Glycoproteomic discovery of serological biomarker candidates for HCV/HBV infection-associated liver fibrosis and hepatocellular carcinoma

Journal of Proteome Research

Volumn 12, Issue 6, 2013, Pages 2630-2640

  Kaji, Hiroyuki ^a   Ocho, Makoto ^a   Togayachi, Akira ^a   Kuno, Atsushi ^a   Sogabe, Maki ^a   Ohkura, Takashi ^a   Nozaki, Hirofumi ^a   Angata, Takashi ^a,c   Chiba, Yasunori ^a   Ozaki, Hidenori ^a   Hirabayashi, Jun ^a   Tanaka, Yasuhito ^b   Mizokami, Masashi ^b,d   Ikehara, Yuzuru ^a   Narimatsu, Hisashi ^a  

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

^b NAGOYA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCES   (Japan)

^c INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

^d 1 7 1 Kohnodai   (Japan)

Author keywords

biomarker; glycan alteration; glycoprotein; glycoproteomics; hepatocellular carcinoma; lectin array; liver fibrosis

Indexed keywords

BIOLOGICAL MARKER; GLYCOPEPTIDE; LECTIN;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CORONAVIRUS INFECTION; DISEASE COURSE; HEPATITIS B; HEPATOMA CELL; HUMAN; LIQUID CHROMATOGRAPHY; LIVER CELL CARCINOMA; LIVER FIBROSIS; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MICROARRAY; PROTEOMICS; SEROLOGY;

EID: 84879349436     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr301217b     Document Type: Article

References (50)

1. Umemura, T.; Ichijo, T.; Yoshizawa, K.; Tanaka, E.; Kiyosawa, K. Epidemiology of hepatocellular carcinoma in Japan J. Gastroenterol. 2009, 44 (Suppl 19) 102-7
2. Yoshida, H.; Shiratori, Y.; Moriyama, M.; Arakawa, Y.; Ide, T.; Sata, M.; Inoue, O.; Yano, M.; Tanaka, M.; Fujiyama, S.; Nishiguchi, S.; Kuroki, T.; Imazeki, F.; Yokosuka, O.; Kinoyama, S.; Yamada, G.; Omata, M. Interferon therapy reduces the risk for hepatocellular carcinoma: national surveillance program of cirrhotic and noncirrhotic patients with chronic hepatitis C in Japan. IHIT Study Group. Inhibition of Hepatocarcinogenesis by Interferon Therapy Ann. Intern. Med. 1999, 131 (3) 174-81
3. Cadranel, J. F.; Rufat, P.; Degos, F. Practices of liver biopsy in France: results of a prospective nationwide survey. For the Group of Epidemiology of the French Association for the Study of the Liver (AFEF) Hepatology 2000, 32 (3) 477-81
4. Castera, L.; Negre, I.; Samii, K.; Buffet, C. Pain experienced during percutaneous liver biopsy Hepatology 1999, 30 (6) 1529-30
5. Ito, K.; Kuno, A.; Ikehara, Y.; Sugiyama, M.; Saito, H.; Aoki, Y.; Matsui, T.; Imamura, M.; Korenaga, M.; Murata, K.; Masaki, N.; Tanaka, Y.; Hige, S.; Izumi, N.; Kurosaki, M.; Nishiguchi, S.; Sakamoto, M.; Kage, M.; Narimatsu, H.; Mizokami, M. LecT-hepa, a glyco-marker derived from multiple lectins, as a predictor of liver fibrosis in chronic hepatitis C patients Hepatology 2012, 56 (4) 1448-56
6. Wai, C. T.; Greenson, J. K.; Fontana, R. J.; Kalbfleisch, J. D.; Marrero, J. A.; Conjeevaram, H. S.; Lok, A. S. A simple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C Hepatology 2003, 38 (2) 518-26
7. Sato, M.; Tateishi, R.; Yasunaga, H.; Horiguchi, H.; Yoshida, H.; Matsuda, S.; Koike, K., Mortality and morbidity of hepatectomy, radiofrequency ablation, and embolization for hepatocellular carcinoma: a national survey of 54,145 patients. J. Gastroenterol. 2012.
8. Minami, Y.; Kudo, M. Radiofrequency ablation of hepatocellular carcinoma: a literature review Int. J. Hepatol. 2011, 104685
9. Takayama, T.; Makuuchi, M.; Hirohashi, S.; Sakamoto, M.; Yamamoto, J.; Shimada, K.; Kosuge, T.; Okada, S.; Takayasu, K.; Yamasaki, S. Early hepatocellular carcinoma as an entity with a high rate of surgical cure Hepatology 1998, 28 (5) 1241-6
10. Rifai, N.; Gillette, M. A.; Carr, S. A. Protein biomarker discovery and validation: the long and uncertain path to clinical utility Nat. Biotechnol. 2006, 24 (8) 971-83
11. Tamura, Y.; Igarashi, M.; Kawai, H.; Suda, T.; Satomura, S.; Aoyagi, Y. Clinical advantage of highly sensitive on-chip immunoassay for fucosylated fraction of alpha-fetoprotein in patients with hepatocellular carcinoma Dig. Dis. Sci. 2010, 55 (12) 3576-83
12. 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 (1) 95-105
13. 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 (3) 1358-67
14. 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 (6) 3019-27
15. 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 (6) 667-72
16. Kaji, H.; Shikanai, T.; Sasaki-Sawa, A.; Wen, H.; Fujita, M.; Suzuki, Y.; Sugahara, D.; Sawaki, H.; Yamauchi, Y.; Shinkawa, T.; Taoka, M.; Takahashi, N.; Isobe, T.; Narimatsu, H. Large-scale identification of N-glycosylated proteins of mouse tissues and construction of a glycoprotein database, GlycoProtDB J. Proteome Res. 2012, 11 (9) 4553-66
17. 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 (1) 99-108
18. Matsumura, K.; Higashida, K.; Ishida, H.; Hata, Y.; Yamamoto, K.; Shigeta, M.; Mizuno-Horikawa, Y.; Wang, X.; Miyoshi, E.; Gu, J.; Taniguchi, N. Carbohydrate binding specificity of a fucose-specific lectin from Aspergillus oryzae: a novel probe for core fucose J. Biol. Chem. 2007, 282 (21) 15700-8
19. Green, E. D.; Brodbeck, R. M.; Baenziger, J. U. Lectin affinity high-performance liquid chromatography: interactions of N-glycanase-released oligosaccharides with leukoagglutinating phytohemagglutinin, concanavalin A, Datura stramonium agglutinin, and Vicia villosa agglutinin Anal. Biochem. 1987, 167 (1) 62-75
20. Moriwaki, K.; Miyoshi, E. Fucosylation and gastrointestinal cancer World J. Hepatol. 2010, 2 (4) 151-61
21. Listinsky, J. J.; Siegal, G. P.; Listinsky, C. M. The emerging importance of alpha-L-fucose in human breast cancer: a review Am. J. Transl. Res. 2011, 3 (4) 292-322
22. Guo, H. B.; Zhang, Y.; Chen, H. L. Relationship between metastasis-associated phenotypes and N-glycan structure of surface glycoproteins in human hepatocarcinoma cells J. Cancer Res. Clin. Oncol. 2001, 127 (4) 231-6
23. Shinohara, Y.; Sota, H.; Kim, F.; Shimizu, M.; Gotoh, M.; Tosu, M.; Hasegawa, Y. Use of a biosensor based on surface plasmon resonance and biotinyl glycans for analysis of sugar binding specificities of lectins J. Biochem. 1995, 117 (5) 1076-82
24. Itakura, Y.; Nakamura-Tsuruta, S.; Kominami, J.; Sharon, N.; Kasai, K.; Hirabayashi, J. Systematic comparison of oligosaccharide specificity of Ricinus communis agglutinin I and Erythrina lectins: a search by frontal affinity chromatography J. Biochem. 2007, 142 (4) 459-69
25. Comunale, M. A.; Wang, M.; Hafner, J.; Krakover, J.; Rodemich, L.; Kopenhaver, B.; Long, R. E.; Junaidi, O.; Bisceglie, A. M.; Block, T. M.; Mehta, A. S. Identification and development of fucosylated glycoproteins as biomarkers of primary hepatocellular carcinoma J. Proteome Res. 2009, 8 (2) 595-602
26. Drake, R. R.; Schwegler, E. E.; Malik, G.; Diaz, J.; Block, T.; Mehta, A.; Semmes, O. J. Lectin capture strategies combined with mass spectrometry for the discovery of serum glycoprotein biomarkers Mol. Cell. Proteomics 2006, 5 (10) 1957-67
27. 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 (5) 913-23
28. Chen, R.; Wang, F.; Tan, Y.; Sun, Z.; Song, C.; Ye, M.; Wang, H.; Zou, H. Development of a combined chemical and enzymatic approach for the mass spectrometric identification and quantification of aberrant N-glycosylation J. Proteomics 2012, 75 (5) 1666-74
29. Hadziyannis, E.; Sialevris, K.; Georgiou, A.; Koskinas, J. Analysis of serum alpha-fetoprotein-L3% and des-gamma carboxyprothrombin markers in cases with misleading hepatocellular carcinoma total alpha-fetoprotein levels Oncol. Rep. 2012, 23174906
30. Biondi, A.; Malaguarnera, G.; Vacante, M.; Berretta, M.; D'Agata, V.; Malaguarnera, M.; Basile, F.; Drago, F.; Bertino, G. Elevated serum levels of Chromogranin A in hepatocellular carcinoma BMC Surg. 2012, 12 (Suppl 1) S7
31. Mounajjed, T.; Zhang, L.; Wu, T. T. Glypican-3 expression in gastrointestinal and pancreatic epithelial neoplasms Hum. Pathol. 2012, 44 (4) 542-50
32. 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 (1) 48-56
33. 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 (5) 527-36
34. Masuzaki, R.; Karp, S. J.; Omata, M. New serum markers of hepatocellular carcinoma Semin. Oncol. 2012, 39 (4) 434-9
35. Yusa, A.; Miyazaki, K.; Kimura, N.; Izawa, M.; Kannagi, R. Epigenetic silencing of the sulfate transporter gene DTDST induces sialyl Lewisx expression and accelerates proliferation of colon cancer cells Cancer Res. 2010, 70 (10) 4064-73
36. Mizuguchi, S.; Inoue, K.; Iwata, T.; Nishida, T.; Izumi, N.; Tsukioka, T.; Nishiyama, N.; Uenishi, T.; Suehiro, S. High serum concentrations of Sialyl Lewisx predict multilevel N2 disease in non-small-cell lung cancer Ann. Surg. Oncol. 2006, 13 (7) 1010-8
37. Peracaula, R.; Tabares, G.; Lopez-Ferrer, A.; Brossmer, R.; de Bolos, C.; de Llorens, R. Role of sialyltransferases involved in the biosynthesis of Lewis antigens in human pancreatic tumour cells Glycoconjugate J. 2005, 22 (3) 135-44
38. Lee, J. K.; Bistrup, A.; van Zante, A.; Rosen, S. D. Activities and expression pattern of the carbohydrate sulfotransferase GlcNAc6ST-3 (I-GlcNAc6ST): functional implications Glycobiology 2003, 13 (4) 245-54
39. Taketa, K.; Ichikawa, E.; Sakuda, H.; Iwamasa, T.; Hayakawa, M.; Taga, H.; Hirai, H. Lectin reactivity of alpha-fetoprotein in a case of renal cell carcinoma Tumour Biol, 1989, 10 (5) 275-80
40. Medical devices; immunology and microbiology devices; classification of AFP-L3% immunological test systems. Final rule. Fed. Regist. 2005, 70 (191), 57748-50.
41. Zhao, Y.; Jia, W.; Wang, J.; Ying, W.; Zhang, Y.; Qian, X. Fragmentation and site-specific quantification of core fucosylated glycoprotein by multiple reaction monitoring-mass spectrometry Anal. Chem. 2011, 83 (22) 8802-9
42. Comunale, M. A.; Lowman, M.; Long, R. E.; Krakover, J.; Philip, R.; Seeholzer, S.; Evans, A. A.; Hann, H. W.; 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 (2) 308-15
43. Marrero, J. A.; Feng, Z.; Wang, Y.; Nguyen, M. H.; Befeler, A. S.; Roberts, L. R.; Reddy, K. R.; Harnois, D.; Llovet, J. M.; Normolle, D.; Dalhgren, J.; Chia, D.; Lok, A. S.; Wagner, P. D.; Srivastava, S.; Schwartz, M. Alpha-fetoprotein, des-gamma carboxyprothrombin, and lectin-bound alpha-fetoprotein in early hepatocellular carcinoma Gastroenterology 2009, 137 (1) 110-8
44. Tan, F.; Weerasinghe, D. K.; Skidgel, R. A.; Tamei, H.; Kaul, R. K.; Roninson, I. B.; Schilling, J. W.; Erdos, E. G. The deduced protein sequence of the human carboxypeptidase N high molecular weight subunit reveals the presence of leucine-rich tandem repeats J. Biol. Chem. 1990, 265 (1) 13-9
45. Wang, Z. E.; Myles, G. M.; Brandt, C. S.; Lioubin, M. N.; Rohrschneider, L. Identification of the ligand-binding regions in the macrophage colony-stimulating factor receptor extracellular domain Mol. Cell. Biol. 1993, 13 (9) 5348-59
46. Mitchell, P. Proteomics retrenches Nat. Biotechnol. 2010, 28 (7) 665-70
47. Rosenberg, W. M.; Voelker, M.; Thiel, R.; Becka, M.; Burt, A.; Schuppan, D.; Hubscher, S.; Roskams, T.; Pinzani, M.; Arthur, M. J. Serum markers detect the presence of liver fibrosis: a cohort study Gastroenterology 2004, 127 (6) 1704-13
48. Kuno, A.; Ikehara, Y.; Tanaka, Y.; Saito, K.; Ito, K.; Tsuruno, C.; Nagai, S.; Takahama, Y.; Mizokami, M.; Hirabayashi, J.; Narimatsu, H. LecT-Hepa: A triplex lectin-antibody sandwich immunoassay for estimating the progression dynamics of liver fibrosis assisted by a bedside clinical chemistry analyzer and an automated pretreatment machine Clin. Chim. Acta 2011, 412 (19-20) 1767-72
49. Du, D.; Zhu, X.; Kuno, A.; Matsuda, A.; Tsuruno, C.; Yu, D.; Zhang, Y.; Ikehara, Y.; Tanaka, Y.; Zhang, X.; Narimatsu, H. Comparison of LecT-Hepa and FibroScan for assessment of liver fibrosis in hepatitis B virus infected patients with different ALT levels Clin. Chim. Acta 2012, 413 (21-22) 1796-9
50. Lau, C. P.; Poon, R. T.; Cheung, S. T.; Yu, W. C.; Fan, S. T. SPARC and Hevin expression correlate with tumour angiogenesis in hepatocellular carcinoma J. Pathol. 2006, 210 (4) 459-68