Identifying N-Glycan Biomarkers in Colorectal Cancer by Mass Spectrometry

Accounts of Chemical Research

Volumn 49, Issue 10, 2016, Pages 2099-2106

  Sethi, Manveen K ^a   Hancock, William S ^a,b   Fanayan, Susan ^a  

^a MACQUARIE UNIVERSITY   (Australia)

^b NORTHEASTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLYSACCHARIDE; TUMOR MARKER;

COLORECTAL TUMOR; HUMAN; MASS SPECTROMETRY;

BIOMARKERS, TUMOR; COLORECTAL NEOPLASMS; HUMANS; MASS SPECTROMETRY; POLYSACCHARIDES;

EID: 84991772201     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/acs.accounts.6b00193     Document Type: Article

References (87)

1. Ferlay, J.; Soerjomataram, I.; Dikshit, R.; Eser, S.; Mathers, C.; Rebelo, M.; Parkin, D. M.; Forman, D.; Bray, F. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012 Int. J. Cancer 2015, 136, E359-386 10.1002/ijc.29210
2. White, V.; Miller, R. Colorectal cancer: prevention and early diagnosis Medicine 2007, 35, 297-301 10.1016/j.mpmed.2007.03.001
3. Etzioni, R.; Urban, N.; Ramsey, S.; McIntosh, M.; Schwartz, S.; Reid, B.; Radich, J.; Anderson, G.; Hartwell, L. The case for early detection Nat. Rev. Cancer 2003, 3, 243-252 10.1038/nrc1041
4. Davies, R. J.; Miller, R.; Coleman, N. Colorectal cancer screening: Prospects for molecular stool analysis Nat. Rev. Cancer 2005, 5, 199-209 10.1038/nrc1569
5. Levin, T. R.; Zhao, W.; Conell, C.; Seeff, L. C.; Manninen, D. L.; Shapiro, J. A.; Schulman, J. Complications of colonoscopy in an integrated health care delivery system Ann. Intern. Med. 2006, 145, 880-886 10.7326/0003-4819-145-12-200612190-00004
6. Tanaka, T.; Tanaka, M.; Tanaka, T.; Ishigamori, R. Biomarkers for colorectal cancer Int. J. Mol. Sci. 2010, 11, 3209-3225 10.3390/ijms11093209
7. Gold, P.; Freedman, S. O. Specific carcinoembryonic antigens of the human digestive system J. Exp. Med. 1965, 122, 467-481 10.1084/jem.122.3.467
8. Duffy, M. J.; O'Sullivan, F.; O'Donoghue, D.; Afdhal, N. H.; Kelleher, D. Ca-19-9, a new marker for gastrointestinal malignancy Ir. J. Med. Sci. 1985, 154, 385-386 10.1007/BF02937186
9. Kuusela, P.; Haglund, C.; Roberts, P. J. Comparison of a new tumour marker CA 242 with CA 19-9, CA 50 and carcinoembryonic antigen (CEA) in digestive tract diseases Br. J. Cancer 1991, 63, 636-640 10.1038/bjc.1991.146
10. Hakomori, S. Aberrant glycosylation in tumours and tumour-associated carbohydrate antigens Adv. Cancer Res. 1989, 52, 257-331 10.1016/S0065-230X(08)60215-8
11. Brooks, S. A.; Carter, T. M.; Royle, L.; Harvey, D. J.; Fry, S. A.; Kinch, C.; Dwek, R. A.; Rudd, P. M. Altered glycosylation of proteins in cancer: What is the potential for new anti-tumour strategies Anti-Cancer Agents Med. Chem. 2008, 8, 2-21 10.2174/187152008783330860
12. 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. Plasma glycoprotein profiling for colorectal cancer biomarker identification by lectin glycoarray and lectin blot J. Proteome Res. 2008, 7, 1693-1703 10.1021/pr700706s
13. Drake, P. M.; Cho, W.; Li, B.; Prakobphol, A.; Johansen, E.; Anderson, N. L.; Regnier, F. E.; Gibson, B. W.; Fisher, S. J. Sweetening the pot: adding glycosylation to the biomarker discovery equation Clin. Chem. 2010, 56, 223-236 10.1373/clinchem.2009.136333
14. Sethi, M. K.; Fanayan, S. Mass spectrometry-based N-glycomics of colorectal cancer Int. J. Mol. Sci. 2015, 16, 29278-29304 10.3390/ijms161226165
15. Kannagi, R.; Sakuma, K.; Cai, B. H.; Yu, S. Y. Tumor-associated glycans and their functional roles in the multistep process of human cancer progression. In Sugar Chains; Suzuki, T.; Ohtsubo, K.; Taniguchi, N., Eds.; Springer: Tokyo, Japan, 2015; pp 139-158.
16. Glavey, S. V.; Huynh, D.; Reagan, M. R.; Manier, S.; Moschetta, M.; Kawano, Y.; Roccaro, A. M.; Ghobrial, I. M.; Joshi, L.; O'Dwyer, M. E. The cancer glycome: Carbohydrates as mediators of metastasis Blood Rev. 2015, 29, 269-279 10.1016/j.blre.2015.01.003
17. Watson, M. E.; Diepeveen, L. A.; Stubbs, K. A.; Yeoh, G. C. Glycosylation-related diagnostic and therapeutic drug target markers in hepatocellular carcinoma J. Gastrointest. Liver Dis. 2015, 24, 349-357 10.15403/jgld.2014.1121.243.mew
18. Wang, D.; Liu, X.; Hsieh, B.; Bruce, R.; Somlo, G.; Huang, J.; Sambucetti, L. Exploring glycan markers for immunotyping and precision-targeting of breast circulating tumor cells Arch. Med. Res. 2015, 46, 642-650 10.1016/j.arcmed.2015.11.007
19. Zhao, Y. P.; Zhou, P. T.; Ji, W. P.; Wang, H.; Fang, M.; Wang, M. M.; Yin, Y. P.; Jin, G.; Gao, C. F. Validation of N-glycan markers that improve the performance of CA19-9 in pancreatic cancer Clin. Exp. Med. 2015, 10.1007/s10238-015-0401-2
20. Apweiler, R.; Hermjakob, H.; Sharon, N. On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database Biochim. Biophys. Acta, Gen. Subj. 1999, 1473, 4-8 10.1016/S0304-4165(99)00165-8
21. Varki, A. Biological roles of oligosaccharides: all of the theories are correct Glycobiology 1993, 3, 97-130 10.1093/glycob/3.2.97
22. Mathias, R. A.; Chen, Y. S.; Kapp, E. A.; Greening, D. W.; Mathivanan, S.; Simpson, R. J. Triton X-114 phase separation in the isolation and purification of mouse liver microsomal membrane proteins Methods 2011, 54, 396-406 10.1016/j.ymeth.2011.01.006
23. Jensen, P. H.; Karlsson, N. G.; Kolarich, D.; Packer, N. H. Structural analysis of N- and O-glycans released from glycoproteins Nat. Protoc. 2012, 7, 1299-1310 10.1038/nprot.2012.063
24. Mechref, Y.; Novotny, M. V. Structural investigations of glycoconjugates at high sensitivity Chem. Rev. 2002, 102, 321-369 10.1021/cr0103017
25. Maley, F.; Trimble, R. B.; Tarentino, A. L.; Plummer, T. H., Jr. Characterization of glycoproteins and their associated oligosaccharides through the use of endoglycosidases Anal. Biochem. 1989, 180, 195-204 10.1016/0003-2697(89)90115-2
26. Hagan, A. K.; Wang, M.; Liu, L. Current approaches to glycoprotein analysis Protein Pept. Lett. 2014, 21, 986-999 10.2174/0929866521666140626095752
27. Alvarez-Manilla, G.; Warren, N. L.; Abney, T.; Atwood, J., 3rd.; Azadi, P.; York, W. S.; Pierce, M.; Orlando, R. Tools for glycomics: relative quantitation of glycans by isotopic permethylation using 13CH3I Glycobiology 2007, 17, 677-687 10.1093/glycob/cwm033
28. Wuhrer, M.; Deelder, A. M.; Hokke, C. H. Protein glycosylation analysis by liquid chromatography-mass spectrometry J. Chromatogr. B: Anal. Technol. Biomed. Life Sci. 2005, 825, 124-133 10.1016/j.jchromb.2005.01.030
29. Chen, X.; Flynn, G. C. Analysis of N-glycans from recombinant immunoglobulin G by on-line reversed-phase high-performance liquid chromatography/mass spectrometry Anal. Biochem. 2007, 370, 147-161 10.1016/j.ab.2007.08.012
30. Wuhrer, M.; Koeleman, C. A.; Deelder, A. M. Two-dimensional HPLC separation with reverse-phase-nano-LC-MS/MS for the characterization of glycan pools after labeling with 2-aminobenzamide Methods Mol. Biol. 2009, 534, 79-91 10.1007/978-1-59745-022-5-6
31. Wuhrer, M.; de Boer, A. R.; Deelder, A. M. Structural glycomics using hydrophilic interaction chromatography (HILIC) with mass spectrometry Mass Spectrom. Rev. 2009, 28, 192-206 10.1002/mas.20195
32. Zauner, G.; Deelder, A. M.; Wuhrer, M. Recent advances in hydrophilic interaction liquid chromatography (HILIC) for structural glycomics Electrophoresis 2011, 32, 3456-3466 10.1002/elps.201100247
33. Rohrer, J. S.; Thayer, J.; Weitzhandler, M.; Avdalovic, N. Analysis of the N-acetylneuraminic acid and N-glycolylneuraminic acid contents of glycoproteins by high-pH anion-exchange chromatography with pulsed amperometric detection Glycobiology 1998, 8, 35-43 10.1093/glycob/8.1.35
34. Ruhaak, L. R.; Deelder, A. M.; Wuhrer, M. Oligosaccharide analysis by graphitized carbon liquid chromatography-mass spectrometry Anal. Bioanal. Chem. 2009, 394, 163-174 10.1007/s00216-009-2664-5
35. Stavenhagen, K.; Kolarich, D.; Wuhrer, M. Clinical glycomics employing graphitized carbon liquid chromatography-mass spectrometry Chromatographia 2015, 78, 307-320 10.1007/s10337-014-2813-7
36. Everest-Dass, A. V.; Jin, D.; Thaysen-Andersen, M.; Nevalainen, H.; Kolarich, D.; Packer, N. H. Comparative structural analysis of the glycosylation of salivary and buccal cell proteins: innate protection against infection by Candida albicans Glycobiology 2012, 22, 1465-1479 10.1093/glycob/cws112
37. Pabst, M.; Grass, J.; Toegel, S.; Liebminger, E.; Strasser, R.; Altmann, F. Isomeric analysis of oligomannosidic N-glycans and their dolichol-linked precursors Glycobiology 2012, 22, 389-399 10.1093/glycob/cwr138
38. Abrahams, J. L.; Packer, N. H.; Campbell, M. P. Relative quantitation of multi-antennary N-glycan classes: combining PGC-LC-ESI-MS with exoglycosidase digestion Analyst 2015, 140, 5444-5449 10.1039/C5AN00691K
39. Palmisano, G.; Larsen, M. R.; Packer, N. H.; Thaysen-Andersen, M. Structural analysis of glycoprotein sialylation-part II: LC-MS based detection RSC Adv. 2013, 3, 22706-22726 10.1039/c3ra42969e
40. Pabst, M.; Bondili, J. S.; Stadlmann, J.; Mach, L.; Altmann, F. 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. 2007, 79, 5051-5057 10.1021/ac070363i
41. Marino, K.; Bones, J.; Kattla, J. J.; Rudd, P. M. A systematic approach to protein glycosylation analysis: a path through the maze Nat. Chem. Biol. 2010, 6, 713-723 10.1038/nchembio.437
42. Alley, W. R., Jr.; Novotny, M. V. Structural glycomic analyses at high sensitivity: a decade of progress Annu. Rev. Anal. Chem. 2013, 6, 237-265 10.1146/annurev-anchem-062012-092609
43. Zaia, J. Mass spectrometry and the emerging field of glycomics Chem. Biol. 2008, 15, 881-892 10.1016/j.chembiol.2008.07.016
44. Harvey, D. J. Fragmentation of negative ions from carbohydrates; Part 2. Fragmentation of high-mannose N-linked glycans J. Am. Soc. Mass Spectrom. 2005, 16, 631-646 10.1016/j.jasms.2005.01.005
45. Harvey, D. J. Fragmentation of negative ions from carbohydrates: Part 3. Fragmentation of hybrid and complex N-linked glycans J. Am. Soc. Mass Spectrom. 2005, 16, 647-659 10.1016/j.jasms.2005.01.006
46. Harvey, D. J. Fragmentation of negative ions from carbohydrates: part 1. Use of nitrate and other anionic adducts for the production of negative ion electrospray spectra from N-linked carbohydrates J. Am. Soc. Mass Spectrom. 2005, 16, 622-630 10.1016/j.jasms.2005.01.004
47. Seymour, J. L.; Costello, C. E.; Zaia, J. The influence of sialylation on glycan negative ion dissociation and energetics J. Am. Soc. Mass Spectrom. 2006, 17, 844-854 10.1016/j.jasms.2006.02.022
48. Ceroni, A.; Maass, K.; Geyer, H.; Geyer, R.; Dell, A.; Haslam, S. M. GlycoWorkbench: a tool for the computer-assisted annotation of mass spectra of glycans J. Proteome Res. 2008, 7, 1650-1659 10.1021/pr7008252
49. Cooper, C. A.; Gasteiger, E.; Packer, N. H. GlycoMod - a software tool for determining glycosylation compositions from mass spectrometric data Proteomics 2001, 1, 340-349 10.1002/1615-9861(200102)1:2<340::AID-PROT340>3.0.CO;2-B
50. Liu, G.; Neelamegham, S. Integration of systems glycobiology with bioinformatics toolboxes, glycoinformatics resources, and glycoproteomics data Wiley interdiscip. Rev. Syst. Biol. Med. 2015, 7, 163-181 10.1002/wsbm.1296
51. Campbell, M. P.; Peterson, R.; Mariethoz, J.; Gasteiger, E.; Akune, Y.; Aoki-Kinoshita, K. F.; Lisacek, F.; Packer, N. H. UniCarbKB: building a knowledge platform for glycoproteomics Nucleic Acids Res. 2014, 42, D215-D221 10.1093/nar/gkt1128
52. Hayes, C. A.; Karlsson, N. G.; Struwe, W. B.; Lisacek, F.; Rudd, P. M.; Packer, N. H.; Campbell, M. P. UniCarb-DB: a database resource for glycomic discovery Bioinformatics 2011, 27, 1343-1344 10.1093/bioinformatics/btr137
53. Sethi, M. K.; Thaysen-Andersen, M.; Smith, J. T.; Baker, M. S.; Packer, N. H.; Hancock, W. S.; Fanayan, S. Comparative N-glycan profiling of colorectal cancer cell lines reveals unique bisecting GlcNAc and alpha-2,3-linked sialic acid determinants are associated with membrane proteins of the more metastatic/aggressive cell lines J. Proteome Res. 2014, 13, 277-288 10.1021/pr400861m
54. Sethi, M. K.; Kim, H.; Park, C. K.; Baker, M. S.; Paik, Y. K.; Packer, N. H.; Hancock, W. S.; Fanayan, S.; Thaysen-Andersen, M. In-depth N-glycome profiling of paired colorectal cancer and non-tumorigenic tissues reveals cancer-, stage- and EGFR-specific protein N-glycosylation Glycobiology 2015, 25, 1064-1078 10.1093/glycob/cwv042
55. Anugraham, M.; Jacob, F.; Nixdorf, S.; Everest-Dass, A. V.; Heinzelmann-Schwarz, V.; Packer, N. H. Specific glycosylation of membrane proteins in epithelial ovarian cancer cell lines: glycan structures reflect gene expression and DNA methylation status Mol. Cell. Proteomics 2014, 13, 2213-2232 10.1074/mcp.M113.037085
56. de Leoz, M. L.; Young, L. J.; An, H. J.; Kronewitter, S. R.; Kim, J.; Miyamoto, S.; Borowsky, A. D.; Chew, H. K.; Lebrilla, C. B. High-mannose glycans are elevated during breast cancer progression Mol. Cell. Proteomics 2011, 10, M110.002717 10.1074/mcp.M110.002717
57. Liu, X.; Nie, H.; Zhang, Y.; Yao, Y.; Maitikabili, A.; Qu, Y.; Shi, S.; Chen, C.; Li, Y. Cell surface-specific N-glycan profiling in breast cancer PLoS One 2013, 8, e72704 10.1371/journal.pone.0072704
58. Chik, J. H.; Zhou, J.; Moh, E. S.; Christopherson, R.; Clarke, S. J.; Molloy, M. P.; Packer, N. H. Comprehensive glycomics comparison between colon cancer cell cultures and tumours: implications for biomarker studies J. Proteomics 2014, 108, 146-162 10.1016/j.jprot.2014.05.002
59. Kaprio, T.; Satomaa, T.; Heiskanen, A.; Hokke, C. H.; Deelder, A. M.; Mustonen, H.; Hagstrom, J.; Carpen, O.; Saarinen, J.; Haglund, C. N-glycomic profiling as a tool to separate rectal adenomas from carcinomas Mol. Cell. Proteomics 2015, 14, 277-288 10.1074/mcp.M114.041632
60. Park, J. J.; Lee, M. Increasing the alpha 2, 6 sialylation of glycoproteins may contribute to metastatic spread and therapeutic resistance in colorectal cancer Gut Liver 2013, 7, 629-641 10.5009/gnl.2013.7.6.629
61. Lu, J.; Isaji, T.; Im, S.; Fukuda, T.; Hashii, N.; Takakura, D.; Kawasaki, N.; Gu, J. β-Galactoside α2,6-Sialyltranferase 1 promotes transforming growth factor-beta-mediated epithelial-mesenchymal transition J. Biol. Chem. 2014, 289, 34627-34641 10.1074/jbc.M114.593392
62. Fernandez-Rodriguez, J.; Feijoo-Carnero, C.; Merino-Trigo, A.; Paez de la Cadena, M.; Rodriguez-Berrocal, F. J.; de Carlos, A.; Butron, M.; Martinez-Zorzano, V. S. Immunohistochemical analysis of sialic acid and fucose composition in human colorectal adenocarcinoma Tumor Biol. 2000, 21, 153-164 10.1159/000030122
63. Recchi, M. A.; Hebbar, M.; Hornez, L.; Harduin-Lepers, A.; Peyrat, J. P.; Delannoy, P. Multiplex reverse transcription polymerase chain reaction assessment of sialyltransferase expression in human breast cancer Cancer Res. 1998, 58, 4066-4070
64. Olio, F. D.; Malagolini, N.; di Stefano, G.; Minni, F.; Marrano, D.; Serafini-Cessi, F. Increased CMP-NeuAc:Gal beta 1,4GlcNAc-R alpha 2,6 sialyltransferase activity in human colorectal cancer tissues Int. J. Cancer 1989, 44, 434-439 10.1002/ijc.2910440309
65. Vierbuchen, M. J.; Fruechtnicht, W.; Brackrock, S.; Krause, K. T.; Zienkiewicz, T. J. Quantitative lectin-histochemical and immunohistochemical studies on the occurrence of alpha(2,3)- and alpha(2,6)-linked sialic acid residues in colorectal carcinomas. Relation to clinicopathologic features Cancer 1995, 76, 727-735 10.1002/1097-0142(19950901)76:5<727::AID-CNCR2820760504>3.0.CO;2-R
66. Asada, M.; Furukawa, K.; Segawa, K.; Endo, T.; Kobata, A. Increased expression of highly branched N-glycans at cell surface is correlated with the malignant phenotypes of mouse tumor cells Cancer Res. 1997, 57, 1073-1080
67. Granovsky, M.; Fata, J.; Pawling, J.; Muller, W. J.; Khokha, R.; Dennis, J. W. Suppression of tumor growth and metastasis in Mgat5-deficient mice Nat. Med. 2000, 6, 306-312 10.1038/73163
68. Gu, J.; Taniguchi, N. Potential of N-glycan in cell adhesion and migration as either a positive or negative regulator Cell Adh. Migr. 2008, 2, 243-245 10.4161/cam.2.4.6748
69. Ferreira, S. A.; Vasconcelos, J. L.; Silva, R. C.; Cavalcanti, C. L.; Bezerra, C. L.; Rego, M. J.; Beltrao, E. I. Expression patterns of alpha2,3-sialyltransferase I and alpha2,6-sialyltransferase I in human cutaneous epithelial lesions Eur. J. Histochem. 2013, 57, e7 10.4081/ejh.2013.e7
70. Cui, H.; Lin, Y.; Yue, L.; Zhao, X.; Liu, J. Differential expression of the alpha2,3-sialic acid residues in breast cancer is associated with metastatic potential Oncol. Rep. 2011, 25, 1365-1371 10.3892/or.2011.1192
71. Perez-Garay, M.; Arteta, B.; Pages, L.; de Llorens, R.; de Bolos, C.; Vidal-Vanaclocha, F.; Peracaula, R. alpha2,3-sialyltransferase ST3Gal III modulates pancreatic cancer cell motility and adhesion in vitro and enhances its metastatic potential in vivo PLoS One 2010, 5, e12524 10.1371/journal.pone.0012524
72. Harvey, B. E.; Toth, C. A.; Wagner, H. E.; Steele, G. D., Jr.; Thomas, P. Sialyltransferase activity and hepatic tumor growth in a nude mouse model of colorectal cancer metastases Cancer Res. 1992, 52, 1775-1779
73. Liu, Y. C.; Yen, H. Y.; Chen, C. Y.; Chen, C. H.; Cheng, P. F.; Juan, Y. H.; Khoo, K. H.; Yu, C. J.; Yang, P. C.; Hsu, T. L.; Wong, C. H. Sialylation and fucosylation of epidermal growth factor receptor suppress its dimerization and activation in lung cancer cells Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 11332-11337 10.1073/pnas.1107385108
74. Sato, Y.; Takahashi, M.; Shibukawa, Y.; Jain, S. K.; Hamaoka, R.; Miyagawa, J.; Yaginuma, Y.; Honke, K.; Ishikawa, M.; Taniguchi, N. Overexpression of N-acetylglucosaminyltransferase III enhances the epidermal growth factor-induced phosphorylation of ERK in HeLaS3 cells by up-regulation of the internalization rate of the receptors J. Biol. Chem. 2001, 276, 11956-11962 10.1074/jbc.M008551200
75. Lin, M. C.; Huang, M. J.; Liu, C. H.; Yang, T. L.; Huang, M. C. GALNT2 enhances migration and invasion of oral squamous cell carcinoma by regulating EGFR glycosylation and activity Oral Oncol. 2014, 50, 478-484 10.1016/j.oraloncology.2014.02.003
76. Liu, J.; Liu, H.; Zhang, W.; Wu, Q.; Liu, W.; Liu, Y.; Pan, D.; Xu, J.; Gu, J. N-acetylglucosaminyltransferase V confers hepatoma cells with resistance to anoikis through EGFR/PAK1 activation Glycobiology 2013, 23, 1097-1109 10.1093/glycob/cwt049
77. Fernandez-Rodriguez, J.; Feijoo-Carnero, C.; Merino-Trigo, A.; Paez de la Cadena, M.; Rodriguez-Berrocal, F. J.; de Carlos, A.; Butron, M.; Martinez-Zorzano, V. S. Immunohistochemical analysis of sialic acid and fucose composition in human colorectal adenocarcinoma Tumor Biol. 2000, 21, 153-164 10.1159/000030122
78. Chen, H. L. Lewis glyco-epitopes: structure, biosynthesis, and functions Adv. Exp. Med. Biol. 2011, 705, 53-80 10.1007/978-1-4419-7877-6-4
79. Takahashi, M.; Kuroki, Y.; Ohtsubo, K.; Taniguchi, N. Core fucose and bisecting GlcNAc, the direct modifiers of the N-glycan core: Their functions and target proteins Carbohydr. Res. 2009, 344, 1387-1390 10.1016/j.carres.2009.04.031
80. Zhang, X.; Wang, Y.; Qian, Y.; Wu, X.; Zhang, Z.; Liu, X.; Zhao, R.; Zhou, L.; Ruan, Y.; Xu, J.; Liu, H.; Ren, S.; Xu, C.; Gu, J. Discovery of specific metastasis-related N-glycan alterations in epithelial ovarian cancer based on quantitative glycomics PLoS One 2014, 9, e87978 10.1371/journal.pone.0087978
81. Song, Y.; Aglipay, J. A.; Bernstein, J. D.; Goswami, S.; Stanley, P. The bisecting GlcNAc on N-glycans inhibits growth factor signaling and retards mammary tumor progression Cancer Res. 2010, 70, 3361-3371 10.1158/0008-5472.CAN-09-2719
82. Miyake, M.; Taki, T.; Hitomi, S.; Hakomori, S. Correlation of expression of H/Ley/Leb antigens with survival in patients with adenocarcinoma of the lung N. Engl. J. Med. 1992, 327, 14-18 10.1056/NEJM199207023270103
83. Shirahama, T.; Ikoma, M.; Muramatsu, T.; Kayajima, T.; Ohi, Y.; Tsushima, T.; Akebi, N.; Ohmori, H.; Hirao, Y.; Okajima, E. The binding site of fucose binding proteins of lotus tetranoglobus is a prognostic marker for transitional cell carcinoma of the human urinary bladder Cancer 1993, 72, 1329-1334 10.1002/1097-0142(19930815)72:4<1329::AID-CNCR2820720430>3.0.CO;2-6
84. Kyselova, Z.; Mechref, Y.; Kang, P.; Goetz, J. A.; Dobrolecki, L. E.; Sledge, G. W.; Schnaper, L.; 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 10.1373/clinchem.2007.087148
85. Aubert, M.; Panicot, L.; Crotte, C.; Gibier, P.; Lombardo, D.; Sadoulet, M. O.; Mas, E. Restoration of alpha(1,2) fucosyltransferase activity decreases adhesive and metastatic properties of human pancreatic cancer cells Cancer Res. 2000, 60, 1449-1456
86. Saldova, R.; Fan, Y.; Fitzpatrick, J. M.; Watson, R. W.; Rudd, P. M. Core fucosylation and alpha2-3 sialylation in serum N-glycome is significantly increased in prostate cancer comparing to benign prostate hyperplasia Glycobiology 2011, 21, 195-205 10.1093/glycob/cwq147
87. Pabst, M.; Altmann, F. Influence of electrosorption, solvent, temperature, and ion polarity on the performance of LC-ESI-MS using graphitic carbon for acidic oligosaccharides Anal. Chem. 2008, 80, 7534-7542 10.1021/ac801024r