1999) The relationship between Helicobacter pylori motility, morphology and phase of growth: implications for gastric colonization and pathology. Microbiology 145: 2803-2811.
70. Yamaoka, Y., Kwon, D.H., and Graham, D.Y. (2000) A M(r) 34,000 proinflammatory outer membrane protein (oipA) of Helicobacter pylori. Proc Natl Acad Sci USA 97: 7533-7538.
71. Yang, Y.H., Buckley, M.J., Duboit, S., and Speed, T.P. (2002) Comparison of methods for image analysis on cDNA microarrays data. J Comput Graph Stat 11: Tech report no. 584.