Simultaneous enrichment of plasma soluble and extracellular vesicular glycoproteins using prolonged ultracentrifugation-electrostatic repulsion-hydrophilic interaction chromatography (PUC-ERLIC) approach

Molecular and Cellular Proteomics

Volumn 14, Issue 6, 2015, Pages 1657-1671

  Cheow, Esther Sok Hwee ^a   Sim, Kae Hwan ^a   De Kleijn, Dominique ^b,c,d   Lee, Chuen Neng ^b,e,f   Sorokin, Vitaly ^b,e,f   Sze, Siu Kwan ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d Interuniversity Institute of the Netherlands   (Netherlands)

^e NATIONAL UNIVERSITY HEALTH SYSTEM   (Singapore)

^f Dept Medicine Endocrinol Diabet   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

EXTRACELLULAR VESICULAR GLYCOPROTEIN; GLYCOPROTEIN; PLASMA PROTEIN; UNCLASSIFIED DRUG; PROTEOME;

ARTICLE; CHROMATOGRAPHY; CLINICAL ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EVALUATION STUDY; EXOSOME; HUMAN; LIQUID CHROMATOGRAPHY; PLASMA; PRIORITY JOURNAL; PROLONGED ULTRACENTRIFUGATION ELECTROSTATIC REPULSION HYDROPHILIC INTERACTION CHROMATOGRAPHY; PROTEIN ANALYSIS; PROTEIN SECRETION; SUSPENSION; TANDEM MASS SPECTROMETRY; ULTRACENTRIFUGATION; BLOOD; CHEMICAL PHENOMENA; CHEMISTRY; HEART DISEASE; PROCEDURES; STATIC ELECTRICITY;

CHROMATOGRAPHY; GLYCOPROTEINS; HEART DISEASES; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; PLASMA; PROTEOME; STATIC ELECTRICITY; ULTRACENTRIFUGATION;

EID: 84930448260     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.O114.046391     Document Type: Article

References (74)

1. Shao, H., Chung, J., Balaj, L., Charest, A., Bigner, D. D., Carter, B. S., Hochberg, F. H., Breakefield, X. O., Weissleder, R., and Lee, H. (2012) Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy. Nat, Med. 18, 1835-1840
2. 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
3. Kaji, H., Shikanai, T., Sasaki-Sawa, A., Wen, H., Fujita, M., Suzuki, Y., Sugahara, D., Sawaki, H., Yamauchi, Y., Shinkawa, T., Taoka, M., Takahashi, N., Isobe, T., and Narimatsu, H. (2012) Large-scale identification of N-glycosylated proteins of mouse tissues and construction of a glycoprotein database, GlycoProtDB. J. Proteome Res. 11, 4553-4566
4. Zielinska, D. F., Gnad, F., Schropp, K., Wisniewski, J. R., and Mann, M. (2012) Mapping N-glycosylation sites across seven evolutionarily distant species reveals a divergent substrate proteome despite a common core machinery. Mol. Cell 46, 542-548
5. Berven, F. S., Ahmad, R., Clauser, K. R., and Carr, S. A. (2010) Optimizing performance of glycopeptide capture for plasma proteomics. J. Proteome Res. 9, 1706-1715
6. Ahn, Y. H., Kim, K. H., Shin, P. M., Ji, E. S., Kim, H., and Yoo, J. S. (2012) Identification of low-abundance cancer biomarker candidate TIMP1 from serum with lectin fractionation and peptide affinity enrichment by ultrahigh- resolution mass spectrometry. Anal. Chem. 84, 1425-1431
7. Qu, Y., Xia, S., Yuan, H., Wu, Q., Li, M., Zou, L., Zhang, L., Liang, Z., and Zhang, Y. (2011) Integrated sample pretreatment system for N-linked glycosylation site profiling with combination of hydrophilic interaction chromatography and PNGase F immobilized enzymatic reactor via a strong cation exchange precolumn. Anal. Chem. 83, 7457-7463
8. Hakimi, A., Auluck, J., Jones, G. D., Ng, L. L., and Jones, D. J. (2014) Assessment of reproducibility in depletion and enrichment workflows for plasma proteomics using label-free quantitative data-independent LCMS. Proteomics 14, 4-13
9. Tang, H. Y., Ali-Khan, N., Echan, L. A., Levenkova, N., Rux, J. J., and Speicher, D. W. (2005) A novel four-dimensional strategy combining protein and peptide separation methods enables detection of low-abundance proteins in human plasma and serum proteomes. Proteomics 5, 3329-3342
10. Keshishian, H., Addona, T., Burgess, M., Kuhn, E., and Carr, S. A. (2007) Quantitative, multiplexed assays for low abundance proteins in plasma by targeted mass spectrometry and stable isotope dilution. Mol. Cell. Proteomics 6, 2212-2229
11. Gonzalez-Begne, M., Lu, B., Liao, L., Xu, T., Bedi, G., Melvin, J. E., and Yates, J. R., 3rd (2011) Characterization of the human submandibular/ sublingual saliva glycoproteome using lectin affinity chromatography coupled to multidimensional protein identification technology. J. Proteome Res. 10, 5031-5046
12. Jung, K., Cho, W., and Regnier, F. E. (2009) Glycoproteomics of plasma based on narrow selectivity lectin affinity chromatography. J. Proteome Res. 8, 643-650
13. Tian, Y., Zhou, Y., Elliott, S., Aebersold, R., and Zhang, H. (2007) Solidphase extraction of N-linked glycopeptides. Nat. Protoc. 2, 334-339
14. Alvarez-Manilla, G., Atwood, J., 3rd, Guo, Y., Warren, N. L., Orlando, R., and Pierce, M. (2006) Tools for glycoproteomic analysis: size exclusion chromatography facilitates identification of tryptic glycopeptides with N-linked glycosylation sites. J. Proteome Res. 5, 701-708
15. Li, H., and Liu, Z. (2012) Recent advances in monolithic column-based boronate-affinity chromatography. TrAC Trends Anal. Chem. 37, 148-161
16. Palmisano, G., Lendal, S. E., Engholm-Keller, K., Leth-Larsen, R., Parker, B. L., and Larsen, M. R. (2010) Selective enrichment of sialic acidcontaining glycopeptides using titanium dioxide chromatography with analysis by HILIC and mass spectrometry. Nat. Protoc. 5, 1974-1982
17. Alpert, A. J., Shukla, M., Shukla, A. K., Zieske, L. R., Yuen, S. W., Ferguson, M. A., Mehlert, A., Pauly, M., and Orlando, R. (1994) Hydrophilic-interaction chromatography of complex carbohydrates. J. Chromatogr. A 676, 191-122
18. Calvano, C. D., Zambonin, C. G., and Jensen, O. N. (2008) Assessment of lectin and HILIC based enrichment protocols for characterization of serum glycoproteins by mass spectrometry. J. Proteomics 71, 304-317
19. Lewandrowski, U., Lohrig, K., Zahedi, R., Walter, D., and Sickmann, A. (2008) Glycosylation site analysis of human platelets by electrostatic repulsion hydrophilic interaction chromatography. Clin. Proteomics 4, 25-36
20. Zhang, H., Guo, T., Li, X., Datta, A., Park, J. E., Yang, J., Lim, S. K., Tam, J. P., and Sze, S. K. (2010) Simultaneous characterization of glyco- and phosphoproteomes of mouse brain membrane proteome with electrostatic repulsion hydrophilic interaction chromatography. Mol. Cell. Proteomics 9, 635-647
21. Bellei, E., Bergamini, S., Monari, E., Fantoni, L. I., Cuoghi, A., Ozben, T., and Tomasi, A. (2011) High-abundance proteins depletion for serum proteomic analysis: concomitant removal of nontargeted proteins. Amino Acids 40, 145-156
22. Cocucci, E., Racchetti, G., and Meldolesi, J. (2009) Shedding microvesicles: artefacts no more. Trends Cell Biol. 19, 43-51
23. van der Pol, E., Boing, A. N., Harrison, P., Sturk, A., and Nieuwland, R. (2012) Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol. Rev. 64, 676-705
24. Simpson, R. J., Lim, J. W. E., Moritz, R. L., and Mathivanan, S. (2009) Exosomes: proteomic insights and diagnostic potential. Exp. Rev. Proteomics 6, 267-283
25. Leroyer, A., Tedgui, A., and Boulanger, C. (2008) Role of microparticles in atherothrombosis. J. Int. Med. 263, 528-537
26. Bala, S., Petrasek, J., Mundkur, S., Catalano, D., Levin, I., Ward, J., Alao, H., Kodys, K., and Szabo, G.(2012) Circulating microRNAs in exosomes indicate hepatocyte injury and inflammation in alcoholic, drug-induced, and inflammatory liver diseases. Hepatology 56, 1946-1957
27. Skog, J., Würdinger, T., Van Rijn, S., Meijer, D. H., Gainche, L., Curry, W. T., Carter, B. S., Krichevsky, A. M., and Breakefield, X. O. (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 10, 1470-1476
28. Choudhuri, K., Llodra, J., Roth, E. W., Tsai, J., Gordo, S., Wucherpfennig, K. W., Kam, L. C., Stokes, D. L., and Dustin, M. L. (2014) Polarized release of T-cell-receptor-enriched microvesicles at the immunological synapse. Nature 507, 118-123
29. Chen, T., Guo, J., Yang, M., Zhu, X., and Cao, X. (2011) Chemokinecontaining exosomes are released from heat-stressed tumor cells via lipid raft-dependent pathway and act as efficient tumor vaccine. J. Immunol. 186, 2219
30. Mittelbrunn, M., Gutierrez-Vazquez, C., Villarroya-Beltri, C., Gonzalez, S., Sanchez-Cabo, F., Gonzalez, M. A., Bernad, A., and Sanchez-Madrid, F. (2011) Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat. Commun. 2, 282
31. Loyer, X., Vion, A. C., Tedgui, A., and Boulanger, C. M. (2014) Microvesicles as cell- cell messengers in cardiovascular diseases. Circ. Res. 114, 345-353
32. Valadi, H., Ekström, K., Bossios, A., Sjöstrand, M., Lee, J. J., and Lötvall, J. O. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654-659
33. Booth, A. M., Fang, Y., Fallon, J. K., Yang, J. M., Hildreth, J. E., and Gould, S. J. (2006) Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane. J. Cell Biol. 172, 923-935
34. Fevrier, B., Vilette, D., Archer, F., Loew, D., Faigle, W., Vidal, M., Laude, H., and Raposo, G. (2004) Cells release prions in association with exosomes. Proc. Natl. Acad. Sci. U.S.A. 101, 9683-9688
35. Bernal-Mizrachi, L., Jy, W., Jimenez, J. J., Pastor, J., Mauro, L. M., Horstman, L. L., de Marchena, E., and Ahn, Y. S. (2003) High levels of circulating endothelial microparticles in patients with acute coronary syndromes. Am. Heart J. 145, 962-970
36. Halkein, J., Tabruyn, S. P., Ricke-Hoch, M., Haghikia, A., Nguyen, N. Q., Scherr, M., Castermans, K., Malvaux, L., Lambert, V., Thiry, M., Sliwa, K., Noel, A., Martial, J. A., Hilfiker-Kleiner, D., and Struman, I. (2013) MicroRNA-146a is a therapeutic target and biomarker for peripartum cardiomyopathy. J. Clin. Invest. 123, 2143-2154
37. Davila, M., Amirkhosravi, A., Coll, E., Desai, H., Robles, L., Colon, J., Baker, C., and Francis, J. (2008) Tissue factor-bearing microparticles derived from tumor cells: impact on coagulation activation. J. Thromb. Haemost. 6, 1517-1524
38. D'Souza-Schorey, C., and Clancy, J. W. (2012) Tumor-derived microvesicles: shedding light on novel microenvironment modulators and prospective cancer biomarkers. Genes Dev. 26, 1287-1299
39. Sabatier, F., Darmon, P., Hugel, B., Combes, V., Sanmarco, M., Velut, J. G., Arnoux, D., Charpiot, P., Freyssinet, J. M., and Oliver, C. (2002) Type 1 and type 2 diabetic patients display different patterns of cellular microparticles. Diabetes 51, 2840-2845
40. Rozmyslowicz, T., Majka, M., Kijowski, J., Murphy, S. L., Conover, D. O., Poncz, M., Ratajczak, J., Gaulton, G. N., and Ratajczak, M. Z. (2003) Platelet-and megakaryocyte-derived microparticles transfer CXCR4 receptor to CXCR4-null cells and make them susceptible to infection by X4-HIV. Aids 17, 33
41. Mack, M., Kleinschmidt, A., Bruhl, H., Klier, C., Nelson, P. J., Cihak, J., Plachy, J., Stangassinger, M., Erfle, V., and Schlondorff, D. (2000) Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: a mechanism for cellular human immunodeficiency virus 1 infection. Nat. Med. 6, 769-775
42. Hao, P., Ren, Y., Alpert, A. J., and Sze, S. K. (2011) Detection, evaluation, and minimization of nonenzymatic deamidation in proteomic sample preparation. Mol. Cell. Proteomics 10, O111 009381
43. Hao, P., Ren, Y., Datta, A., Tam, J. P., and Sze, S. K. (2014) Evaluation of the Effect of Trypsin Digestion Buffers on Artificial Deamidation. Journal of proteome research 14, 1308-1314
44. Zhang, H., Guo, T., Li, X., Datta, A., Park, J. E., Yang, J., Lim, S. K., Tam, J. P., and Sze, S. K. (2010) Simultaneous characterization of glyco-and phosphoproteomes of mouse brain membrane proteome with electrostatic repulsion hydrophilic interaction chromatography. Mol. Cell. Proteomics 9, 635-647
45. Bhatia, V. N., Perlman, D. H., Costello, C. E., and McComb, M. E. (2009) Software tool for researching annotations of proteins: open-source protein annotation software with data visualization. Anal. Chem. 81, 9819-9823
46. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E., Ringwald, M., Rubin, G. M., and Sherlock, G. (2000) Gene Ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29
47. Carbon, S., Ireland, A., Mungall, C. J., Shu, S., Marshall, B., and Lewis, S. (2009) AmiGO: online access to ontology and annotation data. Bioinformatics 25, 288-289
48. Huang da, W., Sherman, B. T., and Lempicki, R. A. (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13
49. Huang da, W., Sherman, B. T., and Lempicki, R. A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57
50. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410
51. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402
52. Ohno, S., Ishikawa, A., and Kuroda, M. (2013) Roles of exosomes and microvesicles in disease pathogenesis. Adv. Drug Deliv. Rev. 65, 398-401
53. Alpert, A. J. (2008) Electrostatic repulsion hydrophilic interaction chromatography for isocratic separation of charged solutes and selective isolation of phosphopeptides. Anal. Chem. 80, 62-76
54. 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
55. Robinson, N. E. (2002) Protein deamidation. Proc. Natl. Acad. Sci. U.S.A. 99, 5283-5288
56. Yang, W., Laeyendecker, O., Wendel, S. K., Zhang, B., Sun, S., Zhou, J.-Y., Ao, M., Moore, R. D., Jackson, J. B., and Zhang, H. (2014) Glycoproteomic study reveals altered plasma proteins associated with HIV elite suppressors. Theranostics 4, 1153
57. Drake, P. M., Schilling, B., Niles, R. K., Braten, M., Johansen, E., Liu, H., Lerch, M., Sorensen, D. J., Li, B., Allen, S., Hall, S. C., Witkowska, H. E., Regnier, F. E., Gibson, B. W., and Fisher, S. J. (2011) A lectin affinity workflow targeting glycosite-specific, cancer-related carbohydrate structures in trypsin-digested human plasma. Anal. Biochem. 408, 71-85
58. Mathivanan, S., Fahner, C. J., Reid, G. E., and Simpson, R. J. (2012) ExoCarta 2012: database of exosomal proteins, RNA, and lipids. Nucleic Acids Res. 40, D1241-D1244
59. Bastos-Amador, P., Royo, F., Gonzalez, E., Conde-Vancells, J., Palomo-Diez, L., Borras, F. E., and Falcon-Perez, J. M. (2012) Proteomic analysis of microvesicles from plasma of healthy donors reveals high individual variability. J. Proteomics 75, 3574-3584
60. Looze, C., Yui, D., Leung, L., Ingham, M., Kaler, M., Yao, X., Wu, W. W., Shen, R.-F., Daniels, M. P., and Levine, S. J. (2009) Proteomic profiling of human plasma exosomes identifies PPARγ as an exosome-associated protein. Biochem. Biophys. Res. Commun. 378, 433-438
61. Caby, M.-P., Lankar, D., Vincendeau-Scherrer, C., Raposo, G., and Bonnerot, C. (2005) Exosomal-like vesicles are present in human blood plasma. Int. Immun. 17, 879-887
62. Hortin, G. L., Sviridov, D., and Anderson, N. L. (2008) High-abundance polypeptides of the human plasma proteome comprising the top four logs of polypeptide abundance. Clin. Chem. 54, 1608-1616
63. Hortin, G. L., and Sviridov, D. (2010) The dynamic range problem in the analysis of the plasma proteome. J. Proteomics 73, 629-636
64. Percy, A. J., Chambers, A. G., Yang, J., and Borchers, C. H. (2013) Multiplexed MRM-based quantitation of candidate cancer biomarker proteins in undepleted and nonenriched human plasma. Proteomics 13, 2202-2215
65. Percy, A. J., Chambers, A. G., Yang, J., Domanski, D., and Borchers, C. H. (2012) Comparison of standard- and nano-flow liquid chromatography platforms for MRM-based quantitation of putative plasma biomarker proteins. Anal. Bioanal. Chem. 404, 1089-1101
66. Hao, P., Ren, Y., Alpert, A. J., and Sze, S. K. (2011) Detection, evaluation, and minimization of nonenzymatic deamidation in proteomic sample preparation. Mol. Cell. Proteomics 10, O111. 009381
67. Nepomuceno, A. I., Gibson, R. J., Randall, S. M., and Muddiman, D. C. (2013) Accurate identification of deamidated peptides in global proteomics using a quadrupole orbitrap mass spectrometer. J. Proteome Res. 13, 777-785
68. Ishikawa, Y., Akishima-Fukasawa, Y., Ito, K., Akasaka, Y., Tanaka, M., Shimokawa, R., Kimura-Matsumoto, M., Morita, H., Sato, S., Kamata, I., and Ishii, T. (2007) Lymphangiogenesis in myocardial remodeling after infarction. Histopathology 51, 345-353
69. Park, J. H., Yoon, J. Y., Ko, S. M., Jin, S. A., Kim, J. H., Cho, C. H., Kim, J. M., Lee, J. H., Choi, S. W., Seong, I. W., and Jeong, J. O. (2011) Endothelial progenitor cell transplantation decreases lymphangiogenesis and adverse myocardial remodeling in a mouse model of acute myocardial infarction. Exp. Mol. Med. 43, 479-485
70. Mayne, J., Starr, A. E., Ning, Z., Chen, R., Chiang, C. K., and Figeys, D. (2014) Fine tuning of proteomic technologies to improve biological findings: advancements in 2011-2013. Anal. Chem. 86, 176-195
71. Percy, A. J., Chambers, A. G., Smith, D. S., and Borchers, C. H. (2013) Standardized protocols for quality control of MRM-based plasma proteomic workflows. J. Proteome Res. 12, 222-233
72. Farrah, T., Deutsch, E. W., Omenn, G. S., Campbell, D. S., Sun, Z., Bletz, J. A., Mallick, P., Katz, J. E., Malmstrom, J., Ossola, R., Watts, J. D., Lin, B., Zhang, H., Moritz, R. L., and Aebersold, R. (2011) A high-confidence human plasma proteome reference set with estimated concentrations in PeptideAtlas. Mol. Cell. Proteomics 10, M110 006353
73. Udby, L., Cowland, J. B., Johnsen, A. H., Sorensen, O. E., Borregaard, N., and Kjeldsen, L. (2002) An ELISA for SGP28/CRISP-3, a cysteine-rich secretory protein in human neutrophils, plasma, and exocrine secretions. J. Immunol. Methods 263, 43-55
74. Nielsen, M. J., Petersen, S. V., Jacobsen, C., Oxvig, C., Rees, D., Moller, H. J., and Moestrup, S. K. (2006) Haptoglobin-related protein is a high-affinity hemoglobin-binding plasma protein. Blood 108, 2846-2849