Site-specific glycoforms of haptoglobin in liver cirrhosis and hepatocellular carcinoma

Molecular and Cellular Proteomics

Volumn 12, Issue 5, 2013, Pages 1281-1293

  Pompach, Petr ^a   Brnakova, Zuzana ^a   Sanda, Miloslav ^a   Wu, Jing ^a   Edwards, Nathan ^b   Goldman, Radoslav ^a,b  

^a GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b 1217 Harris Building ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPEPTIDE; HAPTOGLOBIN;

ARTICLE; CANCER PATIENT; CLINICAL ARTICLE; CONTROLLED STUDY; FUCOSYLATION; HUMAN; HYDROPHILICITY; LIQUID CHROMATOGRAPHY; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVERSED PHASE LIQUID CHROMATOGRAPHY; TANDEM MASS SPECTROMETRY;

AMINO ACID SEQUENCE; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; CARCINOMA, HEPATOCELLULAR; CASE-CONTROL STUDIES; FUCOSE; GLYCOSYLATION; HAPTOGLOBINS; HUMANS; LIVER CIRRHOSIS; LIVER NEOPLASMS; MOLECULAR SEQUENCE DATA; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84875976604     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.023259     Document Type: Article

References (57)

1. Kornfeld, R., and Kornfeld, S. (1985) Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54, 631-664 (Pubitemid 15073660)
2. Roth, J., Taatjes, D. J., Lucocq, J. M., Weinstein, J., and Paulson, J. C. (1985) Demonstration of an extensive trans-tubular network continuous with the Golgi apparatus stack that may function in glycosylation. Cell 43, 287-295 (Pubitemid 16199715)
3. Lairson, L. L., Henrissat, B., Davies, G. J., and Withers, S. G. (2008) Glycosyltransferases: structures, functions, and mechanisms. Annu. Rev. Biochem. 77, 521-555
4. Meany, D. L., and Chan, D. W. (2011) Aberrant glycosylation associated with enzymes as cancer biomarkers. Clin. Proteomics 8, 7
5. Nakagawa, T., Uozumi, N., Nakano, M., Mizuno-Horikawa, Y., Okuyama, N., Taguchi, T., Gu, J., Kondo, A., Taniguchi, N., and Miyoshi, E. (2006) Fucosylation of N-glycans regulates the secretion of hepatic glycoproteins into bile ducts. J. Biol. Chem. 281, 29797-29806 (Pubitemid 44536989)
6. Carlsson, M. C., Cederfur, C., Schaar, V., Balog, C. I., Lepur, A., Touret, F., Salomonsson, E., Deelder, A. M., Fernö, M., Olsson, H., Wuhrer, M., and Leffler, H. (2011) Galectin-1-binding glycoforms of haptoglobin with altered intracellular trafficking and increase in metastatic breast cancer patients. PLoS One 6, e26560
7. Nakano, M., Nakagawa, T., Ito, T., Kitada, T., Hijioka, T., Kasahara, A., Tajiri, M., Wada, Y., Taniguchi, N., and Miyoshi, E. (2008) Site-specific analysis of N-glycans on haptoglobin in sera of patients with pancreatic cancer: a novel approach for the development of tumor markers. Int. J Cancer 122, 2301-2309 (Pubitemid 351542335)
8. Wang, M., Long, R. E., Comunale, M. A., Junaidi, O., Marrero, J., Di Bisceglie, A. M., Block, T. M., and Mehta, A. S. (2009) Novel fucosylated biomarkers for the early detection of hepatocellular carcinoma. Cancer Epidemiol. Biomarkers Prev. 18, 1914-1921
9. 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., and Novotny, M. V. (2009) Detection of hepatocellular carcinoma using glycomic analysis. Clin. Cancer Res. 15, 1808-1813
10. Bekesova, S., Kosti, O., Chandler, K. B., Wu, J., Madej, H. L., Brown, K. C., Simonyan, V., and Goldman, R. (2012) N-Glycans in liver-secreted and immunoglobulin-derived protein fractions. J. Proteomics 75, 2216-2224
11. Vanderschaeghe, D., Laroy, W., Sablon, E., Halfon, P., Van Hecke, A., Delanghe, J., and Callewaert, N. (2009) GlycoFibroTest is a highly performant liver fibrosis biomarker derived from DNA sequencer-based serum protein glycomics. Mol. Cell. Proteomics 8, 986-994
12. Mehta, A. S., Long, R. E., Comunale, M. A., Wang, M., Rodemich, L., Krakover, J., Philip, R., Marrero, J. A., Dwek, R. A., and Block, T. M. (2008) Increased levels of galactose-deficient anti-Gal immunoglobulin G in the sera of hepatitis C virus-infected individuals with fibrosis and cirrhosis. J. Virol. 82, 1259-1270
13. Blomme, B., Van Steenkiste, C., Callewaert, N., and Van Vlierberghe, H. (2009) Alteration of protein glycosylation in liver diseases. J. Hepatol. 50, 592-603
14. Klein, A., Michalski, J. C., and Morelle, W. (2010) Modifications of human total serum N-glycome during liver fibrosis-cirrhosis, is it all about immunoglobulins? Proteomics Clin. Appl. 4, 372-378
15. Bones, J., Mittermayr, S., O'Donoghue, N., Guttman, A., and Rudd, P. M. (2010) Ultra performance liquid chromatographic profiling of serum N-glycans for fast and efficient identification of cancer associated alterations in glycosylation. Anal. Chem. 82, 10208-10215
16. Vanderschaeghe, D., Debruyne, E., Van Vlierberghe, H., Callewaert, N., and Delanghe, J. (2009) Analysis of γ-globulin mobility on routine clinical CE equipment: exploring its molecular basis and potential clinical utility. Electrophoresis 30, 2617-2623
17. Mori, S., Aoyagi, Y., Yanagi, M., Suzuki, Y., and Asakura, H. (1998) Serum N-acetylglucosaminyltransferase III activities in hepatocellular carcinoma. J. Gastroenterol. Hepatol. 13, 610-619 (Pubitemid 28407305)
18. Tsutsumi, M., Wang, J. S., and Takada, A. (1994) Microheterogeneity of serum glycoproteins in alcoholics: is desialo-transferrin the marker of chronic alcohol drinking or alcoholic liver injury? Alcohol. Clin. Exp. Res. 18, 392-397 (Pubitemid 24138336)
19. Sasaki, K., Kurata-Miura, K., Ujita, M., Angata, K., Nakagawa, S., Sekine, S., Nishi, T., and Fukuda, M. (1997) Expression cloning of cDNA encoding a human β-1,3-N-acetylglucosaminyltransferase that is essential for poly-N-acetyllactosamine synthesis. Proc. Natl. Acad. Sci. U.S.A. 94, 14294-14299
20. Campion, B., Léger, D., Wieruszeski, J. M., Montreuil, J., and Spik, G. (1989) Presence of fucosylated triantennary, tetraantennary, and penta-antennary glycans in transferrin synthesized by the human hepatocarcinoma cell line Hep G2. Eur. J. Biochem. 184, 405-413 (Pubitemid 19248627)
21. Blomme, B., Van Steenkiste, C., Grassi, P., Haslam, S. M., Dell, A., Callewaert, N., and Van Vlierberghe, H. (2011) Alterations of serum protein N-glycosylation in two mouse models of chronic liver disease are hepatocyte and not B cell driven. Am. J. Physiol. Gastrointest. Liver Physiol. 300, G833-G842
22. 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., and Rudd, P. M. (2007) Ovarian cancer is associated with changes in glycosylation in both acute-phase proteins and IgG. Glycobiology 17, 1344-1356 (Pubitemid 350131311)
23. Du, M. Q., Hutchinson, W. L., Johnson, P. J., and Williams, R. (1991) Differential α-fetoprotein lectin binding in hepatocellular carcinoma. Diagnostic utility at low serum levels. Cancer 67, 476-480
24. Taketa, K., Sekiya, C., Namiki, M., Akamatsu, K., Ohta, Y., Endo, Y., and Kosaka, K. (1990) Lectin-reactive profiles of α-fetoprotein characterizing hepatocellular carcinoma and related conditions. Gastroenterology 99, 508-518 (Pubitemid 20219108)
25. Sterling, R. K., Jeffers, L., Gordon, F., Sherman, M., Venook, A. P., Reddy, K. R., Satomura, S., and Schwartz, M. E. (2007) Clinical utility of AFP-L3% measurement in North American patients with HCV-related cirrhosis. Am. J. Gastroenterol. 102, 2196-2205 (Pubitemid 47493844)
26. Dobryszycka, W. (1997) Biological functions of haptoglobin-new pieces to an old puzzle. Eur. J. Clin. Chem. Clin. Biochem. 35, 647-654
27. Kristiansen, M., Graversen, J. H., Jacobsen, C., Sonne, O., Hoffman, H. J., Law, S. K., and Moestrup, S. K. (2001) Identification of the haemoglobin scavenger receptor. Nature 409, 198-201 (Pubitemid 32144285)
28. Andersen, C. B., Torvund-Jensen, M., Nielsen, M. J., de Oliveira, C. L., Hersleth, H. P., Andersen, N. H., Pedersen, J. S., Andersen, G. R., and Moestrup, S. K. (2012) Structure of the haptoglobin-haemoglobin complex. Nature 489, 456-459
29. Pompach, P., Chandler, K. B., Lan, R., Edwards, N., and Goldman, R. (2012) Semi-automated identification of N-glycopeptides by hydrophilic interaction chromatography, nano-reverse-phase LC-MS/MS, and Glycan Database Search. J. Proteome Res. 11, 1728-1740
30. Wang, D., Hincapie, M., Rejtar, T., and Karger, B. L. (2011) Ultrasensitive characterization of site-specific glycosylation of affinity-purified haptoglobin from lung cancer patient plasma using 10 μm i.d. porous layer open tubular liquid chromatography-linear ion trap collision-induced dissociation/electron transfer dissociation mass spectrometry. Anal. Chem. 83, 2029-2037
31. Liu, Z., Cao, J., He, Y., Qiao, L., Xu, C., Lu, H., and Yang, P. (2010) Tandem O-18 stable isotope labeling for quantification of N-glycoproteome. J. Proteome Res. 9, 227-236
32. Alley, W. R., Jr., Madera, M., Mechref, Y., and Novotny, M. V. (2010) Chip-based reversed-phase liquid chromatography-mass spectrometry of permethylated N-linked glycans: a potential methodology for cancer-biomarker discovery. Anal. Chem. 82, 5095-5106
33. Mazurier, J., Dauchez, M., Vergoten, G., Montreuil, J., and Spik, G. (1991) Molecular modeling of a disialylated monofucosylated biantennary glycan of the N-acetyllactosamine type. Glycoconj. J. 8, 390-399
34. Royle, L., Campbell, M. P., Radcliffe, C. M., White, D. M., Harvey, D. J., Abrahams, J. L., Kim, Y. G., Henry, G. W., Shadick, N. A., Weinblatt, M. E., Lee, D. M., Rudd, P. M., and Dwek, R. A. (2008) HPLC-based analysis of serum N-glycans on a 96-well plate platform with dedicated database software. Anal. Biochem. 376, 1-12
35. Lucka, L., Fernando, M., Grunow, D., Kannicht, C., Horst, A. K., Nollau, P., and Wagener, C. (2005) Identification of Lewis x structures of the cell adhesion molecule CEACAM1 from human granulocytes. Glycobiology 15, 87-100 (Pubitemid 40202042)
36. Selman, M. H., McDonnell, L. A., Palmblad, M., Ruhaak, L. R., Deelder, A. M., and Wuhrer, M. (2010) Immunoglobulin G glycopeptide profiling by matrix-assisted laser desorption ionization Fourier transform ion cyclotron resonance mass spectrometry. Anal. Chem. 82, 1073-1081
37. Wuhrer, M., Koeleman, C. A., Hokke, C. H., and Deelder, A. M. (2006) Mass spectrometry of proton adducts of fucosylated N-glycans: fucose transfer between antennae gives rise to misleading fragments. Rapid Commun. Mass Spectrom. 20, 1747-1754 (Pubitemid 43793878)
38. Gordon, S., Cleve, H., and Bearn, A. G. (1968) An improved method of preparing haptoglobin polypeptide chains using guanidine hydrochloride. Proc. Soc. Exp. Biol. Med. 127, 52-59
39. Boonyapranai, K., Tsai, H. Y., Chen, M. C., Sriyam, S., Sinchaikul, S., Phutrakul, S., and Chen, S. T. (2011) Glycoproteomic analysis and molecular modeling of haptoglobin multimers. Electrophoresis 32, 1422-1432
40. Polticelli, F., Bocedi, A., Minervini, G., and Ascenzi, P. (2008) Human haptoglobin structure and function-a molecular modelling study. FEBS J. 275, 5648-5656
41. Shu, H., Zhang, S., Kang, X., Li, S., Qin, X., Sun, C., Lu, H., and Liu, Y. (2011) Protein expression and fucosylated glycans of the serum haptoglobin-β subunit in hepatitis B virus-based liver diseases. Acta Biochim. Biophys. Sin. 43, 528-534
42. Lin, Z., Simeone, D. M., Anderson, M. A., Brand, R. E., Xie, X., Shedden, K. A., Ruffin, M. T., and Lubman, D. M. (2011) Mass spectrometric assay for analysis of haptoglobin fucosylation in pancreatic cancer. J. Proteome Res. 10, 2602-2611
43. Park, S. Y., Yoon, S. J., Hakomori, S. I., Kim, J. M., Kim, J. Y., Bernert, B., Ullman, T., Itzkowitz, S. H., and Kim, J. H. (2010) Dimeric Le(a) (Le(a)-on-Le(a)) status of β-haptoglobin in sera of colon cancer, chronic inflammatory disease, and normal subjects. Int. J. Oncol. 36, 1291-1297
44. Clark, G. F., Grassi, P., Pang, P. C., Panico, M., Lafrenz, D., Drobnis, E. Z., Baldwin, M. R., Morris, H. R., Haslam, S. M., Schedin-Weiss, S., Sun, W., and Dell, A. (2012) Tumor biomarker glycoproteins in the seminal plasma of healthy human males are endogenous ligands for DC-SIGN. Mol. Cell. Proteomics 11, Available at: 10.1074/mcp.M111.008730
45. Sun, W., Grassi, P., Engström, A., Sooriyaarachchi, S., Ubhayasekera, W., Hreinsson, J., Wånggren, K., Clark, G. F., Dell, A., and Schedin-Weiss, S. (2011) N-Glycans of human protein C inhibitor: tissue-specific expression and function. PLoS One 6, e29011
46. Sun, W., Parry, S., Panico, M., Morris, H. R., Kjellberg, M., Engström, A., Dell, A., and Schedin-Weiss, S. (2008) N-Glycans and the N terminus of protein C inhibitor affect the cofactor-enhanced rates of thrombin inhibition. J. Biol. Chem. 283, 18601-18611
47. Pang, P. C., Chiu, P. C., Lee, C. L., Chang, L. Y., Panico, M., Morris, H. R., Haslam, S. M., Khoo, K. H., Clark, G. F., Yeung, W. S., and Dell, A. (2011) Human sperm binding is mediated by the sialyl-Lewis(x) oligosaccharide on the zona pellucida. Science 333, 1761-1764
48. Mann, B. F., Goetz, J. A., House, M. G., Schmidt, C. M., and Novotny, M. V. (2012) Glycomic and proteomic profiling of pancreatic cyst fluids identifies hyperfucosylated lactosamines on the N-linked glycans of overexpressed glycoproteins. Mol. Cell. Proteomics Available at: 10.1074/mcp.M111.015792
49. Gilar, M., and Jaworski, A. (2011) Retention behavior of peptides in hydrophilic-interaction chromatography. J. Chromatogr. A 1218, 8890-8896
50. Nilsson, J., Rüetschi, U., Halim, A., Hesse, C., Carlsohn, E., Brinkmalm, G., and Larson, G. (2009) Enrichment of glycopeptides for glycan structure and attachment site identification. Nat. Methods 6, 809-811
51. Mehta, A. S., Norton, P., Liang, H., Comunale, M. A., Wang, M., Rodemich-Betesh, L., Koszycki, A., Noda, K., Miyoshi, E., and Block, T. (2012) Increased levels of tetra-antennary N-linked glycan but not core fucosylation are associated with hepatocellular carcinoma tissue. Cancer Epidemiol. Biomarkers Prev. 21, 925-933
52. Miyoshi, E., and Nakano, M. (2008) Fucosylated haptoglobin is a novel marker for pancreatic cancer: detailed analyses of oligosaccharide structures. Proteomics 8, 3257-3262
53. Fujimura, T., Shinohara, Y., Tissot, B., Pang, P. C., Kurogochi, M., Saito, S., Arai, Y., Sadilek, M., Murayama, K., Dell, A., Nishimura, S., and Hakomori, S. I. (2008) Glycosylation status of haptoglobin in sera of patients with prostate cancer versus benign prostate disease or normal subjects. Int. J. Cancer 122, 39-49 (Pubitemid 350209976)
54. Okuyama, N., Ide, Y., Nakano, M., Nakagawa, T., Yamanaka, K., Moriwaki, K., Murata, K., Ohigashi, H., Yokoyama, S., Eguchi, H., Ishikawa, O., Ito, T., Kato, M., Kasahara, A., Kawano, S., Gu, J., Taniguchi, N., and Miyoshi, E. (2006) Fucosylated haptoglobin is a novel marker for pancreatic cancer: a detailed analysis of the oligosaccharide structure and a possible mechanism for fucosylation. Int. J Cancer 118, 2803-2808 (Pubitemid 43673360)
55. Taketa, K., Endo, Y., Sekiya, C., Tanikawa, K., Koji, T., Taga, H., Satomura, S., Matsuura, S., Kawai, T., and Hirai, H. (1993) A collaborative study for the evaluation of lectin-reactive α-fetoproteins in early detection of hepatocellular carcinoma. Cancer Res. 53, 5419-5423 (Pubitemid 23342160)
56. Comunale, M. A., Rodemich-Betesh, L., Hafner, J., Wang, M., Norton, P., Di Bisceglie, A. M., Block, T., and Mehta, A. (2010) Linkage-specific fucosylation of α-1-antitrypsin in liver cirrhosis and cancer patients: implications for a biomarker of hepatocellular carcinoma. PLoS One 5, e12419
57. Sanda, M., Pompach, P., Brnakova, Z., Wu, J., Makambi, K., Goldman, R., (2013) Quantitative LC-MS-MRM analysis of site-specific glycoforms of haptoglobin in liver disease. Mol Cell Proteomics. 12, 1294-1305