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

Expert Review of Proteomics

Volumn 6, Issue 1, 2009, Pages 75-85

  Balonova, Lucie ^a,b   Hernychova, Lenka ^a   Bilkova, Zuzana ^b  

^a UNIVERSITY OF DEFENCE   (Czech Republic)

^b UNIVERSITY OF PARDUBICE   (Czech Republic)

Author keywords

Electrophoresis; Glycoprotein; Glycosylation; Lectin; Magnetic bead; Mass spectrometry; Prokaryote

Indexed keywords

BACTERIAL PROTEIN; GLYCOPROTEIN; LECTIN;

BACTERIAL STRAIN; EUKARYOTE; MASS SPECTROMETRY; NONHUMAN; PROKARYOTE; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN ISOLATION; PROTEIN STRUCTURE; PROTEOMICS; PSEUDOMONAS AERUGINOSA; REVIEW;

BACTERIAL PROTEINS; CHEMISTRY, ANALYTICAL; EUKARYOTIC CELLS; GLYCOPROTEINS; GLYCOSYLATION; PROKARYOTIC CELLS;

BACTERIA (MICROORGANISMS); EUKARYOTA; PROKARYOTA;

EID: 60549092317     PISSN: 14789450     EISSN: 17448387     Source Type: Journal    
DOI: 10.1586/14789450.6.1.75     Document Type: Review

References (100)

1. Apweiler R, Hermjakob H, Sharon N. On the frequency of protein glycosylation, as deduced from analysis of the SWISS- PROT database. Biochim. Biophys. Acta 1473(1), 4-8 (1999).
2. Messner P. Prokaryotic glycoproteins: unexplored but important. J. Bacteriol. 186(9), 2517-2519 (2004).
3. Eichler J. Facing extremes: archaeal surface-layer (glyco)proteins. Microbiology 149(Pt 12), 3347-3351 (2003).
4. 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).
5. Virji M. Post-translational modifications of meningococcal pili. Identification of common substituents: glycans and α-glycerophosphate - a review. Gene 192(1), 141-147 (1997).
6. Parge HE, Forest KT, Hickey MJ et al. Structure of the fibre-forming protein pilin at 2.6 A resolution. Nature 378(6552), 32-38 (1995).
7. Castric P. pilO, a gene required for glycosylation of Pseudomonas aeruginosa 1244 pilin. Microbiology 141(Pt 5), 1247-1254 (1995).
8. 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).
9. 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).
10. Schmidt MA, Riley LW, Benz I. Sweet new world: glycoproteins in bacterial pathogens. Trends Microbiol. 11(12), 554-561 (2003).
11. 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).
12. Benz I, Schmidt MA. Never say never again: protein glycosylation in pathogeni bacteria. Mol. Microbiol. 45(2), 267-276 (2002).
13. Kuo C, Takahashi N, Swanson AF, Ozek 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).
14. 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).
15. Upreti RK, Kumar M, Shankar V. Bacterial glycoproteins: functions, biosynthesis and applications. Proteomics 3(4), 363-379 (2003).
16. Bisaria VS, Mishra S. Regulatory aspects of cellulase biosynthesis and secretion. Crit. Rev. Biotechnol. 9(2), 61-103 (1989
17. Paulson JC. Glycoproteins: what are the sugar chains for? Trends Biochem. Sci. 14(7), 272-276 (1989).
18. Baumeister W, Lembcke G. Structural features of archaebacterial cell envelopes. J. Bioenerg Biomembr. 24(6), 567-575 (1992).
19. Schäffer C, Messner P. Glycobiology of surface layer proteins. Biochimie 83(7), 591-599 (2001).
20. Helenius A, Aebi M. Intracellular functions of N-linked glycans. Science 291(5512), 2364-2369 (2001).
21. 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. Glycobiology 15(4), 361-367 (2005).
22. 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).
23. Szymanski CM, Burr DH, Guerry P. Campylobacter protein glycosylation affects host-cell interactions. Infect. Immun. 70(4), 2242-2244 (2002).
24. 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).
25. 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).
26. 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. Microbiology 150(Pt 6), 1957-1964 (2004).
27. Maki M, Renkonen R. Biosynthesis of 6-deoxyhexose glycans in bacteria. Glycobiology 14(3), R1-R15 (2004).
28. 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).
29. Szymanski CM, Logan SM, Linton D, Wren BW. Campylobacter - a tale of two protein glycosylation systems. Trends Microbiol. 11(5), 233-238 (2003).
30. 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).
31. 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).
32. 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).
33. 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. USA 101(29), 10798-10803 (2004).
34. 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).
35. Bause E. Structural requirements of N-glycosylation of proteins. Studies with proline peptides as conformational probes. Biochem. J. 209(2), 331-336 (1983).
36. Kowarik M, Young NM, Numao S et al. Definition of the bacterial N-glycosylation site consensus sequence. EMBO J. 25(9), 1957-1966 (2006).
37. Steinberg TH, Pretty On Top K, Berggren KN et al. Rapid and simple single nanogram detection of glycoproteins in polyacrylamide gels and on electroblots. Proteomics 1(7), 841-855 (2001).
38. 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. Electrophoresis 24(4), 588-598 (2003).
39. Morelle W, Canis K, Chirat F, Faid V, Michalski JC. The use of mass spectrometry for the proteomic analysis of glycosylation. Proteomics 6(14), 3993-4015 (2006).
40. O'Shannessy DJ. Hydrazido-derivatized supports in affinity chromatography. J. Chromatogr. 510, 13-21 (1990).
41. 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).
42. 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).
43. 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).
44. 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. Electrophoresis 23 (14), 2184-2193 (2002).
45. Mechref Y, Novotny MV. Structural investigations of glycoconjugates at high sensitivity. Chem. Rev. 102(2), 321-369 (2002).
46. 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).
47. Schlags W, Lachmann B, Walther M, Kratzel M, Noe CR. Two-dimensional electrophoresis of recombinant human erythropoietin: a future method for the European Pharmacopoeia? Proteomics 2(6), 679-682 (2002).
48. Burlingame AL. Characterization of protein glycosylation by mass spectrometry. Curr. Opin. Biotechnol. 7(1), 4-10 (1996).
49. Hirabayashi J, Kasai K. Separation technologies for glycomics. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 771(1-2), 67-87 (2002).
50. 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).
51. Hsu KL, Pilobello KT, Mahal LK. Analyzing the dynamic bacterial glycome with a lectin microarray approach. Nat. Chem. Biol. 2(3), 153-157 (2006).
52. 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).
53. 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).
54. 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).
55. Bond MR, Kohler JJ. Chemical methods for glycoprotein discovery. Curr. Opin. Chem. Biol. 11(1), 52-58 (2007).
56. Bobbitt JM. Periodate oxidation of carbohydrates. Adv. Carbohydr. Chem. 48(11), 1-41 (1956).
57. 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).
58. Rawn JD, Lienhard GE. The binding of boronic acids to chymotr ypsin. Biochemistry 13(15), 3124-3130 (1974).
59. Sparbier K, Koch S, Kessler I, Wenzel T, Kostrzewa M. Selective isolation of glycoproteins and glycopeptides for MALDI-TOF MS detection supported by magnetic pa rticles. J. Biomol. Tech. 16(4), 407-413 (2005).
60. 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).
61. Harvey DJ. Identification of protein-bound carbohydrates by mass spectrometry. Proteomics 1(2), 311-328 (2001).
62. Sambri V, Stefanelli C, Cevenini R. Detection of glycoproteins in Borrelia burgdorferi. Arch. Microbiol. 157(3), 205-208 (1992).
63. 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).
64. Dwek RA, Edge CJ, Harvey DJ, Wormald MR, Parekh RB. Analysis of glycoprotein- associated oligosaccharides. Annu. Rev. Biochem. 62, 65-100 (1993).
65. 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).
66. 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).
67. Ciucanu I, Kerek F. A simple and rapid method for the permethylation of carbohydrates. Carbohydr. Res. 131, 209-217 (1984).
68. 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).
69. 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).
70. Rudd PM, Guile GR, Kuster B et al. Oligosaccharide sequencing technology. Nature 388(6638), 205-207 (1997).
71. Edge CJ, Rademacher TW, Wormald MR et al. Fast sequencing of oligosaccharides: the reagent-array analysis method. Proc. Natl Acad. Sci. USA 89(14), 6338-6342 (1992).
72. 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).
73. Mechref Y, Muzikar J, Novotny MV. Comprehensive assessment of N-glycans derived from a murine monoclonal antibody: a case for multimethodological approach. Electrophoresis 26(10), 2034-2046 (2005).
74. 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).
75. 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).
76. Guttman A, Chen FT, Evangelista RA. Separation of 1-aminopyrene-3,6,8- trisulfonate-labeled asparagine-linked fetuin glycans by capillary gel electrophoresis. Electrophoresis 17(2), 412-417 (1996).
77. 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).
78. Joucla G, Brando T, Remaud-Simeon M, Monsan P, Puzo G. Capillary electrophoresis analysis of glucooligosaccharide regioisomers. Electrophoresis 25(6), 861-869 (2004).
79. 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).
80. Bindila L, Steiner K, Schaffer 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).
81. 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).
82. Duus J, Gotfredsen CH, Bock K. Carbohydrate structural determination by NMR spectroscopy: modern methods and limitations. Chem. Rev. 100(12), 4589-4614 (2000).
83. Wormald MR, Petrescu AJ, Pao YL et al. Conformational studies of oligosaccharides and glycopeptides: complementarity of NMR, x-ray crystallography, and molecula modelling. Chem. Rev. 102(2), 371-386 (2002).
84. Allen PZ, Connelly MC, Apicella MA. Interaction of lectins with Neisseria gonorrhoeae. Can. J. Microbiol. 26(4), 468-474 (1980).
85. Curtis GD, Slack MP. Wheat-germ agglutination of Neisseria gonorrhoeae. A laboratory investigation. Br. J. Vener. Dis. 57(4), 253-255 (1981).
86. Doyle R, Keller K. Lectins in diagnostic microbiology. Eur. J. Clin. Microbiol. 3(1), 4-9 (1984).
87. 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).
88. 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).
89. 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).
90. 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).
91. Wagner M. Interaction of wheat-germ agglutinin with streptococci and streptococcal cell wall polymers. Immunobiology 156(1-2), 57-64 (1979).
92. Kellens JT, Jacobs JA, Peumans WJ, Stobberingh EE. The agglutination of p-haemolytic streptococci by lectins. J. Med. Microbiol. 39(6), 440-445 (1993).
93. 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).
94. Slifkin M, Cumbie R. Identification of group B streptococcal antigen with lectin-bound polystyrene particles. J. Clin. Microbiol. 25(7), 1172-1175 (1987).
95. Munoz A, Lopez A, Llovo J. Lectin typing of p-haemolytic streptococci of groups A and B. J. Med. Microbiol. 41(5), 324-328 (1994).
96. 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).
97. Ottensooser F, Nakamizo Y, Sato M, Miyamoto Y, Takizawa K. Lectins detecting group C streptococci. Infect. Immun. 9(5), 971-973 (1974).
98. Kohler W, Prokop O. [Agglutination experiments with streptococci with the phytagglutinin of Dolichos biflorus]. Z. Immunitatsforsch. Allerg. Klin. Immunol. 133(2), 171-175 (1967).
99. 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).
100. 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).