1887

Abstract

It is known that the Fur protein negatively regulates iron-uptake systems in different bacterial species, including . In this study it has been shown that the intracellular concentration of cyclic AMP (cAMP) is lower in a knockout mutant than in the wild-type strain. According to this, the expression of two cAMP-regulated genes, such as (encoding an α-aspartyl dipeptidase) and the operon, is decreased in cells in comparison with wild-type cells. Introduction of an additional mutation in , encoding a cyclic 3′,5′-cAMP phosphodiesterase, recovers wild-type intracellular cAMP concentration in the mutant. Likewise, expression of and the operon was the same in the double mutant and the wild-type strain. Moreover, these results also demonstrate that the Fur protein positively regulates the expression of the master operon governing the flagellar regulon. This positive control must be mediated by binding of the Fur protein to the promoter as indicated by the fact that this promoter tests positive in a Fur titration assay.

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2002-04-01
2019-10-22
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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. Bagg, A. & Neilands, J. B. ( 1987; ). Ferric uptake regulation protein acts as a repressor, employing iron (II) as a cofactor to bind the operator of an iron transport operon in Escherichia coli. Biochemistry 26, 5471-5477.[CrossRef]
    [Google Scholar]
  3. Bertin, P., Terao, E., Lee, E. H., Lejeune, P., Colson, C., Danchin, A. & Collatz, E. ( 1994; ). The H-NS protein is involved in the biogenesis of flagella in Escherichia coli. J Bacteriol 176, 5537-5540.
    [Google Scholar]
  4. Björkman, J., Hughes, D. & Andersson, D. I. ( 1998; ). Virulence of antibiotic-resistant Salmonella typhimurium. Proc Natl Acad Sci USA 95, 3949-3953.[CrossRef]
    [Google Scholar]
  5. Bosch, M., Tarragó, R., Garrido, M. E., Campoy, S., Fernandez de Henestrosa, A. R., Perez de Rozas, A., Badiola, I. & Barbé, J. ( 2001; ). Expression of the Pasteurella multocida ompH gene is negatively regulated by the Fur protein. FEMS Microbiol Lett 203, 35-40.[CrossRef]
    [Google Scholar]
  6. Chilcott, G. S. & Hughes, K. T. ( 2000; ). Coupling of flagellar gene expression to flagellar assembly in Salmonella enterica serovar Typhimurium and Escherichia coli. Microbiol Mol Biol Rev 64, 694-708.[CrossRef]
    [Google Scholar]
  7. Conlin, C. A., Hakenson, K., Liljas, A. & Miller, C. G. ( 1994; ). Cloning and nucleotide sequence of the cyclic AMP receptor protein-regulated Salmonella typhimurium pepE gene and crystallization of its product, an α-aspartyl dipeptidase. J Bacteriol 176, 166-172.
    [Google Scholar]
  8. Curtiss, R.III & Kelly, S. M. ( 1987; ). Salmonella typhimurium deletion mutants lacking adenylate cyclase and cyclic AMP receptor protein are avirulent and immunogenic. Infect Immun 64, 663-673.
    [Google Scholar]
  9. Davis, R. W., Botstein, D. & Roth, J. R. (1980). Advanced Bacterial Genetics. A Manual for Genetic Engineering. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  10. Delany, I., Spohn, G., Rappuoli, R. & Scarlato, V. ( 2001; ). The Fur repressor controls transcription of iron-activated and -repressed genes in Helicobacter pylori. Mol Microbiol 42, 1297-1309.
    [Google Scholar]
  11. de Lorenzo, V., Herrero, M., Jakubzik, U. & Timmis, K. N. ( 1990; ). Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in Gram-negative eubacteria. J Bacteriol 172, 6568-6572.
    [Google Scholar]
  12. Ditta, G., Schmidhauser, T., Yakobson, E., Lu, P., Liang, X. W., Finlay, D. R., Guiney, D. & Helinski, D. R. ( 1985; ). Plasmids related to the broad host range vector, pRK290, useful for gene cloning and for monitoring gene expression. Plasmid 13, 149-153.[CrossRef]
    [Google Scholar]
  13. Dubrac, S. & Touati, D. ( 2000; ). Fur positive regulation of iron superoxide dismutase in Escherichia coli: functional analysis of the sodB promoter. J Bacteriol 182, 3802-3808.[CrossRef]
    [Google Scholar]
  14. Ernst, J. F., Bennett, R. L. & Rothfield, L. L. ( 1978; ). Constitutive expression of the iron-enterochelin and ferrichrome uptake systems in a mutant strain of Salmonella typhimurium. J Bacteriol 135, 928-934.
    [Google Scholar]
  15. Escolar, L., Perez-Martı́n, J. & de Lorenzo, V. ( 1999; ). Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181, 6223-6229.
    [Google Scholar]
  16. Ferreiros, C. M., Criado, M. T., del Rio, M. C. & Pintor, M. ( 1990; ). Analysis of the expression of outer-membrane proteins in Neisseria meningitidis in iron-replete and iron-deficient media. FEMS Microbiol Lett 71, 49-54.[CrossRef]
    [Google Scholar]
  17. Foster, J. W. & Hall, H. K. ( 1992; ). Effect of Salmonella typhimurium ferric uptake regulator (fur) mutations on iron- and pH-regulated protein synthesis. J Bacteriol 174, 4317-4323.
    [Google Scholar]
  18. Garcia del Portillo, F., Foster, J. W. & Finlay, B. B. ( 1993; ). Role of acid tolerance response genes in Salmonella typhimurium virulence. J Bacteriol 61, 4489-4492.
    [Google Scholar]
  19. Gelfand, M. S., Novichkov, P. S., Novichkova, E. S. & Mironov, A. A. ( 2000; ). Comparative analysis of regulatory patterns in bacterial genetics. Brief Bioinform 1, 357-371.[CrossRef]
    [Google Scholar]
  20. Hall, H. K. & Foster, J. W. ( 1996; ). The role of Fur in the acid tolerance response of Salmonella typhimurium is physiologically and genetically separable from its role in iron acquisition. J Bacteriol 178, 5683-5691.
    [Google Scholar]
  21. Hantke, K. ( 1984; ). Cloning of the repressor protein gene of iron regulated system in Escherichia coli K-12. Mol Gen Genet 197, 337-341.[CrossRef]
    [Google Scholar]
  22. Hantke, K. ( 1987; ). Selection procedure for deregulated iron transport mutants (fur) in Escherichia coli K12: fur not only affects iron metabolism. Mol Gen Genet 210, 135-139.[CrossRef]
    [Google Scholar]
  23. 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]
  24. Herrero, M., de Lorenzo, V. & Timmis, K. N. ( 1990; ). Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion on foreign genes in Gram-negative bacteria. J Bacteriol 172, 6557-6567.
    [Google Scholar]
  25. Imamura, R., Yamanaka, K., Ogura, T., Hiraga, S., Fukita, N., Ishihama, A. & Niki, H. ( 1996; ). Identification of the cpdA gene encoding cyclic 3′,5′-adenosine monophosphate phosphodiesterase in Escherichia coli. J Biol Chem 271, 25423-25429.[CrossRef]
    [Google Scholar]
  26. Ishizuka, H., Hanamura, A., Kunimura, T. & Aiba, H. ( 1993; ). A lowered concentration of cAMP receptor protein caused by glucose is an important determinant for catabolite repression in Escherichia coli. Mol Microbiol 10, 341-350.[CrossRef]
    [Google Scholar]
  27. Kolb, A., Busby, S., Buc, H., Gargres, S. & Adhya, S. ( 1993; ). Transcriptional regulation by cAMP and its receptor protein. Annu Rev Biochem 62, 749-795.[CrossRef]
    [Google Scholar]
  28. Kutsukake, K., Ohya, Y. & Iino, T. ( 1990; ). Transcriptional analysis of the flagellar regulon of Salmonella typhimurium. J Bacteriol 172, 741-747.
    [Google Scholar]
  29. Jordan, A., Aragall, E., Gibert, I. & Barbé, J. ( 1996; ). Promoter identification and expression analysis of Salmonella typhimurium and Escherichia coli nrdEF operons encoding one of two class I ribonucleotide reductases present in both bacteria. Mol Microbiol 19, 777-790.[CrossRef]
    [Google Scholar]
  30. Laemmli, U. K. ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.[CrossRef]
    [Google Scholar]
  31. Lee, J. K. & Kaplan, S. ( 1992; ). cis-acting regulatory elements involved in oxygen and light control of puc operon transcription in Rhodobacter sphaeroides. J Bacteriol 174, 1146-1157.
    [Google Scholar]
  32. Liu, X. & Matsumura, P. ( 1994; ). The FlhD/FlhC complex, a transcriptional activator of the Escherichia coli flagellar class II operons. J Bacteriol 176, 7345-7351.
    [Google Scholar]
  33. Miller, J. H. (1991). A Short Course in Bacterial Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  34. Nielsen, L. D., Monard, D. & Rickenberg, H. V. ( 1973; ). Cyclic 3′,5′-adenosine monophosphate phosphodiesterase of Escherichia coli. J Bacteriol 116, 857-866.
    [Google Scholar]
  35. Ohnishi, K., Kutsukake, K., Suzuki, H. & Iino, T. ( 1990; ). Gene fliA encodes an alternative sigma factor specific for flagellar operon in Salmonella typhimurium. Mol Gen Genet 221, 139-147.
    [Google Scholar]
  36. Prentki, P. & Krisch, H. M. ( 1984; ). In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29, 303-313.[CrossRef]
    [Google Scholar]
  37. Ratledge, C. & Dover, L. G. ( 2000; ). Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54, 881-941.[CrossRef]
    [Google Scholar]
  38. Saier, M. H., Feucht, B. U. & McCaman, M. T. ( 1975; ). Regulation of intracellular adenosyne cyclic 3′:5′-monophosphate levels in Escherichia coli and Salmonella typhimurium. J Biol Chem 250, 7593-7601.
    [Google Scholar]
  39. Schwyn, B. & Neilands, J. B. ( 1987; ). Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160, 47-56.[CrossRef]
    [Google Scholar]
  40. Silverman, M. & Simon, M. ( 1974; ). Characterization of Escherichia coli flagellar mutants that are insensitive to catabolite repression. J Bacteriol 120, 1196-1203.
    [Google Scholar]
  41. Stojiljkovic, I., Bäumer, A. J. & Hantke, K. ( 1994; ). Fur regulon in Gram-negative bacteria. J Mol Biol 236, 531-545.[CrossRef]
    [Google Scholar]
  42. Touati, D., Jacques, M., Tardat, B., Bouchard, L. & Despied, S. ( 1995; ). Lethal oxidative damage and mutagenesis are generated by iron in Δfur mutants of Escherichia coli: protective role of superoxide dismutase. J Bacteriol 177, 2305-2314.
    [Google Scholar]
  43. Tsolis, R. M., Bäumler, A. J., Stojilkovic, I. & Heffron, F. ( 1995; ). Fur regulon of Salmonella typhimurium: identification of new iron-regulated genes. J Bacteriol 177, 4628-4637.
    [Google Scholar]
  44. Wilmes-Riesemberg, M. R., Bearson, B., Foster, J. W. & Curtiss, R.III ( 1996; ). Role of the acid tolerance response in virulence of Salmonella typhimurium. J Bacteriol 64, 1085-1092.
    [Google Scholar]
  45. Yokota, T. & Gots, J. S. ( 1970; ). Requirement of adenosine 3′,5′-cyclic phosphate for flagellum formation in Escherichia coli and Salmonella typhimurium. J Bacteriol 103, 513-516.
    [Google Scholar]
  46. Zheng, M., Doan, B., Schneider, T. D. & Storz, G. ( 1999; ). OxyR and SoxRS regulation of fur. J Bacteriol 181, 4639-4643.
    [Google Scholar]
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