Large-scale identification of core-fucosylated glycopeptide sites in pancreatic cancer serum using mass spectrometry

Journal of Proteome Research

Volumn 14, Issue 4, 2015, Pages 1968-1978

  Tan, Zhijing ^a   Yin, Haidi ^a   Nie, Song ^a   Lin, Zhenxin ^a   Zhu, Jianhui ^a   Ruffin, Mack T ^b   Anderson, Michelle A ^b   Simeone, Diane M ^a   Lubman, David M ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

core fucosylation; glycoproteomics; iTRAQ; lectin; Pancreatic cancer; serum

Indexed keywords

GLYCOPEPTIDE; TRYPSIN; TUMOR MARKER; FUCOSE; LENTIL LECTIN; PLANT LECTIN;

ARTICLE; CANCER GROWTH; CHRONIC PANCREATITIS; COMPARATIVE STUDY; CONTROLLED STUDY; DEGLYCOSYLATION; FUCOSYLATION; GENE ONTOLOGY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; IONIZATION; LENTIL; MASS SPECTROMETRY; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; SIGNAL TRANSDUCTION; ANALYSIS OF VARIANCE; BLOOD; ISOLATION AND PURIFICATION; LIQUID CHROMATOGRAPHY; METABOLISM; PANCREAS TUMOR; PROCEDURES; TANDEM MASS SPECTROMETRY;

ANALYSIS OF VARIANCE; BIOMARKERS, TUMOR; CHROMATOGRAPHY, LIQUID; FUCOSE; GLYCOPEPTIDES; HUMANS; MASS SPECTROMETRY; PANCREATIC NEOPLASMS; PLANT LECTINS; TANDEM MASS SPECTROMETRY; TRYPSIN;

EID: 84926511903     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b00068     Document Type: Article

References (42)

1. Osumi, D.; Takahashi, M.; Miyoshi, E.; Yokoe, S.; Lee, S. H.; Noda, K.; Nakamori, S.; Gu, J.; Ikeda, Y.; Kuroki, Y.; Sengoku, K.; Ishikawa, M.; Taniguchi, N. Core fucosylation of E-cadherin enhances cell-cell adhesion in human colon carcinoma WiDr cells Cancer Sci. 2009, 100, 888-895
2. Dennis, J. W.; Laferte, S.; Waghorne, C.; Breitman, M. L.; Kerbel, R. S. Beta-1-6 branching of Asn-linked oligosaccharides is directly associated with metastasis Science 1987, 236, 582-585
3. Ma, B.; Simala-Grant, J. L.; Taylor, D. E. Fucosylation in prokaryotes and eukaryotes Glycobiology 2006, 16, 158-184
4. Hakomori, S. Tumor malignancy defined by aberrant glycosylation and sphingo(glyco) lipid metabolism Cancer Res. 1996, 56, 5309-5318
5. Muinelo-Romay, L.; Villar-Portela, S.; Cuevas, E.; Gil-Martin, E.; Fernandez-Briera, A. Identification of alpha(1,6)fucosylated proteins differentially expressed in human colorectal cancer BMC Cancer 2011, 11, 508
6. 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
7. Yin, H.; Lin, Z.; Nie, S.; Wu, J.; Tan, Z.; Zhu, J.; Dai, J.; Feng, Z.; Marrero, J.; Lubman, D. M. Mass-selected site-specific core-fucosylation of ceruloplasmin in alcohol-related hepatocellular carcinoma J. Proteome Res. 2014, 13, 2887-2896
8. Nie, S.; Lo, A.; Wu, J.; Zhu, J.; Tan, Z.; Simeone, D. M.; Anderson, M. A.; Shedden, K. A.; Ruffin, M. T.; Lubman, D. M. Glycoprotein biomarker panel for pancreatic cancer discovered by quantitative proteomics analysis J. Proteome Res. 2014, 13, 1873-1884
9. Zhao, J.; Qiu, W. L.; Simeone, D. M.; Lubman, D. M. N-Linked glycosylation profiling of pancreatic cancer serum using capillary liquid phase separation coupled with mass spectrometric analysis J. Proteome Res. 2007, 6, 1126-1138
10. Lin, Z. X.; Yin, H. D.; Lo, A.; Ruffin, M. T.; Anderson, M. A.; Simeone, D. M.; Lubman, D. M. Label-free relative quantification of alpha-2-macroglobulin site-specific core-fucosylation in pancreatic cancer by LC-MS/MS Electrophoresis 2014, 35, 2108-2115
11. Zielinska, D. F.; Gnad, F.; Wisniewski, J. R.; Mann, M. Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints Cell 2010, 141, 897-907
12. Fanayan, S.; Hincapie, M.; Hancock, W. S. Using lectins to harvest the plasma/serum glycoproteome Electrophoresis 2012, 33, 1746-1754
13. Kornfeld, K.; Reitman, M. L.; Kornfeld, R. The carbohydrate-binding specificity of pea and lentil lectins. Fucose is an important determinant J. Biol. Chem. 1981, 256, 6633-6640
14. Tateno, H.; Nakamura-Tsuruta, S.; Hirabayashi, J. Comparative analysis of core-fucose-binding lectins from Lens culinaris and Pisum sativum using frontal affinity chromatography Glycobiology 2009, 19, 527-536
15. Sharon, N.; Lis, H. Legume lectins-A large family of homologous proteins FASEB J. 1990, 4, 3198-3208
16. Jia, W.; Lu, Z.; Fu, Y.; Wang, H. P.; Wang, L. H.; Chi, H.; Yuan, Z. F.; Zheng, Z. B.; Song, L. N.; Han, H. H.; Liang, Y. M.; Wang, J. L.; Cai, Y.; Zhang, Y. K.; Deng, Y. L.; Ying, W. T.; He, S. M.; Qian, X. H. A strategy for precise and large scale identification of core fucosylated glycoproteins Mol. Cell. Proteomics 2009, 8, 913-923
17. Nie, S.; Lo, A.; Zhu, J. H.; Wu, J.; Ruffin, M. T.; Lubman, D. M. Isobaric protein-level labeling strategy for serum glycoprotein quantification analysis by liquid chromatography-tandem mass spectrometry Anal. Chem. 2013, 85, 5353-5357
18. Liu, Y.; He, J.; Li, C.; Benitez, R.; Fu, S.; Marrero, J.; Lubman, D. M. Identification and confirmation of biomarkers using an integrated platform for quantitative analysis of glycoproteins and their glycosylations J. Proteome Res. 2010, 9, 798-805
19. Sharon, N. Lectin carbohydrate complexes of plants and animals-an atomic view Trends Biochem. Sci. 1993, 18, 221-226
20. Loris, R.; Hamelryck, T.; Bouckaert, J.; Wyns, L. Legume lectin structure Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol. 1998, 1383, 9-36
21. Lewandrowski, U.; Moebius, J.; Walter, U.; Sickmann, A. Elucidation of N-glycosylation sites on human platelet proteins-A glycoproteomic approach Mol. Cell. Proteomics 2006, 5, 226-233
22. Kaji, H.; Yamauchi, Y.; Takahashi, N.; Isobe, T. Mass spectrometric identification of N-linked glycopeptides using lectin-mediated affinity capture and glycosylation site-specific stable isotope tagging Nat. Protoc. 2006, 1, 3019-3027
23. Cao, Q.; Zhao, X.; Zhao, Q.; Lv, X.; Ma, C.; Li, X.; Zhao, Y.; Peng, B.; Ying, W.; Qian, X. Strategy integrating stepped fragmentation and glycan diagnostic ion-based spectrum refinement for the identification of core fucosylated glycoproteome using mass spectrometry Anal. Chem. 2014, 86, 6804-6811
24. Hagglund, P.; Bunkenborg, J.; Elortza, F.; Jensen, O. N.; Roepstorff, P. A new strategy for identification of N-glycosylated proteins and unambiguous assignment of their glycosylation sites using HILIC enrichment and partial deglycosylation J. Proteome Res. 2004, 3, 556-566
25. Dell, A.; Morris, H. R. Glycoprotein structure determination by mass spectrometry Science 2001, 291, 2351-2356
26. Peterman, S. M.; Mulholland, J. J. A novel approach for identification and characterization of glycoproteins using a hybrid linear ion trap/FT-ICR mass spectrometer J. Am. Soc. Mass Spectrom. 2006, 17, 168-179
27. Zhang, W.; Wang, H.; Zhang, L.; Yao, J.; Yang, P. Y. Large-scale assignment of N-glycosylation sites using complementary enzymatic deglycosylation Talanta 2011, 85, 499-505
28. Valliere-Douglass, J. F.; Eakin, C. M.; Wallace, A.; Ketchem, R. R.; Wang, W.; Treuheit, M. J.; Balland, A. Glutamine-linked and non-consensus asparagine-linked oligosaccharides present in human recombinant antibodies define novel protein glycosylation motifs J. Biol. Chem. 2010, 285, 16012-16022
29. Lee, J. Y.; Kim, J. Y.; Park, G. W.; Cheon, M. H.; Kwon, K. H.; Ahn, Y. H.; Moon, M. H.; Lee, H. J.; Paik, Y. K.; Yoo, J. S. Targeted mass spectrometric approach for biomarker discovery and validation with nonglycosylated tryptic peptides from N-linked glycoproteins in human plasma Mol. Cell. Proteomics 2011, 10, M111
30. Chen, R.; Jiang, X.; Sun, D.; Han, G.; Wang, F.; Ye, M.; Wang, L.; Zou, H. Glycoproteomics analysis of human liver tissue by combination of multiple enzyme digestion and hydrazide chemistry J. Proteome Res. 2009, 8, 651-661
31. Pan, S.; Tamura, Y.; Chen, R.; May, D.; McIntosh, M. W.; Brentnall, T. A. Large-scale quantitative glycoproteomics analysis of site-specific glycosylation occupancy Mol. Biosyst. 2012, 8, 2850-2856
32. Ferreira, J. A.; Daniel-da-Silva, A. L.; Alves, R. M. P.; Duarte, D.; Vieira, I.; Santos, L. L.; Vitorino, R.; Amado, F. Synthesis and optimization of lectin functionalized nanoprobes for the selective recovery of glycoproteins from human body fluids Anal. Chem. 2011, 83, 7035-7043
33. Ma, C.; Zhang, Q.; Qu, J.; Zhao, X.; Li, X.; Liu, Y.; Wang, P. G. A precise approach in large scale core-fucosylated glycoproteins identification with low- and high-normalized collision energy J. Proteomics 2014, 114, 61-70
34. Wang, L. H.; Li, D. Q.; Fu, Y.; Wang, H. P.; Zhang, J. F.; Yuan, Z. F.; Sun, R. X.; Zeng, R.; He, S. M.; Gao, W. PFind 2.0: a software package for peptide and protein identification via tandem mass spectrometry Rapid Commun. Mass Spectrom. 2007, 21, 2985-2991
35. Wollscheid, B.; Bausch-Fluck, D.; Henderson, C.; OBrien, R.; Bibel, M.; Schiess, R.; Aebersold, R.; Watts, J. D. Mass-spectrometric identification and relative quantification of N-linked cell surface glycoproteins Nat. Biotechnol. 2009, 27, 378-386
36. Lei, Z.; Beuerman, R. W.; Chew, A. P.; Koh, S. K.; Cafaro, T. A.; Urrets-Zavalia, E. A.; Urrets-Zavalia, J. A.; Li, S. F.; Serra, H. M. Quantitative analysis of N-linked glycoproteins in tear fluid of climatic droplet keratopathy by glycopeptide capture and iTRAQ J. Proteome Res. 2009, 8, 1992-2003
37. Zielinska, D. F.; Gnad, F.; Schropp, K.; Wisniewski, J. R.; Mann, M. Mapping N-glycosylation sites across seven evolutionarily distant species reveals a divergent substrate proteome despite a common rore machinery Mol. Cell 2012, 46, 542-548
38. Marshall, R. D. Glycoproteins Annu. Rev. Biochem. 1972, 41, 673-702
39. Gavel Y1, v. H. G. Sequence differences between glycosylated and non-glycosylated Asn-X-Thr/Ser acceptor sites: implications for protein engineering Protein Eng. 1990, 3, 433-442
40. Helenius, A. How N-Linked oligosaccharides affect glycoprotein folding in the endoplasmic-reticulum Mol. Biol. Cell 1994, 5, 253-265
41. Saldova, R.; Wormald, M. R.; Dwek, R. A.; Rudd, P. M. Glycosylation changes on serum glycoproteins in ovarian cancer may contribute to disease pathogenesis Dis. Markers 2008, 25, 219-232
42. Marttila-Ichihara, F.; Turja, R.; Miiluniemi, M.; Karikoski, M.; Maksimow, M.; Niemela, J.; Martinez-Pomares, L.; Salmi, M.; Jalkanen, S. Macrophage mannose receptor on lymphatics controls cell trafficking Blood 2008, 112, 64-72