DOI QR코드

DOI QR Code

Glycoscience aids in biomarker discovery

  • Hua, Serenus (Graduate School of Analytical Science and Technology, Chungnam National University) ;
  • An, Hyun-Joo (Graduate School of Analytical Science and Technology, Chungnam National University)
  • Received : 2012.06.15
  • Published : 2012.06.30

Abstract

The glycome consists of all glycans (or carbohydrates) within a biological system, and modulates a wide range of important biological activities, from protein folding to cellular communications. The mining of the glycome for disease markers represents a new paradigm for biomarker discovery; however, this effort is severely complicated by the vast complexity and structural diversity of glycans. This review summarizes recent developments in analytical technology and methodology as applied to the fields of glycomics and glycoproteomics. Mass spectrometric strategies for glycan compositional profiling are described, as are potential refinements which allow structure-specific profiling. Analytical methods that can discern protein glycosylation at a specific site of modification are also discussed in detail. Biomarker discovery applications are shown at each level of analysis, highlighting the key role that glycoscience can play in helping scientists understand disease biology.

Keywords

References

  1. Apweiler, R., Hermjakob, H. and Sharon, N. (1999) On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. BBA-Gen. Subjects 1473, 4-8.
  2. An, H. J., Gip, P., Kim, J., Wu, S., Park, K. W., McVaugh, C. T., Schaffer, D. V., Bertozzi, C. R. and Lerbilla, C. B. (2011) Extensive determination of glycan heterogeneity reveals an unusual abundance of high-mannose glycans in enriched plasma membranes of human embryonic stem cells. Mol. Cell. Proteom. 11, 1-13.
  3. Arndt, N. X., Tiralongo, J., Madge, P. D., von Itzstein, M. and Day, C. J. (2011) Differential carbohydrate binding and cell surface glycosylation of human cancer cell lines. J. Cell. Biochem. 112, 2230-2240. https://doi.org/10.1002/jcb.23139
  4. Li, Y.-L., Wu, G.-Z., Zeng, L., Dawe, G. S., Sun, L., Loers, G., Tilling, T., Cui, S.-S., Schachner, M. and Xiao, Z.-C. (2009) Cell surface sialylation and fucosylation are regulated by the cell recognition molecule L1 via $PLC{\gamma}$ and cooperate to modulate embryonic stem cell survival and proliferation. FEBS Lett. 583, 703-710. https://doi.org/10.1016/j.febslet.2009.01.013
  5. Baum, L. G. (2002) Developing a taste for sweets. Immunity 16, 5-8. https://doi.org/10.1016/S1074-7613(02)00265-0
  6. An, H. J., Kronewitter, S. R., de Leoz, M. L. A. and Lebrilla, C. B. (2009) Glycomics and disease markers. Curr. Opin. Chem. Biol. 13, 601-607. https://doi.org/10.1016/j.cbpa.2009.08.015
  7. Lebrilla, C. B. and An, H. J. (2009) The prospects of glycan biomarkers for the diagnosis of diseases. Mol. BioSyst. 5, 17-20. https://doi.org/10.1039/b811781k
  8. An, H. J., Ninonuevo, M., Aguilan, J., Liu, H., Lebrilla, C. B., Alvarenga, L. S. and Mannis, M. J. (2005) Glycomics analyses of tear fluid for the diagnostic detection of ocular rosacea. J. Protoeme Res. 4, 1981-1987. https://doi.org/10.1021/pr0501620
  9. Vieira, A. C., An, H. J., Ozcan, S., Kim, J.-H., Lebrilla, C. B. and Mannis, M. J. (2012) Glycomic analysis of tear and saliva in ocular rosacea patients: the search for a biomarker. The Ocular Surface. (In press).
  10. Ninonuevo, M. R., Park, Y., Yin, H., Zhang, J., Ward, R. E., Clowers, B. H., German, J. B., Freeman, S. L., Killeen, K., Grimm, R. and Lebrilla, C. B. (2006) A strategy for annotating the human milk glycome. J. Agric. Food Chem. 54, 7471-7480. https://doi.org/10.1021/jf0615810
  11. Barile, D., Tao, N., Lebrilla, C. B., Coisson, J.-D., Arlorio, M. and German, J. B. (2009) Permeate from cheese whey ultrafiltration is a source of milk oligosaccharides. Int. Dairy J. 19, 524-530. https://doi.org/10.1016/j.idairyj.2009.03.008
  12. Tao, N., DePeters, E. J., Freeman, S., German, J. B., Grimm, R. and Lebrilla, C. B. (2008) Bovine milk glycome. J. Dairy Sci. 91, 3768-3778. https://doi.org/10.3168/jds.2008-1305
  13. LoCascio, R. G., Ninonuevo, M. R., Kronewitter, S. R., Freeman, S. L., German, J. B., Lebrilla, C. B. and Mills, D. A. (2009) A versatile and scalable strategy for glycoprofiling bifidobacterial consumption of human milk oligosaccharides. Microb. Biotechnol. 2, 333-342. https://doi.org/10.1111/j.1751-7915.2008.00072.x
  14. de Leoz, M. L. A., Young, L. J. T., An, H. J., Kronewitter, S. R., Kim, J., Miyamoto, S., Borowsky, A. D., Chew, H. K. and Lebrilla, C. B. (2011) High-mannose glycans are elevated during breast cancer progression. Mol. Cell. Proteom. 10, 1-9.
  15. Kronewitter, S. R., de Leoz, M. L. A., Peacock, K. S., McBride, K. R., An, H. J., Miyamoto, S., Leiserowitz, G. S. and Lebrilla, C. B. (2010) Human serum processing and analysis methods for rapid and reproducible N-glycan mass profiling. J. Protoeme Res. 9, 4952-4959. https://doi.org/10.1021/pr100202a
  16. Barkauskas, D. A., An, H. J., Kronewitter, S. R., de Leoz, M. L., Chew, H. K., de Vere White, R. W., Leiserowitz, G. S., Miyamoto, S., Lebrilla, C. B. and Rocke, D. M. (2009) Detecting glycan cancer biomarkers in serum samples using MALDI FT-ICR mass spectrometry data. Bioinformatics 25, 251-257. https://doi.org/10.1093/bioinformatics/btn610
  17. Hua, S., An, H. J., Ozcan, S., Ro, G. S., Soares, S., DeVere-White, R. and Lebrilla, C. B. (2011) Comprehensive native glycan profiling with isomer separation and quantitation for the discovery of cancer biomarkers. Analyst 136, 3663-3671. https://doi.org/10.1039/c1an15093f
  18. Ruhaak, L. R., Miyamoto, S., Kelly, K. and Lebrilla, C. B. (2011) N-glycan profiling of dried blood spots. Anal. Chem. 84, 396-402.
  19. Wu, S., Tao, N., German, J. B., Grimm, R. and Lebrilla, C. B. (2010) Development of an annotated library of neutral human milk oligosaccharides. J. Protoeme Res. 9, 4138-4151. https://doi.org/10.1021/pr100362f
  20. Wu, S., Grimm, R., German, J. B. and Lebrilla, C. B. (2010) Annotation and structural analysis of sialylated human milk oligosaccharides. J. Protoeme Res. 10, 856-868.
  21. Aldredge, D., An, H. J., Tang, N., Waddell, K. and Lebrilla, C. B. (2012) Annotation of a serum n-glycan library for rapid identification of structures. J. Protoeme Res. 11, 1958-1968. https://doi.org/10.1021/pr2011439
  22. Hua, S., Nwosu, C., Strum, J., Seipert, R., An, H., Zivkovic, A., German, J. and Lebrilla, C. (2012) Site-specific protein glycosylation analysis with glycan isomer differentiation. Anal. Bioanal. Chem. 403, 1291-1302. https://doi.org/10.1007/s00216-011-5109-x
  23. Backstroom, M., Thomsson, K. A., Karlsson, H. and Hansson, G. C. (2008) Sensitive liquid chromatographyelectrospray mass spectrometry allows for the analysis of the o-glycosylation of immunoprecipitated proteins from cells or tissues: application to muc1 glycosylation in cancer. J. Protoeme Res. 8, 538-545.
  24. Bereman, M. S., Williams, T. I. and Muddiman, D. C. (2008) Development of a nanolc ltq orbitrap mass spectrometric method for profiling glycans derived from plasma from healthy, benign tumor control and epithelial ovarian cancer patients. Anal. Chem. 81, 1130-1136.
  25. Bones, J., Mittermayr, S., O'Donoghue, N., Guttman, A. S. and Rudd, P. M. (2010) Ultra performance liquid chromatographic profiling of serum n-glycans for fast and efficient identification of cancer associated alterations in glycosylation. Anal. Chem. 82, 10208-10215. https://doi.org/10.1021/ac102860w
  26. An, H. J., Miyamoto, S., Lancaster, K. S., Kirmiz, C., Li, B., Lam, K. S., Leiserowitz, G. S. and Lebrilla, C. B. (2006) Profiling of glycans in serum for the discovery of potential biomarkers for ovarian cancer. J. Protoeme Res. 5, 1626-1635. https://doi.org/10.1021/pr060010k
  27. Kirmiz, C., Li, B., An, H. J., Clowers, B. H., Chew, H. K., Lam, K. S., Ferrige, A., Alecio, R., Borowsky, A. D. and Sulaimon, S. (2007) A serum glycomics approach to breast cancer biomarkers. Mol. Cell. Proteom. 6, 43-55.
  28. Leiserowitz, G. S., Lebrilla, C., Miyamoto, S., An, H. J., Duong, H., Kirmiz, C., Li, B., Liu, H. and Lam, K. S. (2008) Glycomics analysis of serum: a potential new biomarker for ovarian cancer? Int. J. Gynecol. Cancer 18, 470-475. https://doi.org/10.1111/j.1525-1438.2007.01028.x
  29. de Leoz, M. L. A., An, H. J., Kronewitter, S., Kim, J., Beecroft, S., Vinall, R., Miyamoto, S., de Vere White, R., Lam, K. S. and Lebrilla, C. (2008) Glycomic approach for potential biomarkers on prostate cancer: Profiling of N-linked glycans in human sera and pRNS cell lines. Dis. Markers 25, 243-258. https://doi.org/10.1155/2008/515318
  30. Kyselova, Z., Mechref, Y., Al Bataineh, M. M., Dobrolecki, L. E., Hickey, R. J., Vinson, J., Sweeney, C. J. and Novotny, M. V. (2007) Alterations in the serum glycome due to metastatic prostate cancer. J. Protoeme Res. 6, 1822-1832. https://doi.org/10.1021/pr060664t
  31. Mann, B. F., Goetz, J. A., House, M. G., Schmidt, C. M. and Novotny, M. V. (2012) Glycomic and proteomic profiling of pancreatic cyst fluids identifies hyperfucosylated lactosamines on the N-linked glycans of overexpressed glycoproteins. Mol. Cell. Proteom. [Epub ahead of print].
  32. Alley, W. R., Vasseur, J. A., Goetz, J. A., Svoboda, M., Mann, B. F., Matei, D. E., Menning, N., Hussein, A., Mechref, Y. and Novotny, M. V. (2012) N-linked glycan structures and their expressions change in the blood sera of ovarian cancer patients. J. Protoeme Res. 11, 2282-2300. https://doi.org/10.1021/pr201070k
  33. Balog, C. I. A., Stavenhagen, K., Fung, W. L. J., Koeleman, C. A., McDonnell, L. M., Verhoeven, A., Mesker, W. E., Tollenaar, R. A. E. M., Deelder, A. M. and Wuhrer, M. (2012) N-glycosylation of colorectal cancer tissues: a liquid chromatography and mass spectrometry-based investigation. Mol. Cell. Proteom. [Epub ahead of print].
  34. Alley, W. R., Madera, M., Mechref, Y. and Novotny, M. V. (2010) Chip-based reversed-phase liquid chromatographymass spectrometry of permethylated n-linked glycans: a potential methodology for cancer-biomarker discovery. Anal. Chem. 82, 5095-5106. https://doi.org/10.1021/ac100131e
  35. Prater, B. D., Connelly, H. M., Qin, Q. and Cockrill, S. L. (2009) High-throughput immunoglobulin G N-glycan characterization using rapid resolution reverse-phase chromatography tandem mass spectrometry. Anal. Biochem. 385, 69-79. https://doi.org/10.1016/j.ab.2008.10.023
  36. Yu, S.-Y., Chang, L.-Y., Cheng, C.-W., Chou, C.-C., Fukuda, M. and Khoo, K.-H. (2012) Priming mass spectrometry- based sulfoglycomic mapping for identification of terminal sulfated lacdiNAc glycotope. Glycoconj. J. 1-12. [Epub ahead of print].
  37. Kronewitter, S. R., An, H. J., de Leoz, M. L., Lebrilla, C. B., Miyamoto, S. and Leiserowitz, G. S. (2009) The development of retrosynthetic glycan libraries to profile and classify the human serum N-linked glycome. Proteomics 9, 2986-2994. https://doi.org/10.1002/pmic.200800760
  38. Li, B., Russell, S. C., Zhang, J., Hedrick, J. L. and Lebrilla, C. B. (2011) Structure determination by MALDI-IRMPD mass spectrometry and exoglycosidase digestions o O-linked oligosaccharides from Xenopus borealis egg jelly. Glycobiology 21, 877-894. https://doi.org/10.1093/glycob/cwr003
  39. An, H. J. and Lebrilla, C. B. (2011) Structure elucidation of native N- and O-linked glycans by tandem mass spectrometry (tutorial). Mass Spectrom. Rev. 30, 560-578. https://doi.org/10.1002/mas.20283
  40. Lancaster, K. S., An, H. J., Li, B. and Lebrilla, C. B. (2006) Interrogation of N-linked oligosaccharides using infrared multiphoton dissociation in ft-icr mass spectrometry. Anal. Chem. 78, 4990-4997. https://doi.org/10.1021/ac0600656
  41. Ito, H., Takegawa, Y., Deguchi, K., Nagai, S., Nakagawa, H., Shinohara, Y. and Nishimura, S.-I. (2006) Direct structural assignment of neutral and sialylated N-glycans of glycopeptides using collision-induced dissociation MSn spectral matching. Rapid Commun. Mass Sp. 20, 3557-3565. https://doi.org/10.1002/rcm.2761
  42. Zhang, J., Schubothe, K., Li, B., Russell, S. and Lebrilla, C. B. (2004) Infrared multiphoton dissociation of O-linked mucin-type oligosaccharides. Anal. Chem. 77, 208-214.
  43. Zhao, J., Simeone, D. M., Heidt, D., Anderson, M. A. and Lubman, D. M. (2006) Comparative serum glycoproteomics using lectin selected sialic acid glycoproteins with mass spectrometric analysis: application to pancreatic cancer serum. J. Protoeme Res. 5, 1792-1802. https://doi.org/10.1021/pr060034r
  44. De Reggi, M., Capon, C., Gharib, B., Wieruszeski, J.-M., Michel, R. and Fournet, B. (1995) The glycan moiety of human pancreatic lithostathine. Eur. J. Biochem. 230, 503-510. https://doi.org/10.1111/j.1432-1033.1995.tb20589.x
  45. Hua, S., Lebrilla, C. and An, H. J. (2011) Application of nano-LC-based glycomics towards biomarker discovery. Bioanalysis 3, 2573-2585. https://doi.org/10.4155/bio.11.263
  46. Pabst, M., Bondili, J. S., Stadlmann, J., Mach, L. and Altmann, F. (2007) Mass + retention time = structure: a strategy for the analysis of N-glycans by carbon LC-ESI-MS and its application to fibrin N-glycans. Anal. Chem. 79, 5051-5057. https://doi.org/10.1021/ac070363i
  47. Campbell, M. P., Royle, L., Radcliffe, C. M., Dwek, R. A. and Rudd, P. M. (2008) GlycoBase and autoGU: tools for HPLC-based glycan analysis. Bioinformatics 24, 1214-1216. https://doi.org/10.1093/bioinformatics/btn090
  48. Kreunin, P., Zhao, J., Rosser, C., Urquidi, V., Lubman, D. M. and Goodison, S. (2007) Bladder cancer associated glycoprotein signatures revealed by urinary proteomic profiling. J. Protoeme Res. 6, 2631-2639. https://doi.org/10.1021/pr0700807
  49. Qiu, Y., Patwa, T. H., Xu, L., Shedden, K., Misek, D. E., Tuck, M., Jin, G., Ruffin, M. T., Turgeon, D. K., Synal, S., Bresalier, R., Marcon, N., Brenner, D. E. and Lubman, D. M. (2008) Plasma glycoprotein profiling for colorectal cancer biomarker identification by lectin glycoarray and lectin blot. J. Protoeme Res. 7, 1693-1703. https://doi.org/10.1021/pr700706s
  50. Ahn, Y., Shin, P., Ji, E., Kim, H. and Yoo, J. (2012) A lectin- coupled, multiple reaction monitoring based quantitative analysis of human plasma glycoproteins by mass spectrometry. Anal. Bioanal. Chem. 402, 2101-2112. https://doi.org/10.1007/s00216-011-5646-3
  51. Miyoshi, E. and Nakano, M. (2008) Fucosylated haptoglobin is a novel marker for pancreatic cancer: detailed analyses of oligosaccharide structures. Proteomics 8, 3257-3262. https://doi.org/10.1002/pmic.200800046
  52. Kurogochi, M., Amano, M., Fumoto, M., Takimoto, A., Kondo, H. and Nishimura, S.-I. (2007) Reverse glycoblotting allows rapid-enrichment glycoproteomics of biopharmaceuticals and disease-related biomarkers. Angew. Chem. Int. Ed. 46, 8808-8813. https://doi.org/10.1002/anie.200702919
  53. 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. Protoeme Res. 9, 6440-6449. https://doi.org/10.1021/pr100696n
  54. Zhang, H., Yi, E. C., Li, X.-J., Mallick, P., Kelly-Spratt, K. S., Masselon, C. D., Camp, D. G., Smith, R. D., Kemp, C. J. and Aebersold, R. (2005) High throughput quantitative analysis of serum proteins using glycopeptide capture and liquid chromatography mass spectrometry. Mol. Cell. Proteom. 4, 144-155. https://doi.org/10.1074/mcp.M400090-MCP200
  55. 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. Biotech. 21, 660-666. https://doi.org/10.1038/nbt827
  56. Zhou, Y., Aebersold, R. and Zhang, H. (2007) Isolation of N-linked glycopeptides from plasma. Anal. Chem. 79, 5826-5837. https://doi.org/10.1021/ac0623181
  57. Tsai, H.-Y., Boonyapranai, K., Sriyam, S., Yu, C.-J., Wu, S.-W., Khoo, K.-H., Phutrakul, S. and Chen, S.-T. (2011) Glycoproteomics analysis to identify a glycoform on haptoglobin associated with lung cancer. Proteomics 11, 2162-2170. https://doi.org/10.1002/pmic.201000319
  58. Dallas, D. C., Martin, W. F., Strum, J. S., Zivkovic, A. M., Smilowitz, J. T., Underwood, M. A., Affolter, M., Lebrilla, C. B. and German, J. B. (2011) N-linked glycan profiling of mature human milk by high-performance microfluidic chip liquid chromatography time-of-flight tandem mass spectrometry. J. Agric. Food Chem. 59, 4255-4263. https://doi.org/10.1021/jf104681p
  59. Alley, W. R., Mechref, Y. and Novotny, M. V. (2009) Use of activated graphitized carbon chips for liquid chromatography/ mass spectrometric and tandem mass spectrometric analysis of tryptic glycopeptides. Rapid Commun. Mass Sp. 23, 495-505. https://doi.org/10.1002/rcm.3899
  60. White, K. Y., Rodemich, L., Nyalwidhe, J. O., Comunale, M. A., Clements, M. A., Lance, R. S., Schellhammer, P. F., Mehta, A. S., Semmes, O. J. and Drake, R. R. (2009) Glycomic characterization of prostate-specific antigen and prostatic acid phosphatase in prostate cancer and benign disease seminal plasma fluids. J. Protoeme Res. 8, 620-630. https://doi.org/10.1021/pr8007545
  61. Kuo, C.-W., Wu, I. L., Hsiao, H.-H. and Khoo, K.-H. (2012) Rapid glycopeptide enrichment and N-glycosylation site mapping strategies based on amine-functionalized magnetic nanoparticles. Anal. Bioanal. Chem. 402, 2765-2776. https://doi.org/10.1007/s00216-012-5724-1
  62. Gray, J. S. S., Yang, B. Y. and Montgomery, R. (1998) Heterogeneity of glycans at each N-glycosylation site of horseradish peroxidase. Carbohydr. Res. 311, 61-69. https://doi.org/10.1016/S0008-6215(98)00209-2
  63. Nakano, M., Nakagawa, T., Ito, T., Kitada, T., Hijioka, T., Kasahara, A., Tajiri, M., Wada, Y., Taniguchi, N. and Miyoshi, E. (2008) Site-specific analysis of N-glycans on haptoglobin in sera of patients with pancreatic cancer: A novel approach for the development of tumor markers. Int. J. Cancer 122, 2301-2309. https://doi.org/10.1002/ijc.23364
  64. Wu, Z. L., Ethen, C., Hickey, G. E. and Jiang, W. (2009) Active 1918 pandemic flu viral neuraminidase has distinct N-glycan profile and is resistant to trypsin digestion. Biochem. Biophys. Res. Commun. 379, 749-753. https://doi.org/10.1016/j.bbrc.2008.12.139
  65. Fujihara, J., Yasuda, T., Kunito, T., Fujii, Y., Takatsuka, H., Moritani, T. and Takeshita, H. (2008) Two N-linked glycosylation sites (Asn18 and Asn106) are both required for full enzymatic activity, thermal stability and resistance to proteolysis in mammalian deoxyribonuclease i. Biosci. Biote chnol. Biochem. 72, 3197-3205. https://doi.org/10.1271/bbb.80376
  66. Pompach, P., Chandler, K. B., Lan, R., Edwards, N. and Goldman, R. (2012) Semi-automated identification of n-glycopeptides by hydrophilic interaction chromatography, nano-reverse-phase lc-ms/ms and glycan database search. J. Protoeme Res. 11, 1728-1740. https://doi.org/10.1021/pr201183w
  67. Tajiri, M., Ohyama, C. and Wada, Y. (2008) Oligosaccharide profiles of the prostate specific antigen in free and complexed forms from the prostate cancer patient serum and in seminal plasma: a glycopeptide approach. Glycobiology 18, 2-8. https://doi.org/10.1093/glycob/cwm117
  68. Tajiri, M., Yoshida, S. and Wada, Y. (2005) Differential analysis of site-specific glycans on plasma and cellular fibronectins: application of a hydrophilic affinity method for glycopeptide enrichment, Glycobiology 15, 1332-1340. https://doi.org/10.1093/glycob/cwj019
  69. Neue, K., Mormann, M., Peter-Katalinić, J. and Pohlentz, G. (2011) Elucidation of glycoprotein structures by unspecific proteolysis and direct nanoESI mass spectrometric analysis of ZIC-HILIC-enriched glycopeptides. J. Protoeme Res. 10, 2248-2260. https://doi.org/10.1021/pr101082c
  70. Larsen, M. R., Højrup, P. and Roepstorff, P. (2005) Characterization of gel-separated glycoproteins using two-step proteolytic digestion combined with sequential microcolumns and mass spectrometry. Mol. Cell. Proteom. 4, 107-119. https://doi.org/10.1074/mcp.M400068-MCP200
  71. Xin, L., Zhang, H., Liu, H. and Li, Z. (2012) Equal ratio of graphite carbon to activated charcoal for enrichment of N-glycopeptides prior to matrix-assisted laser desorption/ ionization time-of-flight mass spectrometric identification. Rapid Commun. Mass Sp. 26, 269-274. https://doi.org/10.1002/rcm.5327
  72. Thaysen-Andersen, M., Mysling, S. and Højrup, P. (2009) Site-specific glycoprofiling of N-Linked glycopeptides using MALDI-TOF MS: strong correlation between signal strength and glycoform quantities. Anal. Chem. 81, 3933-3943. https://doi.org/10.1021/ac900231w
  73. Zauner, G., Koeleman, C. A. M., 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. https://doi.org/10.1002/jssc.200900850
  74. Yu, Y. Q., Fournier, J., Gilar, M. and Gebler, J. C. (2007) Identification of N-linked glycosylation sites using glycoprotein digestion with pronase prior to MALDI tandem time-of-flight mass spectrometry. Anal. Chem. 79, 1731- 1738. https://doi.org/10.1021/ac0616052
  75. An, H. J., Froehlich, J. W. and Lebrilla, C. B. (2009) Determination of glycosylation sites and site-specific heterogeneity in glycoproteins. Curr. Opin. Chem. Biol. 13, 421-426. https://doi.org/10.1016/j.cbpa.2009.07.022
  76. 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. https://doi.org/10.1021/ac034414x
  77. Li, H., Li, B., Song, H., Breydo, L., Baskakov, I. V. and Wang, L.-X. (2005) Chemoenzymatic synthesis of HIV-1 V3 glycopeptides carrying two N-glycans and effects of glycosylation on the peptide domain. J. Org. Chem. 70, 9990-9996. https://doi.org/10.1021/jo051729z
  78. Liu, X., McNally, D. J., Nothaft, H., Szymanski, C. M., Brisson, J.-R. and Li, J. (2006) Mass spectrometry-based glycomics strategy for exploring N-linked glycosylation in eukaryotes and bacteria, Anal. Chem. 78, 6081-6087. https://doi.org/10.1021/ac060516m
  79. Dodds, E. D., Seipert, R. R., Clowers, B. H., German, J. B. and Lebrilla, C. B. (2008) Analytical performance of immobilized pronase for glycopeptide footprinting and implications for surpassing reductionist glycoproteomics. J. Protoeme Res. 8, 502-512.
  80. Clowers, B. H., Dodds, E. D., Seipert, R. R. and Lebrilla, C. B. (2007) Site determination of protein glycosylation based on digestion with immobilized nonspecific proteases and fourier transform ion cyclotron resonance mass spectrometry. J. Protoeme Res. 6, 4032-4040. https://doi.org/10.1021/pr070317z
  81. An, H. J., Tillinghast, J. S., Woodruff, D. L., Rocke, D. M. and Lebrilla, C. B. (2006) A new computer program (GlycoX) to determine simultaneously the glycosylation sites and oligosaccharide heterogeneity of glycoproteins. J. Protoeme Res. 5, 2800-2808. https://doi.org/10.1021/pr0602949
  82. Seipert, R. R., Dodds, E. D., Clowers, B. H., Beecroft, S. M., German, J. B. and Lebrilla, C. B. (2008) Factors that influence fragmentation behavior of N-linked glycopeptide ions. Anal. Chem. 80, 3684-3692. https://doi.org/10.1021/ac800067y
  83. Seipert, R. R., Dodds, E. D. and Lebrilla, C. B. (2008) Exploiting differential dissociation chemistries of o-linked glycopeptide ions for the localization of mucin-type protein glycosylation. J. Protoeme Res. 8, 493-501.
  84. Wuhrer, M., Koeleman, C. A. M., Hokke, C. H. and Deelder, A. M. (2004) Protein glycosylation analyzed by normal-phase nano-liquid chromatography-mass spectrometry of glycopeptides. Anal. Chem. 77, 886-894.
  85. Temporini, C., Perani, E., Calleri, E., Dolcini, L., Lubda, D., Caccialanza, G. and Massolini, G. (2006) Pronase-immobilized enzyme reactor: an approach for automation in glycoprotein analysis by LC/LC-ESI/MSn. Anal. Chem. 79, 355-363.
  86. Tang, Z., Varghese, R. S., Bekesova, S., Loffredo, C. A., Hamid, M. A., Kyselova, Z., Mechref, Y., Novotny, M. V., Goldman, R. and Ressom, H. W. (2009) Identification of N-glycan serum markers associated with hepatocellular carcinoma from mass spectrometry data. J. Protoeme Res. 9, 104-112.
  87. Froehlich, J. W., Barboza, M., Chu, C., Lerno, L. A., Clowers, B. H., Zivkovic, A. M., German, J. B. and Lebrilla, C. B. (2011) Nano-LC-MS/MS of glycopeptides produced by nonspecific proteolysis enables rapid and extensive site-specific glycosylation determination. Anal. Chem. 83, 5541-5547. https://doi.org/10.1021/ac2003888
  88. Thaysen-Andersen, M., Thogersen, I. B., Lademann, U., Offenberg, H., Giessing, A. M. B., Enghild, J. J., Nielsen, H. J., Brunner, N. and Hojrup, P. (2008) Investigating the biomarker potential of glycoproteins using comparative glycoprofiling-application to tissue inhibitor of metalloproteinases- 1, Biochimica et Biophysica Acta (BBA) - Proteins &. Proteomics 1784, 455-463.

Cited by

  1. Glyco-Analytical Multispecific Proteolysis (Glyco-AMP): A Simple Method for Detailed and Quantitative Glycoproteomic Characterization vol.12, pp.10, 2013, https://doi.org/10.1021/pr400442y
  2. Antibody approaches to prepare clinically transplantable cells from human embryonic stem cells: Identification of human embryonic stem cell surface markers by monoclonal antibodies vol.9, pp.7, 2014, https://doi.org/10.1002/biot.201300495
  3. Glycocapture-based proteomics for secretome analysis vol.13, pp.3-4, 2013, https://doi.org/10.1002/pmic.201200414
  4. Carbohydrate restriction in the larval diet causes oxidative stress in adult insects of Drosophila melanogaster vol.85, pp.6, 2013, https://doi.org/10.15407/ubj85.05.061
  5. Analytical platform for glycomic characterization of recombinant erythropoietin biotherapeutics and biosimilars by MS vol.5, pp.5, 2013, https://doi.org/10.4155/bio.12.327
  6. Glycoproteomic analysis identifies human glycoproteins secreted from HIV latently infected T cells and reveals their presence in HIV+ plasma vol.11, pp.1, 2014, https://doi.org/10.1186/1559-0275-11-9
  7. Technologies for glycomic characterization of biopharmaceutical erythropoietins vol.68, 2015, https://doi.org/10.1016/j.trac.2015.02.004
  8. Open tubular capillary electrochromatography with anN-phenylacrylamide-styrene copolymer-based stationary phase for the separation of anomers of glucose and structural isomers of maltotriose vol.38, pp.10, 2015, https://doi.org/10.1002/jssc.201401356
  9. Validation of N-glycan markers that improve the performance of CA19-9 in pancreatic cancer vol.17, pp.1, 2017, https://doi.org/10.1007/s10238-015-0401-2
  10. Measurement of Glycosylated Alpha-Fetoprotein Improves Diagnostic Power over the Native Form in Hepatocellular Carcinoma vol.9, pp.10, 2014, https://doi.org/10.1371/journal.pone.0110366
  11. Analysis of carbohydrates and glycoconjugates by matrix-assisted laser desorption/ionization mass spectrometry: An update for 2011-2012 vol.36, pp.3, 2017, https://doi.org/10.1002/mas.21471
  12. Isomer-Specific LC/MS and LC/MS/MS Profiling of the Mouse Serum N-Glycome Revealing a Number of Novel Sialylated N-Glycans vol.85, pp.9, 2013, https://doi.org/10.1021/ac400195h
  13. Comparison of fluorescent tags for analysis of mannose-6-phosphate glycans vol.501, 2016, https://doi.org/10.1016/j.ab.2016.02.004
  14. Automated Assignments of N- and O-Site Specific Glycosylation with Extensive Glycan Heterogeneity of Glycoprotein Mixtures vol.85, pp.12, 2013, https://doi.org/10.1021/ac4006556
  15. The sweet and sour of serological glycoprotein tumor biomarker quantification vol.11, pp.1, 2013, https://doi.org/10.1186/1741-7015-11-31
  16. Glycomic profiling of targeted serum haptoglobin for gastric cancer using nano LC/MS and LC/MS/MS vol.12, pp.12, 2016, https://doi.org/10.1039/C6MB00559D
  17. Systems Glycobiology: Integrating Glycogenomics, Glycoproteomics, Glycomics, and Other ‘Omics Data Sets to Characterize Cellular Glycosylation Processes vol.428, pp.16, 2016, https://doi.org/10.1016/j.jmb.2016.07.005
  18. Isomer-specific chromatographic profiling yields highly sensitive and specific potential N-glycan biomarkers for epithelial ovarian cancer vol.1279, 2013, https://doi.org/10.1016/j.chroma.2012.12.079
  19. Designation of fingerprint glycopeptides for targeted glycoproteomic analysis of serum haptoglobin: insights into gastric cancer biomarker discovery vol.410, pp.6, 2018, https://doi.org/10.1007/s00216-017-0811-y
  20. Do fragments and glycosylated isoforms of alpha-1-antitrypsin in CSF mirror spinal pathophysiological mechanisms in chronic peripheral neuropathic pain? An exploratory, discovery phase study vol.18, pp.1, 2018, https://doi.org/10.1186/s12883-018-1116-2