Structural, functional and mutational analysis of the pfr gene encoding a ferritin from Helicobacter pylori

Microbiology

Volumn 144, Issue 9, 1998, Pages 2505-2516

  Bereswill, Stefan ^a   Waidner, Uta ^a   Odenbreit, Stefan ^b   Lichte, Flavia ^a   Fassbinder, Frank ^a   Bode, Günter ^c   Kist, Manfred ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF ULM   (Germany)

Author keywords

Helicobacter pylori; Iron sequestration; Metal resistance; Prokaryotic ferritin

Indexed keywords

COPPER; FERRITIN; IRON; MANGANESE;

ARTICLE; BACTERIAL GENE; ELECTRON MICROSCOPY; ESCHERICHIA COLI; GENE DELETION; GENE INSERTION; GENE MUTATION; GENE STRUCTURE; HELICOBACTER PYLORI; IMMUNOBLOTTING; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; TRANSCRIPTION INITIATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HELICOBACTER PYLORI; NEGIBACTERIA; PROKARYOTA;

EID: 0031685512     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/00221287-144-9-2505     Document Type: Article

References (53)

1. Asaka, M., Kimura, T., Kato, M., Kudo, M., Miki, K., Ogoshi, K., Kato, T., Tatsuga, M. & Graham, D. Y. (1994). Possible role of Helicobacter infection in early gastric cancer development. Cancer 73, 2691-2694.
2. Atherton, J. C., Cao, P., Peek, R. M., Tummuru, M. K. R., Blaser, J. M. & Cover, T. L. (1995). Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. J Biol Chem 270, 17771-17777.
3. Bereswill, S. & Geider, K. (1997). Characterization of the rcsB gene from Erwinia amylovora and its influence on exopolysaccharide synthesis and virulence of the fire blight pathogen. J Bacteriol 179, 1354-1361.
4. Bereswill, S., Fassbinder, F., Voelzing, C., Haas, R., Reuter, K., Ficner, R. & Kist, M. (1997a). Cloning and functional characterization of the genes encoding 3-dehydroquinate synthase (aroB) and tRNA-guanine transglycosylase (tgt) from Helicobacter pylori. Med Microbiol Immunol 186, 125-134.
5. Bereswill, S., Strobel, S., Lichte, F., Fassbinder, F. & Kist, M. (1997b). Evaluation of microbiological parameters for the study of iron metabolism in Helicobacter pylori. Gut 41 (Suppl. 1), A10.
6. Bereswill, S., Fassbinder, F., Voelzing, C., Covacci, A., Haas, R. & Kist, M. (1998a). Hemolytic properties and riboflavin synthesis of Helicobacter pylori: cloning and functional characterization of the ribA gene encoding GTP-cyclohydrolase II that confers hemolytic activity to Escherichia coli. Med Microbiol Immunol 186, 177-187.
7. Bereswill, S., Lichte, F., Vey, T., Fassbinder, F. & Kist, M. (1998b). Cloning and characterization of the fur gene from Helicobacter pylori. FEMS Microbiology Lett 159, 193-200.
8. Bezkorovainy, A. (1987). Iron proteins. In Iron and Infection: Molecular, Physiological and Clinincal Aspects, pp. 51-55. Chichester: Wiley.
9. Bode, G., Mauch, F., Ditschuneit, H. & Malfertheiner, P. (1993). Identification of structures containing polyphosphate in Helicobacter pylori. J Gen Microbiol 139, 3029-3033.
10. Buck, G. E. (1990). Camplyobacter pylori and gastroduoenal disease, Clin Microbiol Rev 3, 1-12.
11. Bukanov, N. O. & Berg, D. E. (1994). Ordered cosmid library and high resolution physical genetic map of Helicobacter pylori strain NCTC 11638. Mol Microbiol 11, 509-523.
12. Censini, S., Lange, C., Xiang, Z., Crabtree, J. E., Ghiara, P., Borodovsky, M., Rappuoli, R. & Covacci, A. (1996). Cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci USA 93, 14648-14653.
13. Chirgwin, J. M., Przybyla, A. E., MacDonald, R. J. & Rutter, W. J. (1979). Isolation of biological active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18, 5294-5299.
14. Dhaenens, L., Szczebara, F. & Husson, M. O. (1997). Identification, characterization, and immunogenicity of the lactoferrin-binding protein from Helicobacter pylori. Infect Immun 65, 514-518.
15. Doig, P. J., Austin, W. & Trust , T. J. (1993). The Helicobacter pylori 19·6-kilodalton protein is an iron-containing protein resembling ferritin. J Bacteriol 175, 557-560.
16. Earhart, C. F. (1996). Uptake and metabolism of iron and molybdenum. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, 2nd edn, vol. I, pp. 1075-1090. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
17. Evans, D. J., Evans, D. G., Takemura, T., Nakano, H., Lampert, H. C. and Graham, D. Y. (1995a). Characterization of a Helicobacter pylori neutrophil-activating protein. Infect Immun 63, 2213-2220.
18. Evans, D. J., Evans, D. G., Lampert, H. C. & Nakano, H. (1995b). Identification of four new prokaryotic bacterioferritins, from Helicobacter pylori, Anabaena variabilis, Bacillus subtilis and Treponema pallidum, by analysis of gene sequences. Gene 153, 123-127.
19. Forman, D. (1996). Helicobacter pylori and gastric cancer. Scand J Gastroenterol 220, 23-26.
20. Frazier, B. A., Peifer, J. D., Russell, D. G., Falk, P., Olsen, A. N., Hammar, M., Westblom, T. U. & Normark, S. J. (1993). Paracrystalline inclusions of a novel ferritin containing nonheme iron, produced by the human gastric pathogen Helicobacter pylori: evidence for a third class of ferritins. J Bacteriol 175, 966-972.
21. Genco, C. A. & Desai, P. J. (1996). Iron acquisition in the pathogenic Neisseria. Trends Microbiol 4, 179-184.
22. Harrison, P. M. & Arioso, P. (1996). The ferritins: molecular properties, iron storage function and cellular regulation. Biochim Biophys Acta 1275, 161-203.
23. Hempstead, P. D., Hudson, A. J., Artyniuk, P. J., Andrews, S. C., Banfield, M. J., Guest, J. R. & Harrison, P. M. (1994). Direct observation of the iron-binding sites in a ferritin. FEBS Lett 350, 258-262.
24. Hughes, N. J., Kelly, D. J., Clayton, C. L. & Chalk, P. A. (1997). Helicobacter pylori porCDAB and oorDABC genes encode distinct pyruvate:flavodoxin and 2-oxoglutarate:acceptor oxidoreductases which mediate electron transport to NADP. J Bacteriol 180, 1119-1128.
25. Husson, M. O., Legrand, D., Spik, G. & Leclerc, H. (1993). Iron acquisition by Helicobacter pylori: importance of human lactoferrin. Infect Immun 61, 2694-2697.
26. Izuhara, M., Takamune, K. & Takata, R. (1991). Cloning and sequencing of an Escherichia coli gene which encodes a polypeptide having similarity to the human ferritin H subunit. Mol Gen Genet 225, 510-513.
27. Jiang, Q., Hiratsuka, K. & Taylor, D. E. (1996). Variability of gene order in different Helicobacter pylori strains contributes to genome diversity. Mol Microbiol 20, 833-842.
28. Kahrs, A. F., Odenbreit, S., Schmitt, W., Heuermann, D., Meyer, T. F. & Haas, R. (1995). An improved TnMax mini-transposon system suitable for sequencing, shuttle mutagenesis and gene fusions. Gene 167, 53-57.
29. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature 227, 680-685.
30. Lee, A., Fox, J. & Hazell, S. (1993). Pathogenicity of Helicobacter pylori: a perspective. Infect Immun 61, 1601-1610.
31. Litwin, C. M. & Calderwood, S. B. (1993). Role of iron in regulation of virulence genes. Clin Microbiol Rev 6, 137-149.
32. Miller, J. H. (1972). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
33. Miller, R. A. & Britigan, B. E. (1997). Role of oxidants in microbial pathophysiology. Clin Microbiol Rev 10, 1-18.
34. Odenbreit, S., Till, M. & Haas, R. (1996a). Optimized BlaM-transposon shuttle mutagenesis of Helicobacter pylori allows the identification of novel genetic loci involved in bacterial virulence. Mol Microbiol 20, 361-373.
35. Odenbreit, S., Wieland, B. & Haas, R. (1996b). Cloning and genetic characterization of Helicobacter pylori catalase and construction of a catalase-deficient mutant strain. J Bacteriol 178, 6960-6967.
36. Pohlner, J., Krämer, J. & Meyer, T. F. (1993). A plasmid system for high-level expression and in vitro processing of recombinant proteins. Gene 130, 121-126.
37. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
38. Schaeffer, S., Hantke, K. & Braun, V. (1985). Nucleotide sequence of the iron regulatory gene fur. Mol Gen Genet 200, 110-113.
39. Southern, E. M. (1975). Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98, 503.
40. Spiegelhalder, C., Gerstenecker, B., Kersten, A., Schiltz, E. & Kist, M. (1993). Purification of Helicobacter pylori Superoxide dismutase and cloning and sequencing of the gene. Infect Immun 61, 5315-5325.
41. Stojiljkovic, I., Bäumler, A. J. & Hantke, K. (1994). Fur regulon in gram-negative bacteria: identification and characterization of new iron-regulated Escherichia coli genes by a fur titration assay. J Mol Biol 236, 531-545.
42. Strobel, S., Bereswill, S., Allgaier, P., Balig, P., Sonntag, H.-G. & Kist, M. (1998). Identification and analysis of a new vacA genotype variant of Helicobacter pylori in different patient groups in Germany. J Clin Microbiol 36, 1285-1289.
43. Taylor, D. E. (1996). Diversity among Helicobacter pylori isolates. J Clin Microbiol 34, 1041.
44. Tomb, J. F., White, O., Kerlavage, A. R. & other authors (1997). The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388, 539-547.
45. Touati, D., Jacques, M., Tardat, B., Bouchard, L. & Despied, S. (1995). Lethal oxidative damage and mutagenesis are generated by iron in DELTA-fur mutants of Escherichia coli: protective role of Superoxide dismutase. J Bacteriol 177, 2305-2314.
46. Velayudhan, J., Hughes, N. J., Andrews, S. C., Clayton, C. L. & Kelly, D. J. (1997). Iron acquisition in Helicobacter pylori: characterization of tbpA, fecA, and exbB homologues. Gut 41 (Suppl. 1), A109.
47. Wai, S. N., Takata, T., Takade, A., Hamasaki, N. & Amako, K. (1995). Purification and characterization of ferritin from Campylobacter jejuni. Arch Microbiol 164, 1-6.
48. 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.
49. Wai, S. N., Nakayama, K., Takade, A. & Amako, K. (1997). Overproduction of Campylobacter ferritin in Escherichia coli and induction of paracrystalline inclusions by ferrous compound. Microbiol Immunol 41, 461-467.
50. Worst, D. J., Otto, B. R. & de Graaff, J. (1995). Iron-repressible outer membrane proteins of Helicobacter pylori involved in heme uptake. Infect Immun 63, 4161-4165.
51. Worst, D. J., Sparrius, M., Kuipers, E. J., Kusters, J. G. & de Graaff, J. (1996). Human serum antibody response against iron-repressible outer membrane proteins of Helicobacter pylori. FEMS Microbiol Lett 144, 29-32.
52. Yariv, J., Kalb, A. J., Sperling, R., Bauminger, E. R., Cohen, S. G. & Ofer, S. (1981). The composition and the structure of the bacterioferritin of Escherichia coli. Biochem J 197, 171-175.
53. Zimmermann, L., Angerer, A. & Braun, V. (1989). Mechanistically novel iron-III transport system in Serratia marcescens. J Bacteriol 171, 238-243.