1887

Abstract

It has recently been shown that the enteropathogen has an -linked general rotein ycosylation pathway (Pgl) that modifies many of the organism's proteins. To determine the role of the -linked general glycosylation in , the authors studied the gene, which shows high similarity to a family of sugar transferases. mutants were constructed in strains 81116 and 11168H. Both mutants were shown to be deficient in their ability to glycosylate a number of proteins, but their lipooligosaccharide and capsule were unaffected. The mutants had significantly reduced ability to adhere to and invade human epithelial Caco-2 cells. Additionally, the 81116 mutant was severely affected in its ability to colonize chicks. These results suggest that glycosylation is important for the attachment of to human and chicken host cells and imply a role for glycoproteins in the pathogenesis of .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26721-0
2004-06-01
2024-12-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/6/mic1501957.html?itemId=/content/journal/micro/10.1099/mic.0.26721-0&mimeType=html&fmt=ahah

References

  1. Beery J. T., Hugdahl M. B., Doyle M. P. 1988; Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Appl Environ Microbiol 54:2365–2370
    [Google Scholar]
  2. Bereswill S., Kist M. 2003; Recent developments in Campylobacter pathogenesis. Curr Opin Infect Dis 16:487–491 [CrossRef]
    [Google Scholar]
  3. Cawthraw S. A., Wassenaar T. M., Ayling R., Newell D. G. 1996; Increased colonization potential of Campylobacter jejuni strain 81116 after passage through chickens and its implication on the rate of transmission within flocks. Epidemiol Infect 117:213–215 [CrossRef]
    [Google Scholar]
  4. Fry B. N., Korolik V., ten Brinke J. A., Pennings M. T., Zalm R., Teunis B. J., Coloe P. J., van der Zeijst B. A. 1998; The lipopolysaccharide biosynthesis locus of Campylobacter jejuni 81116. Microbiology 144:2049–2061 [CrossRef]
    [Google Scholar]
  5. Fry B. N., Feng S., Chen Y. Y., Newell D. G., Coloe P. J., Korolik V. 2000; The galE gene of Campylobacter jejuni is involved in lipopolysaccharide synthesis and virulence. Infect Immun 68:2594–2601 [CrossRef]
    [Google Scholar]
  6. Guerry P., Doig P., Alm R. A., Burr D. H., Kinsella N., Trust T. J. 1996; Identification and characterization of genes required for post-translational modification of Campylobacter coli VC167 flagellin. Mol Microbiol 19:369–378 [CrossRef]
    [Google Scholar]
  7. Guerry P., Ewing C. P., Hickey T. E., Prendergast M. M., Moran A. P. 2000; Sialylation of lipooligosaccharide cores affects immunogenicity and serum resistance of Campylobacter jejuni. Infect Immun 68:6656–6662 [CrossRef]
    [Google Scholar]
  8. Hendrixson D. R., DiRita V. J. 2004; Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol Microbiol 52:471–484 [CrossRef]
    [Google Scholar]
  9. Jennings M. P., Virji M., Evans D., Foster V., Srikhanta Y. N., Steeghs L., van der Ley P., Moxon E. R. 1998; Identification of a novel gene involved in pilin glycosylation in Neisseria meningitidis. Mol Microbiol 29:975–984 [CrossRef]
    [Google Scholar]
  10. Jin S., Joe A., Lynett J., Hani E. K., Sherman P., Chan V. L. 2001; JlpA, a novel surface-exposed lipoprotein specific to Campylobacter jejuni, mediates adherence to host epithelial cells. Mol Microbiol 39:1225–1236 [CrossRef]
    [Google Scholar]
  11. Karlyshev A. V., Wren B. W. 2001; Detection and initial characterization of novel capsular polysaccharide among diverse Campylobacter jejuni strains using alcian blue dye. J Clin Microbiol 39:279–284 [CrossRef]
    [Google Scholar]
  12. Karlyshev A. V., Linton D., Gregson N. A., Lastovica A. J., Wren B. W. 2000; Genetic and biochemical evidence of a Campylobacter jejuni capsular polysaccharide that accounts for Penner serotype specificity. Mol Microbiol 35:529–541
    [Google Scholar]
  13. Karlyshev A. V., McCrossan M. V., Wren B. W. 2001; Demonstration of polysaccharide capsule in Campylobacter jejuni using electron microscopy. Infect Immun 69:5921–5924 [CrossRef]
    [Google Scholar]
  14. Konkel M. E., Garvis S. G., Tipton S. L., Anderson D. E. Jr Cieplak W. Jr 1997; Identification and molecular cloning of a gene encoding a fibronectin-binding protein (CadF) from Campylobacter jejuni. Mol Microbiol 24:953–963 [CrossRef]
    [Google Scholar]
  15. Linton D., Karlyshev A. V., Hitchen P. G., Morris H. R., Dell A., Gregson N. A., Wren B. W. 2000a; Multiple N-acetylneuraminic acid synthetase (neuB) genes in Campylobacter jejuni: identification and characterization of the gene involved in sialylation of lipo-oligosaccharide. Mol Microbiol 35:1120–1134 [CrossRef]
    [Google Scholar]
  16. Linton D., Gilbert M., Hitchen P. G., Dell A., Morris H. R., Wakarchuk W. W., Gregson N. A., Wren B. W. 2000b; Phase variation of a beta-1,3 galactosyltransferase involved in generation of the ganglioside GM1-like lipo-oligosaccharide of Campylobacter jejuni. Mol Microbiol 37:501–514
    [Google Scholar]
  17. Linton D., Allan E., Karlyshev A. V., Cronshaw A. D., Wren B. W. 2002; Identification of N-acetylgalactosamine-containing glycoproteins PEB3 and CgpA in Campylobacter jejuni. Mol Microbiol 43:497–508 [CrossRef]
    [Google Scholar]
  18. Marceau M., Nassif X. 1999; Role of glycosylation at Ser63 in production of soluble pilin in pathogenic Neisseria. J Bacteriol 181:656–661
    [Google Scholar]
  19. Marceau M., Forest K., Beretti J. L., Tainer J., Nassif X. 1998; Consequences of the loss of O-linked glycosylation of meningococcal type IV pilin on piliation and pilus-mediated adhesion. Mol Microbiol 27:705–715 [CrossRef]
    [Google Scholar]
  20. McSweegan E., Walker R. I. 1986; Identification and characterization of two Campylobacter jejuni adhesins for cellular and mucous substrates. Infect Immun 53:141–148
    [Google Scholar]
  21. Messner P. 1997; Bacterial glycoproteins. Glycoconj J 14:3–11 [CrossRef]
    [Google Scholar]
  22. Moens S., Vanderleyden J. 1997; Glycoproteins in prokaryotes. Arch Microbiol 168:169–175 [CrossRef]
    [Google Scholar]
  23. Muthukumar G., Nickerson K. W. 1987; The glycoprotein toxin of Bacillus thuringiensis subsp. israelensis indicates a lectinlike receptor in the larval mosquito gut. Appl Environ Microbiol 53:2650–2655
    [Google Scholar]
  24. Newell D. G. 2001; Animal models of Campylobacter jejuni colonization and disease and the lessons to be learned from similar Helicobacter pylori models. Symp Ser Soc Appl Microbiol 30:57S–67S
    [Google Scholar]
  25. Newell D. G., Wagenaar J. A. 2000; Poultry infections and their control at the farm level. In Campylobacter, 2nd edn. pp. 497–510Edited by Nachamkin I., Blaser M. J. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  26. Newell D. G., McBride H., Dolby J. M. 1985; Investigations on the role of flagella in the colonization of infant mice with Campylobacter jejuni and attachment of Campylobacter jejuni to human epithelial cell lines. J Hyg 95:217–227 [CrossRef]
    [Google Scholar]
  27. Oldfield N. J., Moran A. P., Millar L. A., Prendergast M. M., Ketley J. M. 2002; Characterization of the Campylobacter jejuni heptosyltransferase II gene, waaF, provides genetic evidence that extracellular polysaccharide is lipid A core independent. J Bacteriol 184:2100–2107 [CrossRef]
    [Google Scholar]
  28. Parkhill J., Wren B. W., Mungall K. & 18 other authors; 2000; The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665–668 [CrossRef]
    [Google Scholar]
  29. Pei Z. H., Ellison R. T. 3rd, Blaser M. J. 1991; Identification, purification, and characterization of major antigenic proteins of Campylobacter jejuni. J Biol Chem 266:16363–16369
    [Google Scholar]
  30. Pei Z., Burucoa C., Grignon B., Baqar S., Huang X. Z., Kopecko D. J., Bourgeois A. L., Fauchere J. L., Blaser M. J. 1998; Mutation in the peb1A locus of Campylobacter jejuni reduces interactions with epithelial cells and intestinal colonization of mice. Infect Immun 66:938–943
    [Google Scholar]
  31. Reeves P. R., Hobbs M., Valvano M. A. & 8 other authors; 1996; Bacterial polysaccharide synthesis and gene nomenclature. Trends Microbiol 4:495–503 [CrossRef]
    [Google Scholar]
  32. Schaffer C., Graninger M., Messner P. 2001; Prokaryotic glycosylation. Electrophoresis 22:248–261
    [Google Scholar]
  33. Szymanski C. M., Yao R., Ewing C. P., Trust T. J., Guerry P. 1999; Evidence for a system of general protein glycosylation in Campylobacter jejuni. Mol Microbiol 32:1022–1030 [CrossRef]
    [Google Scholar]
  34. Szymanski C. M., Burr D. H., Guerry P. 2002; Campylobacter protein glycosylation affects host cell interactions. Infect Immun 70:2242–2244 [CrossRef]
    [Google Scholar]
  35. Szymanski C. M., Logan S. M., Linton D., Wren B. W. 2003a; Campylobacter – a tale of two protein glycosylation systems. Trends Microbiol 11:233–238 [CrossRef]
    [Google Scholar]
  36. Szymanski C. M., St Michael F., Jarrell H. C., Li J., Gilbert M., Larocque S., Vinogradov E., Brisson J. R. 2003b; Detection of conserved N-linked glycans and phase variable lipo-oligosaccharides and capsules from Campylobacter cells by mass spectrometry and high resolution magic angle spinning NMR spectroscopy. J Biol Chem 278:24509–24520 [CrossRef]
    [Google Scholar]
  37. Tsai C. M., Frasch C. E. 1982; A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem 119:115–119 [CrossRef]
    [Google Scholar]
  38. van Vliet A. H., Wooldridge K. G., Ketley J. M. 1998; Iron-responsive gene regulation in a Campylobacter jejuni fur mutant. J Bacteriol 180:5291–5298
    [Google Scholar]
  39. van Vliet A. H., Baillon M. L., Penn C. W., Ketley J. M. 1999; Campylobacter jejuni contains two fur homologs: characterization of iron-responsive regulation of peroxide stress defense genes by the PerR repressor. J Bacteriol 181:6371–6376
    [Google Scholar]
  40. Wacker M., Linton D., Hitchen P. G.8 other authors 2002; N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science 298:1790–1793 [CrossRef]
    [Google Scholar]
  41. Wassenaar T. M., Blaser M. J. 1999; Pathophysiology of Campylobacter jejuni infections of humans. Microbes Infect 1:1023–1033 [CrossRef]
    [Google Scholar]
  42. Wassenaar T. M., Fry B. N., van der Zeijst B. A. 1993a; Genetic manipulation of Campylobacter: Evaluation of natural transformation and electro-transformation. Gene 132:131–135 [CrossRef]
    [Google Scholar]
  43. Wassenaar T. M., van der Zeijst B. A., Ayling R., Newell D. G. 1993b; Colonization of chicks by motility mutants of Campylobacter jejuni demonstrates the importance of flagellin A expression. J Gen Microbiol 139:1171–1175 [CrossRef]
    [Google Scholar]
  44. Wood A. C., Oldfield N. J., O'Dwyer C. A., Ketley J. M. 1999; Cloning, mutation and distribution of a putative lipopolysaccharide biosynthesis locus in Campylobacter jejuni. Microbiology 145:379–388 [CrossRef]
    [Google Scholar]
  45. Young N. M., Brisson J. R., Kelly J.8 other authors 2002; Structure of the N-linked glycan present on multiple glycoproteins in the Gram-negative bacterium, Campylobacter jejuni. J Biol Chem 277:42530–42539 [CrossRef]
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.26721-0
Loading
/content/journal/micro/10.1099/mic.0.26721-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error