Changes of serum-associated fucosylated glycoproteins and changes in glycosylation of IgA in human cirrhosis
Yoann Carré
Unité Mixte de Recherche CNRS/USTL 8576, Glycobiologie Structurale et Fonctionnelle, IFR 147, Université des Sciences et Technologies de Lille 1, Villeneuve d'Ascq, France
Search for more papers by this authorAndré Klein
Unité Mixte de Recherche CNRS/USTL 8576, Glycobiologie Structurale et Fonctionnelle, IFR 147, Université des Sciences et Technologies de Lille 1, Villeneuve d'Ascq, France
Laboratoire de Biochimie et de Biologie Moléculaire, UAM de glycopathologies, Centre de Biologie Pathologie, CHRU Lille, Lille, France
Search for more papers by this authorPhilippe Mathurin
Services d'Hépato-Gastroentérologie, Hôpital Huriez, CHRU Lille, Lille, France
Search for more papers by this authorJean-Claude Michalski
Unité Mixte de Recherche CNRS/USTL 8576, Glycobiologie Structurale et Fonctionnelle, IFR 147, Université des Sciences et Technologies de Lille 1, Villeneuve d'Ascq, France
Search for more papers by this authorCorresponding Author
Willy Morelle Dr.
Unité Mixte de Recherche CNRS/USTL 8576, Glycobiologie Structurale et Fonctionnelle, IFR 147, Université des Sciences et Technologies de Lille 1, Villeneuve d'Ascq, France
Unité Mixte de Recherche CNRS/USTL 8576, Glycobiologie Structurale et Fonctionnelle, IFR 147, Bâtiment C9, Université des Sciences et Technologies de Lille 1, 59655 Villeneuve d'Ascq Cedex, France Fax: +33-3-2043-6555Search for more papers by this authorYoann Carré
Unité Mixte de Recherche CNRS/USTL 8576, Glycobiologie Structurale et Fonctionnelle, IFR 147, Université des Sciences et Technologies de Lille 1, Villeneuve d'Ascq, France
Search for more papers by this authorAndré Klein
Unité Mixte de Recherche CNRS/USTL 8576, Glycobiologie Structurale et Fonctionnelle, IFR 147, Université des Sciences et Technologies de Lille 1, Villeneuve d'Ascq, France
Laboratoire de Biochimie et de Biologie Moléculaire, UAM de glycopathologies, Centre de Biologie Pathologie, CHRU Lille, Lille, France
Search for more papers by this authorPhilippe Mathurin
Services d'Hépato-Gastroentérologie, Hôpital Huriez, CHRU Lille, Lille, France
Search for more papers by this authorJean-Claude Michalski
Unité Mixte de Recherche CNRS/USTL 8576, Glycobiologie Structurale et Fonctionnelle, IFR 147, Université des Sciences et Technologies de Lille 1, Villeneuve d'Ascq, France
Search for more papers by this authorCorresponding Author
Willy Morelle Dr.
Unité Mixte de Recherche CNRS/USTL 8576, Glycobiologie Structurale et Fonctionnelle, IFR 147, Université des Sciences et Technologies de Lille 1, Villeneuve d'Ascq, France
Unité Mixte de Recherche CNRS/USTL 8576, Glycobiologie Structurale et Fonctionnelle, IFR 147, Bâtiment C9, Université des Sciences et Technologies de Lille 1, 59655 Villeneuve d'Ascq Cedex, France Fax: +33-3-2043-6555Search for more papers by this authorAbstract
Many modifications in N-glycosylation have been demonstrated in hepatic cirrhosis. These modifications correspond to an increase of a bisecting core alpha(1,6)-fucosylated biantennary glycan, an increase in core fucosylation, and the presence of an important population of neutral oligosaccharides in human serum of cirrhotic patients. In this study, a glycoproteomic approach which consists of lectin affinity chromatography, MALDI-TOF MS for the characterization of N-glycans released from glycoproteins, one- and 2-D PAGE, electrospray ionization quadrupole ion trap (ESI-QIT) MS was used to identify serum fucosylated glycoproteins related to cirrhosis. Employing this method, we have shown that IgA is one of the major proteins that is responsible of the glycosylation modifications observed in the serum N-glycome of cirrhotic patients. To our knowledge, this is the first time that aberrant N-glycosylation of IgA in cirrhosis is described.
References
- 1 Lowe, J. B., Glycan-dependent leukocyte adhesion and recruitment in inflammation. Curr. Opin. Cell Biol. 2003, 15, 531–538.
- 2 Helenius, A., Aebi, M., Intracellular functions of N-linked glycans. Science 2001, 291, 2364–2369.
- 3 Rudd, P. M., Elliott, T., Cresswell, P., Wilson, I. A., Dwek, R. A., Glycosylation and the immune system. Science 2001, 291, 2370–2376.
- 4 Keir, G., Winchester, B. G., Clayton, P. T., Carbohydrate-deficient glycoprotein syndromes: inborn errors of protein glycosylation. Ann. Clin. Biochem. 1999, 36, 20–36.
- 5 Sturiale, L., Barone, R., Fiumara, A., Perez, M. et al., Hypoglucosylation with increased fucosylation and branching of serum transferrin N-glycans in untreated galactosemia. Glycobiology 2005, 15, 1268–1276.
- 6 Sturla, L., Fruscione, F., Noda, K., Miyoshi, E. et al., Core fucosylation of N-linked glycans in leukocyte adhesion deficiency/congenital disorder of glycosylation IIc fibroblasts. Glycobiology 2005, 15, 924–934.
- 7 Varki, A., Acquired glycosylation changes in human disease. In: A. Varki, R. Cummings, J. Esko, H. Freeze et al., (Eds.), Essentials of Glycobiology. Cold Spring Harbor, New York 1999, pp. 565–580.
- 8 Dennis, J. W., Granovsky, M., Warren, C. E., Glycoprotein glycosylation and cancer progression. Biochim. Biophys. Acta 1999, 1473, 21–34.
- 9 Hakomori, S., Glycosylation defining cancer malignancy: new wine in an old bottle. Proc. Natl. Acad. Sci. USA 2002, 99, 10231–10233.
- 10 Hakomori, S., Tumor malignancy defined by aberrant glycosylation and sphingo(glyco)lipid metabolism. Cancer Res. 1996, 56, 5309–5318.
- 11 Peracaula, R., Tabares, G., Royle, L., Harvey, D. J. et al., Altered glycosylation pattern allows the distinction between prostate-specific antigen (PSA) from normal and tumor origins. Glycobiology 2003, 13, 457–470.
- 12 Comunale, M. A., Lowman, M., Long, R. E., Krakover, J. et al., Proteomic analysis of serum associated fucosylated glycoproteins in the development of primary hepatocellular carcinoma. J. Proteome Res. 2006, 5, 308–315.
- 13 An, H. J., Miyamoto, S., Lancaster, K. S., Kirmiz, C. et al., Profiling of glycans in serum for the discovery of potential biomarkers for ovarian cancer. J. Proteome Res. 2006, 5, 1626–1635.
- 14 Sakuma, K., Fujimoto, I., Hitoshi, S., Tanaka, F. et al., An N-glycan structure correlates with pulmonary metastatic ability of cancer cells. Biochem. Biophys. Res. Commun. 2006, 340, 829–835.
- 15 Anderson, N., Pollacchi, A., Hayes, P., Therapondos, G. et al., A preliminary evaluation of the differences in the glycosylation of alpha-1-acid glycoprotein between individual liver diseases. Biomed. Chromatogr. 2002, 16, 365–372.
- 16 Ryden, I., Pahlsson, P., Lindgren, S., Diagnostic accuracy of alpha(1)-acid glycoprotein fucosylation for liver cirrhosis in patients undergoing hepatic biopsy. Clin. Chem. 2002, 48, 2195–2201.
- 17 Klein, A., Human total serum N-glycome. Adv. Clin. Chem. 2008, 46, 51–85.
- 18 Callewaert, N., Van Vlierberghe, H., Van Hecke, A., Laroy, W. et al., Noninvasive diagnosis of liver cirrhosis using DNA sequencer-based total serum protein glycomics. Nat. Med. 2004, 10, 429–434.
- 19 Morelle, W., Flahaut, C., Michalski, J. C., Louvet, A. et al., Mass spectrometric approach for screening modifications of total serum N-glycome in human diseases: application to cirrhosis. Glycobiology 2006, 16, 281–293.
- 20 Varki, A., Diaz, S., The release and purification of sialic acids from glycoconjugates: methods to minimize the loss and migration of O-acetyl groups. Anal. Biochem. 1984, 137, 236–247.
- 21 Ciucanu, I., Kerek, F., A simple and rapid method for the permethylation of carbohydrates. Carbohydr. Res. 1984, 131, 209–217.
- 22 Morelle, W., Michalski, J. C., Analysis of protein glycosylation by mass spectrometry. Nat. Protoc. 2007, 2, 1585–1602.
- 23 Laemmli, U. K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227, 680–685.
- 24
Shevchenko, A.,
Wilm, M.,
Vorm, O.,
Mann, M.,
Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels.
Anal. Chem.
1996,
68,
850–858.
10.1002/(SICI)1097-4644(199702)64:2<295::AID-JCB12>3.0.CO;2-I CAS PubMed Web of Science® Google Scholar
- 25 Anderson, N. L., Anderson, N. G., The human plasma proteome: history, character, and diagnostic prospects. Mol. Cell. Proteomics 2002, 1, 845–867.
- 26 Wada, Y., Azadi, P., Costello, C. E., Dell, A. et al., Comparison of the methods for profiling glycoprotein glycans—HUPO Human Disease Glycomics/Proteome Initiative multi-institutional study. Glycobiology 2007, 17, 411–422.
- 27 Yamashita, K., Kochibe, N., Ohkura, T., Ueda, I., Kobata, A., Fractionation of L-fucose-containing oligosaccharides on immobilized Aleuria aurantia lectin. J. Biol. Chem. 1985, 260, 4688–4693.
- 28 Kochibe, N., Furukawa, K., Purification and properties of a novel fucose-specific hemagglutinin of Aleuria aurantia. Biochemistry 1980, 19, 2841–2846.
- 29 Faid, V., Chirat, F., Séta, N., Foulquier, F., Morelle, W., A rapid mass spectrometric strategy for the characterization of N- and O-glycan chains in the diagnosis of defects in glycan biosynthesis. Proteomics 2007, 7, 1800–1813.
- 30 Kita, Y., Miura, Y., Furukawa, J. I., Nakano, M. et al., Quantitative glycomics of human whole serum glycoproteins based on the standardized protocol for liberating N-glycans. Mol. Cell. Proteomics 2007, 6, 1437–1445.
- 31 Ryden, I., Pahlsson, P., Lindgren, S., Diagnostic accuracy of α1-acid glycoprotein fucosylation for liver cirrhosis in patients undergoing hepatic biopsy. Clin. Chem. 2002, 48, 2195–2201.
- 32 Gravel, P., Walzer, C., Aubry, C., Balant, L. P. et al., New alterations of serum glycoproteins in alcoholic and cirrhotic patients revealed by high resolution two-dimensional gel electrophoresis. Biochem. Biophys. Res. Commun. 1996, 220, 78–85.
- 33 Agostoni, A., Vergani, C., Stabilini, R., Marasini, B., Determination of seven serum proteins in alcoholic cirrhosis. Clin. Chim. Acta 1969, 26, 351–355.
- 34 Tissot, J. D., Schneider, P., James, R. W., Daigneault, R., Hochstrasser, D. F., High-resolution two-dimensional protein electrophoresis of pathological plasma/serum. Appl. Theor. Electrophor. 1991, 2, 7–12.
- 35 Baenziger, J., Kornfeld, S., Structure of the carbohydrate units of IgA1 immunoglobulin. I. Composition, glycopeptide isolation, and structure of the asparagine-linked oligosaccharide units. J. Biol. Chem. 1974, 249, 7260–7269.
- 36 Field, M. C., Amatayakul-Chantler, S., Rademacher, T. W., Rudd, P. M., Dwek, R. A., Structural analysis of the N-glycans from human immunoglobulin A1: comparison of normal human serum immunoglobulin A1 with that isolated from patients with rheumatoid arthritis. Biochem. J. 1994, 299, 261–275.
- 37 Endo, T., Mestecky, J., Kulhavy, R., Kobata, A., Carbohydrate heterogeneity of human myeloma proteins of the IgA1 and IgA2 subclasses. Mol. Immunol. 1994, 31, 1415–1422
- 38 Lowe, J. B., Marth, J. D., A genetic approach to mammalian glycan function. Ann. Rev. Biochem. 2003, 72, 643–691.
- 39 Ohtsubo, K., Marth, J. D., Glycosylation in cellular mechanisms of health and disease. Cell 2006, 126, 855–867.
- 40 Hollingsworth, M. A., Swanson, B. J., Mucins in cancer: protection and control of the cell surface. Nat. Rev. Cancer 2004, 4, 45–60.
- 41 Morelle, W., Canis, K., Chirat, F., Faid, V., Michalski, J. C., The use of mass spectrometry for the proteomic analysis of glycosylation. Proteomics 2006, 6, 3993–4015.
- 42 Van de Wiel, A., Seifert, W. F., Van der Linden, J. A., Gmelig-Meyling, F. H. et al., Spontaneous IgA synthesis by blood mononuclear cells in alcoholic liver disease. Scand. J. Immunol. 1987, 25, 181–187.
- 43 Tipoe, G. L., Liong, E. C., Casey, C. A., Donohue,T. M. Jr. et al., A voluntary oral ethanol-feeding rat model associated with necroinflammatory liver injury. Alcohol Clin. Exp. Res. 2008, 32, 669–682.
- 44 Arnold, J. N., Wormald, M. R., Sim, R. B., Rudd, P. M., Dwek, R. A., The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu. Rev. Immunol. 2007, 25, 21–50.
