High-performance targeted mass spectrometry with precision data-independent acquisition reveals site-specific glycosylation macroheterogeneity

Analytical Biochemistry

Volumn 510, Issue , 2016, Pages 106-113

  Yeo, K Y Benjamin ^a   Chrysanthopoulos, Panagiotis K ^a   Nouwens, Amanda S ^a   Marcellin, Esteban ^a   Schulz, Benjamin L ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Data independent acquisition; Glycosylation; Macroheterogeneity; Mass spectrometry; Oligosaccharyltransferase

Indexed keywords

MACHINERY; MASS SPECTROMETRY; PROTEINS; YEAST;

DATA-INDEPENDENT ACQUISITION; MACROHETEROGENEITY; MULTIPLE REACTION MONITORING; OLIGOSACCHARYLTRANSFERASE; POST-TRANSLATIONAL MODIFICATIONS; QUANTITATIVE CHARACTERIZATION; SELECTED REACTION MONITORING; SITE-SPECIFIC GLYCOSYLATION;

GLYCOSYLATION;

GLYCOPEPTIDE; GLYCOPROTEIN; SYNTHETIC PEPTIDE; SACCHAROMYCES CEREVISIAE PROTEIN;

ANALYTIC METHOD; ARTICLE; BIOACCUMULATION; CELL WALL; COMPARATIVE STUDY; CONCENTRATION PROCESS; CONTROLLED STUDY; DATA DEPENDENT ACQUISITION; DATA EXTRACTION; GENETIC HETEROGENEITY; MASS SPECTROMETRY; MEASUREMENT ACCURACY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN GLYCOSYLATION; PROTEOMICS; QUANTITATIVE ANALYSIS; SELECTED REACTION MONITORING; SEQUENTIAL WINDOW ACQUISITION OF ALL THEORETICAL FRAGMENT ION; SEQUENTIAL WINDOW ACQUISITION OF TARGETED FRAGMENT ION; YEAST; CHEMISTRY; GLYCOSYLATION; METABOLISM; PROCEDURES; SACCHAROMYCES CEREVISIAE;

GLYCOSYLATION; MASS SPECTROMETRY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84979716013     PISSN: 00032697     EISSN: 10960309     Source Type: Journal    
DOI: 10.1016/j.ab.2016.06.009     Document Type: Article

References (39)

1. [1] Aebersold, R., Mann, M., Mass spectrometry-based proteomics. Nature 422 (2003), 198–207.
2. [2] Domon, B., Aebersold, R., Mass spectrometry and protein analysis. Science 312 (2006), 212–217.
3. [3] Gillet, L.C., Navarro, P., Tate, S., Röst, H., Selevsek, N., Reiter, L., Bonner, R., Aebersold, R., Targeted data extraction of the MS/MS spectra generated by data-independent acquisition: A new concept for consistent and accurate proteome analysis. Mol. Cell. Proteomics, 11, 2012, 10.1074/mcp.O111.016717.
4. [4] Rosenberger, G., Koh, C.C., Guo, T., Röst, H.L., Kouvonen, P., Collins, B.C., Heusel, M., Liu, Y., Caron, E., Vichalkovski, A., Faini, M., Schubert, O.T., Faridi, P., Ebhardt, H.A., Matondo, M., Lam, H., Bader, S.L., Campbell, D.S., Deutsch, E.W., Moritz, R.L., Tate, S., Aebersold, R., A repository of assays to quantify 10,000 human proteins by SWATH–MS. Sci. Data, 1, 2014, 140031.
5. [5] Röst, H.L., Rosenberger, G., Navarro, P., Gillet, L., Miladinovic, S.M., Schubert, O.T., Wolski, W., Collins, B.C., Malmström, J., Malmström, L., Aebersold, R., OpenSWATH enables automated, targeted analysis of data-independent acquisition MS data. Nat. Biotechnol. 32 (2014), 219–223.
6. [6] Liu, Y., Chen, J., Sethi, A., Li, Q.K., Chen, L., Collins, B., Gillet, L.C., Wollscheid, B., Zhang, H., Aebersold, R., Glycoproteomic analysis of prostate cancer tissues by SWATH mass spectrometry discovers N-acylethanolamine acid amidase and protein tyrosine kinase 7 as signatures for tumor aggressiveness. Mol. Cell. Proteomics 13 (2014), 1753–1768.
7. [7] Liu, Y., Hüttenhain, R., Surinova, S., Gillet, L.C., Mouritsen, J., Brunner, R., Navarro, P., Aebersold, R., Quantitative measurements of N-linked glycoproteins in human plasma by SWATH–MS. Proteomics 13 (2013), 1247–1256.
8. [8] Orellana, C.A., Marcellin, E., Schulz, B.L., Nouwens, A.S., Gray, P.P., Nielsen, L.K., High-antibody-producing Chinese hamster ovary cells up-regulate intracellular protein transport and glutathione synthesis. J. Proteome Res. 14 (2015), 609–618.
9. [9] Keller, A., Bader, S.L., Kusebauch, U., Shteynberg, D., Hood, L., Moritz, R.L., Opening a SWATH window on post-translational modifications: automated pursuit of modified peptides. Mol. Cell. Proteomics 15 (2016), 1151–1163.
10. [10] Xu, Y., Bailey, U.M., Schulz, B.L., Automated measurement of site-specific N-glycosylation occupancy with SWATH–MS. Proteomics 15 (2015), 2177–2186.
11. [11] Zhang, H., Qian, P.Y., Ravasi, T., Selective phosphorylation during early macrophage differentiation. Proteomics 15 (2015), 3731–3743.
12. [12] Sidoli, S., Lin, S., Xiong, L., Bhanu, N.V., Karch, K.R., Johansen, E., Hunter, C., Mollah, S., Garcia, B.A., Sequential window acquisition of all theoretical mass spectra (SWATH) analysis for characterization and quantification of histone post-translational modifications. Mol. Cell. Proteomics 14 (2015), 2420–2428.
13. [13] Aebi, M., N-linked protein glycosylation in the ER. Biochem. Biophys. Acta 1833 (2013), 2430–2437.
14. [14] Kelleher, D.J., Gilmore, R., An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology 16 (2006), 47R–62R.
15. [15] Schwarz, M., Knauer, M., Lehle, L., Yeast oligosaccharyltransferase consists of two functionally distinct sub-complexes, specified by either the Ost3p or Ost6p subunit. FEBS Lett. 579 (2005), 6564–6568.
16. [16] Spirig, U., Bodmer, D., Wacker, M., Burda, P., Aebi, M., The 3.4-kDa Ost4 protein is required for the assembly of two distinct oligosaccharyltransferase complexes in yeast. Glycobiology 15 (2005), 1396–1406.
17. [17] Jamaluddin, M.F.B., Bailey, U.-M., Schulz, B.L., Oligosaccharyltransferase subunits bind polypeptide substrate to locally enhance N-glycosylation. Mol. Cell. Proteomics 13 (2014), 3286–3293.
18. [18] Jamaluddin, M.F., Bailey, U.M., Tan, N.Y., Stark, A.P., Schulz, B.L., Polypeptide binding specificities of Saccharomyces cerevisiae oligosaccharyltransferase accessory proteins Ost3p and Ost6p. Protein Sci. 20 (2011), 849–855.
19. [19] Schulz, B.L., Stirnimann, C.U., Grimshaw, J.P., Brozzo, M.S., Fritsch, F., Mohorko, E., Capitani, G., Glockshuber, R., Grutter, M.G., Aebi, M., Oxidoreductase activity of oligosaccharyltransferase subunits Ost3p and Ost6p defines site-specific glycosylation efficiency. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 11061–11066.
20. [20] Mohd Yusuf, S.N., Bailey, U.M., Tan, N.Y., Jamaluddin, M.F., Schulz, B.L., Mixed disulfide formation in vitro between a glycoprotein substrate and yeast oligosaccharyltransferase subunits Ost3p and Ost6p. Biochem. Biophys. Res. Commun. 432 (2013), 438–443.
21. [21] Mohorko, E., Owen, R.L., Malojcic, G., Brozzo, M.S., Aebi, M., Glockshuber, R., Structural basis of substrate specificity of human oligosaccharyl transferase subunit n33/tusc3 and its role in regulating protein N-glycosylation. Structure 22 (2014), 590–601.
22. [22] Schulz, B.L., Aebi, M., Analysis of glycosylation site occupancy reveals a role for Ost3p and Ost6p in site-specific N-glycosylation efficiency. Mol. Cell. Proteomics 8 (2009), 357–364.
23. [23] Picotti, P., Rinner, O., Stallmach, R., Dautel, F., Farrah, T., Domon, B., Holger, W., Aebersold, R., High-throughput generation of selected reaction monitoring assays for proteins and proteomes. Nat. Methods 7 (2010), 43–46.
24. [24] Reiter, L., Rinner, O., Picotti, P., Huttenhain, R., Beck, M., Brusniak, M.Y., Hengartner, M.O., Aebersold, R., mProphet: automated data processing and statistical validation for large-scale SRM experiments. Nat. Methods 8 (2011), 430–435.
25. [25] Surinova, S., Hüttenhain, R., Chang, C.Y., Espona, L., Vitek, O., Aebersold, R., Automated selected reaction monitoring data analysis workflow for large-scale targeted proteomic studies. Nat. Protoc. 8 (2013), 1602–1619.
26. [26] Lange, V., Picotti, P., Domon, B., Aebersold, R., Selected reaction monitoring for quantitative proteomics: A tutorial. Mol. Syst. Biol., 4, 2008, 222.
27. [27] Kim, K.H., Ahn, Y.H., Ji, E.S., Lee, J.Y., Kim, J.Y., An, H.J., Yoo, J.S., Quantitative analysis of low-abundance serological proteins with peptide affinity-based enrichment and pseudo-multiple reaction monitoring by hybrid quadrupole time-of-flight mass spectrometry. Anal. Chim. Acta 882 (2015), 38–48.
28. [28] Schilling, B., MacLean, B., Held, J.M., Sahu, A.K., Rardin, M.J., Sorensen, D.J., Peters, T., Wolfe, A.J., Hunter, C.L., MacCoss, M.J., Gibson, B.W., Multiplexed, scheduled, high-resolution parallel reaction monitoring on a full scan QqTOF Instrument with integrated data-dependent and targeted mass spectrometric workflows. Anal. Chem. 87 (2015), 10222–10229.
29. [29] Ding, X., Ghobarah, H., Zhang, X., Jaochico, A., Liu, X., Deshmukh, G., Liederer, B.M., Hop, C.E., Dean, B., High-throughput liquid chromatography/mass spectrometry method for the quantitation of small molecules using accurate mass technologies in supporting discovery drug screening. Rapid Commun. Mass Spectrom. 27 (2013), 401–408.
30. [30] Gallien, S., Duriez, E., Crone, C., Kellmann, M., Moehring, T., Domon, B., Targeted proteomic quantification on quadrupole–Orbitrap mass spectrometer. Mol. Cell. Proteomics 11 (2012), 1709–1723.
31. [31] Peterson, A.C., Russell, J.D., Bailey, D.J., Westphall, M.S., Coon, J.J., Parallel reaction monitoring for high resolution and high mass accuracy quantitative, targeted proteomics. Mol. Cell. Proteomics 11 (2012), 1475–1488.
32. [32] Law, K.P., Lim, Y.P., Recent advances in mass spectrometry: Data independent analysis and hyper reaction monitoring. Expert Rev. Proteomics 10 (2013), 551–566.
33. [33] Zhu, X., Liu, J., Wu, J., Cao, R., Li, T., Pharmacokinetic study of HS061, a new human insulin, in non-diabetic rat using ultra performance liquid chromatography–tandem mass spectrometry. J. Chromatogr. B 967 (2014), 50–56.
34. [34] Bailey, U.M., Jamaluddin, M.F.B., Schulz, B.L., Analysis of congenital disorder of glycosylation–Id in a yeast model system shows diverse site-specific under-glycosylation of glycoproteins. J. Proteome Res. 11 (2012), 5376–5383.
35. [35] Xu, Y., Bailey, U.M., Punyadeera, C., Schulz, B.L., Identification of salivary N-glycoproteins and measurement of glycosylation site occupancy by boronate glycoprotein enrichment and LC–ESI–MS/MS. Rapid Commun. Mass Spectrom. 28 (2014), 471–482.
36. [36] Thaysen-Andersen, M., Packer, N.H., Schulz, B.L., Maturing glycoproteomics technologies provide unique structural insights into the N-glycoproteome and its regulation in health and disease. Mol. Cell. Proteomics 15 (2016), 1773–1790.
37. [37] Zacchi, L.F., Schulz, B.L., N-Glycoprotein macroheterogeneity: Biological implications and proteomic characterization. Glycoconj. J. 33 (2016), 359–376.
38. [38] Cherepanova, N.A., Shrimal, S., Gilmore, R., Oxidoreductase activity is necessary for N-glycosylation of cysteine-proximal acceptor sites in glycoproteins. J. Cell Biol. 206 (2014), 525–539.
39. [39] Cherepanova, N.A., Gilmore, R., Mammalian cells lacking either the cotranslational or posttranslocational oligosaccharyltransferase complex display substrate-dependent defects in asparagine linked glycosylation. Sci. Rep., 6, 2016, 20946.