N-glycoproteomics: Mass spectrometry-based glycosylation site annotation

Biological Chemistry

Volumn 393, Issue 4, 2012, Pages 249-258

  Pasing, Yvonne ^a   Sickmann, Albert ^a,b   Lewandrowski, Urs ^a  

^a LEIBNIZ INSTITUT FÜR ANALYTISCHE WISSENSCHAFTEN ISAS E V   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Electrostatic repulsion hydrophilic liquid interaction chromatography; Glycopeptide enrichment; Glycoproteome; Glycosylation; Lectin; Titanium dioxide

Indexed keywords

ARGININE; ASPARAGINE; ASPARTIC ACID; FUCOSE; GLYCOPEPTIDASE; GLYCOPEPTIDE; HYDRAZIDE; LECTIN; LYSINE; MEMBRANE PROTEIN; N ACETYL BETA GLUCOSAMINIDASE; N ACETYLGLUCOSAMINE; PRONASE; TITANIUM DIOXIDE; TUMOR MARKER;

AFFINITY CHROMATOGRAPHY; ALGORITHM; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; CANCER DIAGNOSIS; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; COLLISIONALLY ACTIVATED DISSOCIATION; CONFERENCE PAPER; DEAMINATION; DEGLYCOSYLATION; ELECTROSTATIC REPULSION HYDROPHILIC INTERACTION CHROMATOGRAPHY; FRAGMENTATION REACTION; GLYCOSYLATION; GLYCOSYLATION SITE ANNOTATION; HEART MUSCLE ISCHEMIA; HUMAN; HYDROLYSIS; HYDROPHILIC INTERACTION CHROMATOGRAPHY; ION EXCHANGE CHROMATOGRAPHY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METAL OXIDE AFFINITY CHROMATOGRAPHY; N GLYCOPROTEOMICS; NONHUMAN; OXIDATIVE COUPLING; PRECIPITATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEOMICS;

ANIMALS; CHROMATOGRAPHY, LIQUID; GLYCOSYLATION; HUMANS; MASS SPECTROMETRY; PROTEOMICS;

EID: 84859861608     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2011-0245     Document Type: Conference Paper

References (68)

1. Adamczyk, B., Tharmalingam, T., and Rudd, P.M. (2011). Glycans as cancer biomarkers. Biochim. Biophys. Acta [Epub ahead of print].
2. Agrawal, P.K. (1992). NMR spectroscopy in the structural elucidation of oligosaccharides and glycosides. Phytochemistry 31, 3307-3330.
3. An, H.J., Peavy, T.R., Hedrick, J.L., and Lebrilla, C.B. (2003). Determination of N-glycosylation sites and site heterogeneity in glycoproteins. Anal. Chem. 75, 5628-5637. (Pubitemid 37280595)
4. Apweiler, R., Hermjakob, H., and Sharon, N. (1999). On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim. Biophys. Acta 1473, 4-8.
5. Baenziger, J.U. and Fiete, D. (1979). Structural determinants of concanavalin A specificity for oligosaccharides. J. Biol. Chem. 254, 2400-2407.
6. Bause, E. and Legler, G. (1981). The role of the hydroxy amino acid in the triplet sequence Asn-Xaa-Thr(Ser) for the N-glycosylation step during glycoprotein biosynthesis. Biochem. J. 195, 639-644.
7. Beck, F., Lewandrowski, U., Wiltfang, M., Feldmann, I., Geiger, J., Sickmann, A., and Zahedi, R.P. (2011). The good, the bad, the ugly: validating the mass spectrometric analysis of modified peptides. Proteomics 11, 1099-1109.
8. Chelius, D. and Shaler, T.A. (2003). Capture of peptides with N-terminal serine and threonine: a sequence-specific chemical method for peptide mixture simplification. Bioconjug. Chem. 14, 205-211. (Pubitemid 36169034)
9. Debray, H., Decout, D., Strecker, G., Spik, G., and Montreuil, J. (1981). Specificity of twelve lectins towards oligosaccharides and glycopeptides related to N-glycosylproteins. Eur. J. Biochem. 117, 41-55.
10. Engholm-Keller, K. and Larsen, M.R. (2011). Titanium dioxide as chemo-affinity chromatographic sorbent of biomolecular compounds - applications in acidic modification-specific proteomics. J. Proteomics 75, 317-328.
11. Grueninger-Leitch, F., D'Arcy, A., D'Arcy, B., and Chene, C. (1996). Deglycosylation of proteins for crystallization using recombinant fusion protein glycosidases. Protein Sci. 5, 2617-2622. (Pubitemid 26424874)
12. Hagglund, 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)
13. Hakansson, K., Cooper, H.J., Emmett, M.R., Costello, C.E., Marshall, A.G., and 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. (Pubitemid 32868256)
14. Halim, A., Nilsson, J., Ruetschi, U., Hesse, C., and Larson, G. (2011). Human urinary glycoproteomics; attachment site specific analysis of N- and O-linked glycosylations by CID and ECD. Mol. Cell. Proteomics [Epub ahead of print].
15. Hao, P., Guo, T., and Sze, S.K. (2011a). Simultaneous analysis of proteome, phospho- and glycoproteome of rat kidney tissue with electrostatic repulsion hydrophilic interaction chromatography. PLoS One 6, e16884.
16. Hao, P., Ren, Y., Alpert, A.J., and Sze, S.K. (2011b). Detection, evaluation and minimization of nonenzymatic deamidation in proteomic sample preparation. Mol. Cell. Proteomics 10, O111 009381.
17. Harmon, B.J., Gu, X., and Wang, D.I. (1996). Rapid monitoring of site-specific glycosylation microheterogeneity of recombinant human interferon-gamma. Anal. Chem. 68, 1465-1473.
18. Hart, G.W., Housley, M.P., and Slawson, C. (2007). Cycling of O-linked b-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 446, 1017-1022. (Pubitemid 46676063)
19. Hogan, J.M., Pitteri, S.J., Chrisman, P.A., and McLuckey, S.A. (2005). Complementary structural information from a tryptic N-linked glycopeptide via electron transfer ion/ion reactions and collision-induced dissociation. J. Proteome Res. 4, 628-632. (Pubitemid 40548173)
20. Ivancic, M.M., Gadgil, H.S., Halsall, H.B., and Treuheit, M.J. (2010). LC/MS analysis of complex multiglycosylated human a1-acid glycoprotein as a model for developing identification and quantitation methods for intact glycopeptide analysis. Anal. Biochem. 400, 25-32.
21. Kaji, H., Saito, H., Yamauchi, Y., Shinkawa, T., Taoka, M., Hirabayashi, J., Kasai, K., Takahashi, N., and Isobe, T. (2003). Lectin affinity capture, isotope-coded tagging and mass spectrometry to identify N-linked glycoproteins. Nat. Biotechnol. 21, 667-672. (Pubitemid 36638094)
22. Kay, R., Barton, C., Ratcliffe, L., Matharoo-Ball, B., Brown, P., Roberts, J., Teale, P., and Creaser, C. (2008). Enrichment of low molecular weight serum proteins using acetonitrile precipitation for mass spectrometry based proteomic analysis. Rapid Commun. Mass Spectrom. 22, 3255-3260.
23. Khanna, M.R., Stanley, B.A., and Thomas, G.H. (2010). Towards a membrane proteome in Drosophila: a method for the isolation of plasma membrane. BMC Genomics 11, 302.
24. Kronis, K.A. and Carver, J.P. (1982). Specificity of isolectins of wheat germ agglutinin for sialyloligosaccharides: a 360-MHz proton nuclear magnetic resonance binding study. Biochemistry 21, 3050-3057.
25. Lee, A., Nakano, M., Hincapie, M., Kolarich, D., Baker, M.S., Hancock, W.S., and Packer, N.H. (2010). The lectin riddle: glycoproteins fractionated from complex mixtures have similar glycomic profiles. OMICS 14, 487-499.
26. Lewandrowski, U. and Sickmann, A. (2009). N-glycosylation site analysis of human platelet proteins by hydrazide affinity capturing and LC-MS/MS. Methods Mol. Biol. 534, 225-238.
27. Lewandrowski, U., Moebius, J., Walter, U., and Sickmann, A. (2006). Elucidation of N-glycosylation sites on human platelet proteins: a glycoproteomic approach. Mol. Cell. Proteomics 5, 226-233. (Pubitemid 43329301)
28. Lewandrowski, U., Zahedi, R.P., Moebius, J., Walter, U., and Sickmann, A. (2007). Enhanced N-glycosylation site analysis of sialoglycopeptides by strong cation exchange prefractionation applied to platelet plasma membranes. Mol. Cell. Proteomics 6, 1933-1941. (Pubitemid 350201869)
29. Lewandrowski, U., Lohrig, K., Zahedi, R.P., Wolters, D.A., and Sickmann, A. (2008). Glycosylation site analysis of human platelets by electrostatic repulsion hydrophilic interaction chromatography. Clin. Proteomics 4, 25-36.
30. Lundgren, D.H., Han, D.K., and Eng, J.K. (2005). Protein identification using TurboSEQUEST. Curr. Protoc. Bioinformatics Chapter 13, Unit 13.3.
31. Mirgorodskaya, E., Roepstorff, P., and Zubarev, R.A. (1999). Localization of O-glycosylation sites in peptides by electron capture dissociation in a Fourier transform mass spectrometer. Anal. Chem. 71, 4431-4436.
32. Muller, S., Goletz, S., Packer, N., Gooley, A., Lawson, A.M., and Hanisch, F.G. (1997). Localization of O-glycosylation sites on glycopeptide fragments from lactation-associated MUC1. All putative sites within the tandem repeat are glycosylation targets in vivo. J. Biol. Chem. 272, 24780-24793. (Pubitemid 27415647)
33. Mysling, S., Palmisano, G., Hojrup, P., and Thaysen-Andersen, M. (2010). Utilizing ion-pairing hydrophilic interaction chromatography solid phase extraction for efficient glycopeptide enrichment in glycoproteomics. Anal. Chem. 82, 5598-5609.
34. Nesvizhskii, A.I. (2010). A survey of computational methods and error rate estimation procedures for peptide and protein identifi- cation in shotgun proteomics. J. Proteomics 73, 2092-2123.
35. Nielsen, P.A., Olsen, J.V., Podtelejnikov, A.V., Andersen, J.R., Mann, M., and Wisniewski, J.R. (2005). Proteomic mapping of brain plasma membrane proteins. Mol. Cell. Proteomics 4, 402-408. (Pubitemid 40590560)
36. Palmisano, G., Lendal, S.E., Engholm-Keller, K., Leth-Larsen, R., Parker, B.L., and Larsen, M.R. (2010). Selective enrichment of sialic acid-containing glycopeptides using titanium dioxide chromatography with analysis by HILIC and mass spectrometry. Nat. Protoc. 5, 1974-1982.
37. Parker, B.L., Palmisano, G., Edwards, A.V., White, M.Y., Engholm- Keller, K., Lee, A., Scott, N.E., Kolarich, D., Hambly, B.D., Packer, N.H., et al. (2011). Quantitative N-linked glycoproteomics of myocardial ischemia and reperfusion injury reveals early remodeling in the extracellular environment. Mol. Cell. Proteomics 10, M110 006833.
38. Perkins, D.N., Pappin, D.J., Creasy, D.M., and Cottrell, J.S. (1999). Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567. (Pubitemid 30007252)
39. Ranzinger, R., Herget, S., Wetter, T., and von der Lieth, C.W. (2008). GlycomeDB - integration of open-access carbohydrate structure databases. BMC Bioinformatics 9, 384.
40. Robinson, N.E. and Robinson, A.B. (2004). Amide molecular clocks in drosophila proteins: potential regulators of aging and other processes. Mech. Ageing Dev. 125, 259-267. (Pubitemid 38438504)
41. Rush, R.S., Derby, P.L., Smith, D.M., Merry, C., Rogers, G., Rohde, M.F., and Katta, V. (1995). Microheterogeneity of erythropoietin carbohydrate structure. Anal. Chem. 67, 1442-1452.
42. Schachter, H. (2001). Congenital disorders involving defective N-glycosylation of proteins. Cell. Mol. Life Sci. 58, 1085-1104. (Pubitemid 32756519)
43. Scott, N.E., Parker, B.L., Connolly, A.M., Paulech, J., Edwards, A.V., Crossett, B., Falconer, L., Kolarich, D., Djordjevic, S.P., Hojrup, P., et al. (2010). Simultaneous glycan-peptide characterization using hydrophilic interaction chromatography and parallel fragmentation by CID, HCD and ETD-MS applied to the N-linked glycoproteome of Campylobacter jejuni. Mol. Cell. Proteomics 10, M000031-MCP201.
44. Selman, M.H., Hemayatkar, M., Deelder, A.M., and Wuhrer, M. (2011). Cotton HILIC SPE microtips for microscale purification and enrichment of glycans and glycopeptides. Anal. Chem. 83, 2492-2499.
45. Sleat, D.E., Zheng, H., Qian, M., and Lobel, P. (2006). Identification of sites of mannose 6-phosphorylation on lysosomal proteins. Mol. Cell. Proteomics 5, 686-701.
46. Sola, R.J. and Griebenow, K. (2009). Effects of glycosylation on the stability of protein pharmaceuticals. J. Pharm. Sci. 98, 1223-1245.
47. Sorensen, A.L., Rumjantseva, V., Nayeb-Hashemi, S., Clausen, H., Hartwig, J.H., Wandall, H.H., and Hoffmeister, K.M. (2009). Role of sialic acid for platelet life span: exposure of beta-galactose results in the rapid clearance of platelets from the circulation by asialoglycoprotein receptor-expressing liver macrophages and hepatocytes. Blood 114, 1645-1654.
48. Spiro, R.G. (2002). Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology 12, 43R - 56R. (Pubitemid 34760066)
49. Stahl-Zeng, J., Lange, V., Ossola, R., Eckhardt, K., Krek, W., Aebersold, R., and Domon, B. (2007). High sensitivity detection of plasma proteins by multiple reaction monitoring of N-glycosites. Mol. Cell. Proteomics 6, 1809-1817. (Pubitemid 350031682)
50. Stroud, D.A., Oeljeklaus, S., Wiese, S., Bohnert, M., Lewandrowski, U., Sickmann, A., Guiard, B., van der Laan, M., Warscheid, B., and Wiedemann, N. (2011). Composition and topology of the endoplasmic reticulum-mitochondria encounter structure. J. Mol. Biol. 413, 743-750.
51. Syka, J.E., Coon, J.J., Schroeder, M.J., Shabanowitz, J., and Hunt, D.F. (2004). Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc. Natl. Acad. Sci. USA 101, 9528-9533. (Pubitemid 38869270)
52. Taouatas, N., Drugan, M.M., Heck, A.J., and Mohammed, S. (2008). Straightforward ladder sequencing of peptides using a Lys-N metalloendopeptidase. Nat. Methods 5, 405-407. (Pubitemid 351619098)
53. Tarentino, A.L., Plummer, T.H., Jr., and Maley, F. (1974). The release of intact oligosaccharides from specific glycoproteins by endobeta- N-acetylglucosaminidase H. J. Biol. Chem. 249, 818-824.
54. Tarentino, A.L., Gomez, C.M., and Plummer, T.H., Jr. (1985). Deglycosylation of asparagine-linked glycans by peptide: N-glycosidase F. Biochemistry 24, 4665-4671. (Pubitemid 15233719)
55. Temporini, C., Perani, E., Calleri, E., Dolcini, L., Lubda, D., Caccialanza, G., and Massolini, G. (2007). Pronase-immobilized enzyme reactor: an approach for automation in glycoprotein analysis by LC/LC-ESI/MSn. Anal. Chem. 79, 355-363. (Pubitemid 46095069)
56. Tretter, V., Altmann, F., and Marz, L. (1991). Peptide-N4-(Nacetyl- b-glucosaminyl)asparagine amidase F cannot release glycans with fucose attached a 1-3 to the asparagine-linked N-acetylglucosamine residue. Eur. J. Biochem. 199, 647-652.
57. Tyler-Cross, R. and Schirch, V. (1991). Effects of amino acid sequence, buffers, and ionic strength on the rate and mechanism of deamidation of asparagine residues in small peptides. J. Biol. Chem. 266, 22549-22556. (Pubitemid 21908688)
58. Ueda, K., Takami, S., Saichi, N., Daigo, Y., Ishikawa, N., Kohno, N., Katsumata, M., Yamane, A., Ota, M., Sato, T.A., et al. (2010). Development of serum glycoproteomic profiling technique; simultaneous identification of glycosylation sites and site-specific quantification of glycan structure changes. Mol. Cell. Proteomics 9, 1819-1828.
59. Valliere-Douglass, J.F., Kodama, P., Mujacic, M., Brady, L.J., Wang, W., Wallace, A., Yan, B., Reddy, P., Treuheit, M.J., and Balland, A. (2009). Asparagine-linked oligosaccharides present on a nonconsensus amino acid sequence in the CH1 domain of human antibodies. J. Biol. Chem. 284, 32493-32506.
60. Valliere-Douglass, J.F., Eakin, C.M., Wallace, A., Ketchem, R.R., Wang, W., Treuheit, M.J., and Balland, A. (2010). Glutamine-linked and non-consensus asparagine-linked oligosaccharides present in human recombinant antibodies define novel protein glycosylation motifs. J. Biol. Chem. 285, 16012-16022.
61. Wang, H., Chang-Wong, T., Tang, H.Y., and Speicher, D.W. (2010). Comparison of extensive protein fractionation and repetitive LC-MS/MS analyses on depth of analysis for complex proteomes. J. Proteome Res. 9, 1032-1040.
62. Wiesner, J., Premsler, T., and Sickmann, A. (2008). Application of electron transfer dissociation (ETD) for the analysis of posttranslational modifications. Proteomics 8, 4466-4483.
63. Wollscheid, B., Bausch-Fluck, D., Henderson, C., O'Brien, R., Bibel, M., Schiess, R., Aebersold, R., and Watts, J.D. (2009). Mass-spectrometric identification and relative quantification of N-linked cell surface glycoproteins. Nat. Biotechnol. 27, 378-386.
64. Wuhrer, M., de Boer, A.R., and Deelder, A.M. (2009). Structural glycomics using hydrophilic interaction chromatography (HILIC) with mass spectrometry. Mass Spectrom. Rev. 28, 192-206.
65. Zauner, G., Koeleman, C.A., Deelder, A.M., and Wuhrer, M. (2010). Protein glycosylation analysis by HILIC-LC-MS of proteinase K-generated N- and O-glycopeptides. J. Sep. Sci. 33, 903-910.
66. Zeng, X., Hood, B.L., Sun, M., Conrads, T.P., Day, R.S., Weissfeld, J.L., Siegfried, J.M., and Bigbee, W.L. (2010). Lung cancer serum biomarker discovery using glycoprotein capture and liquid chromatography mass spectrometry. J. Proteome Res. 9, 6440-6449.
67. Zhang, H., Li, X.J., Martin, D.B., and Aebersold, R. (2003). Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry. Nat. Biotechnol. 21, 660-666. (Pubitemid 36638093)
68. Zielinska, D.F., Gnad, F., Wisniewski, J.R., and Mann, M. (2010). Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints. Cell 141, 897-907.