Simultaneous glycan-peptide characterization using hydrophilic interaction chromatography and parallel fragmentation by CID, higher energy collisional dissociation, and electron transfer dissociation MS applied to the N-linked glycoproteome of Campylobacter jejuni

Molecular and Cellular Proteomics

Volumn 10, Issue 2, 2011, Pages

  Scott, Nichollas E ^a   Parker, Benjamin L ^a   Connolly, Angela M ^a   Paulech, Jana ^a   Edwards, Alistair V G ^a   Crossett, Ben ^a   Falconer, Linda ^b   Kolarich, Daniel ^c   Djordjevic, Steven P ^b,d   Højrup, Peter ^e   Packer, Nicolle H ^c   Larsen, Martin R ^e   Cordwell, Stuart J ^a,e  

^a UNIVERSITY OF SYDNEY   (Australia)

^b NSW DEPARTMENT OF PRIMARY INDUSTRIES   (Australia)

^c MACQUARIE UNIVERSITY   (Australia)

^d UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^e UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; COLICIN V PRODUCTION PROTEIN; CYTOCHROME BD OXIDASE SUBUNIT I; DISULFIDE BOND FORMATION PROTEIN; GLYCOPEPTIDE; HISTIDINE BINDING PROTEIN HISJ/CJAC; INNER MEMBRANE MULTIDRUG EFFLUX SYSTEM PROTEIN CMEB; MAJOR ANTIGENIC PROTEIN PEB3; OUTER MEMBRANE MULTIDRUG EFFLUX SYSTEM PROTEIN CMEC; PENICILLIN BINDING PROTEIN; PERIPLASMIC MULTIDRUG EFFLUX SYSTEM PROTEIN CMEA; PERIPLASMIC NITRATE REDUCTASE SMALL SUBUNIT; PUTATIVE EXPORTING PROTEIN; PUTATIVE INTEGRAL MEMBRANE PROTEIN; PUTATIVE LIPOPROTEIN; PUTATIVE MECHANOSENSITIVE ION CHANNEL FAMILY PROTEIN; PUTATIVE MEMBRANE PROTEIN; PUTATIVE OMPA FAMILY MEMBRANE PROTEIN; PUTATIVE OUTER MEMBRANE EFFLUX PROTEIN; PUTATIVE PERIPLASMIC PROTEIN; PUTATIVE PERIPLASMIC SOLUTE BINDING PROTEIN; PUTATIVE PROTEIN EXPORT PROTEIN; PUTATIVE SECRETED PROTEASE; PUTATIVE SECRETED TRANSGLYCOSYLASE; PUTATIVE SULFATASE FAMILY PROTEIN; PUTATIVE UNCHARACTERIZED PROTEIN; ROD SHAPE DETERMINING PROTEIN; UNCHARACTERIZED METALLOPHOSPHOESTERASE; UNCLASSIFIED DRUG; UNINDEXED DRUG; UPF0323 LIPOPROTEIN CJ0371; PEPTIDE; POLYSACCHARIDE;

ARTICLE; BACTERIAL STRAIN; BINDING AFFINITY; CAMPYLOBACTER JEJUNI; CARBOHYDRATE ANALYSIS; CHEMICAL ANALYSIS; COLLISIONALLY ACTIVATED DISSOCIATION; ELECTRON TRANSFER DISSOCIATION; ENRICHMENT CULTURE; FRAGMENTATION REACTION; GLYCOSYLATION; HIGHER ENERGY COLLISIONAL DISSOCIATION; HYDROPHILIC INTERACTION CHROMATOGRAPHY; HYDROPHOBICITY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; TWO DIMENSIONAL ELECTROPHORESIS; CELL MEMBRANE; CHEMICAL PHENOMENA; CHEMISTRY; CHROMATOGRAPHY; ELECTRON; ELECTRON TRANSPORT; GENOME; METABOLISM; METHODOLOGY; PROTEIN TERTIARY STRUCTURE; SOYBEAN; TWO DIMENSIONAL GEL ELECTROPHORESIS;

CAMPYLOBACTER JEJUNI; EUKARYOTA; GLYCINE MAX;

CAMPYLOBACTER JEJUNI; CELL MEMBRANE; CHROMATOGRAPHY; ELECTRON TRANSPORT; ELECTRONS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENOME; GLYCOPEPTIDES; GLYCOSYLATION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MASS SPECTROMETRY; PEPTIDES; POLYSACCHARIDES; PROTEIN STRUCTURE, TERTIARY; SOYBEANS;

EID: 79953174969     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M000031-MCP201     Document Type: Article

References (56)

1. Zilbauer, M., Dorrell, N., Wren, B. W., and Bajaj-Elliott, M. (2008) Campylobacter jejuni-mediated disease pathogenesis: an update. Trans. R. Soc. Trop. Med. Hyg. 102, 123-129
2. Young, K. T., Davis, L. M., and Dirita, V. J. (2007) Campylobacter jejuni: molecular biology and pathogenesis. Nat. Rev. Microbiol. 5, 665-679
3. Janssen, R., Krogfelt, K. A., Cawthraw, S. A., van Pelt, W., Wagenaar, J. A., and Owen, R. J. (2008) Host-pathogen interactions in Campylobacter infections: the host perspective. Clin. Microbiol. Rev. 21, 505-518
4. Nachamkin, I. (2002) Chronic effects of Campylobacter infection. Microbes Infect. 4, 399-403
5. Lecuit, M., Abachin, E., Martin, A., Poyart, C., Pochart, P., Suarez, F., Bengoufa, D., Feuillard, J., Lavergne, A., Gordon, J. I., Berche, P., Guillevin, L., and Lortholary, O. (2004) Immunoproliferative small intestinal disease associated with Campylobacter jejuni. N. Engl. J. Med. 350, 239-248
6. Young, N. M., Brisson, J. R., Kelly, J., Watson, D. C., Tessier, L., Lanthier, P. H., Jarrell, H. C., Cadotte, N., St Michael, F., Aberg, E., and Szymanski, C. M. (2002) Structure of the N-linked glycan present on multiple glycoproteins in the Gram-negative bacterium, Campylobacter jejuni. J. Biol. Chem. 277, 42530-42539
7. Kowarik, M., Young, N. M., Numao, S., Schulz, B. L., Hug, I., Callewaert, N., Mills, D. C., Watson, D. C., Hernandez, M., Kelly, J. F., Wacker, M., and Aebi, M. (2006) Definition of the bacterial N-glycosylation site consensus sequence. EMBO J. 25, 1957-1966
8. Linton, D., Dorrell, N., Hitchen, P. G., Amber, S., Karlyshev, A. V., Morris, H. R., Dell, A., Valvano, M. A., Aebi, M., and Wren, B. W. (2005) Functional analysis of the Campylobacter jejuni N-linked protein glycosylation pathway. Mol. Microbiol. 55, 1695-1703
9. Szymanski, C. M., Yao, R., Ewing, C. P., Trust, T. J., and Guerry, P. (1999) Evidence for a system of general protein glycosylation in Campylobacter jejuni. Mol. Microbiol. 32, 1022-1030
10. Wacker, M., Linton, D., Hitchen, P. G., Nita-Lazar, M., Haslam, S. M., North, S. J., Panico, M., Morris, H. R., Dell, A., Wren, B. W., and Aebi, M. (2002) N-Linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science 298, 1790-1793 (Pubitemid 35404123)
11. Nita-Lazar, M., Wacker, M., Schegg, B., Amber, S., and Aebi, M. (2005) The N-X-S/T consensus sequence is required but not sufficient for bacterial N-linked protein glycosylation. Glycobiology 15, 361-367 (Pubitemid 41214166)
12. Kelly, J., Jarrell, H., Millar, L., Tessier, L., Fiori, L. M., Lau, P. C., Allan, B., and Szymanski, C. M. (2006) Biosynthesis of the N-linked glycan in Campylobacter jejuni and addition onto protein through block transfer. J. Bacteriol. 188, 2427-2434
13. Szymanski, C. M., Burr, D. H., and Guerry, P. (2002) Campylobacter protein glycosylation affects host cell interactions. Infect. Immun. 70, 2242-2244
14. Karlyshev, A. V., Everest, P., Linton, D., Cawthraw, S., Newell, D. G., and Wren, B. W. (2004) The Campylobacter jejuni general glycosylation system is important for attachment to human epithelial cells and in the colonization of chicks. Microbiology 150, 1957-1964
15. Helenius, A., and Aebi, M. (2004) Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73, 1019-1049
16. Kowarik, M., Numao, S., Feldman, M. F., Schulz, B. L., Callewaert, N., Kiermaier, E., Catrein, I., and Aebi, M. (2006) N-Linked glycosylation of folded proteins by the bacterial oligosaccharyltransferase. Science 314, 1148-1150 (Pubitemid 44789045)
17. Slynko, V., Schubert, M., Numao, S., Kowarik, M., Aebi, M., and Allain, F. H. (2009) NMR structure determination of a segmentally labeled glycoprotein using in vitro glycosylation. J. Am. Chem. Soc. 131, 1274-1281
18. Rangarajan, E. S., Bhatia, S., Watson, D. C., Munger, C., Cygler, M., Matte, A., and Young, N. M. (2007) Structural context for protein N-glycosylation in bacteria: the structure of PEB3, an adhesin from Campylobacter jejuni. Protein Sci. 16, 990-995
19. Kakuda, T., and DiRita, V. J. (2006) Cj1496c encodes a Campylobacter jejuni glycoprotein that influences invasion of human epithelial cells and colonization of the chick gastrointestinal tract. Infect. Immun. 74, 4715-4723
20. Davis, L. M., Kakuda, T., and DiRita, V. J. (2009) A Campylobacter jejuni znuA orthologue is essential for growth in low zinc environments and chick colonization. J. Bacteriol. 191, 1631-1640
21. Larsen, J. C., Szymanski, C., and Guerry, P. (2004) N-Linked protein glycosylation is required for full competence in Campylobacter jejuni 81-176. J. Bacteriol. 186, 6508-6514 (Pubitemid 39258133)
22. Carrillo, C. D., Taboada, E., Nash, J. H., Lanthier, P., Kelly, J., Lau, P. C., Verhulp, R., Mykytczuk, O., Sy, J., Findlay, W. A., Amoako, K., Gomis, S., Willson, P., Austin, J. W., Potter, A., Babiuk, L., Allan, B., and Szymanski, C. M. (2004) Genome-wide expression analyses of Campylobacter jejuni NCTC11168 reveals coordinate regulation of motility and virulence by flhA. J. Biol. Chem. 279, 20327-20338
23. Gaynor, E. C., Cawthraw, S., Manning, G., MacKichan, J. K., Falkow, S., and Newell, D. G. (2004) The genome-sequenced variant of Campylobacter jejuni NCTC 11168 and the original clonal clinical isolate differ markedly in colonization, gene expression, and virulence-associated phenotypes. J. Bacteriol. 186, 503-517
24. Scott, N. E., Bogema, D. R., Connolly, A. M., Falconer, L., Djordjevic, S. P., and Cordwell, S. J. (2009) Mass spectrometric characterization of the surface-associated 42 kDa lipoprotein JlpA as a glycosylated antigen in strains of Campylobacter jejuni. J. Proteome Res. 8, 4654-4664
25. Liu, X., McNally, D. J., Nothaft, H., Szymanski, C. M., Brisson, J. R., and Li, J. (2006) Mass spectrometry-based glycomics strategy for exploring N-linked glycosylation in eukaryotes and bacteria. Anal. Chem. 78, 6081-6087
26. Ding, W., Nothaft, H., Szymanski, C. M., and Kelly, J. (2009) Identification and quantification of glycoproteins using ion-pairing normal-phase LC and MS. Mol. Cell. Proteomics 8, 2170-2185
27. Cordwell, S. J. (2006) Technologies for bacterial surface proteomics. Curr. Opin. Microbiol. 9, 320-329
28. Lotan, R., Beattie, G., Hubbell, W., and Nicolson, G. L. (1977) Activities of lectins and their immobilized derivatives in detergent solutions. Implications on the use of lectin affinity chromatography for the purification of membrane glycoproteins. Biochemistry 16, 1787-1794
29. Larsen, M. R., Højrup, P., and Roepstorff, P. (2005) Characterization of gel-separated glycoproteins using two-step proteolytic digestion combined with sequential microcolumns and mass spectrometry. Mol. Cell. Proteomics 4, 107-119
30. Selby, D. S., Larsen, M. R., Calvano, C. D., and Jensen, O. N. (2008) Identification and characterization of N-glycosylated proteins using proteomics. Methods Mol. Biol. 484, 263-276
31. Bakhtiar, R., and Guan, Z. (2005) Electron capture dissociation mass spectrometry in characterization of post-translational modifications. Biochem. Biophys. Res. Commun. 334, 1-8
32. Mikesh, L. M., Ueberheide, B., Chi, A., Coon, J. J., Syka, J. E., Shabanowitz, J., and Hunt, D. F. (2006) The utility of ETD mass spectrometry in proteomic analysis. Biochim. Biophys. Acta 1764, 1811-1822
33. Alley, W. R., Jr., Mechref, Y., and Novotny, M. V. (2009) Characterization of glycopeptides by combining collision-induced dissociation and electrontransfer dissociation mass spectrometry data. Rapid Commun. Mass Spectrom. 23, 161-170
34. Catalina, M. I., Koeleman, C. A., Deelder, A. M., and Wuhrer, M. (2007) Electron transfer dissociation of N-glycopeptides: loss of the entire N-glycosylated asparagine side chain. Rapid Commun. Mass Spectrom. 21, 1053-1061
35. Vik, A., Aas, F. E., Anonsen, J. H., Bilsborough, S., Schneider, A., Egge-Jacobsen, W., and Koomey, M. (2009) Broad spectrum O-linked protein glycosylation in the human pathogen Neisseria gonorrhoeae. Proc. Natl. Acad. Sci. U.S.A. 106, 4447-4452
36. Olsen, J. V., Macek, B., Lange, O., Makarov, A., Horning, S., and Mann, M. (2007) Higher-energy C-trap dissociation for peptide modification analysis. Nat. Methods 4, 709-712 (Pubitemid 47338163)
37. Gardy, J. L., Laird, M. R., Chen, F., Rey, S., Walsh, C. J., Ester, M., and Brinkman, F. S. (2005) PSORTb v. 2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics 21, 617-623
38. Cordwell, S. J., Len, A. C., Touma, R. G., Scott, N. E., Falconer, L., Jones, D., Connolly, A., Crossett, B., and Djordjevic, S. P. (2008) Identification of membrane-associated proteins from Campylobacter jejuni strains using complementary proteomics technologies. Proteomics 8, 122-139
39. Hägglund, P., Matthiesen, R., Elortza, F., Højrup, P., Roepstorff, P., Jensen, O. N., and Bunkenborg, J. (2007) An enzymatic deglycosylation scheme enabling identification of core fucosylated N-glycans and O-glycosylation site mapping of human plasma proteins. J. Proteome Res. 6, 3021-3031 (Pubitemid 47310187)
40. Cordwell, S. J. (2002) Acquisition and archiving of information for bacterial proteomics: from sample preparation to database. Methods Enzymol. 358, 207-227
41. Larsen, M. R., Cordwell, S. J., and Roepstorff, P. (2002) Graphite powder as an alternative or supplement to reversed-phase material for desalting and concentration of peptide mixtures prior to matrix-assisted laser desorption/ionization-mass spectrometry. Proteomics 2, 1277-1287
42. Domon, B., and Costello, C. E. (1988) A systematic nomenclature for carbohydrate fragmentation in FAB-MS/MS spectra of glycoconjugate. Glycoconj. J. 5, 397-409
43. Roepstorff, P., and Fohlman, J. (1984) Proposal for a common nomenclature for sequence ions in mass spectra of peptides. Biomed. Mass Spectrom. 11, 601
44. Kjeldsen, F., Hasekmann, K. F., Budnik, B. A., Jensen, F., and Zubarev, R. A. (2002) Dissociative capture of hot (3-13 eV) electrons by polypeptide polycations: an efficient process accompanied by secondary fragmentation. Chem. Phys. Lett. 356, 201-206
45. Good, D. M., Wenger, C. D., McAlister, G. C., Bai, D. L., Hunt, D. F., and Coon, J. J. (2009) Post-acquisition ETD spectral processing for increased peptide identifications. J. Am. Soc. Mass Spectrom. 20, 1435-1440
46. Kjeldsen, F., Giessing, A. M., Ingrell, C. R., and Jensen, O. N. (2007) Peptide sequencing and characterization of post-translational modifications by enhanced ion-charging and liquid chromatography electron-transfer dissociation tandem mass spectrometry. Anal. Chem. 79, 9243-9252
47. Weerapana, E., and Imperiali, B. (2006) Asparagine-linked protein glycosylation: From eukaryotic to prokaryotic systems. Glycobiology 16, 91R-101R
48. Szymanski, C. M., and Wren, B. W. (2005) Protein glycosylation in bacterial mucosal pathogens. Nat. Rev. Microbiol. 3, 225-237
49. Hägglund, P., Bunkenborg, J., Elortza, F., Jensen, O. N., and Roepstorff, P. (2004) A new strategy for identification of N-glycosylated proteins and unambiguous assignment of their glycosylation sites using HILIC enrichment and partial deglycosylation. J. Proteome Res. 3, 556-566 (Pubitemid 39207360)
50. Han, H., Xia, Y., Yang, M., and McLuckey, S. A. (2008) Rapidly alternating transmission mode electron-transfer dissociation and collisional activation for the characterization of polypeptide ions. Anal. Chem. 80, 3492-3497
51. Couttas, T. A., Raftery, M. J., Bernardini, G., and Wilkins, M. R. (2008) Immonium ion scanning for the discovery of post-translational modifications and its application to histones. J. Proteome Res. 7, 2632-2641
52. Paizs, B., and Suhai, S. (2005) Fragmentation pathways of protonated peptides. Mass Spectrom. Rev. 24, 508-548
53. Good, D. M., Wirtala, M., McAlister, G. C., and Coon, J. J. (2007) Performance characteristics of electron transfer dissociation mass spectrometry. Mol. Cell. Proteomics 6, 1942-1951
54. Darula, Z., and Medzihradszky, K. F. (2009) Affinity-enrichment and characterization of mucin core 1-type glycopeptides from bovine serum. Mol. Cell. Proteomics 8, 2515-2526
55. Stintzi, A., Marlow, D., Palyada, K., Naikare, H., Panciera, R., Whitworth, L., and Clarke, C. (2005) Use of genome-wide expression profiling and mutagenesis to study the intestinal lifestyle of Campylobacter jejuni. Infect. Immun. 73, 1797-1810
56. Lin, J., Cagliero, C., Guo, B., Barton, Y. W., Maurel, M. C., Payot, S., and Zhang, Q. (2005) Bile salts modulate expression of the CmeABC multidrug efflux pump in Campylobacter jejuni. J. Bacteriol. 187, 7417-7424 (Pubitemid 41507798)