A Method for Comprehensive Glycosite-Mapping and Direct Quantitation of Serum Glycoproteins

Journal of Proteome Research

Volumn 14, Issue 12, 2015, Pages 5179-5192

  Hong, Qiuting ^a   Ruhaak, L Renee ^a   Stroble, Carol ^a   Parker, Evan ^a   Huang, Jincui ^a   Maverakis, Emanual ^a   Lebrilla, Carlito B ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

absolute quantitation; glycopeptide; immunoglobulin; site specific glycan analysis

Indexed keywords

GLYCOPEPTIDE; GLYCOPROTEIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; PEPTIDE; PLASMA PROTEIN; ALPHA 2 MACROGLOBULIN; IMMUNOGLOBULIN;

ARTICLE; LIMIT OF QUANTITATION; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; REPRODUCIBILITY; SENSITIVITY ANALYSIS; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; AMINO ACID SEQUENCE; BLOOD; CHEMISTRY; GLYCOSYLATION; HUMAN; LIQUID CHROMATOGRAPHY; MOLECULAR GENETICS; PEPTIDE MAPPING; PROCEDURES;

ALPHA-MACROGLOBULINS; AMINO ACID SEQUENCE; CHROMATOGRAPHY, LIQUID; GLYCOPEPTIDES; GLYCOPROTEINS; GLYCOSYLATION; HUMANS; IMMUNOGLOBULINS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; PEPTIDE MAPPING; REPRODUCIBILITY OF RESULTS;

EID: 84949034098     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b00756     Document Type: Article

References (58)

1. de Leoz, M. L.; Young, L. J.; An, H. J.; Kronewitter, S. R.; Kim, J.; Miyamoto, S.; Borowsky, A. D.; Chew, H. K.; Lebrilla, C. B. High-mannose glycans are elevated during breast cancer progression Mol. Cell. Proteomics 2011, 10, M110.002717 10.1074/mcp.M110.002717
2. An, H. J.; Kronewitter, S. R.; de Leoz, M. L. A.; Lebrilla, C. B. Glycomics and disease markers Curr. Opin. Chem. Biol. 2009, 13, 601-607 10.1016/j.cbpa.2009.08.015
3. Fujimura, T.; Shinohara, Y.; Tissot, B.; Pang, P.-C.; Kurogochi, M.; Saito, S.; Arai, Y.; Sadilek, M.; Murayama, K.; Dell, A.; Nishimura, S.-I.; Hakomori, S.-i. Glycosylation status of haptoglobin in sera of patients with prostate cancer vs. benign prostate disease or normal subjects Int. J. Cancer 2008, 122, 39-49 10.1002/ijc.22958
4. Chen, G.; Wang, Y.; Qiu, L.; Qin, X.; Liu, H.; Wang, X.; Wang, Y.; Song, G.; Li, F.; Guo, Y.; Li, F.; Guo, S.; Li, Z. Human IgG Fc-glycosylation profiling reveals associations with age, sex, female sex hormones and thyroid cancer J. Proteomics 2012, 75, 2824-2834 10.1016/j.jprot.2012.02.001
5. Axford, J. S. Glycosylation and rheumatic disease Biochim. Biophys. Acta, Mol. Basis Dis. 1999, 1455, 219-229 10.1016/S0925-4439(99)00057-5
6. Bond, A.; Alavi, A.; Axford, J. S.; Bourke, B. E.; Bruckner, F. E.; Kerr, M. A.; Maxwell, J. D.; Tweed, K. J.; Weldon, M. J.; Youinou, P.; Hay, F. C. A Detailed Lectin Analysis of IgG Glycosylation, Demonstrating Disease Specific Changes in Terminal Galactose and N-acetylglucosamine J. Autoimmun. 1997, 10, 77-85 10.1006/jaut.1996.0104
7. Mestecky, J.; Tomana, M.; Crowley-Nowick, P. A.; Moldoveanu, Z.; Julian, B. A.; Jackson, S. Defective galactosylation and clearance of IgA1 molecules as a possible etiopathogenic factor in IgA nephropathy Contrib. Nephrol. 1993, 104, 172-82 10.1159/000422410
8. Hiki, Y.; Odani, H.; Takahashi, M.; Yasuda, Y.; Nishimoto, A.; Iwase, H.; Shinzato, T.; Kobayashi, Y.; Maeda, K. Mass spectrometry proves under-O-glycosylation of glomerular IgA1 in IgA nephropathy Kidney Int. 2001, 59, 1077-85 10.1046/j.1523-1755.2001.00591.x
9. Basset; Durand; Jamin; Cle′ment; Pennec; Youinou; Dueymes; Roitt Increased N-Linked Glycosylation Leading to Oversialylation of Monomeric Immunoglobulin A1 from Patients with Sjögreńs Syndrome Scand. J. Immunol. 2000, 51, 300-306 10.1046/j.1365-3083.2000.00685.x
10. Coppo, R.; Amore, A. Aberrant glycosylation in IgA nephropathy (IgAN) Kidney Int. 2004, 65, 1544-7 10.1111/j.1523-1755.2004.05407.x
11. Bause, E. Structural requirements of N-glycosylation of proteins. Studies with proline peptides as conformational probes Biochem. J. 1983, 209, 331-6 10.1042/bj2090331
12. Marino, K.; Bones, J.; Kattla, J. J.; Rudd, P. M. A systematic approach to protein glycosylation analysis: a path through the maze Nat. Chem. Biol. 2010, 6, 713-23 10.1038/nchembio.437
13. Ruhaak, L. R.; Zauner, G.; Huhn, C.; Bruggink, C.; Deelder, A. M.; Wuhrer, M. Glycan labeling strategies and their use in identification and quantification Anal. Bioanal. Chem. 2010, 397, 3457-81 10.1007/s00216-010-3532-z
14. Viseux, N.; Hronowski, X.; Delaney, J.; Domon, B. Qualitative and Quantitative Analysis of the Glycosylation Pattern of Recombinant Proteins Anal. Chem. 2001, 73, 4755-4762 10.1021/ac015560a
15. Aldredge, D.; An, H. J.; Tang, N.; Waddell, K.; Lebrilla, C. B. Annotation of a serum N-glycan library for rapid identification of structures J. Proteome Res. 2012, 11, 1958-68 10.1021/pr2011439
16. Wuhrer, M.; Stam, J. C.; van de Geijn, F. E.; Koeleman, C. A.; Verrips, C. T.; Dolhain, R. J.; Hokke, C. H.; Deelder, A. M. Glycosylation profiling of immunoglobulin G (IgG) subclasses from human serum Proteomics 2007, 7, 4070-81 10.1002/pmic.200700289
17. Ahn, J.-M.; Sung, H.-J.; Yoon, Y.-H.; Kim, B.-G.; Yang, W. S.; Lee, C.; Park, H.-M.; Kim, B.-J.; Kim, B.-G.; Lee, S.-Y.; An, H.-J.; Cho, J.-Y. Integrated Glycoproteomics Demonstrates Fucosylated Serum Paraoxonase 1 Alterations in Small Cell Lung Cancer Mol. Cell. Proteomics 2014, 13, 30-48 10.1074/mcp.M113.028621
18. Satomi, Y.; Shimonishi, Y.; Hase, T.; Takao, T. Site-specific carbohydrate profiling of human transferrin by nano-flow liquid chromatography/electrospray ionization mass spectrometry Rapid Commun. Mass Spectrom. 2004, 18, 2983-2988 10.1002/rcm.1718
19. Kolarich, D.; Weber, A.; Turecek, P. L.; Schwarz, H.-P.; Altmann, F. Comprehensive glyco-proteomic analysis of human α1-antitrypsin and its charge isoforms Proteomics 2006, 6, 3369-3380 10.1002/pmic.200500751
20. Harazono, A.; Kawasaki, N.; Itoh, S.; Hashii, N.; Matsuishi-Nakajima, Y.; Kawanishi, T.; Yamaguchi, T. Simultaneous glycosylation analysis of human serum glycoproteins by high-performance liquid chromatography/tandem mass spectrometry J. Chromatogr. B: Anal. Technol. Biomed. Life Sci. 2008, 869, 20-30 10.1016/j.jchromb.2008.05.006
21. Pompach, P.; Brnakova, Z.; Sanda, M.; Wu, J.; Edwards, N.; Goldman, R. Site-specific Glycoforms of Haptoglobin in Liver Cirrhosis and Hepatocellular Carcinoma Mol. Cell. Proteomics 2013, 12, 1281-1293 10.1074/mcp.M112.023259
22. Hirani, S.; Lambris, J. D.; Müller-Eberhard, H. J. Structural analysis of the asparagine-linked oligosaccharides of human complement component C3 Biochem. J. 1986, 233, 613-616 10.1042/bj2330613
23. Ritchie, G. E.; Moffatt, B. E.; Sim, R. B.; Morgan, B. P.; Dwek, R. A.; Rudd, P. M. Glycosylation and the Complement System Chem. Rev. (Washington, DC, U. S.) 2002, 102, 305-320 10.1021/cr990294a
24. Lin, Z.; Lo, A.; Simeone, D. M.; Ruffin, M. T.; Lubman, D. M. An N-glycosylation Analysis of Human Alpha-2-Macroglobulin Using an Integrated Approach J. Proteomics Bioinf. 2012, 5, 127-134 10.4172/jpb.1000224
25. Imre, T.; Schlosser, G.; Pocsfalvi, G.; Siciliano, R.; Molnár-Szöllosi, é.; Kremmer, T.; Malorni, A.; Vékey, K. Glycosylation site analysis of human alpha-1-acid glycoprotein (AGP) by capillary liquid chromatography-electrospray mass spectrometry J. Mass Spectrom. 2005, 40, 1472-1483 10.1002/jms.938
26. Treuheit, M. J.; Costello, C. E.; Halsall, H. B. Analysis of the five glycosylation sites of human alpha 1-acid glycoprotein Biochem. J. 1992, 283 (Pt 1) 105-12 10.1042/bj2830105
27. Arnold, J. N.; Radcliffe, C. M.; Wormald, M. R.; Royle, L.; Harvey, D. J.; Crispin, M.; Dwek, R. A.; Sim, R. B.; Rudd, P. M. The Glycosylation of Human Serum IgD and IgE and the Accessibility of Identified Oligomannose Structures for Interaction with Mannan-Binding Lectin J. Immunol. 2004, 173, 6831-6840 10.4049/jimmunol.173.11.6831
28. Bakovic, M. P.; Selman, M. H.; Hoffmann, M.; Rudan, I.; Campbell, H.; Deelder, A. M.; Lauc, G.; Wuhrer, M. High-throughput IgG Fc N-glycosylation profiling by mass spectrometry of glycopeptides J. Proteome Res. 2013, 12, 821-31 10.1021/pr300887z
29. Baenziger, J.; Kornfeld, S. Structure of the Carbohydrate Units of IgA1 Immunoglobulin: I. COMPOSITION, GLYCOPEPTIDE ISOLATION, AND STRUCTURE OF THE ASPARAGINE-LINKED OLIGOSACCHARIDE UNITS J. Biol. Chem. 1974, 249, 7260-7269
30. Zhao, J.; Qiu, W.; Simeone, D. M.; Lubman, D. M. N-linked Glycosylation Profiling of Pancreatic Cancer Serum Using Capillary Liquid Phase Separation Coupled with Mass Spectrometric Analysis J. Proteome Res. 2007, 6, 1126-1138 10.1021/pr0604458
31. Mattu, T. S.; Pleass, R. J.; Willis, A. C.; Kilian, M.; Wormald, M. R.; Lellouch, A. C.; Rudd, P. M.; Woof, J. M.; Dwek, R. A. The Glycosylation and Structure of Human Serum IgA1, Fab, and Fc Regions and the Role of N-Glycosylation on Fcα Receptor Interactions J. Biol. Chem. 1998, 273, 2260-2272 10.1074/jbc.273.4.2260
32. Arnold, J. N.; Wormald, M. R.; Suter, D. M.; Radcliffe, C. M.; Harvey, D. J.; Dwek, R. A.; Rudd, P. M.; Sim, R. B. Human Serum IgM Glycosylation: IDENTIFICATION OF GLYCOFORMS THAT CAN BIND TO MANNAN-BINDING LECTIN J. Biol. Chem. 2005, 280, 29080-29087 10.1074/jbc.M504528200
33. Strum, J. S.; Nwosu, C. C.; Hua, S.; Kronewitter, S. R.; Seipert, R. R.; Bachelor, R. J.; An, H. J.; Lebrilla, C. B. Automated assignments of N- and O-site specific glycosylation with extensive glycan heterogeneity of glycoprotein mixtures Anal. Chem. 2013, 85, 5666-75 10.1021/ac4006556
34. Song, E.; Pyreddy, S.; Mechref, Y. Quantification of glycopeptides by multiple reaction monitoring liquid chromatography/tandem mass spectrometry Rapid Commun. Mass Spectrom. 2012, 26, 1941-1954 10.1002/rcm.6290
35. Kurogochi, M.; Matsushista, T.; Amano, M.; Furukawa, J.-i.; Shinohara, Y.; Aoshima, M.; Nishimura, S.-I. Sialic Acid-focused Quantitative Mouse Serum Glycoproteomics by Multiple Reaction Monitoring Assay Mol. Cell. Proteomics 2010, 9, 2354-2368 10.1074/mcp.M110.000430
36. Hülsmeier, A. J.; Paesold-Burda, P.; Hennet, T. N-Glycosylation Site Occupancy in Serum Glycoproteins Using Multiple Reaction Monitoring Liquid Chromatography-Mass Spectrometry Mol. Cell. Proteomics 2007, 6, 2132-2138 10.1074/mcp.M700361-MCP200
37. Sanda, M.; Pompach, P.; Brnakova, Z.; Wu, J.; Makambi, K.; Goldman, R. Quantitative liquid chromatography-mass spectrometry-multiple reaction monitoring (LC-MS-MRM) analysis of site-specific glycoforms of haptoglobin in liver disease Mol. Cell. Proteomics 2013, 12, 1294-305 10.1074/mcp.M112.023325
38. Sanda, M.; Pompach, P.; Brnakova, Z.; Wu, J.; Makambi, K.; Goldman, R. Quantitative Liquid Chromatography-Mass Spectrometry-Multiple Reaction Monitoring (LC-MS-MRM) Analysis of Site-specific Glycoforms of Haptoglobin in Liver Disease Mol. Cell. Proteomics 2013, 12, 1294-1305 10.1074/mcp.M112.023325
39. Hong, Q.; Lebrilla, C. B.; Miyamoto, S.; Ruhaak, L. R. Absolute quantitation of immunoglobulin g and its glycoforms using multiple reaction monitoring Anal. Chem. 2013, 85, 8585-93 10.1021/ac4009995
40. Kronewitter, S. R.; An, H. J.; de Leoz, M. L.; Lebrilla, C. B.; Miyamoto, S.; Leiserowitz, G. S. The development of retrosynthetic glycan libraries to profile and classify the human serum N-linked glycome Proteomics 2009, 9, 2986-2994 10.1002/pmic.200800760
41. Nwosu, C. C.; Seipert, R. R.; Strum, J. S.; Hua, S. S.; An, H. J.; Zivkovic, A. M.; German, B. J.; Lebrilla, C. B. Simultaneous and Extensive Site-specific N- and O-Glycosylation Analysis in Protein Mixtures J. Proteome Res. 2011, 10, 2612-2624 10.1021/pr2001429
42. Arnold, J. N.; Wallis, R.; Willis, A. C.; Harvey, D. J.; Royle, L.; Dwek, R. A.; Rudd, P. M.; Sim, R. B. Interaction of mannan binding lectin with alpha2 macroglobulin via exposed oligomannose glycans: a conserved feature of the thiol ester protein family? J. Biol. Chem. 2006, 281, 6955-63 10.1074/jbc.M511432200
43. Ramachandran, P.; Boontheung, P.; Xie, Y.; Sondej, M.; Wong, D. T.; Loo, J. A. Identification of N-Linked Glycoproteins in Human Saliva by Glycoprotein Capture and Mass Spectrometry J. Proteome Res. 2006, 5, 1493-1503 10.1021/pr050492k
44. Picariello, G.; Ferranti, P.; Mamone, G.; Roepstorff, P.; Addeo, F. Identification of N-linked glycoproteins in human milk by hydrophilic interaction liquid chromatography and mass spectrometry Proteomics 2008, 8, 3833-3847 10.1002/pmic.200701057
45. Kerr, M. A. The structure and function of human IgA Biochem. J. 1990, 271, 285-96 10.1042/bj2710285
46. Mellquist, J. L.; Kasturi, L.; Spitalnik, S. L.; Shakin-Eshleman, S. H. The Amino Acid Following an Asn-X-Ser/Thr Sequon Is an Important Determinant of N-Linked Core Glycosylation Efficiency Biochemistry 1998, 37, 6833-6837 10.1021/bi972217k
47. Huhn, C.; Selman, M. H.; Ruhaak, L. R.; Deelder, A. M.; Wuhrer, M. IgG glycosylation analysis Proteomics 2009, 9, 882-913 10.1002/pmic.200800715
48. Mimura, Y.; Ashton, P. R.; Takahashi, N.; Harvey, D. J.; Jefferis, R. Contrasting glycosylation profiles between Fab and Fc of a human IgG protein studied by electrospray ionization mass spectrometry J. Immunol. Methods 2007, 326, 116-126 10.1016/j.jim.2007.07.014
49. Selman, M. H. J.; Derks, R. J. E.; Bondt, A.; Palmblad, M.; Schoenmaker, B.; Koeleman, C. A. M.; van de Geijn, F. E.; Dolhain, R. J. E. M.; Deelder, A. M.; Wuhrer, M. Fc specific IgG glycosylation profiling by robust nano-reverse phase HPLC-MS using a sheath-flow ESI sprayer interface J. Proteomics 2012, 75, 1318-1329 10.1016/j.jprot.2011.11.003
50. Calvano, C. D.; Zambonin, C. G.; Jensen, O. N. Assessment of lectin and HILIC based enrichment protocols for characterization of serum glycoproteins by mass spectrometry J. Proteomics 2008, 71, 304-17 10.1016/j.jprot.2008.06.013
51. Gonzalez-Quintela, A.; Alende, R.; Gude, F.; Campos, J.; Rey, J.; Meijide, L. M.; Fernandez-Merino, C.; Vidal, C. Serum levels of immunoglobulins (IgG, IgA, IgM) in a general adult population and their relationship with alcohol consumption, smoking and common metabolic abnormalities Clin. Exp. Immunol. 2008, 151, 42-50 10.1111/j.1365-2249.2007.03545.x
52. Sinha, S.; Pipes, G.; Topp, E. M.; Bondarenko, P. V.; Treuheit, M. J.; Gadgil, H. S. Comparison of LC and LC/MS Methods for Quantifying N-Glycosylation in Recombinant IgGs J. Am. Soc. Mass Spectrom. 2008, 19, 1643-1654 10.1016/j.jasms.2008.07.004
53. Arnold, J. N.; Wormald, M. R.; Sim, R. B.; Rudd, P. M.; Dwek, R. A. The Impact of Glycosylation on the Biological Function and Structure of Human Immunoglobulins Annu. Rev. Immunol. 2007, 25, 21-50 10.1146/annurev.immunol.25.022106.141702
54. Tanaka, A.; Iwase, H.; Hiki, Y.; Kokubo, T.; Ishii-Karakasa, I.; Toma, K.; Kobayashi, Y.; Hotta, K. Evidence for a site-specific fucosylation of N-linked oligosaccharide of immunoglobulin A1 from normal human serum Glycoconjugate J. 1998, 15, 995-1000 10.1023/A:1006989910120
55. Royle, L.; Roos, A.; Harvey, D. J.; Wormald, M. R.; Van Gijlswijk-Janssen, D.; Redwan, E.-R. M.; Wilson, I. A.; Daha, M. R.; Dwek, R. A.; Rudd, P. M. Secretory IgA N- and O-Glycans Provide a Link between the Innate and Adaptive Immune Systems J. Biol. Chem. 2003, 278, 20140-20153 10.1074/jbc.M301436200
56. Satomi, Y.; Shimonishi, Y.; Takao, T. N-glycosylation at Asn491 in the Asn-Xaa-Cys motif of human transferrin FEBS Lett. 2004, 576, 51-56 10.1016/j.febslet.2004.08.061
57. Comunale, M. A.; Rodemich-Betesh, L.; Hafner, J.; Wang, M.; Norton, P.; Di Bisceglie, A. M.; Block, T.; Mehta, A. Linkage Specific Fucosylation of Alpha-1-Antitrypsin in Liver Cirrhosis and Cancer Patients: Implications for a Biomarker of Hepatocellular Carcinoma PLoS One 2010, 5, e12419 10.1371/journal.pone.0012419
58. Crispin, M. D.; Ritchie, G. E.; Critchley, A. J.; Morgan, B. P.; Wilson, I. A.; Dwek, R. A.; Sim, R. B.; Rudd, P. M. Monoglucosylated glycans in the secreted human complement component C3: implications for protein biosynthesis and structure FEBS Lett. 2004, 566, 270-4 10.1016/j.febslet.2004.04.045