Identification of salivary N-glycoproteins and measurement of glycosylation site occupancy by boronate glycoprotein enrichment and liquid chromatography/electrospray ionization tandem mass spectrometry

Rapid Communications in Mass Spectrometry

Volumn 28, Issue 5, 2014, Pages 471-482

  Xu, Ying ^a   Bailey, Ulla Maja ^a   Punyadeera, Chamindie ^a   Schulz, Benjamin L ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BIOMARKERS; BODY FLUIDS; ELECTROSPRAY IONIZATION; GLYCOSYLATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; PEPTIDES;

BORONATES; GLYCOSYLATION SITE OCCUPANCIES; GLYCOSYLATION SITES; GLYCOSYLATIONS; HEALTHY INDIVIDUALS; LIQUID CHROMATOGRAPHY ELECTROSPRAY; MEASUREMENTS OF; N-GLYCOPROTEIN; SITE-SPECIFIC; SITE-SPECIFIC GLYCOSYLATION;

GLYCOPROTEINS;

GLYCOPROTEIN; SALIVA PROTEIN;

ADULT; AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; ELECTROSPRAY MASS SPECTROMETRY; FEMALE; GLYCOSYLATION; HUMAN; LIQUID CHROMATOGRAPHY; MALE; METHODOLOGY; MOLECULAR GENETICS; TANDEM MASS SPECTROMETRY; YOUNG ADULT;

ADULT; AMINO ACID SEQUENCE; CHROMATOGRAPHY, LIQUID; FEMALE; GLYCOPROTEINS; GLYCOSYLATION; HUMANS; MALE; MOLECULAR SEQUENCE DATA; SALIVARY PROTEINS AND PEPTIDES; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY; YOUNG ADULT;

EID: 84893456266     PISSN: 09514198     EISSN: 10970231     Source Type: Journal    
DOI: 10.1002/rcm.6806     Document Type: Article

References (54)

1. B. L. Schulz, J. C. White, C. Punyadeera,. Saliva proteome research: current status and future outlook. Crit. Rev. Biotechnol. 2013, 33, 246.
2. N. Spielmann, D. T. Wong,. Saliva: diagnostics and therapeutic perspectives. Oral Dis. 2011, 17, 345.
3. E. Topkas, P. Keith, G. Dimeski, J. Cooper-White, C. Punyadeera,. Evaluation of saliva collection devices for the analysis of proteins. Clin. Chim. Acta 2012, 413, 1066.
4. R. Mohamed, J. L. Campbell, J. Cooper-White, G. Dimeski, C. Punyadeera,. The impact of saliva collection and processing methods on CRP, IgE, and Myoglobin immunoassays. Clin. Transl. Med. 2012, 1, 19.
5. J. Y. Foo, Y. Wan, K. Kostner, A. Arivalagan, J. Atherton, J. Cooper-White, G. Dimeski, C. Punyadeera,. NT-ProBNP levels in saliva and its clinical relevance to heart failure. PLoS One 2012, 7, e48452.
6. D. A. Ovchinnikov, M. A. Cooper, P. Pandit, W. B. Coman, J. J. Cooper-White, P. Keith, E. J. Wolvetang, P. D. Slowey, C. Punyadeera,. Tumor-suppressor gene promoter hypermethylation in saliva of head and neck cancer patients. Transl. Oncol. 2012, 5, 321.
7. S. Bandhakavi, S. K. Van Riper, P. N. Tawfik, M. D. Stone, T. Haddad, N. L. Rhodus, J. V. Carlis, T. J. Griffin,. Hexapeptide libraries for enhanced protein PTM identification and relative abundance profiling in whole human saliva. J. Proteome Res. 2010, 10, 1052.
8. E. J. Helmerhorst, F. G. Oppenheim,. Saliva: a dynamic proteome. J. Dent. Res. 2007, 86, 680.
9. T. Pfaffe, J. Cooper-White, P. Beyerlein, K. Kostner, C. Punyadeera,. Diagnostic potential of saliva: current state and future applications. Clin. Chem. 2011, 57, 675.
10. R. Vitorino, R. Alves, A. Barros, A. Caseiro, R. Ferreira, M. C. Lobo, A. Bastos, J. Duarte, D. Carvalho, L. L. Santos, F. L. Amado,. Finding new posttranslational modifications in salivary proline-rich proteins. Proteomics 2010, 10, 3732.
11. C. Hirtz, F. Chevalier, D. Centeno, V. Rofidal, J. C. Egea, M. Rossignol, N. Sommerer, D. Deville de Periere,. MS characterization of multiple forms of alpha-amylase in human saliva. Proteomics 2005, 5, 4597.
12. U. M. Bailey, C. Punyadeera, J. J. Cooper-White, B. L. Schulz,. Analysis of the extreme diversity of salivary alpha-amylase isoforms generated by physiological proteolysis using liquid chromatography-tandem mass spectrometry. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2012, 911, 21.
13. M. D. Stone, X. Chen, T. McGowan, S. Bandhakavi, B. Cheng, N. L. Rhodus, T. J. Griffin,. Large-scale phosphoproteomics analysis of whole saliva reveals a distinct phosphorylation pattern. J. Proteome Res. 2011, 10, 1728.
14. C. Kasinathan, N. Gandhi, P. Ramaprasad, P. Sundaram, N. Ramasubbu,. Tyrosine sulfation of statherin. Int. J. Biol. Sci. 2007, 3, 237.
15. T. Cabras, C. Fanali, J. A. Monteiro, F. Amado, R. Inzitari, C. Desiderio, E. Scarano, B. Giardina, M. Castagnola, I. Messana,. Tyrosine polysulfation of human salivary histatin 1. A post-translational modification specific of the submandibular gland. J. Proteome Res. 2007, 6, 2472.
16. M. Sondej, P. A. Denny, Y. Xie, P. Ramachandran, Y. Si, J. Takashima, W. Shi, D. T. Wong, J. A. Loo, P. C. Denny,. Glycoprofiling of the human salivary proteome. Clin. Proteomics 2009, 5, 52.
17. B. L. Schulz, N. H. Packer, N. G. Karlsson,. Small-scale analysis of O-linked oligosaccharides from glycoproteins and mucins separated by gel electrophoresis. Anal. Chem. 2002, 74, 6088.
18. K. A. Thomsson, B. L. Schulz, N. H. Packer, N. G. Karlsson,. MUC5B glycosylation in human saliva reflects blood group and secretor status. Glycobiology 2005, 15, 791.
19. N. G. Karlsson, K. A. Thomsson,. Salivary MUC7 is a major carrier of blood group I type O-linked oligosaccharides serving as the scaffold for sialyl Lewis x. Glycobiology 2009, 19, 288.
20. D. J. Kelleher, R. Gilmore,. An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology 2006, 16, 47R.
21. E. Mohorko, R. Glockshuber, M. Aebi,. Oligosaccharyl-transferase: the central enzyme of N-linked protein glycosylation. J. Inherit. Metab. Dis. 2011, 34, 869.
22. C. Lizak, S. Gerber, S. Numao, M. Aebi, K. P. Locher,. X-ray structure of a bacterial oligosaccharyltransferase. Nature 2011, 474, 350.
23. B. L. Schulz, in Glycosylation, (Ed:, S. Petrescu,). Intech, 2012.
24. F. Schwarz, M. Aebi,. Mechanisms and principles of N-linked protein glycosylation. Curr. Opin. Struct. Biol. 2011, 21, 576.
25. A. Helenius, M. Aebi,. Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 2004, 73, 1019.
26. K. Ohtsubo, J. D. Marth,. Glycosylation in cellular mechanisms of health and disease. Cell 2006, 126, 855.
27. B. Adamczyk, T. Tharmalingam, P. M. Rudd,. Glycans as cancer biomarkers. Biochim. Biophys. Acta 2011, 1820, 1347.
28. R. Ossola, R. Schiess, P. Picotti, O. Rinner, L. Reiter, R. Aebersold,. Biomarker validation in blood specimens by selected reaction monitoring mass spectrometry of N-glycosites. Methods Mol. Biol. 2011, 728, 179.
29. P. Ramachandran, P. Boontheung, Y. Xie, M. Sondej, D. T. Wong, J. A. Loo,. Identification of N-linked glycoproteins in human saliva by glycoprotein capture and mass spectrometry. J. Proteome Res. 2006, 5, 1493.
30. H. Zhang, X. J. Li, D. B. Martin, R. Aebersold,. Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry. Nat. Biotechnol. 2003, 21, 660.
31. U. Lewandrowski, A. Sickmann,. N-glycosylation site analysis of human platelet proteins by hydrazide affinity capturing and LC-MS/MS. Methods Mol. Biol. 2009, 534, 225.
32. D. F. Zielinska, F. Gnad, J. R. Wisniewski, M. Mann,. Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints. Cell 2010, 141, 897.
33. Y. H. Ahn, P. M. Shin, E. S. Ji, H. Kim, J. S. Yoo,. A lectin-coupled, multiple reaction monitoring based quantitative analysis of human plasma glycoproteins by mass spectrometry. Anal. Bioanal. Chem. 2012, 402, 2101.
34. D. Kolarich, P. H. Jensen, F. Altmann, N. H. Packer,. Determination of site-specific glycan heterogeneity on glycoproteins. Nat. Protocols 2012, 7, 1285.
35. S. Mysling, G. Palmisano, P. Højrup, M. Thaysen-Andersen,. Utilizing ion-pairing hydrophilic interaction chromatography solid phase extraction for efficient glycopeptide enrichment in glycoproteomics. Anal. Chem. 2010, 82, 5598.
36. U. M. Bailey, M. F. B. Jamaluddin, B. L. Schulz,. Analysis of congenital disorder of glycosylation-Id in a yeast model system shows diverse site-specific under-glycosylation of glycoproteins. J. Proteome Res. 2012, 11, 5376.
37. H. H. Freeze, M. Aebi,. Altered glycan structures: the molecular basis of congenital disorders of glycosylation. Curr. Opin. Struct. Biol. 2005, 15, 490.
38. F. Dall'Olio, N. Malagolini, M. Trinchera, M. Chiricolo,. Mechanisms of cancer-associated glycosylation changes. Front. Biosci. 2012, 1, 670.
39. M. Nita-Lazar, V. Noonan, I. Rebustini, J. Walker, A. S. Menko, M. A. Kukuruzinska,. Overexpression of DPAGT1 leads to aberrant N-glycosylation of E-cadherin and cellular discohesion in oral cancer. Cancer Res. 2009, 69, 5673.
40. Y. Li, E. L. Larsson, H. Jungvid, I. Y. Galaev, B. Mattiasson,. Affinity chromatography of neoglycoproteins. Bioseparation 2000, 9, 315.
41. Y. Li, U. Pfüller, E. L. Larsson, H. Jungvid, I. Y. Galaev, B. Mattiasson,. Separation of mistletoe lectins based on the degree of glycosylation using boronate affinity chromatography. J. Chromatogr. A 2001, 925, 115.
42. C. Punyadeera, G. Dimeski, K. Kostner, P. Beyerlein, J. Cooper-White,. One-step homogeneous C-reactive protein assay for saliva. J. Immunol. Methods 2011, 373, 19.
43. Y. Lu, Z. Bie, Y. Liu, Z. Liu,. Fine-tuning the specificity of boronate affinity monoliths toward glycoproteins through pH manipulation. Analyst 2013, 138, 290.
44. S. N. Mohd Yusuf, U. M. Bailey, N. Y. J. Tan, M. F. B. Jamaluddin, B. L. Schulz,. Mixed disulfide formation in vitro between a glycoprotein substrate and yeast oligosaccharyltransferase subunits Ost3p and Ost6p. Biochem. Biophys. Res. Commun. 2013, 432, 438.
45. B. L. Schulz, M. Aebi,. Analysis of glycosylation site occupancy reveals a role for Ost3p and Ost6p in site-specific N-glycosylation efficiency. Mol. Cell. Proteomics 2009, 8, 357.
46. N. L. Wilson, B. L. Schulz, N. G. Karlsson, N. H. Packer,. Sequential analysis of N- and O-linked glycosylation of 2D-PAGE separated glycoproteins. J. Proteome Res. 2002, 1, 521.
47. Available: http://www.uniprot.org/.
48. G. Palmisano, M. N. Melo-Braga, K. Engholm-Keller, B. L. Parker, M. R. Larsen,. Chemical deamidation: a common pitfall in large-scale N-linked glycoproteomic mass spectrometry-based analyses. J. Proteome Res. 2012, 11, 1949.
49. P. Ramachandran, P. Boontheung, E. Pang, W. Yan, D. T. Wong, J. A. Loo,. Comparison of N-linked glycoproteins in human whole saliva, parotid, submandibular, and sublingual glandular secretions identified using hydrazide chemistry and mass spectrometry. Clin. Proteomics 2008, 4, 80.
50. N. E. Robinson, Z. W. Robinson, B. R. Robinson, A. L. Robinson, J. A. Robinson, M. L. Robinson, A. B. Robinson,. Structure-dependent nonenzymatic deamidation of glutaminyl and asparaginyl pentapeptides. J. Pept. Res. 2004, 63, 426.
51. O. V. Krokhin, M. Antonovici, W. Ens, J. A. Wilkins, K. G. Standing,. Deamidation of -Asn-Gly- sequences during sample preparation for proteomics: Consequences for MALDI and HPLC-MALDI analysis. Anal. Chem. 2006, 78, 6645.
52. L. Kasturi, J. R. Eshleman, W. H. Wunner, S. H. Shakin-Eshleman,. The hydroxy amino acid in an Asn-X-Ser/Thr sequon can influence N-linked core glycosylation efficiency and the level of expression of a cell surface glycoprotein. J. Biol. Chem. 1995, 270, 14756.
53. W. Breuer, R. A. Klein, B. Hardt, A. Bartoschek, E. Bause,. Oligosaccharyltransferase is highly specific for the hydroxy amino acid in Asn-Xaa-Thr/Ser. FEBS Lett. 2001, 501, 106.
54. M. Kowarik, S. Numao, M. F. Feldman, B. L. Schulz, N. Callewaert, E. Kiermaier, I. Catrein, M. Aebi,. N-linked glycosylation of folded proteins by the bacterial oligosaccharyltransferase. Science 2006, 314, 1148.