1887

Abstract

Members of the ferritin-like Dps protein family are found in a number of bacterial species, where they demonstrate the potential to bind iron, and have been implicated in tolerance to oxidative stress. In this study of the food-borne pathogen , the gene encoding a Dps homologue was deleted, and, compared to wild-type cells, it was found that the resulting mutant was less resistant to hydrogen peroxide, and demonstrated reduced survival following long-term (7–11 days) incubation in laboratory media. In view of this, it is shown that gene expression is controlled by the hydrogen peroxide regulator PerR, as well as the general stress sigma factor . When mutant cells were transferred to iron-limiting conditions, growth was retarded relative to wild-type cells, indicating that Fri may be required for iron storage. This notion is supported by the observation that the genome appears not to encode other ferritin-like proteins. Given the role of Fri in resistance to oxidative stress, and growth under iron-limiting conditions, the ability of the mutant to infect mice was examined. When injected by the intraperitoneal route, the mutant demonstrated a reduced capacity to proliferate in the organs of infected mice relative to the wild-type, whereas when the bacteria were supplied intravenously this effect was mitigated. In addition, the mutant was impaired in its ability to survive and grow in J774.A1 mouse macrophage cells. Thus, the data suggest that Fri contributes to the ability of to survive in environments where oxidative stress and low iron availability may impede bacterial proliferation.

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2005-03-01
2024-03-29
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References

  1. Abdul-Tehrani H., Hudson A. J., Chang Y. S., Timms A. R., Hawkins C., Williams J. M., Harrison P. M., Guest J. R., Andrews S. C. 1999; Ferritin mutants of Escherichia coli are iron deficient and growth impaired, and fur mutants are iron deficient. J Bacteriol 181:1415–1428
    [Google Scholar]
  2. Adams T. J., Vartivarian S., Cowart R. E. 1990; Iron acquisition systems of Listeria monocytogenes. Infect Immun 58:2715–2718
    [Google Scholar]
  3. Almirón M., Link A. J., Furlong D., Kolter R. 1992; A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli . Genes Dev 6:2646–2654 [CrossRef]
    [Google Scholar]
  4. Altuvia S., Almirón M., Huisman G., Kolter R., Storz G. 1994; The dps promoter is activated by OxyR during growth and by IHF and σS in stationary phase. Mol Microbiol 13:265–272 [CrossRef]
    [Google Scholar]
  5. Andrews S. C. 1998; Iron storage in bacteria. Adv Microb Physiol 40:281–351
    [Google Scholar]
  6. Antelmann H., Engelmann S., Schmid R., Sorokin A., Lapidus A., Hecker M. 1997; Expression of a stress- and starvation-induced dps/pexB-homologous gene is controlled by the alternative sigma factorσB in Bacillus subtilis . J Bacteriol 179:7251–7256
    [Google Scholar]
  7. Bockmann R., Dickneite C., Middendorf B., Goebel W., Sokolovic Z. 1996; Specific binding of the Listeria monocytogenes transcriptional regulator PrfA to target sequences requires additional factor(s) and is influenced by iron. Mol Microbiol 22:643–653 [CrossRef]
    [Google Scholar]
  8. Bozzi M., Mignogna G., Stefanini S., Barra D., Longhi C., Valenti P., Chiancone E. 1997; A novel non-heme iron-binding ferritin related to the DNA-binding proteins of the Dps family in Listeria innocua . J Biol Chem 272:3259–3265 [CrossRef]
    [Google Scholar]
  9. Brondsted L., Kallipolitis B. H., Ingmer H., Knochel S. 2003; kdpE and a putative RsbQ homologue contribute to growth of Listeria monocytogenes at high osmolarity and low temperature. FEMS Microbiol Lett 219:233–239 [CrossRef]
    [Google Scholar]
  10. Brown J. S., Holden D. W. 2002; Iron acquisition by Gram-positive bacterial pathogens. Microbes Infect 11:1149–1156
    [Google Scholar]
  11. Ceci P., Ilari A., Falvo E., Chiancone E. 2003; The Dps protein of Agrobacterium tumefaciens does not bind to DNA, but protects it towards oxidative cleavage. X-ray crystal structure, iron binding and hydroxyl-radical scavenging properties. J Biol Chem 278:20319–20326 [CrossRef]
    [Google Scholar]
  12. Chen L., Helmann J. D. 1995; Bacillus subtilis MrgA is a Dps (PexB) homologue: evidence for metalloregulation of an oxidative-stress gene. Mol Microbiol 18:295–300 [CrossRef]
    [Google Scholar]
  13. Cohen S. N., Chang A. C., Hsu L. 1972; Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA. Proc Natl Acad Sci U S A 69:2110–2114 [CrossRef]
    [Google Scholar]
  14. Conte M. P., Longhi C., Polidoro M. & 7 other authors; 1996; Iron availability affects entry of Listeria monocytogenes into the enterocyte-like cell line Caco-2. Infect Immun 64:3925–3929
    [Google Scholar]
  15. Conte M. P., Longhi C., Petrone G., Polidoro M., Valenti P., Seganti L. 2000; Modulation of actA gene expression in Listeria monocytogenes by iron. J Med Microbiol 49:681–683
    [Google Scholar]
  16. Coulanges V., André P., Vidon D. J. M. 1996; Esculetin antagonizes iron-chelating agents and increases the virulence of Listeria monocytogenes . Res Microbiol 147:677–685 [CrossRef]
    [Google Scholar]
  17. Cowart R. E., Foster B. G. 1985; Differential effects of iron on the growth of Listeria monocytogenes: minimum requirements and mechanism of acquisition. J Infect Dis 151:721–730 [CrossRef]
    [Google Scholar]
  18. Dramsi S., Biswas I., Maguin E., Braun L., Mastroeni P., Cossart P. 1995; Entry of Listeria monocytogenes into hepatocytes requires expression of inIB, a surface protein of the internalin multigene family. Mol Microbiol 16:251–261 [CrossRef]
    [Google Scholar]
  19. Dukan S., Nystrom T. 1998; Bacterial senescence: stasis results in increased and differential oxidation of cytoplasmic proteins leading to developmental induction of the heat shock regulon. Genes Dev 12:3431–3441 [CrossRef]
    [Google Scholar]
  20. Ermolaeva S., Karpova T., Novella S., Wagner M., Scortti M., Tartakovskii I, Vázquez-Boland J. A. 2003; A simple method for the differentiation of Listeria monocytogenes based on induction of lecithinase activity by charcoal. Int J Food Microbiol 82:87–94 [CrossRef]
    [Google Scholar]
  21. Farber J. M., Peterkin P. I. 2000; Listeria monocytogenes. In The Microbiological Safety and Quality of Foods pp. 1178–1232 Edited by Lund B. M., Baird-Parker T. C., Gould G. W. Gaithersberg, MD: Aspen Publishers;
    [Google Scholar]
  22. Forbes J. R., Gros P. 2001; Divalent-metal transport by NRAMP proteins at the interface of host–pathogen interactions. Trends Microbiol 9:397–403 [CrossRef]
    [Google Scholar]
  23. Fuangthong M., Helmann J. D. 2003; Recognition of DNA by three ferric uptake regulator (Fur) homologs in Bacillus subtilis. J Bacteriol 185:6348–6357 [CrossRef]
    [Google Scholar]
  24. Fuangthong M., Herbig A. F., Bsat N., Helmann J. D. 2002; Regulation of the Bacillus subtilis fur and perR genes by PerR: not all members of the PerR regulon are peroxide inducible. J Bacteriol 184:3276–3286 [CrossRef]
    [Google Scholar]
  25. Glaser P., Frangeul L., Buchrieser C. & 52 other authors; 2001; Comparative genomics of Listeria species. Science 294:849–852
    [Google Scholar]
  26. Grant R. A., Filman D. J., Finkel S. E., Kolter R., Hogle J. M. 1998; The crystal structure of Dps, a ferritin homolog that binds and protects DNA. Nat Struct Biol 5:294–303 [CrossRef]
    [Google Scholar]
  27. Gupta S., Chatterji D. 2003; Bimodal protection of DNA by Mycobacterium smegmatis Dps. J Biol Chem 278:5235–5241 [CrossRef]
    [Google Scholar]
  28. Gupta S., Pandit S. B., Srinivasan N., Chatterji D. 2002; Proteomics analysis of carbon-starved Mycobacterium smegmatis: induction of Dps-like protein. Protein Eng 15:503–511 [CrossRef]
    [Google Scholar]
  29. Halsey T. A., Vazquez-Torres A., Gravdahl D. J., Fang F. C., Libby S. J. 2004; The ferritin-like Dps protein is required for Salmonella enterica serovar Typhimurium oxidative stress resistance and virulence. Infect Immun 72:1155–1158 [CrossRef]
    [Google Scholar]
  30. Hartford T., O'Brien S., Andrew P. W., Jones D., Roberts I. S. 1993; Utilization of transferrin-bound iron by Listeria monocytogenes. FEMS Microbiol Lett 108:311–318 [CrossRef]
    [Google Scholar]
  31. Hébraud M., Guzzo J. 2000; The main cold shock protein of Listeria monocytogenes belongs to the family of ferritin-like proteins. FEMS Microbiol Lett 190:29–34 [CrossRef]
    [Google Scholar]
  32. Henle E. S., Linn S. 1997; Formation, prevention, and repair of DNA damage by iron/hydrogen peroxide. J Biol Chem 272:19095–19098 [CrossRef]
    [Google Scholar]
  33. Herbert K. C., Foster S. J. 2001; Starvation survival in Listeria monocytogenes: characterization of the response and the role of known and novel components. Microbiology 147:2275–2284
    [Google Scholar]
  34. Horton R. M., Cai Z. L., Ho S. N., Pease L. R. 1990; Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8:528–535
    [Google Scholar]
  35. Ilari A., Stefanini S., Chiancone E., Tsernoglou D. 2000; The dodecameric ferritin from Listeria innocua contains a novel intersubunit iron-binding site. Nat Struct Biol 7:38–43 [CrossRef]
    [Google Scholar]
  36. Ishikawa T., Mizunoe Y., Kawabata S., Takade A., Harada M., Wai S. N., Yoshida S. 2003; The iron-binding protein Dps confers hydrogen peroxide stress resistance to Campylobacter jejuni . J Bacteriol 185:1010–1017 [CrossRef]
    [Google Scholar]
  37. Kolter R., Siegele D. A., Tormo A. 1993; The stationary phase of the bacterial life cycle. Annu Rev Microbiol 47:855–874 [CrossRef]
    [Google Scholar]
  38. Leimeister-Wachter M., Chakraborty T. 1989; Detection of listeriolysin, the thiol-dependent hemolysin in Listeria monocytogenes, Listeria ivanovii, and Listeria seeligeri . Infect Immun 57:2350–2357
    [Google Scholar]
  39. Liu S., Graham J. E., Bigelow L., Morse P. D., Wilkinson B. J. 2002; Identification of Listeria monocytogenes genes expressed in response to growth at low temperature. Appl Environ Microbiol 68:1697–1705 [CrossRef]
    [Google Scholar]
  40. Lomovskaya O. L., Kidwell J. P., Matin A. 1994; Characterization of the σ38-dependent expression of a core Escherichia coli starvation gene,pexB . J Bacteriol 176:3928–3935
    [Google Scholar]
  41. Luo Y., Han Z., Chin S. M., Linn S. 1994; Three chemically distinct types of oxidants formed by iron-mediated Fenton reactions in the presence of DNA. Proc Natl Acad Sci U S A 91:12438–12442 [CrossRef]
    [Google Scholar]
  42. Martinez A., Kolter R. 1997; Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J Bacteriol 179:5188–5194
    [Google Scholar]
  43. Michán C., Manchado M., Dorado G., Pueyo C. 1999; In vivo transcription of the Escherichia coli oxyR regulon as a function of growth phase and in response to oxidative stress. J Bacteriol 181:2759–2764
    [Google Scholar]
  44. Nair S., Finkel S. E. 2004; Dps protects cells against multiple stesses during stationary phase. J Bacteriol 186:4192–4198 [CrossRef]
    [Google Scholar]
  45. Papinutto E., Dundon W. G., Pitulis N., Battistutta R., Montecucco C., Zanotti G. 2002; Structure of two iron-binding proteins from Bacillus anthracis. J Biol Chem 277:15093–15098 [CrossRef]
    [Google Scholar]
  46. Peña M. M. O., Bullerjahn G. S. 1995; The DpsA protein of Synechococcus sp. strain PCC7942 is a DNA-binding hemoprotein. J Biol Chem 270:22478–22482 [CrossRef]
    [Google Scholar]
  47. Phan-Thanh L., Gormon T. 1995; Analysis of heat and cold shock proteins in Listeria by two-dimensional electrophoresis. Electrophoresis 16:444–450 [CrossRef]
    [Google Scholar]
  48. Phan-Thanh L., Gormon T. 1997; A chemically defined minimal medium for the optimal culture of Listeria. Int J Food Microbiol 35:91–95 [CrossRef]
    [Google Scholar]
  49. Polidoro M., Biase D., de Montagnini B., Guarrera L., Cavallo S., Valenti P., Stefanini S., Chiancone E. 2002; The expression of the dodecameric ferritin in Listeria spp. is induced by iron limitation and stationary growth phase. Gene 296:121–128 [CrossRef]
    [Google Scholar]
  50. Portnoy D. A., Auerbuch V., Glomski I. J. 2002; The cell biology of Listeria monocytogenes infection: the intersection of bacterial pathogenesis and cell-mediated immunity. J Cell Biol 158:409–414 [CrossRef]
    [Google Scholar]
  51. Pulliainen A. T., Haataja S., Kahkonen S., Finne J. 2003; Molecular basis of H2O2 resistance mediated by streptococcal Dpr. Demonstration of the functional involvement of the putative ferroxidase center by site-directed mutagenesis in Streptococcus suis. J Biol Chem 278:7996–8005 [CrossRef]
    [Google Scholar]
  52. Rea R. B., Gahan C. G., Hill C. 2004; Disruption of putative regulatory loci in Listeria monocytogenes demonstrates a significant role for Fur and PerR in virulence. Infect Immun 72:717–727 [CrossRef]
    [Google Scholar]
  53. Sadowski P. 1986; Site-specific recombinases: changing partners and doing the twist. J Bacteriol 165:341–347
    [Google Scholar]
  54. Schaferkordt S., Chakraborty T. 1995; Vector plasmid for insertional mutagenesis and directional cloning in Listeria spp. Biotechniques 19:720–725
    [Google Scholar]
  55. Sword C. P. 1966; Mechanisms of pathogenesis in Listeria monocytogenes infection. Influence of iron. J Bacteriol 92:536–542
    [Google Scholar]
  56. Tonello F., Dundon W. G., Satin B., Molinari M., Tognon G., Grandi G., Del Giudice G., Rappuoli R., Montecucco C. 1999; The Helicobacter pylori neutrophil-activating protein is an iron-binding protein with dodecameric structure. Mol Microbiol 34:238–246 [CrossRef]
    [Google Scholar]
  57. Ueshima J., Shoji M., Ratnayake D. B., Abe K., Yoshida S., Yamamoto K., Nakayama K. 2003; Purification, gene cloning, gene expression, and mutants of Dps from the obligate anaerobe Porphyromonas gingivalis . Infect Immun 71:1170–1178 [CrossRef]
    [Google Scholar]
  58. Vázquez-Boland J. A., Kuhn M., Berche P., Chakraborty T., Dominguez-Bernal G., Goebel W., Gonzalez-Zorn B., Wehland J., Kreft J. 2001; Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14:584–640 [CrossRef]
    [Google Scholar]
  59. Wai S. N., Nakayama K., Umene K., Moriya T., Amako K. 1996; Construction of a ferritin-deficient mutant of Campylobacter jejuni: contribution of ferritin to iron storage and protection against oxidative stress. Mol Microbiol 20:1127–1134 [CrossRef]
    [Google Scholar]
  60. Watson S. P., Clements M. O., Foster S. J. 1998; Characterization of the starvation-survival response of Staphylococcus aureus. J Bacteriol 180:1750–1758
    [Google Scholar]
  61. Wolf S. G., Frenkiel D., Arad T., Finkel S. E., Kolter R., Minsky A. 1999; DNA protection by stress-induced biocrystallization. Nature 400:83–85 [CrossRef]
    [Google Scholar]
  62. Yamamoto Y., Poole L. B., Hantgan R. R., Kamio Y. 2002; An iron-binding protein, Dpr, from Streptococcus mutans prevents iron-dependent hydroxyl radical formation in vitro . J Bacteriol 184:2931–2939 [CrossRef]
    [Google Scholar]
  63. Zhao G., Ceci P., Ilari A., Giangiacomo L., Laue T. M., Chiancone E., Chasteen N. D. 2002; Iron and hydrogen peroxide detoxification properties of DNA-binding protein from starved cells. A ferritin-like DNA-binding protein of Escherichia coli . J Biol Chem 277:27689–27696 [CrossRef]
    [Google Scholar]
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