1887

Abstract

To study the role of carbohydrates, in particular glucose, glucose 6-phosphate and mannose, as carbon substrates for extra- and intracellular replication of facultative intracellular enteric bacteria, mutants of two enteroinvasive (EIEC) strains and a serovar Typhimurium isolate were constructed that were defective in the uptake of glucose and mannose (Δ, ), glucose 6-phosphate (Δ) or all three carbohydrates (Δ, , ). The ability of these mutants to grow in RPMI medium containing the respective carbohydrates and in Caco-2 cells was compared with that of the corresponding wild-type strains. In the three strains, deletions of , or resulted in considerably different levels of inhibition of growth in the presence of glucose, mannose and glucose 6-phosphate, respectively, but hardly reduced their capability for intracellular replication in Caco-2 cells. Even the triple mutants Δ, , of the three enterobacterial strains were still able to replicate in Caco-2 cells, albeit at strain-specific lower rates than the corresponding wild-type strains.

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2010-04-01
2021-10-18
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References

  1. Bell K. S., Sebaihia M., Pritchard L., Holden M. T., Hyman L. J., Holeva M. C., Thomson N. R., Bentley S. D., Churcher L. J. other authors 2004; Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc Natl Acad Sci U S A 101:11105–11110
    [Google Scholar]
  2. Beuzón C. R., Meresse S., Unsworth K. E., Ruiz-Albert J., Garvis S., Waterman S. R., Ryder T. A., Boucrot E., Holden D. W. 2000; Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J 19:3235–3249
    [Google Scholar]
  3. Beuzón C. R., Salcedo S. P., Holden D. W. 2002; Growth and killing of a Salmonella enterica serovar Typhimurium sifA mutant strain in the cytosol of different host cell lines. Microbiology 148:2705–2715
    [Google Scholar]
  4. Bolivar F., Rodriguez R. L., Greene P. J., Betlach M. C., Heynker H. L., Boyer H. W., Crosa J. H., Falkow S. 1992; Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. 1977. Biotechnology 24:153–171
    [Google Scholar]
  5. Bowden S. D., Rowley G., Hinton J. C., Thompson A. 2009; Glucose and glycolysis are required for the successful infection of macrophages and mice by Salmonella enterica serovar Typhimurium. Infect Immun 77:3117–3126
    [Google Scholar]
  6. Brumell J. H., Grinstein S. 2004; Salmonella redirects phagosomal maturation. Curr Opin Microbiol 7:78–84
    [Google Scholar]
  7. Clermont O., Bonacorsi S., Bingen E. 2000; Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66:4555–4558
    [Google Scholar]
  8. Cossart P., Sansonetti P. J. 2004; Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304:242–248
    [Google Scholar]
  9. Covarrubias L., Cervantes L., Covarrubias A., Soberon X., Vichido I., Blanco A., Kupersztoch-Portnoy Y. M., Bolivar F. 1981; Construction and characterization of new cloning vehicles. V. Mobilization and coding properties of pBR322 and several deletion derivatives including pBR327 and pBR328. Gene 13:25–35
    [Google Scholar]
  10. Dagberg B., Uhlin B. E. 1992; Regulation of virulence-associated plasmid genes in enteroinvasive Escherichia coli. J Bacteriol 174:7606–7612
    [Google Scholar]
  11. Datsenko K. A., Wanner B. L. 2000; One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640–6645
    [Google Scholar]
  12. Death A., Ferenci T. 1993; The importance of the binding-protein-dependent Mgl system to the transport of glucose in Escherichia coli growing on low sugar concentrations. Res Microbiol 144:529–537
    [Google Scholar]
  13. Erni B., Zanolari B. 1985; The mannose-permease of the bacterial phosphotransferase system. Gene cloning and purification of the enzyme IIMan/IIIMan complex of Escherichia coli. J Biol Chem 260:15495–15503
    [Google Scholar]
  14. Erni B., Zanolari B., Kocher H. P. 1987; The mannose permease of Escherichia coli consists of three different proteins. Amino acid sequence and function in sugar transport, sugar phosphorylation, and penetration of phage lambda DNA. J Biol Chem 262:5238–5247
    [Google Scholar]
  15. Eylert E., Schar J., Mertins S., Stoll R., Bacher A., Goebel W., Eisenreich W. 2008; Carbon metabolism of Listeria monocytogenes growing inside macrophages. Mol Microbiol 69:1008–1017
    [Google Scholar]
  16. Hautefort I., Thompson A., Eriksson-Ygberg S., Parker M. L., Lucchini S., Danino V., Bongaerts R. J., Ahmad N., Rhen M., Hinton J. C. 2008; During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell Microbiol 10:958–984
    [Google Scholar]
  17. Henderson P. J., Giddens R. A., Jones-Mortimer M. C. 1977; Transport of galactose, glucose and their molecular analogues by Escherichia coli K12. Biochem J 162:309–320
    [Google Scholar]
  18. Island M. D., Wei B. Y., Kadner R. J. 1992; Structure and function of the uhp genes for the sugar phosphate transport system in Escherichia coli and Salmonella typhimurium. J Bacteriol 174:2754–2762
    [Google Scholar]
  19. Jin Q., Yuan Z., Xu J., Wang Y., Shen Y., Lu W., Wang J., Liu H., Yang J. other authors 2002; Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157. Nucleic Acids Res 30:4432–4441
    [Google Scholar]
  20. Johnson T. J., Kariyawasam S., Wannemuehler Y., Mangiamele P., Johnson S. J., Doetkott C., Skyberg J. A., Lynne A. M., Johnson J. R., Nolan L. K. 2007; The genome sequence of avian pathogenic Escherichia coli strain O1 : K1 : H7 shares strong similarities with human extraintestinal pathogenic E. coli genomes. J Bacteriol 189:3228–3236
    [Google Scholar]
  21. Klumpp J., Fuchs T. M. 2007; Identification of novel genes in genomic islands that contribute to Salmonella typhimurium replication in macrophages. Microbiology 153:1207–1220
    [Google Scholar]
  22. Lafont F., van der Goot F. G. 2005; Bacterial invasion via lipid rafts. Cell Microbiol 7:613–620
    [Google Scholar]
  23. Lucchini S., Liu H., Jin Q., Hinton J. C., Yu J. 2005; Transcriptional adaptation of Shigella flexneri during infection of macrophages and epithelial cells: insights into the strategies of a cytosolic bacterial pathogen. Infect Immun 73:88–102
    [Google Scholar]
  24. McClelland M., Sanderson K. E., Spieth J., Clifton S. W., Latreille P., Courtney L., Porwollik S., Ali J., Dante M. other authors 2001; Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413:852–856
    [Google Scholar]
  25. Meyer D., Schneider-Fresenius C., Horlacher R., Peist R., Boos W. 1997; Molecular characterization of glucokinase from Escherichia coli K-12. J Bacteriol 179:1298–1306
    [Google Scholar]
  26. Nicoletti M., Superti F., Conti C., Calconi A., Zagaglia C. 1988; Virulence factors of lactose-negative Escherichia coli strains isolated from children with diarrhea in Somalia. J Clin Microbiol 26:524–529
    [Google Scholar]
  27. Phalipon A., Sansonetti P. J. 2007; Shigella's ways of manipulating the host intestinal innate and adaptive immune system: a tool box for survival?. Immunol Cell Biol 85:119–129
    [Google Scholar]
  28. Postma P. W. 1977; Galactose transport in Salmonella typhimurium. J Bacteriol 129:630–639
    [Google Scholar]
  29. Postma P. W., Lengeler J. W., Jacobson G. R. 1993; Phosphoenolpyruvate : carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 57:543–594
    [Google Scholar]
  30. Sansonetti P. J., d'Hauteville H., Formal S. B., Toucas M. 1982; Plasmid-mediated invasiveness of “ Shigella-like” Escherichia coli. Ann Microbiol (Paris 133:351–355
    [Google Scholar]
  31. Scherer C. A., Hantman M. J., Miller S. I. 1997; Salmonella invasion and delivery of protein effectors to mammalian cell cytoplasm. Trends Microbiol 5:127–129
    [Google Scholar]
  32. Schwoppe C., Winkler H. H., Neuhaus H. E. 2002; Properties of the glucose-6-phosphate transporter from Chlamydia pneumoniae (HPTcp) and the glucose-6-phosphate sensor from Escherichia coli (UhpC. J Bacteriol 184:2108–2115
    [Google Scholar]
  33. Schwoppe C., Winkler H. H., Neuhaus H. E. 2003; Connection of transport and sensing by UhpC, the sensor for external glucose-6-phosphate in Escherichia coli. Eur J Biochem 270:1450–1457
    [Google Scholar]
  34. Stock J. B., Waygood E. B., Meadow N. D., Postma P. W., Roseman S. 1982; Sugar transport by the bacterial phosphotransferase system. The glucose receptors of the Salmonella typhimurium phosphotransferase system. J Biol Chem 257:14543–14552
    [Google Scholar]
  35. Vazquez-Torres A., Fang F. C. 2000; Cellular routes of invasion by enteropathogens. Curr Opin Microbiol 3:54–59
    [Google Scholar]
  36. Verhamme D. T., Postma P. W., Crielaard W., Hellingwerf K. J. 2002; Cooperativity in signal transfer through the Uhp system of Escherichia coli. J Bacteriol 184:4205–4210
    [Google Scholar]
  37. Welch R. A., Burland V., Plunkett G. III, Redford P., Roesch P., Rasko D., Buckles E. L., Liou S. R., Boutin A. other authors 2002; Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci U S A 99:17020–17024
    [Google Scholar]
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