Glycoproteomics approach for identifying glycobiomarker candidate molecules for tissue type classification of non-small cell lung carcinoma

Journal of Proteome Research

Volumn 13, Issue 11, 2014, Pages 4705-4716

  Hirao, Yoshitoshi ^a   Matsuzaki, Hideki ^a   Iwaki, Jun ^a   Kuno, Atsushi ^a   Kaji, Hiroyuki ^a   Ohkura, Takashi ^a   Togayachi, Akira ^a   Abe, Minako ^a   Nomura, Masaharu ^b   Noguchi, Masayuki ^c   Ikehara, Yuzuru ^a   Narimatsu, Hisashi ^a  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^b TOKYO MEDICAL UNIVERSITY   (Japan)

^c UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Biomarker; glycoproteomics; glycosylation; lectin microarray; lung cancer; tissue

Indexed keywords

ALEURIA AURANTIA LECTIN; CONCANAVALIA ENSIFORMIS AGGLUTININ; GLYCOPROTEIN; HIPPEASTRUM HYBRID LECTIN; LECTIN; TUMOR MARKER; UNCLASSIFIED DRUG; FIBRONECTIN; PEANUT AGGLUTININ;

ARTICLE; BIOMICS; CLINICAL ARTICLE; GLYCOPROTEOMICS; GLYCOSYLATION; HUMAN; HUMAN TISSUE; LUNG CANCER CELL LINE; MICROARRAY ANALYSIS; NON SMALL CELL LUNG CANCER; PROTEIN ANALYSIS; PROTEIN EXPRESSION; CLASSIFICATION; GENETICS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; PATHOLOGY; PROCEDURES; PROTEOMICS; TUMOR CELL LINE; WESTERN BLOTTING;

BIOMARKERS, TUMOR; BLOTTING, WESTERN; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CHROMATOGRAPHY, LIQUID; FIBRONECTINS; GLYCOPROTEINS; GLYCOSYLATION; HUMANS; LECTINS; MASS SPECTROMETRY; MICROARRAY ANALYSIS; PEANUT AGGLUTININ; PROTEOMICS;

EID: 84908880907     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr5006668     Document Type: Article

References (56)

1. Jemal, A.; Siegel, R.; Ward, E.; Hao, Y.; Xu, J.; Thun, M. J. Cancer statistics, 2009 Ca-Cancer J. Clin. 2009, 59, 225-49
2. Plebani, M.; Basso, D.; Navaglia, F.; De Paoli, M.; Tommasini, A.; Cipriani, A. Clinical evaluation of seven tumour markers in lung cancer diagnosis: can any combination improve the results? Br. J. Cancer 1995, 72, 170-3
3. Sung, H. J.; Cho, J. Y. Biomarkers for the lung cancer diagnosis and their advances in proteomics BMB Rep 2008, 41, 615-25
4. Miyake, M.; Zenita, K.; Tanaka, O.; Okada, Y.; Kannagi, R. Stage-specific expression of SSEA-1-related antigens in the developing lung of human embryos and its relation to the distribution of these antigens in lung cancers Cancer Res. 1988, 48, 7150-8
5. Shiota, T.; Matsubara, Y.; Ikeda, S.; Ishida, H.; Katsura, A.; Hanawa, T.; Yagi, K.; Kosaba, S.; Hatakenaka, R.; Funatsu, T. [Evaluation of sialyl SSEA-1 antigen in patients with lung cancer] Nihon Gan Chiryo Gakkai Shi 1989, 24, 1067-73
6. Ueda, K.; Katagiri, T.; Shimada, T.; Irie, S.; Sato, T. A.; Nakamura, Y.; Daigo, Y. Comparative profiling of serum glycoproteome by sequential purification of glycoproteins and 2-nitrobenzensulfenyl (NBS) stable isotope labeling: a new approach for the novel biomarker discovery for cancer J. Proteome Res. 2007, 6, 3475-83
7. Kawamura, T.; Nomura, M.; Tojo, H.; Fujii, K.; Hamasaki, H.; Mikami, S.; Bando, Y.; Kato, H.; Nishimura, T. Proteomic analysis of laser-microdissected paraffin-embedded tissues: (1) stage-related protein candidates upon non-metastatic lung adenocarcinoma J. Proteomics 2010, 73, 1089-99
8. Nishimura, T.; Nomura, M.; Tojo, H.; Hamasaki, H.; Fukuda, T.; Fujii, K.; Mikami, S.; Bando, Y.; Kato, H. Proteomic analysis of laser-microdissected paraffin-embedded tissues: (2) MRM assay for stage-related proteins upon non-metastatic lung adenocarcinoma J. Proteomics 2010, 73, 1100-10
9. Li, Q. K.; Gabrielson, E.; Zhang, H. Application of glycoproteomics for the discovery of biomarkers in lung cancer Proteomics: Clin. Appl. 2012, 6, 244-56
10. Patwa, T.; Li, C.; Simeone, D. M.; Lubman, D. M. Glycoprotein analysis using protein microarrays and mass spectrometry Mass Spectrom. Rev. 2010, 29, 830-844
11. Adamczyk, B.; Tharmalingam, T.; Rudd, P. M. Glycans as cancer biomarkers Biochim. Biophys. Acta 2012, 1820, 1347-53
12. Block, T. M.; Comunale, M. A.; Lowman, M.; Steel, L. F.; Romano, P. R.; Fimmel, C.; Tennant, B. C.; London, W. T.; Evans, A. A.; Blumberg, B. S.; Dwek, R. A.; Mattu, T. S.; Mehta, A. S. Use of targeted glycoproteomics to identify serum glycoproteins that correlate with liver cancer in woodchucks and humans Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 779-784
13. Abbott, K. L.; Pierce, J. M. Lectin-based glycoproteomic techniques for the enrichment and identification of potential biomarkers Methods Enzymol. 2010, 480, 461-76
14. Dennis, J. W.; Laferte, S.; Yagel, S.; Breitman, M. L. Asparagine-linked oligosaccharides associated with metastatic cancer Cancer Cells 1989, 1, 87-92
15. Singhal, A.; Hakomori, S. Molecular changes in carbohydrate antigens associated with cancer BioEssays 1990, 12, 223-30
16. Stuchlova Horynova, M.; Raska, M.; Clausen, H.; Novak, J. Aberrant O-glycosylation and anti-glycan antibodies in an autoimmune disease IgA nephropathy and breast adenocarcinoma Cell. Mol. Life Sci. 2013, 70, 829-39
17. Dai, Z.; Zhou, J.; Qiu, S. J.; Liu, Y. K.; Fan, J. Lectin-based glycoproteomics to explore and analyze hepatocellular carcinoma-related glycoprotein markers Electrophoresis 2009, 30, 2957-66
18. Tsai, H. Y.; Boonyapranai, K.; Sriyam, S.; Yu, C. J.; Wu, S. W.; Khoo, K. H.; Phutrakul, S.; Chen, S. T. Glycoproteomics analysis to identify a glycoform on haptoglobin associated with lung cancer Proteomics 2011, 11, 2162-70
19. 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, 1755-64
20. Narimatsu, H.; Sawaki, H.; Kuno, A.; Kaji, H.; Ito, H.; Ikehara, Y. A strategy for discovery of cancer glyco-biomarkers in serum using newly developed technologies for glycoproteomics FEBS J. 2010, 277, 95-105
21. Kuno, A.; Uchiyama, N.; Koseki-Kuno, S.; Ebe, Y.; Takashima, S.; Yamada, M.; Hirabayashi, J. Evanescent-field fluorescence-assisted lectin microarray: a new strategy for glycan profiling Nat. Methods 2005, 2, 851-6
22. Kameyama, A.; Kikuchi, N.; Nakaya, S.; Ito, H.; Sato, T.; Shikanai, T.; Takahashi, Y.; Takahashi, K.; Narimatsu, H. A strategy for identification of oligosaccharide structures using observational multistage mass spectral library Anal. Chem. 2005, 77, 4719-4725
23. Kaji, H.; Saito, H.; Yamauchi, Y.; Shinkawa, T.; Taoka, M.; Hirabayashi, J.; Kasai, K.; Takahashi, N.; Isobe, T. Lectin affinity capture, isotope-coded tagging and mass spectrometry to identify N-linked glycoproteins Nat. Biotechnol. 2003, 21, 667-72
24. Kuno, A.; Matsuda, A.; Ikehara, Y.; Narimatsu, H.; Hirabayashi, J. Differential glycan profiling by lectin microarray targeting tissue specimens Methods Enzymol. 2010, 478, 165-79
25. Matsuda, A.; Kuno, A.; Ishida, H.; Kawamoto, T.; Shoda, J.; Hirabayashi, J. Development of an all-in-one technology for glycan profiling targeting formalin-embedded tissue sections Biochem. Biophys. Res. Commun. 2008, 370, 259-63
26. 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, 3019-27
27. Ito, H.; Kameyama, A.; Sato, T.; Sukegawa, M.; Ishida, H. K.; Narimatsu, H. Strategy for the fine characterization of glycosyltransferase specificity using isotopomer assembly Nat. Methods 2007, 4, 577-82
28. Kuno, A.; Kato, Y.; Matsuda, A.; Kaneko, M. K.; Ito, H.; Amano, K.; Chiba, Y.; Narimatsu, H.; Hirabayashi, J. Focused differential glycan analysis with the platform antibody-assisted lectin profiling for glycan-related biomarker verification Mol. Cell. Proteomics 2009, 8, 99-108
29. Ito, H.; Kuno, A.; Sawaki, H.; Sogabe, M.; Ozaki, H.; Tanaka, Y.; Mizokami, M.; Shoda, J.; Angata, T.; Sato, T.; Hirabayashi, J.; Ikehara, Y.; Narimatsu, H. Strategy for glycoproteomics: identification of glyco-alteration using multiple glycan profiling tools J. Proteome Res. 2009, 8, 1358-67
30. Matsuda, A.; Kuno, A.; Kawamoto, T.; Matsuzaki, H.; Irimura, T.; Ikehara, Y.; Zen, Y.; Nakanuma, Y.; Yamamoto, M.; Ohkohchi, N.; Shoda, J.; Hirabayashi, J.; Narimatsu, H. Wisteria floribunda agglutinin-positive mucin 1 is a sensitive biliary marker for human cholangiocarcinoma Hepatology 2010, 52, 174-82
31. Kuno, A.; Ikehara, Y.; Tanaka, Y.; Angata, T.; Unno, S.; Sogabe, M.; Ozaki, H.; Ito, K.; Hirabayashi, J.; Mizokami, M.; Narimatsu, H. Multilectin assay for detecting fibrosis-specific glyco-alteration by means of lectin microarray Clin. Chem. 2011, 57, 48-56
32. Ocho, M.; Togayachi, A.; Iio, E.; Kaji, H.; Kuno, A.; Sogabe, M.; Korenaga, M.; Gotoh, M.; Tanaka, Y.; Ikehara, Y.; Mizokami, M.; Narimatsu, H. Application of a glycoproteomics-based biomarker development method: alteration in glycan structure on colony stimulating factor 1 receptor as a possible glycobiomarker candidate for evaluation of liver cirrhosis J. Proteome Res. 2014, 13, 1428-37
33. Matsuda, A.; Kuno, A.; Matsuzaki, H.; Kawamoto, T.; Shikanai, T.; Nakanuma, Y.; Yamamoto, M.; Ohkohchi, N.; Ikehara, Y.; Shoda, J.; Hirabayashi, J.; Narimatsu, H. Glycoproteomics-based cancer marker discovery adopting dual enrichment with Wisteria floribunda agglutinin for high specific glyco-diagnosis of cholangiocarcinoma J. Proteomics 2013, 85, 1-11
34. Kaji, H.; Ocho, M.; Togayachi, A.; Kuno, A.; Sogabe, M.; Ohkura, T.; Nozaki, H.; Angata, T.; Chiba, Y.; Ozaki, H.; Hirabayashi, J.; Tanaka, Y.; Mizokami, M.; Ikehara, Y.; Narimatsu, H. Glycoproteomic discovery of serological biomarker candidates for HCV/HBV infection-associated liver fibrosis and hepatocellular carcinoma J. Proteome Res. 2013, 12, 2630-40
35. Kuno, A.; Ikehara, Y.; Tanaka, Y.; Ito, K.; Matsuda, A.; Sekiya, S.; Hige, S.; Sakamoto, M.; Kage, M.; Mizokami, M.; Narimatsu, H. A serum sweet-doughnut protein facilitates fibrosis evaluation and therapy assessment in patients with viral hepatitis Sci. Rep. 2013, 3, 1065
36. Sogabe, M.; Nozaki, H.; Tanaka, N.; Kubota, T.; Kaji, H.; Kuno, A.; Togayachi, A.; Gotoh, M.; Nakanishi, H.; Nakanishi, T.; Mikami, M.; Suzuki, N.; Kiguchi, K.; Ikehara, Y.; Narimatsu, H. Novel glycobiomarker for ovarian cancer that detects clear cell carcinoma J. Proteome Res. 2014, 13, 1624-35
37. Tan, B.; Matsuda, A.; Zhang, Y.; Kuno, A.; Narimatsu, H. Multilectin-assisted fractionation for improved single-dot tissue glycome profiling in clinical glycoproteomics Mol. BioSyst 2013, 10, 201-5
38. Chapman, S.; Schenk, P.; Kazan, K.; Manners, J. Using biplots to interpret gene expression patterns in plants Bioinformatics 2002, 18, 202-204
39. Sharov, A. A.; Dudekula, D. B.; Ko, M. S. A web-based tool for principal component and significance analysis of microarray data Bioinformatics 2005, 21, 2548-9
40. Giaccone, G.; Battey, J.; Gazdar, A. F.; Oie, H.; Draoui, M.; Moody, T. W. Neuromedin B is present in lung cancer cell lines Cancer Res. 1992, 52, 2732s-2736s
41. Rothenberg, M. L. Irinotecan (CPT-11): recent developments and future directions-colorectal cancer and beyond Oncologist 2001, 6, 66-80
42. Han, S.; Sidell, N.; Roser-Page, S.; Roman, J. Fibronectin stimulates human lung carcinoma cell growth by inducing cyclooxygenase-2 (COX-2) expression J. Int. Cancer 2004, 111, 322-31
43. Hynes, R. Molecular biology of fibronectin Annu. Rev. Cell Biol. 1985, 1, 67-90
44. Pankov, R.; Yamada, K. M. Fibronectin at a glance J. Cell Sci. 2002, 115, 3861-3863
45. Ruoslahti, E. Fibronectin and its receptors Annu. Rev. Biochem. 1988, 57, 375-413
46. Matsuura, H.; Hakomori, S. I. The oncofetal domain of fibronectin defined by monoclonal antibody FDC-6: its presence in fibronectins from fetal and tumor tissues and its absence in those from normal adult tissues and plasma Proc. Natl. Acad. Sci. U.S.A. 1985, 82, 6517-6521
47. Matsuura, H.; Takio, K.; Titani, K.; Greene, T.; Levery, S. B.; Salyan, M. E.; Hakomori, S. The oncofetal structure of human fibronectin defined by monoclonal antibody FDC-6. Unique structural requirement for the antigenic specificity provided by a glycosylhexapeptide J. Biol. Chem. 1988, 263, 3314-22
48. Jakowlew, S. B.; Mariano, J. M.; You, L.; Mathias, A. Differential regulation of protease and extracellular matrix protein expression by transforming growth factor-beta 1 in non-small cell lung cancer cells and normal human bronchial epithelial cells Biochim. Biophys. Acta 1997, 1353, 157-70
49. Han, J. Y.; Kim, H. S.; Lee, S. H.; Park, W. S.; Lee, J. Y.; Yoo, N. J. Immunohistochemical expression of integrins and extracellular matrix proteins in non-small cell lung cancer: correlation with lymph node metastasis Lung Cancer 2003, 41, 65-70
50. Ravishankar, R.; Ravindran, M.; Suguna, K.; Surolia, A.; Vijayan, M. Crystal structure of the peanut lectin-T-antigen complex. Carbohydrate specificity generated by water bridges Curr. Sci. 1997, 72, 855-861
51. Ikehara, Y.; Sato, T.; Niwa, T.; Nakamura, S.; Gotoh, M.; Ikehara, S. K.; Kiyohara, K.; Aoki, C.; Iwai, T.; Nakanishi, H.; Hirabayashi, J.; Tatematsu, M.; Narimatsu, H. Apical Golgi localization of N,N′-diacetyllactosediamine synthase, beta4GalNAc-T3, is responsible for LacdiNAc expression on gastric mucosa Glycobiology 2006, 16, 777-85
52. Rinderle, S. J.; Goldstein, I. J.; Matta, K. L.; Ratcliffe, R. M. Isolation and characterization of amaranthin, a lectin present in the seeds of Amaranthus caudatus, that recognizes the T-antigen (or cryptic-T)-antigen J. Biol. Chem. 1989, 264, 16123-16131
53. Ueda, K.; Takami, S.; Saichi, N.; Daigo, Y.; Ishikawa, N.; Kohno, N.; Katsumata, M.; Yamane, A.; Ota, M.; Sato, T. A.; Nakamura, Y.; Nakagawa, H. Development of serum glycoproteomic profiling technique; simultaneous identification of glycosylation sites and site-specific quantification of glycan structure changes Mol. Cell. Proteomics 2010, 9, 1819-28
54. Mechref, Y.; Hu, Y.; Garcia, A.; Zhou, S.; Desantos-Garcia, J. L.; Hussein, A. Defining putative glycan cancer biomarkers by MS Bioanalysis 2012, 4, 2457-69
55. Hoagland, L. F. M.; Campa, M. J.; Gottlin, E. B.; Herndon, J. E.; Patz, E. F. Haptoglobin and posttranslational glycan-modified derivatives as serum biomarkers for the diagnosis of nonsmall cell lung cancer Cancer 2007, 110, 2260-2268
56. Heo, S. H.; Lee, S. J.; Ryoo, H. M.; Park, J. Y.; Cho, J. Y. Identification of putative serum glycoprotein biomarkers for human lung adenocarcinoma by multilectin affinity chromatography and LC-MS/MS Proteomics 2007, 7, 4292-302