1887

Abstract

Glycosylated proteins are ubiquitous components of eukaryote cellular surfaces, where the glycan moieties are implicated in a wide range of cell–cell recognition events. Once thought to be restricted to eukaryotes, glycosylation is now being increasingly reported in prokaryotes. Many of these discoveries have grown from advances in analytical technologies and genome sequencing. This review highlights the capabilities of high-sensitivity mass spectrometry for carbohydrate structure determination of bacterial glycoproteins and the emergence of glycoproteomic strategies that have evolved from proteomics and genomics for the functional analysis of bacterial glycosylation.

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2006-06-01
2024-04-20
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References

  1. Andersen J. S, Mann M. 2000; Functional genomics by mass spectrometry. FEBS Lett 480:25–31 [CrossRef]
    [Google Scholar]
  2. Benz I, Schmidt M. A. 2002; Never say never again: protein glycosylation in pathogenic bacteria. Mol Microbiol 45:267–276 [CrossRef]
    [Google Scholar]
  3. Bock K, Schuster-Kolbe J, Altman E, Allmaier G, Stahl B, Christian R, Sleytr U. B, Messner P. 1994; Primary structure of the O -glycosidically linked glycan chain of the crystalline surface layer glycoprotein of Thermoanaerobacter thermohydrosulfuricus L111-69. Galactosyl tyrosine as a novel linkage unit. J Biol Chem 269:7137–7144
    [Google Scholar]
  4. Castric P, Cassels F. J, Carlson R. W. 2001; Structural characterization of the Pseudomonas aeruginosa 1244 pilin glycan. J Biol Chem 276:26479–26485 [CrossRef]
    [Google Scholar]
  5. Dell A, Morris H. R. 2001; Glycoprotein structure determination by mass spectrometry. Science 291:2351–2356 [CrossRef]
    [Google Scholar]
  6. Dempski R. E., Jr, Imperiali B. 2002; Oligosaccharyl transferase: gatekeeper to the secretory pathway. Curr Opin Chem Biol 6:844–850 [CrossRef]
    [Google Scholar]
  7. Dobos K. M, Khoo K. H, Swiderek K. M, Brennan P. J, Belisle J. T. 1996; Definition of the full extent of glycosylation of the 45-kilodalton glycoprotein of Mycobacterium tuberculosis . J Bacteriol 178:2498–2506
    [Google Scholar]
  8. Feldman M. F, Wacker M, Hernandez M. 7 other authors 2005; Engineering N -linked protein glycosylation with diverse O antigen lipopolysaccharide structures in Escherichia coli . Proc Natl Acad Sci U S A 102:3016–3021 [CrossRef]
    [Google Scholar]
  9. Fry B. N, Korolik V, Pennings M. T, Zalm R, Teunis B. J, Coloe P. J, ten Brinke J. A, van der Zeijst B. A. 1998; The lipopolysaccharide biosynthesis locus of Campylobacter jejuni 81116. Microbiology 144:2049–2061 [CrossRef]
    [Google Scholar]
  10. Goon S, Kelly J. F, Logan S. M, Ewing C. P, Guerry P. 2003; Pseudaminic acid, the major modification on Campylobacter flagellin , is synthesized via the Cj1293 gene. Mol Microbiol 50:659–671 [CrossRef]
    [Google Scholar]
  11. 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]
  12. Hakansson K, Cooper H. J, Emmett M. R, Costello C. E, Marshall A. G, Nilsson C. L. 2001; Electron capture dissociation and infrared multiphoton dissociation MS/MS of an N -glycosylated tryptic peptic to yield complementary sequence information. Anal Chem 73:4530–4536 [CrossRef]
    [Google Scholar]
  13. Hegge F. T, Hitchen P. G, Aas F. E. 9 other authors 2004; Unique modifications with phosphocholine and phosphoethanolamine define alternate antigenic forms of Neisseria gonorrhoeae type IV pili. Proc Natl Acad Sci U S A 101:10798–10803 [CrossRef]
    [Google Scholar]
  14. 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]
  15. Linton D, Dorrell N, Hitchen P. G. 7 other authors 2005; Functional analysis of the Campylobacter jejuni N -linked protein glycosylation pathway. Mol Microbiol 55:1695–1703 [CrossRef]
    [Google Scholar]
  16. Mann M, Hendrickson R. C, Pandey A. 2001; Analysis of proteins and proteomes by mass spectrometry. Annu Rev Biochem 70:437–473 [CrossRef]
    [Google Scholar]
  17. Medzihradszky K. F, Campbell J. M, Baldwin M. A, Falick A. M, Juhasz P, Vestal M. L, Burlingame A. L. 2000; The characteristics of peptide collision-induced dissociation using a high-performance MALDI-TOF/TOF tandem mass spectrometer. Anal Chem 72:552–558 [CrossRef]
    [Google Scholar]
  18. Mescher M. F, Strominger J. L. 1976; Purification and characterization of a prokaryotic glucoprotein from the cell envelope of Halobacterium salinarium . J Biol Chem 251:2005–2014
    [Google Scholar]
  19. 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]
  20. Power P. M, Jennings M. P. 2003; The genetics of glycosylation in Gram-negative bacteria. FEMS Microbiol Lett 218:211–222 [CrossRef]
    [Google Scholar]
  21. Schaffer C, Messner P. 2004; Surface-layer glycoproteins: an example for the diversity of bacterial glycosylation with promising impacts on nanobiotechnology. Glycobiology 14:31R–42R [CrossRef]
    [Google Scholar]
  22. Schirm M, Soo E. C, Aubry A. J, Austin J, Thibault P, Logan S. M. 2003; Structural, genetic and functional characterization of the flagellin glycosylation process in Helicobacter pylori . Mol Microbiol 48:1579–1592 [CrossRef]
    [Google Scholar]
  23. Schirm M, Arora S. K, Verma A, Vinogradov E, Thibault P, Ramphal R, Logan S. M. 2004a; Structural and genetic characterization of glycosylation of type a flagellin in Pseudomonas aeruginosa . J Bacteriol 186:2523–2531 [CrossRef]
    [Google Scholar]
  24. Schirm M, Kalmokoff M, Aubry A, Thibault P, Sandoz M, Logan S. M. 2004b; Flagellin from Listeria monocytogenes is glycosylated with beta- O -linked N -acetylglucosamine. J Bacteriol 186:6721–6727 [CrossRef]
    [Google Scholar]
  25. Schirm M, Schoenhofen I. C, Logan S. M, Waldron K. C, Thibault P. 2005; Identification of unusual bacterial glycosylation by tandem mass spectrometry analyses of intact proteins. Anal Chem 77:7774–7782 [CrossRef]
    [Google Scholar]
  26. Schoenhofen I. C, McNally D. J, Vinogradov E, Whitfield D, Young N. M, Dick S, Wakarchuk W. W, Brisson J. R, Logan S. M. 2006; Functional characterization of dehydratase/aminotransferase pairs from Helicobacter and Campylobacter : enzymes distinguishing the pseudaminic acid and bacillosamine biosynthetic pathways. J Biol Chem 281:723–732 [CrossRef]
    [Google Scholar]
  27. Shevchenko A, Loboda A, Ens W, Standing K. G. 2000; MALDI quadrupole time-of-flight mass spectrometry: a powerful tool for proteomic research. Anal Chem 72:2132–2141 [CrossRef]
    [Google Scholar]
  28. Stimson E, Virji M, Makepeace K. 9 other authors 1995; Meningococcal pilin: a glycoprotein substituted with digalactosyl 2,4-diacetamido-2,4,6-trideoxyhexose. Mol Microbiol 17:1201–1214 [CrossRef]
    [Google Scholar]
  29. Szymanski C. M, Wren B. W. 2005; Protein glycosylation in bacterial mucosal pathogens. Nat Rev Microbiol 3:225–237 [CrossRef]
    [Google Scholar]
  30. 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]
  31. Szymanski C. M, Michael F. S, Jarrell H. C, Li J, Gilbert M, Larocque S, Vinogradov E, Brisson J. R. 2003; Detection of conserved N -linked glycans and phase-variable lipooligosaccharides 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]
  32. Taylor M. T, Drickamer K. 2002 Introduction to Glycobiology Oxford: Oxford University Press;
    [Google Scholar]
  33. Thibault P, Logan S. M, Kelly J. F, Brisson J. R, Ewing C. P, Trust T. J, Guerry P. 2001; Identification of the carbohydrate moieties and glycosylation motifs in Campylobacter jejuni flagellin. J Biol Chem 276:34862–34870 [CrossRef]
    [Google Scholar]
  34. Upreti R. K, Kumar M, Shankar V. 2003; Bacterial glycoproteins: functions, biosynthesis and applications. Proteomics 3:363–379 [CrossRef]
    [Google Scholar]
  35. Voisin S, Houliston R. S, Kelly J, Brisson J. R, Watson D, Bardy S. L, Jarrell K. F, Logan S. M. 2005; Identification and characterization of the unique N -linked glycan common to the flagellins and S-layer glycoprotein of Methanococcus voltae . J Biol Chem 280:16586–16593 [CrossRef]
    [Google Scholar]
  36. 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]
  37. Yates J. R., 3rd. 2004; Mass spectral analysis in proteomics. Annu Rev Biophys Biomol Struct 33:297–316 [CrossRef]
    [Google Scholar]
  38. 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]
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