Delineating diseases by IMS-MS profiling of serum N-linked glycans

Journal of Proteome Research

Volumn 11, Issue 2, 2012, Pages 576-585

  Isailovic, Dragan ^a,d   Plasencia, Manolo D ^a,e   Gaye, Maissa M ^a   Stokes, Sarah T ^a   Kurulugama, Ruwan T ^a,f   Pungpapong, Vitara ^b   Zhang, Min ^b   Kyselova, Zuzana ^a   Goldman, Radoslav ^c   Mechref, Yehia ^a,g   Novotny, Milos V ^a   Clemmer, David E ^a  

^a INDIANA UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^d UNIVERSITY OF TOLEDO   (United States)

^e WASHINGTON UNIVERSITY   (United States)

^f PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^g TEXAS TECH UNIVERSITY   (United States)

Author keywords

cancer; ESI mass spectrometry; glycans; ion mobility; principal component analysis

Indexed keywords

GLYCAN;

ARTICLE; CARBOHYDRATE ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; HUMAN; ION MOBILITY SPECTROMETRY; ISOMER; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; MAJOR CLINICAL STUDY; MASS SPECTROMETRY; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL;

ADOLESCENT; ADULT; COMPUTATIONAL BIOLOGY; GLYCOPROTEINS; HUMANS; LIVER CIRRHOSIS; LIVER NEOPLASMS; POLYSACCHARIDES; PRINCIPAL COMPONENT ANALYSIS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; STATISTICS, NONPARAMETRIC; TANDEM MASS SPECTROMETRY;

EID: 84863048501     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr200777u     Document Type: Article

References (82)

1. Anderson, N. L.; Anderson, N. G. The Human Plasma Proteome History, Character, and Diagnostic Prospects Mol. Cell. Proteomics 2002, 1, 845-867
2. Aebersold, R.; Mann, M. Mass spectrometry-based proteomics Nature 2003, 422, 198-207
3. Giddings, C. Unified separation science; Wiley: New York, 1991.
4. Domon, B.; Aebersold, R. Mass Spectrometry and Protein Analysis Science 2006, 322, 212-217
5. Liu, H.; Lin, D.; Yates, J. R., III Multidimensional separations for protein/peptide analysis in the post-genomic era Biotechniques 2002, 32, 898-911
6. Jacobs, J. M.; Adkins, J. N.; Qian, W. J.; Liu, T.; Shen, Y.; Camp, D. G., II; Smith, R. D. Utilizing Human Blood Plasma for Proteomic Biomarker Discovery J. Proteome Res. 2005, 4, 1073-1085
7. Novotny, M. V.; Mechref, Y. New hyphenated methodologies in high-sensitivity glycoprotein analysis J. Sep. Sci. 2005, 28, 1956-1968
8. Mechref, Y.; Novotny, M. V. Glycomic analysis by capillary electrophoresis-mass spectrometry Mass Spectrom. Rev. 2009, 28, 207-222
9. Valentine, S. J.; Counterman, A. E.; Hoaglund, C. S.; Reilly, J. P.; Clemmer, D. E. Gas-Phase Separations of Protease Digests J. Am. Soc. Mass Spectrom. 1998, 9, 1213-1216
10. Hoaglund, C. S.; Valentine, S. J.; Sporleder, C. R.; Reilly, J. P.; Clemmer, D. E. Three-Dimensional Ion Mobility/TOFMS Analysis of Electrosprayed Biomolecules Anal. Chem. 1998, 70, 2236-2242
11. Gillig, K. J.; Ruotolo, B.; Stone, E. G.; Russell, D. H.; Fuhrer, K.; Gonin, M.; Schultz, A. J. Coupling High-Pressure MALDI with Ion Mobility/Orthogonal Time-of-Flight Mass Spectrometry Anal. Chem. 2000, 72, 3965-3971
12. Thalassinos, K.; Slade, S. E.; Jennings, K. R.; Scrivens, J. H.; Giles, K.; Wildgoose, J.; Hoyes, J.; Bateman, R. H.; Bowers, M. T. Ion Mobility Mass Spectrometry of Proteins in a Modified Commercial Mass Spectrometer Int. J. Mass Spectrom. 2004, 236, 55-63
13. Clowers, B. H.; Dwivedi, P.; Steiner, W. E.; Bendiak Hill, B.; Hill, H. H. Separation of Sodiated Isobaric Disaccharides and Trisaccharides Using Electrospray Ionization-Atmospheric Pressure Ion Mobility-Time of Flight Mass Spectrometry J. Am. Soc. Mass Spectrom. 2005, 16, 660-669
14. Tang, K.; Shvartsburg, A. A.; Lee, H.; Prior, D. C.; Buschbach, M. A.; Li, F.; Tomachev, A.; Anderson, G. A.; Smith, R. D. High-sensitivity ion mobility spectrometry/mass spectrometry using electrodynamic ion funnel interfaces Anal. Chem. 2005, 77, 3330-3339
15. Fenn, L. S.; McLean, J. A. Biomolecular structural separations by ion mobility-mass spectrometry Anal. Bioanal. Chem. 2008, 391, 905-909
16. Fenn, J. B.; Mann, M.; Meng, C. K.; Wong, S. F.; Whitehouse, C. M. Electrospray ionization for mass spectrometry of large biomolecule Science 1989, 246, 64
17. Liu, Y.; Clemmer, D. E. Characterizing Oligosaccharides Using Injected-ion Mobility/Mass Spectrometry Anal. Chem. 1997, 69, 2504-2509
18. Koeniger, S. L.; Merenbloom, S. I.; Valentine, S. J.; Jarrold, M. F.; Udseth, H. R.; Smith, R. D.; Clemmer, D. E. An IMS-MS Analogue of MS-MS Anal. Chem. 2006, 78, 4161-4174
19. Revercomb, H. E.; Mason, E. A. Theory of Plasma Chromatography/Gaseous Electrophoresis - A Review Anal. Chem. 1975, 47, 970-983
20. Shvartsburg, A. A.; Jarrold, M. F. An Exact Hard-Spheres Scattering Model for the Mobilities of Polyatomic Ions Chem. Phys. Lett. 1996, 261, 86-91
21. Mesleh, M. F.; Hunter, J. M.; Shvartsburg, A. A.; Schatz, G. C.; Jarrold, M. F. Structural Information from Ion Mobility Measurements: Effects of the Long-Range Potential J. Phys. Chem. 1996, 100, 16082-16086
22. Wyttenbach, T.; von Helden, G.; Batka, J. J.; Carlat, D.; Bowers, M. T. Effect of the Long-Range Potential on Ion Mobility Measurements J. Am. Soc. Mass Spectrom. 1997, 8, 275-282
23. Bowers, M. T.; Kemper, P. R.; von Helden, G.; Koppen, P. A. M. Gas-Phase Ion Chromatography: Transition Metal State Selection and Carbon Cluster Formation Science 1993, 260, 1446-1451
24. Clemmer, D. E.; Shelimov, K. B.; Jarrold, M. F. Bonding of Metals to Carbon Rings: LaCn+ Isomers with La+ Inserted and Attached to the Ring J. Am. Chem. Soc. 1994, 116, 5971-5972
25. Hunter, J.; Fye, J.; Jarrold, M. F. Annealing C60+: Synthesis of Fullerenes and Large Carbon Rings Science 1993, 260, 784-786
26. Bohrer, B. C.; Merenbloom, S. I.; Koeniger, S. L.; Hilderbrand, A. E.; Clemmer, D. E. Biomolecule Analysis by Ion Mobility Spectrometry Annu. Rev. Anal. Chem. 2008, 1 (10) 1-10
27. Taraszka, J. A.; Counterman, A. E.; Clemmer, D. E. Gas-Phase separations of complex tryptic peptide mixtures Fresenius J. Anal. Chem. 2001, 369, 234-245
28. Valentine, S. J.; Plasencia, M. D.; Liu, X.; Krishnan, M.; Naylor, S.; Udseth, H. R.; Smith, R. D.; Clemmer, D. E. Toward Plasma Proteome Profiling with Ion Mobility-Mass Spectrometry J. Proteome Res. 2006, 5, 2977-2984
29. Dwivedi, P.; Wu, P.; Klopsch, S.; Puzon, G.; Xun, L.; Hill, H. H., Jr. Metabolic profiling by ion mobility mass spectrometry (IMMS) Metabolomics 2008, 4, 63-68
30. Isailovic, D.; Kurulugama, R. T.; Plasencia, M. D.; Stokes, S. T.; Kyselova, Z.; Goldman, R.; Mechref, Y.; Novotny, M. V.; Clemmer, D. E. Profiling of human serum glycans associated with liver cancer and cirrhosis by IMS-MS J. Proteome Res. 2008, 7, 1109-1117
31. Harvey, D. J.; Sobott, F.; Crispin, M.; Wrobel, A.; Bonomelli, C.; Vasiljevic, S.; Scanlan, C. N.; Scarff, C. A.; Thalassinos, K.; Scrivens, J. H. Ion Mobility Mass Spectrometry for Extracting Spectra of N-Glycans Directly from Incubation Mixtures Following Glycan Release: Application to Glycans from Engineered Glycoforms of Intact, Folded HIV gp120 J. Am. Soc. Mass Spectrom. 2011, 22 (3) 568-581
32. Schenauer, M. R.; Meissen, J. K.; Seo, Y.; Ames, J. B.; Leary, J. A. Heparan sulfate separation, sequencing, and isomeric differentiation: ion mobility spectrometry reveals specific iduronic and glucuronic acid-containing hexasaccharides Anal. Chem. 2009, 81 (24) 10179-10185
33. Yamagaki, T.; Sato, A. Peak width-mass correlation in CID MS/MS of isomeric oligosaccharides using traveling-wave ion mobility mass spectrometry J. Mass Spectrom. 2009, 44 (10) 1509-1517
34. Yamagaki, T.; Sato, A. Isomeric oligosaccharides analyses using negative-ion electrospray ionization ion mobility spectrometry combined with collision-induced dissociation MS/MS Anal. Sci. 2009, 25 (8) 985-988
35. Zhu, M.; Bendiak, B.; Clowers, B.; Hill, H. H., Jr. Ion mobility-mass spectrometry analysis of isomeric carbohydrate precursor ions Anal. Bioanal. Chem. 2009, 394 (7) 1853-1867
36. Kang, P.; Madera, M.; William, R.; Alley; Radoslav, G.; Mechref, Y.; Novotny, M. V. Glycomic alterations in the highly-abundant and lesser-abundant blood serum protein fractions for patients diagnosed with hepatocellular carcinoma Int. J. Mass Spectrom. 2011, 305 (2-3) 185-198
37. Cummings, R. D.; Pierce, J. M., Eds. Handbook of Glycomics; Elsevier: Oxford, UK, 2009.
38. Varki, A.; Cummings, R.; Esko, J.; Freeze, H.; Hart, G.; Marth, J., Eds. Essentials of Glycobiology; CSHL Press: Cold Spring Harbor, NY, 1999.
39. Kyselova, Z.; Mechref, Y.; Al Bataineh, M. M.; Dobrolecki, L. E.; Hickey, R. J.; Vinson, J.; Sweeney, C. J.; Novotny, M. V. Alterations in the serum glycome due to metastatic prostate cancer J. Proteome Res. 2007, 6, 1822-1832
40. Saldova, R.; Royle, L.; Radcliffe, C. M.; Abd Hamid, U. M.; Evans, R.; Arnold, J. N.; Banks, R. E.; Hutson, R.; Harvey, D. J.; Antrobus, R.; Petrescu, S. M.; Dwek, R. A.; Rudd, P. M. Ovarian Cancer is Associated with Changes in Glycosylation in Both Acute Phase Proteins and IgG Glycobiology 2007, 17 (12) 1344-1356
41. Goldman, R.; Ressom, H. W.; Varghese, R. S.; Goldman, L.; Bascug, G.; Loffredo, C. A.; Abdel-Hamid, M.; Gouda, I.; Ezzat, S.; Kyselova, Z.; Mechref, Y.; Novotny, M. V. Detection of Hepatocellular Carcinoma using Glycomic Analysis. Clin Cancer Res. 2009, 15, 1808-1813
42. Mechref, Y.; Hussein, A.; Bekesova, S.; Pungpapong, V.; Zhang, M.; Dobrolecki, L. E.; Hickey, R. J.; Hammond, Z. T.; Novotny, M. V. Quantitative Serum Glycomics of Esophageal Adenocarcinoma, and Other Esophageal Disease Onsets J. Proteome Res. 2009, 8, 2656-2666
43. Arnold, J. N.; Saldova, R.; Hamid, U. M. A.; Rudd, P. M. Evaluation of the serum N-linked glycome for the diagnosis of cancer and chronic inflammation Proteomics 2008, 8, 3284-3293
44. Arnold, J. N.; Saldova, R.; Galligan, M. C.; Murphy, T. B.; Mimura-Kimura, Y.; Telford, J. E.; Godwin, A. K.; Rudd, P. M. Novel Glycan Biomarkers for the Detection of Lung Cancer J. Proteome Res. 2011, 10 (4) 1755-1764
45. Robbe-Masselot, C.; Herrmann, A.; Maes, E.; Carlstedt, I.; Michalski, J. C.; Capon, C. Expression of a Core 3 Disialyl-Lex Hexasaccharide in Human Colorectal Cancers: A Potential Marker of Malignant Transformation in Colon J. Proteome Res. 2009, 8, 702-711
46. Kornak, U.; Reynders, E.; Dimopoulou, A.; van Reeuwijk, J.; Fischer, B.; Rajab, A.; Budde, B.; Nürnberg, P.; Foulquier, F.; Lefeber, D.; Urban, Z.; Gruenewald, S.; Annaert, W.; Brunner, H. G.; van Bokhoven, H.; Wevers, R.; Morava, E.; Matthijs, G.; Van Maldergem, L.; Mundlos, S. Impaired glycosylation and cutis laxa caused by mutations in the vesicular H+-ATPase subunit ATP6V0A2 Nat. Genet. 2008, 40, 32-34
47. Kranz, C.; Ng, B. G.; Sun, L. W.; Sharma, V.; Eklund, E. A.; Miura, Y.; Ungar, D.; Lupashin, V.; Winkel, R. D.; Cipollo, J. F.; Costello, C. E.; Loh, E.; Hong, W.; Freeze, H. H. COG8 deficiency causes new congenital disorder of glycosylation type IIh Hum. Mol. Genet. 2007, 16, 731-741
48. An, H. J.; Miyamoto, S.; Lancaster, K. S.; Kirmiz, C.; Li, B. S.; Lam, K. S.; Leiserowitz, G. S.; Lebrilla, C. B. Profiling of glycans in serum for the discovery of potential biomarkers for ovarian cancer J. Proteome Res. 2006, 5, 1626-1635
49. Zhao, J.; Simeone, D. M.; Heidt, D.; Anderson, M. A.; Lubman, D. M. Comparative serum glycoproteomics using lectin selected sialic acid glycoproteins with mass spectrometric analysis: Application to pancreatic cancer serum J. Proteome Res. 2006, 5, 1792-1802
50. Comunale, M. A.; Lowman, M.; Long, R. E.; Krakover, J.; Philip, R.; Seeholzer, S.; Evans, A. A.; Hann, H. W. L.; Block, T. M.; Mehta, A. S. Proteomic analysis of serum associated fucosylated glycoproteins in the development of primary hepatocellular carcinoma J. Proteome Res. 2006, 5, 308-315
51. Steel, L. F.; Mattu, T. S.; Mehta, A.; Hebestreit, H.; Dwek, R.; Evans, A. A.; London, W. T.; Block, T. A proteomic approach for the discovery of early detection markers of hepatocellular carcinoma Disease Markers 2001, 17 (3) 179-189
52. Dai, Z.; Liu, Y. K.; Cui, J. F.; Shen, H. L.; Chen, J.; Sun, R. X.; Zhang, Y.; Zhou, X. W.; Yang, P. Y.; Tang, Z. Y. Identification and analysis of altered alpha 1,6-fucosylated glycoproteins associated with hepatocellular carcinoma metastasis Proteomics 2006, 6, 5857-5867
53. Kyselova, Z.; Mechref, Y.; Kang, P.; Goetz, J. A.; Dobrolecki, L. E.; Hickey, R. J.; Malkas, L. H.; Novotny, M. V. Breast cancer diagnosis and prognosis through quantitative measurements of serum glycan profiles Clin. Chem. 2008, 54, 1166-1175
54. Ressom, H. W.; Varghese, R. S.; Goldman, L.; An, Y.; Loffredo, C. A; Abdel-Hamid, M.; Kyselova, Z.; Mechref, Y.; Novotny, M. V.; Drake, S. K.; Goldman, R. J. Analysis of MALDI-TOF mass spectrometry data for discovery of peptide and glycan biomarkers of hepatocellular carcinoma J. Proteome Res. 2008, 7, 603-610
55. Tousi, F.; Hancock, W. S.; Hincapie, M. S. Technologies and strategies for glycoproteomics and glycomics and their application to clinical biomarker research Anal. Methods 2011, 3 (1) 20-32
56. Beretta, L. Proteomics from the clinical perspective: many hopes and much debate Nat. Methods 2007, 4, 785-786
57. Ezzat, S.; Abdel-Hamid, M.; Eissa, S. A.; Mokhtar, N.; Labib, N. A.; El Ghorory, L.; Mikhail, N. N.; Abdel-Hamid, A.; Hifnawy, T.; Strickland, G. T.; Loffredo, C. A. Associations of Pesticides, HCV, HBV, and Hepatocellular Carcinoma in Egypt Int. J. Hyg. Environ. Health 2005, 208 (5) 329-339
58. Goldman, R.; Ressom, H. W.; Abdel-Hamid, M.; Goldman, L.; Wang, A.; Varghese, R. S.; An, Y.; Loffredo, C. A.; Drake, S. K.; Eissa, S. A.; Gouda, I.; Ezzat, S.; Moiseiwitchs, F. S. Candidate markers for the detection of hepatocellular carcinoma in low-molecular weight fraction of serum Carcinogenesis 2007, 28, 2149-2153
59. Ezzat, S.; Abdel-Hamid, M.; Eissa, S. A.; Mokhtar, N.; Labib, N. A.; El-Ghory, R.; Mikhaill, N. N.; Abdel-Hamid, A.; Hifnay, T.; Strickland, G. T.; Loffredo, C. A. Associations of pesticides, HCV, HBV, and hepatocellular carcinoma in Egypt Int. J. Hyg. Environ. Health 2005, 208, 329-339
60. Kang, P.; Mechref, Y.; Klouckova, I.; Novotny, M. V. Solid-phase permethylation of glycans for mass spectrometric analysis Rapid Commun. Mass Spectrom. 2005, 19, 3421-3428
61. Kang, P.; Mechref, Y.; Novotny, M. V. High-throughput Solid-phase Spin-column Permethylation for MALDI-TOF-MS Analysis Rapid Commun. Mass Spectrom. 2008, 22 (5) 721-734
62. Kurulugama, R. T.; Valentine, S. J.; Sowell, R. A.; Clemmer, D. E. Development of a high-throughput IMS-IMS-MS approach for analyzing mixtures of biomolecules J. Proteomics 2008, 71 (3) 318-331
63. Mason, E. A.; McDaniel, E. W. Transport Properties of Ions in Gases; Wiley: New York, 1988.
64. Clemmer, D. E.; Jarrold, M. F. Ion Mobility Measurements and their Applications to Clusters and Biomolecules J. Mass Spectrom. 1997, 32, 577-592
65. St. Louis, R. H.; Hill, H. H. Ion Mobility Spectrometry in Analytical Chemistry Crit. Rev. Anal. Chem. 1990, 21, 321-355
66. Hoaglund-Hyzer, C. S.; Counterman, A. E.; Clemmer, D. E. Anhydrous Protein Ions Chem. Rev. 1999, 99, 3037-3079
67. Myung, S.; Badman, E. R.; Lee, Y. J.; Clemmer, D. E. Structural Transitions of Electrosprayed Ubiquitin Ions Stored in an Ion Trap over ∼ 10 ms to 30 s J. Phys. Chem. A 2002, 106, 9976-9982
68. Chen, Y. H.; Siems, W. F.; Hill, H. H., Jr. Fourier Transform Electrospray Ion Mobility Spectrometry Anal. Chim. Acta 1996, 334, 75-84
69. Hoaglund-Hyzer, C. S.; Clemmer, D. E. Ion Trap/Ion Mobility/Quadrupole/ Time-of-Flight Mass Spectrometry for Peptide Mixture Analysis Anal. Chem. 2001, 73, 177-184
70. Shaffer, S. A.; Prior, D. C.; Anderson, G. A.; Udseth, H. R.; Smith, R. D. An Ion Funnel Interface for Improved Ion Focusing and Sensitivity Using Electrospray Ionization Mass Spectrometry Anal. Chem. 1998, 70, 4111-4119
71. Valentine, S. J.; Kurulugama, R. T.; Bohrer, B. C.; Merenbloom, S. I.; Sowell, R. A.; Mechref, Y; Clemmer, D. E. Developing IMS-IMS-MS for rapid characterization of abundant proteins in human plasma Int. J. Mass Spectrom. 2009, 283, 149-160
72. Kruskal, W. H.; Wallis, W. A. Use of ranks in one-criterion variance analysis J. Am. Stat. Assoc. 1952, 47, 583-621
73. Benjamini, Y.; Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing J. R. Stat. Soc., Ser B. 1995, 57, 289-300
74. Consortium for functional glycomics and Nature publishing group. (2006, Functional Glycomics Gateway, available at www.functionalglycomics.org
75. Plasencia, M. D.; Isailovic, D.; Merenbloom, S. I.; Mechref, Y.; Clemmer, D. E. Resolving and Assigning N-linked Glycan Structural Isomers from Ovalbumin by IMS-MS J. Am. Soc. Mass Spectrom. 2008, 19 (11) 1706-1715
76. Miller, J. N; Miller, J. C. Statistics and Chemometrics for Analytical Chemistry; Pearson Education Limited: Harlow, England, 2000.
77. Prasad, S; Pierce, K. M.; Schmidt, H.; Rao, J. V.; Guth, R.; Bader, S.; Synovec, R. E.; Smith, G. B.; Eiceman, G. A. Analysis of bacteria by pyrolysis gas chromatography-differential mobility spectrometry and isolation of chemical components with a dependence on growth temperature Analyst 2007, 132, 1031-1039
78. Ivosev, G.; Burton, L; Bonner, R. Dimensionality reduction and visualization in principal component analysis Anal. Chem. 2008, 80, 4933-4944
79. Bereman, M. S.; Young, D. D.; Deiters, A.; Muddiman, D. C. Development of a robust and high throughput method for profiling N-linked glycans derived from plasma glycoproteins by nano LC FT-ICR mass spectrometry J. Proteome Res. 2009, 8, 3764-3770
80. Bereman, M. S.; Williams, T. I.; Muddiman, D. C. 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. 2009, 81 (3) 1130-1136
81. Sowell, R. A.; Koeniger, S. L.; Valentine, S. J.; Moon, M. H.; Clemmer, D. E. Nanoflow LC/IMS-MS (and -CID/MS) of Protein Mixtures J. Am. Soc. Mass Spectrom. 2004, 15, 1341-1353
82. Hua, S.; An, H. J.; Ozcan, S.; Ro, G. S.; Soares, S.; DeVere-White, R.; Lebrilla, C. B. Comprehensive native glycan profiling with isomer separation and quantitation for the discovery of cancer biomarkers Analyst 2011, 136, 3663-3671