Iron-responsive regulation of the Helicobacter pylori iron-cofactored superoxide dismutase sodB is mediated by Fur

Journal of Bacteriology

Volumn 187, Issue 11, 2005, Pages 3687-3692

  Ernst, Florian D ^a,b,c   Homuth, Georg ^c,d   Stoof, Jeroen ^a   Mäder, Ulrike ^c,d   Waidner, Barbara ^b   Kuipers, Ernst J ^a   Kist, Manfred ^b   Kusters, Johannes G ^a   Bereswill, Stefan ^b,e   Van Vliet, Arnoud H M ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY OF GREIFSWALD   (Germany)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

^e CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE I; IRON; IRON RESPONSIVE REGULATOR FUR; MANGANESE; REACTIVE OXYGEN METABOLITE; RECOMBINANT PROTEIN; REGULATOR PROTEIN; RNA; SUPEROXIDE; SUPEROXIDE DISMUTASE; SUPEROXIDE DISMUTASE SODB; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; DNA FOOTPRINTING; GENE CONTROL; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSCRIPTION; HELICOBACTER PYLORI; IRON METABOLISM; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SODB GENE; TRANSCRIPTION INITIATION SITE;

BACTERIAL PROTEINS; BASE SEQUENCE; DNA FOOTPRINTING; GENE EXPRESSION REGULATION, BACTERIAL; HELICOBACTER PYLORI; IRON; OXIDATIVE STRESS; PROMOTER REGIONS (GENETICS); REPRESSOR PROTEINS; SUPEROXIDE DISMUTASE; SUPEROXIDES; TRANSCRIPTION, GENETIC;

ESCHERICHIA COLI; HELICOBACTER PYLORI;

EID: 21044458727     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.11.3687-3692.2005     Document Type: Article

References (42)

1. Alamuri, P., and R. J. Maier. 2005. Methionine sulphoxide reductase is an important antioxidant enzyme in the gastric pathogen Helicobacter pylori. Mol. Microbiol. 55:653.
2. Andrews, S. C., A. K. Robinson, and F. Rodriguez-Quinones. 2003. Bacterial iron homeostasis. FEMS Microbiol. Rev. 27:215-237.
3. Barnard, F. M., M. F. Loughlin, H. P. Fainberg, M. P. Messenger, D. W. Ussery, P. Williams, and P. J. Jenks. 2004. Global regulation of virulence and the stress response by CsrA in the highly adapted human gastric pathogen Helicobacter pylori. Mol. Microbiol. 51:15-32.
4. Bereswill, S., S. Greiner, A. H. M. van Vliet, B. Waidner, F. Fassbinder, E. Schiltz, J. G. Kusters, and M. Kist. 2000. Regulation of ferritin-mediated cytoplasmic iron storage by the ferric uptake regulator homolog (Fur) of Helicobacter pylori. J. Bacteriol. 182:5948-5953.
5. Bernhardt, J., K. Buttner, C. Scharf, and M. Hecker. 1999. Dual channel imaging of two-dimensional electropherograms in Bacillus subtilis. Electrophoresis 20:2225-2240.
6. Bijlsma, J. J. E., B. Waidner, A. H. M. van Vliet, N. J. Hughes, S. Hag, S. Bereswill, D. J. Kelly, C. M. J. E. Vandenbroucke-Grauls, M. Kist, and J. G. Kusters. 2002. The ferric uptake regulator (Fur) homologue of Helicobacter pylori is involved in acid resistance. Infect. Immun. 70:606-611.
7. Blaser, M. J., and J. C. Atherton. 2004. Helicobacter pylori persistence: biology and disease. J. Clin. Investig. 113:321-333.
8. Bury-Mone, 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.
9. Büttner, K., J. Bernhardt, C. Scharf, R. Schmid, U. Mader, C. Eymann, H. Antelmann, A. Volker, U. Volker, and M. Hecker. 2001. A comprehensive two-dimensional map of cytosolic proteins of Bacillus subtilis. Electrophoresis 22:2908-2935.
10. Cooksley, C., P. J. Jenks, A. Green, A. Cockayne, R. P. Logan, and K. R. Hardie. 2003. NapA protects Helicobacter pylori from oxidative stress damage, and its production is influenced by the ferric uptake regulator. J. Med. Microbiol. 52:461-469.
11. Delany, I., A. B. F. Pacheco, G. Spohn, R. Rappuoli, and V. Scarlato. 2001. Iron-dependent transcription of the frpB gene of Helicobacter pylori is controlled by the Fur protein. J. Bacteriol. 183:4932-4937.
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. de Vries, N., E. M. van Ark, J. Stoof, E. J. Kuipers, A. H. M. van Vliet, and J. G. Kusters. 2003. The stress-induced hsp12 gene shows genetic variation among Helicobacter pylori strains. FEMS Immunol. Med. Microbiol. 38:45-51.
14. 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.
15. Escolar, L., J. Perez-Martin, and V. de Lorenzo. 1999. Opening the iron-box: transcriptional metalloregulation by the Fur protein. J. Bacteriol. 181:6223-6229.
16. Harris, A. G., F. E. Hinds, A. G. Beckhouse, T. Kolesnikow, and S. L. Hazell. 2002. Resistance to hydrogen peroxide in Helicobacter pylori: role of catalase (KatA) and Fur, and functional analysis of a novel gene product designated 'KatA-associated protein,' KapA (HP0874). Microbiology 148:3813-3825.
17. Harris, A. G., J. E. Wilson, S. J. Danon, M. F. Dixon, K. Donegan, and S. L. Hazell. 2003. Catalase (KatA) and KatA-associated protein (KapA) are essential to persistent colonization in the Helicobacter pylori SS1 mouse model. Microbiology 149:665-672.
18. Jungblut, P. R., D. Bumann, G. Haas, U. Zimny-Arndt, P. Holland, S. Lamer, F. Siejak, A. Aebischer, and T. F. Meyer. 2000. Comparative proteome analysis of Helicobacter pylori. Mol. Microbiol. 36:710-725.
19. 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.
20. Kuipers, E. J. 1998. Review article: relationship between Helicobacter pylori, atrophic gastritis and gastric cancer. Aliment. Pharmacol. Ther. 12:25-36.
21. Masse, E., F. E. Escorcia, and S. Gottesman. 2003. Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev. 17:2374-2383.
22. Masse, E., and S. Gottesman. 2002. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc. Natl. Acad. Sci. USA 99:4620-4625.
23. Miehlke, S., R. Reddy, M. S. Osato, P. P. Ward, O. M. Conneely, and D. Y. Graham. 1996. Direct activity of recombinant human lactoferrin against Helicobacter pylori. J. Clin. Microbiol. 34:2593-2594.
24. Miller, R. A., and B. E. Britigan. 1997. Role of oxidants in microbial pathophysiology. Clin. Microbiol. Rev. 10:1-18.
25. Niederhoffer, E. C., C. M. Naranjo, K. L. Bradley, and J. A. Fee. 1990. Control of Escherichia coli superoxide dismutase (sodA and sodB) genes by the ferric uptake regulation (fur) locus. J. Bacteriol. 172:1930-1938.
26. Olczak, A. A., J. W. Olson, and R. J. Maier. 2002. Oxidative-stress resistance mutants of Helicobacter pylori. J. Bacteriol. 184:3186-3193.
27. Olczak, A. A., R. W. Seyler, Jr., J. W. Olson, and R. J. Maier. 2003. Association of Helicobacter pylori antioxidant activities with host colonization proficiency. Infect. Immun. 71:580-583.
28. Olson, J. W., and R. J. Maier. 2002. Molecular hydrogen as an energy source for Helicobacter pylori. Science 298:1788-1790.
29. Pesci, E. C., and C. L. Pickett. 1994. Genetic organization and enzymatic activity of a superoxide dismutase from the microaerophilic human pathogen, Helicobacter pylori. Gene 143:111-116.
30. Seyler, R. W., Jr., J. W. Olson, and R. J. Maier. 2001. Superoxide dismutase-deficient mutants of Helicobacter pylori are hypersensitive to oxidative stress and defective in host colonization. Infect. Immun. 69:4034-4040.
31. Slonczewski, J. L., D. J. McGee, J. Phillips, C. Kirkpatrick, and H. L. Mobley. 2000. pH-dependent protein profiles of Helicobacter pylori analyzed by two-dimensional gels. Helicobacter 5:240-247.
32. Spiegelhalder, C., B. Gerstenecker, A. Kersten, E. Schiltz, and M. Kist. 1993. Purification of Helicobacter pylori superoxide dismutase and cloning and sequencing of the gene. Infect. Immun. 61:5315-5325.
33. Storz, G., and J. A. Imlay. 1999. Oxidative stress. Curr. Opin. Microbiol. 2:188-194.
34. Suerbaum, S., and P. Michetti. 2002. Helicobacter pylori infection. N. Engl. J. Med. 347:1175-1186.
35. 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, 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. Karpk, 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.
36. 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.
37. 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.
38. 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.
39. van Vliet, A. H. M., J. Stoof, R. Vlasblom, S. A. Wainwright, N. J. Hughes, D. J. Kelly, S. Bereswill, J. J. E. Bijlsma, T. Hoogenboezem, C. M. J. E. Vandenbroucke-Grauls, M. Kist, E. J. Kuipers, and J. G. Kusters. 2002. The role of the ferric uptake regulator (Fur) in regulation of Helicobacter pylori iron uptake. Helicobacter 7:237-244.
40. Waidner, B., S. Greiner, S. Odenbreit, H. Kavermann, J. Velayudhan, F. Stähler, E. Bisse, A. H. M. van Vliet, S. C. Andrews, J. G. Kusters, D. J. Kelly, R. Haas, M. Kist, and S. Bereswill. 2002. Essential role of ferritin Pfr in Helicobacter pylori iron metabolism and gastric colonization. Infect. Immun. 70:3923-3929.
41. Wang, G., and R. J. Maier. 2004. An NADPH quinone reductase of Helicobacter pylori plays an important role in oxidative stress resistance and host colonization. Infect. Immun. 72:1391-1396.
42. Wang, G., A. A. Olczak, J. P. Walton, and R. J. Maier. 2005. Contribution of the Helicobacter pylori thiol peroxidase bacterioferritin comigratory protein to oxidative stress resistance and host colonization. Infect. Immun. 73:378-384.