DOI QR코드

DOI QR Code

Multi-Level Characterization of Protein Glycosylation

  • Hua, Serenus (Cancer Research Institute, Chungnam National University) ;
  • Oh, Myung Jin (Graduate School of Analytical Science and Technology, Chungnam National University) ;
  • An, Hyun Joo (Cancer Research Institute, Chungnam National University)
  • Received : 2013.03.15
  • Accepted : 2013.03.25
  • Published : 2013.03.29

Abstract

Recent developments in MS-based glycomics and glycoproteomics have rapidly advanced the field and pushed the boundaries of glyco-analysis into new territories. This review will lay out current workflows and strategies for characterization of the glycoproteome, including (in order of increasing complexity and information content) preliminary site mapping, compositional glycan profiling, isomer-specific glycan profiling, glycosite-specific glycopeptide profiling, and finally, glycoproteomic profiling.

Keywords

References

  1. Apweiler, R.; Hermjakob, H.; Sharon, N. Biochimica et Biophysica Acta (BBA) - General Subjects 1999, 1473, 4. https://doi.org/10.1016/S0304-4165(99)00165-8
  2. An, H. J.; Gip, P.; Kim, J.; Wu, S.; Park, K. W.; McVaugh, C. T.; Schaffer, D. V.; Bertozzi, C. R.; Lerbilla, C. B. Molecular & Cellular Proteomics 2012, 11. 1. https://doi.org/10.1074/mcp.E112.019653
  3. Arndt, N. X.; Tiralongo, J.; Madge, P. D.; von Itzstein, M.; Day, C. J., Journal of Cellular Biochemistry 2011, 112, 2230. 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.; Xiao, Z.-C. FEBS Letters 2009, 583, 703. https://doi.org/10.1016/j.febslet.2009.01.013
  5. Dube, S.; Fisher, J. W.; Powell, J. S. Journal of Biological Chemistry 1988, 263, 17516.
  6. Oh, M. J.; Hua, S.; Kim, B. J.; Jeong, H. N.; Jeong, S. H.; Grimm, R.; Yoo, J. S.; An, H. J. Bioanalysis 2013, 5, 545. https://doi.org/10.4155/bio.12.327
  7. Chen, W.; Zhong, Y.; Qin, Y.; Sun, S.; Li, Z. PLoS ONE 2012, 7, pe49224.
  8. Matsuoka, Y.; Swayne, D. E.; Thomas, C.; Rameix-Welti, M.-A.; Naffakh, N.; Warnes, C.; Altholtz, M.; Donis, R.; Subbarao, K. Journal of Virology 2009, 83, 4704. https://doi.org/10.1128/JVI.01987-08
  9. Peracaula, R.; Tabares, G.; Royle, L.; Harvey, D. J.; Dwek, R. A.; Rudd, P. M.; de Llorens, R. Glycobiology 2003, 13, 457. https://doi.org/10.1093/glycob/cwg041
  10. Meany, D. L.; Zhang, Z.; Sokoll, L. J.; Zhang, H.; Chan, D. W. Journal of Proteome Research 2008, 8, 613.
  11. Creaney, J.; Segal, A.; Sterrett, G.; Platten, M. A.; Baker, E.; Murch, A. R.; Nowak, A. K.; Robinson, B. W. S.; Millward, M. J. Br. J. Cancer 2008, 98, 1562. https://doi.org/10.1038/sj.bjc.6604340
  12. An, H. J.; Kronewitter, S. R.; de Leoz, M. L. A.; Lebrilla, C. B. Current Opinion in Chemical Biology 2009, 13, 601. https://doi.org/10.1016/j.cbpa.2009.08.015
  13. Lebrilla, C. B.; An, H. J. Molecular BioSystems 2009, 5, 17. https://doi.org/10.1039/b811781k
  14. Baum, L. G. Immunity 2002, 16, 5. https://doi.org/10.1016/S1074-7613(02)00265-0
  15. Hua, S.; Lebrilla, C.; An, H. J. Bioanalysis 2011, 3, 2573. https://doi.org/10.4155/bio.11.263
  16. Kreunin, P.; Zhao, J.; Rosser, C.; Urquidi, V.; Lubman, D. M.; Goodison, S. Journal of Proteome Research 2007, 6, 2631. https://doi.org/10.1021/pr0700807
  17. 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.; Lubman, D. M. Journal of Proteome Research 2008, 7, 1693. https://doi.org/10.1021/pr700706s
  18. Ahn, Y.; Shin, P.; Ji, E.; Kim, H.; Yoo, J. Analytical and Bioanalytical Chemistry 2012, 402, 2101. https://doi.org/10.1007/s00216-011-5646-3
  19. Miyoshi, E.; Nakano, M. Proteomics 2008, 8, 3257. https://doi.org/10.1002/pmic.200800046
  20. Kurogochi, M.; Amano, M.; Fumoto, M.; Takimoto, A.; Kondo, H.; Nishimura, S.-I. Angewandte Chemie International Edition 2007, 46, 8808. https://doi.org/10.1002/anie.200702919
  21. Zeng, X.; Hood, B. L.; Sun, M.; Conrads, T. P.; Day, R. S.; Weissfeld, J. L.; Siegfried, J. M.; Bigbee, W. L. Journal of Proteome Research 2010, 9, 6440. https://doi.org/10.1021/pr100696n
  22. 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.; Aebersold, R. Molecular & Cellular Proteomics 2005, 4, 144. https://doi.org/10.1074/mcp.M400090-MCP200
  23. Zhang, H.; Li, X.-j.; Martin, D. B.; Aebersold, R. Nat. Biotech. 2003, 21, 660. https://doi.org/10.1038/nbt827
  24. Zhou, Y.; Aebersold, R.; Zhang, H. Analytical Chemistry 2007, 79, 5826. https://doi.org/10.1021/ac0623181
  25. An, H. J.; Froehlich, J. W.; Lebrilla, C. B. Current Opinion in Chemical Biology 2009, 13, 421. https://doi.org/10.1016/j.cbpa.2009.07.022
  26. Nilsson, J.; Ruetschi, U.; Halim, A.; Hesse, C.; Carlsohn, E.; Brinkmalm, G.; Larson, G. Nat. Meth. 2009, 6, 809. https://doi.org/10.1038/nmeth.1392
  27. Whelan, S. A.; Lu, M.; He, J.; Yan, W.; Saxton, R. E.; Faull, K. F.; Whitelegge, J. P.; Chang, H. R. Journal of Proteome Research 2009, 8, 4151. https://doi.org/10.1021/pr900322g
  28. Chaerkady, R.; Thuluvath, P.; Kim, M.-S.; Nalli, A.; Vivekanandan, P.; Simmers, J.; Torbenson, M.; Pandey, A. Clin. Proteom. 2008, 4, 137. https://doi.org/10.1007/s12014-008-9013-0
  29. Zielinska, D. F.; Gnad, F.; Winiewski, J. R.; Mann, M. Cell 2010, 141, 897. https://doi.org/10.1016/j.cell.2010.04.012
  30. Morelle, W.; Faid, V.; Chirat, F.; Michalski, J. C. Methods in molecular biology (Clifton, N.J.) 2009, 534, 5.
  31. Tong, W.; Han, H.; Song, Z.; Ma, C.; Pan, Y.; Zhang, Y.; Qin, W.; Qian, X. Analytical Methods 2012, 4, 3531. https://doi.org/10.1039/c2ay25663k
  32. Royle, L.; Campbell, M. P.; Radcliffe, C. M.; White, D. M.; Harvey, D. J.; Abrahams, J. L.; Kim, Y.-G.; Henry, G. W.; Shadick, N. A.; Weinblatt, M. E.; Lee, D. M.; Rudd, P. M.; Dwek, R. A. Analytical Biochemistry 2008, 376, 1. https://doi.org/10.1016/j.ab.2007.12.012
  33. Hu, Y.; Mechref, Y. Electrophoresis 2012, 33, 1768. https://doi.org/10.1002/elps.201100703
  34. Costello, C. E.; Contado-Miller, J. M.; Cipollo, J. F. Journal of the American Society for Mass Spectrometry 2007, 18, 1799. https://doi.org/10.1016/j.jasms.2007.07.016
  35. Hung, W.-T.; Wang, S.-H.; Chen, Y.-T.; Yu, H.-M.; Chen, C.-H.; Yang, W.-B. Molecules 2012, 17, 4950. https://doi.org/10.3390/molecules17054950
  36. Kronewitter, S. R.; de Leoz, M. L. A.; Peacock, K. S.; McBride, K. R.; An, H. J.; Miyamoto, S.; Leiserowitz, G. S.; Lebrilla, C. B. Journal of Proteome Research 2010, 9, 4952. https://doi.org/10.1021/pr100202a
  37. Harvey, D. J. Journal of Chromatography B 2011, 879, 1196. https://doi.org/10.1016/j.jchromb.2010.11.010
  38. Song, X.; Lasanajak, Y.; Xia, B.; Smith, D. F.; Cummings, R. D. ACS Chemical Biology 2009, 4, 741. https://doi.org/10.1021/cb900067h
  39. Hua, S.; Williams, C. C.; Dimapasoc, L. M.; Ro, G. S.; Ozcan, S.; Miyamoto, S.; Lebrilla, C. B.; An, H. J.; Leiserowitz, G. S. Journal of Chromatography A 2013, 1279, 58. https://doi.org/10.1016/j.chroma.2012.12.079
  40. Wada, Y.; Azadi, P.; Costello, C. E.; Dell, A.; Dwek, R. A.; Geyer, H.; Geyer, R.; Kakehi, K.; Karlsson, N. G.; Kato, K.; Kawasaki, N.; Khoo, K.-H.; Kim, S.; Kondo, A.; Lattova, E.; Mechref, Y.; Miyoshi, E.; Nakamura, K.; Narimatsu, H.; Novotny, M. V.; Packer, N. H.; Perreault, H.; Peter-Katalini, J.; Pohlentz, G.; Reinhold, V. N.; Rudd, P. M.; Suzuki, A.; Taniguchi, N. Glycobiology 2007, 17, 411. https://doi.org/10.1093/glycob/cwl086
  41. Kronewitter, S. R.; De Leoz, M. L. A.; Strum, J. S.; An, H. J.; Dimapasoc, L. M.; Guerrero, A.; Miyamoto, S.; Lebrilla, C. B.; Leiserowitz, G. S. Proteomics 2012, 12, 2523. https://doi.org/10.1002/pmic.201100273
  42. Cooper, C. A.; Gasteiger, E.; Packer, N. H. Proteomics 2001, 1, 340. https://doi.org/10.1002/1615-9861(200102)1:2<340::AID-PROT340>3.0.CO;2-B
  43. von der Lieth, C.-W.; Bohne-Lang, A.; Lohmann, K. K.; Frank, M. Briefings in Bioinformatics 2004, 5, 164. https://doi.org/10.1093/bib/5.2.164
  44. Schachter, H.; Brockhausen, I. Symposia of the Society for Experimental Biology 1989, 43, 1.
  45. Kronewitter, S. R.; An, H. J.; de Leoz, M. L.; Lebrilla, C. B.; Miyamoto, S.; Leiserowitz, G. S. Proteomics 2009, 9, 2986. https://doi.org/10.1002/pmic.200800760
  46. Hua, S.; An, H. J.; Ozcan, S.; Ro, G. S.; Soares, S.; DeVere-White, R.; Lebrilla, C. B. Analyst 2011, 136, 3663. https://doi.org/10.1039/c1an15093f
  47. Zhao, J.; Simeone, D. M.; Heidt, D.; Anderson, M. A.; Lubman, D. M. Journal of Proteome Research 2006, 5, 1792. https://doi.org/10.1021/pr060034r
  48. Reggi, M.; Capon, C.; Gharib, B.; Wieruszeski, J.-M.; Michel, R.; Fournet, B. European Journal of Biochemistry 1995, 230, 503. https://doi.org/10.1111/j.1432-1033.1995.tb20589.x
  49. Bereman, M. S.; Williams, T. I.; Muddiman, D. C. Analytical Chemistry 2008, 81, 1130.
  50. Bones, J.; Mittermayr, S.; O'Donoghue, N.; Guttman, A. s.; Rudd, P. M. Analytical Chemistry 2010, 82, 10208. https://doi.org/10.1021/ac102860w
  51. Ruhaak, L. R.; Miyamoto, S.; Kelly, K.; Lebrilla, C. B. Analytical Chemistry 2011, 84, 396.
  52. Wu, S.; Grimm, R.; German, J. B.; Lebrilla, C. B. Journal of Proteome Research 2010, 10, 856.
  53. Aldredge, D.; An, H. J.; Tang, N.; Waddell, K.; Lebrilla, C. B. Journal of Proteome Research 2012, 11, 1958. https://doi.org/10.1021/pr2011439
  54. Hua, S.; Nwosu, C.; Strum, J.; Seipert, R.; An, H.; Zivkovic, A.; German, J.; Lebrilla, C. Analytical and Bioanalytical Chemistry 2012, 403, 1291. https://doi.org/10.1007/s00216-011-5109-x
  55. Backstrom, M.; Thomsson, K. A.; Karlsson, H.; Hansson, G. C. Journal of Proteome Research 2008, 8, 538.
  56. Tao, N.; Wu, S.; Kim, J.; An, H. J.; Hinde, K.; Power, M. L.; Gagneux, P.; German, J. B.; Lebrilla, C. B. Journal of Proteome Research 2011, 10, 1548. https://doi.org/10.1021/pr1009367
  57. 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.; Wuhrer, M. Molecular & Cellular Proteomics 2012, 11, 571. https://doi.org/10.1074/mcp.M111.011601
  58. Nwosu, C. C.; Aldredge, D. L.; Lee, H.; Lerno, L. A.; Zivkovic, A. M.; German, J. B.; Lebrilla, C. B. Journal of Proteome Research 2012, 11, 2912. https://doi.org/10.1021/pr300008u
  59. Bowden, T. A.; Baruah, K.; Coles, C. H.; Harvey, D. J.; Yu, X.; Song, B.-D.; Stuart, D. I.; Aricescu, A. R.; Scanlan, C. N.; Jones, E. Y.; Crispin, M. Journal of the American Chemical Society 2012, 134, 17554. https://doi.org/10.1021/ja306068g
  60. Ito, H.; Takegawa, Y.; Deguchi, K.; Nagai, S.; Nakagawa, H.; Shinohara, Y.; Nishimura, S.-I. Rapid Communications in Mass Spectrometry 2006, 20, 3557. https://doi.org/10.1002/rcm.2761
  61. Prien, J. M.; Ashline, D. J.; Lapadula, A. J.; Zhang, H.; Reinhold, V. N. Journal of the American Society for Mass Spectrometry 2009, 20, 539. https://doi.org/10.1016/j.jasms.2008.11.012
  62. Zhu, F.; Lee, S.; Valentine, S.; Reilly, J.; Clemmer, D. Journal of the American Society for Mass Spectrometry 2012, 23, 2158. https://doi.org/10.1007/s13361-012-0491-y
  63. Isailovic, D.; Kurulugama, R. T.; Plasencia, M. D.; Stokes, S. T.; Kyselova, Z.; Goldman, R.; Mechref, Y.; Novotny, M. V.; Clemmer, D. E. Journal of Proteome Research 2008, 7, 1109. https://doi.org/10.1021/pr700702r
  64. Harvey, D.; Scarff, C.; Crispin, M.; Scanlan, C.; Bonomelli, C.; Scrivens, J. Journal of the American Society for Mass Spectrometry 2012, 23, 1955. https://doi.org/10.1007/s13361-012-0425-8
  65. Ali, L.; Kenny, D. T.; Hayes, C. A.; Karlsson, N. G. Metabolites 2012, 2, 648. https://doi.org/10.3390/metabo2040648
  66. Robinson, L. N.; Artpradit, C.; Raman, R.; Shriver, Z. H.; Ruchirawat, M.; Sasisekharan, R. Electrophoresis 2012, 33, 797. https://doi.org/10.1002/elps.201100231
  67. Schroeder Jr, H. W.; Cavacini, L. Journal of Allergy and Clinical Immunology 2010, 125, S41. https://doi.org/10.1016/j.jaci.2009.09.046
  68. Neu, U.; Maginnis, M. S.; Palma, A. S.; Stroh, L. J.; Nelson, C. D. S.; Feizi, T.; Atwood, W. J.; Stehle, T. Cell Host & Microbe 2010, 8, 309. https://doi.org/10.1016/j.chom.2010.09.004
  69. Gray, J. S. S.; Yang, B. Y.; Montgomery, R. Carbohydrate Research 1998, 311, 61. https://doi.org/10.1016/S0008-6215(98)00209-2
  70. Alley, W. R.; Mechref, Y.; Novotny, M. V. Rapid Communications in Mass Spectrometry 2009, 23, 495. https://doi.org/10.1002/rcm.3899
  71. Kuo, C.-W.; Wu, I. L.; Hsiao, H.-H.; Khoo, K.-H. Analytical and Bioanalytical Chemistry 2012, 402, 2765. https://doi.org/10.1007/s00216-012-5724-1
  72. Nakano, M.; Nakagawa, T.; Ito, T.; Kitada, T.; Hijioka, T.; Kasahara, A.; Tajiri, M.; Wada, Y.; Taniguchi, N.; Miyoshi, E. International Journal of Cancer 2008, 122, 2301. https://doi.org/10.1002/ijc.23364
  73. Tajiri, M.; Ohyama, C.; Wada, Y.,Glycobiology 2008, 18, 2. https://doi.org/10.1093/glycob/cwm117
  74. Tajiri, M.; Yoshida, S.; Wada, Y. Glycobiology 2005, 15, 1332. https://doi.org/10.1093/glycob/cwj019
  75. Pompach, P.; Chandler, K. B.; Lan, R.; Edwards, N.; Goldman, R. Journal of Proteome Research 2012, 11, 1728. https://doi.org/10.1021/pr201183w
  76. Neue, K.; Mormann, M.; Peter-Katalinic, J.; Pohlentz, G. Journal of Proteome Research 2011, 10, 2248. https://doi.org/10.1021/pr101082c
  77. Froehlich, J. W.; Barboza, M.; Chu, C.; Lerno, L. A.; Clowers, B. H.; Zivkovic, A. M.; German, J. B.; Lebrilla, C. B. Analytical Chemistry 2011, 83, 5541. https://doi.org/10.1021/ac2003888
  78. Nwosu, C. C.; Seipert, R. R.; Strum, J. S.; Hua, S. S.; An, H. J.; Zivkovic, A. M.; German, B. J.; Lebrilla, C. B. Journal of Proteome Research 2011, 10, 2612. https://doi.org/10.1021/pr2001429
  79. Yu, Y. Q.; Fournier, J.; Gilar, M.; Gebler, J. C. Analytical Chemistry 2007, 79, 1731. https://doi.org/10.1021/ac0616052
  80. An, H. J.; Peavy, T. R.; Hedrick, J. L.; Lebrilla, C. B. Analytical Chemistry 2003, 75, 5628. https://doi.org/10.1021/ac034414x
  81. Li, H.; Li, B.; Song, H.; Breydo, L.; Baskakov, I. V.; Wang, L.-X. The Journal of Organic Chemistry 2005, 70, 9990. https://doi.org/10.1021/jo051729z
  82. Liu, X.; McNally, D. J.; Nothaft, H.; Szymanski, C. M.; Brisson, J.-R.; Li, J., Analytical Chemistry 2006, 78, 6081. https://doi.org/10.1021/ac060516m
  83. Dodds, E. D.; Seipert, R. R.; Clowers, B. H.; German, J. B.; Lebrilla, C. B. Journal of Proteome Research 2008, 8, 502.
  84. Clowers, B. H.; Dodds, E. D.; Seipert, R. R.; Lebrilla, C. B. Journal of Proteome Research 2007, 6, 4032. https://doi.org/10.1021/pr070317z
  85. Kim, J. Y.; Kim, S.-K.; Kang, D.; Moon, M. H. Analytical Chemistry 2012, 84, 5343. https://doi.org/10.1021/ac300772w
  86. Schlosser, A.; Vanselow, J. T.; Kramer, A. Analytical Chemistry 2005, 77, 5243. https://doi.org/10.1021/ac050232m
  87. Dallas, D. C.; Martin, W. F.; Hua, S.; German, J. B. Briefings in Bioinformatics 2012. doi:10.1093/bib/bbs045
  88. Seipert, R. R.; Dodds, E. D.; Clowers, B. H.; Beecroft, S. M.; German, J. B.; Lebrilla, C. B. Analytical Chemistry 2008, 80, 3684. https://doi.org/10.1021/ac800067y
  89. Seipert, R. R.; Dodds, E. D.; Lebrilla, C. B. Journal of Proteome Research 2008, 8, 493.
  90. Wuhrer, M.; Koeleman, C. A. M.; Hokke, C. H.; Deelder, A. M. Analytical Chemistry 2004, 77, 886.
  91. Temporini, C.; Perani, E.; Calleri, E.; Dolcini, L.; Lubda, D.; Caccialanza, G.; Massolini, G. Analytical Chemistry 2006, 79, 355.
  92. Tsai, H.-Y.; Boonyapranai, K.; Sriyam, S.; Yu, C.-J.; Wu, S.-W.; Khoo, K.-H.; Phutrakul, S.; Chen, S.-T. Proteomics 2011, 11, 2162. https://doi.org/10.1002/pmic.201000319
  93. Horvatovich, P.; Hoekman, B.; Govorukhina, N.; Bischoff, R. Journal of Separation Science 2010, 33, 1421. https://doi.org/10.1002/jssc.201000050
  94. Sandra, K.; Moshir, M.; D'hondt, F.; Tuytten, R.; Verleysen, K.; Kas, K.; François, I.; Sandra, P. Journal of Chromatography B 2009, 877, 1019. https://doi.org/10.1016/j.jchromb.2009.02.050
  95. Zhang, X.; Fang, A.; Riley, C. P.; Wang, M.; Regnier, F. E.; Buck, C. Analytica Chimica Acta 2010, 664, 101. https://doi.org/10.1016/j.aca.2010.02.001
  96. Nwosu, C. C.; Huang, J.; Aldredge, D. L.; Strum, J. S.; Hua, S.; Seipert, R. R.; Lebrilla, C. B. Analytical Chemistry 2012, 85, 956.

Cited by

  1. Matrix Additives in MALDI-TOF MS Analysis of Glycans vol.37, pp.1, 2016, https://doi.org/10.1002/bkcs.10617
  2. MS Platform for Erythropoietin Glycome Characterization vol.6, pp.3, 2015, https://doi.org/10.5478/MSL.2015.6.3.53
  3. Enhanced Detection of Glycans by MALDI-TOF Mass Spectrometry Using a Binary Matrix of 2,5-Dihydroxybenzoic Acid and 2,6-Dihydroxybenzoic Acid vol.4, pp.2, 2013, https://doi.org/10.5478/MSL.2013.4.1.38