This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Waidner, B.
Right arrow Articles by Bereswill, S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Waidner, B.
Right arrow Articles by Bereswill, S.

 Previous Article  |  Next Article 

Infection and Immunity, July 2002, p. 3923-3929, Vol. 70, No. 7
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.7.3923-3929.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Essential Role of Ferritin Pfr in Helicobacter pylori Iron Metabolism and Gastric Colonization

Barbara Waidner,1 Stefan Greiner,1 Stefan Odenbreit,2 Holger Kavermann,2 Jyoti Velayudhan,3 Frank Stähler,1,4 Johannes Guhl,1 Emmanuel Bissé,5 Arnoud H. M. van Vliet,6 Simon C. Andrews,7 Johannes G. Kusters,6 David J. Kelly,3 Rainer Haas,2 Manfred Kist,1 and Stefan Bereswill1*

Institute of Medical Microbiology and Hygiene, Department of Medical Microbiology and Hygiene, University Hospital of Freiburg,1 Faculty of Biology III, University of Freiburg, D-79104 Freiburg,4 Max von Pettenkofer Institute for Hygiene and Medical Microbiology, Ludwig-Maximilians University Munich, Munich,2 Central Laboratory Unit, University Hospital of Freiburg, D-79106 Freiburg, Germany,5 Department of Gastroenterology and Hepatology, Erasmus Medical Center, 3015 GD Rotterdam, The Netherlands,6 Department of Molecular Biology and Biotechnology, University of Sheffield, Western Bank, Sheffield S10 2TN,3 School of Animal and Microbial Sciences, University of Reading, Whiteknights, Reading RG6 6AJ, United Kingdom7

Received 26 December 2001/ Returned for modification 19 March 2002/ Accepted 2 April 2002

The reactivity of the essential element iron necessitates a concerted expression of ferritins, which mediate iron storage in a nonreactive state. Here we have further established the role of the Helicobacter pylori ferritin Pfr in iron metabolism and gastric colonization. Iron stored in Pfr enabled H. pylori to multiply under severe iron starvation and protected the bacteria from acid-amplified iron toxicity, as inactivation of the pfr gene restricted growth of H. pylori under these conditions. The lowered total iron content in the pfr mutant, which is probably caused by decreased iron uptake rates, was also reflected by an increased resistance to superoxide stress. Iron induction of Pfr synthesis was clearly diminished in an H. pylori feoB mutant, which lacked high-affinity ferrous iron transport, confirming that Pfr expression is mediated by changes in the cytoplasmic iron pool and not by extracellular iron. This is well in agreement with the recent discovery that iron induces Pfr synthesis by abolishing Fur-mediated repression of pfr transcription, which was further confirmed here by the observation that iron inhibited the in vitro binding of recombinant H. pylori Fur to the pfr promoter region. The functions of H. pylori Pfr in iron metabolism are essential for survival in the gastric mucosa, as the pfr mutant was unable to colonize in a Mongolian gerbil-based animal model. In summary, the pfr phenotypes observed give new insights into prokaryotic ferritin functions and indicate that iron storage and homeostasis are of extraordinary importance for H. pylori to survive in its hostile natural environment.

* Corresponding author. Mailing address: Department of Medical Microbiology, Institute of Medical Microbiology and Hygiene, University Hospital Freiburg, Hermann-Herder-Str. 11, D-79104 Freiburg, Germany. Phone: 49-761-203-6539. Fax: 49-761-203-6562. E-mail: bereswil{at}ukl.uni-freiburg.de.

Editor: J. T. Barbieri

Infection and Immunity, July 2002, p. 3923-3929, Vol. 70, No. 7
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.7.3923-3929.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Wang, S.-W., Chen, C.-Y., Tseng, J. T., Liang, S.-H., Chen, S.-C., Hsieh, C., Chen, Y.-h., Chen, C.-C. (2009). orf4 of the Bacillus cereus sigB Gene Cluster Encodes a General Stress-Inducible Dps-Like Bacterioferritin. J. Bacteriol. 191: 4522-4533 [Abstract] [Full Text]  
  • Kitphati, W., Ngok-ngam, P., Suwanmaneerat, S., Sukchawalit, R., Mongkolsuk, S. (2007). Agrobacterium tumefaciens fur Has Important Physiological Roles in Iron and Manganese Homeostasis, the Oxidative Stress Response, and Full Virulence. Appl. Environ. Microbiol. 73: 4760-4768 [Abstract] [Full Text]  
  • Belzer, C., van Schendel, B. A. M., Kuipers, E. J., Kusters, J. G., van Vliet, A. H. M. (2007). Iron-Responsive Repression of Urease Expression in Helicobacter hepaticus Is Mediated by the Transcriptional Regulator Fur. Infect. Immun. 75: 745-752 [Abstract] [Full Text]  
  • Baldwin, D. N., Shepherd, B., Kraemer, P., Hall, M. K., Sycuro, L. K., Pinto-Santini, D. M., Salama, N. R. (2007). Identification of Helicobacter pylori Genes That Contribute to Stomach Colonization. Infect. Immun. 75: 1005-1016 [Abstract] [Full Text]  
  • Wang, G., Hong, Y., Olczak, A., Maier, S. E., Maier, R. J. (2006). Dual Roles of Helicobacter pylori NapA in Inducing and Combating Oxidative Stress. Infect. Immun. 74: 6839-6846 [Abstract] [Full Text]  
  • Kusters, J. G., van Vliet, A. H. M., Kuipers, E. J. (2006). Pathogenesis of Helicobacter pylori Infection. Clin. Microbiol. Rev. 19: 449-490 [Abstract] [Full Text]  
  • Stahler, F. N., Odenbreit, S., Haas, R., Wilrich, J., Vliet, A. H. M. V., Kusters, J. G., Kist, M., Bereswill, S. (2006). The Novel Helicobacter pylori CznABC Metal Efflux Pump Is Required for Cadmium, Zinc, and Nickel Resistance, Urease Modulation, and Gastric Colonization. Infect. Immun. 74: 3845-3852 [Abstract] [Full Text]  
  • Sgouros, S N, Bergele, C (2006). Clinical outcome of patients with Helicobacter pylori infection: the bug, the host, or the environment?. Postgrad. Med. J. 82: 338-342 [Abstract] [Full Text]  
  • Gancz, H., Censini, S., Merrell, D. S. (2006). Iron and pH Homeostasis Intersect at the Level of Fur Regulation in the Gastric Pathogen Helicobacter pylori. Infect. Immun. 74: 602-614 [Abstract] [Full Text]  
  • Mey, A. R., Wyckoff, E. E., Kanukurthy, V., Fisher, C. R., Payne, S. M. (2005). Iron and Fur Regulation in Vibrio cholerae and the Role of Fur in Virulence. Infect. Immun. 73: 8167-8178 [Abstract] [Full Text]  
  • Ernst, F. D., Kuipers, E. J., Heijens, A., Sarwari, R., Stoof, J., Penn, C. W., Kusters, J. G., van Vliet, A. H. M. (2005). The Nickel-Responsive Regulator NikR Controls Activation and Repression of Gene Transcription in Helicobacter pylori. Infect. Immun. 73: 7252-7258 [Abstract] [Full Text]  
  • Thiele, I., Vo, T. D., Price, N. D., Palsson, B. O. (2005). Expanded Metabolic Reconstruction of Helicobacter pylori (iIT341 GSM/GPR): an In Silico Genome-Scale Characterization of Single- and Double-Deletion Mutants. J. Bacteriol. 187: 5818-5830 [Abstract] [Full Text]  
  • Waidner, B., Melchers, K., Stahler, F. N., Kist, M., Bereswill, S. (2005). The Helicobacter pylori CrdRS Two-Component Regulation System (HP1364/HP1365) Is Required for Copper-Mediated Induction of the Copper Resistance Determinant CrdA. J. Bacteriol. 187: 4683-4688 [Abstract] [Full Text]  
  • Ernst, F. D., Homuth, G., Stoof, J., Mader, U., Waidner, B., Kuipers, E. J., Kist, M., Kusters, J. G., Bereswill, S., van Vliet, A. H. M. (2005). Iron-Responsive Regulation of the Helicobacter pylori Iron-Cofactored Superoxide Dismutase SodB Is Mediated by Fur. J. Bacteriol. 187: 3687-3692 [Abstract] [Full Text]  
  • Ernst, F. D., Bereswill, S., Waidner, B., Stoof, J., Mader, U., Kusters, J. G., Kuipers, E. J., Kist, M., van Vliet, A. H. M., Homuth, G. (2005). Transcriptional profiling of Helicobacter pylori Fur- and iron-regulated gene expression. Microbiology 151: 533-546 [Abstract] [Full Text]  
  • Thompson, L. J., Danon, S. J., Wilson, J. E., O'Rourke, J. L., Salama, N. R., Falkow, S., Mitchell, H., Lee, A. (2004). Chronic Helicobacter pylori Infection with Sydney Strain 1 and a Newly Identified Mouse-Adapted Strain (Sydney Strain 2000) in C57BL/6 and BALB/c Mice. Infect. Immun. 72: 4668-4679 [Abstract] [Full Text]  
  • Rocha, E. R., Smith, C. J. (2004). Transcriptional regulation of the Bacteroides fragilis ferritin gene (ftnA) by redox stress. Microbiology 150: 2125-2134 [Abstract] [Full Text]  
  • Merrell, D. S., Thompson, L. J., Kim, C. C., Mitchell, H., Tompkins, L. S., Lee, A., Falkow, S. (2003). Growth Phase-Dependent Response of Helicobacter pylori to Iron Starvation. Infect. Immun. 71: 6510-6525 [Abstract] [Full Text]  
  • Cooksley, C., Jenks, P. J., Green, A., Cockayne, A., Logan, R. P. H., Hardie, K. R. (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 [Abstract] [Full Text]  
  • van Vliet, A. H. M., Stoof, J., Poppelaars, S. W., Bereswill, S., Homuth, G., Kist, M., Kuipers, E. J., Kusters, J. G. (2003). Differential Regulation of Amidase- and Formamidase-mediated Ammonia Production by the Helicobacter pylori Fur Repressor. J. Biol. Chem. 278: 9052-9057 [Abstract] [Full Text]  
  • Waidner, B., Melchers, K., Ivanov, I., Loferer, H., Bensch, K. W., Kist, M., Bereswill, S. (2002). Identification by RNA Profiling and Mutational Analysis of the Novel Copper Resistance Determinants CrdA (HP1326), CrdB (HP1327), and CzcB (HP1328) in Helicobacter pylori. J. Bacteriol. 184: 6700-6708 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»