Bioanalytical tools for the discovery of eukaryotic glycoproteins applied to the analysis of bacterial glycoproteins

References

• Apweiler R, Hermjakob H, Sharon N. On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim. Biophys. Acta1473(1), 4–8 (1999).
   PubMed Web of Science ®Google Scholar
• Messner P. Prokaryotic glycoproteins: unexplored but important. J. Bacteriol.186(9), 2517–2519 (2004).
   Google Scholar
• Eichler J. Facing extremes: archaeal surface-layer (glyco)proteins. Microbiology149(Pt 12), 3347–3351 (2003).
   Google Scholar
• Messner P, Schäffer C. Prokaryotic glycoproteins. In: Progress in the Chemistry of Organic Natural Products. Herz W, Falk H, Kirby GW (Eds). Springer-Verlag, Vienna, Austria 85, 51–124 (2003).
   Google Scholar
• Virji M. Post-translational modifications of meningococcal pili. Identification of common substituents: glycans and α-glycerophosphate – a review. Gene192(1), 141–147 (1997).
   PubMedGoogle Scholar
• Parge HE, Forest KT, Hickey MJ et al. Structure of the fibre-forming protein pilin at 2.6 A resolution. Nature378(6552), 32–38 (1995).
   PubMedGoogle Scholar
• Castric P. pilO, a gene required for glycosylation of Pseudomonas aeruginosa 1244 pilin. Microbiology141(Pt 5), 1247–1254 (1995).
   Google Scholar
• Mescher MF, Strominger JL. Purification and characterization of a prokaryotic glucoprotein from the cell envelope of Halobacterium salinarium. J. Biol. Chem.251(7), 2005–2014 (1976).
   Google Scholar
• Power PM, Roddam LF, Rutter K et al. Genetic characterization of pilin glycosylation and phase variation in Neisseria meningitidis. Mol. Microbiol.49(3), 833–847 (2003).
   Google Scholar
• Schmidt MA, Riley LW, Benz I. Sweet new world: glycoproteins in bacterial pathogens. Trends Microbiol.11(12), 554–561 (2003).
   PubMed Web of Science ®Google Scholar
• Dobos KM, Khoo KH, Swiderek KM, Brennan PJ, Belisle JT. Definition of the full extent of glycosylation of the 45-kilodalton glycoprotein of Mycobacterium tuberculosis. J. Bacteriol.178(9), 2498–2506 (1996).
   Google Scholar
• Benz I, Schmidt MA. Never say never again: protein glycosylation in pathogenic bacteria. Mol. Microbiol.45(2), 267–276 (2002).
   PubMed Web of Science ®Google Scholar
• Kuo C, Takahashi N, Swanson AF, Ozeki Y, Hakomori S. An N-linked high-mannose type oligosaccharide, expressed at the major outer membrane protein of Chlamydia trachomatis, mediates attachment and infectivity of the microorganism to HeLa cells. J. Clin. Invest.98(12), 2813–2818 (1996).
   PubMed Web of Science ®Google Scholar
• Aas FE, Vik A, Vedde J, Koomey M, Egge-Jacobsen W. Neisseria gonorrhoeae O -linked pilin glycosylation: functional analyses define both the biosynthetic pathway and glycan structure. Mol. Microbiol.65(3), 607–624 (2007).
   PubMed Web of Science ®Google Scholar
• Upreti RK, Kumar M, Shankar V. Bacterial glycoproteins: functions, biosynthesis and applications. Proteomics3(4), 363–379 (2003).
   PubMed Web of Science ®Google Scholar
• Bisaria VS, Mishra S. Regulatory aspects of cellulase biosynthesis and secretion. Crit. Rev. Biotechnol.9(2), 61–103 (1989).
   PubMed Web of Science ®Google Scholar
• Paulson JC. Glycoproteins: what are the sugar chains for? Trends Biochem. Sci.14(7), 272–276 (1989).
   PubMed Web of Science ®Google Scholar
• Baumeister W, Lembcke G. Structural features of archaebacterial cell envelopes. J. Bioenerg. Biomembr.24(6), 567–575 (1992).
   Google Scholar
• Schäffer C, Messner P. Glycobiology of surface layer proteins. Biochimie83(7), 591–599 (2001).
   Google Scholar
• Helenius A, Aebi M. Intracellular functions of N-linked glycans. Science291(5512), 2364–2369 (2001).
   PubMed Web of Science ®Google Scholar
• Nita-Lazar M, Wacker M, Schegg B, Amber S, Aebi M. The N–X–S/T consensus sequence is required but not sufficient for bacterial N-linked protein glycosylation. Glycobiology15(4), 361–367 (2005).
   PubMed Web of Science ®Google Scholar
• Linton D, Allan E, Karlyshev AV, Cronshaw AD, Wren BW. Identification of N-acetylgalactosamine-containing glycoproteins PEB3 and CgpA in Campylobacter jejuni. Mol. Microbiol.43(2), 497–508 (2002).
   PubMed Web of Science ®Google Scholar
• Szymanski CM, Burr DH, Guerry P. Campylobacter protein glycosylation affects host–cell interactions. Infect. Immun.70(4), 2242–2244 (2002).
   PubMed Web of Science ®Google Scholar
• Grass S, Buscher AZ, Swords WE et al. The Haemophilus influenzae HMW1 adhesin is glycosylated in a process that requires HMW1C and phosphoglucomutase, an enzyme involved in lipooligosaccharide biosynthesis. Mol. Microbiol.48(3), 737–751 (2003).
   PubMed Web of Science ®Google Scholar
• Arora SK, Neely AN, Blair B, Lory S, Ramphal R. Role of motility and flagellin glycosylation in the pathogenesis of Pseudomonas aeruginosa burn wound infections. Infect. Immun.73(7), 4395–4398 (2005).
   PubMed Web of Science ®Google Scholar
• Karlyshev AV, Everest P, Linton D et al. The Campylobacter jejuni general glycosylation system is important for attachment to human epithelial cells and in the colonization of chicks. Microbiology150(Pt 6), 1957–1964 (2004).
   PubMed Web of Science ®Google Scholar
• Maki M, Renkonen R. Biosynthesis of 6-deoxyhexose glycans in bacteria. Glycobiology14(3), R1–R15 (2004).
   PubMed Web of Science ®Google Scholar
• Szymanski CM, Yao R, Ewing CP, Trust TJ, Guerry P. Evidence for a system of general protein glycosylation in Campylobacter jejuni. Mol. Microbiol.32(5), 1022–1030 (1999).
   PubMed Web of Science ®Google Scholar
• Szymanski CM, Logan SM, Linton D, Wren BW. Campylobacter – a tale of two protein glycosylation systems. Trends Microbiol.11(5), 233–238 (2003).
   Google Scholar
• Young NM, Brisson JR, Kelly J et al. Structure of the N-linked glycan present on multiple glycoproteins in the Gram-negative bacterium, Campylobacter jejuni. J. Biol. Chem.277(45), 42530–42539 (2002).
   Web of Science ®Google Scholar
• Stimson E, Virji M, Makepeace K et al. Meningococcal pilin: a glycoprotein substituted with digalactosyl 2,4-diacetamido-2,4,6-trideoxyhexose. Mol. Microbiol.17(6), 1201–1214 (1995).
   Google Scholar
• Thibault P, Logan SM, Kelly JF et al. Identification of the carbohydrate moieties and glycosylation motifs in Campylobacter jejuni flagellin. J. Biol. Chem.276(37), 34862–34870 (2001).
   PubMed Web of Science ®Google Scholar
• Hegge FT, Hitchen PG, Aas FE et al. Unique modifications with phosphocholine and phosphoethanolamine define alternate antigenic forms of Neisseria gonorrhoeae type IV pili. Proc. Natl Acad. Sci. USA101(29), 10798–10803 (2004).
   PubMedGoogle Scholar
• Gavel Y, von Heijne G. Sequence differences between glycosylated and non-glycosylated Asn–X–Thr/Ser acceptor sites: implications for protein engineering. Protein Eng.3(5), 433–442 (1990).
   PubMedGoogle Scholar
• Bause E. Structural requirements of N-glycosylation of proteins. Studies with proline peptides as conformational probes. Biochem. J.209(2), 331–336 (1983).
   PubMed Web of Science ®Google Scholar
• Kowarik M, Young NM, Numao S et al. Definition of the bacterial N-glycosylation site consensus sequence. EMBO J.25(9), 1957–1966 (2006).
   PubMed Web of Science ®Google Scholar
• Steinberg TH, Pretty On Top K, Berggren KN et al. Rapid and simple single nanogram detection of glycoproteins in polyacrylamide gels and on electroblots. Proteomics1(7), 841–855 (2001).
   PubMed Web of Science ®Google Scholar
• Hart C, Schulenberg B, Steinberg TH, Leung WY, Patton WF. Detection of glycoproteins in polyacrylamide gels and on electroblots using Pro-Q® Emerald 488 dye, a fluorescent periodate Schiff-base stain. Electrophoresis24(4), 588–598 (2003).
   PubMed Web of Science ®Google Scholar
• Morelle W, Canis K, Chirat F, Faid V, Michalski JC. The use of mass spectrometry for the proteomic analysis of glycosylation. Proteomics6(14), 3993–4015 (2006).
   PubMed Web of Science ®Google Scholar
• O’Shannessy DJ. Hydrazido-derivatized supports in affinity chromatography. J. Chromatogr.510, 13–21 (1990).
   PubMedGoogle Scholar
• Bayer EA, Ben-Hur H, Wilchek M. Biocytin hydrazide – a selective label for sialic acids, galactose, and other sugars in glycoconjugates using avidin-biotin technology. Anal. Biochem.170(2), 271–281 (1988).
   PubMed Web of Science ®Google Scholar
• Virji M, Stimson E, Makepeace K et al. Posttranslational modifications of meningococcal pili. Identification of a common trisaccharide substitution on variant pilins of strain C311. Ann. NY Acad. Sci.797, 53–64 (1996).
   Google Scholar
• Zhao Z, Aliwarga Y, Willcox MD. Intrinsic protein fluorescence interferes with detection of tear glycoproteins in SDS-polyacrylamide gels using extrinsic fluorescent dyes. J. Biomol. Tech.18(5), 331–335 (2007).
   PubMedGoogle Scholar
• Fryksdale BG, Jedrzejewski PT, Wong DL, Gaertner AL, Miller BS. Impact of deglycosylation methods on two-dimensional gel electrophoresis and matrix assisted laser desorption/ionization-time of flight-mass spectrometry for proteomic analysis. Electrophoresis23(14), 2184–2193 (2002).
   Google Scholar
• Mechref Y, Novotny MV. Structural investigations of glycoconjugates at high sensitivity. Chem. Rev.102(2), 321–369 (2002).
   PubMed Web of Science ®Google Scholar
• Bruneel A, Robert T, Lefeber DJ et al. Two-dimensional gel electrophoresis of apolipoprotein C-III and other serum glycoproteins for the combined screening of human congenital disorders of O- and N-glycosylation. Proteomics Clin. Appl.1, 321–324 (2007).
   Google Scholar
• Schlags W, Lachmann B, Walther M, Kratzel M, Noe CR. Two-dimensional electrophoresis of recombinant human erythropoietin: a future method for the European Pharmacopoeia? Proteomics2(6), 679–682 (2002).
   PubMed Web of Science ®Google Scholar
• Burlingame AL. Characterization of protein glycosylation by mass spectrometry. Curr. Opin. Biotechnol.7(1), 4–10 (1996).
   PubMed Web of Science ®Google Scholar
• Hirabayashi J, Kasai K. Separation technologies for glycomics. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci.771(1–2), 67–87 (2002).
   PubMedGoogle Scholar
• Madera M, Mechref Y, Novotny MV. Combining lectin microcolumns with high-resolution separation techniques for enrichment of glycoproteins and glycopeptides. Anal. Chem.77(13), 4081–4090 (2005).
   PubMed Web of Science ®Google Scholar
• Hsu KL, Pilobello KT, Mahal LK. Analyzing the dynamic bacterial glycome with a lectin microarray approach. Nat. Chem. Biol.2(3), 153–157 (2006).
   PubMed Web of Science ®Google Scholar
• Faridmoayer A, Fentabil MA, Mills DC, Klassen JS, Feldman MF. Functional characterization of bacterial oligosaccharyltransferases involved in O-linked protein glycosylation. J. Bacteriol.189(22), 8088–8098 (2007).
   PubMed Web of Science ®Google Scholar
• Ge Y, Li C, Corum L, Slaughter CA, Charon NW. Structure and expression of the FlaA periplasmic flagellar protein of Borrelia burgdorferi. J. Bacteriol.180(9), 2418–2425 (1998).
   PubMed Web of Science ®Google Scholar
• Sparbier K, Wenzel T, Kostrzewa M. Exploring the binding profiles of ConA, boronic acid and WGA by MALDI-TOF/TOF MS and magnetic particles. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci.840(1), 29–36 (2006).
   Google Scholar
• Bond MR, Kohler JJ. Chemical methods for glycoprotein discovery. Curr. Opin. Chem. Biol.11(1), 52–58 (2007).
   Google Scholar
• Bobbitt JM. Periodate oxidation of carbohydrates. Adv. Carbohydr. Chem.48(11), 1–41 (1956).
   PubMedGoogle Scholar
• Zhang H, Li XJ, Martin DB, Aebersold R. Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry. Nat. Biotechnol.21(6), 660–666 (2003).
   PubMed Web of Science ®Google Scholar
• Rawn JD, Lienhard GE. The binding of boronic acids to chymotrypsin. Biochemistry13(15), 3124–3130 (1974).
   Google Scholar
• Sparbier K, Koch S, Kessler I, Wenzel T, Kostrzewa M. Selective isolation of glycoproteins and glycopeptides for MALDI-TOF MS detection supported by magnetic particles. J. Biomol. Tech.16(4), 407–413 (2005).
   Google Scholar
• Lee JH, Kim Y, Ha MY, Lee EK, Choo J. Immobilization of aminophenylboronic acid on magnetic beads for the direct determination of glycoproteins by matrix assisted laser desorption ionization mass spectrometry. J. Am. Soc. Mass Spectrom.16(9), 1456–1460 (2005).
   PubMed Web of Science ®Google Scholar
• Harvey DJ. Identification of protein-bound carbohydrates by mass spectrometry. Proteomics1(2), 311–328 (2001).
   PubMedGoogle Scholar
• Sambri V, Stefanelli C, Cevenini R. Detection of glycoproteins in Borrelia burgdorferi. Arch. Microbiol.157(3), 205–208 (1992).
   Google Scholar
• Sterba J, Vancova M, Rudenko N et al. Flagellin and outer surface proteins from Borrelia burgdorferi are not glycosylated. J. Bacteriol.190(7), 2619–2623 (2008).
   Google Scholar
• Dwek RA, Edge CJ, Harvey DJ, Wormald MR, Parekh RB. Analysis of glycoprotein-associated oligosaccharides. Annu. Rev. Biochem.62, 65–100 (1993).
   PubMed Web of Science ®Google Scholar
• Liu X, McNally DJ, Nothaft H et al. Mass spectrometry-based glycomics strategy for exploring N-linked glycosylation in eukaryotes and bacteria. Anal. Chem.78(17), 6081–6087 (2006).
   PubMed Web of Science ®Google Scholar
• An HJ, Peavy TR, Hedrick JL, Lebrilla CB. Determination of N-glycosylation sites and site heterogeneity in glycoproteins. Anal. Chem.75(20), 5628–5637 (2003).
   PubMed Web of Science ®Google Scholar
• Ciucanu I, Kerek F. A simple and rapid method for the permethylation of carbohydrates. Carbohydr. Res.131, 209–217 (1984).
   Web of Science ®Google Scholar
• Kuster B, Naven TJ, Harvey DJ. Rapid approach for sequencing neutral oligosaccharides by exoglycosidase digestion and matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. J. Mass Spectrom.31(10), 1131–1140 (1996).
   Google Scholar
• Kannicht C, Grunow D, Lucka L. Enzymatic sequence analysis of N-glycans by exoglycosidase cleavage and mass spectrometry – detection of Lewis X structures. Methods Mol. Biol.446, 255–266 (2008).
   Google Scholar
• Rudd PM, Guile GR, Kuster B et al. Oligosaccharide sequencing technology. Nature388(6638), 205–207 (1997).
   PubMed Web of Science ®Google Scholar
• Edge CJ, Rademacher TW, Wormald MR et al. Fast sequencing of oligosaccharides: the reagent-array analysis method. Proc. Natl Acad. Sci. USA89(14), 6338–6342 (1992).
   Google Scholar
• Mechref Y, Novotny MV. Mass spectrometric mapping and sequencing of N-linked oligosaccharides derived from submicrogram amounts of glycoproteins. Anal. Chem.70(3), 455–463 (1998).
   PubMed Web of Science ®Google Scholar
• Mechref Y, Muzikar J, Novotny MV. Comprehensive assessment of N-glycans derived from a murine monoclonal antibody: a case for multimethodological approach. Electrophoresis26(10), 2034–2046 (2005).
   PubMed Web of Science ®Google Scholar
• Kilar F, Hjerten S. Separation of the human transferrin isoforms by carrier-free high-performance zone electrophoresis and isoelectric focusing. J. Chromatogr.480, 351–357 (1989).
   Google Scholar
• Guttman A, Chen FT, Evangelista RA, Cooke N. High-resolution capillary gel electrophoresis of reducing oligosaccharides labeled with 1-aminopyrene-3,6,8-trisulfonate. Anal. Biochem.233(2), 234–242 (1996).
   PubMed Web of Science ®Google Scholar
• Guttman A, Chen FT, Evangelista RA. Separation of 1-aminopyrene-3,6,8-trisulfonate-labeled asparagine-linked fetuin glycans by capillary gel electrophoresis. Electrophoresis17(2), 412–417 (1996).
   PubMed Web of Science ®Google Scholar
• Gennaro LA, Salas-Solano O, Ma S. Capillary electrophoresis-mass spectrometry as a characterization tool for therapeutic proteins. Anal. Biochem.355(2), 249–258 (2006).
   PubMed Web of Science ®Google Scholar
• Joucla G, Brando T, Remaud-Simeon M, Monsan P, Puzo G. Capillary electrophoresis analysis of glucooligosaccharide regioisomers. Electrophoresis25(6), 861–869 (2004).
   Google Scholar
• Gennaro LA, Salas-Solano O. On-line CE-LIF-MS technology for the direct characterization of N-linked glycans from therapeutic antibodies. Anal. Chem.80(10), 3838–3845 (2008).
   PubMed Web of Science ®Google Scholar
• Bindila L, Steiner K, Schäffer C et al. Sequencing of O-glycopeptides derived from an S-layer glycoprotein of Geobacillus stearothermophilus NRS 2004/3a containing up to 51 monosaccharide residues at a single glycosylation site by fourier transform ion cyclotron resonance infrared multiphoton dissociation mass spectrometry. Anal. Chem.79(9), 3271–3279 (2007).
   Google Scholar
• von der Lieth CW, Bohne-Lang A, Lohmann KK, Frank M. Bioinformatics for glycomics: status, methods, requirements and perspectives. Brief Bioinform.5(2), 164–178 (2004).
   PubMed Web of Science ®Google Scholar
• Duus J, Gotfredsen CH, Bock K. Carbohydrate structural determination by NMR spectroscopy: modern methods and limitations. Chem. Rev.100(12), 4589–4614 (2000).
   PubMed Web of Science ®Google Scholar
• Wormald MR, Petrescu AJ, Pao YL et al. Conformational studies of oligosaccharides and glycopeptides: complementarity of NMR, x-ray crystallography, and molecular modelling. Chem. Rev.102(2), 371–386 (2002).
   PubMed Web of Science ®Google Scholar
• Allen PZ, Connelly MC, Apicella MA. Interaction of lectins with Neisseria gonorrhoeae. Can. J. Microbiol.26(4), 468–474 (1980).
   Google Scholar
• Curtis GD, Slack MP. Wheat-germ agglutination of Neisseria gonorrhoeae. A laboratory investigation. Br. J. Vener. Dis.57(4), 253–255 (1981).
   Google Scholar
• Doyle R, Keller K. Lectins in diagnostic microbiology. Eur. J. Clin. Microbiol.3(1), 4–9 (1984).
   Google Scholar
• Moyes A, Young H. An analysis of lectin agglutination as a means of sub-dividing gonococcal serovars. J. Med. Microbiol.37(1), 51–55 (1992).
   Google Scholar
• Frasch CE. Role of lipopolysaccharide in wheat germ agglutinin-mediated agglutination of Neisseria meningitidis and Neisseria gonorrhoeae. J. Clin. Microbiol.12(4), 498–501 (1980).
   Google Scholar
• McSweegan EF, Pistole TG. Interaction of the lectin limulin with capsular polysaccharides from Neisseria meningitidis and Escherichia coli. Biochem. Biophys. Res. Commun.106(4), 1390–1397 (1982).
   Google Scholar
• Chatterjee BP, Guha AK, Pal R, Bhattacharyya M. Lectin typing of Pseudomonas aeruginosa strains of different serogroups, Habs and Fisher types. Zentralbl. Bakteriol.271(3), 364–371 (1989).
   Google Scholar
• Wagner M. Interaction of wheat-germ agglutinin with streptococci and streptococcal cell wall polymers. Immunobiology156(1–2), 57–64 (1979).
   Google Scholar
• Kellens JT, Jacobs JA, Peumans WJ, Stobberingh EE. The agglutination of β-haemolytic streptococci by lectins. J. Med. Microbiol.39(6), 440–445 (1993).
   Google Scholar
• Holm SE, Bergholm AM, Wagner B, Wagner M. A sialic-acid-specific lectin from Cepaea hortensis that promotes phagocytosis of a group-B, type-Ia, streptococcal strain. J. Med. Microbiol.19(3), 317–323 (1985).
   Google Scholar
• Slifkin M, Cumbie R. Identification of group B streptococcal antigen with lectin-bound polystyrene particles. J. Clin. Microbiol.25(7), 1172–1175 (1987).
   Google Scholar
• Munoz A, Lopez A, Llovo J. Lectin typing of β-haemolytic streptococci of groups A and B. J. Med. Microbiol.41(5), 324–328 (1994).
   Google Scholar
• Kohler W, Nagai T. Reactions of the lectin anti-AHP from the edible snail Helix pomatia with N-acetyl-D-galactosamine of streptococci. Kitasato Arch. Exp. Med.62(2–3), 107–113 (1989).
   Google Scholar
• Ottensooser F, Nakamizo Y, Sato M, Miyamoto Y, Takizawa K. Lectins detecting group C streptococci. Infect. Immun.9(5), 971–973 (1974).
   Google Scholar
• Kohler W, Prokop O. [Agglutination experiments with streptococci with the phytagglutinin of Dolichos biflorus]. Z. Immunitatsforsch. Allerg. Klin. Immunol.133(2), 171–175 (1967).
   Google Scholar
• Goldstein IJ, Misaki A. Interaction of concanavalin A with an arabinogalactan from the cell wall of Mycobacterium bovis. J. Bacteriol.103(2), 422–425 (1970).
   Google Scholar
• Jackson M, Chan R, Matoba AY, Robin JB. The use of fluorescein-conjugated lectins for visualizing atypical mycobacteria. Arch. Ophthalmol.107(8), 1206–1209 (1989).
   Google Scholar